A secreted low-molecular-weight protein from Helicobacter pylori induces cell-cycle arrest of T cells

Gastroenterology

Volumn 128, Issue 5, 2005, Pages 1327-1339

  Gerhard, Markus ^a,c   Schmees, Christian ^a   Voland, Petra ^a   Endres, Nicole ^a   Sander, Markus ^a   Reindl, Wolfgang ^a   Rad, Roland ^a   Oelsner, Madlene ^a   Decker, Thomas ^a   Mempel, Martin ^a   Hengst, Ludger ^b   Prinz, Christian ^a,d  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c HUBRECHT INSTITUTE   (Netherlands)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CD69 ANTIGEN; CYCLIN D3; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; GAMMA INTERFERON; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; MONOCLONAL ANTIBODY CD3; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR NFAT; VACUOLATING TOXIN; VIRULENCE FACTOR;

ANIMAL CELL; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; BACTERIAL STRAIN; BACTERIUM CULTURE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME INHIBITION; FEMALE; FIBROBLAST; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; INCUBATION TIME; INTERFERON PRODUCTION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; STIMULATION; SUPERNATANT; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION INITIATION; UPREGULATION; WESTERN BLOTTING;

EID: 21044439786     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2005.03.018     Document Type: Article

References (46)

1. M.J. Blaser Helicobacter pylori and gastric diseases BMJ 316 1998 1507 1510
2. K.B. Bamford, X. Fan, S.E. Crowe, J.F. Leary, W.K. Gourley, G.K. Luthra, E.G. Brooks, D.Y. Graham, V.E. Reyes, P.B. Ernst Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype Gastroenterology 114 1998 482 492
3. M.M. D'Elios, M. Manghetti, M. De Carli, F. Costa, C.T. Baldari, D. Burroni, J.L. Telford, S. Romagnani, G. Del Prete T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease J Immunol 158 1997 962 967
4. E. Stromberg, A. Lundgren, A. Edebo, S. Lundin, A.M. Svennerholm, C. Lindholm Increased frequency of activated T-cells in the Helicobacter pylori-infected antrum and duodenum FEMS Immunol Med Microbiol 36 2003 159 168
5. M. Quiding-Jarbrink, B.S. Lundin, H. Lonroth, A.M. Svennerholm CD4+ and CD8+ T cell responses in Helicobacter pylori-infected individuals Clin Exp Immunol 123 2001 81 87
6. A.M. Terres, J.M. Pajares An increased number of follicles containing activated CD69+ helper T cells and proliferating CD71+ B cells are found in H. pylori-infected gastric mucosa Am J Gastroenterol 93 1998 579 583
7. L.A. Allen, L.S. Schlesinger, B. Kang Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages J Exp Med 191 2000 115 128
8. N. Ramarao, S.D. Gray-Owen, S. Backert, T.F. Meyer Helicobacter pylori inhibits phagocytosis by professional phagocytes involving type IV secretion components Mol Microbiol 37 2000 1389 1404
9. J. Zabaleta, D.J. McGee, A.H. Zea, C.P. Hernandez, P.C. Rodriguez, R.A. Sierra, P. Correa, A.C. Ochoa Helicobacter pylori arginase inhibits T cell proliferation and reduces the expression of the TCR zeta-chain (CD3zeta) J Immunol 173 2004 586 593
10. K. Putsep, C.I. Branden, H.G. Boman, S. Normark Antibacterial peptide from H. pylori Nature 398 1999 671 672
11. A. Betten, J. Bylund, T. Cristophe, F. Boulay, A. Romero, K. Hellstrand, C. Dahlgren A proinflammatory peptide from Helicobacter pylori activates monocytes to induce lymphocyte dysfunction and apoptosis J Clin Invest 108 2001 1221 1228
12. A.A. Akhiani, J. Pappo, Z. Kabok, K. Schon, W. Gao, L.E. Franzen, N. Lycke Protection against Helicobacter pylori infection following immunization is IL-12-dependent and mediated by Th1 cells J Immunol 169 2002 6977 6984
13. M. Boncristiano, S.R. Paccani, S. Barone, C. Ulivieri, L. Patrussi, D. Ilver, A. Amedei, M.M. D'Elios, J.L. Telford, C.T. Baldari The Helicobacter pylori vacuolating toxin inhibits T cell activation by two independent mechanisms J Exp Med 198 2003 1887 1897
14. B. Gebert, W. Fischer, E. Weiss, R. Hoffmann, R. Haas Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation Science 301 2003 1099 1102
15. M.S. Sundrud, V.J. Torres, D. Unutmaz, T.L. Cover Inhibition of primary human T cell proliferation by Helicobacter pylori vacuolating toxin (VacA) is independent of VacA effects on IL-2 secretion Proc Natl Acad Sci U S A 101 2004 7727 7732
16. J. Wang, E.G. Brooks, K.B. Bamford, T.L. Denning, J. Pappo, P.B. Ernst Negative selection of T cells by Helicobacter pylori as a model for bacterial strain selection by immune evasion J Immunol 167 2001 926 934
17. R. Karttunen Blood lymphocyte proliferation, cytokine secretion and appearance of T cells with activation surface markers in cultures with Helicobacter pylori Comparison of the responses of subjects with and without antibodies to H. pylori Clin Exp Immunol 83 1991 396 400
18. X.G. Fan, J. Yakoob, X.J. Fan, P.W. Keeling Effect of IL-4 on peripheral blood lymphocyte proliferation implication in immunopathogenesis of H pylori infection. Immunol Lett 48 1995 45 48
19. U. Knipp, S. Birkholz, W. Kaup, W. Opferkuch Immune suppressive effects of Helicobacter pylori on human peripheral blood mononuclear cells Med Microbiol Immunol (Berl) 182 1993 63 76
20. U. Knipp, S. Birkholz, W. Kaup, K. Mahnke, W. Opferkuch Suppression of human mononuclear cell response by Helicobacter pylori effects on isolated monocytes and lymphocytes FEMS Immunol Med Microbiol 8 1994 157 166
21. W. Chen, D. Shu, V.S. Chadwick Inhibition of mitogen-induced murine lymphocyte proliferation by Helicobacter pylori cell-free extract J Gastroenterol Hepatol 15 2000 1000 1006
22. M. Gerhard, N. Lehn, N. Neumayer, T. Boren, R. Rad, W. Schepp, S. Miehlke, M. Classen, C. Prinz Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin Proc Natl Acad Sci U S A 96 1999 12778 12783
23. R.H. Kehlenbach, A. Dickmanns, L. Gerace Nucleocytoplasmic shuttling factors including Ran and CRM1 mediate nuclear export of NFAT In vitro J Cell Biol 141 1998 863 874
24. N. Shastri, F. Gonzalez Endogenous generation and presentation of the ovalbumin peptide/Kb complex to T cells J Immunol 150 1993 2724 2736
25. T. Maurer, A. Heit, H. Hochrein, F. Ampenberger, M. O'Keeffe, S. Bauer, G.B. Lipford, R.M. Vabulas, H. Wagner CpG-DNA aided cross-presentation of soluble antigens by dendritic cells Eur J Immunol 32 2002 2356 2364
26. E. Dufour, G. Carcelain, C. Gaudin, C. Flament, M.F. Avril, F. Faure Diversity of the cytotoxic melanoma-specific immune response some CTL clones recognize autologous fresh tumor cells and not tumor cell lines J Immunol 158 1997 3787 3795
27. M. Gerhard, N. Neumayer, E. Presecan-Siedel, R. Zanner, E. Lengyel, T. Cramer, M. Hocker, C. Prinz Gastrin induces expression and promoter activity of the vesicular monoamine transporter subtype 2 Endocrinology 142 2001 3663 3672
28. S.I. Reed Control of the G1/S transition Cancer Surv 29 1997 7 23
29. X.G. Fan, D. Kelleher, X.J. Fan, H.X. Xia, P.W. Keeling Helicobacter pylori increases proliferation of gastric epithelial cells Gut 38 1996 19 22
30. R.M. Peek Jr, H.P. Wirth, S.F. Moss, M. Yang, A.M. Abdalla, K.T. Tham, T. Zhang, L.H. Tang, I.M. Modlin, M.J. Blaser Helicobacter pylori alters gastric epithelial cell cycle events and gastrin secretion in Mongolian gerbils Gastroenterology 118 2000 48 59
31. S.F. Moss, J. Calam, B. Agarwal, S. Wang, P.R. Holt Induction of gastric epithelial apoptosis by Helicobacter pylori Gut 38 1996 498 501
32. H. Shirin, E.M. Sordillo, T.K. Kolevska, H. Hibshoosh, Y. Kawabata, S.H. Oh, J.F. Kuebler, T. Delohery, C.M. Weghorst, I.B. Weinstein, S.F. Moss Chronic Helicobacter pylori infection induces an apoptosis-resistant phenotype associated with decreased expression of p27(kip1) Infect Immun 68 2000 5321 5328
33. H. Shirin, E.M. Sordillo, S.H. Oh, H. Yamamoto, T. Delohery, I.B. Weinstein, S.F. Moss Helicobacter pylori inhibits the G1 to S transition in AGS gastric epithelial cells Cancer Res 59 1999 2277 2281
34. A. Ahmed, D. Smoot, G. Littleton, R. Tackey, C.S. Walters, F. Kashanchi, C.R. Allen, H. Ashktorab Helicobacter pylori inhibits gastric cell cycle progression Microbes Infect 2 2000 1159 1169
35. P. Sommi, M. Savio, L.A. Stivala, C. Scotti, P. Mignosi, E. Prosperi, V. Vannini, E. Solcia Helicobacter pylori releases a factor(s) inhibiting cell cycle progression of human gastric cell lines by affecting cyclin E/cdk2 kinase activity and Rb protein phosphorylation through enhanced p27(KIP1) protein expression Exp Cell Res 281 2002 128 139
36. Y. Hirata, S. Maeda, Y. Mitsuno, M. Akanuma, Y. Yamaji, K. Ogura, H. Yoshida, Y. Shiratori, M. Omata Helicobacter pylori activates the cyclin D1 gene through mitogen-activated protein kinase pathway in gastric cancer cells Infect Immun 69 2001 3965 3971
37. J. Yu, W.K. Leung, E.K. Ng, K.F. To, M.P. Ebert, M.Y. Go, W.Y. Chan, F.K. Chan, S.C. Chung, P. Malfertheiner, J.J. Sung Effect of Helicobacter pylori eradication on expression of cyclin D2 and p27 in gastric intestinal metaplasia Aliment Pharmacol Ther 15 2001 1505 1511
38. J.G. Fox, T.C. Wang, A.B. Rogers, T. Poutahidis, Z. Ge, N. Taylor, C.A. Dangler, D.A. Israel, U. Krishna, K. Gaus, R.M. Peek Jr Host and microbial constituents influence helicobacter pylori-induced cancer in a murine model of hypergastrinemia Gastroenterology 124 2003 1879 1890
39. J.G. Fox, A.B. Rogers, M. Ihrig, N.S. Taylor, M.T. Whary, G. Dockray, A. Varro, T.C. Wang Helicobacter pylori-associated gastric cancer in INS-GAS mice is gender specific Cancer Res 63 2003 942 950
40. N. Kim, D.L. Weeks, J.M. Shin, D.R. Scott, M.K. Young, G. Sachs Proteins released by Helicobacter pylori in vitro J Bacteriol 184 2002 6155 6162
41. D. Bumann, S. Aksu, M. Wendland, K. Janek, U. Zimny-Arndt, N. Sabarth, T.F. Meyer, P.R. Jungblut Proteome analysis of secreted proteins of the gastric pathogen Helicobacter pylori Infect Immun 70 2002 3396 3403
42. T.L. Cover, U.S. Krishna, D.A. Israel, R.M. Peek Jr Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin Cancer Res 63 2003 951 957
43. A. Galmiche, J. Rassow, A. Doye, S. Cagnol, J.C. Chambard, S. Contamin, T.V. de, I. Just, V. Ricci, E. Solcia, E. Van Obberghen, P. Boquet The N-terminal 34 kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release EMBO J 19 2000 6361 6370
44. U. Knipp, S. Birkholz, W. Kaup, W. Opferkuch Partial characterization of a cell proliferation-inhibiting protein produced by Helicobacter pylori Infect Immun 64 1996 3491 3496
45. S. Miyatake, H. Nakano, S.Y. Park, T. Yamazaki, K. Takase, H. Matsushime, A. Kato, T. Saito Induction of G1 arrest by down-regulation of cyclin D3 in T cell hybridomas J Exp Med 182 1995 401 408
46. L. Hengst A second RING to destroy p27(Kip1) Nat Cell Biol 6 2004 1153 1155