Helicobacter pylori Dampens Gut Epithelial Self-Renewal by Inhibiting Apoptosis, a Bacterial Strategy to Enhance Colonization of the Stomach

Cell Host and Microbe

Volumn 2, Issue 4, 2007, Pages 250-263

  Mimuro, Hitomi ^a   Suzuki, Toshihiko ^a   Nagai, Shigenori ^c,d   Rieder, Gabriele ^e   Suzuki, Masato ^a   Nagai, Takeshi ^a   Fujita, Yukihiro ^a   Nagamatsu, Kanna ^a   Ishijima, Nozomi ^a   Koyasu, Shigeo ^c,d   Haas, Rainer ^e   Sasakawa, Chihiro ^a,b,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b THE UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

MICROBIO; SIGNALING

Indexed keywords

CAGA PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN MCL 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL ACTIVATION; CELL LOSS; CELL RENEWAL; CELL SURVIVAL; CONTROLLED STUDY; EPITHELIUM CELL; GENETIC CODE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HOST PATHOGEN INTERACTION; MALE; MICROBIAL ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; STOMACH EPITHELIUM;

ANIMALS; ANTIGENS, BACTERIAL; APOPTOSIS; BACTERIAL PROTEINS; CELL LINE, TUMOR; GERBILLINAE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; HYPERPLASIA; INTESTINAL MUCOSA; NEOPLASM PROTEINS; PROTEIN TYROSINE PHOSPHATASES; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; UP-REGULATION;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI; MERIONES UNGUICULATUS;

EID: 34848863375     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2007.09.005     Document Type: Article

References (61)

