Skip to main content
Top
Published in: Journal of Gastrointestinal Cancer 4/2016

01-12-2016 | Original Research

Helicobacter pylori Peptidyl Prolyl Isomerase Expression Is Associated with the Severity of Gastritis

Authors: Akbar Oghalaie, Samaneh Saberi, Maryam Esmaeili, Fatemeh Ebrahimzadeh, Farzaneh Barkhordari, Abdolreza Ghamarian, Mohammad Tashakoripoor, Afshin Abdirad, Mahmoud Eshagh Hosseini, Vahid Khalaj, Marjan Mohammadi

Published in: Journal of Gastrointestinal Cancer | Issue 4/2016

Login to get access

Abstract

Purpose

Helicobacter pylori secretory peptidyl prolyl isomerase, HP0175, is progressively identified as a pro-inflammatory and pro-carcinogenic protein, which serves to link H. pylori infection to its more severe clinical outcomes. Here, we have analyzed host HP0175-specific antibody responses in relation to the severity of gastritis.

Methods

The HP0175 gene fragment was PCR-amplified, cloned, expressed and purified by Ni-NTA affinity chromatography. Serum antigen-specific antibody responses of non-ulcer dyspeptic patients (N = 176) against recombinant HP0175 were detected by western blotting. The infection status of these subjects was determined by rapid urease test, culture, histology, and serology. The grade of inflammation and stage of atrophy were scored blindly according to the OLGA staging system.

Results

The recombinant HP0175 (rHP0175) was expressed as a ~35 kDa protein and its identity was confirmed by western blotting using anti-6X His tag antibody and pooled H. pylori-positive sera. Serum IgG antibodies against rHP0175 segregated our patients into two similar-sized groups of sero-positives (90/176, 51.1 %) and sero-negatives (86/176, 48.9 %). The former presented with higher grades of gastric inflammation (OR = 4.4, 95 % CI = 1.9–9.9, P = 0.001) and stages of gastric atrophy (OR = 18.3, 95 %CI = 1.4-246.6, P = 0.028).

