Differential regulation of ERK1/2 and p38 MAP kinases in VacA-induced apoptosis of gastric epithelial cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 294, Issue 3, 2008, Pages

  Ki, Mi Ran ^a   Lee, Hye Rim ^a   Goo, Moon Jung ^a   Hong, Il Hwa ^a   Do, Sun Hee ^a   Jeong, Da Hee ^a   Yang, Hai Jie ^a   Yuan, Dong Wei ^a   Park, Jin Kyu ^a   Jeong, Kyu Shik ^a  

^a Kyungpook National University   (South Korea)

Author keywords

Helicobacter pylori; MAP kinase signaling; SOD 1; VacA; Villin

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACTIN; COPPER ZINC SUPEROXIDE DISMUTASE; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAX; PROTEIN BCL 2; VACUOLATING TOXIN; VILLIN;

APOPTOSIS; ARTICLE; CELL DAMAGE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; EPITHELIUM CELL; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; STOMACH EPITHELIUM;

APOPTOSIS; BACTERIAL PROTEINS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; EPITHELIAL CELLS; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; GASTRIC MUCOSA; HELICOBACTER PYLORI; HUMANS; INDOLES; MICROFILAMENT PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PLASMIDS; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUPEROXIDE DISMUTASE; VACUOLES;

EID: 41549100950     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00281.2007     Document Type: Article

References (73)

