MECHANISMS OF INTERRACTION OF HELICOBACTER PYLORI WITH EPITHELIUM OF GASTRIC MUCOSA. I. PATHOGENIC FACTORS PROMOTING SUCCESSFUL COLONIZATION
- Authors: Pozdeev О.К.1, Pozdeeva А.О.1, Valeeva Y.V.2, Gulyaev P.E.3
-
Affiliations:
- Kazan State Medical Academy — Branch Campus of the Russian Medical Academy of Continuous Professional Education.
- Kazan (Volga region) Federal University.
- Kazan State Medical University.
- Issue: Vol 8, No 3 (2018)
- Pages: 273-283
- Section: REVIEWS
- Submitted: 01.11.2018
- Accepted: 01.11.2018
- Published: 01.11.2018
- URL: https://iimmun.ru/iimm/article/view/777
- DOI: https://doi.org/10.15789/2220-7619-2018-3-273-283
- ID: 777
Cite item
Full Text
Abstract
H. pylori is a Gram-negative, crimp and motile bacterium that colonizes the hostile microniche of the human stomach roughly one half of the human population. Then persists for the host’s entire life, but only causes overt gastric disease in a subset of infected hosts. To the reasons contributing to the development of diseases, usually include: concomitant infections of the gastrointestinal tract, improper sterilization of medical instruments, usually endoscopes, nonobservance of personal hygiene rules, prolonged contact with infected or carriers, including family members and a number of other factors. Clinically, H. pylori plays a causative role in the development of a wide spectrum of diseases including chronic active gastritis, peptic and duodenal ulceration, gastric adenocarcinoma, and gastric mucosa-associated lymphoid tissue lymphoma. Due to the global distribution of H. pylori, we are able to conclude that smart strategies are contributing to adaptation of the bacterium in an aggressive environment of a stomach and lifelong permanent circulation in its host. Thirty-four years after the discovery of this bacterium, there are still many unanswered questions. For example, which strategies help the bacterium to survive in this inhospitable conditions? Understanding the mechanisms governing H. pylori persistence will improve identification of the increased risk of different gastric diseases in persons infected with this bacterium. A well-defined and long-term equilibrium between the human host and H. pylori allows bacterial persistence in the gastric microniche; although this coexistence leads to a high risk of severe diseases the diseases which are listed above. In this review, we discuss the pathogenesis of this bacterium and the mechanisms it uses to promote persistent colonization of the gastric mucosa, with a focus on recent insights into the role of some virulence factors like urease, LPS, outer membrane proteins, cytotoxins, factors, promoting invasion. Information on the mechanisms related to H. pylori persistence can also provide the direction for future research concerning effective therapy and management of gastroduodenal disorders. The topics presented in the current review are important for elucidating the strategies used by H. pylori to help the bacterium persist in relation to the many unfavorable features of living in the gastric microniche.
About the authors
О. К. Pozdeev
Kazan State Medical Academy — Branch Campus of the Russian Medical Academy of Continuous Professional Education.
Author for correspondence.
Email: pozdeevoskar@rambler.ru
PhD, MD (Medicine), Professor, Head of the Department of Microbiology.
420012, Russian Federation, Kazan, Butlerova str., 36.
Phone: +7 919 693-02-04 (mobile).
РоссияА. О. Pozdeeva
Kazan State Medical Academy — Branch Campus of the Russian Medical Academy of Continuous Professional Education.
Email: fake@neicon.ru
Assistant of the Department of Therapy and Family Medicine.
Kazan. РоссияYu. V. Valeeva
Kazan (Volga region) Federal University.
Email: fake@neicon.ru
PhD (Medicine), Associate Professor, Department Emergency Medical Care and Simulatory Medicine.
Kazan. РоссияP. E. Gulyaev
Kazan State Medical University.
Email: fake@neicon.ru
Assistant of the Department of Microbiology.
Kazan.