1. Asahi M., Azuma T., Ito S., Ito Y., Suto H., Nagai Y., Tsubokawa M., Tohyama Y., Maeda S., Omata M., et al. Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J. Exp. Med. 191 (2000) 593-602
2. Backert S., and Meyer T.F. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr. Opin. Microbiol. 9 (2006) 207-217
3. Bannerman D.D., Tupper J.C., Ricketts W.A., Bennett C.F., Winn R.K., and Harlan J.M. A constitutive cytoprotective pathway protects endothelial cells from lipopolysaccharide-induced apoptosis. J. Biol. Chem. 276 (2001) 14924-14932
4. Blaser M.J. Helicobacter pylori and the pathogenesis of gastroduodenal inflammation. J. Infect. Dis. 161 (1990) 626-633
5. Blaser M.J., Perez-Perez G.I., Kleanthous H., Cover T.L., Peek J.R.M., Chyou P.H., Stemmermann G.N., and Nomura A. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 55 (1995) 2111-2115
6. Boquet P., Ricci V., Galmiche A., and Gauthier N.C. Gastric cell apoptosis and H. pylori: Has the main function of VacA finally been identified?. Trends Microbiol. 11 (2003) 410-413
7. Boucher M.J., Morisset J., Vachon P.H., Reed J.C., Laine J., and Rivard N. MEK/ERK signaling pathway regulates the expression of Bcl-2, Bcl-X(L), and Mcl-1 and promotes survival of human pancreatic cancer cells. J. Cell. Biochem. 79 (2000) 355-369
8. Brandt S., Kwok T., Hartig R., Konig W., and Backert S. NF-kappaB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc. Natl. Acad. Sci. USA 102 (2005) 9300-9305
9. Budd R.C., Yeh W.C., and Tschopp J. cFLIP regulation of lymphocyte activation and development. Nat. Rev. Immunol. 6 (2006) 196-204
10. Camorlinga-Ponce M., Romo C., Gonzalez-Valencia G., Munoz O., and Torres J. Topographical localisation of cagA positive and cagA negative Helicobacter pylori strains in the gastric mucosa; an in situ hybridisation study. J. Clin. Pathol. 57 (2004) 822-828
11. Choi I.J., Kim J.S., Kim J.M., Jung H.C., and Song I.S. Effect of inhibition of extracellular signal-regulated kinase 1 and 2 pathway on apoptosis and bcl-2 expression in Helicobacter pylori-infected AGS cells. Infect. Immun. 71 (2003) 830-837
12. Croxton R., Ma Y., Song L., Haura E.B., and Cress W.D. Direct repression of the Mcl-1 promoter by E2F1. Oncogene 21 (2002) 1359-1369
13. Eck M., Schmausser B., Haas R., Greiner A., Czub S., and Muller-Hermelink H.K. MALT-type lymphoma of the stomach is associated with Helicobacter pylori strains expressing the CagA protein. Gastroenterology 112 (1997) 1482-1486
14. El-Etr S.H., Mueller A., Tompkins L.S., Falkow S., and Merrell D.S. Phosphorylation-independent effects of CagA during interaction between Helicobacter pylori and T84 polarized monolayers. J. Infect. Dis. 190 (2004) 1516-1523
15. Falk P., Roth K.A., Boren T., Westblom T.U., Gordon J.I., and Normark S. An in vitro adherence assay reveals that Helicobacter pylori exhibits cell lineage-specific tropism in the human gastric epithelium. Proc. Natl. Acad. Sci. USA 90 (1993) 2035-2039
16. Fox J.G., Dangler C.A., Taylor N.S., King A., Koh T.J., and Wang T.C. High-salt diet induces gastric epithelial hyperplasia and parietal cell loss, and enhances Helicobacter pylori colonization in C57BL/6 mice. Cancer Res. 59 (1999) 4823-4828
17. Franco A.T., Israel D.A., Washington M.K., Krishna U., Fox J.G., Rogers A.B., Neish A.S., Collier-Hyams L., Perez-Perez G.I., Hatakeyama M., et al. Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc. Natl. Acad. Sci. USA 102 (2005) 10646-10651
18. Galmiche A., Rassow J., Doye A., Cagnol S., Chambard J.C., Contamin S., de Thillot V., Just I., Ricci V., Solcia E., et al. The N-terminal 34 kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release. EMBO J. 19 (2000) 6361-6370
19. Higashi H., Tsutsumi R., Muto S., Sugiyama T., Azuma T., Asaka M., and Hatakeyama M. SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295 (2002) 683-686
20. Hirata Y., Maeda S., Mitsuno Y., Tateishi K., Yanai A., Akanuma M., Yoshida H., Kawabe T., Shiratori Y., and Omata M. Helicobacter pylori CagA protein activates serum response element-driven transcription independently of tyrosine phosphorylation. Gastroenterology 123 (2002) 1962-1971
21. Houghton J., Stoicov C., Nomura S., Rogers A.B., Carlson J., Li H., Cai X., Fox J.G., Goldenring J.R., and Wang T.C. Gastric cancer originating from bone marrow-derived cells. Science 306 (2004) 1568-1571
