Outer membrane protein expression profile in Helicobacter pylori clinical isolates

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 3782-3790

  Odenbreit, Stefan ^a   Swoboda, Kirstin ^a   Barwig, Iris ^a   Ruhl, Stefan ^b   Borén, Thomas ^c   Koletzko, Sibylle ^d   Haas, Rainer ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY AT BUFFALO   (United States)

^c UMEÅ UNIVERSITY   (Sweden)

^d LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CAGA PROTEIN; INTERLEUKIN 8; OUTER MEMBRANE PROTEIN; PROTEIN ALPA; PROTEIN ALPB; UNCLASSIFIED DRUG;

ALPA GENE; ALPB GENE; ARTICLE; BABA GENE; BABC GENE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; GENE EXPRESSION; HELICOBACTER PYLORI; HOPM GENE; NONHUMAN; OIPA GENE; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN EXPRESSION; SABA GENE;

ADHESINS, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CELL LINE, TUMOR; COLLAGEN TYPE IV; HELICOBACTER PYLORI; HUMANS; INTERLEUKIN-8; STOMACH;

EID: 69049106524     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00364-09     Document Type: Article

References (53)

1. Alm, R. A., J. Bina, B. M. Andrews, P. Doig, R. E. Hancock, and T. J. Trust. 2000. Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect. Immun. 68:4155-4168.
2. Alm, R. A., L. S. Ling, D. T. Moir, B. L. King, E. D. Brown, P. C. Doig, D. R. Smith, B. Noonan, B. C. Guild, B. L. deJonge, G. Carmel, P. J. Tummino, A. Caruso, M. Uria-Nickelsen, D. M. Mills, C. Ives, R. Gibson, D. Merberg, S. D. Mills, Q. Jiang, D. E. Taylor, G. F. Vovis, and T. J. Trust. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
3. Aspholm, M., A. Kalia, S. Ruhl, S. Schedin, A. Arnqvist, S. Linden, R. Sjostrom, M. Gerhard, C. Semino-Mora, A. Dubois, M. Unemo, D. Danielsson, S. Teneberg, W. K. Lee, D. E. Berg, and T. Boren. 2006. Helicobacter pylori adhesion to carbohydrates. Methods Enzymol. 417:293-339.
4. Aspholm, M., F. O. Olfat, J. Norden, B. Sonden, C. Lundberg, R. Sjostrom, S. Altraja, S. Odenbreit, R. Haas, T. Wadstrom, L. Engstrand, C. Semino-Mora, H. Liu, A. Dubois, S. Teneberg, A. Arnqvist, and T. Boren. 2006. SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog. 2:e110.
5. Aspholm-Hurtig, M., G. Dailide, M. Lahmann, A. Kalia, D. Ilver, N. Roche, S. Vikstrom, R. Sjostrom, S. Linden, A. Backstrom, C. Lundberg, A. Arnqvist, J. Mahdavi, U. J. Nilsson, B. Velapatino, R. H. Gilman, M. Gerhard, T. Alarcon, M. Lopez-Brea, T. Nakazawa, J. G. Fox, P. Correa, M. G. Dominguez-Bello, G. I. Perez-Perez, M. J. Blaser, S. Normark, I. Carlstedt, S. Oscarson, S. Teneberg, D. E. Berg, and T. Boren. 2004. Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 305:519-522.
6. Backstrom, A., C. Lundberg, D. Kersulyte, D. E. Berg, T. Boren, and A. Arnqvist. 2004. Metastability of Helicobacter pylori bab adhesin genes and dynamics in Lewis b antigen binding. Proc. Natl. Acad. Sci. USA 101:16923-16928.
7. Blaser, M. J., and D. Kirschner. 1999. Dynamics of Helicobacter pylori colonization in relation to the host response. Proc. Natl. Acad. Sci. USA 96:8359-8364.
8. Bouvier, M., C. M. Sharma, F. Mika, K. H. Nierhaus, and J. Vogel. 2008. Small RNA binding to 5-mRNA coding region inhibits translational initiation. Mol. Cell 32:827-837.
