Top

European Journal of Clinical Microbiology & Infectious Diseases

Published in:

01-10-2020 | Helicobacter Pylori | Review

Virulence of Helicobacter pylori outer membrane proteins: an updated review

Authors: Chenjing Xu, Djaleel Muhammad Soyfoo, Yao Wu, Shunfu Xu

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 10/2020

Abstract

Helicobacter pylori (H. pylori) infection is associated with some gastric diseases, such as gastritis, peptic ulcer, and gastric cancer. CagA and VacA are known virulence factors of H. pylori, which play a vital role in severe clinical outcomes. Additionally, the expression of outer membrane proteins (OMPs) helps H. pylori attach to gastric epithelial cells at the primary stage and increases the virulence of H. pylori. In this review, we have summarized the paralogs of H. pylori OMPs, their genomic loci, and the different receptors of OMPs identified so far. We focused on five OMPs, BabA (HopS), SabA (HopP), OipA (HopH), HopQ, and HopZ, and one family of OMPs: Hom. We highlight the coexpression of OMPs with other virulence factors and their relationship with clinical outcomes. In conclusion, OMPs are closely related to the pathogenic processes of adhesion, colonization, persistent infection, and severe clinical consequences. They are potential targets for the prevention and treatment of H. pylori–related diseases.

Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, Malfertheiner P, Graham DY, Wong VWS, Wu JCY, Chan FKL, Sung JJY, Kaplan GG (2017) Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology 153(2):420–429. https://doi.org/10.1053/j.gastro.2017.04.022CrossRefPubMed

Zamani M, Ebrahimtabar F, Zamani V, Miller WH, Alizadeh-Navaei R, Shokri-Shirvani J (2018) Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther 47(7):868–876. https://doi.org/10.1111/apt.14561CrossRefPubMed

Kim A, Servetas SL, Kang J, Kim J, Jang S, Cha HJ, Lee WJ, Kim J, Romero-Gallo J, Peek RM, Merrell DS (2015) Helicobacter pylori bab paralog distribution and association with cagA, vacA, and homA/B genotypes in American and South Korean clinical isolates. PLoS One 10(8):e0137078. https://doi.org/10.1371/journal.pone.0137078CrossRefPubMedPubMedCentral

Kalach N, Bontems P (2017) Helicobacter pylori infection in children. Helicobacter. https://doi.org/10.1111/hel.12414

Boehnke KF, Brewster RK, Sánchez BN, Valdivieso M, Bussalleu A, Guevara M, Saenz CG, Alva SO, Gil E (2018) An assessment of drinking water contamination with Helicobacter pylori in Lima, Peru. Helicobacter 23(2):e12462. https://doi.org/10.1111/hel.12462CrossRefPubMed

Siavoshi F, Sahraee M, Ebrahimi H, Sarrafnejad A (2018) Natural fruits, flowers, honey, and honeybees harbor Helicobacter pylori-positive yeasts. Helicobacter 23(2):e12471. https://doi.org/10.1111/hel.12471CrossRefPubMed

Chen Q, Liang X, Long X, Yu L, Liu W (2019) Cost-effectiveness analysis of screen-and-treat strategy in asymptomatic Chinese for preventing Helicobacter pylori-associated diseases. Helicobacter 24(2):e12563. https://doi.org/10.1111/hel.12563CrossRefPubMed

Qiao S, Luo Q, Zhao Y, Zhang XC, Huang Y (2014) Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature 511(7507):108–111. https://doi.org/10.1038/nature13484CrossRefPubMed

Egan AJF (2018) Bacterial outer membrane constriction. Mol Microbiol 107(6):676–687. https://doi.org/10.1111/mmi.13908CrossRefPubMed

10.

Waskito LA, Salama NR (2018) Pathogenesis of Helicobacter pylori infection. Helicobacter:e12516. https://doi.org/10.1111/hel.12516

11.

Koebnik R, Locher KP (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37(2):239–253. https://doi.org/10.1046/j.1365-2958.2000.01983.xCrossRefPubMed

12.

Alm RA, Bina J, Andrews BM, Doig P, Hancock RE (2000) Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect Immun 68(7):4155–4168. https://doi.org/10.1128/iai.68.7.4155-4168.2000CrossRefPubMedPubMedCentral

13.

Kennemann L, Brenneke B, Andres S, Engstrand L, Meyer TF, Aebischer T, Josenhans C (2012) In vivo sequence variation in HopZ, a phase-variable outer membrane protein of Helicobacter pylori. Infect Immun 80(12):4364–4373. https://doi.org/10.1128/iai.00977-12CrossRefPubMedPubMedCentral

14.