РоссияReferences
- Amedei A., Cappon A., Codolo G., Cabrelle A., Polenghi A., Benagiano M., Tasca E., Azzurri A., D’Elios M.M., Del Prete G., de Bernard M. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J. Clin. Invest., 2006, vol. 116, no. 4, pp. 1092–1101. doi: 10.1172/JCI27177
- Aspholm M., Olfat F.O., Norden J., Sonden 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., Boren T. SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog., 2006, vol. 2, no. 10, pp. 110. doi: 10.1371/journal.ppat.0020110
- Atuma C., Strugala V., Allen A., Holm L. The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am. J. Physiol. Gastrointest. Liver Physiol., 2001, vol. 280, no. 5, pp. 922–929. doi: 10.1152/ajpgi.2001.280.5.G922
- Backert S., Clyne M., Tegtmeyer N. Molecular mechanisms of gastric epithelial cell adhesion and injection of CagA by Helicobacter pylori. Cell Commun. Signal., 2011, vol. 9, pp. 28. doi: 10.1186/1478-811X-9-28
- Blaser M.J., Atherton J.C. Helicobacter pylori persistence: biology and disease. J. Clin. Invest., 2004, vol. 113, no. 3, pp. 321–333. doi: 10.1172/JCI20925
- Carlsohn E., Nystrom J., Bolin I., Nilsson C.L., Svennerholm A.M. HpaA is essential for Helicobacter pylori colonization in mice. Infect. Immun., 2006, vol. 74, no 2, pp. 920–926. doi: 10.1128/IAI.74.2.920-926.2006
- Celli J.P., Turner B.S., Afdhal N.H., Keates S., Ghiran I. Kelly C.P., Ewoldt R.H., McKinley G.H., So P., Erramilli S., Bansil R. Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. Proc. Natl. Acad. Sci. USA, 2009, vol. 106, no. 34, pp. 14321–14326. doi: 10.1073/pnas.0903438106
- Celli J.P., Turner B.S., Afdhal, N.H., Ewoldt R.H., McKinley G.H., Bansil R., Erramilli S. Rheology of gastric mucin exhibits a pH-dependent sol-gel transition. Biomacromolecules, 2007, vol. 8, no. 5, pp. 1580–1586. doi: 10.1021/bm0609691
- Chevalier C., Thiberge J.M., Ferrero R.L., Labigne A. Essential role of Helicobacter pylori gamma-glutamyltranspeptidase for the colonization of the gastric mucosa of mice. Mol. Microbiol., 1999, vol. 31, no. 5, pp. 1359–1372. doi: 10.1046/j.1365-2958.1999.01271.x
- Cover T.L. Role of Helicobacter pylori CagL in modulating gastrin expression. Gut, 2012, vol. 61, no. 7, pp. 965–966. doi: 10.1136/gutjnl-2012-302142
- Cover T.L., Blanke S.R. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat. Rev. Microbiol., 2005, vol. 3, no. 4, pp. 320–332. doi: 10.1038/nrmicro1095
- Crampton J.R. Gastroduodenal mucus and bicarbonate – the defensive zone. Quart. J. Med., 1988, vol. 67, no. 252, pp. 269–272.
- De Bernard M., D’Elios M.M. The immune modulating activity of the Helicobacter pylori HP-NAP: Friend or foe? Toxicon, 2010, vol. 56, no. 7, pp. 1186–1192. doi: 10.1016/j.toxicon.2009.09.020
- De Jonge R., Durrani Z., Rijpkema S.G., Kuipers E.J., Van Vliet A.H.M., Kusters J.G. Role of the Helicobacter pylori outermembrane proteins AlpA and AlpB in colonization of the guinea pig stomach. J. Med. Microbiol., 2004, vol. 53, no 5, pp. 375–379. doi: 10.1099/jmm.0.45551-0
- Doig P., Austin J.W., Trust T.J. The Helicobacter pylori 19.6-kilodalton protein is an iron-containing protein resembling ferritin. J. Bacteriol., 1993, vol. 175, no. 2, pp. 557–560.
- El-Omar E.M., Carrington M., Chow W.H., McColl K.E.L., Bream J.H., Young H.A., Herrera J., Lissowska J., Yuan C.C., Rothman N., Lanyon G., Martin M., Fraumeni J.F., Rabkin C.S. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature, 2000, vol. 404, no. 6776, pp. 398–402. doi: 10.1038/35006081
- Evans D.J., Evans D.G., Takemura T., Nakano H. Lampert H.C., Graham D.Y., Granger D.N., Kvietys P.R. Characterization of a Helicobacter pylori neutrophil-activating protein. Infect. Immun., 1995, vol. 63, no. 6, pp. 2213–2220.
- Fanchi L., Park J.H., Shaw, M.H., Marina-Garcia N., Chen G., Kim Y.G., Nunez G. Intracellular NOD-like receptors in innate immunity, infection and disease. Cell. Microbiol., 2008, vol. 10, no. 1, pp. 1–8. doi: 10.1111/j.1462-5822.2007.01059.x
- Figura N., Vindigni C., Presenti L., Carducci A. New acquisitions in Helicobacter pylori characteristics. Ital. J. Gastroenterol. Hepatol., 1998, vol. 30, suppl. 3, pp. S254–S258.