Conclusion

Our findings lend further support to the pro-inflammatory nature of H. pylori peptidyl prolyl isomerase (HP0175) and recommends this antigen as a non-invasive serum biomarker of the severity of H. pylori-associated gastritis.
Literature
3.
go back to reference Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, Nelson K, Quackenbush J, Zhou L, Kirkness EF, Peterson S, Loftus B, Richardson D, Dodson R, Khalak HG, Glodek A, McKenney K, Fitzegerald LM, Lee N, Adams MD, Hickey EK, Berg DE, Gocayne JD, Utterback TR, Peterson JD, Kelley JM, Cotton MD, Weidman JM, Fujii C, Bowman C, Watthey L, Wallin E, Hayes WS, Borodovsky M, Karp PD, Smith HO, Fraser CM, Venter JC. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature. 1997;388(6642):539–47. doi:10.1038/41483.CrossRefPubMed Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, Nelson K, Quackenbush J, Zhou L, Kirkness EF, Peterson S, Loftus B, Richardson D, Dodson R, Khalak HG, Glodek A, McKenney K, Fitzegerald LM, Lee N, Adams MD, Hickey EK, Berg DE, Gocayne JD, Utterback TR, Peterson JD, Kelley JM, Cotton MD, Weidman JM, Fujii C, Bowman C, Watthey L, Wallin E, Hayes WS, Borodovsky M, Karp PD, Smith HO, Fraser CM, Venter JC. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature. 1997;388(6642):539–47. doi:10.​1038/​41483.CrossRefPubMed
4.
go back to reference McAtee CP, Lim MY, Fung K, Velligan M, Fry K, Chow TP, Berg DE. Characterization of a Helicobacter pylori vaccine candidate by proteome techniques. J Chromatogr B Biomed Sci Appl. 1998;714(2):325–33.CrossRefPubMed McAtee CP, Lim MY, Fung K, Velligan M, Fry K, Chow TP, Berg DE. Characterization of a Helicobacter pylori vaccine candidate by proteome techniques. J Chromatogr B Biomed Sci Appl. 1998;714(2):325–33.CrossRefPubMed
5.
go back to reference Gong YH, Chen M, Xu Y, Dong N, Sang Z, Liu J, Yuan Y. Subtractive hybridization analysis of gastric diseases-associated Helicobacter pylori identifies peptidyl-prolyl isomerase as a potential marker for gastric cancer. FEMS Microbiol Lett. 2011;320(2):103–9. doi:10.1111/j.1574-6968.2011.02296.x.CrossRefPubMed Gong YH, Chen M, Xu Y, Dong N, Sang Z, Liu J, Yuan Y. Subtractive hybridization analysis of gastric diseases-associated Helicobacter pylori identifies peptidyl-prolyl isomerase as a potential marker for gastric cancer. FEMS Microbiol Lett. 2011;320(2):103–9. doi:10.​1111/​j.​1574-6968.​2011.​02296.​x.CrossRefPubMed
6.
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(5):714–29. doi:10.1111/cmi.12396.CrossRefPubMed 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(5):714–29. doi:10.​1111/​cmi.​12396.CrossRefPubMed
7.
go back to reference Basak C, Pathak SK, Bhattacharyya A, Pathak S, Basu J, Kundu M. The secreted peptidyl prolyl cis,trans-isomerase HP0175 of Helicobacter pylori induces apoptosis of gastric epithelial cells in a TLR4- and apoptosis signal-regulating kinase 1-dependent manner. J Immunol. 2005;174(9):5672–80.CrossRefPubMed Basak C, Pathak SK, Bhattacharyya A, Pathak S, Basu J, Kundu M. The secreted peptidyl prolyl cis,trans-isomerase HP0175 of Helicobacter pylori induces apoptosis of gastric epithelial cells in a TLR4- and apoptosis signal-regulating kinase 1-dependent manner. J Immunol. 2005;174(9):5672–80.CrossRefPubMed
9.
go back to reference Basu S, Pathak SK, Chatterjee G, Pathak S, Basu J, Kundu M. Helicobacter pylori protein HP0175 transactivates epidermal growth factor receptor through TLR4 in gastric epithelial cells. J Biol Chem. 2008;283(47):32369–76. doi:10.1074/jbc.M805053200.CrossRefPubMed Basu S, Pathak SK, Chatterjee G, Pathak S, Basu J, Kundu M. Helicobacter pylori protein HP0175 transactivates epidermal growth factor receptor through TLR4 in gastric epithelial cells. J Biol Chem. 2008;283(47):32369–76. doi:10.​1074/​jbc.​M805053200.CrossRefPubMed
10.
go back to reference Zhu Y, Chen M, Gong Y, Liu Z, Li A, Kang D, Han F, Liu J, Liu J, Yuan Y. Helicobacter pylori FKBP-type PPIase promotes gastric epithelial cell proliferation and anchorage-independent growth through activation of ERK-mediated mitogenic signaling pathway. FEMS Microbiol Lett. 2015;362(7). doi:10.1093/femsle/fnv023. Zhu Y, Chen M, Gong Y, Liu Z, Li A, Kang D, Han F, Liu J, Liu J, Yuan Y. Helicobacter pylori FKBP-type PPIase promotes gastric epithelial cell proliferation and anchorage-independent growth through activation of ERK-mediated mitogenic signaling pathway. FEMS Microbiol Lett. 2015;362(7). doi:10.​1093/​femsle/​fnv023.