Oleastro M, Cordeiro R, Ménard A, Yamaoka Y, Queiroz D, Mégraud F (2009) Allelic diversity and phylogeny of homB, a novel co-virulence marker of Helicobacter pylori. BMC Microbiol 9:248. https://doi.org/10.1186/1471-2180-9-248CrossRefPubMedPubMedCentral

15.

Harvey VC, Acio CR, Bredehoft AK, Zhu L, Hallinger DR, Quinlivan-Repasi V, Harvey SE (2014) Repetitive sequence variations in the promoter region of the adhesin-encoding gene sabA of Helicobacter pylori affect transcription. J Bacteriol 196(19):3421–3429. https://doi.org/10.1128/jb.01956-14CrossRefPubMedPubMedCentral

16.

Moonens K, Gideonsson P, Subedi S, Bugaytsova J, Romaõ E, Mendez M, Nordén J, Fallah M, Rakhimova L, Shevtsova A, Lahmann M, Castaldo G, Brännström K, Coppens F, Lo AW, Ny T, Solnick JV, Vandenbussche G, Oscarson S, Hammarström L, Arnqvist A, Berg DE, Muyldermans S, Borén T (2016) Structural insights into polymorphic ABO glycan binding by Helicobacter pylori. Cell Host Microbe 19(1):55–66. https://doi.org/10.1016/j.chom.2015.12.004CrossRefPubMedPubMedCentral

17.

Pride DT, Meinersmann RJ, Blaser MJ (2001) Allelic variation within Helicobacter pylori babA and babB. Infect Immun 69(2):1160–1171. https://doi.org/10.1128/iai.69.2.1160-1171.2001CrossRefPubMedPubMedCentral

18.

Ansari S, Kabamba ET, Shrestha PK, Aftab H, Myint T, Tshering L, Sharma RP, Ni N, Aye TT, Subsomwong P, Uchida T, Ratanachu-Ek T, Vilaichone RK, Mahachai V, Matsumoto T, Akada J (2017) Helicobacter pylori bab characterization in clinical isolates from Bhutan, Myanmar, Nepal and Bangladesh. PLoS One 12(11):e0187225. https://doi.org/10.1371/journal.pone.0187225CrossRefPubMedPubMedCentral

19.

Ilver D, Arnqvis A, Ogren J, Frick IM, Kersulyte D, Incecik ET, Berg DE, Covacci A, Engstrand L (1998) Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279(5349):373–377. https://doi.org/10.1126/science.279.5349.373CrossRefPubMed

20.

Pride DT, Blaser MJ (2002) Concerted evolution between duplicated genetic elements in Helicobacter pylori. J Mol Biol 316(3):640–642. https://doi.org/10.1006/jmbi.2001.5311CrossRef

21.

Bäckström A, Lundberg C, Kersulyte D, Berg DE, Borén T (2004) Metastability of Helicobacter pylori bab adhesin genes and dynamics in Lewis b antigen binding. Proc Natl Acad Sci U S A 101(48):16923–16928. https://doi.org/10.1073/pnas.0404817101CrossRefPubMedPubMedCentral

22.

Nell S, Kennemann L, Schwarz S, Josenhans C (2014) Dynamics of Lewis b binding and sequence variation of the babA adhesin gene during chronic Helicobacter pylori infection in humans. mBio 5(6):e02281–e02214CrossRef

23.

Kable ME, Hansen LM, Styer CM, Deck SL, Rakhimova O, Shevtsova A, Eaton KA, Martin ME, Gideonsson P, Borén T (2017) Host determinants of expression of the Helicobacter pylori BabA adhesin. Sci Rep 7:46499. https://doi.org/10.1038/srep46499CrossRefPubMedPubMedCentral

24.

Bugaytsova JA, Björnham O, Chernov YA, Gideonsson P, Henriksson S, Mendez M, Sjöström R, Mahdavi J, Shevtsova A, Ilver D, Moonens K, Quintana-Hayashi MP, Moskalenko R, Aisenbrey C, Bylund G, Schmidt A, Åberg A, Brännström K, Königer V, Vikström S, Rakhimova L, Hofer A, Ögren J, Liu H, Goldman MD, Whitmire JM, Ådén J, Younson J, Kelly CG, Gilman RH, Chowdhury A, Mukhopadhyay AK, Nair GB, Papadakos KS, Martinez-Gonzalez B, Sgouras DN, Engstrand L, Unemo M, Danielsson D, Suerbaum S, Oscarson S, Morozova-Roche LA, Olofsson A, Gröbner G, Holgersson J, Esberg A, Strömberg N, Landström M, Eldridge AM, Chromy BA, Hansen LM, Solnick JV, Lindén SK, Haas R, Dubois A, Merrell DS, Schedin S, Remaut H, Arnqvist A, Berg DE (2017) Helicobacter pylori adapts to chronic infection and gastric disease via pH-responsive BabA-mediated adherence. Cell Host Microbe 21(3):376–389. https://doi.org/10.1016/j.chom.2017.02.013CrossRefPubMedPubMedCentral

25.

