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Published in: Infection 2/2024

25-01-2024 | Helicobacter Pylori | Review

Infiltration to infection: key virulence players of Helicobacter pylori pathogenicity

Authors: Arghyadeep Bhattacharjee, Om Saswat Sahoo, Ahana Sarkar, Saurabh Bhattacharya, Rukhsana Chowdhury, Samarjit Kar, Oindrilla Mukherjee

Published in: Infection | Issue 2/2024

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Abstract

Purpose

This study aims to comprehensively review the multifaceted factors underlying the successful colonization and infection process of Helicobacter pylori (H. pylori), a prominent Gram-negative pathogen in humans. The focus is on elucidating the functions, mechanisms, genetic regulation, and potential cross-interactions of these elements.

Methods

Employing a literature review approach, this study examines the intricate interactions between H. pylori and its host. It delves into virulence factors like VacA, CagA, DupA, Urease, along with phase variable genes, such as babA, babC, hopZ, etc., giving insights about the bacterial perspective of the infection The association of these factors with the infection has also been added in the form of statistical data via Funnel and Forest plots, citing the potential of the virulence and also adding an aspect of geographical biasness to the virulence factors. The biochemical characteristics and clinical relevance of these factors and their effects on host cells are individually examined, both comprehensively and statistically.

Results

H. pylori is a Gram-negative, spiral bacterium that successfully colonises the stomach of more than half of the world's population, causing peptic ulcers, gastric cancer, MALT lymphoma, and other gastro-duodenal disorders. The clinical outcomes of H. pylori infection are influenced by a complex interplay between virulence factors and phase variable genes produced by the infecting strain and the host genetic background. A meta-analysis of the prevalence of all the major virulence factors has also been appended.

Conclusion

This study illuminates the diverse elements contributing to H. pylori's colonization and infection. The interplay between virulence factors, phase variable genes, and host genetics determines the outcome of the infection. Despite biochemical insights into many factors, their comprehensive regulation remains an understudied area. By offering a panoramic view of these factors and their functions, this study enhances understanding of the bacterium’s perspective, i.e. H. pylori's journey from infiltration to successful establishment within the host's stomach.
Literature
1.
go back to reference Robin Warren J, Marshall B. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet. 1983;321:1273–5.CrossRef Robin Warren J, Marshall B. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet. 1983;321:1273–5.CrossRef
2.
go back to reference Giuppi M, La Salvia A, Evangelista J, Ghidini M. The role and expression of angiogenesis-related miRNAs in gastric cancer. Biology (Basel). 2021;10:146.PubMed Giuppi M, La Salvia A, Evangelista J, Ghidini M. The role and expression of angiogenesis-related miRNAs in gastric cancer. Biology (Basel). 2021;10:146.PubMed
3.
go back to reference Gravina AG, Zagari RM, De Musis C, Romano L, Loguercio C, Romano M. Helicobacter pylori and extragastric diseases: a review. World J Gastroenterol. 2018;24:3204–21.PubMedPubMedCentralCrossRef Gravina AG, Zagari RM, De Musis C, Romano L, Loguercio C, Romano M. Helicobacter pylori and extragastric diseases: a review. World J Gastroenterol. 2018;24:3204–21.PubMedPubMedCentralCrossRef
7.
go back to reference Ha NC, Oh ST, Sung JY, Cha KA, Lee MH, Oh BH. Supramolecular assembly and acid resistance of Helicobacter pylori urease. Nat Struct Biol. 2001;8:505–9.PubMedCrossRef Ha NC, Oh ST, Sung JY, Cha KA, Lee MH, Oh BH. Supramolecular assembly and acid resistance of Helicobacter pylori urease. Nat Struct Biol. 2001;8:505–9.PubMedCrossRef
8.
10.
go back to reference Blaser MJ. Epidemiology and pathophysiology of campylobacter pylori Infections. Rev Infect Dis. 1990;12:S99-106.PubMedCrossRef Blaser MJ. Epidemiology and pathophysiology of campylobacter pylori Infections. Rev Infect Dis. 1990;12:S99-106.PubMedCrossRef
11.
go back to reference Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C. Bacteria and host interactions in the gut epithelial barrier. Nat Chem Biol. 2012;8:36–45.CrossRef Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C. Bacteria and host interactions in the gut epithelial barrier. Nat Chem Biol. 2012;8:36–45.CrossRef
12.
go back to reference Machado JC, Figueiredo C, Canedo P, Pharoah P, Carvalho R, Nabais S, et al. A proinflammatory genetic profile increases the risk for chronic atrophic gastritis and gastric carcinoma. Gastroenterology. 2003;125:364–71.PubMedCrossRef Machado JC, Figueiredo C, Canedo P, Pharoah P, Carvalho R, Nabais S, et al. A proinflammatory genetic profile increases the risk for chronic atrophic gastritis and gastric carcinoma. Gastroenterology. 2003;125:364–71.PubMedCrossRef
14.
go back to reference Oh JD, Kling-Bäckhed H, Giannakis M, Xu J, Fulton RS, Fulton LA, et al. The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. Proc Natl Acad Sci USA. 2006;103:9999–10004.PubMedPubMedCentralCrossRef Oh JD, Kling-Bäckhed H, Giannakis M, Xu J, Fulton RS, Fulton LA, et al. The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. Proc Natl Acad Sci USA. 2006;103:9999–10004.PubMedPubMedCentralCrossRef
15.
go back to reference Van Doorn LJ, Figueiredo C, Sanna R, Pena S, Midolo P, Ng EKW, et al. Expanding allelic diversity of Helicobacter pylori vacA. J Clin Microbiol. 1998;36:2597–603.PubMedPubMedCentralCrossRef Van Doorn LJ, Figueiredo C, Sanna R, Pena S, Midolo P, Ng EKW, et al. Expanding allelic diversity of Helicobacter pylori vacA. J Clin Microbiol. 1998;36:2597–603.PubMedPubMedCentralCrossRef
16.
go back to reference Lu H, Yamaoka Y, Graham DY. Helicobacter pylori virulence factors: facts and fantasies. Curr Opin Gastroenterol. 2005;21:653–9.PubMedCrossRef Lu H, Yamaoka Y, Graham DY. Helicobacter pylori virulence factors: facts and fantasies. Curr Opin Gastroenterol. 2005;21:653–9.PubMedCrossRef
17.
go back to reference Ansari S, Yamaoka Y. Survival of Helicobacter pylori in gastric acidic territory. Helicobacter. 2017;22:1–13.CrossRef Ansari S, Yamaoka Y. Survival of Helicobacter pylori in gastric acidic territory. Helicobacter. 2017;22:1–13.CrossRef
23.
go back to reference Tegtmeyer N, Wessler S, Backert S. Role of the cag-pathogenicity island encoded type IV secretion system in Helicobacter pylori pathogenesis. FEBS J. 2011;278:1190–202.PubMedPubMedCentralCrossRef Tegtmeyer N, Wessler S, Backert S. Role of the cag-pathogenicity island encoded type IV secretion system in Helicobacter pylori pathogenesis. FEBS J. 2011;278:1190–202.PubMedPubMedCentralCrossRef
24.
go back to reference Tegtmeyer N, Neddermann M, Asche CI, Backert S. Subversion of host kinases: a key network in cellular signaling hijacked by Helicobacter pylori CagA. Mol Microbiol. 2017;105:358–72.PubMedCrossRef Tegtmeyer N, Neddermann M, Asche CI, Backert S. Subversion of host kinases: a key network in cellular signaling hijacked by Helicobacter pylori CagA. Mol Microbiol. 2017;105:358–72.PubMedCrossRef
25.
go back to reference Gorrell RJ, Guan J, Xin Y, Tafreshi MA, Hutton ML, Mcguckin MA, et al. A novel NOD1- and CagA-independent pathway of interleukin-8 induction mediated by the Helicobacter pylori type IV secretion system. Cell Microbiol. 2013;15:554–70.PubMedCrossRef Gorrell RJ, Guan J, Xin Y, Tafreshi MA, Hutton ML, Mcguckin MA, et al. A novel NOD1- and CagA-independent pathway of interleukin-8 induction mediated by the Helicobacter pylori type IV secretion system. Cell Microbiol. 2013;15:554–70.PubMedCrossRef
26.
go back to reference Radin JN, González-Rivera C, Ivie SE, McClain MS, Cover TL. Helicobacter pylori VacA induces programmed necrosis in gastric epithelial cells. Infect Immun. 2011;79:2535–43.PubMedPubMedCentralCrossRef Radin JN, González-Rivera C, Ivie SE, McClain MS, Cover TL. Helicobacter pylori VacA induces programmed necrosis in gastric epithelial cells. Infect Immun. 2011;79:2535–43.PubMedPubMedCentralCrossRef
27.
go back to reference Wang MY, Chen C, Shao C, Wang SB, Wang AC, Yang YC, et al. Intact long-type DupA protein in Helicobacter pylori is an ATPase involved in multifunctional biological activities. Microb Pathog. 2015;81:53–9.PubMedCrossRef Wang MY, Chen C, Shao C, Wang SB, Wang AC, Yang YC, et al. Intact long-type DupA protein in Helicobacter pylori is an ATPase involved in multifunctional biological activities. Microb Pathog. 2015;81:53–9.PubMedCrossRef
28.
go back to reference Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: Links to genetic instability. Carcinogenesis. 2009;30:1073–81.PubMedCrossRef Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: Links to genetic instability. Carcinogenesis. 2009;30:1073–81.PubMedCrossRef
29.
go back to reference Murata-Kamiya N, Kurashima Y, Teishikata Y, Yamahashi Y, Saito Y, Higashi H, et al. Helicobacter pylori CagA interacts with E-cadherin and deregulates the β-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene. 2007;26:4617–26.PubMedCrossRef Murata-Kamiya N, Kurashima Y, Teishikata Y, Yamahashi Y, Saito Y, Higashi H, et al. Helicobacter pylori CagA interacts with E-cadherin and deregulates the β-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene. 2007;26:4617–26.PubMedCrossRef
30.
go back to reference Lancellotti M, Brocchi M, da Silvedeira W. Bacteria-induced apoptosis: an approach to bacterial pathogenesis. Braz J Morphol Sci. 2006;23:75–86. Lancellotti M, Brocchi M, da Silvedeira W. Bacteria-induced apoptosis: an approach to bacterial pathogenesis. Braz J Morphol Sci. 2006;23:75–86.
31.
go back to reference Akopyants NS, Clifton SW, Kersulyte D, Crabtree JE, Youree BE, Reece CA, et al. Analyses of the cag pathogenicity island of Helicobacter pylori. Mol Microbiol. 1998;28:37–53.PubMedCrossRef Akopyants NS, Clifton SW, Kersulyte D, Crabtree JE, Youree BE, Reece CA, et al. Analyses of the cag pathogenicity island of Helicobacter pylori. Mol Microbiol. 1998;28:37–53.PubMedCrossRef
34.
go back to reference Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, et al. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol. 2004;5:1166–74.PubMedCrossRef Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, et al. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol. 2004;5:1166–74.PubMedCrossRef
38.
go back to reference Backert S, Tegtmeyer N, Fischer W. Composition, structure and function of the Helicobacter pylori cag pathogenicity island encoded type IV secretion system. Future Microbiol. 2015;10:955–65.PubMedCrossRef Backert S, Tegtmeyer N, Fischer W. Composition, structure and function of the Helicobacter pylori cag pathogenicity island encoded type IV secretion system. Future Microbiol. 2015;10:955–65.PubMedCrossRef
39.
go back to reference Saha A, Backert S, Hammond CE, Gooz M, Smolka AJ. Helicobacter pylori CagL Activates ADAM17 to induce repression of the gastric H K-ATPase α subunit. Gastroenterology. 2010;139:239–48.PubMedCrossRef Saha A, Backert S, Hammond CE, Gooz M, Smolka AJ. Helicobacter pylori CagL Activates ADAM17 to induce repression of the gastric H K-ATPase α subunit. Gastroenterology. 2010;139:239–48.PubMedCrossRef
40.
go back to reference Ding SZ, Zheng PY. Helicobacter pylori infection induced gastric cancer; Advance in gastric stem cell research and the remaining challenges. Gut Pathog. 2012;4:1–11.CrossRef Ding SZ, Zheng PY. Helicobacter pylori infection induced gastric cancer; Advance in gastric stem cell research and the remaining challenges. Gut Pathog. 2012;4:1–11.CrossRef
41.
go back to reference Backert S, Clyne M, Tegtmeyer N. Molecular mechanisms of gastric epithelial cell adhesion and injection of CagA by Helicobacter pylori. Cell Commun Signal. 2011;9:1–11.CrossRef Backert S, Clyne M, Tegtmeyer N. Molecular mechanisms of gastric epithelial cell adhesion and injection of CagA by Helicobacter pylori. Cell Commun Signal. 2011;9:1–11.CrossRef
42.
go back to reference Backert S, Ziska E, Brinkmann V, Zimny-Arndt U, Fauconnier A, Jungblut PR, et al. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell Microbiol. 2000;2:155–64.PubMedCrossRef Backert S, Ziska E, Brinkmann V, Zimny-Arndt U, Fauconnier A, Jungblut PR, et al. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell Microbiol. 2000;2:155–64.PubMedCrossRef
43.
go back to reference Tafreshi M, Guan J, Gorrell RJ, Chew N, Xin Y, Deswaerte V, et al. Helicobacter pylori type IV secretion system and its adhesin subunit, CagL, mediate potent inflammatory responses in primary human endothelial cells. Front Cell Infect Microbiol. 2018;8:1–15.CrossRef Tafreshi M, Guan J, Gorrell RJ, Chew N, Xin Y, Deswaerte V, et al. Helicobacter pylori type IV secretion system and its adhesin subunit, CagL, mediate potent inflammatory responses in primary human endothelial cells. Front Cell Infect Microbiol. 2018;8:1–15.CrossRef
44.
go back to reference Chew Y, Chung HY, Lin PY, Wu DC, Huang SK, Kao MC. Outer membrane vesicle production by helicobacter pylori represents an approach for the delivery of virulence factors caga, vaca and urea into human gastric adenocarcinoma (Ags) cells. Int J Mol Sci. 2021;22:3942.PubMedPubMedCentralCrossRef Chew Y, Chung HY, Lin PY, Wu DC, Huang SK, Kao MC. Outer membrane vesicle production by helicobacter pylori represents an approach for the delivery of virulence factors caga, vaca and urea into human gastric adenocarcinoma (Ags) cells. Int J Mol Sci. 2021;22:3942.PubMedPubMedCentralCrossRef
45.
go back to reference Ohnishi N, Yuasa H, Tanaka S, Sawa H, Miura M, Matsui A, et al. Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci USA. 2008;105:1003–8.PubMedPubMedCentralCrossRef Ohnishi N, Yuasa H, Tanaka S, Sawa H, Miura M, Matsui A, et al. Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci USA. 2008;105:1003–8.PubMedPubMedCentralCrossRef
47.
go back to reference Hatakeyama M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat Rev Cancer. 2004;4:688–94.PubMedCrossRef Hatakeyama M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat Rev Cancer. 2004;4:688–94.PubMedCrossRef
48.
go back to reference Rudi J, Kolb C, Maiwald M, Kuck D, Sieg A, Galle PR, et al. Diversity of Helicobacter pylori vacA and cagA genes and relationship to VacA and CagA protein expression, cytotoxin production, and associated disease. J Clin Microbiol. 1998;36:944–8.PubMedPubMedCentralCrossRef Rudi J, Kolb C, Maiwald M, Kuck D, Sieg A, Galle PR, et al. Diversity of Helicobacter pylori vacA and cagA genes and relationship to VacA and CagA protein expression, cytotoxin production, and associated disease. J Clin Microbiol. 1998;36:944–8.PubMedPubMedCentralCrossRef
49.
go back to reference Gaddy JA, Radin JN, Loh JT, Zhang F, Kay Washington M, Peek RM, et al. High dietary salt intake exacerbates Helicobacter pylori-induced gastric carcinogenesis. Infect Immun. 2013;81:2258–67.PubMedPubMedCentralCrossRef Gaddy JA, Radin JN, Loh JT, Zhang F, Kay Washington M, Peek RM, et al. High dietary salt intake exacerbates Helicobacter pylori-induced gastric carcinogenesis. Infect Immun. 2013;81:2258–67.PubMedPubMedCentralCrossRef
50.
go back to reference Xu Y, Jing JJ, Gong YH, Xu Q, Zhang WL, Piao Y, et al. Changes in biological and virulent characteristics of Helicobacter pylori exposed to high salt. Asian Pac J Cancer Prev. 2011;12:2637–41.PubMed Xu Y, Jing JJ, Gong YH, Xu Q, Zhang WL, Piao Y, et al. Changes in biological and virulent characteristics of Helicobacter pylori exposed to high salt. Asian Pac J Cancer Prev. 2011;12:2637–41.PubMed
51.
go back to reference Loh JT, Friedman DB, Piazuelo MB, Bravo LE, Wilson KT, Peek RM, et al. Analysis of helicobacter pylori caga promoter elements required for salt-induced upregulation of caga expression. Infect Immun. 2012;80:3094–106.PubMedPubMedCentralCrossRef Loh JT, Friedman DB, Piazuelo MB, Bravo LE, Wilson KT, Peek RM, et al. Analysis of helicobacter pylori caga promoter elements required for salt-induced upregulation of caga expression. Infect Immun. 2012;80:3094–106.PubMedPubMedCentralCrossRef
52.
go back to reference Baidya AK, Bhattacharya S, Chowdhury R. Role of the flagellar hook-length control protein flik and σ28 in cagA expression in gastric cell-adhered Helicobacter pylori. J Infect Dis. 2015;211:1779–89.PubMedCrossRef Baidya AK, Bhattacharya S, Chowdhury R. Role of the flagellar hook-length control protein flik and σ28 in cagA expression in gastric cell-adhered Helicobacter pylori. J Infect Dis. 2015;211:1779–89.PubMedCrossRef
54.
go back to reference Galperin MY, Frishman D. 11 Towards automated prediction of protein function from microbial genomic sequences. Methods microbiology. Elsevier; 1999. p. 245–63. Galperin MY, Frishman D. 11 Towards automated prediction of protein function from microbial genomic sequences. Methods microbiology. Elsevier; 1999. p. 245–63.