1. Abdollahi T, Robertson NM, Abdollahi A, Litwack G. Inhibition of TRAIL-induced apoptosis by IL-8 is mediated by the p38-MAPK pathway in OVCAR3 cells. Apoptosis 10: 1383-1393, 2005.
2. Albertson R, Riggs B, Sullivan W. Membrane traffic: a driving force in cytokinesis. Trends Cell Biol 15: 92-101, 2005.
3. Alonso G, Ambrosino C, Jones M, Nebreda AR. Differential activation of p38 mitogen-activated protein kinase isoforms depending on signal strength. J Biol Chem 275: 40641-40648, 2000.
4. Antonsson B, Montessuit S, Sanchez B, Martinou JC. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 276: 11615-11623, 2001.
5. Aquilano K, Vigilanza P, Rotilio G, Ciriolo MR. Mitochondrial damage due to SOD1 deficiency in SH-SY5Y neuroblastoma cells: a rationale for the redundancy of SOD1. FASEB J 20: 1683-1685, 2006.
6. Atherton JC, Cao P, Peek RM Jr, Tummuru MK, Blaser MJ, Cover TL. 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, 1995.
7. Athman R, Louvard D, Robine S. The epithelial cell cytoskeleton and intracellular trafficking. III. How is villin involved in the actin cytoskeleton dynamics in intestinal cells? Am J Physiol Gastrointest Liver Physiol 283: G496-G502, 2002.
8. Athman R, Louvard D, Robine S. Villin enhances hepatocyte growth factor-induced actin cytoskeleton remodeling in epithelial cells. Mol Biol Cell 14: 4641-4653, 2003.
9. Avruch J. MAP kinase pathways: the first twenty years. Biochim Biophys Acta 1773: 1150-1160, 2007.
10. Baik SC, Youn HS, Chung MH, Lee WK, Cho MJ, Ko GH, Park CK, Kasai H, Rhee KH. Increased oxidative DNA damage in Helicobacter pylori-infected human gastric mucosa. Cancer Res 56: 1279-1282, 1996.
11. Bao M, Lou Y. Isorhamnetin prevent endothelial cell injuries from oxidized LDL via activation of p38MAPK. Eur J Pharmacol 547: 22-30, 2006.
12. Blander G, de Oliveira RM, Conboy CM, Haigis M, Guarente L. Superoxide dismutase 1 knock-down induces senescence in human fibroblasts. J Biol Chem 278: 38966-38969, 2003.
13. Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH, Stemmermann GN, Nomura A. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55: 2111-2115, 1995.
14. Boncristiano M, Paccani SR, Barone S, Ulivieri C, Patrussi L, Ilver D, Amedei A, D'Elios MM, Telford JL, Baldari CT. The Helicobacter pylori vacuolating toxin inhibits T cell activation by two independent mechanisms. J Exp Med 198: 1887-1897, 2003.
15. Bretscher A, Weber K. Villin: the major microfilament-associated protein of the intestinal microvillus. Proc Natl Acad Sci USA 76: 2321-2325, 1979.
16. Briede JJ, Pot RG, Kuipers EJ, van Vliet AH, Kleinjans JC, Kusters JG. The presence of the cag pathogenicity island is associated with increased superoxide anion radical scavenging activity by Helicobacter pylori. FEMS Immunol Med Microbiol 44: 227-232, 2005.
17. Brown L, Benchimol S. The involvement of MAPK signaling pathways in determining the cellular response to p53 activation: cell cycle arrest or apoptosis. J Biol Chem 281: 3832-3840. 2006.
18. Caputo R, Tuccillo C, Manzo BA, Zarrilli R, Tortora G, del Vecchio Blanco C, Ricci V, Ciardiello F, Romano M. Helicobacter pylori VacA toxin up-regulates vascular endothelial growth factor expression in MKN 28 gastric cells through an epidermal growth factor receptor-, cyclooxygenase-2- dependent mechanism. Clin Cancer Res 9: 2015-2021, 2003.
19. Chang L, Karin M. Mammalian MAP kinase signaling cascades. Nature 410: 37-40, 2001.
20. Correa P. Does Helicobacter pylori cause gastric cancer via oxidative stress? Biol Chem 387: 361-364, 2006.
21. Cover TL, Krishna US, Israel DA, Peek RM Jr. Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res 63: 951-957, 2003.