Hage N, Howard T, Phillips C, Brassington C, Overman R, Debreczeni J, Gellert P, Stolnik S, Winkler GS (2015) Structural basis of Lewis(b) antigen binding by the Helicobacter pylori adhesin BabA. Sci Adv 1(7):e1500315. https://doi.org/10.1126/sciadv.1500315CrossRefPubMedPubMedCentral

26.

Odenbreit S, Swoboda K, Iris B, Stefan R, Rainer H (2009) Outer membrane protein expression profile in Helicobacter pylori clinical isolates. Infect Immun 77(9):3782–3790. https://doi.org/10.1128/IAI.00364-09CrossRefPubMedPubMedCentral

27.

Chang WL, Yeh YC, Sheu BS (2018) The impacts of H. pylori virulence factors on the development of gastroduodenal diseases. J Biomed Sci 25(1):68. https://doi.org/10.1186/s12929-018-0466-9CrossRefPubMedPubMedCentral

28.

Ishijima N, Suzuki M, Ashida H, Ichikawa Y, Kanegae Y, Saito I, Borén T, Haas R, Sasakawa C (2011) BabA-mediated adherence is a potentiator of the Helicobacter pylori type IV secretion system activity. J Biol Chem 286(28):25256–25264. https://doi.org/10.1074/jbc.M111.233601CrossRefPubMedPubMedCentral

29.

Guillemin K, Salama NR, Tompkins LS (2002) Cag pathogenicity island-specific responses of gastric epithelial cells to Helicobacter pylori infection. Proc Natl Acad Sci U S A 99(23):15136–15141. https://doi.org/10.1073/pnas.182558799CrossRefPubMedPubMedCentral

30.

Talarico S, Whitefield SE, Fero J, Haas R (2012) Regulation of Helicobacter pylori adherence by gene conversion. Mol Microbiol 84(6):1050–1061. https://doi.org/10.1111/j.1365-2958.2012.08073.xCrossRefPubMedPubMedCentral

31.

Yamaoka Y (2008) Increasing evidence of the role of Helicobacter pylori SabA in the pathogenesis of gastroduodenal disease. J Infect Dev Ctries 2(3):174. https://doi.org/10.3855/jidc.259CrossRefPubMedPubMedCentral

32.

Michael P, Patricia D, Jennifer S, Beier D (2004) Genetic evidence for histidine kinase HP165 being an acid sensor of Helicobacter pylori. FEMS Microbiol Lett 234(1):51–61. https://doi.org/10.1016/j.femsle.2004.03.023CrossRef

33.

Loh JT, Gupta SS, Friedman DB, Krezel AM (2010) Analysis of protein expression regulated by the Helicobacter pylori ArsRS two-component signal transduction system. J Bacteriol 192(8):2034–2043. https://doi.org/10.1128/jb.01703-08CrossRefPubMedPubMedCentral

34.

Pang SS, Nguyen ST, Perry AJ, Day CJ, Panjikar S, Tiralongo J, Whisstock JC, T K (2014) The three-dimensional structure of the extracellular adhesion domain of the sialic acid-binding adhesin SabA from Helicobacter pylori. J Biol Chem 289(10):6332–6340. https://doi.org/10.1074/jbc.M113.513135CrossRefPubMed

35.

Marcos NT, Magalhães A, Ferreira B, Oliveira MJ, Carvalho AS, Mendes N, Gilmartin T, Head SR, Figueiredo C, David L, Santos-Silva F (2008) Helicobacter pylori induces beta3GnT5 in human gastric cell lines, modulating expression of the SabA ligand sialyl-Lewis x. J Clin Invest 118(6):2325–2336. https://doi.org/10.1172/jci34324CrossRefPubMedPubMedCentral

36.

Benktander J, Barone A, Johansson MM (2018) Helicobacter pylori SabA binding gangliosides of human stomach. Virulence 9(1):738–751. https://doi.org/10.1080/21505594.2018.1440171CrossRefPubMedPubMedCentral

37.

Mahdavi J, Sondén B, Hurtig M, Olfat FO, Forsberg L, Roche N, Angstrom J, Larsson T, Teneberg S, Karlsson KA, Altraja S, Wadström T, Kersulyte D, Berg DE, Dubois A, Petersson C, Magnusson KE, Norberg T, Lindh F, Lundskog BB, Arnqvist A, Hammarström L (2002) Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297(5581):573–578. https://doi.org/10.1126/science.1069076CrossRefPubMedPubMedCentral

38.

