Inducible cAMP early repressor suppresses gastrin-mediated activation of cyclin D1 and c-fos gene expression

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 292, Issue 4, 2007, Pages

  Steigedal, Tonje S ^a   Bruland, Torunn ^a   Misund, Kristine ^a   Thommesen, Liv ^a   Lægreid, Astrid ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Gastrin; Gastrointestinal proliferation; Neuroendocrine gene regulation

Indexed keywords

CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIN D1; GASTRIN; PROTEIN C FOS;

ANIMAL CELL; ARTICLE; CELL LINE; CELL PROLIFERATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; RAT; REPRESSOR GENE; TRANSCRIPTION INITIATION;

ANIMALS; CELL LINE, TUMOR; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT MODULATOR; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLINS; FORSKOLIN; GASTRINS; GENE EXPRESSION; GENES, REPORTER; KINETICS; LUCIFERASES; PANCREAS, EXOCRINE; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PROMOTER REGIONS (GENETICS); PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANS-ACTIVATION (GENETICS); TRANSFECTION;

EID: 34147163917     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00287.2006     Document Type: Article

References (56)

1. D'Adda T, Annibale B, Delle Fave G, Bordi C. Oxyntic endocrine cells of hypergastrinaemic patients. Differential response to antrectomy or octreotide. Gut 38: 668-674, 1996.
2. Desdouets C, Matesic G, Molina CA, Foulkes NS, Sassone-Corsi P, Brechot C, Sobczak-Thepot J. Cell cycle regulation of cyclin A gene expression by the cyclic AMP-responsive transcription factors CREB and CREM. Mol Cell Biol 15: 3301-3309, 1995.
3. Deutsch PJ, Sun Y. The 38-amino acid form of pituitary adenylate cyclase-activating polypeptide stimulates dual signaling cascades in PC12 cells and promotes neurite outgrowth. J Biol Chem 267: 5108-5113, 1992.
4. Dockray G, Dimaline R, Varro A. Gastrin: old hormone, new functions. Pflügers Arch 449: 344-355, 2005.
5. Dockray GJ, Varro A, Dimaline R, Wang T. The gastrins: their production and biological activities. Annu Rev Physiol 63: 119-139, 2001.
6. Foulkes NS, Borjigin J, Snyder SH, Sassone-Corsi P. Transcriptional control of circadian hormone synthesis via the CREM feedback loop. Proc Natl Acad Sci USA 93: 14140-14145, 1996.
7. Friis-Hansen L, Sundler F, Li Y, Gillespie PJ, Saunders TL, Greenson JK, Owyang C, Rehfeld JF, Samuelson LC. Impaired gastric acid secretion in gastrin-deficient mice. Am J Physiol Gastrointest Liver Physiol 274: G561-G568, 1998.
8. Gilman MZ, Wilson RN, Weinberg RA. Multiple protein-binding sites in the 5-flanking region regulate c-fos expression. Mol Cell Biol 6: 4305-4316, 1986.
9. Gough DB, Thompson GB, Crotty TB, Donohue JH, Kvols LK, Carney JA, Grant CS, Nagorney DM. Diverse clinical and pathologic features of gastric carcinoid and the relevance of hypergastrinemia. World J Surg 18: 473-479; discussion 479-480, 1994.
10. Hofsli E, Thommesen L, Norsett K, Falkmer S, Syversen U, Sandvik A, Laegreid A. Expression of chromogranin A and somatostatin receptors in pancreatic AR42J cells. Mol Cell Endocrinol 194: 165-173, 2002.
11. Inada A, Hamamoto Y, Tsuura Y, Miyazaki J, Toyokuni S, Ihara Y, Nagai K, Yamada Y, Bonner-Weir S, Seino Y. Overexpression of inducible cyclic AMP early repressor inhibits transactivation of genes and cell proliferation in pancreatic beta cells. Mol Cell Biol 24: 2831-2841, 2004.