- Flahou B., Haesebrouck F., Chiers K.,Van Deun K., De Smet L., Devreese B., Vandenberghe I., Favoreel H., Smet A., Pasmans F., D’Herde K., Ducatelle R. Gastric epithelial cell death caused by Helicobacter suis and Helicobacter pylori γ-glutamyl transpeptidase is mainly glutathione degradation-dependent. Cell. Microbiol., 2011, vol. 13, no. 12, pp. 1933–1955. doi: 10.1111/j.1462-5822.2011.01682.x
- Garcia-Gonzalez M.A., Lanas A., Santolaria S., Crusius J.B.A., Serrano M.T., Pena A.S. The polymorphic IL-1/3 and IL-1RN genes in the aetiopathogenesis of peptic ulcer. Clin. Exp. Immunol., 2001, vol. 125, no. 3, pp. 368–375. doi: 10.1046/j.1365-2249.2001.01593.x
- Garcia-Gonzalez M.A., Lanas A., Savelkoul P.H.M., Santolaria S., Benito R., Crusius J.B.A., Pena. A.S. Association of interleukin 1 gene family polymorphisms with duodenal ulcer disease. Clin. Exp. Immunol., 2003, vol. 134, no. 3, pp. 525–531. doi: 10.1046/j.1365-2249.2003.02325.x
- Garner J.A., Cover T.L. Binding and internalization of the Helicobacter pylori vacuolating cytotoxin by epithelial cells. Infect. Immun., 1996, vol. 64, no. 10, pp. 4197–4203.
- Garrington T.P., Johnson G.L. Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr. Opin. Cell. Biol., 1999, vol. 11, no. 2, pp. 211–218. doi: 10.1016/S0955-0674(99)80028-3
- Giannakis M., Bäckhed H.K., Chen S.L., Faith J.J., Wu M., Guruge J.L., Engstrand L., Gordon J.I. Response of gastric epithelial progenitors to Helicobacter pylori Isolates obtained from Swedish patients with chronic atrophic gastritis. J. Biol. Chem., 2009, vol. 284, no. 44, pp. 30383–30394. doi: 10.1074/jbc.M109.052738
- Gong M., Ling S.S., Lui S.Y., Yeoh K.G., Ho B. Helicobacter pylori gamma-glutamyl transpeptidase is a pathogenic factor in the development of peptic ulcer disease. Gastroenterology, 2010, vol. 139, no. 2, pp. 564–573. doi: 10.1053/j.gastro.2010.03.050
- Gumbiner B.M. Regulation of cadherin adhesive activity. J. Cell. Biol., 2000, vol. 148, no. 3, pp. 399–404. doi: 10.1083/jcb.148.3.399
- Hessey S.J., Spencer J., Wyatt J.I., Sobala G., Rathbone B.J., Axon Atr., Dixon M.F. Bacterial adhesion and disease activity in Helicobacter associated chronic gastritis. Gut, 1990, vol. 31, no. 2, pp. 134–138. doi: 10.1136/gut.31.2.134
- Hoy B., Löwer M., Weydig C.,Carra G., Tegtmeyer N., Geppert T., Schröder P., Sewald N., Backert S., Schneider G., Wessler S. Helicobacter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion. EMBO Rep., 2010, vol. 11, no. 10, pp. 798–804. doi: 10.1038/embor.2010.114
- Ikenoue T., Maeda S., Ogura K., Akanuma M., Mitsuno Y., Imai Y., Yoshida H., Shiratori Y., Omata M. Determination of Helicobacter pylori virulence by simple gene analysis of the cag pathogenicity island. Clin. Diagn. Lab. Imm., 2001, vol. 8, no. 1, pp. 181–186. doi: 10.1128/CDLI.8.1.181-186.2001
- Ilver D., Arnqvist A., Ogren J., Frick I.M., Kersulyte D., Incecik E.T., Berg D.E., Covacci A., Engstrand L., Boren T. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science, 1998, vol. 279, no. 5349, pp. 373–377. doi: 10.1126/science.279.5349.373