55.
go back to reference Ansari S, Yamaoka Y. Helicobacter pylori virulence factor cytotoxin-associated gene a (Caga)-mediated gastric pathogenicity. Int J Mol Sci. 2020;21:1–16.CrossRef Ansari S, Yamaoka Y. Helicobacter pylori virulence factor cytotoxin-associated gene a (Caga)-mediated gastric pathogenicity. Int J Mol Sci. 2020;21:1–16.CrossRef
56.
go back to reference Zhang XS, Tegtmeyer N, Traube L, Jindal S, Perez-Perez G, Sticht H, et al. A specific A/T polymorphism in western tyrosine phosphorylation b-motifs regulates Helicobacter pylori CagA epithelial cell interactions. PLoS Pathog. 2015;11:1–25.CrossRef Zhang XS, Tegtmeyer N, Traube L, Jindal S, Perez-Perez G, Sticht H, et al. A specific A/T polymorphism in western tyrosine phosphorylation b-motifs regulates Helicobacter pylori CagA epithelial cell interactions. PLoS Pathog. 2015;11:1–25.CrossRef
61.
go back to reference Bronte-Tinkew DM, Terebiznik M, Franco A, Ang M, Ahn D, Mimuro H, et al. Helicobacter pylori cytotoxin-associated gene a activates the signal transducer and activator of transcription 3 pathway in vitro and in vivo. Cancer Res. 2009;69:632–9.PubMedPubMedCentralCrossRef Bronte-Tinkew DM, Terebiznik M, Franco A, Ang M, Ahn D, Mimuro H, et al. Helicobacter pylori cytotoxin-associated gene a activates the signal transducer and activator of transcription 3 pathway in vitro and in vivo. Cancer Res. 2009;69:632–9.PubMedPubMedCentralCrossRef
64.
go back to reference Abadi ATB, Rafiei A, Ajami A, Hosseini V, Taghvaei T, Jones KR, et al. Helicobacter pylori homB, but not cagA, is associated with gastric cancer in Iran. J Clin Microbiol. 2011;49:3191–7.CrossRef Abadi ATB, Rafiei A, Ajami A, Hosseini V, Taghvaei T, Jones KR, et al. Helicobacter pylori homB, but not cagA, is associated with gastric cancer in Iran. J Clin Microbiol. 2011;49:3191–7.CrossRef
65.
go back to reference Abadi ATB, Taghvaei T, Wolfram L, Kusters JG. Infection with Helicobacter pylori strains lacking dupa is associated with an increased risk of gastric ulcer and gastric cancer development. J Med Microbiol. 2012;61:23–30.CrossRef Abadi ATB, Taghvaei T, Wolfram L, Kusters JG. Infection with Helicobacter pylori strains lacking dupa is associated with an increased risk of gastric ulcer and gastric cancer development. J Med Microbiol. 2012;61:23–30.CrossRef
66.
go back to reference Gonçalves Oliveira A, Santos A, Becattini Guerra J, Rocha GA, Camargos Rocha AM, Oliveira CA, et al. babA2- and cagA-positive Helicobacter pylori strains are associated with duodenal ulcer and gastric carcinoma in Brazil. J Clin Microbiol. 2003;41:3964–6.CrossRef Gonçalves Oliveira A, Santos A, Becattini Guerra J, Rocha GA, Camargos Rocha AM, Oliveira CA, et al. babA2- and cagA-positive Helicobacter pylori strains are associated with duodenal ulcer and gastric carcinoma in Brazil. J Clin Microbiol. 2003;41:3964–6.CrossRef
67.
go back to reference Song H, Michel A, Nyrén O, Ekström AM, Pawlita M, Ye W. A CagA-independent cluster of antigens related to the risk of noncardia gastric cancer: Associations between Helicobacter pylori antibodies and gastric adenocarcinoma explored by multiplex serology. Int J Cancer. 2014;134:2942–50.PubMedCrossRef Song H, Michel A, Nyrén O, Ekström AM, Pawlita M, Ye W. A CagA-independent cluster of antigens related to the risk of noncardia gastric cancer: Associations between Helicobacter pylori antibodies and gastric adenocarcinoma explored by multiplex serology. Int J Cancer. 2014;134:2942–50.PubMedCrossRef
68.
go back to reference Sugimoto M, Yamaoka Y. The association of vacA genotype and Helicobacter pylori-related disease in Latin American and African populations. Clin Microbiol Infect. 2009;15:835–42.PubMedPubMedCentralCrossRef Sugimoto M, Yamaoka Y. The association of vacA genotype and Helicobacter pylori-related disease in Latin American and African populations. Clin Microbiol Infect. 2009;15:835–42.PubMedPubMedCentralCrossRef
69.
go back to reference Vega AE, Cortiñas TI, Puig ON, Silva HJ. Molecular characterization and susceptibility testing of Helicobacter pylori strains isolated in Western Argentina. Int J Infect Dis. 2010;14:85.CrossRef Vega AE, Cortiñas TI, Puig ON, Silva HJ. Molecular characterization and susceptibility testing of Helicobacter pylori strains isolated in Western Argentina. Int J Infect Dis. 2010;14:85.CrossRef
70.
go back to reference Wang X, Gong Y, He L, Zhao L, Wang Y, Zhang J, et al. Clinical relevance and distribution of Helicobacter pylori virulence factors in isolates from Chinese patients. Ann Transl Med. 2023;11:301.PubMedPubMedCentralCrossRef Wang X, Gong Y, He L, Zhao L, Wang Y, Zhang J, et al. Clinical relevance and distribution of Helicobacter pylori virulence factors in isolates from Chinese patients. Ann Transl Med. 2023;11:301.PubMedPubMedCentralCrossRef
71.
go back to reference Yamaoka Y, Ojo O, Fujimoto S, Odenbreit S, Haas R, Gutierrez O, et al. Helicobacter pylori outer membrane proteins and gastroduodenal disease. Gut. 2006;55:775–81.PubMedPubMedCentralCrossRef Yamaoka Y, Ojo O, Fujimoto S, Odenbreit S, Haas R, Gutierrez O, et al. Helicobacter pylori outer membrane proteins and gastroduodenal disease. Gut. 2006;55:775–81.PubMedPubMedCentralCrossRef
73.
go back to reference Alsaadi ZH, Kadhim Hindi NK, Al-Marzoqi AH, Memariani M, Kohansal M, Ghasemian A. The association of cagA, vacA, babA2, babB and oipA of Helicobacter pylori with risk of gastric carcinoma development. J Adv Biomed Sci. 2022;12:406–11. Alsaadi ZH, Kadhim Hindi NK, Al-Marzoqi AH, Memariani M, Kohansal M, Ghasemian A. The association of cagA, vacA, babA2, babB and oipA of Helicobacter pylori with risk of gastric carcinoma development. J Adv Biomed Sci. 2022;12:406–11.
74.
go back to reference Aziz F, Chen X, Yang X, Yan Q. Prevalence and correlation with clinical diseases of Helicobacter pylori cagA and vacA genotype among gastric patients from northeast China. Biomed Res Int. 2014;2014:1–8. Aziz F, Chen X, Yang X, Yan Q. Prevalence and correlation with clinical diseases of Helicobacter pylori cagA and vacA genotype among gastric patients from northeast China. Biomed Res Int. 2014;2014:1–8.
75.
go back to reference Baghaei K, Shokrzadeh L, Jagari F, Dabiri H, Yamaoka Y, Bolfion M, et al. Determination of Helicobacter pylori virulence by analysis of the cag pathogenicity island isolated from Iranian population. Dig Liver Dis. 2009;41:634–8.PubMedPubMedCentralCrossRef Baghaei K, Shokrzadeh L, Jagari F, Dabiri H, Yamaoka Y, Bolfion M, et al. Determination of Helicobacter pylori virulence by analysis of the cag pathogenicity island isolated from Iranian population. Dig Liver Dis. 2009;41:634–8.PubMedPubMedCentralCrossRef
76.
go back to reference Elnosh MM, Hamedelnil YF, Elshareef WA, Abugrain AY, Osman EH, Albasha AM, et al. The cagA, cagE, vacA, dupA and iceA1 genes of Helicobacter pylori in Sudanese gastritis patients: distribution and relationship with clinical outcomes and histological alterations. Malays J Microbiol. 2022;18:261–70. Elnosh MM, Hamedelnil YF, Elshareef WA, Abugrain AY, Osman EH, Albasha AM, et al. The cagA, cagE, vacA, dupA and iceA1 genes of Helicobacter pylori in Sudanese gastritis patients: distribution and relationship with clinical outcomes and histological alterations. Malays J Microbiol. 2022;18:261–70.
77.
go back to reference Erzin Y, Koksal V, Altun S, Dobrucali A, Aslan M, Erdamar S, et al. Role of host interleukin 1β gene (IL-1B) and interleukin 1 receptor antagonist gene (IL-1RN) polymorphisms in clinical outcomes in Helicobacter pylori-positive Turkish patients with dyspepsia. J Gastroenterol. 2008;43:705–10.PubMedCrossRef Erzin Y, Koksal V, Altun S, Dobrucali A, Aslan M, Erdamar S, et al. Role of host interleukin 1β gene (IL-1B) and interleukin 1 receptor antagonist gene (IL-1RN) polymorphisms in clinical outcomes in Helicobacter pylori-positive Turkish patients with dyspepsia. J Gastroenterol. 2008;43:705–10.PubMedCrossRef
78.
go back to reference Gao L, Michel A, Weck MN, Arndt V, Pawlita M, Brenner H. Helicobacter pylori infection and gastric cancer risk: evaluation of 15 H. pylori proteins determined by novel multiplex serology. Cancer Res. 2009;69:6164–70.PubMedCrossRef Gao L, Michel A, Weck MN, Arndt V, Pawlita M, Brenner H. Helicobacter pylori infection and gastric cancer risk: evaluation of 15 H. pylori proteins determined by novel multiplex serology. Cancer Res. 2009;69:6164–70.PubMedCrossRef
79.
go back to reference Haddadi MH, Bazargani A, Khashei R, Fattahi MR, Lankarani KB, Moini M, et al. Different distribution of Helicobacter pylori EPIYA- cagA motifs and dupA genes in the upper gastrointestinal diseases and correlation with clinical outcomes in Iranian patients. Gastroenterol Hepatol. 2015;8:S37-46. Haddadi MH, Bazargani A, Khashei R, Fattahi MR, Lankarani KB, Moini M, et al. Different distribution of Helicobacter pylori EPIYA- cagA motifs and dupA genes in the upper gastrointestinal diseases and correlation with clinical outcomes in Iranian patients. Gastroenterol Hepatol. 2015;8:S37-46.
80.
go back to reference Kim IJ, Blanke SR. Remodeling the host environment: modulation of the gastric epithelium by the Helicobacter pylori vacuolating toxin (VacA). Front Cell Infect Microbiol. 2012;2:37.PubMedPubMedCentralCrossRef Kim IJ, Blanke SR. Remodeling the host environment: modulation of the gastric epithelium by the Helicobacter pylori vacuolating toxin (VacA). Front Cell Infect Microbiol. 2012;2:37.PubMedPubMedCentralCrossRef
81.
go back to reference Schmitt W, Haas R. Genetic analysis of the Helicobacter pylori vacuoiating cytotoxin: structural similarities with the IgA protease type of exported protein. Mol Microbiol. 1994;12:307–19.PubMedCrossRef Schmitt W, Haas R. Genetic analysis of the Helicobacter pylori vacuoiating cytotoxin: structural similarities with the IgA protease type of exported protein. Mol Microbiol. 1994;12:307–19.PubMedCrossRef
82.
go back to reference Leunk RD, Johnson PT, David BC, Kraft WG, Morgan DR. Cytotoxic activity in broth-culture filtrates of Campylobacter pylori. J Med Microbiol. 1988;26:93–9.PubMedCrossRef Leunk RD, Johnson PT, David BC, Kraft WG, Morgan DR. Cytotoxic activity in broth-culture filtrates of Campylobacter pylori. J Med Microbiol. 1988;26:93–9.PubMedCrossRef
83.
go back to reference Cover TL, Blanke SR. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol. 2005;3:320–32.PubMedCrossRef Cover TL, Blanke SR. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol. 2005;3:320–32.PubMedCrossRef
84.
go back to reference McClain MS, Beckett AC, Cover TL. Helicobacter pylori vacuolating toxin and gastric cancer. Toxins (Basel). 2017;9:23–5.CrossRef McClain MS, Beckett AC, Cover TL. Helicobacter pylori vacuolating toxin and gastric cancer. Toxins (Basel). 2017;9:23–5.CrossRef
85.
go back to reference Chauhan N, Tay ACY, Marshall BJ, Jain U. Helicobacter pylori VacA, a distinct toxin exerts diverse functionalities in numerous cells: an overview. Helicobacter. 2019;24:1–9.CrossRef Chauhan N, Tay ACY, Marshall BJ, Jain U. Helicobacter pylori VacA, a distinct toxin exerts diverse functionalities in numerous cells: an overview. Helicobacter. 2019;24:1–9.CrossRef
86.
go back to reference De Bernard M, Arico B, Papini E, Rizzuto R, Grandi G, Rappuoli R, et al. Helicobacter pylori toxin VacA induces vacuole formation by acting in the cell cytosol. Mol Microbiol. 1997;26:665–74.PubMedCrossRef De Bernard M, Arico B, Papini E, Rizzuto R, Grandi G, Rappuoli R, et al. Helicobacter pylori toxin VacA induces vacuole formation by acting in the cell cytosol. Mol Microbiol. 1997;26:665–74.PubMedCrossRef
87.
go back to reference McClain MS, Iwamoto H, Cao P, Vinion-Dubiel AD, Li Y, Szabo G, et al. Essential role of a GXXXG motif for membrane channel formation by Helicobacter pylori vacuolating toxin. J Biol Chem. 2003;278:12101–8.PubMedCrossRef McClain MS, Iwamoto H, Cao P, Vinion-Dubiel AD, Li Y, Szabo G, et al. Essential role of a GXXXG motif for membrane channel formation by Helicobacter pylori vacuolating toxin. J Biol Chem. 2003;278:12101–8.PubMedCrossRef
88.