12. Koh TJ, Goldenring JR, Ito S, Mashimo H, Kopin AS, Varro A, Dockray GJ, Wang TC. Gastrin deficiency results in altered gastric differentiation and decreased colonic proliferation in mice. Gastroenterology 113: 1015-1025, 1997.
13. Kucharczak J, Pannequin J, Camby I, Decaestecker C, Kiss R, Martinez J. Gastrin induces over-expression of genes involved in human U373 glioblastoma cell migration. Oncogene 20: 7021-7028, 2001.
14. Lalli E, Sassone-Corsi P. Signal transduction and gene regulation: the nuclear response to cAMP. J Biol Chem 269: 17359-17362, 1994.
15. Lauffer JM, Modlin IM, Hinoue T, Kidd M, Zhang T, Schmid SW, Tang LH. Pituitary adenylate cyclase-activating polypeptide modulates gastric enterochromaffin-like cell proliferation in rats. Gastroenterology 116: 623-635, 1999.
16. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408, 2001.
17. Miller AD, Curran T, Verma IM. c-fos protein can induce cellular transformation: a novel mechanism of activation of a cellular oncogene. Cell 36: 51-60, 1984.
18. Molina CA, Foulkes NS, Lalli E, Sassone-Corsi P. Inducibility and negative autoregulation of CREM: an alternative promoter directs the expression of ICER, an early response repressor. Cell 75: 875-886, 1993.
19. Motokura T, Arnold A. PRAD1/cyclin D1 proto-oncogene: genomic organization, 5- DNA sequence, and sequence of a tumor-specific rearrangement breakpoint. Genes Chromosomes Cancer 7: 89-95, 1993.
20. Mousses S, Caplen NJ, Cornelison R, Weaver D, Basik M, Hautaniemi S, Elkahloun AG, Lotufo RA, Choudary A, Dougherty ER, Suh E, Kallioniemi O. RNAi microarray analysis in cultured mammalian cells. Genome Res 13: 2341-2347, 2003.
21. Oda K, Okabayashi T, Kataoka M, Takeda A, Shibuya Y, Orita K, Tanaka N. Evaluation of cyclin D1 mRNA expression in gastric and colorectal cancers. Res Commun Mol Pathol Pharmacol 105: 237-252, 1999.
22. Pestell RG, Albanese C, Reutens AT, Segall JE, Lee RJ, Arnold A. The cyclins and cyclin-dependent kinase inhibitors in hormonal regulation of proliferation and differentiation. Endocr Rev 20: 501-534, 1999.
23. Pradeep A, Sharma C, Sathyanarayana P, Albanese C, Fleming JV, Wang TC, Wolfe MM, Baker KM, Pestell RG, Rana B. Gastrin-mediated activation of cyclin D1 transcription involves beta-catenin and CREB pathways in gastric cancer cells. Oncogene 23: 3689-3699, 2004.
24. Qvigstad G, Falkmer S, Westre B, Waldum HL. Clinical and histopathological tumour progression in ECL cell carcinoids ("ECLomas" ). APMIS 107: 1085-1092, 1999.
25. Qvigstad G, Qvigstad T, Westre B, Sandvik AK, Brenna E, Waldum HL. Neuroendocrine differentiation in gastric adenocarcinomas associated with severe hypergastrinemia and/or pernicious anemia. APMIS 110: 132-139, 2002.
26. Razavi R, Ramos JC, Yehia G, Schlotter F, Molina CA. ICER-IIgamma is a tumor suppressor that mediates the antiproliferative activity of cAMP. Oncogene 17: 3015-3019, 1998.
27. Reubi JC, Laderach U, Waser B, Gebbers JO, Robberecht P, Laissue JA. Vasoactive intestinal peptide/pituitary adenylate cyclase-activating peptide receptor subtypes in human tumors and their tissues of origin. Cancer Res 60: 3105-3112, 2000.
28. Richards ML, Gauger P, Thompson NW, Giordano TJ. Regression of type II gastric carcinoids in multiple endocrine neoplasia type 1 patients with Zollinger-Ellison syndrome after surgical excision of all gastrinomas. World J Surg 28: 652-658, 2004.
