Helicobacter pylori and mitogen-activated protein kinases regulate the cell cycle, proliferation and apoptosis in gastric epithelial cells

Journal of Gastroenterology and Hepatology (Australia)

Volumn 23, Issue 7 PT2, 2008, Pages

  Ding, Song Ze ^a   Smith Jr , Michael F ^a   Goldberg, Joanna B ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

Apoptosis; Cell cycle; Gastric epithelial cell; Helicobacter pylori; Mitogen activated protein kinases; Proliferation

Indexed keywords

CELL CYCLE PROTEIN; CYCLIN D1; CYCLIN E; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P21; PROTEIN P27; STRESS ACTIVATED PROTEIN KINASE;

ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CELL COUNT; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVATION; ENZYME INHIBITION; EPITHELIUM CELL; FLOW CYTOMETRY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STOMACH EPITHELIUM; WESTERN BLOTTING;

EID: 47649095344     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/j.1440-1746.2007.04912.x     Document Type: Article

References (57)

1. Wagner S, Beil W, Westermann J et al. Regulation of gastric epithelial cell growth by Helicobacter pylori: evidence for a major role of apoptosis. Gastroenterology 1997 113 : 1836 47.
2. Choi IJ, Kim JS, Kim JM, Jung HC, Song IS. 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. 2003 71 : 830 7.
3. Ahmed A, Smoot D, Littleton G et al. Helicobacter pylori inhibits gastric cell cycle progression. Microbes Infect. 2000 2 : 1159 69.
4. Jang TJ, Kim JR. Proliferation and apoptosis in gastric antral epithelial cells of patients infected with Helicobacter pylori. J. Gastroenterol. 2000 35 : 265 71.
5. Suzuki M, Suzuki H, Masaoka T, Tanaka S, Suzuki K, Ishii H. Helicobacter pylori eradication treatment modulates epithelial cell proliferation and tissue content of hepatocyte growth factor in the gastric mucosa. Aliment. Pharmacol. Ther. 2004 20 (Suppl. 1 158 64.
6. Israel DA, Peek RM Jr. The role of persistence in Helicobacter pylori pathogenesis. Curr. Opin. Gastroenterol. 2006 22 : 3 7.
7. El-Omar EM, Carrington M, Chow WH et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 2000 404 : 398 402.
8. El-Omar EM, Rabkin CS, Gammon MD et al. Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 2003 124 : 1193 201.
9. Ernst PB, Peura DA, Crowe SE. The translation of Helicobacter pylori basic research to patient care. Gastroenterology 2006 130 : 188 206 quiz 212-13.
10. Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature 2001 410 : 37 40.
11. Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002 298 : 1911 12.
12. Ono K, Han J. The p38 signal transduction pathway: activation and function. Cell Sign. 2000 12 : 1 13.
13. Chiou CC, Chan CC, Kuo YP, Chan EC. Helicobacter pylori inhibits activity of cdc2 kinase and delays G2/M to G1 progression in gastric adenocarcinoma cell line. Scand. J. Gastroenterol. 2003 38 : 147 52.
14. Sommi P, Savio M, Stivala LA et al. 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. 2002 281 : 128 39.
15. De Luca A, Baldi A, Russo P et al. Coexpression of Helicobacter pylori's proteins CagA and HspB induces cell proliferation in AGS gastric epithelial cells, independently from the bacterial infection. Cancer Res. 2003 63 : 6350 6.
16. Peek RM Blaser MJ, Mays DJ et al. Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res. 1999 59 : 6124 31.
17. Zhang ZW, Patchett SE, Farthing MJ. Role of Helicobacter pylori and p53 in regulation of gastric epithelial cell cycle phase progression. Dig. Dis. Sci. 2002 47 : 987 95.
18. Eguchi H, Herschenhous N, Kuzushita N, Moss SF. Helicobacter pylori increases proteasome-mediated degradation of p27 (kip1) in gastric epithelial cells. Cancer Res. 2003 63 : 4739 46.
19. Gerhard M, Schmees C, Voland P et al. A secreted low-molecular-weight protein from Helicobacter pylori induces cell-cycle arrest of T cells. Gastroenterology 2005 128 : 1327 39.
20. Keates S, Keates AC, Warny M, Peek RM Murray PG, Kelly CP. Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cag+ and cag- Helicobacter pylori. J. Immunol. 1999 163 : 5552 9.
21. Torok AM, Bouton AH, Goldberg JB. Helicobacter pylori induces interleukin-8 secretion by Toll-like receptor 2- and Toll-like receptor 5-dependent and independent pathways. Infect. Immun. 2005 73 : 1523 31.
22. Akopyants NS, Clifton SW, Kersulyte D et al. Analyses of the cag pathogenicity island of Helicobacter pylori. Mol. Microbiol. 1998 28 : 37 53.
23. 2 increase AP endonuclease-1/redox factor-1 expression in human gastric epithelial cells. Gastroenterology 2004 127 : 845 58.
24. Ding SZ, Torok AM, Smith MF Goldberg JB. Toll-like receptor 2-mediated gene expression in epithelial cells during Helicobacter pylori infection. Helicobacter 2005 10 : 193 204.
25. Shaulian E, Karin M. AP-1 in cell proliferation and survival. Oncogene 2001 20 : 2390 400.
26. Balmanno K, Cook SJ. Sustained MAP kinase activation is required for the expression of cyclin D1, 21Cip1 and a subset of AP-1 proteins in CCL39 cells. Oncogene 1999 18 : 3085 97.