22. Cover TL, Puryear W, Pérez-Pérez GI, Blaser MJ. Effect of urease on HeLa cell vacuolation induced by Helicobacter pylori cytotoxin. Infect Immun 59: 1264-1270, 1991.
23. Ding M, Shi X, Dong Z, Chen F, Lu Y, Castranova V, Vallyathan V. Freshly fractured crystalline silica induces activator protein-1 activation through ERKs and p38 MAPK. J Biol Chem 274: 30611-30616, 1999.
24. Farkas R, Pronai L, Tulassay Z, Selmeci L. Relationship between eradication of Helicobacter pylori and gastric mucosal superoxide dismutase activity. Anticancer Res 25: 4763-4767, 2005.
25. Farkas R, Selmeci L, Tulassay Z, Pronai L. Superoxide-dismutase activity of the gastric mucosa in patients with Helicobacter pylori infection. Anticancer Res 23: 4309-4312, 2003.
26. Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124: 619-626, 1994.
27. 2+ and acute thermal stress induce protective events via the p38-MAPK signalling pathway in the perfused Rana ridibunda heart. J Exp Biol 210: 438-446, 2007.
28. Galmiche A, Rassow J, Doye A, Cagnol S, Chambard JC, Contamin S, de Thillot V, Just I, Ricci V, Solcia E, Van Obberghen E, Boquet P. The N-terminal 34 kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release. EMBO J 19: 6361-6370, 2000.
29. Gauthier NC, Monzo P, Gonzalez T, Doye A, Oldani A, Gounon P, Ricci V, Cormont M, Boquet P. Early endosomes associated with dynamic F-actin structures are required for late trafficking of H. pylori VacA toxin. J Cell Biol 177: 343-354, 2007.
30. Gauthier NC, Ricci V, Gounon P, Doye A, Tauc M, Poujeol P, Boquet P. Glycosylphosphatidylinositol-anchored proteins and actin cytoskeleton modulate chloride transport by channels formed by the Helicobacter pylori vacuolating cytotoxin VacA in HeLa cells. J Biol Chem 279: 9481-9489, 2004.
31. Gebert B, Fischer W, Weiss E, Hoffmann R, Haas R. Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301: 1099-1102, 2003.
32. Hale KK, Trollinger D, Rihanek M, Manthey CL. Differential expression and activation of p38 mitogen-activated protein kinase alpha, beta, gamma, and delta in inflammatory cell lineages. J Immunol 162: 4246-4252, 1999.
33. Hisatsune J, Yamasaki E, Nakayama M, Shirasaka D, Kurazono H, Katagata Y, Inoue H, Han J, Sap J, Yahiro K, Moss J, Hirayama T. Helicobacter pylori VacA enhances prostaglandin E(2) production through induction of cyclooxygenase 2 expression via a p38 mitogen-activated protein kinase/activating transcription factor 2 cascade in AZ-521 cells. Infect Immun 75: 4472-4481, 2007.
34. Huang P, Feng L, Oldham EA, Keating MJ, Plunkett W. Superoxide dismutase as a target for the selective killing of cancer cells. Nature 407: 390-395, 2000.
35. Huang Q, Bu S, Yu Y, Guo Z, Ghatnekar G, Bu M, Yang L, Lu B, Feng Z, Liu S, Wang F. Diazoxide prevents diabetes through inhibiting pancreatic beta-cells from apoptosis via Bcl-2/Bax rate and p38-beta mitogen-activated protein kinase. Endocrinology 148: 81-91, 2007.
36. Kapur R, Chandra S, Cooper R, McCarthy J, Williams DA. Role of p38 and ERK MAP kinase in proliferation of erythroid progenitors in response to stimulation by soluble and membrane isoforms of stem cell factor. Blood 100: 1287-1293, 2002.
37. Keates S, Keates AC, Warny M, Peek RM Jr, Murray PG, Kelly CP. Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cag+ and cag- Helicobacter pylori. J Immunol 163: 5552-5559, 1999.
38. Kim SJ, Ju JW, Oh CD, Yoon YM, Song WK, Kim JH, Yoo YJ, Bang OS, Kang SS, Chun JS. ERK-1/2 and p38 kinase oppositely regulate nitric oxide-induced apoptosis of chondrocytes in association with p53, caspase-3, and differentiation status. J Biol Chem 277: 1332-1339, 2002.
