Glycine-extended gastrin inhibits apoptosis in colon cancer cells via separate activation of Akt and JNK pathways

Molecular and Cellular Endocrinology

Volumn 247, Issue 1-2, 2006, Pages 140-149

  Beales, Ian L P ^a,b   Ogunwobi, O ^b  

^a NORFOLK AND NORWICH UNIVERSITY HOSPITAL   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Akt protein; Gastrin; Janus kinase 2; JNK mitogen activated protein kinases; STAT3 protein; Transcription factor AP 1

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CELECOXIB; GASTRIN; GLYCINE; JANUS KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; P13 PROTEIN; PROTEIN; PROTEIN INHIBITOR; PROTEIN KINASE B; PROTEIN KINASE B BETA; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA FLANKING REGION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SERUM; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANTHRACENES; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; CHROMONES; COLONIC NEOPLASMS; GASTRINS; HUMANS; JANUS KINASE 2; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MORPHOLINES; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PYRAZOLES; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SULFONAMIDES; TRANSCRIPTION FACTOR AP-1; TYROSINE; TYRPHOSTINS;

EID: 33244495716     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2005.12.050     Document Type: Article

References (64)

1. S. Ahmed, R.F. Murphy, and S. Lovas Importance of N- and C-terminal regions of gastrin-Gly for preferential binding to high and low affinity gastrin-Gly receptors Peptides 26 2005 1207 1212
2. A. Aly, A. Shulkes, and G.S. Baldwin Short term infusion of glycine-extended gastrin(17) stimulates both proliferation and formation of aberrant crypt foci in rat colonic mucosa Int. J. Cancer 94 2001 307 313
3. S. Arico, S. Pattingre, C. Bauvy, P. Gane, A. Barbat, P. Codogno, and E. Ogier-Denis Celecoxib induces apoptosis by inhibiting 3-phosphoinositide- dependent protein kinase-1 activity in the human colon cancer HT-29 cell line J. Biol. Chem. 277 2002 27613 27621
4. R. Ashida, K. Tominaga, E. Sasaki, T. Watanabe, Y. Fujiwara, N. Oshitani, K. Higuchi, S. Mitsuyama, H. Iwao, and T. Arakawa AP-1 and colorectal cancer Inflammopharmacology 13 2005 113 125
5. S. Attoub, V. Noe, L. Pirola, E. Bruyneel, E. Chastre, M. Mareel, M.P. Wymann, and C. Gespach Leptin promotes invasiveness of kidney and colonic epithelial cells via phosphoinositide 3-kinase-, rho-, and rac-dependent signaling pathways FASEB J. 14 2000 2329 2338
6. G.S. Baldwin, and A. Shulkes Gastrin, gastrin receptors and colorectal carcinoma Gut 42 1998 581 584
7. I.L. Beales Gastrin and interleukin-1beta stimulate growth factor secretion from cultured rabbit gastric parietal cells Life Sci. 75 2004 2983 2995
8. J. Bromberg Stat proteins and oncogenesis J. Clin. Invest. 109 2002 1139 1142
9. J.F. Bromberg, M.H. Wrzeszczynska, G. Devgan, Y. Zhao, R.G. Pestell, C. Albanese, and J.E. Darnell Jr Stat3 as an oncogene Cell 98 1999 295 303
10. T.O. Chan, S.E. Rittenhouse, and P.N. Tsichlis AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide- dependent phosphorylation Annu. Rev. Biochem. 68 1999 965 1014
11. G.D. Ciccotosto, A. McLeish, K.J. Hardy, and A. Shulkes Expression, processing, and secretion of gastrin in patients with colorectal carcinoma Gastroenterology 109 1995 1142 1153