27. Angel P, Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta 1991 1072 : 129 57.
28. Karin M, Hunter T. Transcriptional control by protein phosphorylation: signal transmission from the cell surface to the nucleus. Curr. Biol. 1995 5 : 747 57.
29. Sherr CJ. The ins and outs of RB: coupling gene expression to the cell cycle clock. Trends Cell Biol. 1994 4 : 15 18.
30. Ohtsubo M, Theodoras AM, Schumacher J, Roberts JM, Pagano M. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol. Cell Biol. 1995 15 : 2612 24.
31. Sherr CJ. G1 phase progression: cycling on cue. Cell 1994 79 : 551 5.
32. Shirin H, Weinstein IB, Moss SF. Effects of H. pylori infection of gastric epithelial cells on cell cycle control. Front Biosci. 2001 6 : E104 18.
33. Meyer-ter-Vehn T, Covacci A, Kist M, Pahl HL. Helicobacter pylori activates mitogen-activated protein kinase cascades and induces expression of the proto-oncogenes c-fos and c-jun. J. Biol. Chem. 2000 275 : 16064 72.
34. Mitsuno Y, Yoshida H, Maeda S et al. Helicobacter pylori induced transactivation of SRE and AP-1 through the ERK signalling pathway in gastric cancer cells. Gut 2001 49 : 18 22.
35. Berra E, Diaz-Meco MT, Moscat J. The activation of p38 and apoptosis by the inhibition of Erk is antagonized by the phosphoinositide 3-kinase/Akt pathway. J. Biol. Chem. 1998 273 : 10792 7.
36. Surapisitchat J, Hoefen RJ, Pi X, Yoshizumi M, Yan C, Berk BC. Fluid shear stress inhibits TNF-alpha activation of JNK but not ERK1/2 or p38 in human umbilical vein endothelial cells: inhibitory crosstalk among MAPK family members. Proc. Natl Acad. Sci. USA 2001 98 : 6476 81.
37. Xiao YQ, Malcolm K, Worthen GS et al. Cross-talk between ERK and p38 MAPK mediates selective suppression of pro-inflammatory cytokines by transforming growth factor-beta. J. Biol. Chem. 2002 277 : 14884 93.
38. Sharma GD, He J, Bazan HE. p38 and ERK1/2 coordinate cellular migration and proliferation in epithelial wound healing: evidence of cross-talk activation between MAP kinase cascades. J. Biol. Chem. 2003 278 : 21989 97.
39. Hotokezaka H, Sakai E, Kanaoka K et al. U0126 and PD98059, specific inhibitors of MEK, accelerate differentiation of RAW264.7 cells into osteoclast-like cells. J. Biol. Chem. 2002 277 : 47366 72.
40. Matsushime H, Roussel MF, Ashmun RA, Sherr CJ. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 1991 65 : 701 13.
41. Lavoie JN, L'Allemain G, Brunet A, Muller R, Pouyssegur J. Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J. Biol. Chem. 1996 271 : 20608 16.
42. Lavoie JN, Rivard N, L'Allemain G, Pouyssegur J. A temporal and biochemical link between growth factor-activated MAP kinases, cyclin D1 induction and cell cycle entry. Prog. Cell Cycle Res. 1996 2 : 49 58.
43. Gallo KA, Johnson GL. Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat. Rev. Mol Cell Biol. 2002 3 : 663 72.
44. Bulavin DV, Higashimoto Y, Popoff IJ et al. Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 2001 411 : 102 7.
45. Bulavin DV, Higashimoto Y, Demidenko ZN et al. Dual phosphorylation controls Cdc25 phosphatases and mitotic entry. Nat. Cell Biol. 2003 5 : 545 51.
46. Bulavin DV, Fornace AJ Jr. p38 MAP kinase's emerging role as a tumor suppressor. Adv. Cancer Res. 2004 92 : 95 118.
47. Jochum W, Passegue E, Wagner EF. AP-1 in mouse development and tumorigenesis. Oncogene 2001 20 : 2401 12.
48. Mingo-Sion AM, Marietta PM, Koller E, Wolf DM, Van Den Berg CL. Inhibition of JNK reduces G2/M transit independent of p53, leading to endoreduplication, decreased proliferation, and apoptosis in breast cancer cells. Oncogene 2004 23 : 596 604.
49. Schwabe RF, Bradham CA, Uehara T et al. c-Jun-N-terminal kinase drives cyclin D1 expression and proliferation during liver regeneration. Hepatology 2003 37 : 824 32.
50. Wada T, Joza N, Cheng HY et al. MKK7 couples stress signalling to G2/M cell-cycle progression and cellular senescence. Nat. Cell Biol. 2004 6 : 215 26.
51. Wada T, Penninger JM. Stress kinase MKK7: savior of cell cycle arrest and cellular senescence. Cell Cycle 2004 3 : 577 9.
52. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995 270 : 1326 31.
53. Tang D, Wu D, Hirao A et al. ERK activation mediates cell cycle arrest and apoptosis after DNA damage independently of p53. J. Biol. Chem. 2002 277 : 12710 17.
54. Tran SE, Holmstrom TH, Ahonen M, Kahari VM, Eriksson JE. MAPK/ERK overrides the apoptotic signaling from Fas, TNF, and TRAIL receptors. J. Biol. Chem. 2001 276 : 16484 90.
55. Rudi J, Kuck D, Strand S et al. Involvement of the CD95 (APO-1/Fas) receptor and ligand system in Helicobacter pylori-induced gastric epithelial apoptosis. J. Clin. Invest. 1998 102 : 1506 14.
56. Eguchi H, Carpentier S, Kim SS, Moss SF. P27kip1 regulates the apoptotic response of gastric epithelial cells to Helicobacter pylori. Gut 2004 53 : 797 804.
57. Blundell R, Harrison DJ, O'Dea S. p21 (Waf1/Cip1) regulates proliferation and apoptosis in airway epithelial cells and alternative forms have altered binding activities. Exp. Lung Res. 2004 30 : 447 64.