- Ishijima N., Suzuki M., Ashida H., Ichikawa Y., Kanegae Y., Saito I., Borén T., Haas R., Sasakawa C., Mimuro H. BabAmediated adherence is a potentiator of the Helicobacter pylori type IV secretion system activity. J. Biol. Chem., 2011, vol. 286, no. 28, pp. 25256–25264. doi: 10.1074/jbc.M111.233601
- Iwamoto H., Czajkowsky D.M., Cover T.L., Szabo G., Shao Z. VacA from Helicobacter pylori: a hexameric chloride channel. FEBS Lett., 1999, vol. 450, no. 1–2, pp. 101–104. doi: 10.1016/S0014-5793(99)00474-3
- Jiménez-Soto L.F., Kutter S., Sewald X., Ertl C., Weiss E., Kapp U., Rohde M., Pirch T., Jung K., Retta S.F., Terradot L., Fischer W., Haas R. Helicobacter pylori type IV secretion apparatus exploits beta 1 integrin in a novel RGD-independent manner. PLoS Pathog., 2009, vol. 5, no. 12, pp. e1000684. doi: 10.1371/journal.ppat.1000684
- Joo J.S., Park K.C., Song J.Y., Kim D.H., Lee K.J., Kwon Y.C., Kim J.M., Kim K.M., Youn H.S., Kang H.L., Baik S.C., Lee W.K., Cho M.J., Rhee K.H. A thin-layer liquid culture technique for the growth o fHelicobacter pylori. Helicobacter, 2010, vol. 15, no. 4, pp. 295–302. doi: 10.1111/j.1523-5378.2010.00767.x
- Karim Q.N., Logan R.P., Puels J., Karnholz A., Worku M.L. Measurement of motility of Helicobacter pylori, Campylobacter jejuni, and Escherichia coli by real time computer tracking using the Hobson BacTracker. J. Clin. Pathol., 1998, vol. 51, no. 8, pp. 623–628. doi: 10.1136/jcp.51.8.623
- Kudo T., Lu H., Wu J.Y., Ohno T., Wu M.J., Genta R.M., Graham D.Y., Yamaoka Y. Pattern of transcription factor activation in Helicobacter pylori-infected Mongolian gerbils. Gastroenterology, 2007, vol. 132, no. 3, pp. 1024–1038. doi: 10.1053/j.gastro.2007.01.009
- Kwok T., Zabler D., Urman S., Rohde M., Hartig R., Wessler S., Misselwitz R., Berger J., Sewald N., König W., Backert S. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature, 2007, vol. 449, no. 7164, pp. 862–866. doi: 10.1038/nature06187
- Lichtenberger L.M. The hydrophobic barrier properties of gastrointestinal mucus. Annu. Rev. Physiol., 1995, vol 57, pp. 565–583. doi: 10.1146/annurev.ph.57.030195.003025
- Löwer M., Weydig C., Metzler D., Reuter A., Starzinski-Powitz A., Wessler S., Schneider G. Prediction of extracellular proteases of the human pathogen Helicobacter pylori reveals proteolytic activity of the Hp1018/19 protein HtrA. PLoS One, 2008, vol. 3, no. 10, pp. e3510. doi: 10.1371/journal.pone.0003510
- Lu H., Wu J.Y., Beswick E.J., Ohno T., Odenbreit S., Haas R., Reyes V.E., Kita M., Graham D.Y., Yamaoka Y. Functional and intracellular signaling differences associated with the Helicobacter pylori AlpAB adhesin from Western and East Asian strains. J. Biol. Chem., 2007, vol. 282, no. 9, pp. 6242–6254. doi: 10.1074/jbc.M611178200
- Lu H., Wu J.Y., Kudo T., Ohno T., Graham D.Y., Yamaoka Y. Regulation of interleukin-6 promoter activation in gastric epithelial cells infected with Helicobacter pylori. Mol. Biol. Cell, 2005, vol. 16, no. 10, pp. 4954–4966. doi: 10.1091/mbc.E05-05-0426
- Machado J.C., Figueiredo C., Canedo P., Nabais S., Doorn L.J.V., Caldas C., Seruca R., Carneiro F., Sobrinho-Simões M. A proinflammatory genetic profile increases the risk for chronic atrophic gastritis and gastric сarcinoma. Gastroenterology, 2003, vol. 125, no. 2, pp. 364–371.
