Helicobacter pylori is one of the most successful human pathogens, which colonizes the mucus layer of the gastric epithelium of more than 50% of the world’s population. This curved, microaerophilic, Gram-negative bacterium induces a chronic active gastritis, often asymptomatic, in all infected individuals. In some cases, this gastritis evolves to more severe diseases such as peptic ulcer disease, gastric adenocarcinoma, and gastric mucosa-associated lymphoid tissue lymphoma. H. pylori has developed a unique set of factors, actively supporting its successful survival and persistence in its natural hostile ecological niche, the human stomach, throughout the individual’s life, unless treated. In the human stomach, the vast majority of H. pylori cells are motile in the mucus layer lining, but a small percentage adheres to the epithelial cell surfaces. Adherence to the gastric epithelium is important for the ability of H. pylori to cause disease because this intimate attachment facilitates: (1) colonization and persistence, by preventing the bacteria from being eliminated from the stomach, by mucus turnover and gastric peristalsis; (2) evasion from the human immune system and (3) efficient delivery of proteins into the gastric cell, such as the CagA oncoprotein. Therefore, bacteria with better adherence properties colonize the host at higher densities. H. pylori is one of the most genetically diverse bacterial species known and is equipped with an extraordinarily large set of outer membrane proteins, whose role in the infection and persistence process will be discussed in this review, as well as the different receptor structures that have been so far described for mucosal adherence.
References
[1]
Marshall, B.J.; Warren, J.R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984, 1, 1311–1315, doi:10.1016/S0140-6736(84)91816-6.
[2]
Falush, D.; Wirth, T.; Linz, B.; Pritchard, J.K.; Stephens, M.; Kidd, M.; Blaser, M.J.; Graham, D.Y.; Vacher, S.; Perez-Perez, G.I.; et al. Traces of human migrations in Helicobacter pylori populations. Science 2003, 299, 1582–1585, doi:10.1126/science.1080857.
[3]
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Schistosomes, liver flukes and Helicobacter pylori. In Monographs on the Evaluation of Carcinogenic Risks to Humans; World Health Organization, International Agency for Research on Cancer: Lyon, France, 1994; Volume 61, pp. 1–241.
[4]
González, C.; Megraud, F.; Buissonniere, A.; Lujan Barroso, L.; Agudo, A.; Duell, E.J.; Boutron-Ruault, M.C.; Clavel-Chapelon, F.; Palli, D.; Krogh, V.; et al. Helicobacter pylori infection assessed by ELISA and by immunoblot and noncardia gastric cancer risk in a prospective study: The Eurgast-EPIC project. Ann. Oncol. 2012, 23, 1320–1324, doi:10.1093/annonc/mdr384.
[5]
Banic, M.; Franceschi, F.; Babic, Z.; Gasbarrini, A. Extragastric manifestations of Helicobacter pylori infection. Helicobacter 2012, 17, 49–55.
[6]
Fukase, K.; Kato, M.; Kikuchi, S.; Inoue, K.; Uemura, N.; Okamoto, S.; Terao, S.; Amagai, K.; Hayashi, S.; Asaka, M.; The Japan Gast Study Group. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: An open-label, randomised controlled trial. Lancet 2008, 372, 392–397, doi:10.1016/S0140-6736(08)61159-9.
[7]
Malfertheiner, P.; Megraud, F.; O’Morain, C.; Bazzoli, F.; El-Omar, E.; Graham, D.; Hunt, R.; Rokkas, T.; Vakil, N.; Kuipers, E.J.; et al. Current concepts in the management of Helicobacter pylori infection: The Maastricht III Consensus Report. Gut 2007, 56, 772–781, doi:10.1136/gut.2006.101634.
[8]
Backert, S.; Clyne, M.; Tegtmeyer, N. Molecular mechanisms of gastric epithelial cell adhesion and injection of CagA by Helicobacter pylori. Cell Commun. Signal 2011, 9, 28, doi:10.1186/1478-811X-9-28.
[9]
Suerbaum, S.; Achtman, M. Evolution of Helicobacter pylori: The role of recombination. Trends Microbiol. 1999, 7, 182–184, doi:10.1016/S0966-842X(99)01505-X.
[10]
Falush, D.; Kraft, C.; Taylor, N.S.; Correa, P.; Fox, J.G.; Achtman, M.; Suerbaum, S. Recombination and mutation during long-term gastric colonization by Helicobacter pylori: Estimates of clock rates, recombination size, and minimal age. Proc. Natl. Acad. Sci. USA 2001, 98, 15056–15061.
[11]
Odenbreit, S.; Swoboda, K.; Barwig, I.; Ruhl, S.; Borén, T.; Koletzko, S.; Haas, R. Outer membrane protein expression profile in Helicobacter pylori clinical isolates. Infect. Immun. 2009, 77, 3782–3790, doi:10.1128/IAI.00364-09.