Lehours P, Ménard A, Dupouy S, Bergey B, Richy F, Zerbib F, Ruskoné-Fourmestraux A, Delchier JC (2004) Evaluation of the association of nine Helicobacter pylori virulence factors with strains involved in low-grade gastric mucosa-associated lymphoid tissue lymphoma. Infect Immun 72(2):880–888. https://doi.org/10.1128/iai.72.2.880-888.2004CrossRefPubMedPubMedCentral

39.

Yamaoka Y, Ojo O, Fujimoto S, Odenbreit S, Haas R, Gutierrez O, El-Zimaity HM, Reddy R, Arnqvist A (2006) Helicobacter pylori outer membrane proteins and gastroduodenal disease. Gut 55(6):775–781. https://doi.org/10.1136/gut.2005.083014CrossRefPubMedPubMedCentral

40.

Yanai A, Maeda S, Hikiba Y, Shibata W, Ohmae T, Hirata Y, Ogura K, Yoshida H, Omata M (2007) Clinical relevance of Helicobacter pylori sabA genotype in Japanese clinical isolates. J Gastroenterol 22(12):2228–2232. https://doi.org/10.1111/j.1440-1746.2007.04831.xCrossRef

41.

Yamaoka Y, Dong HK, Graham DYA (2000) A M(r) 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc Natl Acad Sci U S A 97(13):7533–7538. https://doi.org/10.1073/pnas.130079797CrossRefPubMedPubMedCentral

42.

Horridge DN, Begley AA, Kim J, Aravindan N, Fan K, Forsyth MH (2017) Outer inflammatory protein a (OipA) of Helicobacter pylori is regulated by host cell contact and mediates CagA translocation and interleukin-8 response only in the presence of a functional cag pathogenicity island type IV secretion system. Pathog Dis 75(8). https://doi.org/10.1093/femspd/ftx113

43.

Farzi N, Yadegar A, Aghdaei HA, Yamaoka Y, Zali MR (2018) Genetic diversity and functional analysis of oipA gene in association with other virulence factors among Helicobacter pylori isolates from Iranian patients with different gastric diseases. Infect Genet Evol 60:26–34. https://doi.org/10.1016/j.meegid.2018.02.017CrossRefPubMed

44.

Yamaoka Y, Kikuchi S, el-Zimaity HM, Gutierrez O, Osato MS, Graham DY (2002) Importance of Helicobacter pylori oipA in clinical presentation, gastric inflammation, and mucosal interleukin 8 production. Gastroenterology 123(2):414–424. https://doi.org/10.1053/gast.2002.34781CrossRefPubMed

45.

Al-Maleki AR, Loke MF, Lui SY, Ramli NSK, Khosravi Y, Ng CG, Venkatraman G, Goh KL, Ho B, Vadivelu J (2017) Helicobacter pylori outer inflammatory protein A (OipA) suppresses apoptosis of AGS gastric cells in vitro. Cell Microbiol 19(12). https://doi.org/10.1111/cmi.12771

46.

Franco AT, Johnston E, Krishna U, Yamaoka Y, Israel DA, Nagy TA, Wroblewski LE, Piazuelo MB, Correa P, Peek RM (2008) Regulation of gastric carcinogenesis by Helicobacter pylori virulence factors. Cancer Res 68(2):379–387. https://doi.org/10.1158/0008-5472.Can-07-0824CrossRefPubMedPubMedCentral

47.

Su B, Ceponis PJM, Sherman PM (2003) Cytoskeletal rearrangements in gastric epithelial cells in response to Helicobacter pylori infection. J Med Microbiol 52:861–867. https://doi.org/10.1099/jmm.0.05229-0CrossRefPubMed

48.

Moese S, Selbach M, Kwok T, Brinkmann V, König W, Meyer TF (2004) Helicobacter pylori induces AGS cell motility and elongation via independent signaling pathways. Infect Immun 72(6):3646–3649. https://doi.org/10.1128/iai.72.6.3646-3649.2004CrossRefPubMedPubMedCentral

49.

Tabassam FH, Graham DY, Yamaoka Y (2008) OipA plays a role in Helicobacter pylori-induced focal adhesion kinase activation and cytoskeletal re-organization. Cell Microbiol 10(4):1008–1020. https://doi.org/10.1111/j.1462-5822.2007.01104.xCrossRefPubMed

50.