- Mahdavi J., Sondén B., Hurtig M., Olfat F.O., Forsberg L., Roche N., Angstrom J., Larsson T., Teneberg S., Karlsson K.A., Altraja S., Wadström T., Kersulyte D., Berg D.E., Dubois A., Petersson C., Magnusson K.E., Norberg T., Lindh F., Lundskog B.B., Arnqvist A., Hammarström L., Borén T. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science, 2002, vol. 297, no. 5581, pp. 573–578. doi: 10.1126/science.1069076
- Marshall B.J., Langton S.R. Urea hydrolysis in patients with Campylobacter pyloridis infection. Lancet, 1986, vol. 1, no. 8487, pp. 965–966. doi: http://dx.doi.org/10.1016/S0140-6736(86)91060-3
- McClain M.S., Iwamoto H., Cao P., Vinion-Dubiel A.D., Li Y., Szabo G., Shao Z., Cover T.L. Essential role of a GXXXG motif for membrane channel formation by Helicobacter pylori vacuolating toxin. J. Biol. Chem., 2003, vol. 278, no. 14, pp. 12101–12108. doi: 10.1074/jbc.M212595200
- McClain M.S., Schraw W., Ricci V., Boquet P., Cover T.L. Acid activation of Helicobacter pylori vacuolating cytotoxin (VacA) results in toxin internalization by eukaryotic cells. Mol. Microbiol., 2000, vol. 37, no. 2, pp. 433–442. doi: 10.1046/j.1365-2958.2000.02013.x
- Merrell D.S., Goodrich M.L., Otto G., Tompkins L.S., Falkow S. pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect. Immun., 2003, vol. 71, no. 6, pp. 3529–3539. doi: 10.1128/IAI.71.6.3529-3539.2003
- Monteiro M.A., St Michael F., Rasko D.A., Taylor D.E., Conlan J.W., Chan K.H., Logan S.M., Appelmelk B.J., Perry M.B. Helicobacter pylori from asymptomatic hosts expressing heptoglycan but lacking Lewis O-chains: Lewis blood-group O-chains may play a role in Helicobacter pylori induced pathology. Biochem. Cell. Biol., 2001, vol. 79. no. 4, pp. 449–459. doi: 10.1139/bcb-79-4-449
- Monteiro M.A., Zheng P., Ho B., Yokota S., Amano K., Pan Z., Berg D.E., Chan K.H., MacLean L.L., Perry M.B. Expression of histo-blood group antigens by lipopolysaccharides of Helicobacter pylori strains from asian hosts: the propensity to express type 1 blood-group antigens. Glycobiology, 2000, vol. 10, no. 7, pp. 701–713. doi: 10.1093/glycob/10.7.701
- Moran A.P. Pathogenic properties of Helicobacter pylori – In response. Scand. J. Gastroenterol., 1997, vol. 32, no. 4, pp. 399–400.
- Moran A.P. Relevance of fucosylation and Lewis antigen expression in the bacterial gastroduodenal pathogen Helicobacter pylori. Carbohydr. Res., 2008, vol. 343, no. 12, pp. 1952–1965. doi: 10.1016/j.carres.2007.12.012
- Noach L.A., Rolf T.M., Tytgat G.N. Electron microscopic study of association between Helicobacter pylori and gastric and duodenal mucosa. J. Clin. Pathol., 1994, vol. 47, no.8, pp. 699–704. doi: 10.1136/jcp.47.8.699
- Odenbreit S. Adherence properties of Helicobacter pylori: impact on pathogenesis and adaptation to the host. Int. J. Med. Microbiol., 2005, vol. 295, no. 5, pp. 317–324. doi: 10.1016/j.ijmm.2005.06.003
- Odenbreit S., Püls J., Sedlmaier B., Gerland E., Fischer W., Haas R. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science, 2000, vol. 287, no. 5457, pp. 1497–1500. doi: 10.1126/science.287.5457.1497
- 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, vol. 31, no. 5, pp. 1537–1548. doi: 10.1046/j.1365-2958.1999.01300.x
- Olofsson A., Vallström A., Petzold K., Tegtmeyer N., Schleucher J., Carlsson S., Haas R., Backert S., Wai S.N., Gröbner G., Arnqvist A. Biochemical and functional characterization of Helicobacter pylori vesicles. Mol. Microbiol., 2010, vol. 77, no. 6, pp. 1539–1555. doi: 10.1111/j.1365-2958.2010.07307.x
- Pai R., Cover T.L., Tarnawski A.S. Helicobacter pylori vacuolating cytotoxin (VacA) disorganizes the cytoskeletal architecture of gastric epithelial cells. Biochem. Biophys. Res. Commun., 1999, vol. 262, no. 1, pp. 245–250. doi: 10.1006/bbrc.1999.1194
- Pai R., Sasaki E., Tarnawski A.S. Helicobacter pylori vacuolating cytotoxin (VacA) alters cytoskeleton-associated proteins and interferes with re-epithelialization of wounded gastric epithelial monolayers. Cell. Biol. Int., 2000, vol. 24, no. 5, pp. 291–301. doi: 10.1006/cbir.2000.0510
- Pallen M.J., Wren B.W. The HtrA famy of serine proteases. Mol. Microbiol., 1997, vol. 26, no. 2, pp. 209–221.