39. Konturek PC, Kania J, Konturek JW, Nikiforuk A, Konturek SJ, Hahn EG. H. pylori infection, atrophic gastritis, cytokines, gastrin, COX-2, PPAR gamma and impaired apoptosis in gastric carcinogenesis. Med Sci Monit 9: SR53-SR66, 2003.
40. Kuck D, Kolmerer B, Iking-Konert C, Krammer PH, Stremmel W, Rudi J. Vacuolating cytotoxin of Helicobacter pylori induces apoptosis in the human gastric epithelial cell line AGS. Infect Immun 69: 5080-5087, 2001.
41. Li Y, Wandinger-Ness A, Goldenring JR, Cover TL. Clustering and redistribution of late endocytic compartments in response to Helicobacter pylori vacuolating toxin. Mol Biol Cell 15: 1946-1959, 2004.
42. Lin Y, Kikuchi S, Obata Y, Yagyu K; Tokyo Research Group on Prevention of Gastric Cancer. Serum copper/zinc superoxide dismutase (Cu/Zn SOD) and gastric cancer risk: a case-control study. Jpn J Cancer Res 93: 1071-1075, 2002.
43. McClain MS, Cover TL. Expression of Helicobacter pylori vacuolating toxin in Escherichia coli. Infect Immun 71: 2266-2271, 2003.
44. Mizuki I, Shimoyama T, Fukuda S, Liu Q, Nakaji S, Munakata A. Association of gastric epithelial apoptosis with the ability of Helicobacter pylori to induce a neutrophil oxidative burst. J Med Microbiol 49: 521-524, 2000.
45. Nakayama M, Hisatsune J, Yamasaki E, Nishi Y, Wada A, Kurazono H, Sap J, Yahiro K, Moss J, Hirayama T. Clustering of Helicobacter pylori VacA in lipid rafts, mediated by its receptor, receptor-like protein tyrosine phosphatase beta, is required for intoxication in AZ-521 cells. Infect Immun 74: 6571-6580, 2006.
46. Nakayama M, Kimura M, Wada A, Yahiro K, Ogushi K, Niidome T, Fujikawa A, Shirasaka D, Aoyama N, Kurazono H, Noda M, Moss J, Hirayama T. Helicobacter pylori VacA activates the p38/activating transcription factor 2-mediated signal pathway in AZ-521 cells. J Biol Chem 279: 7024-7028, 2004.
47. Obst B, Wagner S, Sewing KF, Beil W. Helicobacter pylori causes DNA damage in gastric epithelial cells. Carcinogenesis 21: 1111-1115, 2000.
48. Pai P, Cover TL, Tarnawski AS. Helicobacter pylori vacuolating cytotoxin (VacA) disorganizes the cytoskeletal architecture of gastric epithelial cells. Biochem Biophys Res Commun 262: 245-250, 1999.
49. Papini E, Zoratti M, Cover TL. In search of the Helicobacter pylori VacA mechanism of action. Toxicon 39: 1757-1767, 2001.
50. Pillinger MH, Marjanovic N, Kim SY, Lee YC, Scher JU, Roper J, Abeles AM, Izmirly PI, Axelrod M, Pillinger MY, Tolani S, Dinsell V, Abramson SB, Blaser MJ. Helicobacter pylori stimulates gastric epithelial cell MMP-1 secretion via CagA-dependent and -independent ERK activation. J Biol Chem 282: 18722-18731, 2007.
51. Pinson KI, Dunbar L, Samuelson L, Gumucio DL. Targeted disruption of the mouse villin gene does not impair the morphogenesis of microvilli. Dev Dyn 211: 109-121, 1998.
52. Porras A, Zuluaga S, Black E, Valladares A, Alvarez AM, Ambrosino C, Benito M, Nebreda AR. P38 alpha mitogen-activated protein kinase sensitizes cells to apoptosis induced by different stimuli. Mol Biol Cell 15: 922-933, 2004.
53. Ranganathan AC, Nelson KK, Rodriguez AM, Kim KH, Tower GB, Rutter JL, Brinckerhoff CE, Huang TT, Epstein CJ, Jeffrey JJ, Melendez JA. Manganese superoxide dismutase signals matrix metalloproteinase expression via H2O2-dependent ERK1/2 activation. J Biol Chem 276: 14264-14270, 2001.
54. Recio JA, Merlino G. Hepatocyte growth factor/scatter factor activates proliferation in melanoma cells through p38 MAPK, ATF-2 and cyclin D1. Oncogene 21: 1000-1008, 2002.
55. Revenu C, Courtois M, Michelot A, Sykes C, Louvard D, Robine S. Villin severing activity enhances actin-based motility in vivo. Mol Biol Cell 18: 827-838, 2007.
56. Revenu C, Athman R, Robine S, Louvard D. The co-workers of actin filaments: from cell structures to signals. Nat Rev Mol Cell Biol 5: 635-646, 2004.