11.
go back to reference Amedei A, Munari F, Bella CD, Niccolai E, Benagiano M, Bencini L, Cianchi F, Farsi M, Emmi G, Zanotti G, de Bernard M, Kundu M, D’Elios MM. Helicobacter pylori secreted peptidyl prolyl cis, trans-isomerase drives Th17 inflammation in gastric adenocarcinoma. Intern Emerg Med. 2014;9(3):303–9. doi:10.1007/s11739-012-0867-9.CrossRefPubMed Amedei A, Munari F, Bella CD, Niccolai E, Benagiano M, Bencini L, Cianchi F, Farsi M, Emmi G, Zanotti G, de Bernard M, Kundu M, D’Elios MM. Helicobacter pylori secreted peptidyl prolyl cis, trans-isomerase drives Th17 inflammation in gastric adenocarcinoma. Intern Emerg Med. 2014;9(3):303–9. doi:10.​1007/​s11739-012-0867-9.CrossRefPubMed
13.
go back to reference Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney system. International workshop on the histopathology of gastritis, Houston 1994. Am J Surg Pathol. 1996;20(10):1161–81.CrossRefPubMed Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney system. International workshop on the histopathology of gastritis, Houston 1994. Am J Surg Pathol. 1996;20(10):1161–81.CrossRefPubMed
15.
go back to reference Mohammadi M, Talebkhan Y, Khalili G, Mahboudi F, Massarrat S, Zamaninia L, Oghalaei A. Advantage of using a home-made ELISA kit for detection of Helicobacter pylori infection over commercially imported kits. Indian J Med Microbiol. 2008;26(2):127–31.CrossRefPubMed Mohammadi M, Talebkhan Y, Khalili G, Mahboudi F, Massarrat S, Zamaninia L, Oghalaei A. Advantage of using a home-made ELISA kit for detection of Helicobacter pylori infection over commercially imported kits. Indian J Med Microbiol. 2008;26(2):127–31.CrossRefPubMed
16.
go back to reference Mohammadi M, Kashani SS, Garoosi YT, Tazehkand SJ. In vivo measurement of Helicobacter pylori infection. Methods in molecular biology (Clifton, NJ). 2012;921:239–56. doi:10.1007/978-1-62703-005-2_26. Mohammadi M, Kashani SS, Garoosi YT, Tazehkand SJ. In vivo measurement of Helicobacter pylori infection. Methods in molecular biology (Clifton, NJ). 2012;921:239–56. doi:10.​1007/​978-1-62703-005-2_​26.
17.
go back to reference Shin CM, Kim N, Lee HS, Lee HE, Lee SH, Park YS, Hwang JH, Kim JW, Jeong SH, Lee DH, Jung HC, Song IS. Validation of diagnostic tests for Helicobacter pylori with regard to grade of atrophic gastritis and/or intestinal metaplasia. Helicobacter. 2009;14(6):512–9. doi:10.1111/j.1523-5378.2009.00726.x.CrossRefPubMed Shin CM, Kim N, Lee HS, Lee HE, Lee SH, Park YS, Hwang JH, Kim JW, Jeong SH, Lee DH, Jung HC, Song IS. Validation of diagnostic tests for Helicobacter pylori with regard to grade of atrophic gastritis and/or intestinal metaplasia. Helicobacter. 2009;14(6):512–9. doi:10.​1111/​j.​1523-5378.​2009.​00726.​x.CrossRefPubMed
18.
19.
go back to reference Atanassov C, Pezennec L, d’Alayer J, Grollier G, Picard B, Fauchere JL. Novel antigens of Helicobacter pylori correspond to ulcer-related antibody pattern of sera from infected patients. J Clin Microbiol. 2002;40(2):547–52.CrossRefPubMedPubMedCentral Atanassov C, Pezennec L, d’Alayer J, Grollier G, Picard B, Fauchere JL. Novel antigens of Helicobacter pylori correspond to ulcer-related antibody pattern of sera from infected patients. J Clin Microbiol. 2002;40(2):547–52.CrossRefPubMedPubMedCentral
20.
Metadata
Title
Helicobacter pylori Peptidyl Prolyl Isomerase Expression Is Associated with the Severity of Gastritis
Authors
Akbar Oghalaie
Samaneh Saberi
Maryam Esmaeili
Fatemeh Ebrahimzadeh
Farzaneh Barkhordari
Abdolreza Ghamarian
Mohammad Tashakoripoor
Afshin Abdirad
Mahmoud Eshagh Hosseini
Vahid Khalaj
Marjan Mohammadi
Publication date
01-12-2016
Publisher
Springer US
Published in
Journal of Gastrointestinal Cancer / Issue 4/2016
Print ISSN: 1941-6628
Electronic ISSN: 1941-6636
DOI
https://doi.org/10.1007/s12029-016-9849-x

Other articles of this Issue 4/2016

Journal of Gastrointestinal Cancer 4/2016 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

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

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

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

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

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