- Papini E., Satin B., Norais N., de Bernard M., Telford J.L., Rappuoli R., Montecucco C. Selective increase of the permeability of polarized epithelial cell monolayers by Helicobacter pylori vacuolating toxin. J. Clin. Invest., 1998, vol. 102, no. 4, pp. 813–820. doi: 10.1172/JCI2764
- Park J., Song J.Y., Kwon Y.C., Chung M.J., Jun J.S., Park J.W., Park S.G., Hwang H.R., Choi S.H., Baik S.C., Kang H.L., Youn H.S., Lee W.K., Cho M.J., Rhee K.H. Effect of the urease accessory genes on activation of the Helicobacter pylori urease apoprotein. Mol. Cells, 2005, vol. 20, no. 3, pp. 371–377.
- Peck B., Ortkamp M., Diehl K.D., Hundt E., Knapp B. Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. Nucl. Acids Res., 1999, vol. 27, no. 16, pp. 3325–3333. doi: 10.1093/nar/27.16.3325
- Peek R.M. Jr, Crabtree J.E. Helicobacter infection and gastric neoplasia. Pathol., 2006, vol. 208, no. 2, pp. 233–248. doi: 10.1002/path.1868
- Pflock M., Kennard S., Finsterer N., Beier D. Acid-responsive gene regulation in the human pathogen Helicobacter pylori. J. Biotechnol., 2006, vol. 126, no. 1, pp. 52–60. doi: 10.1016/j.jbiotec.2006.03.045
- Phadais S.H., Ilver D., Janzon L., Normark S., Westblom T.U. Pathological significance and molecular characterization of the vacuolating toxin gene of Helicobacter pylori. Infect. Immun., 1994, vol. 62, no. 5, pp. 1557–1565.
- Pohl M.A., Romero-Gallo J., Guruge J.L., Tse D.B., Gordon J.I., Blaser M.J. Host-dependent Lewis (Le) antigen expression in Helicobacter pylori cells recovered from Leb-transgenic mice. J. Exp. Med., 2009, vol. 206, no. 13, pp. 3061–3072. doi: 10.1084/jem.20090683
- Poppe M., Feller S.M., Römer G., Wessler S. Phosphorylation of Helicobacter pylori CagA by c-Abl leads to cell motility. Oncogene, 2007, vol. 26, no. 24, pp. 3462–3472. doi: 10.1038/sj.onc.1210139
- Rad R., Dossumbekova A., Neu B., Lang R., Bauer S., Saur D., Gerhard M., Prinz C. Cytokine gene polymorphisms influence mucosal cytokine expression, gastric inflammation, and host specific colonization during Helicobacter pylori infection. Gut, 2004, vol. 53, no. 8, pp. 1082–1089. doi: 10.1136/gut.2003.029736
- Reyrat J.M., Lanzavecchia S., Lupetti P., de Bernard M., Pagliaccia C., Pelicic V., Charrel M., Ulivieri C., Norais N., Ji X., Cabiaux V., Papini E., Rappuoli R., Telford J.L. 3D imaging of the 58 kDa cell binding subunit of the Helicobacter pylori cytotoxin. J. Mol. Biol., 1999, vol. 290, no. 2, pp. 459–470. doi: 10.1006/jmbi.1999.2877
- Ricci V., Ciacci C., Zarrilli R., Sommi P., Tummuru M.K., Del Vecchio Blanco C., Bruni C.B., Cover T.L., Blaser M.J., Romano M. Effect of Helicobacter pylori on gastric epithelial cell migration and proliferation in vitro: role of VacA and CagA. Infect. Immun., 1996, vol. 64, no. 7, pp. 2829–2833.
- Ricci V., Sommi P., Fiocca R., Romano M., Solcia E., Ventura U. Helicobacter pylori vacuolating toxin accumulates within the endosomal-vacuolar compartment of cultured gastric cells and potentiates the vacuolating activity of ammonia. J. Pathol., 1997, vol. 183, no. 4, pp. 453–459.
- Ricci V., Sommi P., Romano M. The vacuolating toxin of Helicobacter pylori: a few answers, many questions. Digest. Liver Dis., 2000, vol. 32, suppl. 3, pp. S178–S181.