9. Brandt, S., T. Kwok, R. Hartig, W. König, and S. Backert. 2005. NF-κB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc. Natl. Acad. Sci. USA 102:9300-9305.
10. Cao, P., K. J. Lee, M. J. Blaser, and T. L. Cover. 2005. Analysis of hopQ alleles in East Asian and Western strains of Helicobacter pylori. FEMS Microbiol. Lett. 251:37-43.
11. Censini, S., C. Lange, Z. Y. Xiang, J. E. Crabtree, P. Ghiara, M. Borodovsky, R. Rappuoli, and A. Covacci. 1996. Cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93:14648-14653.
12. Colbeck, J. C., L. M. Hansen, J. M. Fong, and J. V. Solnick. 2006. Genotypic profile of the outer membrane proteins BabA and BabB in clinical isolates of Helicobacter pylori. Infect. Immun. 74:4375-4378.
13. Dossumbekova, A., C. Prinz, J. Mages, R. Lang, J. G. Kusters, A. H. van Vliet, W. Reindl, S. Backert, D. Saur, R. M. Schmid, and R. Rad. 2006. Helicobacter pylori HopH (OipA) and bacterial pathogenicity: genetic and functional genomic analysis of hopH gene polymorphisms. J. Infect. Dis. 194:1346-1355.
14. Fischer, W., J. Püls, R. Buhrdorf, B. Gebert, S. Odenbreit, and R. Haas. 2001. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol. Microbiol. 42:1337-1348.
15. Fleiss, J. L. 1981. Statistical methods for rates and proportions, 2nd ed., p. 59-60. John Wiley & Sons, Inc., New York, NY.
16. Fujimoto, S., O. O. Olaniyi, A. Arnqvist, J. Y. Wu, S. Odenbreit, R. Haas, D. Y. Graham, and Y. Yamaoka. 2007. Helicobacter pylori BabA expression, gastric mucosal injury, and clinical outcome. Clin. Gastroenterol. Hepatol. 5:49-58.
17. Gerhard, M., S. Hirno, T. Wadström, H. Miller-Podraza, S. Teneberg, K.-A. Karlsson, B. Appelmelk, S. Odenbreit, R. Haas, A. Arnquvist, and T. Borén. 2001. Helicobacter pylori, an adherent pain in the stomach, p. 185-206. In S. S. M. Achtman (ed.), Helicobacter pylori: molecular and cellular biology, 1st ed. Horizon Scientific Press, Wymondham, United Kingdom.
18. Gerhard, M., N. Lehn, N. Neumayer, T. Boren, R. Rad, W. Schepp, S. Miehlke, M. Classen, and C. Prinz. 1999. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc. Natl. Acad. Sci. USA 96:12778-12783.
19. Goodwin, A. C., D. M. Weinberger, C. B. Ford, J. C. Nelson, J. D. Snider, J. D. Hall, C. I. Paules, R. M. Peek, Jr., and M. H. Forsyth. 2008. Expression of the Helicobacter pylori adhesin SabA is controlled via phase variation and the ArsRS signal transduction system. Microbiology 154:2231-2240.
20. Haas, R., T. F. Meyer, and J. P. M. van Putten. 1993. Aflagellated mutants of Helicobacter pylori generated by genetic transformation of naturally competent strains using transposon shuttle mutagenesis. Mol. Microbiol. 8:753-760.
21. Hennig, E. E., R. Mernaugh, J. Edl, P. Cao, and T. L. Cover. 2004. Heterogeneity among Helicobacter pylori strains in expression of the outer membrane protein BabA. Infect. Immun. 72:3429-3435.
22. Hessey, S. J., J. Spencer, J. I. Wyatt, G. Sobala, B. J. Rathbone, A. T. R. Axon, and M. F. Dixon. 1990. Bacterial adhesion and disease activity in Helicobacter associated chronic gastritis. Gut 31:134-138.
23. Ilver, D., A. Arnqvist, J. Ogren, I. M. Frick, D. Kersulyte, E. T. Incecik, D. E. Berg, A. Covacci, L. Engstrand, and T. Borén. 1998. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279:373-377.