Dabiri H, Maleknejad P, Yamaoka Y, Feizabadi MM, Jafari F, Rezadehbashi M, Nakhjavani FA, Mirsalehian A, Zali MR (2009) Distribution of Helicobacter pylori cagA, cagE, oipA and vacA in different major ethnic groups in Tehran, Iran. J Gastroenterol Hepatol 24(8):1380–1386. https://doi.org/10.1111/j.1440-1746.2009.05876.xCrossRefPubMedPubMedCentral

51.

Liu J, He C, Chen M, Wang Z, Xing C, Yuan Y (2013) Association of presence/absence and on/off patterns of Helicobacter pylori oipA gene with peptic ulcer disease and gastric cancer risks: a meta-analysis. BMC Infect Dis 13:555. https://doi.org/10.1186/1471-2334-13-555CrossRefPubMedPubMedCentral

52.

Braga LLBC, Batista MHR, de Azevedo OGR, da Silva Costa KC, Gomes AD, Rocha GA, Queiroz DMM (2019) oipA “on” status of Helicobacter pylori is associated with gastric cancer in North-Eastern Brazil. BMC Cancer 19(1):48. https://doi.org/10.1186/s12885-018-5249-xCrossRefPubMedPubMedCentral

53.

Mahboubi M, Falsafi T, Sadeghizadeh M, Mahjoub F (2017) The role of outer inflammatory protein A (OipA) in vaccination of theC57BL/6 mouse model infected by Helicobacter pylori. Turk J Med Sci 47(1):326–333. https://doi.org/10.3906/sag-1505-108CrossRefPubMed

54.

Yakoob J, Abbas Z, Jafri W, Khan R, Salim SA, Awan S, Abid S, Hamid S, Ahmad Z (2016) Helicobacter pylori outer membrane protein and virulence marker differences in expatriate patients. Epidemiol Infect 144(10):2200–2208. https://doi.org/10.1017/s095026881600025xCrossRefPubMed

55.

Ohno T, Sugimoto M, Nagashima A, Ogiwara H, Vilaichone RK, Mahachai V, Graham DY, Yamaoka Y (2009) Relationship between Helicobacter pylori hopQ genotype and clinical outcome in Asian and Western populations. J Gastroenterol Hepatol 24(3):462–468. https://doi.org/10.1111/j.1440-1746.2008.05762.xCrossRefPubMedPubMedCentral

56.

Belogolova E, Bauer B, Pompaiah M, Asakura H, Brinkman V, Ertl C, Bartfeld S, Nechitaylo TY, Haas R, Machuy N, Salama N, Churin Y (2013) Helicobacter pylori outer membrane protein HopQ identified as a novel T4SS-associated virulence factor. Cell Microbiol 15(11):1896–1912. https://doi.org/10.1111/cmi.12158CrossRefPubMedPubMedCentral

57.

Tegtmeyer N, Harrer A, Schmitt V, Singer BB (2019) Expression of CEACAM1 or CEACAM5 in AZ-521 cells restores the type IV secretion deficiency for translocation of CagA by Helicobacter pylori. Cell Microbiol 21(1):e12965. https://doi.org/10.1111/cmi.12965CrossRefPubMed

58.

Moonens K, Hamway Y, Neddermann M, Reschke M, Tegtmeyer N, Kruse T, Kammerer R, Mejías-Luque R, Singer BB, Backert S, Gerhard M (2018) Helicobacter pylori adhesin HopQ disrupts dimerization in human CEACAMs. EMBO J 37(13). https://doi.org/10.15252/embj.201798665

59.

Königer V, Holsten L, Harrison U, Busch B, Loell E, Zhao Q, Bonsor DA, Roth A, Kengmo-Tchoupa A, Smith SI, Mueller S, Sundberg EJ, Zimmermann W, Fischer W, Hauck CR (2016) Erratum: Helicobacter pylori exploits human CEACAMs via HopQ for adherence and translocation of CagA. Nat Microbiol 2:16233. https://doi.org/10.1038/nmicrobiol.2016.233CrossRefPubMed

60.

Teymournejad O, Mobarez AM, Hassan ZM (2017) Binding of the Helicobacter pylori OipA causes apoptosis of host cells via modulation of Bax/Bcl-2 levels. Sci Rep 7(1):8036. https://doi.org/10.1038/s41598-017-08176-7CrossRefPubMedPubMedCentral

61.

Sheu BS, Yang HB, Yeh YC (2010) Helicobacter pylori colonization of the human gastric epithelium: a bug’s first step is a novel target for us. J Gastroenterol Hepatol 25(1):26–32. https://doi.org/10.1111/j.1440-1746.2009.06141.xCrossRefPubMed

62.

Peck B, Ortkamp M, Diehl KD, Hundt E (1999) Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. Nucleic Acids Res 27(16):3325–3333. https://doi.org/10.1093/nar/27.16.3325CrossRefPubMedPubMedCentral

63.