- Schmitt W., Haas R. Genetic analysis of the Helicobacter pylori vacuolating cytotoxin: structural similarities with the IgA protease type of exported protein. Mol. Microbiol., 1994, vol. 12, no. 2, pp. 307–319. doi: 10.1111/j.1365-2958.1994.tb01019.x
- Senkovich O.A., Yin J., Ekshyyan V., Conant C., Traylor J., Adegboyega P., McGee D.J., Rhoads R.E., Slepenkov S., Testerman T.L. Helicobacter pylori AlpA and AlpB bind host laminin and influence gastric inflammation in gerbils. Infect. Immun., 2011, vol. 79, no. 8, pp. 3106–3116. doi: 10.1128/IAI.01275-10
- Sewald X., Fischer W., Haas R. Sticky socks: Helicobacter pylori VacA takes shape. Trends Microbiol., 2008, vol. 16, no. 3, pp. 89–92. doi: 10.1016/j.tim.2008.01.001
- Shaffer C.L., Gaddy J.A., Loh J.T., Johnson E.M., Hill S., Hennig E.E., Mc Clain M.S., Mc Donald W.H., Cover T.L. Helicobacter pylori exploits a unique repertoire of type IV secretion system components for pilus assembly at the bacteria-host cell interface. PLoS Pathog., 2011, vol. 7, no. 9, pp. e1002237. doi: 10.1371/journal.ppat.1002237
- Sharma S.A., Tummuru M.K., Blaser M.J., Kerr L.D. Activation of IL-8 gene expression by Helicobacter pylori is regulated by transcription factor nuclear factor-kappa B in gastric epithelial cells. J. Immunol., 1998, vol. 160, no. 5, pp. 2401–2407.
- Simoons-Smit I.M., Appelmelk B.J., Verboom T., Negrini R., Penner J.L., Aspinall G.O., Moran A.P., Fei S.F., Shi B.S., Rudnica W., Savio A., de Graaff J. Typing of Helicobacter pylori with monoclonal antibodies against Lewis antigens in lipopolysaccharide. J. Clin. Microbiol., 1996, vol. 34, no. 9, pp. 2196–2200.
- Smith J.L. The physiological role of ferritin-like compounds in bacteria. Crit. Rev. Microbiol., 2004, vol. 30, no. 3, pp. 173–185. doi: 10.1080/10408410490435151
- Sommi P., Ricci V., Fiocca R., Necchi V., Romano M., Telford J.L., Solcia E., Ventura U. Persistence of Helicobacter pylori VacA toxin and vacuolating potential in cultured gastric epithelial cells. Am. J. Physiol., 1998, vol. 275, no. 4, pp. 681–688.
- Stein M., Bagnoli F., Halenbeck R., Rappuoli R., Fantl W.J., Covacci A. c-Src/Lyn kinases activate Helicobacter pylori CagA through tyrosine phosphorylation of the EPIYA motifs. Mol. Microbiol., 2002, vol. 43, no. 4, pp. 971–980. doi: 10.1046/j.1365-2958.2002.02781.x
- Suerbaum S., Michetti P. Helicobacter pylori infection. N. Tngl. J. Med., 2002, vol. 347, no. 15, pp. 1175–1186. doi: 10.1056/NEJMra020542
- Szabo I., Brutache S., Tombola F., Moschioni M., Satin B., Telford J.L., Rappuoli R., Montecucco C., Papini E., Zoratti M. Formation of anion-selective channels in the cell plasma membrane by the toxin VacA of Helicobacter pylori is required for its biological activity. EMBO J., 1999, vol. 18, no. 20, pp. 5517–5527. doi: 10.1093/emboj/18.20.5517
- Tabassam F.H., Graham D.Y., Yamaoka Y. OipA plays a role in Helicobacter pylori-induced focal adhesion kinase activation and cytoskeletal re-organization. Cell. Microbiol., 2008, vol. 10, no. 4, pp. 1008–1020. doi: 10.1111/j.1462-5822.2007.01104.x
- Tammer I., Brandt S., Hartig R., Konig W., Backert S. Activation of Abl by Helicobacter pylori: a novel kinase for CagA and crucial mediator of host cell scattering. Gastroenterology, 2007, vol. 132, no. 4, pp. 1309–1319. doi: 10.1053/j.gastro.2007.01.050
- Tee W., Lambert J.R., Dwyer B. Cytotoxin production by Helicobacter pylori from patients with upper gastrointestinal tract diseases. J. Clin. Microbiol., 1995, vol. 33, no. 5, pp. 1203–1205.