go back to reference Domańska G, Motz C, Meinecke M, Harsman A, Papatheodorou P, Reljic B, et al. Helicobacter pylori VacA toxin/subunit p34: targeting of an anion channel to the inner mitochondrial membrane. PLoS Pathog. 2010;6:1–14.CrossRef Domańska G, Motz C, Meinecke M, Harsman A, Papatheodorou P, Reljic B, et al. Helicobacter pylori VacA toxin/subunit p34: targeting of an anion channel to the inner mitochondrial membrane. PLoS Pathog. 2010;6:1–14.CrossRef
89.
go back to reference Calore F, Genisset C, Casellato A, Rossato M, Codolo G, Esposti MD, et al. Endosome-mitochondria juxtaposition during apoptosis induced by H. pylori VacA. Cell Death Differ. 2010;17:1707–16.PubMedCrossRef Calore F, Genisset C, Casellato A, Rossato M, Codolo G, Esposti MD, et al. Endosome-mitochondria juxtaposition during apoptosis induced by H. pylori VacA. Cell Death Differ. 2010;17:1707–16.PubMedCrossRef
91.
go back to reference Rhead JL, Letley DP, Mohammadi M, Hussein N, Mohagheghi MA, Eshagh Hosseini M, et al. A new Helicobacter pylori vacuolating cytotoxin determinant, the intermediate region is associated with gastric cancer. Gastroenterology. 2007;133:926–36.PubMedCrossRef Rhead JL, Letley DP, Mohammadi M, Hussein N, Mohagheghi MA, Eshagh Hosseini M, et al. A new Helicobacter pylori vacuolating cytotoxin determinant, the intermediate region is associated with gastric cancer. Gastroenterology. 2007;133:926–36.PubMedCrossRef
92.
go back to reference Van Doorn LJ, Figueiredo C, Megraud F, Pena S, Midolo P, Queiroz DMM, et al. Geographic distribution of vacA allelic types of Helicobacter pylori. Gastroenterology. 1999;116:823–30.PubMedCrossRef Van Doorn LJ, Figueiredo C, Megraud F, Pena S, Midolo P, Queiroz DMM, et al. Geographic distribution of vacA allelic types of Helicobacter pylori. Gastroenterology. 1999;116:823–30.PubMedCrossRef
93.
go back to reference Figueiredo C, Machado JC, Pharoah P, Seruca R, Sousa S, Carvalho R, et al. Helicobacter pylori and interleukin 1 genotyping: an opportunity of identify high-risk individuals for gastric carcinoma (multiple letters) [4]. J Natl Cancer Inst. 2002;94:1680–7.PubMedCrossRef Figueiredo C, Machado JC, Pharoah P, Seruca R, Sousa S, Carvalho R, et al. Helicobacter pylori and interleukin 1 genotyping: an opportunity of identify high-risk individuals for gastric carcinoma (multiple letters) [4]. J Natl Cancer Inst. 2002;94:1680–7.PubMedCrossRef
94.
go back to reference Chung C, Olivares A, Torres E, Yilmaz O, Cohen H, Perez-Perez G. Diversity of VacA intermediate region among Helicobacter pylori strains from several regions of the world. J Clin Microbiol. 2010;48:690–6.PubMedPubMedCentralCrossRef Chung C, Olivares A, Torres E, Yilmaz O, Cohen H, Perez-Perez G. Diversity of VacA intermediate region among Helicobacter pylori strains from several regions of the world. J Clin Microbiol. 2010;48:690–6.PubMedPubMedCentralCrossRef
95.
go back to reference Kountouras J, Boziki M, Polyzos SA, Katsinelos P, Gavalas E, Zeglinas C, et al. Impact of reactive oxygen species generation on Helicobacter pylori-related extragastric diseases: a hypothesis. Free Radic Res. 2017;51:73–9.PubMedCrossRef Kountouras J, Boziki M, Polyzos SA, Katsinelos P, Gavalas E, Zeglinas C, et al. Impact of reactive oxygen species generation on Helicobacter pylori-related extragastric diseases: a hypothesis. Free Radic Res. 2017;51:73–9.PubMedCrossRef
96.
go back to reference Molnar B, Galamb O, Sipos F, Leiszter K, Tulassay Z. Molecular pathogenesis of Helicobacter pylori infection: the role of bacterial virulence factors. Dig Dis. 2010;28:604–8.PubMedCrossRef Molnar B, Galamb O, Sipos F, Leiszter K, Tulassay Z. Molecular pathogenesis of Helicobacter pylori infection: the role of bacterial virulence factors. Dig Dis. 2010;28:604–8.PubMedCrossRef
97.
go back to reference Bartchewsky W, Martini MR, Masiero M, Squassoni AC, Alvarez MC, Ladeira MS, et al. Effect of Helicobacter pylori infection on IL-8, IL-1β and COX-2 expression in patients with chronic gastritis and gastric cancer. Scand J Gastroenterol. 2009;44:153–61.PubMedCrossRef Bartchewsky W, Martini MR, Masiero M, Squassoni AC, Alvarez MC, Ladeira MS, et al. Effect of Helicobacter pylori infection on IL-8, IL-1β and COX-2 expression in patients with chronic gastritis and gastric cancer. Scand J Gastroenterol. 2009;44:153–61.PubMedCrossRef
98.
go back to reference Palframan SL, Kwok T, Gabriel K. Vacuolating cytotoxin A (VacA), a key toxin for Helicobacter pylori pathogenesis. Front Cell Infect Microbiol. 2012;2:92.PubMedPubMedCentralCrossRef Palframan SL, Kwok T, Gabriel K. Vacuolating cytotoxin A (VacA), a key toxin for Helicobacter pylori pathogenesis. Front Cell Infect Microbiol. 2012;2:92.PubMedPubMedCentralCrossRef
99.
go back to reference Schmidt HMA, Andres S, Nilsson C, Kovach Z, Kaakoush NO, Engstrand L, et al. The cag PAI is intact and functional but HP0521 varies significantly in Helicobacter pylori isolates from Malaysia and Singapore. Eur J Clin Microbiol Infect Dis. 2010;29:439–51.PubMedCrossRef Schmidt HMA, Andres S, Nilsson C, Kovach Z, Kaakoush NO, Engstrand L, et al. The cag PAI is intact and functional but HP0521 varies significantly in Helicobacter pylori isolates from Malaysia and Singapore. Eur J Clin Microbiol Infect Dis. 2010;29:439–51.PubMedCrossRef
100.
go back to reference Shiota S, Cruz M, Abreu JAJ, Mitsui T, Terao H, Disla M, et al. Virulence genes of Helicobacter pylori in the Dominican Republic. J Med Microbiol. 2014;63:1189–96.PubMedPubMedCentralCrossRef Shiota S, Cruz M, Abreu JAJ, Mitsui T, Terao H, Disla M, et al. Virulence genes of Helicobacter pylori in the Dominican Republic. J Med Microbiol. 2014;63:1189–96.PubMedPubMedCentralCrossRef
101.
go back to reference Yamaoka Y, Kikuchi S, ElZimaity HMT, Gutierrez O, Osato MS, Graham DY. Importance of Helicobacter pylori oipA in clinical presentation, gastric inflammation, and mucosal interleukin 8 production. Gastroenterology. 2002;123:414–24.PubMedCrossRef Yamaoka Y, Kikuchi S, ElZimaity HMT, Gutierrez O, Osato MS, Graham DY. Importance of Helicobacter pylori oipA in clinical presentation, gastric inflammation, and mucosal interleukin 8 production. Gastroenterology. 2002;123:414–24.PubMedCrossRef
102.
go back to reference Zhang Z, Zheng Q, Chen X, Xiao S, Liu W, Lu H. The Helicobacter pylori duodenal ulcer promoting gene, dupA in China. BMC Gastroenterol. 2008;8:1–6.CrossRef Zhang Z, Zheng Q, Chen X, Xiao S, Liu W, Lu H. The Helicobacter pylori duodenal ulcer promoting gene, dupA in China. BMC Gastroenterol. 2008;8:1–6.CrossRef
104.
go back to reference Khamis AS, Al-Jibouri LF, Al-Marzoqi AH, Shalan AA, Al-Taee ZM, Al Morshdi SF, et al. Helicobacter pylori genotype as predicts risk of (Ulcer disease, gastric cancer, non-ulcer dyspepsia); role of some genes mediated signaling in infection. J Pharm Sci Res. 2018;10:1373–6. Khamis AS, Al-Jibouri LF, Al-Marzoqi AH, Shalan AA, Al-Taee ZM, Al Morshdi SF, et al. Helicobacter pylori genotype as predicts risk of (Ulcer disease, gastric cancer, non-ulcer dyspepsia); role of some genes mediated signaling in infection. J Pharm Sci Res. 2018;10:1373–6.
105.
go back to reference Ohno T, Sugimoto M, Nagashima A, Ogiwara H, Vilaichone RK, Mahachai V, et al. Relationship between Helicobacter pylori hopQ genotype and clinical outcome in Asian and Western opulations. J Gastroenterol Hepatol. 2009;24:462–8.PubMedPubMedCentralCrossRef Ohno T, Sugimoto M, Nagashima A, Ogiwara H, Vilaichone RK, Mahachai V, et al. Relationship between Helicobacter pylori hopQ genotype and clinical outcome in Asian and Western opulations. J Gastroenterol Hepatol. 2009;24:462–8.PubMedPubMedCentralCrossRef
106.
go back to reference Román-Román A, Martínez-Carrillo DN, Atrisco-Morales J, Azúcar-Heziquio JC, Cuevas-Caballero AS, Castañón-Sánchez CA, et al. Helicobacter pylori vacA s1m1 genotype but not cagA or babA2 increase the risk of ulcer and gastric cancer in patients from Southern Mexico. Gut Pathog BioMed Cent. 2017;9:1–12. Román-Román A, Martínez-Carrillo DN, Atrisco-Morales J, Azúcar-Heziquio JC, Cuevas-Caballero AS, Castañón-Sánchez CA, et al. Helicobacter pylori vacA s1m1 genotype but not cagA or babA2 increase the risk of ulcer and gastric cancer in patients from Southern Mexico. Gut Pathog BioMed Cent. 2017;9:1–12.
107.
go back to reference Saxena A, Shukla S, Prasad KN, Ghoshal UC. Virulence attributes of Helicobacter pylori isolates and their association with gastroduodenal disease. Indian J Med Res. 2011;133:514–20.PubMedPubMedCentral Saxena A, Shukla S, Prasad KN, Ghoshal UC. Virulence attributes of Helicobacter pylori isolates and their association with gastroduodenal disease. Indian J Med Res. 2011;133:514–20.PubMedPubMedCentral
108.
go back to reference Lu H, Hsu PI, Graham DY, Yamaoka Y. Duodenal ulcer promoting gene of Helicobacter pylori. Gastroenterology. 2005;128:833–48.PubMedCrossRef Lu H, Hsu PI, Graham DY, Yamaoka Y. Duodenal ulcer promoting gene of Helicobacter pylori. Gastroenterology. 2005;128:833–48.PubMedCrossRef
109.
go back to reference Pereira WN, Ferraz MA, Zabaglia LM, de Labio RW, Orcini WA, Bianchi Ximenez JP, et al. Association among H. pylori virulence markers dupA, cagA and vacAin Brazilian patients. J Venom Anim Toxins Incl Trop Dis. 2014;20:2–6.CrossRef Pereira WN, Ferraz MA, Zabaglia LM, de Labio RW, Orcini WA, Bianchi Ximenez JP, et al. Association among H. pylori virulence markers dupA, cagA and vacAin Brazilian patients. J Venom Anim Toxins Incl Trop Dis. 2014;20:2–6.CrossRef
110.
go back to reference Shiota S, Matsunari O, Watada M, Hanada K, Yamaoka Y. Systematic review and meta-analysis: the relationship between the Helicobacter pylori dupA gene and clinical outcomes. Gut Pathog. 2010;2:1–6.CrossRef Shiota S, Matsunari O, Watada M, Hanada K, Yamaoka Y. Systematic review and meta-analysis: the relationship between the Helicobacter pylori dupA gene and clinical outcomes. Gut Pathog. 2010;2:1–6.CrossRef
111.
go back to reference Alam J, Sarkar A, Karmakar BC, Ganguly M, Paul S, Mukhopadhyay AK. Novel virulence factor dupA of Helicobacter pylori as an important risk determinant for disease manifestation: an overview. World J Gastroenterol. 2020;26:4739–52.PubMedPubMedCentralCrossRef Alam J, Sarkar A, Karmakar BC, Ganguly M, Paul S, Mukhopadhyay AK. Novel virulence factor dupA of Helicobacter pylori as an important risk determinant for disease manifestation: an overview. World J Gastroenterol. 2020;26:4739–52.PubMedPubMedCentralCrossRef
112.
go back to reference Argent RH, Burette A, Miendje Deyi VY, Atherton JC. The presence of dupA in Helicobacter pylori is not significantly associated with duodenal ulceration in Belgium, South Africa, China, or North America. Clin Infect Dis. 2007;45:1204–6.PubMedCrossRef Argent RH, Burette A, Miendje Deyi VY, Atherton JC. The presence of dupA in Helicobacter pylori is not significantly associated with duodenal ulceration in Belgium, South Africa, China, or North America. Clin Infect Dis. 2007;45:1204–6.PubMedCrossRef
113.
go back to reference Arachchi HSJ, Kalra V, Lal B, Bhatia V, Baba CS, Chakravarthy S, et al. Prevalence of duodenal ulcer-promoting gene (dupA) of Helicobacter pylori in patients with duodenal ulcer in North Indian population. Helicobacter. 2007;12:591–7.PubMedCrossRef Arachchi HSJ, Kalra V, Lal B, Bhatia V, Baba CS, Chakravarthy S, et al. Prevalence of duodenal ulcer-promoting gene (dupA) of Helicobacter pylori in patients with duodenal ulcer in North Indian population. Helicobacter. 2007;12:591–7.PubMedCrossRef
114.
go back to reference Abadi ATB, Perez-Perez G. Role of dupA in virulence of Helicobacter pylori. World J Gastroenterol. 2016;22:10118–23.CrossRef Abadi ATB, Perez-Perez G. Role of dupA in virulence of Helicobacter pylori. World J Gastroenterol. 2016;22:10118–23.CrossRef
116.
go back to reference Abadi A. The Helicobacter pylori dupA: a novel biomarker for digestive diseases. Front Med. 2014;1:13. Abadi A. The Helicobacter pylori dupA: a novel biomarker for digestive diseases. Front Med. 2014;1:13.