12. T. Decker, and P. Kovarik Serine phosphorylation of STATs Oncogene 19 2000 2628 2637
13. C.J. Dickinson Relationship of gastrin processing to colon cancer Gastroenterology 109 1996 1384 1387
14. G.J. Dockray, A. Varro, R. Dimaline, and T. Wang The gastrins: their production and biological activities Annu. Rev. Physiol. 63 2001 119 139
15. R. Eferl, and E.F. Wagner AP-1: a double-edged sword in tumorigenesis Nat. Rev. Cancer 3 2003 859 868
16. A. Ferrand, A. Kowalski-Chauvel, C. Bertrand, L. Pradayrol, D. Fourmy, M. Dufresne, and C. Seva Involvement of JAK2 upstream of the PI 3-kinase in cell-cell adhesion regulation by gastrin Exp. Cell Res. 301 2004 128 138
17. A. Ferrand, C. Bertrand, G. Portolan, G. Cui, J. Carlson, L. Pradayrol, D. Fourmy, M. Dufresne, T.C. Wang, and C. Seva Signaling pathways associated with colonic mucosa hyperproliferation in mice overexpressing gastrin precursors Cancer Res. 65 2005 2770 2777
18. H. Frucht, A.F. Gazdar, J.A. Park, H. Oie, and R.T. Jensen Characterization of functional receptors for gastrointestinal hormones on human colon cancer cells Cancer Res. 52 1992 1114 1122
19. R. Grau, M.A. Iniguez, and M. Fresno Inhibition of activator protein 1 activation, vascular endothelial growth factor, and cyclooxygenase-2 expression by 15-deoxy-Delta12 14-prostaglandin J2 in colon carcinoma cells: evidence for a redox-sensitive peroxisome proliferator-activated receptor-gamma-independent mechanism Cancer Res. 64 2004 5162 5171
20. F. Hollande, A. Imdahl, T. Mantamadiotis, G.D. Ciccotosto, A. Shulkes, and G.S. Baldwin Glycine-extended gastrin acts as an autocrine growth factor in a nontransformed colon cell line Gastroenterology 113 1997 1576 1588
21. G. Huls, J.J. Koornstra, and J.H. Kleibeuker Non-steroidal anti-inflammatory drugs and molecular carcinogenesis of colorectal carcinomas Lancet 362 2003 230 232
22. Y.T. Ip, and R.J. Davis Signal transduction by the c-Jun N-terminal kinase (JNK) - from inflammation to development Curr. Opin. Cell Biol. 10 1998 205 219
23. V.N. Ivanov, M. Krasilnikov, and Z. Ronai Regulation of Fas expression by STAT3 and c-Jun is mediated by phosphatidylinositol 3-kinase-AKT signaling J. Biol. Chem. 277 2002 4932 4944
24. K. Iwase, B.M. Evers, M.R. Hellmich, Y.S. Guo, S. Higashide, H.J. Kim, and C.M. Townsend Jr. Regulation of growth of human gastric cancer by gastrin and glycine-extended progastrin Gastroenterology 113 1997 782 790
25. S.M. Jacobs-Helber, A. Wickrema, M.J. Birrer, and S.T. Sawyer AP1 regulation of proliferation and initiation of apoptosis in erythropoietin- dependent erythroid cells Mol. Cell Biol. 18 1998 3699 3707
26. S. Jensen, K. Borch, L. Hilsted, and J.F. Rehfeld Progastrin processing during antral G-cell hypersecretion in humans Gastroenterology 96 1989 1063 1070
27. X.H. Jiang, S.K. Lam, M.C. Lin, S.H. Jiang, H.F. Kung, E.D. Slosberg, J.W. Soh, I.B. Weinstein, and B.C. Wong Novel target for induction of apoptosis by cyclo-oxygenase-2 inhibitor SC-236 through a protein kinase C-beta(1)-dependent pathway Oncogene 21 2002 6113 6122
28. W.S. Jeong, I.W. Kim, R. Hu, and A.N. Kong Modulation of AP-1 by natural chemopreventative compounds in human colon HT-29 cancer cell line Pharm. Res. 21 2004 649 660
29. T. Kallunki, T. Deng, M. Hibi, and M. Karin c-Jun can recruit JNK to phosphorylate dimerization partners via specific docking interactions Cell 87 1996 929 939