- Tegtmeyer N., Hartig R., Delahay R.M., Rohde M., Brandt S., Conradi J., Takahashi S., Smolka A.J., Sewald N., Backert S. A small fibronectin-mimicking protein from bacteria induces cell spreading and focal adhesion formation. J. Biol. Chem., 2010, vol. 85, no. 30, pp. 23515–23526. doi: 10.1074/jbc.M109.096214
- Teymournejad O., Mobarez A.M., Hassan Z.M., Moazzeni S.M., Ahmadabad H.N. In vitro suppression of dendritic cells by Helicobacter pylori OipA. Helicobacter, 2014, vol. 19, no. 2, pp. 136–143. doi: 10.1111/hel.12107
- Thomsen L., Tasman-Jones C., Morris A., Wiggins P., Lee S., Forlong C. Ammonia produced by Campylobacter pylori neutralizes H+ moving through gastric mucus. Scand. J. Gastroenterol., 1989, vol. 24, no. 6, pp. 761–768. doi: 10.3109/00365528909093119
- Tsujii M., Kawano S., Tsuji S., Fusamoto H., Kamada T., Sato N. Mechanism of gastric mucosal damage induced by ammonia. Gastroenterology, 1992, vol. 102, no. 6, pp. 1881–1888. doi: 10.1016/0016-5085(92)90309-M
- Van Doorn L.J., Figueiredo C., Sanna R., Plaisier A., Schneeberger P., de Boer W., Quint W. Clinical relevance of the cagA, vacA, and iceA status of Helicobacter pylori. Gastroenterology, 1998, vol. 115, no. 1, pp. 58–66. doi: 10.1016/S0016-5085(98)70365-8
- Viala J., Chaput C., Boneca I.G., Cardona A., Girardin S.E., Moran A.P., Athman R., Mémet S., Huerre M.R., Coyle A.J., DiStefano P.S., Sansonetti P.J., Labigne A., Bertin J., Philpott D.J., Ferrero R.L. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol., 2004, vol. 5, no. 11, pp. 1166–1174. doi: 10.1038/ni1131
- Walz A,. Odenbreit S., Mahdavi J., Borén T., Ruhl S. Identification and characterization of binding properties of Helicobacter pylori by glycoconjugate arrays. Glycobiology, 2005, vol. 15, no. 7, pp. 700–708. doi: 10.1093/glycob/cwi049
- Weeks D.L., Eskandari S., Scott D.R., Sachs G. A H+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science, 2000, vol. 287, no. 5452, pp. 482–485. doi: 10.1126/science.287.5452.482
- Wessler S., Backert S. Molecular mechanisms of epithelial-barrier disruption by Helicobacter pylori. Trends Microbiol., 2008, vol. 16, no. 8, pp. 397–405. doi: 10.1016/j.tim.2008.05.005
- Wroblewski L.E., Peek R.M. Jr. Targeted disruption of the epithelial-barrier by Helicobacter pylori. Cell. Commun. Signal., 2011, vol. 9, pp. e29. doi: 10.1186/1478-811X-9-29
- Wu J.Y., Lu H., Sun Y., Graham D.Y., Cheung H.S., Yamaoka Y. Balance between polyoma enhancing activator 3 and activator protein 1 regulates Helicobacter pylori-stimulated matrix metalloproteinase 1 expression. Cancer Res., 2006, vol. 66, no. 10, pp. 5111–5120. doi: 10.1158/0008-5472.CAN-06-0383
- Yamaoka Y. Increasing evidence of the role of Helicobacter pylori SabA in the pathogenesis of gastroduodenal disease. J. Infect. Dev. Ctries, 2008, vol. 2, no. 3, pp. 174–181.
- Yamaoka Y., Kikuchi S., El Zimaity H.M., Gutierrez O., Osato M.S., Graham D.Y. Importance of Helicobacter pylori oipA in clinical presentation, gastric inflammation, and mucosal interleukin 8 production. Gastroenterology, 2002, vol. 123, no. 2, pp. 414–424. doi: 10.1053/gast.2002.34781
- Yamaoka Y., Kwon D.H., Graham D.Y. AM(r) 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 13, pp. 7533–7538. doi: 10.1073/pnas.130079797
- Yokota S., Amano K., Hayashi S., Kubota T., Fujii N., Yokochi T. Human antibody response to Helicobacter pylori lipopolysaccharide: presence of an immunodominant epitope in the polysaccharide chain of lipopolysaccharide. Infect. Immun., 1998, vol. 66, no. 6, pp. 3006–3011.
- Yokota S., Okabayashi T, Rehli M., Fujii N., Amano K. 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, vol. 78, no. 1, pp. 468–476. doi: 10.1128/IAI.00903-09
- Zarrilli R., Ricci V., Romano M. Molecular response of gastric epithelial cells to Helicobacter pylori-induced cell damage. Cell. Microbiol., 1999, vol. 1, no. 2, pp. 93–99. doi: 10.1046/j.1462-5822.1999.00018.x