Expression of Helicobacter pylori virulence factors and associated expression profiles of inflammatory genes in the human gastric mucosa

Infection and Immunity

Volumn 75, Issue 11, 2007, Pages 5118-5126

  Wen, Sicheng ^a   Velin, Dominique ^b   Felley, Christian P ^b   Du, Likun ^a   Michetti, Pierre ^b   Pan Hammarström, Qiang ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BABA2 PROTEIN; CAGA PROTEIN; CELL ADHESION MOLECULE; UNCLASSIFIED DRUG; VACAS1 PROTEIN; VACAS2 PROTEIN; VACUOLATING TOXIN; VIRULENCE FACTOR;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE EXPRESSION; HELICOBACTER PYLORI; HUMAN; HUMAN TISSUE; INFLAMMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH ANTRUM; STOMACH MUCOSA;

ADHESINS, BACTERIAL; ADULT; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CYTOKINES; GASTRIC MUCOSA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MIDDLE AGED; VIRULENCE FACTORS;

EID: 35648982933     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00334-07     Document Type: Article

References (55)

1. 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.
2. Atherton, J. C., R. M. Peek, Jr., K. T. Tham, T. L. Cover, and M. J. Blaser. 1997. Clinical and pathological importance of heterogeneity in vacA, the vacuolating cytotoxin gene of Helicobacter pylori. Gastroenterology 112:92-99.
3. Audibert, C., B. Janvier, B. Grignon, L. Salaun, C. Burucoa, J. C. Lecron, and J. L. Fauchere. 2000. Correlation between IL-8 induction, cagA status and vacA genotypes in 153 French Helicobacter pylori isolates. Res. Microbiol. 151:191-200.
4. Basso, D., and M. Plebani. 2004. H. pylori infection: bacterial virulence factors and cytokine gene polymorphisms as determinants of infection outcome. Crit. Rev. Clin. Lab. Sci. 41:313-337.
5. Blaser, M. J., G. I. Perez-Perez, H. Kleanthous, T. L. Cover, R. M. Peek, P. H. Chyou, G. N. Stemmermann, and A. Nomura. 1995. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 55:2111-2115.
6. Boren, T., P. Falk, K. A. Roth, G. Larson, and S. Normark. 1993. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262:1892-1895.
7. Boren, T., S. Normark, and P. Falk. 1994. Helicobacter pylori: molecular basis for host recognition and bacterial adherence. Trends Microbiol. 2:221-228.
8. Censini, S., C. Lange, Z. Xiang, J. E. Crabtree, P. Ghiara, M. Borodovsky, R. Rappuoli, and A. Covacci. 1996. cag, a pathogenicity island of Helicobacter pylori, encodes type 1-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93:14648-14653.
9. 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.
10. Crabtree, J. E., A. Covacci, S. M. Farmery, Z. Xiang, D. S. Tompkins, S. Perry, I. J. Lindley, and R. Rappuoli. 1995. Helicobacter pylori induced interleukin-8 expression in gastric epithelial cells is associated with CagA positive phenotype. J. Clin. Pathol. 48:41-45.
11. Crabtree, J. E., Z. Xiang, I. J. Lindley, O. S. Tompkins, R. Rappuoli, and A. Covacci. 1995. Induction of interleukin-8 secretion from gastric epithelial cells by a cagA negative isogenic mutant of Helicobacter pylori. J. Clin. Pathol. 48:967-969.
12. 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.
13. Eck, M., B. Schmausser, R. Haas, A. Greiner, S. Czub, and H. K. Muller-Hermelink. 1997. MALT-type lymphoma of the stomach is associated with Helicobacter pylori strains expressing the CagA protein. Gastroenterology 112:1482-1486.
14. Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95:14863-14868.
15. 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.
16. Graham, D. Y., R. M. Genta, D. P. Graham, and J. E. Crabtree. 1996. Serum CagA antibodies in asymptomatic subjects and patients with peptic ulcer: lack of correlation of IgG antibody in patients with peptic ulcer or asymptomatic Helicobacter pylori gastritis. J. Clin. Pathol. 49:829-832.
17. Hamlet, A., A. C. Thoreson, O. Nilsson, A. M. Svennerholm, and L. Olbe. 1999. Duodenal Helicobacter pylori infection differs in cagA genotype between asymptomatic subjects and patients with duodenal ulcers. Gastroenterology 116:259-268.