30. M.L. Kochman, J. DelValle, C.J. Dickinson, and C.R. Boland Post-translational processing of gastrin in neoplastic human colonic tissues Biochem. Biophys. Res. Commun. 189 1992 1165 1169
31. T.J. Koh, G.J. Dockray, A. Varro, R.J. Cahill, C.A. Dangler, J.G. Fox, and T.C. Wang Overexpression of glycine-extended gastrin in transgenic mice results in increased colonic proliferation J. Clin. Invest. 103 1999 1119 1126
32. T.J. Koh, C.J. Bulitta, J.V. Fleming, G.J. Dockray, A. Varro, and T.C. Wang Gastrin is a target of the beta-catenin/TCF-4 growth-signaling pathway in a model of intestinal polyposis J. Clin. Invest. 106 2000 533 539
33. X.T. Ma, S. Wang, Y.J. Ye, R.Y. Du, Z.R. Cui, and M. Somsouk Constitutive activation of Stat3 signaling pathway in human colorectal carcinoma World J. Gastroenterol. 10 2004 1569 1573
34. Y. Matsushima, Y. Kinoshita, H. Nakata, Y. Inomoto-Naribayashi, M. Asahara, C. Kawanami, A. Nakamura, M. Ito, T. Matsui, and T. Fujiwara Gastrin receptor gene expression in several human carcinomas Jpn. J. Cancer Res. 85 1994 819 824
35. F. Mechta-Grigoriou, D. Gerald, and M. Yaniv The mammalian Jun proteins: redundancy and specificity Oncogene 20 2001 2378 2389
36. J. Nemeth, B. Taylor, S. Pauwels, A. Varro, and G.J. Dockray Identification of progastrin derived peptides in colorectal carcinoma extracts Gut 34 1993 90 95
37. R. Pai, C. Lin, T. Tran, and A. Tarnawski Leptin activates STAT and ERK2 pathways and induces gastric cancer cell proliferation Biochem. Biophys. Res. Commun. 331 2005 984 992
38. S. Park, E.R. Hahm, D.K. Lee, and C.H. Yang Inhibition of AP-1 transcription activator induces myc-dependent apoptosis in HL60 cells J. Cell Biochem. 91 2004 973 986
39. Ogunwobi, O.O., Beales, I.L., 2005. Glycine-extended gastrin stimulates proliferation and inhibits apoptosis in colon cancer cells via cyclo-oxygenase-independent pathways. Regul. Pept. epub. doi: 10.1016/j.regpep.2005.08.002.
40. S. Okugawa, Y. Ota, T. Kitazawa, K. Nakayama, S. Yanagimoto, K. Tsukada, M. Kawada, and S. Kimura Janus kinase 2 is involved in lipopolysaccharide- induced activation of macrophages Am. J. Physiol. Cell Physiol. 285 2003 C399 C408
41. S. Ramamoorthy, V. Stepan, and A. Todisco Intracellular mechanisms mediating the anti-apoptotic action of gastrin Biochem. Biophys. Res. Commun. 323 2004 44 48
42. C. Seva, C.J. Dickinson, and T. Yamada Growth-promoting effects of glycine-extended progastrin Science 265 1994 410 412
43. E. Shaulian, and M. Karin AP-1 in cell proliferation and survival Oncogene 20 2001 2390 2400
44. E. Shaulian, and M. Karin AP-1 as a regulator of cell life and death Nat. Cell Biol. 4 2002 E131 E136
45. R.K. Siddheshwar, J.C. Gray, and S.B. Kelly Plasma levels of progastrin but not amidated gastrin or glycine extended gastrin are elevated in patients with colorectal carcinoma Gut 48 2001 47 52
46. A.M. Smith, and S.A. Watson Gastrin and gastrin receptor activation: an early event in the adenoma-carcinoma sequence Gut 47 2000 820 824
47. R.F. Souza, K. Shewmake, L.S. Terada, and S.J. Spechler Acid exposure activates the mitogen-activated protein kinase pathways in Barrett's esophagus Gastroenterology 122 2002 299 307
48. G. Steinbach, P.M. Lynch, R.K. Phillips, M.H. Wallace, E. Hawk, G.B. Gordon, N. Wakabayashi, B. Saunders, Y. Shen, T. Fujimura, L.K. Su, and B. Levin The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis N. Engl. J. Med. 342 2000 1946 1952