[12]
Suerbaum, S.; Josenhans, C. Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat. Rev. Microbiol. 2007, 5, 441–452, doi:10.1038/nrmicro1658.
[13]
Morelli, G.; Didelot, X.; Kusecek, B.; Schwarz, S.; Bahlawane, C.; Falush, D.; Suerbaum, S.; Achtman, M. Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet. 2010, 6, e1001036, doi:10.1371/journal.pgen.1001036.
[14]
Kuipers, E.J.; Israel, D.A.; Kusters, J.G.; Gerrits, M.M.; Weel, J.; van der Ende, A.; van der Hulst, R.; Wirth, H.P.; H??k-Nikanne, J.; Thompson, S.A.; et al. Quasispecies development of Helicobacter pylori observed in paired isolates obtained years apart from the same host. J. Infect. Dis. 2000, 181, 273–282, doi:10.1086/315173.
Edwards, N.J.; Monteiro, M.A.; Faller, G.; Walsh, E.J.; Moran, A.P.; Roberts, I.S.; High, N.J. Lewis X structures in the O antigen side-chain promote adhesion of Helicobacter pylori to the gastric epithelium. Mol. Microbiol. 2000, 35, 1530–1539.
[19]
Monteiro, M.A.; Chan, K.H.N.; Rasko, D.A.; Taylor, D.E.; Zheng, P.Y.; Appelmelk, B.J.; Wirth, H.P.; Yang, M.; Blaser, M.J.; Hynes, S.O.; et al. Simultaneous expression of type 1 and type 2 Lewis blood group antigens by Helicobacter pylori lipopolysaccharides. J. Biol. Chem. 1998, 273, 11533–11543, doi:10.1074/jbc.273.19.11533.
[20]
Osaki, T.; Yamaguchi, H.; Taguchi, H.; Fukuda, M.; Kawakami, H.; Hirano, H.; Watanabe, S.; Takagi, A.; Kamiya, S. Establishment and characterisation of a monoclonal antibody to inhibit adhesion of Helicobacter pylori to gastric epithelial cells. J. Med. Microbiol. 1998, 47, 505–512.
[21]
Fowler, M.; Thomas, R.J.; Atherton, J.; Roberts, I.S.; High, N.J. Galectin-3 binds to Helicobacter pylori O-antigen: It is upregulated and rapidly secreted by gastric epithelial cells in response to H. pylori adhesion. Cell. Microbiol. 2006, 8, 44–54, doi:10.1111/j.1462-5822.2005.00599.x.
[22]
Odenbreit, S.; Faller, G.; Haas, R. Role of the AlpAB proteins and lipopolysaccharide in adhesion of Helicobacter pylori to human gastric tissue. Int. Med. Microbiol. 2002, 292, 247–256, doi:10.1078/1438-4221-00204.
[23]
Mahdavi, J.; Boren, T.; Vandenbroucke Grauls, C.; Appelmelk, B.J. Limited role of lipopolysaccharide lewis antigens in adherence of Helicobacter pylori to the human gastric epithelium. Infect. Immun. 2003, 71, 2876–2880, doi:10.1128/IAI.71.5.2876-2880.2003.
[24]
Alm, R.A.; Bina, J.; Andrews, B.M.; Doig, P.; Hancock, R.E.W.; Trust, T.J. Comparative genomics of Helicobacter pylori: Analysis of the outer membrane protein families. Infect. Immun. 2000, 68, 4155–4168, doi:10.1128/IAI.68.7.4155-4168.2000.
[25]
Doig, P.; Exner, M.M.; Hancock, R.E.W.; Trust, T.J. Isolation and characterization of a conserved porin protein from Helicobacter pylori. J. Bacteriol. 1995, 177, 5447–5452.
[26]
Exner, M.M.; Doig, P.; Trust, T.J.; Hancock, R.E. Isolation and characterization of a family of porin proteins from Helicobacter pylori. Infect. Immun. 1995, 63, 1567–1572.
Mahdavi, J.; Sonden, B.; Hurtig, M.; Olfat, F.O.; Forsberg, L.; Roche, N.; ?ngstr?m, J.; Larsson, T.; Teneberg, S.; Karlsson, K.A.; et al. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 2002, 297, 573–578, doi:10.1126/science.1069076.
[29]
Oleastro, M.; Cordeiro, R.; Ferrand, J.; Nunes, B.; Lehours, P.; Carvalho-Oliveira, I.; Mendes, A.L.; Monteiro, L.; Mégraud, F.; Ménard, A. Evaluation of the clinical significance of homB, a novel candidate marker of Helicobacter pylori strains associated with peptic ulcer disease. J. Infect. Dis. 2008, 198, 1379–1387, doi:10.1086/592166.