Kennemann L, Didelot X, Aebischer T, Kuhn S, Drescher B, Droege M, Reinhardt R, Correa P, Meyer TF, Josenhans C, Falush D (2011) Helicobacter pylori genome evolution during human infection. Proc Natl Acad Sci U S A 108(12):5033–5038. https://doi.org/10.1073/pnas.1018444108CrossRefPubMedPubMedCentral

64.

Odenbreit S, Kavermann H, Püls J, Haas R (2002) 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 292:257–266. https://doi.org/10.1078/1438-4221-00205CrossRefPubMed

65.

Servetas SL, Kim A, Su H, Cha JH (2018) Comparative analysis of the Hom family of outer membrane proteins in isolates from two geographically distinct regions: the United States and South Korea. Helicobacter 23(2):e12461. https://doi.org/10.1111/hel.12461CrossRefPubMed

66.

Oleastro M, Cordeiro R, Ménard A, Gomes JP (2010) Allelic diversity among Helicobacter pylori outer membrane protein genes homB and homA generated by recombination. J Bacteriol 192(15):3961–3968. https://doi.org/10.1128/jb.00395-10CrossRefPubMedPubMedCentral

67.

Kim A, Servetas SL, Kang J, Kim J, Jang S, Choi YH, Su H, Jeon YE, Hong YA, Yoo YJ, Merrell DS (2016) Helicobacter pylori outer membrane protein, HomC, shows geographic dependent polymorphism that is influenced by the Bab family. J Microbiol 54(12):846–852. https://doi.org/10.1007/s12275-016-6434-8CrossRefPubMed

68.

Oleastro M, Monteiro L, Lehours P, Mégraud F (2006) Identification of markers for Helicobacter pylori strains isolated from children with peptic ulcer disease by suppressive subtractive hybridization. Infect Immun 74(7):4064–4074. https://doi.org/10.1128/iai.00123-06CrossRefPubMedPubMedCentral

69.

Oleastro M, Cordeiro R, Yamaoka Y, Queiroz D, Mégraud F, Monteiro L (2009) Disease association with two Helicobacter pylori duplicate outer membrane protein genes, homB and homA. J Gut pathogens 1(1):12. https://doi.org/10.1186/1757-4749-1-12CrossRef

70.

Jung SW, Sugimoto M, Graham DY (2009) homB status of Helicobacter pylori as a novel marker to distinguish gastric cancer from duodenal ulcer. J Biol Chem 47(10):3241–3245. https://doi.org/10.1128/jcm.00293-09CrossRef

71.

Kang J, Jones KR, Jang S, Olsen CH, Yoo YJ, Merrell DS (2012) The geographic origin of Helicobacter pylori influences the association of the homB gene with gastric cancer. J Clin Microbiol 50(3):1082–1085. https://doi.org/10.1128/jcm.06293-11CrossRefPubMedPubMedCentral

72.

Zeng M, Mao XH, Li JX, Tong WD, Wang B, Zhang YJ, Guo G, Zhao ZJ, Li L, Wu DL, Lu DS, Tan ZM, Liang HY, Wu C, Li DH, Luo P, Zeng H, Zhang WJ, Zhang JY, Guo BT, Zhu FC (2015) Efficacy, safety, and immunogenicity of an oral recombinant Helicobacter pylori vaccine in children in China: a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 386(10002):1457–1464. https://doi.org/10.1016/s0140-6736(15)60310-5CrossRefPubMed

73.

Fallone CA, Moss SF, Malfertheiner P (2019) Reconciliation of recent Helicobacter pylori treatment guidelines in a time of increasing resistance to antibiotics. Gastroenterology 157(1):44–53. https://doi.org/10.1053/j.gastro.2019.04.011CrossRefPubMed

74.

Minhu C, Adrian L, Stuart H (1992) Immunisation against gastric helicobacter infection in a mouse/Helicobacter felis model. Lancet. https://doi.org/10.1016/0140-6736(92)90720-N

75.

Mirzaei N, Poursina F, Moghim S, Rashidi N, Safaei HG (2017) The study of H. pylori putative candidate factors for single- and multi-component vaccine development. Crit Rev Microbiol 43(5):631–650. https://doi.org/10.1080/1040841X.2017.1291578CrossRefPubMed

76.

Larena M, Holmgren J, Lebens M, Terrinoni M (2015) Cholera toxin, and the related nontoxic adjuvants mmCT and dmLT, promote human Th17 responses via cyclic AMP-protein kinase A and inflammasome-dependent IL-1 signaling. J Immunol 194(8):3829–3839. https://doi.org/10.4049/jimmunol.1401633CrossRefPubMed

77.

