Helicobacter pylori outer membrane vesicles modulate proliferation and interleukin-8 production by gastric epithelial cells

Infection and Immunity

Volumn 71, Issue 10, 2003, Pages 5670-5675

  Ismail, Salim ^a   Hampton, Mark B ^a   Keenan, Jacqueline I ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; INTERLEUKIN 8; VIRULENCE FACTOR;

ARTICLE; BACTERIAL OUTER MEMBRANE; CELL PROLIFERATION; CELL VACUOLE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; GASTRITIS; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MEMBRANE VESICLE; PRIORITY JOURNAL; STOMACH EPITHELIUM;

CELL DIVISION; CELL LINE; CELL MEMBRANE; EPITHELIAL CELLS; GASTRITIS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; INTERLEUKIN-8; STOMACH; VIRULENCE;

EID: 0141780971     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.10.5670-5675.2003     Document Type: Article

References (68)

1. Aihara, M., D. Tsuchimoto, H. Takizawa, A. Azuma, H. Wakebe, Y. Ohmoto, K. Imagawa, M. Kikuchi, N. Mukaida, and K. Matsushima: 1997. Mechanisms involved in Helicobacter pylori-induced interleukin-8 production by a gastric cancer cell line, MKN45. Infect. Immun. 65:3218-3224.
2. Ando, T., R. M. Peek, Jr., Y. C. Lee, U. Krishna, K. Kusugami, and M. J. Blaser. 2002. Host cell responses to genotypically similar Helicobacter pylori isolates from United States and Japan. Clin. Diagn. Lab. Immunol. 9:167-175.
3. Atherton, J. C., P. Cao, R. M. Peek, Jr., M. K. Tummuru, M. J. Blaser, and T. L. Cover. 1995. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vaca types with cytotoxin production and peptic ulceration. J. Biol. Chem. 270:17771-17777.
4. Backhed, F., B. Rokbi, E. Torstensson, Y. Zhao, C. Nilsson, D. Seguin, S. Normark, A. M. Buchan, and A. Richter-Dahlfors. 2003. Gastric mucosal recognition of Helicobacter pylori is independent of Toll-like receptor 4. J. Infect. Dis. 187:829-836.
5. Blaser, M. J. 1992. Helicobacter pylori: its role in disease. Clin. Infect. Dis. 15:386-391.
6. Blaser, M. J. 1995. The role of Helicobacter pylori in gastritis and its progression to peptic ulcer disease. Aliment. Pharmacol. Ther. 9:27-30.
7. Blaser, M. J., and D. E. Berg. 2001. Helicobacter pylori genetic diversity and risk of human disease. J. Clin. Investig. 107:767-773.
8. Blaser, M. J., and J. Parsonnet. 1994. Parasitism by the "slow" bacterium Helicobacter pylori leads to altered gastric homeostasis and neoplasia. J. Clin. Investig. 94:4-8.
9. Cario, E., and D. K. Podolsky. 2000. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect. Immun. 68:7010-7017.
10. 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 I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93:14648-14653.
11. Censini, S., M. Stein, and A. Covacci. 2001. Cellular responses induced after contact with Helicobacter pylori. Curr. Opin. Microbiol. 4:41-46.
12. Chensue, S. W. 2001. Molecular machinations: chemokine signals in host-pathogen interactions. Clin. Microbiol. Rev. 14:821-835.
13. Cover, T. L., P. Cao, C. D. Lind, K. T. Tham, and M. J. Blaser. 1993. Correlation between vacuolating cytotoxin production by Helicobacter pylori isolates in vitro and in vivo. Infect. Immun. 61:5008-5012.
14. Cover, T. L., C. P. Dooley, and M. J. Blaser. 1990. Characterization of and human serologic response to proteins in Helicobacter pylori broth culture supernatants with vacuolizing cytotoxin activity. Infect. Immun. 58:603-610.