[30]
Yamaoka, Y. Roles of Helicobacter pylori BabA in gastroduodenal pathogenesis. World J. Gastroenterol. 2008, 14, 4265–4272, doi:10.3748/wjg.14.4265.
[31]
Moore, M.; Borén, T.; Solnick, J. Life at the margins: Modulation of attachment proteins in Helicobacter pylori. Gut Microbes 2011, 2, 42–46, doi:10.4161/gmic.2.1.14626.
[32]
Borén, T.; Falk, P.; Roth, K.A.; Larson, G.; Normark, S. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 1993, 262, 1892–1895.
[33]
Aspholm-Hurtig, M.; Dailide, G.; Lahmann, M.; Kalia, A.; Ilver, D.; Roche, N.; Vikstr?m, S.; Lindén, S.; B?ckstr?m, A.; Lundberg, C.; et al. Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 2004, 305, 519–522, doi:10.1126/science.1098801.
[34]
Sakamoto, S.; Watanabe, T.; Tokumaru, T.; Takagi, H.; Nakazato, H.; Lloyd, K.O. Expression of Lewisa, Lewisb, Lewisx, Lewisy, siayl-Lewisa, and sialyl-Lewisx blood group antigens in human gastric carcinoma and in normal gastric tissue. Cancer Res. 1989, 49, 745–752.
[35]
Benktander, J.; ?ngstr?m, J.; Breimer, M.; Teneberg, S. Redefinition of the carbohydrate binding specificity of Helicobacter pylori BabA adhesin. J. Biol. Chem. 2012, 287, 31712–31724.
[36]
Walz, A.; Odenbreit, S.; Mahdavi, J.; Boren, T.; Ruhl, S. Identification and characterization of binding properties of Helicobacter pylori by glycoconjugate arrays. Glycobiology 2005, 15, 700–708, doi:10.1093/glycob/cwi049.
[37]
Walz, A.; Odenbreit, S.; Stühler, K.; Wattenberg, A.; Meyer, H.E.; Mahdavi, J.; Borén, T.; Ruhl, S. Identification of glycoprotein receptors within the human salivary proteome for the lectin-like BabA and SabA adhesins of Helicobacter pylori by fluorescence-based 2-D bacterial overlay. Proteomics 2009, 9, 1582–1592, doi:10.1002/pmic.200700808.
[38]
Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731–2739, doi:10.1093/molbev/msr121.
[39]
Tamura, K.; Nei, M.; Kumar, S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 2004, 101, 11030–11035, doi:10.1073/pnas.0404206101.
[40]
Aspholm, M.; Olfat, F.O.; Nordén, J.; Sondén, B.; Lundberg, C.; Sj?str?m, R.; Altraja, S.; Odenbreit, S.; Haas, R.; Wadstr?m, T.; et al. SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog 2006, 2, e110, doi:10.1371/journal.ppat.0020110.
[41]
Unemo, M.; Aspholm-Hurtig, M.; Ilver, D.; Bergstr?m, J.; Borén, T.; Danielsson, D.; Teneberg, S. The sialic acid binding SabA adhesin of Helicobacter pylori is essential for nonopsonic activation of human neutrophils. J. Biol. Chem. 2005, 280, 15390–15397.
[42]
Odenbreit, S.; Till, M.; Hofreuter, D.; Faller, G.; Haas, R. Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol. Microbiol. 1999, 31, 1537–1548, doi:10.1046/j.1365-2958.1999.01300.x.
Pride, D.T.; Blaser, M.J. Concerted evolution between duplicated genetic elements in Helicobacter pylori. J. Mol. Biol. 2002, 316, 629–642, doi:10.1006/jmbi.2001.5311.
[45]
Pride, D.T.; Meinersmann, R.J.; Blaser, M.J. Allelic variation within Helicobacter pylori babA and babB. Infect. Immun. 2001, 69, 1160–1171, doi:10.1128/IAI.69.2.1160-1171.2001.
[46]
Colbeck, J.C.; Hansen, L.M.; Fong, J.M.; Solnick, J.V. Genotypic profile of the outer membrane proteins BabA and BabB in clinical isolates of Helicobacter pylori. Infect. Immun. 2006, 74, 4375–4378, doi:10.1128/IAI.00485-06.
[47]
Backstrom, A.; Lundberg, C.; Kersulyte, D.; Berg, D.E.; Boren, T.; Arnqvist, A. Metastability of Helicobacter pylori bab adhesin genes and dynamics in Lewis b antigen binding. Proc. Natl. Acad. Sci. USA 2004, 101, 16923–16928.