117.
go back to reference Takahashi A, Shiota S, Matsunari O, Watada M, Suzuki R, Nakachi S, et al. Intact long-type dupa as a marker for gastroduodenal diseases in Okinawan Subpopulation Japan. Helicobacter. 2013;18:66–72.PubMedCrossRef Takahashi A, Shiota S, Matsunari O, Watada M, Suzuki R, Nakachi S, et al. Intact long-type dupa as a marker for gastroduodenal diseases in Okinawan Subpopulation Japan. Helicobacter. 2013;18:66–72.PubMedCrossRef
118.
go back to reference Yamaoka Y. Roles of the plasticity regions of Helicobacter pylori in gastroduodenal pathogenesis. J Med Microbiol. 2008;57:545–53.PubMedCrossRef Yamaoka Y. Roles of the plasticity regions of Helicobacter pylori in gastroduodenal pathogenesis. J Med Microbiol. 2008;57:545–53.PubMedCrossRef
120.
go back to reference Schmidt HMA, Andres S, Kaakoush NO, Engstrand L, Eriksson L, Goh KL, et al. The prevalence of the duodenal ulcer promoting gene (dupA) in Helicobacter pylori isolates varies by ethnic group and is not universally associated with disease development: a case-control study. Gut Pathog. 2009;1:1–8.CrossRef Schmidt HMA, Andres S, Kaakoush NO, Engstrand L, Eriksson L, Goh KL, et al. The prevalence of the duodenal ulcer promoting gene (dupA) in Helicobacter pylori isolates varies by ethnic group and is not universally associated with disease development: a case-control study. Gut Pathog. 2009;1:1–8.CrossRef
122.
go back to reference Douraghi M, Mohammadi M, Oghalaie A, Abdirad A, Mohagheghi MA, Hosseini ME, et al. dupA as a risk determinant in Helicobacter pylori infection. J Med Microbiol. 2008;57:554–62.PubMedCrossRef Douraghi M, Mohammadi M, Oghalaie A, Abdirad A, Mohagheghi MA, Hosseini ME, et al. dupA as a risk determinant in Helicobacter pylori infection. J Med Microbiol. 2008;57:554–62.PubMedCrossRef
123.
go back to reference Gomes LI, Rocha GA, Rocha AMC, Soares TF, Oliveira CA, Bittencourt PFS, et al. Lack of association between Helicobacter pylori infection with dupA-positive strains and gastroduodenal diseases in Brazilian patients. Int J Med Microbiol. 2008;298:223–30.PubMedCrossRef Gomes LI, Rocha GA, Rocha AMC, Soares TF, Oliveira CA, Bittencourt PFS, et al. Lack of association between Helicobacter pylori infection with dupA-positive strains and gastroduodenal diseases in Brazilian patients. Int J Med Microbiol. 2008;298:223–30.PubMedCrossRef
124.
go back to reference Jung SW, Sugimoto M, Shiota S, Graham DY, Yamaoka Y. The intact dupA cluster is a more reliable Helicobacter pylori virulence marker than dupA alone. Infect Immun. 2012;80:381–7.PubMedPubMedCentralCrossRef Jung SW, Sugimoto M, Shiota S, Graham DY, Yamaoka Y. The intact dupA cluster is a more reliable Helicobacter pylori virulence marker than dupA alone. Infect Immun. 2012;80:381–7.PubMedPubMedCentralCrossRef
126.
go back to reference Ladeira MSP, Bueno RCA, Dos Santos BF, Pinto CLS, Prado RP, Silveira MG, et al. Relationship among oxidative DNA damage, gastric mucosal density and the relevance of cagA, vacA and iceA genotypes of Helicobacter pylori. Dig Dis Sci. 2008;53:248–55.PubMedCrossRef Ladeira MSP, Bueno RCA, Dos Santos BF, Pinto CLS, Prado RP, Silveira MG, et al. Relationship among oxidative DNA damage, gastric mucosal density and the relevance of cagA, vacA and iceA genotypes of Helicobacter pylori. Dig Dis Sci. 2008;53:248–55.PubMedCrossRef
128.
go back to reference Ma YJ, Duan GC, Zhang RG, Fan QT, Zhang WD. Mutation of iceA in Helicobacter pylori compromised IL-8 induction from human gastric epithelial cells. J Basic Microbiol. 2010;50:83–8.CrossRef Ma YJ, Duan GC, Zhang RG, Fan QT, Zhang WD. Mutation of iceA in Helicobacter pylori compromised IL-8 induction from human gastric epithelial cells. J Basic Microbiol. 2010;50:83–8.CrossRef
129.
go back to reference Chiurillo MA, Moran Y, Cañas M, Valderrama E, Alvarez A, Armanie E. Combination of Helicobacter pylori-iceA2 and proinflammatory interleukin-1 polymorphisms is associated with the severity of histological changes in Venezuelan chronic gastritis patients. FEMS Immunol Med Microbiol. 2010;59:170–6.PubMedCrossRef Chiurillo MA, Moran Y, Cañas M, Valderrama E, Alvarez A, Armanie E. Combination of Helicobacter pylori-iceA2 and proinflammatory interleukin-1 polymorphisms is associated with the severity of histological changes in Venezuelan chronic gastritis patients. FEMS Immunol Med Microbiol. 2010;59:170–6.PubMedCrossRef
130.
go back to reference Baj J, Forma A, Sitarz M, Portincasa P, Garruti G, Krasowska D, et al. Helicobacter pylori virulence factors—mechanisms of bacterial pathogenicity in the gastric microenvironment. Cells. 2021;10:1–37. Baj J, Forma A, Sitarz M, Portincasa P, Garruti G, Krasowska D, et al. Helicobacter pylori virulence factors—mechanisms of bacterial pathogenicity in the gastric microenvironment. Cells. 2021;10:1–37.
131.
go back to reference Talebi BAA, Taghvaei T, Mohabbati MA, Vaira G, Vaira D. High correlation of babA2-positive strains of Helicobacter pylori with the presence of gastric cancer. Intern Emerg Med. 2013;8:497–501.CrossRef Talebi BAA, Taghvaei T, Mohabbati MA, Vaira G, Vaira D. High correlation of babA2-positive strains of Helicobacter pylori with the presence of gastric cancer. Intern Emerg Med. 2013;8:497–501.CrossRef
132.
go back to reference Chomvarin C, Namwat W, Chaicumpar K, Mairiang P, Sangchan A, Sripa B, et al. Prevalence of Helicobacter pylori vacA, cagA, cagE, iceA and babA2 genotypes in Thai dyspeptic patients. Int J Infect Dis. 2008;12:30–6.PubMedCrossRef Chomvarin C, Namwat W, Chaicumpar K, Mairiang P, Sangchan A, Sripa B, et al. Prevalence of Helicobacter pylori vacA, cagA, cagE, iceA and babA2 genotypes in Thai dyspeptic patients. Int J Infect Dis. 2008;12:30–6.PubMedCrossRef
133.
go back to reference Erzin Y, Koksal V, Altun S, Dobrucali A, Aslan M, Erdamar S, et al. Prevalence of Helicobacter pylori vacA, cagA, cagE, iceA, babA2 genotypes and correlation with clinical outcome in Turkish patients with dyspepsia. Helicobacter. 2006;11:574–80.PubMedCrossRef Erzin Y, Koksal V, Altun S, Dobrucali A, Aslan M, Erdamar S, et al. Prevalence of Helicobacter pylori vacA, cagA, cagE, iceA, babA2 genotypes and correlation with clinical outcome in Turkish patients with dyspepsia. Helicobacter. 2006;11:574–80.PubMedCrossRef
134.
go back to reference Han YH, Liu WZ, Zhu HY, Xiao SD. Clinical relevance if iceA and babA2 genotypes of Helicobacter pylori in a Shanghai population. Chin J Dig Dis. 2004;5:181–5.PubMedCrossRef Han YH, Liu WZ, Zhu HY, Xiao SD. Clinical relevance if iceA and babA2 genotypes of Helicobacter pylori in a Shanghai population. Chin J Dig Dis. 2004;5:181–5.PubMedCrossRef
135.
go back to reference Kim SM, Kwon CH, Shin N, Park DY, Moon HJ, Kim GH, et al. Decreased Muc5AC expression is associated with poor prognosis in gastric cancer. Int J Cancer. 2014;134:114–24.PubMedCrossRef Kim SM, Kwon CH, Shin N, Park DY, Moon HJ, Kim GH, et al. Decreased Muc5AC expression is associated with poor prognosis in gastric cancer. Int J Cancer. 2014;134:114–24.PubMedCrossRef
136.
go back to reference Ricci V, Giannouli M, Romano M, Zarrilli R. Helicobacter pylori gamma-glutamyl transpeptidase and its pathogenic role. World J Gastroenterol. 2014;20:630–8.PubMedPubMedCentralCrossRef Ricci V, Giannouli M, Romano M, Zarrilli R. Helicobacter pylori gamma-glutamyl transpeptidase and its pathogenic role. World J Gastroenterol. 2014;20:630–8.PubMedPubMedCentralCrossRef
137.
go back to reference Chiozzi V, Mazzini G, Oldani A, Sciullo A, Ventura U, Romano M, et al. Relationship between VacA toxin and ammonia in Helicobacter pylori-induced apoptosis in human gastric epithelial cells. J Physiol Pharmacol. 2009;60:23–30.PubMed Chiozzi V, Mazzini G, Oldani A, Sciullo A, Ventura U, Romano M, et al. Relationship between VacA toxin and ammonia in Helicobacter pylori-induced apoptosis in human gastric epithelial cells. J Physiol Pharmacol. 2009;60:23–30.PubMed
138.
go back to reference Flahou B, Haesebrouck F, Chiers K, Van Deun K, De Smet L, Devreese B, et al. Gastric epithelial cell death caused by Helicobacter suis and Helicobacter pylori γ-glutamyl transpeptidase is mainly glutathione degradation-dependent. Cell Microbiol. 2011;13:1933–55.PubMedCrossRef Flahou B, Haesebrouck F, Chiers K, Van Deun K, De Smet L, Devreese B, et al. Gastric epithelial cell death caused by Helicobacter suis and Helicobacter pylori γ-glutamyl transpeptidase is mainly glutathione degradation-dependent. Cell Microbiol. 2011;13:1933–55.PubMedCrossRef
139.
go back to reference Kim KM, Lee SG, Park MG, Song JY, Kang HL, Lee WK, et al. γ-Glutamyltranspeptidase of Helicobacter pylori induces mitochondria-mediated apoptosis in AGS cells. Biochem Biophys Res Commun. 2007;355:562–7.PubMedCrossRef Kim KM, Lee SG, Park MG, Song JY, Kang HL, Lee WK, et al. γ-Glutamyltranspeptidase of Helicobacter pylori induces mitochondria-mediated apoptosis in AGS cells. Biochem Biophys Res Commun. 2007;355:562–7.PubMedCrossRef
140.
go back to reference Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol. 2001;39:1452–63.PubMedCrossRef Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol. 2001;39:1452–63.PubMedCrossRef
141.
go back to reference Kim KM, Lee SG, Kim JM, Kim DS, Song JY, Kang HL, et al. Helicobacter pylori γ-glutamyltranspeptidase induces cell cycle arrest at the G1-S phase transition. J Microbiol. 2010;48:372–7.PubMedCrossRef Kim KM, Lee SG, Kim JM, Kim DS, Song JY, Kang HL, et al. Helicobacter pylori γ-glutamyltranspeptidase induces cell cycle arrest at the G1-S phase transition. J Microbiol. 2010;48:372–7.PubMedCrossRef
142.
go back to reference Boonyanugomol W, Chomvarin C, Song JY, Kim KM, Kim JM, Cho MJ, et al. Effects of Helicobacter pylori gamma-glutamyltranspeptidase on apoptosis and inflammation in human biliary cells. Dig Dis Sci. 2012;57:2615–24.PubMedCrossRef Boonyanugomol W, Chomvarin C, Song JY, Kim KM, Kim JM, Cho MJ, et al. Effects of Helicobacter pylori gamma-glutamyltranspeptidase on apoptosis and inflammation in human biliary cells. Dig Dis Sci. 2012;57:2615–24.PubMedCrossRef
143.
go back to reference Busiello I, Acquaviva R, Popolo A, Blanchard T, Ricci V, Romano M, et al. Helicobacter pylori gamma-glutamyltranspeptidase upregulates COX-2 and EGF-related peptide expression in human gastric cells. Cell Microbiol. 2004;6:255–67.PubMedCrossRef Busiello I, Acquaviva R, Popolo A, Blanchard T, Ricci V, Romano M, et al. Helicobacter pylori gamma-glutamyltranspeptidase upregulates COX-2 and EGF-related peptide expression in human gastric cells. Cell Microbiol. 2004;6:255–67.PubMedCrossRef
145.
go back to reference Chevalier C, Thiberge JM, Ferrero RL, Labigne A. Essential role of Helicobacter pylori γ-glutamyltranspeptidase for the colonization of the gastric mucosa of mice. Mol Microbiol. 1999;31:1359–72.PubMedCrossRef Chevalier C, Thiberge JM, Ferrero RL, Labigne A. Essential role of Helicobacter pylori γ-glutamyltranspeptidase for the colonization of the gastric mucosa of mice. Mol Microbiol. 1999;31:1359–72.PubMedCrossRef
146.
go back to reference Shibayama K, Wachino JI, Arakawa Y, Saidijam M, Rutherford NG, Henderson PJF. Metabolism of glutamine and glutathione via γ-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism. Mol Microbiol. 2007;64:396–406.PubMedCrossRef Shibayama K, Wachino JI, Arakawa Y, Saidijam M, Rutherford NG, Henderson PJF. Metabolism of glutamine and glutathione via γ-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism. Mol Microbiol. 2007;64:396–406.PubMedCrossRef
148.
go back to reference Saini M, Kashyap A, Bindal S, Saini K, Gupta R. Bacterial gamma-glutamyl transpeptidase, an emerging biocatalyst: insights into structure-function relationship and its biotechnological applications. Front Microbiol. 2021;12:1–30.CrossRef Saini M, Kashyap A, Bindal S, Saini K, Gupta R. Bacterial gamma-glutamyl transpeptidase, an emerging biocatalyst: insights into structure-function relationship and its biotechnological applications. Front Microbiol. 2021;12:1–30.CrossRef
149.
go back to reference Valenzuela M, Bravo D, Canales J, Sanhueza C, Díaz N, Almarza O, et al. Helicobacter pylori-induced loss of survivin and gastric cell viability is attributable to secreted bacterial gamma-glutamyl transpeptidase activity. J Infect Dis. 2013;208:1131–41.PubMedCrossRef Valenzuela M, Bravo D, Canales J, Sanhueza C, Díaz N, Almarza O, et al. Helicobacter pylori-induced loss of survivin and gastric cell viability is attributable to secreted bacterial gamma-glutamyl transpeptidase activity. J Infect Dis. 2013;208:1131–41.PubMedCrossRef
150.
go back to reference Hoshino H, Tsuchida A, Kametani K, Mori M, Nishizawa T, Suzuki T, et al. Membrane-associated activation of cholesterol α-glucosyltransferase, an enzyme responsible for biosynthesis of cholesteryl-α-d-glucopyranoside in Helicobacter pylori critical for its survival. J Histochem Cytochem. 2011;59:98–105.PubMedPubMedCentralCrossRef Hoshino H, Tsuchida A, Kametani K, Mori M, Nishizawa T, Suzuki T, et al. Membrane-associated activation of cholesterol α-glucosyltransferase, an enzyme responsible for biosynthesis of cholesteryl-α-d-glucopyranoside in Helicobacter pylori critical for its survival. J Histochem Cytochem. 2011;59:98–105.PubMedPubMedCentralCrossRef
151.
go back to reference Morey P, Pfannkuch L, Pang E, Boccellato F, Sigal M, Imai-Matsushima A, et al. Helicobacter pylori depletes cholesterol in gastric glands to prevent interferon gamma signaling and escape the inflammatory response. Gastroenterology. 2018;154:1391–404.PubMedCrossRef Morey P, Pfannkuch L, Pang E, Boccellato F, Sigal M, Imai-Matsushima A, et al. Helicobacter pylori depletes cholesterol in gastric glands to prevent interferon gamma signaling and escape the inflammatory response. Gastroenterology. 2018;154:1391–404.PubMedCrossRef
152.
go back to reference Wang HJ, Cheng WC, Cheng HH, Lai CH, Wang WC. Helicobacter pylori cholesteryl glucosides interfere with host membrane phase and affect type IV secretion system function during infection in AGS cells. Mol Microbiol. 2012;83:67–84.PubMedCrossRef Wang HJ, Cheng WC, Cheng HH, Lai CH, Wang WC. Helicobacter pylori cholesteryl glucosides interfere with host membrane phase and affect type IV secretion system function during infection in AGS cells. Mol Microbiol. 2012;83:67–84.PubMedCrossRef
153.
go back to reference Lai CH, Huang JC, Cheng HH, Wu MC, Huang MZ, Hsu HY, et al. Helicobacter pylori cholesterol glucosylation modulates autophagy for increasing intracellular survival in macrophages. Cell Microbiol. 2018;20:1–11.CrossRef Lai CH, Huang JC, Cheng HH, Wu MC, Huang MZ, Hsu HY, et al. Helicobacter pylori cholesterol glucosylation modulates autophagy for increasing intracellular survival in macrophages. Cell Microbiol. 2018;20:1–11.CrossRef
154.
go back to reference Lee H, Kobayashi M, Wang P, Nakayama J, Seeberger PH, Fukuda M. Expression cloning of cholesterol α-glucosyltransferase, a unique enzyme that can be inhibited by natural antibiotic gastric mucin O-glycans, from Helicobacter pylori. Biochem Biophys Res Commun. 2006;349:1235–41.PubMedCrossRef Lee H, Kobayashi M, Wang P, Nakayama J, Seeberger PH, Fukuda M. Expression cloning of cholesterol α-glucosyltransferase, a unique enzyme that can be inhibited by natural antibiotic gastric mucin O-glycans, from Helicobacter pylori. Biochem Biophys Res Commun. 2006;349:1235–41.PubMedCrossRef
155.