57. Rogers AB, Taylor NS, Whary MT, Stefanich ED, Wang TC, Fox JG. Helicobacter pylori but not high salt induces gastric intraepithelial neoplasia in B6129 mice. Cancer Res 65: 10709-10715, 2005.
58. Romano M, Ricci V, Zarrilli R. Mechanisms of disease: Helicobacter pylori-related gastric carcinogenesis-implications for chemoprevention. Nat Clin Pract Gastroenterol Hepatol 3: 622-632, 2006.
59. Rothstein JD, Bristol LA, Hosler B, Brown RH Jr, Kuncl RW. Chronic inhibition of superoxide dismutase produces apoptotic death of spinal neurons. Proc Natl Acad Sci USA 91: 4155-4159, 1994.
60. Seidman R, Gitelman I, Sagi O, Horwitz SB, Wolfson M. The role of ERK1/2 and p38 MAP-kinase pathways in taxol-induced apoptosis in human ovarian carcinoma cells. Exp Cell Res 268: 84 -92, 2001.
61. Smoot DT, Elliott TB, Verspaget HW, Jones D, Allen CR, Vernon KG, Bremner T, Kidd LC, Kim KS, Groupman JD, Ashktorab H. Influence of Helicobacter pylori on reactive oxygen-induced gastric epithelial cell injury. Carcinogenesis 21: 2091-2095, 2000.
62. Su B, Ceponis PJ, Sherman PM. Cytoskeletal rearrangements in gastric epithelial cells in response to Helicobacter pylori infection. J Med Microbiol 52: 861-867, 2003.
63. Tourian L Jr, Zhao H, Srikant CB. p38alpha, but not p38beta, inhibits the phosphorylation and presence of c-FLIPS in DISC to potentiate Fas-mediated caspase-8 activation and type I apoptotic signaling. J Cell Sci 117: 6459-6471, 2004.
64. Van Laethem A, Van Kelst S, Lippens S, Declercq W, Vandenabeele P, Janssens S, Vandenheede JR, Garmyn M, Agostinis P. Activation of p38 MAPK is required for Bax translocation to mitochondria, cytochrome c release and apoptosis induced by UVB irradiation in human keratinocytes. FASEB J 18: 1946-1948, 2004.
65. Willhite DC, Blanke SR. Helicobacter pylori vacuolating cytotoxin enters cells, localizes to the mitochondria, and induces mitochondrial membrane permeability changes correlated to toxin channel activity. Cell Microbiol 6: 143-154, 2004.
66. Willhite DC, Cover TL, Blank SR. Cellular vacuolation and mitochondrial cytochrome c release are independent outcomes of Helicobacter pylori vacuolating cytotoxin activity that are each dependent on membrane channel formation. J Biol Chem 278: 48204-48209, 2003.
67. Woo CH, You HJ, Cho SH, Eom YW, Chun JS, Yoo YJ, Kim JH. Leukotriene B(4) stimulates Rac-ERK cascade to generate reactive oxygen species that mediates chemotaxis. J Biol Chem 277: 8572-8578, 2002.
68. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326-1331. 1995.
69. Xu Q, Konta T, Nakayama K, Furusu A, Moreno-Manzano V, Lucio-Cazana J, Ishikawa Y, Fine LG, Yao J, Kitamura M. Cellular defense against H2O2-induced apoptosis via MAP kinase-MKP-1 pathway. Free Radic Biol Med 36: 985-993, 2004.
70. Yamasaki E, Wada A, Kumatori A, Nakagawa I, Funao J, Nakayama M, Hisatsune J, Kimura M, Moss J, Hirayama T. Helicobacter pylori vacuolating cytotoxin induces activation of the proapoptotic proteins Bax and Bak, leading to cytochrome c release and cell death, independent of vacuolation. J Biol Chem 281: 11250-11259, 2006.
71. Yoshimura T, Shimoyama T, Tanaka M, Sasaki Y, Fukuda S, Munakata A. Gastric mucosal inflammation and epithelial cell turnover are associated with gastric cancer in patients with Helicobacter pylori infection. J Clin Pathol 53: 532-536, 2000.
72. Zhuang S, Schnellmann RG. A death-promoting role for extracellular signal-regulated kinase. J Pharmacol Exp Ther 319: 991-997, 2006.
73. Zhuang S, Yan Y, Daubert RA, Schnellmann RG. Epiregulin promotes proliferation and migration of renal proximal tubular cells. Am J Physiol Renal Physiol 292: F440-F447, 2007.