[48]
Solnick, J.V.; Hansen, L.M.; Salama, N.R.; Boonjakuakul, J.K.; Syvanen, M. Modification of Helicobacter pylori outer membrane protein expression during experimental infection of Rhesus macaques. Proc. Natl. Acad. Sci. USA 2004, 101, 2106–2111.
[49]
Matteo, M.; Armitano, R.; Romeo, M.; Wonaga, A.; Olmos, M.; Catalano, M. Helicobacter pylori bab genes during chronic colonization. Int. J. Mol. Epidemiol. Genet. 2011, 30, 286–291.
[50]
Styer, C.M.; Hansen, L.M.; Cooke, C.L.; Gundersen, A.M.; Choi, S.S.; Berg, D.E.; Benghezal, M.; Peek, R.M.; Borén, T.; Solnick, J.V.; et al. Expression of the BabA adhesin during experimental infection with Helicobacter pylori. Infect. Immun. 2010, 78, 1593–1600, doi:10.1128/IAI.01297-09.
[51]
Ohno, T.; Vallstr?m, A.; Rugge, M.; Ota, H.; Graham, D.Y.; Arnqvist, A.; Yamaoka, Y. Effects of blood group antigen-binding adhesin expression during Helicobacter pylori infection of Mongolian gerbils. J. Infect. Dis. 2011, 203, 726–735, doi:10.1093/infdis/jiq090.
[52]
Hennig, E.; Allen, J.; Cover, T. Multiple chromosomal loci for the babA gene in Helicobacter pylori. Infect. Immun. 2006, 74, 3046–3051, doi:10.1128/IAI.74.5.3046-3051.2006.
[53]
Armitano, R.; Matteo, M.; Goldman, C.; Wonaga, A.; Viola, L.A.; de Palma, G.Z.; Catalano, M. Helicobacter pylori heterogeneity in patients with gastritis and peptic ulcer disease. Infect. Genet. Evol. 2013, 16, 377–385, doi:10.1016/j.meegid.2013.02.024.
[54]
Ishijima, N.; Suzuki, M.; Ashida, H.; Ichikawa, Y.; Kanegae, Y.; Saito, I.; Borén, T.; Haas, R.; Sasakawa, C.; Mimuro, H. BabA-mediated adherence is a potentiator of the Helicobacter pylori type IV secretion system activity. J. Biol. Chem. 2011, 286, 25256–25264, doi:10.1074/jbc.M111.233601.
[55]
Toller, I.M.; Neelsen, K.J.; Steger, M.; Hartung, M.L.; Hottiger, M.O.; Stucki, M.; Kalali, B.; Gerhard, M.; Sartori, A.A.; Lopes, M.; et al. Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc. Natl. Acad. Sci. USA 2011, 108, 14944–14949, doi:10.1073/pnas.1100959108.
Azevedo, M.; Eriksson, S.; Mendes, N.; Serpa, J.; Figueiredo, C.; Resende, L.P.; Ruvo?n-Clouet, N.; Haas, R.; Bor?n, T.; Le Pedun, J.; et al. Infection by Helicobacter pylori expressing the BabA adhesin is influenced by the secretor phenotype. J. Pathol. 2008, 215, 308–316, doi:10.1002/path.2363.
[58]
Gerhard, M.; Lehn, N.; Neumayer, N.; Borén, T.; Rad, R.; Schepp, W.; Miehlke, S.; Classen, M.; Prinz, C. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc. Natl. Acad. Sci. USA 1999, 96, 12778–12783, doi:10.1073/pnas.96.22.12778.
[59]
Yamaoka, Y. Increasing evidence of the role of Helicobacter pylori SabA in the pathogenesis of gastroduodenal disease. J. Infect. Dev. Ctries. 2008, 2, 174–181, doi:10.3855/jidc.259.
Saunders, N.J.; Boonmee, P.; Peden, J.F.; Jarvis, S.A. Inter-species horizontal transfer resulting in core-genome and niche-adaptive variation within Helicobacter pylori. BMC Genomics 2005, 6, 9.
[66]
Kao, C.Y.; Sheu, B.S.; Sheu, S.M.; Yang, H.B.; Chang, W.L.; Cheng, H.C.; Wu, J.J. Higher motility enhances bacterial density and inflammatory response in dyspeptic patients infected with Helicobacter pylori. Helicobacter 2012, 17, 411–416, doi:10.1111/j.1523-5378.2012.00974.x.
[67]
Sheu, B.; Odenbreit, S.; Hung, K.H.; Liu, C.P.; Sheu, S.M.; Yang, H.B.; Wu, J.J. Interaction between host gastric Sialyl-Lewis X and H. pylori SabA enhances H. pylori density in patients lacking gastric Lewis B antigen. Am. J. Gastroenterol. 2006, 101, 36–44, doi:10.1111/j.1572-0241.2006.00358.x.