24. Kirschner, D. E., and M. J. Blaser. 1995. The dynamics of Helicobacter pylori infection of the human stomach. J. Theor. Biol. 176:281-290.
25. Kizuka, Y., K. Kobayashi, S. Kakuda, Y. Nakajima, S. Itoh, N. Kawasaki, and S. Oka. 2008. Laminin-1 is a novel carrier glycoprotein for the nonsulfated HNK-1 epitope in mouse kidney. Glycobiology 18:331-338.
26. Kudo, T., Z. Z. Nurgalieva, M. E. Conner, S. Crawford, S. Odenbreit, R. Haas, D. Y. Graham, and Y. Yamaoka. 2004. Correlation between Helicobacter pylori OipA protein expression and oipA gene switch status. J. Clin. Microbiol. 42:2279-2281.
27. Loh, J. T., V. J. Torres, H. M. Algood, M. S. McClain, and T. L. Cover. 2008. Helicobacter pylori HopQ outer membrane protein attenuates bacterial adherence to gastric epithelial cells. FEMS Microbiol. Lett. 289:53-58.
28. Lu, H., J. Y. Wu, E. J. Beswick, T. Ohno, S. Odenbreit, R. Haas, V. E. Reyes, M. Kita, D. Y. Graham, and Y. Yamaoka. 2007. Functional and intracellular signaling differences associated with the Helicobacter pylori AlpAB adhesin from Western and East Asian strains. J. Biol. Chem. 282:6242-6254.
29. Mahdavi, J., B. Sonden, M. Hurtig, F. O. Olfat, L. Forsberg, N. Roche, J. Angstrom, T. Larsson, S. Teneberg, K. A. Karlsson, S. Altraja, T. Wadström, D. Kersulyte, D. E. Berg, A. Dubois, C. Petersson, K. E. Magnusson, T. Norberg, F. Lindh, B. B. Lundskog, A. Arnqvist, L. Hammarstrom, and T. Borén. 2002. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297:573-578.
30. Odenbreit, S. 2005. Adherence properties of Helicobacter pylori: impact on pathogenesis and adaptation to the host. Int. J. Med. Microbiol. 295:317-324.
31. Odenbreit, S., G. Faller, and R. Haas. 2002. Role of the alpAB proteins and lipopolysaccharide in adhesion of Helicobacter pylori to human gastric tissue. Int. J. Med. Microbiol. 292:247-256.
32. Odenbreit, S., and R. Haas. 2002. Helicobacter pylori: impact of gene transfer and the role of the cag pathogenicity island for host adaptation and virulence. Curr. Top. Microbiol. Immunol. 264:1-22.
33. Odenbreit, S., H. Kavermann, J. Puls, and R. Haas. 2002. CagA tyrosine phosphorylation and interleukin-8 induction by Helicobacter pylori are independent from alpAB, HopZ and bab group outer membrane proteins. Int. J. Med. Microbiol. 292:257-266.
34. Odenbreit, S., J. Püls, B. Sedlmaier, E. Gerland, W. Fischer, and R. Haas. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287:1497-1500.
35. Odenbreit, S., M. Till, and R. Haas. 1996. Optimized BlaM-transposon shuttle mutagenesis of Helicobacter pylori allows the identification of novel genetic loci involved in bacterial virulence. Mol. Microbiol. 20:361-373.
36. Odenbreit, S., M. Till, D. Hofreuter, G. Faller, and R. Haas. 1999. Genetic and functional characterisation of the alpAB gene locus essential for adhesion of Helicobacter pylori to human gastric tissue. Mol. Microbiol. 31:1537-1548.
37. Pohlner, J., J. Krämer, and T. F. Meyer. 1993. A plasmid system for highlevel expression and in vitro processing of recombinant proteins. Gene 130:121-126.
38. Pride, D. T., R. J. Meinersmann, and M. J. Blaser. 2001. Allelic variation within Helicobacter pylori babA and babB. Infect. Immun. 69:1160-1171.