49. V.M. Stepan, D.F. Krametter, M. Matsushima, A. Todisco, J. DelValle, and C.J. Dickinson Glycine-extended gastrin regulates HEK cell growth Am. J. Physiol. 277 1999 R572 R581
50. V.M. Stepan, M. Sawada, A. Todisco, and C.J. Dickinson Glycine-extended gastrin exerts growth-promoting effects on human colon cancer cells Mol. Med. 5 1999 147 159
51. V. Stepan, S. Ramamoorthy, N. Pausawasdi, C.D. Logsdon, F.K. Askari, and A. Todisco Role of small GTP binding proteins in the growth-promoting and antiapoptotic actions of gastrin Am. J. Physiol. Gastrointest. Liver Physiol. 287 2004 G715 G725
52. R. Suto, K. Tominaga, H. Mizuguchi, E. Sasaki, K. Higuchi, S. Kim, H. Iwao, and T. Arakawa Dominant-negative mutant of c-Jun gene transfer: a novel therapeutic strategy for colorectal cancer Gene Ther. 11 2004 187 193
53. K. Tanabe, S. Okuya, Y. Tanizawa, A. Matsutani, and Y. Oka Leptin induces proliferation of pancreatic beta cell line MIN6 through activation of mitogen-activated protein kinase Biochem. Biophys. Res. Commun. 241 1997 765 768
54. J.E. Thompson, and C.B. Thompson Putting the rap on Akt J. Clin. Oncol. 22 2004 4217 4226
55. C.M. Thorburn, G.D. Friedman, C.J. Dickinson, J.H. Vogelman, N. Orentreich, and J. Parsonnet Gastrin and colorectal cancer: a prospective study Gastroenterology 115 1998 275 280
56. A. Todisco, Y. Takeuchi, C. Seva, C.J. Dickinson, and T. Yamada Gastrin and glycine-extended progastrin processing intermediates induce different programs of early gene activation J. Biol. Chem. 270 1995 28337 28341
57. A. Todisco, Y. Takeuchi, A. Urumov, J. Yamada, V.M. Stepan, and T. Yamada Molecular mechanisms for the growth factor action of gastrin Am. J. Physiol. 273 1997 G891 G898
58. A. Todisco, S. Ramamoorthy, T. Witham, N. Pausawasdi, S. Srinivasan, C.J. Dickinson, F.K. Askari, and D. Krametter Molecular mechanisms for the antiapoptotic action of gastrin Am. J. Physiol. Gastrointest. Liver Physiol. 280 2001 G298 G307
59. A. Varro, S. Voronina, and G.J. Dockray Pathways of processing of the gastrin precursor in rat antral mucosa J. Clin. Invest. 95 1995 1642 1649
60. T.C. Wang, T.J. Koh, A. Varro, R.J. Cahill, C.A. Dangler, J.G. Fox, and G.J. Dockray Processing and proliferative effects of human progastrin in transgenic mice J. Clin. Invest. 98 1996 1918 1929
61. S.A. Watson, D. Michaeli, S. Grimes, T.M. Morris, G. Robinson, A. Varro, T.A. Justin, and J.D. Hardcastle Gastrimmune raises antibodies that neutralize amidated and glycine-extended gastrin-17 and inhibit the growth of colon cancer Cancer Res. 56 1996 880 885
62. B.C. Wong, X.H. Jiang, M.C. Lin, S.P. Tu, J.T. Cui, S.H. Jiang, W.M. Wong, M.F. Yuen, S.K. Lam, and H.F. Kung Cyclooxygenase-2 inhibitor (SC-236) suppresses activator protein-1 through c-Jun NH2-terminal kinase Gastroenterology 126 2004 136 147
63. R. Yamazaki, N. Kusunoki, T. Matsuzaki, S. Hashimoto, and S. Kawai Selective cyclooxygenase-2 inhibitors show a differential ability to inhibit proliferation and induce apoptosis of colon adenocarcinoma cells FEBS Lett. 531 2002 278 284
64. X.M. Zhou, B.C. Wong, X.M. Fan, H.B. Zhang, M.C. Lin, H.F. Kung, D.M. Fan, and S.K. Lam Non-steroidal anti-inflammatory drugs induce apoptosis in gastric cancer cells through up-regulation of bax and bak Carcinogenesis 22 2001 1393 1397