15. Cover, T. L., U. S. Krishna, D. A. Israel, and R. M. Peek, Jr. 2003. Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res. 63:951-957.
16. Crabtree, J. E., Z. Xiang, I. J. Lindley, D. 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.
17. Fan, X. G., D. Kelleher, X. J. Fan, H. X. Xia, and P. W. Keeling. 1996. Helicobacter pylori increases proliferation of gastric epithelial cells. Gut 38:19-22.
18. Fiocca, R., V. Necchi, P. Sommi, V. Ricci, J. Telford, T. L. Cover, and E. Solcia. 1999. Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J. Pathol. 188:220-226.
19. Forsyth, M. H., J. C. Atherton, M. J. Blaser, and T. L. Cover. 1998. Heterogeneity in levels of vacuolating cytotoxin gene (vacA) transcription among Helicobacter pylori strains. Infect. Immun. 66:3088-3094.
20. Fujikawa, A., D. Shirasaka, S. Yamamoto, H. Ota, K. Yahiro, M. Fukada, T. Shintani, A. Wada, N. Aoyama, T. Hirayama, H. Fukamachi, and M. Noda. 2003. Mice deficient in protein tyrosine phosphatase receptor type Z are resistant to gastric ulcer induction by VacA of Helicobacter pylori. Nat. Genet. 33:375-381.
21. Galmiche, A., J. Rassow, A. Doye, S. Cagnol, J. C. Chambard, S. Contamin, V. de Thillot, I. Just, V. Ricci, E. Solcia, E. Van Obberghen, and P. Boquet. 2000. The N-terminal 34 kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release. EMBO J. 19:6361-6370.
22. Garner, J. A., and T. L. Cover. 1996. Binding and internalization of the Helicobacter pylori vacuolating cytotoxin by epithelial cells. Infect. Immun. 64:4197-4203.
23. Glocker, E., C. Lange, A. Covacci, S. Bereswill, M. Kist, and H. L. Pahl. 1998. Proteins encoded by the cag pathogenicity island of Helicobacter pylori are required for NF-κB activation. Infect. Immun. 66:2346-2348.
24. Guruge, J. L., P. G. Falk, R. G. Lorenz, M. Dans, H. P. Wirth, M. J. Blaser, D. E. Berg, and J. I. Gordon. 1998. Epithelial attachment alters the outcome of Helicobacter pylori infection. Proc. Natl. Acad. Sci. USA 95:3925-3930.
25. Huang, J., P. W. O'Toole, P. Doig, and T. J. Trust. 1995. Stimulation of interleukin-8 production in epithelial cell lines by Helicobacter pylori. Infect. Immun. 63:1732-1738.
26. 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.
27. Kassai, K., T. Yoshikawa, N. Yoshida, A. Hashiramoto, M. Kondo, and H. Murase. 1999. Helicobacter pylori water extract induces interleukin-8 production by gastric epithelial cells. Dig. Dis. Sci. 44:237-242.
28. Kawahara, T., Y. Kuwano, S. Teshima-Kondo, T. Kawai, T. Nikawa, K. Kishi, and K. Rokutan. 2001. Toll-like receptor 4 regulates gastric pit cell responses to Helicobacter pylori infection. J. Med. Investig. 48:190-197.
29. Keenan, J., T. Day, S. Neal, B. Cook, G. Perez-Perez, R. Allardyce, and P. Bagshaw. 2000. A role for the bacterial outer membrane in the pathogenesis of Helicobacter pylori infection. FEMS Microbiol. Lett. 182:259-264.
30. Keenan, J., J. Oliaro, N. Domigan, H. Potter, G. Aitken, R. Allardyce, and J. Roake. 2000. Immune response to an 18-kilodalton outer membrane antigen identifies lipoprotein 20 as a Helicobacter pylori vaccine candidate. Infect. Immun. 68:3337-3343.