39. Schulte, R., and I. B. Autenrieth. 1998. Yersinia enterocolitica-induced interleukin-8 secretion by human intestinal epithelial cells depends on cell differentiation. Infect. Immun. 66:1216-1224.
40. Sheu, B. S., S. Odenbreit, K. H. Hung, C. P. Liu, S. M. Sheu, H. B. Yang, and J. J. Wu. 2006. 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. 101:36-44.
41. Sheu, B. S., S. M. Sheu, H. B. Yang, A. H. Huang, and J. J. Wu. 2003. Host gastric Lewis expression determines the bacterial density of Helicobacter pylori in babA2 genopositive infection. Gut 52:927-932.
42. Solnick, J. V., L. M. Hansen, N. R. Salama, J. K. Boonjakuakul, and M. Syvanen. 2004. Modification of Helicobacter pylori outer membrane protein expression during experimental infection of rhesus macaques. Proc. Natl. Acad. Sci. USA 101:2106-2111.
43. Stern, A., M. Brown, P. Nickel, and T. F. Meyer. 1986. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47:61-71.
44. Suerbaum, S., and C. Josenhans. 2007. Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat. Rev. Microbiol. 5:441-452.
45. Suerbaum, S., and P. Michetti. 2002. Helicobacter pylori infection. N. Engl. J. Med. 347:1175-1186.
46. Suerbaum, S., J. M. Smith, K. Bapumia, G. Morelli, J. M. Smith, E. Kunstmann, I. Dyrek, and M. Achtman. 1998. Free recombination within Helicobacter pylori. Proc. Natl. Acad. Sci. USA 95:12619-12624.
47. Tomb, J.-F., O. White, A. R. Kerlavage, R. A. Clayton, G. G. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quakenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G. Khalak, A. Glodek, K. McKenney, L. M. Fitzegerald, N. Lee, M. D. Adams, E. K. Hickey, D. E. Berg, J. D. Gocayne, T. R. Utterback, J. D. Peterson, J. M. Kelley, M. D. Cotton, J. M. Weidman, C. Fujii, C. Bowman, L. Watthey, E. Wallin, W. S. Hayes, M. Borodovsky, P. D. Karp, H. O. Smith, C. M. Fraser, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
48. Trust, T. J., P. Doig, L. Emody, Z. Kienle, T. Wadström, and P. O'Toole. 1991. High-affinity binding of the basement membrane proteins collagen type IV and laminin to the gastric pathogen Helicobacter pylori. Infect. Immun. 59:4398-4404.
49. Walz, A., S. Odenbreit, J. Mahdavi, T. Boren, and S. Ruhl. 2005. Identifi-cation and characterization of binding properties of Helicobacter pylori by glycoconjugate arrays. Glycobiology 15:700-708.
50. Wang, G., M. Z. Humayun, and D. E. Taylor. 1999. Mutation as an origin of genetic variability in Helicobacter pylori. Trends Microbiol. 7:488-493.
51. Yamaoka, Y., S. Kikuchi, H. M. el Zimaity, O. Gutierrez, M. S. Osato, and D. Y. Graham. 2002. Importance of Helicobacter pylori oipA in clinical presentation, gastric inflammation, and mucosal interleukin 8 production. Gastroenterology 123:414-424.
52. Yamaoka, Y., D. H. Kwon, and D. Y. Graham. 2000. A M(r) 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc. Natl. Acad. Sci. USA 97:7533-7538.
53. Yamaoka, Y., J. Souchek, S. Odenbreit, R. Haas, A. Arnqvist, T. Boren, T. Kodama, M. S. Osato, O. Gutierrez, J. G. Kim, and D. Y. Graham. 2002. Discrimination between cases of duodenal ulcer and gastritis on the basis of putative virulence factors of Helicobacter pylori. J. Clin. Microbiol. 40:2244-2246.