Maisonneuve C, Bertholet S, Philpott DJ, De GE (2014) Unleashing the potential of NOD- and Toll-like agonists as vaccine adjuvants. Proc Natl Acad Sci U S A 111(34):12294–12299. https://doi.org/10.1073/pnas.1400478111CrossRefPubMedPubMedCentral

78.

He P, Zou Y, Hu Z (2015) Advances in aluminum hydroxide-based adjuvant research and its mechanism. Hum Vaccin Immunother 11(2):477–488. https://doi.org/10.1080/21645515.2014.1004026CrossRefPubMedPubMedCentral

79.

Keikha M, Eslami M, Yousefi B, Ghasemian A (2019) Potential antigen candidates for subunit vaccine development against Helicobacter pylori infection. J Cell Physiol 234(12):21460–21470. https://doi.org/10.1002/jcp.28870CrossRefPubMed

80.

Ebbensgaard A, Mordhorst H, Aarestrup FM, Hansen EB (2018) The role of outer membrane proteins and lipopolysaccharides for the sensitivity of Escherichia coli to antimicrobial peptides. Front Microbiol 9:2153. https://doi.org/10.3389/fmicb.2018.02153CrossRefPubMedPubMedCentral

81.

Barbosa AS, Monaris D, Silva LB, Morais ZM, Vasconcellos SA, Cianciarullo AM, Isaac L (2010) Functional characterization of LcpA, a surface-exposed protein of Leptospira spp. that binds the human complement regulator C4BP. Infect Immun 78(7):3207–3216. https://doi.org/10.1128/iai.00279-10CrossRefPubMedPubMedCentral

82.

Liu C, Pan X, Xia B, Chen F, Jin Y, Bai F, Priebe G, Cheng Z, Jin S (2018) Construction of a protective vaccine against lipopolysaccharide-heterologous Pseudomonas aeruginosa strains based on expression profiling of outer membrane proteins during infection. Front Immunol 9:1737. https://doi.org/10.3389/fimmu.2018.01737CrossRefPubMedPubMedCentral

83.

Tohidi F, Teymournejad O, Taravati A, Ahmadi KJA (2015) Analysis of important H. pylori outer membrane proteins by detection of common sequences in exposed areas; in silico study. Biosci Biotechnol Res Asia 12(Spl. Edn. 2):135–143. https://doi.org/10.13005/bbra/2020CrossRef

84.

Ofek I, Hasty DL, Sharon N (2003) Anti-adhesion therapy of bacterial diseases: prospects and problems. Med Microbiol Immunol 38(3):181–191. https://doi.org/10.1016/s0928-8244(03)00228-1CrossRef

85.

Delcour AH (2009) Outer membrane permeability and antibiotic resistance. Biochim Biophys Acta 1794(5):808–816. https://doi.org/10.1016/j.bbapap.2008.11.005CrossRefPubMed

86.

Chen J, Li N, She F (2014) Helicobacter pylori outer inflammatory protein DNA vaccine-loaded bacterial ghost enhances immune protective efficacy in C57BL/6 mice. Vaccine 32(46):6054–6060. https://doi.org/10.1016/j.vaccine.2014.09.014CrossRefPubMed

87.

George L, Goldberg JB (2012) Outer membrane biogenesis in Escherichia coli, Neisseria meningitidis, and Helicobacter pylori: paradigm deviations in H. pylori. Front Cell Infect Microbiol 2:–29. https://doi.org/10.3389/fcimb.2012.00029

88.

Peck B, Ortkamp M, Nau U, Niederweis M, Hundt E (2001) Characterization of four members of a multigene family encoding outer membrane proteins of Helicobacter pylori and their potential for vaccination. Microbes Infect 3(3):171–179. https://doi.org/10.1016/s1286-4579(01)01377-6CrossRefPubMed

89.

Aspholm-Hurtig M, Dailide G, Lahmann M, Kalia A, Ilver D, Roche N, Vikström S, Sjöström R, Lindén S, Bäckström A, Lundberg C, Arnqvist A, Mahdavi J, Nilsson UJ, Velapatiño B, Gilman RH, Gerhard M, Alarcon T, López-Brea M, Nakazawa T, Fox JG, Correa P, Dominguez-Bello MG, Perez-Perez GI, Blaser MJ, Normark S, Carlstedt I, Oscarson S, Teneberg S, Berg DE (2004) Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 305(5683):519–522. https://doi.org/10.1126/science.1098801CrossRefPubMed

90.

Walz A, Odenbreit S, Stühler K, Wattenberg A, Meyer HE, Mahdavi J, Borén T (2009) 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 9(6):1582–1592. https://doi.org/10.1002/pmic.200700808CrossRefPubMed

91.