18. 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.
19. Ilver, D., A. Arnqvist, J. Ogren, I. M. Frick, D. Kersulyte, E. T. Incecik, D. E. Berg, A. Covacci, L. Engstrand, and T. Boren. 1998. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279:373-377.
20. Jenks, P. J., F. Megraud, and A. Labigne. 1998. Clinical outcome after infection with Helicobacter pylori does not appear to be reliably predicted by the presence of any of the genes of the cag pathogenicity island. Gut 43: 752-758.
21. Kim, J. M., J. S. Kim, H. C. Jung, I. S. Song, and C. Y. Kim. 2000. Virulence factors of Helicobacter pylori in Korean isolates do not influence proinflammatory cytokine gene expression and apoptosis in human gastric epithelial cells, nor do these factors influence the clinical outcome. J. Gastroenterol. 35:898-906.
22. Kranzer, K., L. Sollner, M. Aigner, N. Lehn, L. Demi, M. Rehli, and W. Schneider-Brachert. 2005. Impact of Helicobacter pylori virulence factors and compounds on activation and maturation of human dendritic cells. Infect. Immun. 73:4180-4189.
23. Kuipers, E. J., G. I. Perez-Perez, S. G. Meuwissen, and M. J. Blaser. 1995. Helicobacter pylori and atrophic gastritis: importance of the cagA status. J. Natl. Cancer Inst. 87:1777-1780.
24. Lim, C. Y., K. H. Lee, M. J. Cho, M. W. Chang, S. Y. Kim, N. H. Myong, W. K. Lee, K. H. Rhee, and Y. H. Kook. 2003. Detection of Helicobacter pylori in gastric mucosa of patients with gastroduodenal diseases by PCR-restriction analysis using the RNA polymerase gene (rpoB). J. Clin. Microbiol. 41:3387-3391.
25. Loeb, M., P. Jayaratne, N. Jones, A. Sihoe, and P. Sherman. 1998. Lack of correlation between vacuolating cytotoxin activity, cagA gene in Helicobacter pylori, and peptic ulcer disease in children. Eur. J. Clin. Microbiol. Infect. Dis. 17:653-656.
26. Lunet, N., and H. Barros. 2003. Helicobacter pylori infection and gastric cancer: facing the enigmas. Int. J. Cancer. 106:953-960.
27. Machida-Montani, A., S. Sasazuki, M. Inoue, S. Natsukawa, K. Shaura, Y. Koizumi, Y. Kasuga, T. Hanaoka, and S. Tsugane. 2004. Association of Helicobacter pylori infection and environmental factors in non-cardia gastric cancer in Japan. Gastric Cancer 7:46-53.
28. Mattar, R., A. F. dos Santos, J. N. Eisig, T. N. Rodrigues, F. M. Silva, R. M. Lupinacci, K. Iriya, and F. J. Carrilho. 2005. No correlation of babA2 with vacA and cagA genotypes of Helicobacter pylori and grading of gastritis from peptic ulcer disease patients in Brazil. Helicobacter 10:601-608.
29. Mizushima, T., T. Sugiyama, Y. Komatsu, J. Ishizuka, M. Kato, and M. Asaka. 2001. Clinical relevance of the babA2 genotype of Helicobacter pylori in Japanese clinical isolates. J. Clin. Microbiol. 39:2463-2465.
30. Odenhreit, S., J. Puis, 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.
31. Olfat, F. O., Q. Zheng, M. Oleastro, P. Voland, T. Boren, R. Karttunen, L. Engstrand, R. Rad, C. Prinz, and M. Gerhard. 2005. Correlation of the Helicobacter pylori adherence factor BabA with duodenal ulcer disease in four European countries. FEMS Immunol. Med. Microbiol. 44:151-156.
32. Pan-Hammarstrom, Q., S. Wen, and L. Hammarstrom. 2006. Cytokine gene expression profiles in human lymphocytes induced by a formula of traditional Chinese medicine, vigconic VI-28. J. Interferon Cytokine Res. 26:628-636.
33. + strains and dissociation of gastric epithelial cell proliferation from apoptosis. J. Natl. Cancer Inst. 89:863-868.
34. Pride, D. T., R. J. Meinersmann, and M. J. Blaser. 2001. Allelic variation within Helicobacter pylori babA and babB. Infect. Immun. 69:1160-1171.
35. Prinz, C., M. Schoniger, R. Rad, I. Becker, E. Keiditsch, S. Wagenpfeil, M. Classen, T. Roseh, W. Schepp, and M. Gerhard. 2001. Key importance of the Helicobacter pylori adherence factor blood group antigen binding adhesin during chronic gastric inflammation. Cancer Res. 61:1903-1909.