[68]
Marcos, N.T.; Magalh?es, A.; Ferreira, B.; Oliveira, M.J.; Carvalho, A.S.; Mendes, N.; Gilmartin, T.; Head, S.R.; Figueiredo, C.; David, L.; et al. Helicobacter pylori induces beta3GnT5 in human gastric cell lines, modulating expression of the SabA ligand sialyl-Lewis x. J. Clin. Invest. 2008, 118, 2325–2336.
[69]
Bernarde, C.; Lehours, P.; Lasserre, J.P.; Castroviejo, M.; Mégraud, F.; Ménard, A. Complexomics study of two Helicobacter pylori strains of two pathological origins: Potential targets for vaccine development and new insight in bacteria metabolism. Mol. Cell Proteomics 2010, 9, 2796–2826, doi:10.1074/mcp.M110.001065.
[70]
Alm, R.A.; Ling, L.S.L.; Moir, D.T.; King, B.L.; Brown, E.D.; Doig, P.C.; Smith, D.R.; Noonan, B.; Guild, B.C.; deJonge, B.L.; et al. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 1999, 397, 176–180, doi:10.1038/16495.
[71]
Baik, S.C.; Kim, K.M.; Song, S.M.; Kim, D.S.; Jun, J.S.; Lee, S.G.; Song, J.Y.; Park, J.U.; Kang, H.L.; Lee, W.K.; et al. Proteomic analysis of the sarcosine-insoluble outer membrane fraction of Helicobacter pylori strain 26695. J. Bacteriol. 2004, 186, 949–955, doi:10.1128/JB.186.4.949-955.2004.
[72]
Odenbreit, S.; Till, M.; Hofreuter, D.; Haas, R. Outer membrane proteins AlpA and AlpB are involved in H. pylori binding to epithelial cells. Gut 1997, 41, A107, doi:10.1136/gut.41.1.107.
[73]
De Jonge, R.; Durrani, Z.; Rijpkema, S.G.; Kuipers, E.J.; van Vliet, A.H.; Kusters, J.G. Role of the Helicobacter pylori outer-membrane proteins AlpA and AlpB in colonization of the guinea pig stomach. J. Med. Microbiol. 2004, 53, 375–379, doi:10.1099/jmm.0.45551-0.
[74]
Sugimoto, M.; Ohno, T.; Graham, D.; Yamaoka, Y. Helicobacter pylori outer membrane proteins on gastric mucosal interleukin 6 and 11 expression in Mongolian gerbils. J. Gastroenterol. Hepatol. 2011, 26, 1677–1684, doi:10.1111/j.1440-1746.2011.06817.x.
[75]
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, 282, 6242–6254.
[76]
Huang, C.H.; Chiou, S.H. Proteomic analysis of upregulated proteins in Helicobacter pylori under oxidative stress induced by hydrogen peroxide. Kaohsiung J. Med. Sci. 2011, 27, 544–553.
[77]
Xue, J.; Bai, Y.; Chen, Y.; Wang, J.D.; Zhang, Z.S.; Zhang, Y.L.; Zhou, D.Y. Expression of Helicobacter pylori AlpA protein and its immunogenicity. World J. Gastroenterol. 2005, 11, 2260–2263.
[78]
Bai, Y.; Zhang, Y.; Wang, J.; Lin, H.; Zhang, Z.; Zhou, D. Conservative region of the genes encoding four adhesins of Helicobacter pylori: Cloning, sequence analysis and biological information analysis. Di Yi Jun Yi Da Xue Xue Bao 2002, 22, 869–871.
[79]
Sun, Z.L.; Bi, Y.W.; Bai, C.M.; Gao, D.D.; Li, Z.H.; Dai, Z.X.; Li, J.F.; Xu, W.M. Expression of Helicobacter pylori alpA gene in Lactococcus lactis and its immunogenicity analysis. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 2010, 26, 203–206.
[80]
Yamaoka, Y.; Kwon, D.H.; Graham, D.Y. A M(r) 34,000 proinflammatory outer membrane protein (OipA) of Helicobacter pylori. Proc. Natl. Acad. Sci. USA 2000, 97, 111–133.
Tabassam, F.H.; Graham, D.Y.; Yamaoka, Y. Helicobacter pylori-associated regulation of forkhead transcription factors FoxO1/3a in human gastric cells. Helicobacter 2012, 17, 193–202, doi:10.1111/j.1523-5378.2012.00939.x.
[83]
Dossumbekova, A.; Prinz, C.; Mages, J.; Lang, R.; Kusters, J.G.; van Vliet, A.H.; Reindl, W.; Backert, S.; Saur, D.; Schmid, R.M.; et al. Helicobacter pylori HopH (OipA) and bacterial pathogenicity: Genetic and functional genomic analysis of hopH gene polymorphisms. J. Infect. Dis. 2006, 194, 1346–1355, doi:10.1086/508426.