31. Keenan, J. I., and R. A. Allardyce. 2000. Iron influences the expression of Helicobacter pylori outer membrane vesicle-associated virulence factors. Eur. J. Gastroenterol. Hepatol. 12:1267-1273.
32. Keenan, J. I., R. A. Allardyce, and P. F. Bagshaw. 1997. Dual silver staining to characterise Helicobacter spp. outer membrane components. J. Immunol. Methods 209:17-24.
33. Knipp, U., S. Birkholz, W. Kaup, and W. Opferkuch. 1996. Partial characterization of a cell proliferation-inhibiting protein produced by Helicobacter pylori. Infect. Immun. 64:3491-3496.
34. Kuck, D., B. Kolmerer, C. Iking-Konert, P. H. Krammer, W. Stremmel, and J. Rudi. 2001. Vacuolating cytotoxin of Helicobacter pylori induces apoptosis in the human gastric epithelial cell line AGS. Infect. Immun. 69:5080-5087.
35. Le'Negrate, G., V. Ricci, V. Hofman, B. Mograbi, P. Hofman, and B. Rossi. 2001. Epithelial intestinal cell apoptosis induced by Helicobacter pylori depends on expression of the cag pathogenicity island phenotype. Infect. Immun. 69:5001-5009.
36. Leunk, R. D., P. T. Johnson, B. C. David, W. G. Kraft, and D. R. Morgan. 1988. Cytotoxic activity in broth-culture filtrates of Campylobacter pylori. J. Med. Microbiol. 26:93-99.
37. Mai, U. E., G. I. Perez-Perez, J. B. Allen, S. M. Wahl, M. J. Blaser, and P. D. Smith. 1992. Surface proteins from Helicobacter pylori exhibit chemotactic activity for human leukocytes and are present in gastric mucosa. J. Exp. Med. 175:517-525.
38. Markwell, M. A., S. M. Haas, L. L. Bieber, and N. E. Tolbert. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87:206-210.
39. Massari, P., R. Manetti, D. Burroni, S. Nuti, N. Norais, R. Rappuoli, and J. L. Telford. 1998. Binding of the Helicobacter pylori vacuolating cytotoxin to target cells. Infect. Immun. 66:3981-3984.
40. Medzhitov, R., and C. A. Janeway, Jr. 1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295-298.
41. Moran, A. P. 1996. Pathogenic properties of Helicobacter pylori. Scand. J. Gastroenterol. Suppl. 215:22-31.
42. Moran, A. P., I. M. Helander, and T. U. Kosunen. 1992. Compositional analysis of Helicobacter pylori rough-form lipopolysaccharides. J. Bacteriol. 174:1370-1377.
43. Muotiala, A., I. M. Helander, L. Pyhala, T. U. Kosunen, and A. P. Moran. 1992. Low biological activity of Helicobacter pylori lipopolysaccharide. Infect. Immun. 60:1714-1716.
44. Odenbreit, S., H. Kavermann, J. Puls, and R. Haas. 2002. CagA tyrosine phosphorylation and interleukin-8 induction by Helicobacter pyroli are independent from alpAB, HopZ and bab group outer membrane proteins. Int. J. Med. Microbiol. 292:257-266.
45. Odenbreit, S., J. Puls, 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.
46. Pai, R., T. L. Cover, and A. S. Tarnawski. 1999. Helicobacter pylori vacuolating cytotoxin (VacA) disorganizes the cytoskeletal architecture of gastric epithelial cells. Biochem. Biophys. Res. Commun. 262:245-250.
47. Parsonnet, J. 1995. Bacterial infection as a cause of cancer. Environ. Health Perspect. 103(Suppl. 8):263-268.
48. Peek, R. M., Jr. 2001. Helicobacter pylori strain-specific activation of signal transduction cascades related to gastric inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G525-G530.
49. Peek, R. M., Jr., M. J. Blaser, D. J. Mays, M. H. Forsyth, T. L. Cover, S. Y. Song, U. Krishna, and J. A. Pietenpol. 1999. Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res. 59:6124-6131.