36. Rad, R., M. Gerhard, R. Lang, M. Schoniger, T. Rosch, W. Schepp, I. Becker, H. Wagner, and C. Prinz. 2002. The Helicobacter pylori blood group antigen-binding adhesin facilitates bacterial colonization and augments a non-specific immune response. J. Immunol. 168:3033-3041.
37. Rudi, J., C. Kolb, M. Maiwald, D. Kuck, A. Sieg, P. R. Galle, and W. Stremmel. 1998. Diversity of Helicobacter pylori vacA and cagA genes and relationship to VacA and CagA protein expression, cytotoxin production, and associated diseases. J. Clin. Microbiol. 36:944-948.
38. Segal, E. D., C. Lange, A. Covacci, L. S. Tompkins, and S. Falkow. 1997. Induction of host signal transduction pathways by Helicobacter pylori. Proc. Natl. Acad. Sci. USA 94:7595-7599.
39. Sharma, S. A., M. K. Tummuru, G. G. Miller, and M. J. Blaser. 1995. Interleukin-8 response of gastric epithelial cell lines to Helicobacter pylori stimulation in vitro. Infect. Immun. 63:1681-1687.
40. Shimoyama, T., S. M. Everett, M. F. Dixon, A. T. Axon, and J. E. Crabtree. 1998. Chemokine mRNA expression in gastric mucosa is associated with Helicobacter pylori cagA positivity and severity of gastritis. J. Clin. Pathol. 51:765-770.
41. Smoot, D. T., J. H. Resau, M. H. Earlington, M. Simpson, and T. L. Cover. 1996. Effects of Helicobacter pylori vacuolating cytotoxin on primary cultures of human gastric epithelial cells. Gut 39:795-799.
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. Suerbaum, S., and P. Michetti. 2002. Helicobacter pylori infection. N. Engl. J. Med. 347:1175-1186.
44. Weel, J. F., R. W. van der Hulst, Y. Gerrits, P. Roorda, M. Feller, J. Dankert, G. N. Tytgat, and A. van der Ende. 1996. The interrelationship between cytotoxin-associated gene A, vacuolating cytotoxin, and Helicobacter pylori-related diseases. J. Infect. Dis. 173:1171-1175.
45. Wen, S., C. P. Felley, H. Bouzourene, M. Reimers, P. Michetti, and Q. Pan-Hammarstrom. 2004. Inflammatory gene profiles in gastric mucosa during Helicobacter pylori infection in humans. J. Immunol. 172:2595-2606.
46. Xiang, Z., S. Censini, P. F. Bayeli, J. L. Telford, N. Figura, R. Rappuoli, and A. Covacci. 1995. Analysis of expression of CagA and VacA virulence factors in 43 strains of Helicobacter pylori reveals that clinical isolates can be divided into two major types and that CagA is not necessary for expression of the vacuolating cytotoxin. Infect. Immun. 63:94-98.
47. 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.
48. Yamaoka, Y., M. Kita, T. Kodama, N. Sawai, and J. Imanishi. 1996. Helicobacter pylori cagA gene and expression of cytokine messenger RNA in gastric mucosa. Gastroenterology 110:1744-1752.
49. Yamaoka, Y., M. Kita, T. Kodama, N. Sawai, K. Kashima, and J. Imanishi. 1997. Induction of various cytokines and development of severe mucosal inflammation by cagA gene positive Helicobacter pylori strains. Gut 41:442-451.
50. Yamaoka, Y., M. Kita, T. Kodama, N. Sawai, T. Tanahashi, K. Kashima, and J. Imanishi. 1998. Chemokines in the gastric mucosa in Helicobacter pylori infection. Gut 42:609-617.
51. Yamaoka, Y., T. Kodama, O. Gutierrez, J. G. Kim, K. Kashima, and D. Y. Graham. 1999. Relationship between Helicobacter pylori iceA, cagA, and vacA status and clinical outcome: studies in four different countries. J. Clin. Microbiol. 37:2274-2279.
52. Yamaoka, Y., T. Kodama, M. Kita, J. Imanishi, K. Kashima, and D. Y. Graham. 1998. Relationship of vacA genotypes of Helicobacter pylori to cagA status, cytotoxin production, and clinical outcome. Helicobacter 3:241-253.
53. r 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc. Natl. Acad. Sci. USA 97:7533-7538.
54. 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.
55. Zambon, C. F., F. Navaglia, D. Basso, M. Rugge, and M. Plebani. 2003. Helicobacter pylori babA2, cagA, and s1 vacA genes work synergistically in causing intestinal metaplasia. J. Clin. Pathol. 56:287-291.