[84]
Franco, A.T.; Johnston, E.; Krishna, U.; Yamaoka, Y.; Israel, D.A.; Nagy, T.A.; Wroblewski, L.E.; Piazuelo, M.B.; Correa, P.; Peek, R.M., Jr. Regulation of gastric carcinogenesis by Helicobacter pylori virulence factors. Cancer Res. 2008, 68, 379–387, doi:10.1158/0008-5472.CAN-07-0824.
[85]
Teymournejad, O.; Mobarez, A.M.; Hassan, Z.M.; Moazzeni, S.M.; Yakhchali, B.; Eskandari, V. In silico prediction of exposure amino acid sequences of outer inflammatory protein A of Helicobacter pylori for surface display on Escherichia coli. Indian J. Hum. Genet. 2012, 18, 83–86, doi:10.4103/0971-6866.96659.
Markovska, R.; Boyanova, L.; Yordanov, D.; Gergova, G.; Mitov, I. Helicobacter pylori oipA genetic diversity and its associations with both disease and cagA, vacA s,m, and i alleles among Bulgarian patients. Diagn. Microbiol. Infect. Dis. 2011, 71, 335–340, doi:10.1016/j.diagmicrobio.2011.08.008.
[88]
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, 10, 1008–1020, doi:10.1111/j.1462-5822.2007.01104.x.
[89]
Tabassam, F.H.; Graham, D.Y.; Yamaoka, Y. Paxillin is a novel cellular target for converging Helicobacter pylori-induced cellular signaling. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 301, G601–G611, doi:10.1152/ajpgi.00375.2010.
[90]
Chen, J.; Lin, M.; Li, N.; Lin, L.; She, F. Therapeutic vaccination with Salmonella-delivered codon-optimized outer inflammatory protein DNA vaccine enhances protection in Helicobacter pylori infected mice. Vaccine 2012, 30, 5310–5315, doi:10.1016/j.vaccine.2012.06.052.
[91]
Chen, J.; Lin, L.; Li, N.; She, F. Enhancement of Helicobacter pylori outer inflammatory protein DNA vaccine efficacy by co-delivery of interleukin-2 and B subunit heat-labile toxin gene encoded plasmids. Microbiol. Immunol. 2012, 56, 85–92, doi:10.1111/j.1348-0421.2011.00409.x.
[92]
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, 27, 3325–3333, doi:10.1093/nar/27.16.3325.
[93]
Giannakis, M.; B?ckhed, 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, 284, 30383–30394, doi:10.1074/jbc.M109.052738.
[94]
Kennemann, L.; Didelot, X.; Aebischer, T.; Kuhn, S.; Drescher, B.; Droege, M.; Reinhardt, R.; Correa, P.; Meyer, T.F.; Josenhans, C.; et al. Helicobacter pylori genome evolution during human infection. Proc. Natl. Acad. Sci. USA 2011, 108, 5033–5038, doi:10.1073/pnas.1018444108.
[95]
Kennemann, L.; Brenneke, B.; Andres, S.; Engstrand, L.; Meyer, T.F.; Aebischer, T.; Josenhans, C.; Suerbaum, S. In vivo sequence variation in HopZ, a phase-variable outer membrane protein of Helicobacter pylori. Infect. Immun. 2012, 80, 4364–4373, doi:10.1128/IAI.00977-12.
[96]
De Jonge, R.; Pot, R.G.J.; Loffeld, R.J.L.F.; van Vliet, A.H.M.; Kuipers, E.J.; Kusters, J.G. The functional status of the Helicobacter pylori sabB adhesin gene as a putative marker for disease outcome. Helicobacter 2004, 9, 158–164, doi:10.1111/j.1083-4389.2004.00213.x.
[97]
Chiarini, A.; Calà, C.; Bonura, C.; Gullo, A.; Giuliana, G.; Peralta, S.; D’Arpa, F.; Giammanco, A. Prevalence of virulence-associated genotypes of Helicobacter pylori and correlation with severity of gastric pathology in patients from western Sicily, Italy. Eur. J. Clin. Microbiol. Infect. Dis. 2009, 28, 437–446, doi:10.1007/s10096-008-0644-x.
[98]
Lehours, P.; Ménard, A.; Dupouy, S.; Bergey, B.; Richy, F.; Zerbib, F.; Ruskoné-Fourmestraux, A.; Delchier, J.C.; Mégraud, F. Evaluation of the association of nine Helicobacter pylori virulence factors with strains involved in low-grade gastric mucosa-associated lymphoid tissue lymphoma. Infect. Immun. 2004, 72, 880–888, doi:10.1128/IAI.72.2.880-888.2004.