go back to reference Lusini P, Figura N, Valassina M, Roviello F, Vindigni C, Trabalzini L, et al. Increased phospholipase activity in Helicobacter pylori strains isolated from patients with gastric carcinoma. Dig Liver Dis. 2005;37:232–9.PubMedCrossRef Lusini P, Figura N, Valassina M, Roviello F, Vindigni C, Trabalzini L, et al. Increased phospholipase activity in Helicobacter pylori strains isolated from patients with gastric carcinoma. Dig Liver Dis. 2005;37:232–9.PubMedCrossRef
156.
go back to reference Sitaraman R, Israel DA, Romero-Gallo J, Peek RM. Cell-associated hemolysis induced by Helicobacter pylori is mediated by phospholipases with mitogen-activated protein kinase-activating properties. J Clin Microbiol. 2012;50:1014–8.PubMedPubMedCentralCrossRef Sitaraman R, Israel DA, Romero-Gallo J, Peek RM. Cell-associated hemolysis induced by Helicobacter pylori is mediated by phospholipases with mitogen-activated protein kinase-activating properties. J Clin Microbiol. 2012;50:1014–8.PubMedPubMedCentralCrossRef
157.
go back to reference Schmidt TP, Perna AM, Fugmann T, Böhm M, Hiss J, Haller S, et al. Identification of E-cadherin signature motifs functioning as cleavage sites for Helicobacter pylori HtrA. Sci Rep. 2016;6:1–12.CrossRef Schmidt TP, Perna AM, Fugmann T, Böhm M, Hiss J, Haller S, et al. Identification of E-cadherin signature motifs functioning as cleavage sites for Helicobacter pylori HtrA. Sci Rep. 2016;6:1–12.CrossRef
158.
go back to reference Waskito LA, Salama NR, Yamaoka Y. Pathogenesis of Helicobacter pylori infection. Helicobacter. 2018;23:1–6.CrossRef Waskito LA, Salama NR, Yamaoka Y. Pathogenesis of Helicobacter pylori infection. Helicobacter. 2018;23:1–6.CrossRef
159.
go back to reference Zawilak-Pawlik A, Zarzecka U, Żyła-Uklejewicz D, Lach J, Strapagiel D, Tegtmeyer N, et al. Establishment of serine protease htrA mutants in Helicobacter pylori is associated with secA mutations. Sci Rep. 2019;9:1–13.CrossRef Zawilak-Pawlik A, Zarzecka U, Żyła-Uklejewicz D, Lach J, Strapagiel D, Tegtmeyer N, et al. Establishment of serine protease htrA mutants in Helicobacter pylori is associated with secA mutations. Sci Rep. 2019;9:1–13.CrossRef
161.
go back to reference Sharafutdinov I, Tegtmeyer N, Linz B, Rohde M, Vieth M, Tay A, et al. A single-nucleotide polymorphism in Helicobacter pylori promotes gastric cancer development. Cell Host Microbe. 2023;31:1345–58.PubMedCrossRef Sharafutdinov I, Tegtmeyer N, Linz B, Rohde M, Vieth M, Tay A, et al. A single-nucleotide polymorphism in Helicobacter pylori promotes gastric cancer development. Cell Host Microbe. 2023;31:1345–58.PubMedCrossRef
162.
go back to reference Tegtmeyer N, Moodley Y, Yamaoka Y, Pernitzsch SR, Schmidt V, Traverso FR, et al. Characterisation of worldwide Helicobacter pylori strains reveals genetic conservation and essentiality of serine protease HtrA. Mol Microbiol. 2016;99:925–44.PubMedCrossRef Tegtmeyer N, Moodley Y, Yamaoka Y, Pernitzsch SR, Schmidt V, Traverso FR, et al. Characterisation of worldwide Helicobacter pylori strains reveals genetic conservation and essentiality of serine protease HtrA. Mol Microbiol. 2016;99:925–44.PubMedCrossRef
163.
go back to reference Nishioka H, Baesso I, Semenzato G, Trentin L, Rappuoli R, Del Giudice G, et al. The neutrophil-activating protein of Helicobacter pylori (HP-NAP) activates the MAPK pathway in human neutrophils. Eur J Immunol. 2003;33:840–9.PubMedCrossRef Nishioka H, Baesso I, Semenzato G, Trentin L, Rappuoli R, Del Giudice G, et al. The neutrophil-activating protein of Helicobacter pylori (HP-NAP) activates the MAPK pathway in human neutrophils. Eur J Immunol. 2003;33:840–9.PubMedCrossRef
165.
go back to reference Montemurro P, Barbuti G, Dundon WG, Del Giudice G, Rappuoli R, Colucci M, et al. Helicobacter pylori neutrophil-activating protein stimulates tissue factor and plasminogen activator inhibitor-2 production by human blood mononuclear cells. J Infect Dis. 2001;183:1055–62.PubMedCrossRef Montemurro P, Barbuti G, Dundon WG, Del Giudice G, Rappuoli R, Colucci M, et al. Helicobacter pylori neutrophil-activating protein stimulates tissue factor and plasminogen activator inhibitor-2 production by human blood mononuclear cells. J Infect Dis. 2001;183:1055–62.PubMedCrossRef
166.
go back to reference Fu HW. Helicobacter pylori neutrophil-activating protein: from molecular pathogenesis to clinical applications. World J Gastroenterol. 2014;20:5294–301.PubMedPubMedCentralCrossRef Fu HW. Helicobacter pylori neutrophil-activating protein: from molecular pathogenesis to clinical applications. World J Gastroenterol. 2014;20:5294–301.PubMedPubMedCentralCrossRef
167.
go back to reference Codolo G, Fassan M, Munari F, Volpe A, Bassi P, Rugge M, et al. HP-NAP inhibits the growth of bladder cancer in mice by activating a cytotoxic Th1 response. Cancer Immunol Immunother. 2012;61:31–40.PubMedCrossRef Codolo G, Fassan M, Munari F, Volpe A, Bassi P, Rugge M, et al. HP-NAP inhibits the growth of bladder cancer in mice by activating a cytotoxic Th1 response. Cancer Immunol Immunother. 2012;61:31–40.PubMedCrossRef
169.
go back to reference Amedei A, Cappon A, Codolo G, Cabrelle A, Polenghi A, Benagiano M, et al. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J Clin Invest. 2006;116:1092–101.PubMedPubMedCentralCrossRef Amedei A, Cappon A, Codolo G, Cabrelle A, Polenghi A, Benagiano M, et al. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J Clin Invest. 2006;116:1092–101.PubMedPubMedCentralCrossRef
170.
go back to reference Ceci P, Mangiarotti L, Rivetti C, Chiancone E. The neutrophil-activating Dps protein of Helicobacter pylori, HP-NAP, adopts a mechanism different from Escherichia coli Dps to bind and condense DNA. Nucl Acids Res. 2007;35:2247–56.PubMedPubMedCentralCrossRef Ceci P, Mangiarotti L, Rivetti C, Chiancone E. The neutrophil-activating Dps protein of Helicobacter pylori, HP-NAP, adopts a mechanism different from Escherichia coli Dps to bind and condense DNA. Nucl Acids Res. 2007;35:2247–56.PubMedPubMedCentralCrossRef
171.
go back to reference Dundon WG, Polenghi A, Del Guidice G, Rappuoli R, Montecucco C. Neutrophil-activating protein (HP-NAP) versus ferritin (Pfr): comparison of synthesis in Helicobacter pylori. FEMS Microbiol Lett. 2001;199:143–9.PubMedCrossRef Dundon WG, Polenghi A, Del Guidice G, Rappuoli R, Montecucco C. Neutrophil-activating protein (HP-NAP) versus ferritin (Pfr): comparison of synthesis in Helicobacter pylori. FEMS Microbiol Lett. 2001;199:143–9.PubMedCrossRef
172.
go back to reference Zhang J, Zhang X, Wu C, Lu D, Guo G, Mao X, et al. Expression, purification and characterization of arginase from Helicobacter pylori in its apo form. PLoS ONE. 2011;6:1–8. Zhang J, Zhang X, Wu C, Lu D, Guo G, Mao X, et al. Expression, purification and characterization of arginase from Helicobacter pylori in its apo form. PLoS ONE. 2011;6:1–8.
173.
go back to reference Zabaleta J, McGee DJ, Zea AH, Hernández CP, Rodriguez PC, Sierra RA, et al. Helicobacter pylori arginase inhibits T cell proliferation and reduces the expression of the TCR ζ-chain (CD3ζ). J Immunol. 2004;173:586–93.PubMedCrossRef Zabaleta J, McGee DJ, Zea AH, Hernández CP, Rodriguez PC, Sierra RA, et al. Helicobacter pylori arginase inhibits T cell proliferation and reduces the expression of the TCR ζ-chain (CD3ζ). J Immunol. 2004;173:586–93.PubMedCrossRef
175.
go back to reference Gobert AP, McGee DJ, Akhtar M, Mendz GL, Newton JC, Cheng Y, et al. Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc Natl Acad Sci USA. 2001;98:13844–9.PubMedPubMedCentralCrossRef Gobert AP, McGee DJ, Akhtar M, Mendz GL, Newton JC, Cheng Y, et al. Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc Natl Acad Sci USA. 2001;98:13844–9.PubMedPubMedCentralCrossRef
176.
go back to reference Lewis ND, Asim M, Barry DP, Singh K, de Sablet T, Boucher J-L, et al. Arginase II restricts host defense to Helicobacter pylori by attenuating inducible nitric oxide synthase translation in macrophages. J Immunol. 2010;184:2572–82.PubMedCrossRef Lewis ND, Asim M, Barry DP, Singh K, de Sablet T, Boucher J-L, et al. Arginase II restricts host defense to Helicobacter pylori by attenuating inducible nitric oxide synthase translation in macrophages. J Immunol. 2010;184:2572–82.PubMedCrossRef
177.
go back to reference Gobert A, Cheng Y, Wang J, Boucher J, Iyer R, Cederbaum S, et al. Helicobacter pylori induces macrophage apoptosis by activation of arginase II. J Immunol. 2002;168:4692–700.PubMedCrossRef Gobert A, Cheng Y, Wang J, Boucher J, Iyer R, Cederbaum S, et al. Helicobacter pylori induces macrophage apoptosis by activation of arginase II. J Immunol. 2002;168:4692–700.PubMedCrossRef
178.
go back to reference Keenan JI, Davis KA, Beaugie CR, McGovern JJ, Moran AP. Alterations in Helicobacter pylori outer membrane and outer membrane vesicle-associated lipopolysaccharides under iron-limiting growth conditions. Innate Immun. 2008;14:279–90.PubMedCrossRef Keenan JI, Davis KA, Beaugie CR, McGovern JJ, Moran AP. Alterations in Helicobacter pylori outer membrane and outer membrane vesicle-associated lipopolysaccharides under iron-limiting growth conditions. Innate Immun. 2008;14:279–90.PubMedCrossRef
179.
go back to reference Pfannkuch L, Hurwitz R, Trauisen J, Sigulla J, Poeschke M, Matzner L, et al. ADP heptose, a novel pathogen-associated molecular pattern identified in Helicobacter pylori. FASEB J. 2019;33:9087–99.PubMedPubMedCentralCrossRef Pfannkuch L, Hurwitz R, Trauisen J, Sigulla J, Poeschke M, Matzner L, et al. ADP heptose, a novel pathogen-associated molecular pattern identified in Helicobacter pylori. FASEB J. 2019;33:9087–99.PubMedPubMedCentralCrossRef
180.
go back to reference Zimmermann S, Pfannkuch L, Al-Zeer MA, Bartfeld S, Koch M, Liu J, et al. ALPK1- and TIFA-dependent innate immune response triggered by the helicobacter pylori type IV secretion system. Cell Rep. 2017;20:2384–95.PubMedCrossRef Zimmermann S, Pfannkuch L, Al-Zeer MA, Bartfeld S, Koch M, Liu J, et al. ALPK1- and TIFA-dependent innate immune response triggered by the helicobacter pylori type IV secretion system. Cell Rep. 2017;20:2384–95.PubMedCrossRef
182.
go back to reference Li H, Xia JQ, Zhu FS, Xi ZH, Pan CY, Gu LM, et al. LPS promotes the expression of PD-L1 in gastric cancer cells through NF-κB activation. J Cell Biochem. 2018;119:9997–1004.PubMedCrossRef Li H, Xia JQ, Zhu FS, Xi ZH, Pan CY, Gu LM, et al. LPS promotes the expression of PD-L1 in gastric cancer cells through NF-κB activation. J Cell Biochem. 2018;119:9997–1004.PubMedCrossRef
183.
go back to reference Yokota SI, Okabayashi T, Rehli M, Fujii N, Amano KI. Helicobacter pylori lipopolysaccharides upregulate toll-like receptor 4 expression and proliferation of gastric epithelial cells via the MEK1/2-ERK1/2 mitogen-activated protein kinase pathway. Infect Immun. 2010;78:468–76.PubMedCrossRef Yokota SI, Okabayashi T, Rehli M, Fujii N, Amano KI. Helicobacter pylori lipopolysaccharides upregulate toll-like receptor 4 expression and proliferation of gastric epithelial cells via the MEK1/2-ERK1/2 mitogen-activated protein kinase pathway. Infect Immun. 2010;78:468–76.PubMedCrossRef
184.
go back to reference Li N, Xu H, Ou Y, Feng Z, Zhang Q, Zhu Q, et al. LPS-induced CXCR7 expression promotes gastric cancer proliferation and migration via the TLR4/MD-2 pathway. Diagn Pathol. 2019;14:1–10.CrossRef Li N, Xu H, Ou Y, Feng Z, Zhang Q, Zhu Q, et al. LPS-induced CXCR7 expression promotes gastric cancer proliferation and migration via the TLR4/MD-2 pathway. Diagn Pathol. 2019;14:1–10.CrossRef
186.
go back to reference Slomiany BL, Slomiany A. Disruption in gastric mucin synthesis by Helicobacter pylori lipopolysaccharide involves ERK and p38 mitogen-activated protein kinase participation. Biochem Biophys Res Commun. 2002;294:220–4.PubMedCrossRef Slomiany BL, Slomiany A. Disruption in gastric mucin synthesis by Helicobacter pylori lipopolysaccharide involves ERK and p38 mitogen-activated protein kinase participation. Biochem Biophys Res Commun. 2002;294:220–4.PubMedCrossRef
187.
go back to reference Smith SM, Freeley M, Moynagh PN, Kelleher DP. Differential modulation of Helicobacter pylori lipopolysaccharide-mediated TLR2 signaling by individual Pellino proteins. Helicobacter. 2017;22:1–14.CrossRef Smith SM, Freeley M, Moynagh PN, Kelleher DP. Differential modulation of Helicobacter pylori lipopolysaccharide-mediated TLR2 signaling by individual Pellino proteins. Helicobacter. 2017;22:1–14.CrossRef
188.
go back to reference Xu L, Gong C, Li G, Wei J, Wang T, Meng W, et al. Ebselen suppresses inflammation induced by Helicobacter pylori lipopolysaccharide via the p38 mitogen-activated protein kinase signaling pathway. Mol Med Rep. 2018;17:6847–51.PubMed Xu L, Gong C, Li G, Wei J, Wang T, Meng W, et al. Ebselen suppresses inflammation induced by Helicobacter pylori lipopolysaccharide via the p38 mitogen-activated protein kinase signaling pathway. Mol Med Rep. 2018;17:6847–51.PubMed
189.
go back to reference Švagelj D, Terzić V, Dovhanj J, Švagelj M, Cvrković M, Švagelj I. Superoxide dismutases in chronic gastritis. APMIS. 2016;124:252–6.PubMedCrossRef Švagelj D, Terzić V, Dovhanj J, Švagelj M, Cvrković M, Švagelj I. Superoxide dismutases in chronic gastritis. APMIS. 2016;124:252–6.PubMedCrossRef
190.
go back to reference Smoot DT, Elliott TB, Verspaget HW, Jones D, Allen CR, Vernon KG, et al. Influence of Helicobacter pylori on reactive oxygen-induced gastric epithelial cell injury. Carcinogenesis. 2000;21:2091–5.PubMedCrossRef Smoot DT, Elliott TB, Verspaget HW, Jones D, Allen CR, Vernon KG, et al. Influence of Helicobacter pylori on reactive oxygen-induced gastric epithelial cell injury. Carcinogenesis. 2000;21:2091–5.PubMedCrossRef
192.
go back to reference Seyler J, Olson JW, Maier RJ. Superoxide dismutase-deficient mutants of Helicobacter pylori are hypersensitive to oxidative stress and defective in host colonization. Infect Immun. 2001;69:4034–40.PubMedPubMedCentralCrossRef Seyler J, Olson JW, Maier RJ. Superoxide dismutase-deficient mutants of Helicobacter pylori are hypersensitive to oxidative stress and defective in host colonization. Infect Immun. 2001;69:4034–40.PubMedPubMedCentralCrossRef
193.
go back to reference Takahashi-Kanemitsu A, Lu M, Knight C, Yamamoto T, Hayashi T, Mii Y, et al. The Helicobacter pylori CagA oncoprotein disrupts Wnt/PCP signaling and promotes hyperproliferation of pyloric gland base cells. Sci Signal. 2023;16:eabp9020.PubMedCrossRef Takahashi-Kanemitsu A, Lu M, Knight C, Yamamoto T, Hayashi T, Mii Y, et al. The Helicobacter pylori CagA oncoprotein disrupts Wnt/PCP signaling and promotes hyperproliferation of pyloric gland base cells. Sci Signal. 2023;16:eabp9020.PubMedCrossRef
194.
go back to reference Wang H, Zhao M, Shi F, Zheng S, Xiong L, Zheng L. A review of signal pathway induced by virulent protein CagA of Helicobacter pylori. Front Cell Infect Microbiol. 2023;13:1–10. Wang H, Zhao M, Shi F, Zheng S, Xiong L, Zheng L. A review of signal pathway induced by virulent protein CagA of Helicobacter pylori. Front Cell Infect Microbiol. 2023;13:1–10.