50. + Helicobacter pylori strains. Lab. Investig. 73:760-770.
51. + proportion of Helicobacter pylori infections. Int. J. Cancer 72:453-456.
52. Perez-Perez, G. I., V. L. Shepherd, J. D. Morrow, and M. J. Blaser. 1995. Activation of human THP-1 cells and rat bone marrow-derived macrophages by Helicobacter pylori lipopolysaccharide. Infect. Immun. 63:1183-1187.
53. Qureshi, S. T., L. Lariviere, G. Leveque, S. Clermont, K. J. Moore, P. Gros, and D. Malo. 1999. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (TIr4). J. Exp. Med. 189:615-625.
54. Ricci, V., C. Ciacci, R. Zarrilli, P. Sommi, M. K. Tummuru, C. Del Vecchio Blanco, C. B. Bruni, T. L. Cover, M. J. Blaser, and M. Romano. 1996. Effect of Helicobacter pylori on gastric epithelial cell migration and proliferation in vitro: role of VacA and CagA. Infect. Immun. 64:2829-2833.
55. Rieder, G., R. A. Hatz, A. P. Moran, A. Walz, M. Stolte, and G. Enders. 1997. Role of adherence in interleukin-8 induction in Helicobacter pylori-associated gastritis. Infect. Immun. 65:3622-3630.
56. Sakagami, T., J. Vella, M. F. Dixon, J. O'Rourke, F. Radcliff, P. Sutton, T. Shimoyama, K. Beagley, and A. Lee. 1997. The endotoxin of Helicobacter pylori is a modulator of host-dependent gastritis. Infect. Immun. 65:3310-3316.
57. Segal, E. D., J. Cha, J. Lo, S. Falkow, and L. S. Tompkins. 1999. Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc. Natl. Acad. Sci. USA 96:14559-14564.
58. Selbach, M., S. Moese, T. F. Meyer, and S. Backert. 2002. Functional analysis of the Helicobacter pylori cag pathogenicity island reveals both VirD4-CagA-dependent and VirD4-CagA-independent mechanisms. Infect. Immun. 70:665-671.
59. Sharma, S. A., M. K. Tummuru, M. J. Blaser, and L. D. Kerr. 1998. Activation of IL-8 gene expression by Helicobacter pylori is regulated by transcription factor nuclear factor-kappa B in gastric epithelial cells. J. Immunol. 160:2401-2407.
60. 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.
61. 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.
62. Smoot, D. T., Z. Wynn, T. B. Elliott, C. R. Allen, G. Mekasha, T. Naab, and H. Ashktorab. 1999. Effects of Helicobacter pylori on proliferation of gastric epithelial cells in vitro. Am. J. Gastroenterol. 94:1508-1511.
63. Stein, M., R. Rappuoli, and A. Covacci. 2000. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc. Natl. Acad. Sci. USA 97:1263-1268.
64. Takagi, A., S. Watanabe, M. Igarashi, J. Koike, K. Hasumi, R. Deguchi, Y. Koga, and T. Miwa. 2000. The effect of Helicobacter pylori on cell proliferation and apoptosis in gastric epithelial cell lines. Aliment. Pharmacol. Ther. 14(Suppl. 1):188-192.
65. Vasselon, T., and P. A. Detmers. 2002. Toll receptors: a central element in innate immune responses. Infect. Immun. 70:1033-1041.
66. Wagner, S., W. Beil, J. Westermann, R. P. Logan, C. T. Bock, C. Trautwein, J. S. Bleck, and M. P. Manns. 1997. Regulation of gastric epithelial cell growth by Helicobacter pylori: evidence for a major role of apoptosis. Gastroenterology 113:1836-1847.
67. Yamaoka, Y., T. Kodama, M. Kita, J. Imanishi, K. Kashima, and D. Y. Graham. 1999. Relation between clinical presentation, Helicobacter pylori density, interleukin 1beta and 8 production, and cagA status. Gut 45:804-811.
68. 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.