{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,14]],"date-time":"2026-04-14T03:56:24Z","timestamp":1776138984531,"version":"3.50.1"},"reference-count":40,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,8,28]],"date-time":"2022-08-28T00:00:00Z","timestamp":1661644800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Taif University Researchers Supporting project","award":["TURSP.2020\/93"],"award-info":[{"award-number":["TURSP.2020\/93"]}]},{"name":"Taif University Researchers Supporting project","award":["HEC\/R&D\/NRPU-5896"],"award-info":[{"award-number":["HEC\/R&D\/NRPU-5896"]}]},{"name":"Higher Education Commission of Pakistan","award":["TURSP.2020\/93"],"award-info":[{"award-number":["TURSP.2020\/93"]}]},{"name":"Higher Education Commission of Pakistan","award":["HEC\/R&D\/NRPU-5896"],"award-info":[{"award-number":["HEC\/R&D\/NRPU-5896"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Background and Objective: Helicobacter pylori is a human-stomach-dwelling organism that causes many gastric illnesses, including gastritis, ulcer, and gastric cancer. The purpose of the study was to perform differential proteomic analysis on H. pylori isolates from gastritis, ulcer, and gastric cancer patients. Materials and Methods: H. pylori was isolated from antrum and fundus biopsies obtained from patients who visited the Department of Gastroenterology. Using nano-LC-QTOF MS\/MS analysis, differentially regulated proteins were identified through proteome profiling of pooled samples of H. pylori isolated from gastritis, ulcer, and gastric cancer patients. Antigenic scores and cellular localization of proteins were determined using additional prediction tools. Results: A total of 14 significantly regulated proteins were identified in H. pylori isolated from patients with either gastritis, ulcer, or gastric cancer. Comparative analysis of groups revealed that in the case of cancer vs. gastritis, six proteins were overexpressed, out of which two proteins, including hydrogenase maturation factor (hypA) and nucleoside diphosphate kinase (ndk) involved in bacterial colonization, were only upregulated in isolates from cancer patients. Similarly, in cancer vs. ulcer, a total of nine proteins were expressed. Sec-independent protein translocase protein (tatB), involved in protein translocation, and pseudaminic acid synthase I (pseI), involved in the synthesis of functional flagella, were upregulated in cancer, while hypA and ndk were downregulated. In ulcer vs. gastritis, eight proteins were expressed. In this group, tatB was overexpressed. A reduction in thioredoxin peroxidase (bacterioferritin co-migratory protein (bcp)) was observed in ulcer vs. gastritis and cancer vs. ulcer. Conclusion: Our study suggested three discrete protein signatures, hypA, tatB, and bcp, with differential expression in gastritis, ulcer, and cancer. Protein expression profiles of H. pylori isolated from patients with these gastric diseases will help to understand the virulence and pathogenesis of H. pylori.<\/jats:p>","DOI":"10.3390\/medicina58091168","type":"journal-article","created":{"date-parts":[[2022,8,29]],"date-time":"2022-08-29T03:34:56Z","timestamp":1661744096000},"page":"1168","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Differential Proteomics of Helicobacter pylori Isolates from Gastritis, Ulcer, and Cancer Patients: First Study from Northwest Pakistan"],"prefix":"10.3390","volume":"58","author":[{"given":"Syed Ali Raza","family":"Shah","sequence":"first","affiliation":[{"name":"Department of Microbiology, Abdul Wali Khan University, Mardan 23200, KP, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hazir","family":"Rahman","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Abdul Wali Khan University, Mardan 23200, KP, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Muhammad","family":"Qasim","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Kohat University of Science and Technology, Kohat 26000, KP, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9706-3152","authenticated-orcid":false,"given":"Muhammad Safwan","family":"Akram","sequence":"additional","affiliation":[{"name":"National Horizons Centre, Teesside University, Darlington DL11HG, UK"},{"name":"School of Health & Life Sciences, Teesside University, Middlesbrough TS1 3BX, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3293-373X","authenticated-orcid":false,"given":"Yasemin","family":"Saygideger","sequence":"additional","affiliation":[{"name":"Department of Pulmonary, Cukurova University School of Medicine, 01330 Adana, Turkey"},{"name":"Department of Translational Medicine, Institute of Health Sciences, Cukurova University, 01330 Adana, Turkey"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nanda","family":"Puspita","sequence":"additional","affiliation":[{"name":"National Horizons Centre, Teesside University, Darlington DL11HG, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5179-0522","authenticated-orcid":false,"given":"Burcu","family":"Sayg\u0131de\u011fer Demir","sequence":"additional","affiliation":[{"name":"Department of Biotechnology, Institute of Natural and Applied Sciences, Cukurova University, 01330 Adana, Turkey"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6688-0106","authenticated-orcid":false,"given":"Khalid J.","family":"Alzahrani","sequence":"additional","affiliation":[{"name":"Department of Clinical Laboratories Sciences, College of Applied Medical Sciences, Taif University, Taif 21944, Saudi Arabia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2901-7212","authenticated-orcid":false,"given":"Muhammad Fayyaz ur","family":"Rehman","sequence":"additional","affiliation":[{"name":"Institute of Chemistry, University of Sargodha, Sargodha 40100, Pakistan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6930-5214","authenticated-orcid":false,"given":"Fuad