195.
go back to reference Brasil-Costa I, de Souza CO, Monteiro LCR, Santos MES, De Oliveira EHC, Burbano RMR. H. pylori Infection and Virulence Factors cagA and vacA (s and m regions) in gastric adenocarcinoma from Pará State, Brazil. Pathogens. 2022;11:414.PubMedPubMedCentralCrossRef Brasil-Costa I, de Souza CO, Monteiro LCR, Santos MES, De Oliveira EHC, Burbano RMR. H. pylori Infection and Virulence Factors cagA and vacA (s and m regions) in gastric adenocarcinoma from Pará State, Brazil. Pathogens. 2022;11:414.PubMedPubMedCentralCrossRef
198.
go back to reference Reuter S, Raspe J, Uebner H, Contoyannis A, Pastille E, Westendorf AM, et al. Treatment with Helicobacter pylori-derived VacA attenuates allergic airway disease. Front Immunol. 2023;14:1–14.CrossRef Reuter S, Raspe J, Uebner H, Contoyannis A, Pastille E, Westendorf AM, et al. Treatment with Helicobacter pylori-derived VacA attenuates allergic airway disease. Front Immunol. 2023;14:1–14.CrossRef
200.
go back to reference Cho H, Cho H, Song W, Yoon S. Structural analysis of the virulence gene protein IceA2 from Helicobacter pylori. Biochem Biophys Res Commun. 2022;612:162–8.PubMedCrossRef Cho H, Cho H, Song W, Yoon S. Structural analysis of the virulence gene protein IceA2 from Helicobacter pylori. Biochem Biophys Res Commun. 2022;612:162–8.PubMedCrossRef
201.
go back to reference Baskerville MJ, Kovalyova Y, Mejías-Luque R, Gerhard M, Hatzios SK. Isotope tracing reveals bacterial catabolism of host-derived glutathione during Helicobacter pylori infection. PLoS Pathog. 2023;19:1–18.CrossRef Baskerville MJ, Kovalyova Y, Mejías-Luque R, Gerhard M, Hatzios SK. Isotope tracing reveals bacterial catabolism of host-derived glutathione during Helicobacter pylori infection. PLoS Pathog. 2023;19:1–18.CrossRef
202.
go back to reference Syahniar R, Kharisma D, Rayhana C. Helicobacter pylori challenge vaccine for humans. Cham: IntechOpen; 2021. Syahniar R, Kharisma D, Rayhana C. Helicobacter pylori challenge vaccine for humans. Cham: IntechOpen; 2021.
203.
go back to reference Šudomová M, Hassan STS. Gossypol from Gossypium spp. inhibits Helicobacter pylori clinical strains and urease enzyme activity: bioactivity and safety assessments. Sci Pharm. 2022;90:11.CrossRef Šudomová M, Hassan STS. Gossypol from Gossypium spp. inhibits Helicobacter pylori clinical strains and urease enzyme activity: bioactivity and safety assessments. Sci Pharm. 2022;90:11.CrossRef
204.
go back to reference Cagnoni M, Pagnini C, Crovaro M, Aucello A, Urgesi R, Pallotta L, et al. Evaluation of accuracy and feasibility of a New-generation ultra-rapid urease test for detection of Helicobacter pylori infection. Gastrointest Disord. 2022;4:205–13.CrossRef Cagnoni M, Pagnini C, Crovaro M, Aucello A, Urgesi R, Pallotta L, et al. Evaluation of accuracy and feasibility of a New-generation ultra-rapid urease test for detection of Helicobacter pylori infection. Gastrointest Disord. 2022;4:205–13.CrossRef
206.
go back to reference Codolo G, Facchinello N, Papa N, Bertocco A, Coletta S, Benna C, et al. Macrophage-mediated melanoma reduction after HP-NAP treatment in a Zebrafish xenograft model. Int J Mol Sci. 2022;23:55.CrossRef Codolo G, Facchinello N, Papa N, Bertocco A, Coletta S, Benna C, et al. Macrophage-mediated melanoma reduction after HP-NAP treatment in a Zebrafish xenograft model. Int J Mol Sci. 2022;23:55.CrossRef
208.
go back to reference Kobayashi J, Kawakubo M, Fujii C, Arisaka N, Miyashita M, Sato Y, et al. Cholestenone functions as an antibiotic against Helicobacter pylori by inhibiting biosynthesis of the cell wall component CGL. Proc Natl Acad Sci USA. 2021;118:1–8.CrossRef Kobayashi J, Kawakubo M, Fujii C, Arisaka N, Miyashita M, Sato Y, et al. Cholestenone functions as an antibiotic against Helicobacter pylori by inhibiting biosynthesis of the cell wall component CGL. Proc Natl Acad Sci USA. 2021;118:1–8.CrossRef
209.
go back to reference Frauenlob T, Neuper T, Mehinagic M, Dang HH, Boraschi D, Horejs-Hoeck J. Helicobacter pylori infection of primary human monocytes boosts subsequent immune responses to LPS. Front Immunol. 2022;13:1–11.CrossRef Frauenlob T, Neuper T, Mehinagic M, Dang HH, Boraschi D, Horejs-Hoeck J. Helicobacter pylori infection of primary human monocytes boosts subsequent immune responses to LPS. Front Immunol. 2022;13:1–11.CrossRef
211.
go back to reference Zhou WT, Dai YY, Liao LJ, Yang SX, Chen H, Huang L, et al. Linolenic acid-metronidazole inhibits the growth of Helicobacter pylori through oxidation. World J Gastroenterol. 2023;29:4860–72.PubMedPubMedCentralCrossRef Zhou WT, Dai YY, Liao LJ, Yang SX, Chen H, Huang L, et al. Linolenic acid-metronidazole inhibits the growth of Helicobacter pylori through oxidation. World J Gastroenterol. 2023;29:4860–72.PubMedPubMedCentralCrossRef
212.
go back to reference Ansari S, Yamaoka Y. Helicobacter pylori virulence factors exploiting gastric colonization and its pathogenicity. Toxins (Basel). 2019;11:1–26.CrossRef Ansari S, Yamaoka Y. Helicobacter pylori virulence factors exploiting gastric colonization and its pathogenicity. Toxins (Basel). 2019;11:1–26.CrossRef
213.
go back to reference Nakazawa T. Growth cycle of Helicobacter pylori in gastric mucous layer. Keio J Med. 2002;51:15–9.PubMedCrossRef Nakazawa T. Growth cycle of Helicobacter pylori in gastric mucous layer. Keio J Med. 2002;51:15–9.PubMedCrossRef
214.
go back to reference Akada JK, Shirai M, Takeuchi H, Tsuda M, Nakazawa T. Identification of the urease operon in Helicobacter pylori and its control by mRNA decay in response to pH. Mol Microbiol. 2000;36:1071–84.PubMedCrossRef Akada JK, Shirai M, Takeuchi H, Tsuda M, Nakazawa T. Identification of the urease operon in Helicobacter pylori and its control by mRNA decay in response to pH. Mol Microbiol. 2000;36:1071–84.PubMedCrossRef
215.
go back to reference Marcus EA, Sachs G, Wen Y, Scott DR. Phosphorylation-dependent and phosphorylation-independent regulation of Helicobacter pylori acid acclimation by the ArsRS two-component system. Helicobacter. 2016;21:69–81.PubMedCrossRef Marcus EA, Sachs G, Wen Y, Scott DR. Phosphorylation-dependent and phosphorylation-independent regulation of Helicobacter pylori acid acclimation by the ArsRS two-component system. Helicobacter. 2016;21:69–81.PubMedCrossRef
216.
go back to reference Wen Y, Feng J, Scott DR, Marcus EA, Sachs G. The pH-responsive regulon of HP0244 (FlgS), the cytoplasmic histidine kinase of Helicobacter pylori. J Bacteriol. 2009;191:449–60.PubMedCrossRef Wen Y, Feng J, Scott DR, Marcus EA, Sachs G. The pH-responsive regulon of HP0244 (FlgS), the cytoplasmic histidine kinase of Helicobacter pylori. J Bacteriol. 2009;191:449–60.PubMedCrossRef
217.
go back to reference Ge RG, Wang DX, Hao MC, Sun XS. Nickel trafficking system responsible for urease maturation in Helicobacter pylori. World J Gastroenterol. 2013;19:8211–8.PubMedPubMedCentralCrossRef Ge RG, Wang DX, Hao MC, Sun XS. Nickel trafficking system responsible for urease maturation in Helicobacter pylori. World J Gastroenterol. 2013;19:8211–8.PubMedPubMedCentralCrossRef
218.
219.
go back to reference Kainulainen V, Korhonen TK. Dancing to another tune-adhesive moonlighting proteins in bacteria. Biology (Basel). 2014;3:178–204.PubMed Kainulainen V, Korhonen TK. Dancing to another tune-adhesive moonlighting proteins in bacteria. Biology (Basel). 2014;3:178–204.PubMed
220.
221.
go back to reference Henderson B, Martin A. Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun. 2011;79:3476–91.PubMedPubMedCentralCrossRef Henderson B, Martin A. Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun. 2011;79:3476–91.PubMedPubMedCentralCrossRef
222.
go back to reference Henderson B, Pockley AG. Molecular chaperones and cell signalling. 1st ed. Cambridge University Press; 2005.CrossRef Henderson B, Pockley AG. Molecular chaperones and cell signalling. 1st ed. Cambridge University Press; 2005.CrossRef
223.
go back to reference Yunoki N, Yokota K, Mizuno M, Kawahara Y, Adachi M, Okada H, et al. Antibody to heat shock protein can be used for early serological monitoring of Helicobacter pylori eradication treatment. Clin Diagn Lab Immunol. 2000;7:574–7.PubMedPubMedCentralCrossRef Yunoki N, Yokota K, Mizuno M, Kawahara Y, Adachi M, Okada H, et al. Antibody to heat shock protein can be used for early serological monitoring of Helicobacter pylori eradication treatment. Clin Diagn Lab Immunol. 2000;7:574–7.PubMedPubMedCentralCrossRef
224.
225.
go back to reference Hoy B, Löwer M, Weydig C, Carra G, Tegtmeyer N, Geppert T, et al. Helicobacter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion. EMBO Rep. 2010;11:798–804.PubMedPubMedCentralCrossRef Hoy B, Löwer M, Weydig C, Carra G, Tegtmeyer N, Geppert T, et al. Helicobacter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion. EMBO Rep. 2010;11:798–804.PubMedPubMedCentralCrossRef
226.
go back to reference Halder P, Datta C, Kumar R, Sharma AK, Basu J, Kundu M. The secreted antigen, HP0175, of Helicobacter pylori links the unfolded protein response (UPR) to autophagy in gastric epithelial cells. Cell Microbiol. 2015;17:714–29.PubMedCrossRef Halder P, Datta C, Kumar R, Sharma AK, Basu J, Kundu M. The secreted antigen, HP0175, of Helicobacter pylori links the unfolded protein response (UPR) to autophagy in gastric epithelial cells. Cell Microbiol. 2015;17:714–29.PubMedCrossRef
227.
go back to reference Harris AG, Wilson JE, Danon SJ, Dixon MF, Donegan K, Hazell SL. Catalase (KatA) and KatA-associated protein (KapA) are essential to persistent colonization in the Helicobacter pylori SS1 mouse model. Microbiology. 2003;149:665–72.PubMedCrossRef Harris AG, Wilson JE, Danon SJ, Dixon MF, Donegan K, Hazell SL. Catalase (KatA) and KatA-associated protein (KapA) are essential to persistent colonization in the Helicobacter pylori SS1 mouse model. Microbiology. 2003;149:665–72.PubMedCrossRef
230.
go back to reference Handa O, Naito Y, Yoshikawa T. Redox biology and gastric carcinogenesis: the role of Helicobacter pylori. Redox Rep. 2011;16:1–7.PubMedCrossRef Handa O, Naito Y, Yoshikawa T. Redox biology and gastric carcinogenesis: the role of Helicobacter pylori. Redox Rep. 2011;16:1–7.PubMedCrossRef
231.
go back to reference Westblom TU, Phadnis S, Langenberg W, Yoneda K, Madan E, Midkiff BR. Catalase negative mutants of Helicobacter pylori. Eur J Clin Microbiol Infect Dis. 1992;11:522–6.PubMedCrossRef Westblom TU, Phadnis S, Langenberg W, Yoneda K, Madan E, Midkiff BR. Catalase negative mutants of Helicobacter pylori. Eur J Clin Microbiol Infect Dis. 1992;11:522–6.PubMedCrossRef
233.
go back to reference Odenbreit S, Swoboda K, Barwig I, Ruhl S, Borén T, Koletzko S, et al. Outer membrane protein expression profile in Helicobacter pylori clinical isolates. Infect Immun. 2009;77:3782–90.PubMedPubMedCentralCrossRef Odenbreit S, Swoboda K, Barwig I, Ruhl S, Borén T, Koletzko S, et al. Outer membrane protein expression profile in Helicobacter pylori clinical isolates. Infect Immun. 2009;77:3782–90.PubMedPubMedCentralCrossRef
234.
go back to reference Bäckström A, Lundberg C, Kersulyte D, Berg DE, Borén T, Arnqvist A. Metastability of Helicobacter pylori bab adhesin genes and dynamics in Lewis b antigen binding. Proc Natl Acad Sci USA. 2004;101:16923–8.PubMedPubMedCentralCrossRef Bäckström A, Lundberg C, Kersulyte D, Berg DE, Borén T, Arnqvist A. Metastability of Helicobacter pylori bab adhesin genes and dynamics in Lewis b antigen binding. Proc Natl Acad Sci USA. 2004;101:16923–8.PubMedPubMedCentralCrossRef
235.
go back to reference Magalhães A, Reis CA. Helicobacter pylori adhesion to gastric epithelial cells is mediated by glycan receptors. Braz J Med Biol Res. 2010;43:611–8.PubMedCrossRef Magalhães A, Reis CA. Helicobacter pylori adhesion to gastric epithelial cells is mediated by glycan receptors. Braz J Med Biol Res. 2010;43:611–8.PubMedCrossRef
236.
go back to reference Doohan D, Annisa Y, Rezkitha A, Waskito LA, Yamaoka Y. Helicobacter pylori BabA – SabA key roles in the adherence. Toxins (Basel). 2021;13:1–12.CrossRef Doohan D, Annisa Y, Rezkitha A, Waskito LA, Yamaoka Y. Helicobacter pylori BabA – SabA key roles in the adherence. Toxins (Basel). 2021;13:1–12.CrossRef
237.