Borén T, Falk P, Roth KA, Larson G (1993) Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262(5141):1892–1895. https://doi.org/10.1126/science.8018146CrossRefPubMed

92.

Royle L, Roos A, Harvey DJ, Wormald MR, van Gijlswijk-Janssen D, Redwan e-RM, Wilson IA, Daha MR, Dwek RA (2003) Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems. J Biol Chem 278(22):20140–20153. https://doi.org/10.1074/jbc.M301436200CrossRefPubMed

93.

Issa S, Moran AP, Ustinov SN, Lin JH, Ligtenberg AJ (2010) O-linked oligosaccharides from salivary agglutinin: Helicobacter pylori binding sialyl-Lewis x and Lewis b are terminating moieties on hyperfucosylated oligo-N-acetyllactosamine. Glycobiology 20(8):1046–1057. https://doi.org/10.1093/glycob/cwq066CrossRefPubMed

94.

Lindén S, Mahdavi J, Hedenbro J, Borén T, Carlstedt I (2004) Effects of pH on Helicobacter pylori binding to human gastric mucins: identification of binding to non-MUC5AC mucins. Biochem J 384:263–270. https://doi.org/10.1042/bj20040402CrossRefPubMedPubMedCentral

95.

Kenny DT, Skoog EC, Lindén SK, Struwe WB, Rudd PM (2012) Presence of terminal N-acetylgalactosamineβ1-4N-acetylglucosamine residues on O-linked oligosaccharides from gastric MUC5AC: involvement in Helicobacter pylori colonization? Glycobiology 22(8):1077–1085. https://doi.org/10.1093/glycob/cws076CrossRefPubMed

96.

Lindén SK, Sheng YH, Every AL, Miles KM, Skoog EC, Florin TH, Sutton P (2009) MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy. PLoS Pathog 5(10):e1000617. https://doi.org/10.1371/journal.ppat.1000617CrossRefPubMedPubMedCentral

97.

Cohen M, Drut R, Cueto RE (2003) SIALYL-Tn antigen distribution in Helicobacter pylori chronic gastritis in children: an immunohistochemical study. Pediatr Pathol Mol Med 22(2):117–129. https://doi.org/10.1080/pdp.22.2.117.129CrossRefPubMed

98.

Walz A, Odenbreit S, Mahdavi J, Borén T (2005) Identification and characterization of binding properties of Helicobacter pylori by glycoconjugate arrays. Glycobiology 15(7):700–708. https://doi.org/10.1093/glycob/cwi049CrossRefPubMed

99.

Aspholm M, Olfat FO, Nordén J, Sondén B, Lundberg C, Sjöström R, Altraja S, Odenbreit S, Haas R, Wadström T, Engstrand L, Semino-Mora C, Liu H, Dubois A, Teneberg S, Arnqvist A (2006) SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog 2(10):e110. https://doi.org/10.1371/journal.ppat.0020110CrossRefPubMedPubMedCentral

100.

Unemo M, Aspholm-Hurtig M, Ilver D, Bergström J, Borén T, Danielsson D (2005) The sialic acid binding SabA adhesin of Helicobacter pylori is essential for nonopsonic activation of human neutrophils. J Biol Chem 280(15):15390–15397. https://doi.org/10.1074/jbc.M412725200CrossRefPubMed

101.

Matsuo Y, Kido Y, Yamaoka Y (2017) Helicobacter pylori outer membrane protein-related pathogenesis. Toxins 9(3). https://doi.org/10.3390/toxins9030101

Title: Virulence of Helicobacter pylori outer membrane proteins: an updated review
Authors: Chenjing Xu
Djaleel Muhammad Soyfoo
Yao Wu
Shunfu Xu
Publication date: 01-10-2020
Publisher: Springer Berlin Heidelberg
Keywords: Helicobacter Pylori
Gastric Cancer
Gastric Cancer
Published in: European Journal of Clinical Microbiology & Infectious Diseases / Issue 10/2020
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI: https://doi.org/10.1007/s10096-020-03948-y

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

Illustration of figure on mountain summit/© Orapun / Stock.adobe.com, STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 10/2020

Screening and evaluation of Mycobacterium tuberculosis diagnostic antigens

Nosocomial outbreak linked to a flexible gastrointestinal endoscope contaminated with an amikacin-resistant ST17 clone of Pseudomonas aeruginosa

Septic shock caused by Capnocytophaga canis after a cat scratch

Changing epidemiology and resistance patterns of pathogens causing neonatal bacteremia

Relationships among streptococci from the mitis group, misidentified as Streptococcus pneumoniae

Effect of angiotensin II blockers on the prognosis of COVID-19: a toxicological view

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage