The role of Helicobacter pylori outer membrane proteins in adherence and pathogenesis

Biology

Volumn 2, Issue 3, 2013, Pages 1110-1134

  Oleastro, Mónica ^a   Ménard, Armelle ^b,c  

^a NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^b INSERM   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Adhesin; Bacterial adherence; Gastric disease; Lewis antigen; Outer membrane protein; Receptor; Virulence

Indexed keywords

EID: 84901301963     PISSN: None     EISSN: 20797737     Source Type: Journal    
DOI: 10.3390/biology2031110     Document Type: Review

References (127)

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.
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.
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.
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.
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.
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.
9. Suerbaum, S.; Achtman, M. Evolution of Helicobacter pylori: The role of recombination. Trends Microbiol. 1999, 7, 182-184.
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.
12. Suerbaum, S.; Josenhans, C. Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat. Rev. Microbiol. 2007, 5, 441-452.
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.
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.; Höök-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.
15. Muotiala, A.; Helander, I.M.; Pyhala, L.; Kosunen, T.U.; Moran, A.P. Low biological activity of Helicobacter pylori lipopolysaccharide. Infect. Immun. 1992, 60, 1714-1716.
16. Monteiro, M.A.; Appelmelk, B.J.; Rasko, D.A.; Moran, A.P.; Hynes, S.O.; MacLean, L.L.; Chan, K.H.; Michael, F.S.; Logan, S.M.; O'Rourke, J.; et al. Lipopolysaccharide structures of Helicobacter pylori genomic strains 26695 and J99, mouse model H-pylori Sydney strain, H-pylori P466 carrying sialyl Lewis X, and H-pylori UA915 expressing Lewis B-Classification of H-pylori lipopolysaccharides into glycotype families. Eur. J. Biochem. 2000, 267, 305-320.
17. Appelmelk, B.J.; Shiberu, B.; Trinks, C.; Tapsi, N.; Zheng, P.Y.; Verboom, T.; Maaskant, J.; Hokke, C.H.; Schiphorst, W.E.; Blanchard, D.; et al. Phase variation in Helicobacter pylori lipopolysaccharide. Infect. Immun. 1998, 66, 70-76.
18. 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.
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.
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.
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.
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.
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.
27. Ilver, D.; Arnqvist, A.; Ögren, J.; Frick, I.M.; Kersulyte, D.; Incecik, E.T.; Berg, D.E.; Covacci, A.; Engstrand, L.; Borén, T. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1998, 279, 373-377.
28. Mahdavi, J.; Sonden, B.; Hurtig, M.; Olfat, F.O.; Forsberg, L.; Roche, N.; Ǎngström, 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.
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.
30. Yamaoka, Y. Roles of Helicobacter pylori BabA in gastroduodenal pathogenesis. World J. Gastroenterol. 2008, 14, 4265-4272.
31. Moore, M.; Borén, T.; Solnick, J. Life at the margins: Modulation of attachment proteins in Helicobacter pylori. Gut Microbes 2011, 2, 42-46.
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.; Vikström, S.; Lindén, S.; Bäckström, A.; Lundberg, C.; et al. Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 2004, 305, 519-522.
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.; Ångström, 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.
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.
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.
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.
40. Aspholm, M.; Olfat, F.O.; Nordén, J.; Sondén, B.; Lundberg, C.; Sjöström, R.; Altraja, S.; Odenbreit, S.; Haas, R.; Wadström, T.; et al. SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog. 2006, 2, e110.
41. Unemo, M.; Aspholm-Hurtig, M.; Ilver, D.; Bergström, 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.
43. 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, 79, 3106-3116.
44. Pride, D.T.; Blaser, M.J. Concerted evolution between duplicated genetic elements in Helicobacter pylori. J. Mol. Biol. 2002, 316, 629-642.
45. Pride, D.T.; Meinersmann, R.J.; Blaser, M.J. Allelic variation within Helicobacter pylori babA and babB. Infect. Immun. 2001, 69, 1160-1171.
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.
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.
51. Ohno, T.; Vallström, 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.
52. Hennig, E.; Allen, J.; Cover, T. Multiple chromosomal loci for the babA gene in Helicobacter pylori. Infect. Immun. 2006, 74, 3046-3051.
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.
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.
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.
56. Fujimoto, S.; Olaniyi, O.O.; Arnqvist, A.; Wu, J.Y.; Odenbreit, S.; Haas, R.; Graham, D.Y.; Yamaoka, Y. Helicobacter pylori BabA expression, gastric mucosal injury, and clinical outcome. Clin. Gastroenterol. Hepatol. 2007, 5, 49-58.
57. Azevedo, M.; Eriksson, S.; Mendes, N.; Serpa, J.; Figueiredo, C.; Resende, L.P.; Ruvoën-Clouet, N.; Haas, R.; Borën, 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.
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.
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.
60. Talarico, S.; Whitefield, S.E.; Fero, J.; Haas, R.; Salama, N.R. Regulation of Helicobacter pylori adherence by gene conversion. Mol. Microbiol. 2012, 84, 1050-1061.
61. Yamaoka, Y.; Kita, M.; Kodama, T.; Imamura, S.; Ohno, T.; Sawai, N.; Ishimaru, A.; Imanishi, J.; Graham, D.Y. Helicobacter pylori infection in mice: Role of outer membrane proteins in colonization and inflammation. Gastroenterology 2002, 123, 1992-2004.
62. Loh, J.T.; Torres, V.J.; Algood, H.M.; McClain, M.S.; Cover, T.L. Helicobacter pylori HopQ outer membrane protein attenuates bacterial adherence to gastric epithelial cells. FEMS Microbiol. Lett. 2008, 289, 53-58.
63. 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, 71, 3529-3539.
64. Yamaoka, Y.; Ojo, O.; Fujimoto, S.; Odenbreit, S.; Haas, R.; Gutierrez, O.; El-Zimaity, H.M.T.; Reddy, R.; Arnqvist, A.; Graham, D.Y. Helicobacter pylori outer membrane proteins and gastroduodenal disease. Gut 2006, 55, 775-781.
65. 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.
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.
68. Marcos, N.T.; Magalhães, 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.
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.
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.
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.
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.
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.
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.
81. Yamaoka, Y.; Kikuchi, S.; El-Zimaity, H.M.T.; 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, 123, 414-424.
82. 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.
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.
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.
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.
86. Saunders, N.J.; Peden, J.F.; Hood, D.W.; Moxon, E.R. Simple sequence repeats in the Helicobacter pylori genome. Mol. Microbiol. 1998, 27, 1091-1098.
87. 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.
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.
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.
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.
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.
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.
93. 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, 284, 30383-30394.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
108. Morris, A.; Nicholson, G.; Zwi, J.; Vanderwee, M. Campylobacter pylori infection in Meckel's diverticula containing gastric mucosa. Gut 1989, 30, 1233-1235.
109. Kestemberg, A.; Mariño, 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.
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.
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.
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.
116. Magalhães, 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.
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.; Schöniger, M.; Rösch, 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.
120. Marionneau, S.; Cailleau-Thomas, A.; Rocher, J.; Le Moullac-Vaidye, B.; Ruvoën, 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.
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.
122. Murata-Kamiya, N. Pathophysiological functions of the CagA oncoprotein during infection by Helicobacter pylori. Microbes Infect. 2011, 13, 799-807.
123. Hatakeyama, M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat. Rev. Cancer 2004, 4, 688-694.
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.
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.
126. Skoog, E.; Sjöling, Å.; 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.