22. Houghton J., and Wang T.C. Helicobacter pylori and gastric cancer: A new paradigm for inflammation-associated epithelial cancers. Gastroenterology 128 (2005) 1567-1578
23. Ilver D., Arnqvist A., Ogren J., Frick I.M., Kersulyte D., Incecik E.T., Berg D.E., Covacci A., Engstrand L., and Boren T. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279 (1998) 373-377
24. Isomoto H., Kobayashi S., Werneburg N.W., Bronk S.F., Guicciardi M.E., Frank D.A., and Gores G.J. Interleukin 6 upregulates myeloid cell leukemia-1 expression through a STAT3 pathway in cholangiocarcinoma cells. Hepatology 42 (2005) 1329-1338
25. Jiang X., and Wang X. Cytochrome C-mediated apoptosis. Annu. Rev. Biochem. 73 (2004) 87-106
26. Karam S.M., and Leblond C.P. Dynamics of epithelial cells in the corpus of the mouse stomach. II. Outward migration of pit cells. Anat. Rec. 236 (1993) 280-296
27. Kasza A., O'Donnell A., Gascoigne K., Zeef L.A., Hayes A., and Sharrocks A.D. The ETS domain transcription factor Elk-1 regulates the expression of its partner protein, SRF. J. Biol. Chem. 280 (2005) 1149-1155
28. Kawahara T., Kuwano Y., Teshima-Kondo S., Sugiyama T., Kawai T., Nikawa T., Kishi K., and Rokutan K. Helicobacter pylori lipopolysaccharide from type I, but not type II strains, stimulates apoptosis of cultured gastric mucosal cells. J. Med. Invest. 48 (2001) 167-174
29. Kawakubo M., Ito Y., Okimura Y., Kobayashi M., Sakura K., Kasama S., Fukuda M.N., Fukuda M., Katsuyama T., and Nakayama J. Natural antibiotic function of a human gastric mucin against Helicobacter pylori infection. Science 305 (2004) 1003-1006
30. Kuipers E.J., Perez-Perez G.I., Meuwissen S.G., and Blaser M.J. Helicobacter pylori and atrophic gastritis: Importance of the cagA status. J. Natl. Cancer Inst. 87 (1995) 1777-1780
31. Mahdavi J., Sonden B., Hurtig M., Olfat F.O., Forsberg L., Roche N., Angstrom J., Larsson T., Teneberg S., Karlsson K.A., et al. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297 (2002) 573-578
32. Maurer U., Charvet C., Wagman A.S., Dejardin E., and Green D.R. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol. Cell 21 (2006) 749-760
33. Mills J.C., Andersson N., Hong C.V., Stappenbeck T.S., and Gordon J.I. Molecular characterization of mouse gastric epithelial progenitor cells. Proc. Natl. Acad. Sci. USA 99 (2002) 14819-14824
34. Mimuro H., Suzuki T., Tanaka J., Asahi M., Haas R., and Sasakawa C. Grb2 is a key mediator of Helicobacter pylori CagA protein activities. Mol. Cell 10 (2002) 745-755
35. Nagai S., Mimuro H., Yamada T., Baba Y., Moro K., Nochi T., Kiyono H., Suzuki T., Sasakawa C., and Koyasu S. Role of Peyer's patches in the induction of Helicobacter pylori-induced gastritis. Proc. Natl. Acad. Sci. USA 104 (2007) 8971-8976
36. Odenbreit S., Puls J., Sedlmaier B., Gerland E., Fischer W., and Haas R. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287 (2000) 1497-1500
37. Oh J.D., Karam S.M., and Gordon J.I. Intracellular Helicobacter pylori in gastric epithelial progenitors. Proc. Natl. Acad. Sci. USA 102 (2005) 5186-5191
38. Opferman J.T., Iwasaki H., Ong C.C., Suh H., Mizuno S., Akashi K., and Korsmeyer S.J. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307 (2005) 1101-1104
39. Parsonnet J., Friedman G.D., Vandersteen D.P., Chang Y., Vogelman J.H., Orentreich N., and Sibley R.K. Helicobacter pylori infection and the risk of gastric carcinoma. N. Engl. J. Med. 325 (1991) 1127-1131
40. Parsonnet J., Hansen S., Rodriguez L., Gelb A.B., Warnke R.A., Jellum E., Orentreich N., Vogelman J.H., and Friedman G.D. Helicobacter pylori infection and gastric lymphoma. N. Engl. J. Med. 330 (1994) 1267-1271
41. Peek Jr. R.M., Moss S.F., Tham K.T., Perez-Perez G.I., Wang S., Miller G.G., Atherton J.C., Holt P.R., and Blaser M.J. Helicobacter pylori cagA+ strains and dissociation of gastric epithelial cell proliferation from apoptosis. J. Natl. Cancer Inst. 89 (1997) 863-868
42. Peek Jr. R.M., Wirth H.P., Moss S.F., Yang M., Abdalla A.M., Tham K.T., Zhang T., Tang L.H., Modlin I.M., and Blaser M.J. Helicobacter pylori alters gastric epithelial cell cycle events and gastrin secretion in Mongolian gerbils. Gastroenterology 118 (2000) 48-59