238.
go back to reference Hansen LM, Gideonsson P, Canfield DR, Borén T, Solnick JV. Dynamic expression of the BabA adhesin and its BabB paralog during Helicobacter pylori infection in rhesus macaques. Infect Immun. 2017;85:1–14.CrossRef Hansen LM, Gideonsson P, Canfield DR, Borén T, Solnick JV. Dynamic expression of the BabA adhesin and its BabB paralog during Helicobacter pylori infection in rhesus macaques. Infect Immun. 2017;85:1–14.CrossRef
239.
go back to reference Kim A, Servetas SL, Kang J, Kim J, Jang S, Choi YH, et al. Helicobacter pylori outer membrane protein, HomC, shows geographic dependent polymorphism that is influenced by the Bab family. J Microbiol. 2016;54:846–52.PubMedCrossRef Kim A, Servetas SL, Kang J, Kim J, Jang S, Choi YH, et al. Helicobacter pylori outer membrane protein, HomC, shows geographic dependent polymorphism that is influenced by the Bab family. J Microbiol. 2016;54:846–52.PubMedCrossRef
240.
go back to reference Matteo MJ, Armitano RI, Romeo M, Wonaga A, Olmos M, Catalano M. Helicobacter pylori bab genes during chronic colonization. Int J Mol Epidemiol Genet. 2011;2:286–91.PubMedPubMedCentral Matteo MJ, Armitano RI, Romeo M, Wonaga A, Olmos M, Catalano M. Helicobacter pylori bab genes during chronic colonization. Int J Mol Epidemiol Genet. 2011;2:286–91.PubMedPubMedCentral
241.
go back to reference Ishijima N, Suzuki M, Ashida H, Ichikawa Y, Kanegae Y, Saito I, et al. BabA-mediated adherence is a potentiator of the Helicobacter pylori type IV secretion system activity. J Biol Chem. 2011;286:25256–64.PubMedPubMedCentralCrossRef Ishijima N, Suzuki M, Ashida H, Ichikawa Y, Kanegae Y, Saito I, et al. BabA-mediated adherence is a potentiator of the Helicobacter pylori type IV secretion system activity. J Biol Chem. 2011;286:25256–64.PubMedPubMedCentralCrossRef
243.
go back to reference Safaei HG, Havaei SA, Tavakkoli H, Eshaghei M, Navabakbar F, Salehei R. Relation of bab A2 genotype of Helicobacter pylori infection with chronic active gastritis, duodenal ulcer and non-cardia active gastritis in Alzahra hospital Isfahan Iran. Jundishapur J Microbiol. 2010;3:93–8. Safaei HG, Havaei SA, Tavakkoli H, Eshaghei M, Navabakbar F, Salehei R. Relation of bab A2 genotype of Helicobacter pylori infection with chronic active gastritis, duodenal ulcer and non-cardia active gastritis in Alzahra hospital Isfahan Iran. Jundishapur J Microbiol. 2010;3:93–8.
244.
go back to reference Yanai A, Maeda S, Hikiba Y, Shibata W, Ohmae T, Hirata Y, et al. Clinical relevance of Helicobacter pylori sabA genotype in Japanese clinical isolates. J Gastroenterol Hepatol. 2007;22:2228–32.PubMedCrossRef Yanai A, Maeda S, Hikiba Y, Shibata W, Ohmae T, Hirata Y, et al. Clinical relevance of Helicobacter pylori sabA genotype in Japanese clinical isolates. J Gastroenterol Hepatol. 2007;22:2228–32.PubMedCrossRef
245.
go back to reference Gerhard M, Lehn N, Neumayer N, Borén T, Rad R, Schepp W, et al. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc Natl Acad Sci USA. 1999;96:12778–83.PubMedPubMedCentralCrossRef Gerhard M, Lehn N, Neumayer N, Borén T, Rad R, Schepp W, et al. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc Natl Acad Sci USA. 1999;96:12778–83.PubMedPubMedCentralCrossRef
246.
go back to reference Jalilian S, Alvandi A, Jouybari TA, Pajavand H, Abiri R. Lack of association association between the presence of dupA and babA 2 genes in Helicobacter pylori and gastroduodenal disorders 1. Mol Genet Microbiol Virol. 2017;32:55–61.CrossRef Jalilian S, Alvandi A, Jouybari TA, Pajavand H, Abiri R. Lack of association association between the presence of dupA and babA 2 genes in Helicobacter pylori and gastroduodenal disorders 1. Mol Genet Microbiol Virol. 2017;32:55–61.CrossRef
247.
go back to reference Kpoghomou MA, Wang J, Wang T, Jin G. Association of Helicobacter pylori babA2 gene and gastric cancer risk: a meta-analysis. BMC Cancer. 2020;20:1–7.CrossRef Kpoghomou MA, Wang J, Wang T, Jin G. Association of Helicobacter pylori babA2 gene and gastric cancer risk: a meta-analysis. BMC Cancer. 2020;20:1–7.CrossRef
248.
go back to reference Mizushima T, Sugiyama T, Komatsu Y, Ishizuka J, Kato M, Asaka M. Clinical relevance of the babA2 genotype of Helicobacter pylori in Japanese clinical isolates. J Clin Microbiol. 2001;39:2463–5.PubMedPubMedCentralCrossRef Mizushima T, Sugiyama T, Komatsu Y, Ishizuka J, Kato M, Asaka M. Clinical relevance of the babA2 genotype of Helicobacter pylori in Japanese clinical isolates. J Clin Microbiol. 2001;39:2463–5.PubMedPubMedCentralCrossRef
249.
go back to reference Walz A, Odenbreit S, Mahdavi J, Borén T, Ruhl S. Identification and characterization of binding properties of Helicobacter pylori by glycoconjugate arrays. Glycobiology. 2005;15:700–8.PubMedCrossRef Walz A, Odenbreit S, Mahdavi J, Borén T, Ruhl S. Identification and characterization of binding properties of Helicobacter pylori by glycoconjugate arrays. Glycobiology. 2005;15:700–8.PubMedCrossRef
250.
go back to reference Aspholm M, Olfat FO, Nordén J, Sondén B, Lundberg C, Sjöström R, et al. SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog. 2006;2:0989–1001.CrossRef Aspholm M, Olfat FO, Nordén J, Sondén B, Lundberg C, Sjöström R, et al. SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog. 2006;2:0989–1001.CrossRef
251.
go back to reference Walz A, Odenbreit S, Stühler K, Wattenberg A, Meyer HE, Mahdavi J, et al. Identification of glycoprotein receptors within the human salivary proteome for the lectin-like BabA and SabA adhesins of Helicobacter pylori by fluorescence-based 2-D bacterial overlay. Proteomics. 2009;9:1582–92.PubMedCrossRef Walz A, Odenbreit S, Stühler K, Wattenberg A, Meyer HE, Mahdavi J, et al. Identification of glycoprotein receptors within the human salivary proteome for the lectin-like BabA and SabA adhesins of Helicobacter pylori by fluorescence-based 2-D bacterial overlay. Proteomics. 2009;9:1582–92.PubMedCrossRef
252.
go back to reference Marcos NT, Magalhães A, Ferreira B, Oliveira MJ, Carvalho AS, Mendes N, et al. Helicobacter pylori induces β3GnT5 in human gastric cell lines, modulating expression of the SabA ligand sialyl-Lewis x. J Clin Invest. 2008;118:2325–36.PubMedPubMedCentral Marcos NT, Magalhães A, Ferreira B, Oliveira MJ, Carvalho AS, Mendes N, et al. Helicobacter pylori induces β3GnT5 in human gastric cell lines, modulating expression of the SabA ligand sialyl-Lewis x. J Clin Invest. 2008;118:2325–36.PubMedPubMedCentral
253.
go back to reference Mahdavi J, Sondén B, Hurtig M, Olfat FO, Forsberg L, Roche N, et al. Helicobacter pylori sabA adhesin in persistent infection and chronic inflammation. Science (80-). 2002;297:573–8.CrossRef Mahdavi J, Sondén B, Hurtig M, Olfat FO, Forsberg L, Roche N, et al. Helicobacter pylori sabA adhesin in persistent infection and chronic inflammation. Science (80-). 2002;297:573–8.CrossRef
254.
go back to reference Oleastro M, Ménard A. The role of Helicobacter pylori outer membrane proteins in adherence and pathogenesis. Biology (Basel). 2013;2:1110–34.PubMed Oleastro M, Ménard A. The role of Helicobacter pylori outer membrane proteins in adherence and pathogenesis. Biology (Basel). 2013;2:1110–34.PubMed
255.
go back to reference Unemo M, Aspholm-Hurtig M, Ilver D, Bergström J, Borén T, Danielsson D, et al. The sialic acid binding SabA adhesin of Helicobacter pylori is essential for nonopsonic activation of human neutrophils. J Biol Chem. 2005;280:15390–7.PubMedCrossRef Unemo M, Aspholm-Hurtig M, Ilver D, Bergström J, Borén T, Danielsson D, et al. The sialic acid binding SabA adhesin of Helicobacter pylori is essential for nonopsonic activation of human neutrophils. J Biol Chem. 2005;280:15390–7.PubMedCrossRef
256.
go back to reference De Jonge R, Pot RGJ, Loffeld RJLF, Van Vliet AHM, Kuipers EJ, Kusters JG. The functional status of the Helicobacter pylori sabB adhesin gene as a putative marker for disease outcome. Helicobacter. 2004;9:158–64.PubMedCrossRef De Jonge R, Pot RGJ, Loffeld RJLF, Van Vliet AHM, Kuipers EJ, Kusters JG. The functional status of the Helicobacter pylori sabB adhesin gene as a putative marker for disease outcome. Helicobacter. 2004;9:158–64.PubMedCrossRef
257.
go back to reference Pakbaz Z, Shirazi MH, Ranjbar R, Pourm MR, Gholi MK, Aliramezani A, et al. Frequency of sabA gene in Helicobacter pylori strains isolated from patients in Tehran. Iran Iran Red Crescent Med J. 2013;15:767–70.PubMed Pakbaz Z, Shirazi MH, Ranjbar R, Pourm MR, Gholi MK, Aliramezani A, et al. Frequency of sabA gene in Helicobacter pylori strains isolated from patients in Tehran. Iran Iran Red Crescent Med J. 2013;15:767–70.PubMed
258.
go back to reference Yamaoka Y, Kwon DH, Graham DY. A Mr 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc Natl Acad Sci USA. 2000;97:7533–8.PubMedPubMedCentralCrossRef Yamaoka Y, Kwon DH, Graham DY. A Mr 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc Natl Acad Sci USA. 2000;97:7533–8.PubMedPubMedCentralCrossRef
259.
go back to reference Tabassam FH, Graham DY, Yamaoka Y. Helicobacter pylori-associated regulation of forkhead transcription factors FoxO1/3a in human gastric cells. Helicobacter. 2012;17:193–202.PubMedPubMedCentralCrossRef Tabassam FH, Graham DY, Yamaoka Y. Helicobacter pylori-associated regulation of forkhead transcription factors FoxO1/3a in human gastric cells. Helicobacter. 2012;17:193–202.PubMedPubMedCentralCrossRef
260.
go back to reference Odenbreit S, Kavermann H, Püls J, Haas R. CagA tyrosine phosphorylation and interleukin-8 induction by Helicobacter pylori are independent from AlpAB, HopZ and Bab group outer membrane proteins. Int J Med Microbiol. 2002;292:257–66.PubMedCrossRef Odenbreit S, Kavermann H, Püls J, Haas R. CagA tyrosine phosphorylation and interleukin-8 induction by Helicobacter pylori are independent from AlpAB, HopZ and Bab group outer membrane proteins. Int J Med Microbiol. 2002;292:257–66.PubMedCrossRef
261.
go back to reference Dossumbekova A, Prinz C, Mages J, Lang R, Kusters JG, Van Vliet AHM, et al. Helicobacter pylori HopH (OipA) and bacterial pathogenicity: genetic and functional genomic analysis of hopH gene polymorphisms. J Infect Dis. 2006;194:1346–55.PubMedCrossRef Dossumbekova A, Prinz C, Mages J, Lang R, Kusters JG, Van Vliet AHM, et al. Helicobacter pylori HopH (OipA) and bacterial pathogenicity: genetic and functional genomic analysis of hopH gene polymorphisms. J Infect Dis. 2006;194:1346–55.PubMedCrossRef
262.
go back to reference Teymournejad O, Mobarez AM, Hassan ZM, Moazzeni SM, Ahmadabad HN. In vitro suppression of dendritic cells by Helicobacter pylori OipA. Helicobacter. 2014;19:136–43.PubMedCrossRef Teymournejad O, Mobarez AM, Hassan ZM, Moazzeni SM, Ahmadabad HN. In vitro suppression of dendritic cells by Helicobacter pylori OipA. Helicobacter. 2014;19:136–43.PubMedCrossRef
263.
go back to reference Armitano RI, Matteo MJ, Goldman C, Wonaga A, Viola LA, De Palma GZ, et al. Helicobacter pylori heterogeneity in patients with gastritis and peptic ulcer disease. Infect Genet Evol. 2013;16:377–85.PubMedCrossRef Armitano RI, Matteo MJ, Goldman C, Wonaga A, Viola LA, De Palma GZ, et al. Helicobacter pylori heterogeneity in patients with gastritis and peptic ulcer disease. Infect Genet Evol. 2013;16:377–85.PubMedCrossRef
265.
266.
go back to reference Franco AT, Johnston E, Krishna U, Yamaoka Y, Israel DA, Nagy TA, et al. Regulation of gastric carcinogenesis by Helicobacter pylori virulence factors. Cancer Res. 2008;68:379–87.PubMedPubMedCentralCrossRef Franco AT, Johnston E, Krishna U, Yamaoka Y, Israel DA, Nagy TA, et al. Regulation of gastric carcinogenesis by Helicobacter pylori virulence factors. Cancer Res. 2008;68:379–87.PubMedPubMedCentralCrossRef
267.
go back to reference Mahboubi M, Falsafi T, Sadeghizadeh M, Mahjoub F. The role of outer inflammatory protein a (OipA) in vaccination of the C57BL/6 mouse model infected by Helicobacter pylori. Turk J Med Sci. 2017;47:326–33.PubMedCrossRef Mahboubi M, Falsafi T, Sadeghizadeh M, Mahjoub F. The role of outer inflammatory protein a (OipA) in vaccination of the C57BL/6 mouse model infected by Helicobacter pylori. Turk J Med Sci. 2017;47:326–33.PubMedCrossRef
269.
go back to reference Chen J, Lin L, Li N, She F. Enhancement of Helicobacter pylori outer inflammatory protein DNA vaccine efficacy by co-delivery of interleukin-2 and B subunit heat-labile toxin gene encoded plasmids. Microbiol Immunol. 2012;56:85–92.PubMedCrossRef Chen J, Lin L, Li N, She F. Enhancement of Helicobacter pylori outer inflammatory protein DNA vaccine efficacy by co-delivery of interleukin-2 and B subunit heat-labile toxin gene encoded plasmids. Microbiol Immunol. 2012;56:85–92.PubMedCrossRef
270.
go back to reference Dadashzadeh K. Relevance of Helicobacter pylori dupa and oipa genotypes and development of gastric disease. Biomed Res. 2017;28:8179–83. Dadashzadeh K. Relevance of Helicobacter pylori dupa and oipa genotypes and development of gastric disease. Biomed Res. 2017;28:8179–83.
271.
go back to reference Kim JY, Kim N, Nam RH, Suh JH, Chang H, Lee JW, et al. Association of polymorphisms in virulence factor of Helicobacter pylori and gastroduodenal diseases in South Korea. J Gastroenterol Hepatol. 2014;29:984–91.PubMedCrossRef Kim JY, Kim N, Nam RH, Suh JH, Chang H, Lee JW, et al. Association of polymorphisms in virulence factor of Helicobacter pylori and gastroduodenal diseases in South Korea. J Gastroenterol Hepatol. 2014;29:984–91.PubMedCrossRef
272.
go back to reference Souod N, Sarshar M, Dabiri H, Momtaz H, Kargar M. The study of the oipA and dupA genes in Helicobacter pylori strains and their relationship with different gastroduodenal diseases. Gastroenterol Hepatol. 2015;8:47–53. Souod N, Sarshar M, Dabiri H, Momtaz H, Kargar M. The study of the oipA and dupA genes in Helicobacter pylori strains and their relationship with different gastroduodenal diseases. Gastroenterol Hepatol. 2015;8:47–53.