M.","family":"Alzahrani","sequence":"additional","affiliation":[{"name":"Department of Clinical Laboratories Sciences, College of Applied Medical Sciences, Taif University, Taif 21944, Saudi Arabia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3536-9276","authenticated-orcid":false,"given":"Mohamed A.","family":"Alblihd","sequence":"additional","affiliation":[{"name":"Department of Medical Microbiology, College of Medicine, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1053\/j.gastro.2017.04.022","article-title":"Systematic Review and Meta-Analysis","volume":"153","author":"Hooi","year":"2017","journal-title":"Gastroenterology"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1097\/MCG.0b013e31820fb8f6","article-title":"World Gastroenterology Organisation Global Guideline Helicobacter pylori in Developing Countries","volume":"45","author":"Hunt","year":"2011","journal-title":"J. Clin. Gastroenterol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e12403","DOI":"10.1111\/hel.12403","article-title":"Epidemiology of Helicobacter pylori infection","volume":"22","author":"Burucoa","year":"2017","journal-title":"Helicobacter"},{"key":"ref_4","first-page":"299","article-title":"Helicobacter pylori in developing countries. World gastroenterology organisation global guideline","volume":"20","author":"Hunt","year":"2011","journal-title":"J. Gastrointest. Liver Dis. JGLD"},{"key":"ref_5","first-page":"233","article-title":"Helicobacter infection and gastric neoplasia","volume":"208","author":"Peek","year":"2006","journal-title":"J. Pathol. A J. Pathol. Soc. Great Br. Irel."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1097\/00001432-200310000-00011","article-title":"Helicobacter\u00a0pylori","volume":"16","author":"Moss","year":"2003","journal-title":"Curr. Opin. Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.tim.2016.12.004","article-title":"Helicobacter pylori: A paradigm pathogen for subverting host cell signal transmission","volume":"25","author":"Naumann","year":"2017","journal-title":"Trends Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"984","DOI":"10.1016\/j.cmi.2015.06.004","article-title":"Helicobacter pylori infection and gastric carcinoma","volume":"21","author":"Varon","year":"2015","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"400","DOI":"10.4291\/wjgp.v5.i4.400","article-title":"Helicobacter pylori and neurological diseases: Married by the laws of inflammation","volume":"5","year":"2014","journal-title":"World J. Gastrointest. Pathophysiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1510","DOI":"10.3748\/wjg.v20.i6.1510","article-title":"Helicobacter pylori and skin autoimmune diseases","volume":"20","author":"Magen","year":"2014","journal-title":"World J. Gastroenterol. WJG"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Zhou, J., Wang, W., Xie, Y., Zhao, Y., Chen, X., Xu, W., Wang, Y., and Guan, Z. (2016). Proteomics-based identification and analysis of proteins associated with Helicobacter pylori in gastric cancer. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0146521"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.canlet.2010.07.014","article-title":"Helicobacter pylori in the pathogenesis of gastric cancer and gastric lymphoma","volume":"305","author":"Kim","year":"2011","journal-title":"Cancer Lett."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.1158\/1055-9965.EPI-05-0901","article-title":"Effect of Helicobacter pylori infection combined with CagA and pepsinogen status on gastric cancer development among Japanese men and women: A nested case-control study","volume":"15","author":"Sasazuki","year":"2006","journal-title":"Cancer Epidemiol. Prev. Biomark."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Ghalia, K., Jibran, S., Muhammad, I.M., Sameh, S., Soliman, M., and Christophe, B. (2019). Prevalence of Helicobacter pylori and Its Associated Factors among Healthy Asymptomatic Residents in the United Arab Emirates. Pathogens, 8.","DOI":"10.3390\/pathogens8020044"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1007\/s00431-007-0552-6","article-title":"Helicobacter pylori infection: Effect on malnutrition and growth failure in dyspeptic children","volume":"167","author":"Soylu","year":"2008","journal-title":"Eur. J. Pediatr."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1328","DOI":"10.1126\/science.284.5418.1328","article-title":"Helicobacter pylori virulence and genetic geography","volume":"284","author":"Covacci","year":"1999","journal-title":"Science"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1016\/S0016-5085(99)70065-X","article-title":"Geographic distribution of vacA allelic types of Helicobacter pylori","volume":"116","author":"Figueiredo","year":"1999","journal-title":"Gastroenterology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1038\/nature18270","article-title":"Defining the consequences of genetic variation on a proteome-wide scale","volume":"534","author":"Joel","year":"2016","journal-title":"Nature"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1720","DOI":"10.1128\/MCB.19.3.1720","article-title":"Correlation between Protein and mRNA Abundance in Yeast","volume":"19","author":"Steven","year":"1999","journal-title":"Mol. Cell Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1186\/s13027-017-0133-x","article-title":"Protein signature characterizing Helicobacter pylori strains of patients with autoimmune atrophic gastritis, duodenal ulcer and gastric cancer","volume":"12","author":"Valli","year":"2017","journal-title":"Infect. Agents Cancer"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1817","DOI":"10.1111\/jam.12187","article-title":"Proteome variability among Helicobacter pylori isolates clustered according to genomic methylation","volume":"114","author":"Vitoriano","year":"2013","journal-title":"J. Appl. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1111\/j.1523-5378.2011.00825.x","article-title":"Antigenic diversity among Portuguese clinical isolates of Helicobacter pylori","volume":"16","author":"Vitoriano","year":"2011","journal-title":"Helicobacter"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1016\/j.tim.2003.10.004","article-title":"Sweet new world: Glycoproteins in bacterial pathogens","volume":"11","author":"Schmidt","year":"2003","journal-title":"Trends Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1046\/j.1365-2958.2003.03725.x","article-title":"Pseudaminic acid, the major modification on Campylobacter flagellin, is synthesized via the Cj1293 gene","volume":"50","author":"Goon","year":"2003","journal-title":"Mol. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"7086","DOI":"10.1128\/JB.00378-09","article-title":"Functional characterization of flagellin glycosylation in Campylobacter jejuni 81-176","volume":"191","author":"Ewing","year":"2009","journal-title":"J. Bacteriol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1249","DOI":"10.1099\/mic.0.28735-0","article-title":"Flagellar glycosylation\u2014A new component of the motility repertoire?","volume":"152","author":"Logan","year":"2006","journal-title":"Microbiology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"338352","DOI":"10.1016\/j.aca.2021.338352","article-title":"Tailor-made recombinant prokaryotic lectins for characterisation of glycoproteins","volume":"1155","author":"Padros","year":"2021","journal-title":"Anal. Chim. Acta"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"29893","DOI":"10.1021\/acsomega.1c04382","article-title":"Probing Transferrin Receptor Overexpression in Gastric Cancer Mice Models","volume":"6","author":"Lodhi","year":"2021","journal-title":"ACS Omega"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Hopf, P.S., Ford, R.S., Zebian, N., Merkx-Jacques, A., Vijayakumar, S., Ratnayake, D., Hayworth, J., and Creuzenet, C. (2011). Protein glycosylation in Helicobacter pylori: Beyond the flagellins?. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0025722"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1579","DOI":"10.1046\/j.1365-2958.2003.03527.x","article-title":"Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori","volume":"48","author":"Schirm","year":"2003","journal-title":"Mol. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1120","DOI":"10.1046\/j.1365-2958.2000.01780.x","article-title":"Multiple N-acetyl neuraminic acid synthetase (neuB) genes in Campylobacter jejuni: Identification and characterization of the gene involved in sialylation of lipo-oligosaccharide","volume":"35","author":"Linton","year":"2000","journal-title":"Mol. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2924","DOI":"10.1074\/jbc.275.4.2924","article-title":"Thioredoxin-dependent hydroperoxide peroxidase activity of bacterioferritin comigratory protein (BCP) as a new member of the thiol-specific antioxidant protein (TSA)\/alkyl hydroperoxide peroxidase C (AhpC) family","volume":"275","author":"Jeong","year":"2000","journal-title":"J. Biol. Chem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1146\/annurev-anchem-071213-020143","article-title":"Engineered proteins for bioelectrochemistry","volume":"7","author":"Akram","year":"2014","journal-title":"Annu. Rev. Anal. Chem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1099\/mic.0.25896-0","article-title":"Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori","volume":"149","author":"Comtois","year":"2003","journal-title":"Microbiology"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/j.molbiopara.2007.12.010","article-title":"Leishmania-released nucleoside diphosphate kinase prevents ATP-mediated cytolysis of macrophages","volume":"158","author":"Kolli","year":"2008","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3024","DOI":"10.1099\/mic.0.049221-0","article-title":"Secretory nucleoside diphosphate kinase from both the intra-and extra-cellular pathogenic bacteria are functionally indistinguishable","volume":"157","author":"Prasad","year":"2011","journal-title":"Microbiology"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"334","DOI":"10.3390\/ijms12010334","article-title":"The role of reactive-oxygen-species in microbial persistence and inflammation","volume":"12","author":"Spooner","year":"2011","journal-title":"Int. J. Mol. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"851","DOI":"10.2217\/fon.10.37","article-title":"Helicobacter pylori infection, oncogenic pathways and epigenetic mechanisms in gastric carcinogenesis","volume":"6","author":"Ding","year":"2010","journal-title":"Futur. Oncol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1452","DOI":"10.1126\/science.1113752","article-title":"Protein translocation across biological membranes","volume":"310","author":"Wickner","year":"2005","journal-title":"Science"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1080\/09687860500063308","article-title":"Sec-dependent protein translocation across biological membranes: Evolutionary conservation of an essential protein transport pathway","volume":"22","author":"Stephenson","year":"2005","journal-title":"Mol. Membr. Biol."}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/58\/9\/1168\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:18:59Z","timestamp":1760141939000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/58\/9\/1168"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,28]]},"references-count":40,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["medicina58091168"],"URL":"https:\/\/doi.org\/10.3390\/medicina58091168","relation":{},"ISSN":["1648-9144"],"issn-type":[{"value":"1648-9144","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,28]]}}}