43. Peek Jr. R.M., and Blaser M.J. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2 (2002) 28-37
44. Piret J.P., Minet E., Cosse J.P., Ninane N., Debacq C., Raes M., and Michiels C. Hypoxia-inducible factor-1-dependent overexpression of myeloid cell factor-1 protects hypoxic cells against tert-butyl hydroperoxide-induced apoptosis. J. Biol. Chem. 280 (2005) 9336-9344
45. Price M.A., Rogers A.E., and Treisman R. Comparative analysis of the ternary complex factors Elk-1, SAP-1a and SAP-2 (ERP/NET). EMBO J. 14 (1995) 2589-2601
46. Rieder G., Merchant J.L., and Haas R. Helicobacter pylori cag-type IV secretion system facilitates corpus colonization to induce precancerous conditions in Mongolian gerbils. Gastroenterology 128 (2005) 1229-1242
47. Rudi J., Kuck D., Strand S., von Herbay A., Mariani S.M., Krammer P.H., Galle P.R., and Stremmel W. Involvement of the CD95 (APO-1/Fas) receptor and ligand system in Helicobacter pylori-induced gastric epithelial apoptosis. J. Clin. Invest. 102 (1998) 1506-1514
48. Segal E.D., Cha J., Lo J., Falkow S., and Tompkins L.S. Altered states: Involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc. Natl. Acad. Sci. USA 96 (1999) 14559-14564
49. Selbach M., Moese S., Hauck C.R., Meyer T.F., and Backert S. Src is the kinase of the Helicobacter pylori CagA protein in vitro and in vivo. J. Biol. Chem. 277 (2002) 6775-6778
50. Shibayama K., Kamachi K., Nagata N., Yagi T., Nada T., Doi Y., Shibata N., Yokoyama K., Yamane K., Kato H., et al. A novel apoptosis-inducing protein from Helicobacter pylori. Mol. Microbiol. 47 (2003) 443-451
51. Strasser A. The role of BH3-only proteins in the immune system. Nat. Rev. Immunol. 5 (2005) 189-200
52. Suzuki M., Mimuro H., Suzuki T., Park M., Yamamoto T., and Sasakawa C. Interaction of CagA with Crk plays an important role in Helicobacter pylori-induced loss of gastric epithelial cell adhesion. J. Exp. Med. 202 (2005) 1235-1247
53. Townsend K.J., Zhou P., Qian L., Bieszczad C.K., Lowrey C.H., Yen A., and Craig R.W. Regulation of MCL1 through a serum response factor/Elk-1-mediated mechanism links expression of a viability-promoting member of the BCL2 family to the induction of hematopoietic cell differentiation. J. Biol. Chem. 274 (1999) 1801-1813
54. Viala J., Chaput C., Boneca I.G., Cardona A., Girardin S.E., Moran A.P., Athman R., Memet S., Huerre M.R., Coyle A.J., et al. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5 (2004) 1166-1174
55. Vickers E.R., Kasza A., Kurnaz I.A., Seifert A., Zeef L.A., O'Donnell A., Hayes A., and Sharrocks A.D. Ternary complex factor-serum response factor complex-regulated gene activity is required for cellular proliferation and inhibition of apoptotic cell death. Mol. Cell. Biol. 24 (2004) 10340-10351
56. Wang J.M., Chao J.R., Chen W., Kuo M.L., Yen J.J., and Yang-Yen H.F. The antiapoptotic gene mcl-1 is up-regulated by the phosphatidylinositol 3-kinase/Akt signaling pathway through a transcription factor complex containing CREB. Mol. Cell. Biol. 19 (1999) 6195-6206
57. Yamasaki E., Wada A., Kumatori A., Nakagawa I., Funao J., Nakayama M., Hisatsune J., Kimura M., Moss J., and Hirayama T. Helicobacter pylori vacuolating cytotoxin induces activation of the proapoptotic protein Bax and Bak, leading to cytochrome c release and cell death, independent of vacuolation. J. Biol. Chem. 281 (2006) 11250-11259
58. Yanai A., Hirata Y., Mitsuno Y., Maeda S., Shibata W., Akanuma M., Yoshida H., Kawabe T., and Omata M. Helicobacter pylori induces antiapoptosis through Nuclear factor-KB activation. J. Infect. Dis. 188 (2003) 1741-1751
59. Yokoyama K., Higashi H., Ishikawa S., Fujii Y., Kondo S., Kato H., Azuma T., Wada A., Hirayama T., Aburatani H., and Hatakeyama M. Functional antagonism between Helicobacter pylori CagA and vacuolating toxin VacA in control of the NFAT signaling pathway in gastric epithelial cells. Proc. Natl. Acad. Sci. USA 102 (2005) 9661-9666
60. Zhang B., Gojo I., and Fenton R.G. Myeloid cell factor-1 is a critical survival factor for multiple myeloma. Blood 99 (2002) 1885-1893
61. Zhu Y., Wang C., Huang J., Ge Z., Dong Q., Zhong X., Su Y., and Zheng S. The Helicobacter pylori virulence factor CagA promotes Erk1/2-mediated Bad phosphorylation in lymphocytes: A mechanism of CagA-inhibited lymphocyte apoptosis. Cell. Microbiol. 9 (2007) 952-961