[99]
Oleastro, M.; Cordeiro, R.; Ménard, A.; Yamaoka, Y.; Queiroz, D.; Mégraud, F.; Monteiro, L. Allelic diversity and phylogeny of homB, a novel co-virulence marker of Helicobacter pylori. BMC Microbiol. 2009, 9, 248, doi:10.1186/1471-2180-9-248.
[100]
Oleastro, M.; Cordeiro, R.; Ménard, A.; Gomes, J.P. Allelic diversity among Helicobacter pylori outer membrane protein genes homB and homA generated by recombination. J. Bacteriol. 2010, 192, 3961–3968, doi:10.1128/JB.00395-10.
[101]
Oleastro, M.; Monteiro, L.; Lehours, P.; Mégraud, F.; Ménard, A. Identification of markers for Helicobacter pylori strains isolated from children with peptic ulcer disease by suppressive subtractive hybridization. Infect. Immun. 2006, 74, 4064–4074, doi:10.1128/IAI.00123-06.
[102]
Oleastro, M.; Cordeiro, R.; Yamaoka, Y.; Queiroz, D.; Mégraud, F.; Monteiro, L.; Ménard, A. Disease association with two Helicobacter pylori duplicate outer membrane protein genes, homB and homA. Gut Pathog 2009, doi:10.1186/1757-4749-1-12.
[103]
Jung, S.W.; Sugimoto, M.; Graham, D.Y.; Yamaoka, Y. homB status of Helicobacter pylori as a novel marker to distinguish gastric cancer from duodenal ulcer. J. Clin. Microbiol. 2009, 47, 3241–3245, doi:10.1128/JCM.00293-09.
[104]
Abadi, A.T.B.; Rafiei, A.; Ajami, A.; Hosseini, V.; Taghvaei, T.; Jones, K.R.; Merrell, D.S. Helicobacter pylori homB, but not cagA, is associated with gastric cancer in Iran. J. Clin. Microbiol. 2011, 49, 3191–3197, doi:10.1128/JCM.00947-11.
[105]
Hussein, N.R. A study of Helicobacter pylori outer-membrane proteins (hom) A and B in Iraq and Turkey. J. Infect. Public Health 2011, 4, 135–139, doi:10.1016/j.jiph.2011.03.004.
[106]
Kang, J.; Jones, K.R.; Jang, S.; Olsen, C.H.; Yoo, Y.J.; Merrell, D.S.; Cha, J.H. The geographic origin of Helicobacter pylori influences the association of the homB gene with gastric cancer. J. Clin. Microbiol. 2012, 50, 1082–1085, doi:10.1128/JCM.06293-11.
[107]
Tomb, J.F.; White, O.; Kerlavage, A.R.; Clayton, R.A.; Sutton, G.G.; Fleischmann, R.D.; Ketchum, K.A.; Klenk, H.P.; Gill, S.; Dougherty, B.A.; et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997, 388, 539–547, doi:10.1038/41483.
[108]
Morris, A.; Nicholson, G.; Zwi, J.; Vanderwee, M. Campylobacter pylori infection in Meckel’s diverticula containing gastric mucosa. Gut 1989, 30, 1233–1235, doi:10.1136/gut.30.9.1233.
[109]
Kestemberg, A.; Mari?o, G.; de Lima, E.; Garcia, F.; Carrascal, E.; Arredondo, J.L. Gastric heterotopic mucosa in the rectum with Helicobacter pylori-like organisms: A rare cause of rectal bleeding. Int. J. Colorectal Dis. 1993, 8, 9–12.
[110]
Genta, R.M.; Gurer, I.E.; Graham, D.Y.; Krishnan, B.; Segura, A.M.; Gutierrez, O.; Kim, J.G.; Burchette, J.L., Jr. Adherence of Helicobacter pylori to areas of incomplete intestinal metaplasia in the gastric mucosa. Gastroenterology 1996, 111, 1206–1211, doi:10.1053/gast.1996.v111.pm8898634.
[111]
Lindén, S.; Nordman, H.; Hedenbro, J.; Hurtig, M.; Borén, T.; Carlstedt, I. Strain- and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms. Gastroenterology 2002, 123, 1923–1930, doi:10.1053/gast.2002.37076.
[112]
Van den Brink, G.R.; Tytgat, K.; van der Hulst, R.; van der Loos, C.M.; Einerhand, A.; Buller, H.; Dekker, J. H. pylori colocalises with MUC5AC in the human stomach. Gut 2000, 46, 601–607, doi:10.1136/gut.46.5.601.