273.
go back to reference Odenbreit S, Till M, Hofreuter D, Faller G, Haas R. Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol Microbiol. 1999;31:1537–48.PubMedCrossRef Odenbreit S, Till M, Hofreuter D, Faller G, Haas R. Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol Microbiol. 1999;31:1537–48.PubMedCrossRef
275.
go back to reference Lu H, Jeng YW, Beswick EJ, Ohno T, Odenbreit S, Haas R, et al. Functional and intracellular signaling differences associated with the Helicobacter pylori AlpAB adhesin from Western and East Asian strains. J Biol Chem. 2007;282:6242–54.PubMedCrossRef Lu H, Jeng YW, Beswick EJ, Ohno T, Odenbreit S, Haas R, et al. Functional and intracellular signaling differences associated with the Helicobacter pylori AlpAB adhesin from Western and East Asian strains. J Biol Chem. 2007;282:6242–54.PubMedCrossRef
276.
go back to reference Xue J, Bai Y, Chen Y, De WJ, Zhang ZS, Zhang YL, et al. Expression of Helicobacter pylori AlpA protein and its immunogenicity. World J Gastroenterol. 2005;11:2260–3.PubMedPubMedCentralCrossRef Xue J, Bai Y, Chen Y, De WJ, Zhang ZS, Zhang YL, et al. Expression of Helicobacter pylori AlpA protein and its immunogenicity. World J Gastroenterol. 2005;11:2260–3.PubMedPubMedCentralCrossRef
277.
go back to reference Alm RA, Bina J, Andrews BM, Doig P, Hancock REW, Trust TJ. Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect Immun. 2000;68:4155–68.PubMedPubMedCentralCrossRef Alm RA, Bina J, Andrews BM, Doig P, Hancock REW, Trust TJ. Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect Immun. 2000;68:4155–68.PubMedPubMedCentralCrossRef
278.
go back to reference Kennemann L, Brenneke B, Andres S, Engstrand L, Meyer TF, Aebischer T, et al. In vivo sequence variation in HopZ, a phase-variable outer membrane protein of Helicobacter pylori. Infect Immun. 2012;80:4364–73.PubMedPubMedCentralCrossRef Kennemann L, Brenneke B, Andres S, Engstrand L, Meyer TF, Aebischer T, et al. In vivo sequence variation in HopZ, a phase-variable outer membrane protein of Helicobacter pylori. Infect Immun. 2012;80:4364–73.PubMedPubMedCentralCrossRef
279.
go back to reference Peck B, Ortkamp M, Diehl KD, Hundt E, Knapp B. Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. Nucl Acids Res. 1999;27:3325–33.PubMedPubMedCentralCrossRef Peck B, Ortkamp M, Diehl KD, Hundt E, Knapp B. Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. Nucl Acids Res. 1999;27:3325–33.PubMedPubMedCentralCrossRef
281.
go back to reference Lehours P, Ménard A, Dupouy S, Bergey B, Richy F, Zerbib F, et al. Evaluation of the association of nine Helicobacter pylori virulence factors with strains involved in low-grade gastric mucosa-associated lymphoid tissue lymphoma. Infect Immun. 2004;72:880–8.PubMedPubMedCentralCrossRef Lehours P, Ménard A, Dupouy S, Bergey B, Richy F, Zerbib F, et al. Evaluation of the association of nine Helicobacter pylori virulence factors with strains involved in low-grade gastric mucosa-associated lymphoid tissue lymphoma. Infect Immun. 2004;72:880–8.PubMedPubMedCentralCrossRef
282.
go back to reference Oleastro M, Cordeiro R, Ménard A, Gomes JP. Allelic diversity among Helicobacter pylori outer membrane protein genes homB and homA generated by recombination. J Bacteriol. 2010;192:3961–8.PubMedPubMedCentralCrossRef Oleastro M, Cordeiro R, Ménard A, Gomes JP. Allelic diversity among Helicobacter pylori outer membrane protein genes homB and homA generated by recombination. J Bacteriol. 2010;192:3961–8.PubMedPubMedCentralCrossRef
283.
go back to reference Oleastro M, Cordeiro R, Ferrand J, Nunes B, Lehours P, Carvalho-Oliveira I, et al. Evaluation of the clinical significance of homB, a novel candidate marker of Helicobacter pylori strains associated with peptic ulcer disease. J Infect Dis. 2008;198:1379–87.PubMedCrossRef Oleastro M, Cordeiro R, Ferrand J, Nunes B, Lehours P, Carvalho-Oliveira I, et al. Evaluation of the clinical significance of homB, a novel candidate marker of Helicobacter pylori strains associated with peptic ulcer disease. J Infect Dis. 2008;198:1379–87.PubMedCrossRef
284.
go back to reference Oleastro M, Cordeiro R, Ménard A, Yamaoka Y, Queiroz D, Mégraud F, et al. Allelic diversity and phylogeny of homB, a novel co-virulence marker of Helicobacter pylori. BMC Microbiol. 2009;9:1–12.CrossRef Oleastro M, Cordeiro R, Ménard A, Yamaoka Y, Queiroz D, Mégraud F, et al. Allelic diversity and phylogeny of homB, a novel co-virulence marker of Helicobacter pylori. BMC Microbiol. 2009;9:1–12.CrossRef
285.
go back to reference Sung WJ, Sugimoto M, Graham DY, Yamaoka Y. homB status of Helicobacter pylori as a novel marker to distinguish gastric cancer from duodenal ulcer. J Clin Microbiol. 2009;47:3241–5.CrossRef Sung WJ, Sugimoto M, Graham DY, Yamaoka Y. homB status of Helicobacter pylori as a novel marker to distinguish gastric cancer from duodenal ulcer. J Clin Microbiol. 2009;47:3241–5.CrossRef
287.
go back to reference Mthembu YH, Jin C, Padra M, Liu J, Edlund JO, Ma H, et al. Recombinant mucin-type proteins carrying Lacdi NAc on different O-glycan core chains fail to support H. pylori binding. Mol Omics. 2020;16:243–57.PubMedCrossRef Mthembu YH, Jin C, Padra M, Liu J, Edlund JO, Ma H, et al. Recombinant mucin-type proteins carrying Lacdi NAc on different O-glycan core chains fail to support H. pylori binding. Mol Omics. 2020;16:243–57.PubMedCrossRef
289.
290.
go back to reference Olofsson A, Vallström A, Petzold K, Tegtmeyer N, Schleucher J, Carlsson S, et al. Biochemical and functional characterization of Helicobacter pylori vesicles. Mol Microbiol. 2010;77:1539–55.PubMedPubMedCentralCrossRef Olofsson A, Vallström A, Petzold K, Tegtmeyer N, Schleucher J, Carlsson S, et al. Biochemical and functional characterization of Helicobacter pylori vesicles. Mol Microbiol. 2010;77:1539–55.PubMedPubMedCentralCrossRef
292.
go back to reference Lekmeechai S, Su YC, Brant M, Alvarado-Kristensson M, Vallström A, Obi I, et al. Helicobacter pylori outer membrane vesicles protect the pathogen from reactive oxygen species of the respiratory burst. Front Microbiol. 2018;9:1–6.CrossRef Lekmeechai S, Su YC, Brant M, Alvarado-Kristensson M, Vallström A, Obi I, et al. Helicobacter pylori outer membrane vesicles protect the pathogen from reactive oxygen species of the respiratory burst. Front Microbiol. 2018;9:1–6.CrossRef
293.
go back to reference Ismail S, Hampton MB, Keenan JI. Helicobacter pylori outer membrane vesicles modulate proliferation and interleukin-8 production by gastric epithelial cells. Infect Immun. 2003;71:5670–5.PubMedPubMedCentralCrossRef Ismail S, Hampton MB, Keenan JI. Helicobacter pylori outer membrane vesicles modulate proliferation and interleukin-8 production by gastric epithelial cells. Infect Immun. 2003;71:5670–5.PubMedPubMedCentralCrossRef
294.
go back to reference Hock BD, McKenzie JL, Keenan JI. Helicobacter pylori outer membrane vesicles inhibit human T cell responses via induction of monocyte COX-2 expression. Pathog Dis. 2017;75:1–4.CrossRef Hock BD, McKenzie JL, Keenan JI. Helicobacter pylori outer membrane vesicles inhibit human T cell responses via induction of monocyte COX-2 expression. Pathog Dis. 2017;75:1–4.CrossRef
295.
go back to reference Song Z, Li B, Zhang Y, Li R, Ruan H, Wu J, et al. Outer membrane vesicles of Helicobacter pylori 713 as adjuvants promote protective efficacy against Helicobacter pylori infection. Front Microbiol. 2020;11:1–13.CrossRef Song Z, Li B, Zhang Y, Li R, Ruan H, Wu J, et al. Outer membrane vesicles of Helicobacter pylori 713 as adjuvants promote protective efficacy against Helicobacter pylori infection. Front Microbiol. 2020;11:1–13.CrossRef
296.
go back to reference Yonezawa H, Osaki T, Kurata S, Fukuda M, Kawakami H, Ochiai K, et al. Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol. 2009;9:197.PubMedPubMedCentralCrossRef Yonezawa H, Osaki T, Kurata S, Fukuda M, Kawakami H, Ochiai K, et al. Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol. 2009;9:197.PubMedPubMedCentralCrossRef
297.
go back to reference Kaparakis M, Turnbull L, Carneiro L, Firth S, Coleman HA, Parkington HC, et al. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol. 2010;12:372–85.PubMedCrossRef Kaparakis M, Turnbull L, Carneiro L, Firth S, Coleman HA, Parkington HC, et al. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol. 2010;12:372–85.PubMedCrossRef
298.
go back to reference Turner L, Praszkier J, Hutton ML, Steer D, Ramm G, Kaparakis-Liaskos M, et al. Increased outer membrane vesicle formation in a Helicobacter pylori tolB mutant. Helicobacter. 2015;20:269–83.PubMedCrossRef Turner L, Praszkier J, Hutton ML, Steer D, Ramm G, Kaparakis-Liaskos M, et al. Increased outer membrane vesicle formation in a Helicobacter pylori tolB mutant. Helicobacter. 2015;20:269–83.PubMedCrossRef
299.
go back to reference Fiocca R, Necchi V, Sommi P, Ricci V, Telford J, Cover TL, et al. Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J Pathol. 1999;188:220–6.PubMedCrossRef Fiocca R, Necchi V, Sommi P, Ricci V, Telford J, Cover TL, et al. Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J Pathol. 1999;188:220–6.PubMedCrossRef
300.
go back to reference Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, et al. Traces of human migrations in Helicobacter pylori populations. Science (80-). 2003;299:1582–5.CrossRef Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, et al. Traces of human migrations in Helicobacter pylori populations. Science (80-). 2003;299:1582–5.CrossRef
301.
go back to reference Roszczenko-Jasińska P, Wojtyś MI, Jagusztyn-Krynicka EK. Helicobacter pylori treatment in the post-antibiotics era—searching for new drug targets. Appl Microbiol Biotechnol. 2020;104:9891–905.PubMedPubMedCentralCrossRef Roszczenko-Jasińska P, Wojtyś MI, Jagusztyn-Krynicka EK. Helicobacter pylori treatment in the post-antibiotics era—searching for new drug targets. Appl Microbiol Biotechnol. 2020;104:9891–905.PubMedPubMedCentralCrossRef
302.
go back to reference González-Valencia G, Atherton JC, Muñoz O, Dehesa M, Madrazo-De-la-Garza A, Torres J. Helicobacter pylori vacA and cagA genotypes in Mexican adults and children. J Infect Dis. 2000;182:1450–4.PubMedCrossRef González-Valencia G, Atherton JC, Muñoz O, Dehesa M, Madrazo-De-la-Garza A, Torres J. Helicobacter pylori vacA and cagA genotypes in Mexican adults and children. J Infect Dis. 2000;182:1450–4.PubMedCrossRef
303.
go back to reference Foegeding NJ, Caston RR, McClain MS, Ohi MD, Cover TL. An overview of Helicobacter pylori VacA toxin biology. Toxins (Basel). 2016;8:1–21.CrossRef Foegeding NJ, Caston RR, McClain MS, Ohi MD, Cover TL. An overview of Helicobacter pylori VacA toxin biology. Toxins (Basel). 2016;8:1–21.CrossRef
304.
go back to reference Sugimoto M, Zali MR, Yamaoka Y. The association of vacA genotypes and Helicobacter pylori-related gastroduodenal diseases in the Middle East. Eur J Clin Microbiol Infect Dis. 2009;28:1227–36.PubMedPubMedCentralCrossRef Sugimoto M, Zali MR, Yamaoka Y. The association of vacA genotypes and Helicobacter pylori-related gastroduodenal diseases in the Middle East. Eur J Clin Microbiol Infect Dis. 2009;28:1227–36.PubMedPubMedCentralCrossRef
305.
go back to reference Qabandi AA, Mustafa AS, Siddique I, Khajah AK, Madda JP, Junaid TA. Distribution of vacA and cagA genotypes of Helicobacter pylori in Kuwait. Acta Trop. 2005;93:283–8.PubMedCrossRef Qabandi AA, Mustafa AS, Siddique I, Khajah AK, Madda JP, Junaid TA. Distribution of vacA and cagA genotypes of Helicobacter pylori in Kuwait. Acta Trop. 2005;93:283–8.PubMedCrossRef
306.
go back to reference Yamaoka Y, Reddy R, Graham DY. Helicobacter pylori virulence factor genotypes in children in the United States: clues about genotype and outcome relationships. J Clin Microbiol. 2010;48:2550–1.PubMedPubMedCentralCrossRef Yamaoka Y, Reddy R, Graham DY. Helicobacter pylori virulence factor genotypes in children in the United States: clues about genotype and outcome relationships. J Clin Microbiol. 2010;48:2550–1.PubMedPubMedCentralCrossRef
307.
go back to reference Sicinschi LA, Correa P, Bravo LE, Peek RM, Wilson KT, Loh JT, et al. Non-invasive genotyping of Helicobacter pylori cagA, vacA, and hopQ from asymptomatic children. Helicobacter. 2012;17:96–106.PubMedPubMedCentralCrossRef Sicinschi LA, Correa P, Bravo LE, Peek RM, Wilson KT, Loh JT, et al. Non-invasive genotyping of Helicobacter pylori cagA, vacA, and hopQ from asymptomatic children. Helicobacter. 2012;17:96–106.PubMedPubMedCentralCrossRef
308.
go back to reference Chen MY, He CY, Meng X, Yuan Y. Association of Helicobacter pylori babA2 with peptic ulcer disease and gastric cancer. World J Gastroenterol. 2013;19:4242–51.PubMedPubMedCentralCrossRef Chen MY, He CY, Meng X, Yuan Y. Association of Helicobacter pylori babA2 with peptic ulcer disease and gastric cancer. World J Gastroenterol. 2013;19:4242–51.PubMedPubMedCentralCrossRef
309.
go back to reference Schmees C, Prinz C, Treptau T, Rad R, Hengst L, Voland P, et al. Inhibition of T-cell proliferation by Helicobacter pylori γ-glutamyl transpeptidase. Gastroenterology. 2007;132:1820–33.PubMedCrossRef Schmees C, Prinz C, Treptau T, Rad R, Hengst L, Voland P, et al. Inhibition of T-cell proliferation by Helicobacter pylori γ-glutamyl transpeptidase. Gastroenterology. 2007;132:1820–33.PubMedCrossRef
Metadata
Title
Infiltration to infection: key virulence players of Helicobacter pylori pathogenicity
Authors
Arghyadeep Bhattacharjee
Om Saswat Sahoo
Ahana Sarkar
Saurabh Bhattacharya
Rukhsana Chowdhury
Samarjit Kar
Oindrilla Mukherjee
Publication date
25-01-2024
Publisher
Springer Berlin Heidelberg
Published in
Infection / Issue 2/2024
Print ISSN: 0300-8126
Electronic ISSN: 1439-0973
DOI
https://doi.org/10.1007/s15010-023-02159-9

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