[113]
Nordman, H.; Davies, J.R.; Lindell, G.; de Bolós, C.; Real, F.; Carlstedt, I. Gastric MUC5AC and MUC6 are large oligomeric mucins that differ in size, glycosylation and tissue distribution. Biochem. J. 2002, 364, 191–200.
[114]
Kawakubo, M.; Ito, Y.; Okimura, Y.; Kobayashi, M.; Sakura, K.; Kasama, S.; Fukuda, M.N.; Katsuyama, T.; Nakayama, J. Natural antibiotic function of a human gastric mucin against Helicobacter pylori infection. Science 2004, 305, 1003–1006.
[115]
Van de Bovenkamp, J.H.; Mahdavi, J.; Korteland-Van Male, A.M.; Büller, H.A.; Einerhand, A.W.; Borén, T.; Dekker, J. The MUC5AC glycoprotein is the primary receptor for Helicobacter pylori in the human stomach. Helicobacter 2003, 8, 521–532, doi:10.1046/j.1523-5378.2003.00173.x.
[116]
Magalh?es, A.; Gomes, J.; Ismail, M.N.; Haslam, S.M.; Mendes, N.; Osório, H.; David, L.; Le Pendu, J.; Haas, R.; Dell, A.; et al. Fut2-null mice display an altered glycosylation profile and impaired BabA-mediated Helicobacter pylori adhesion to gastric mucosa. Glycobiology 2009, 19, 1525–1536, doi:10.1093/glycob/cwp131.
[117]
Correa, P. Human gastric carcinogenesis: A multistep and multifactorial process-First american cancer society award lecture on cancer epidemiology and prevention. Cancer Res. 1992, 52, 6735–6740.
[118]
Rad, R.; Gerhard, M.; Lang, R.; Sch?niger, M.; R?sch, T.; Schepp, W.; Becker, I.; Wagner, H.; Prinz, C. The Helicobacter pylori blood group antigen-binding adhesin facilitates bacterial colonization and augments a nonspecific immune response. J. Immunol. 2002, 168, 3033–3041.
[119]
Sheu, B.S.; Sheu, S.M.; Yang, H.B.; Huang, A.H.; Wu, J. Host gastric Lewis expression determines the bacterial density of Helicobacter pylori in babA2 genopositive infection. Gut 2003, 52, 927–932, doi:10.1136/gut.52.7.927.
[120]
Marionneau, S.; Cailleau-Thomas, A.; Rocher, J.; Le Moullac-Vaidye, B.; Ruvo?n, N.; Clément, M.; Le Pendu, J. ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 2001, 83, 565–573, doi:10.1016/S0300-9084(01)01321-9.
[121]
Lindén, S.; Mahdavi, J.; Semino-Mora, C.; Oslen, C.; Carlstedt, I.; Borén, T.; Dubois, A. Role of ABO secretor status in mucosal innate immunity and H. pylori infection. PLoS Pathog. 2008, 4, e2, doi:10.1371/journal.ppat.0040002.
[122]
Murata-Kamiya, N. Pathophysiological functions of the CagA oncoprotein during infection by Helicobacter pylori. Microbes Infect. 2011, 13, 799–807, doi:10.1016/j.micinf.2011.03.011.
[123]
Hatakeyama, M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat. Rev. Cancer 2004, 4, 688–694, doi:10.1038/nrc1433.
[124]
Zambon, C.F.; Navaglia, F.; Basso, D.; Rugge, M.; Plebani, M. Helicobacter pylori babA2, cagA, and s1 vacA genes work synergistically in causing intestinal metaplasia. J. Clin. Pathol. 2003, 56, 287–291, doi:10.1136/jcp.56.4.287.
[125]
Olfat, F.O.; Zheng, Q.; Oleastro, M.; Voland, P.; Borén, T.; Karttunen, R.; Engstrand, L.; Rad, R.; Prinz, C.; Gerhard, M. Correlation of the Helicobacter pylori adherence factor BabA with duodenal ulcer disease in four European countries. Fems Immunol. Med. Microbiol. 2005, 44, 151–156, doi:10.1016/j.femsim.2004.10.010.
[126]
Skoog, E.; Sj?ling, ?.; Navabi, N.; Holgersson, J.; Lundin, S.B.; Lindén, S.K. Human gastric mucins differently regulate Helicobacter pylori proliferation, gene expression and interactions with host cells. PLoS One 2012, 7, e36378.
[127]
Guruge, J.L.; Falk, P.G.; Lorenz, R.G.; Dans, M.; Wirth, H.P.; Blaser, M.J.; Berg, D.E.; Gordon, J.I. Epithelial attachment alters the outcome of Helicobacter pylori infection. Proc. Natl. Acad. Sci. USA 1998, 95, 3925–3930, doi:10.1073/pnas.95.7.3925.