29. Rindi G, Luinetti O, Cornaggia M, Capella C, Solcia E. Three subtypes of gastric argyrophil carcinoid and the gastric neuroendocrine carcinoma: a clinicopathologic study. Gastroenterology 104: 994-1006, 1993.
30. Rosenberg D, Groussin L, Jullian E, Perlemoine K, Bertagna X, Bertherat J. Role of the PKA-regulated transcription factor CREB in development and tumorigenesis of endocrine tissues. Ann NY Acad Sci 968: 65-74, 2002.
31. Ruchaud S, Seite P, Foulkes NS, Sassone-Corsi P, Lanotte M. The transcriptional repressor ICER and cAMP-induced programmed cell death. Oncogene 15: 827-836, 1997.
32. Sassone-Corsi P. Transcription factors responsive to cAMP. Annu Rev Cell Dev Biol 11: 355-377, 1995.
33. Scemama JL, De Vries L, Pradayrol L, Seva C, Tronchere H, Vaysse N. Cholecystokinin and gastrin peptides stimulate ODC activity in a rat pancreatic cell line. Am J Physiol Gastrointest Liver Physiol 256: G846-G850, 1989.
34. Servillo G, Penna L, Foulkes NS, Magni MV, Della Fazia MA, Sassone-Corsi P. Cyclic AMP signalling pathway and cellular proliferation: induction of CREM during liver regeneration. Oncogene 14: 1601-1606, 1997.
35. Seva C, Scemama JL, Bastie MJ, Pradayrol L, Vaysse N. Lorglumide and loxiglumide inhibit gastrin-stimulated DNA synthesis in a rat tumoral acinar pancreatic cell line (AR42J). Cancer Res 50: 5829-5833, 1990.
36. Shankley NP, Welsh NJ, Black JW. Histamine dependence of pentagastrin-stimulated gastric acid secretion in rats. Yale J Biol Med 65: 613-619, 1992.
37. Sherwood NM, Krueckl SL, McRory JE. The origin and function of the pituitary adenylate cyclase-activating polypeptide (PACAP)/glucagon superfamily. Endocr Rev 21: 619-670, 2000.
38. Smith AM, Watson SA, Caplin M, Clarke P, Griffin N, Varro A, Hardcastle JD. Gastric carcinoid expresses the gastrin autocrine pathway. Br J Surg 85: 1285-1289, 1998.
39. Solcia E, Rindi G, Havu N, Elm G. Qualitative studies of gastric endocrine cells in patients treated long-term with omeprazole. Scand J Gastroenterol Suppl 166: 129-137; discussion 138-129, 1989.
40. Song DH, Rana B, Wolfe JR, Crimmins G, Choi C, Albanese C, Wang TC, Pestell RG, Wolfe MM. Gastrin-induced gastric adenocarcinoma growth is mediated through cyclin D1. Am J Physiol Gastrointest Liver Physiol 285: G217-G222, 2003.
41. Stehle JH, Foulkes NS, Molina CA, Simonneaux V, Pevet P, Sassone-Corsi P. Adrenergic signals direct rhythmic expression of transcriptional repressor CREM in the pineal gland. Nature 365: 314-320, 1993.
42. Thommesen L, Hofsli E, Paulssen RH, Anthonsen MW, Laegreid A. Molecular mechanisms involved in gastrin-mediated regulation of cAMP-responsive promoter elements. Am J Physiol Endocrinol Metab 281: E1316-E1325, 2001.
43. Thommesen L, Norsett K, Sandvik AK, Hofsli E, Laegreid A. Regulation of inducible cAMP early repressor expression by gastrin and cholecystokinin in the pancreatic cell line AR42J. J Biol Chem 275: 4244-4250, 2000.
44. Todisco A, Takeuchi Y, Urumov A, Yamada J, Stepan VM, Yamada T. Molecular mechanisms for the growth factor action of gastrin. Am J Physiol Gastrointest Liver Physiol 273: G891-G898, 1997.
45. Treisman R. Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5- element and c-fos 3- sequences. Cell 42: 889-902, 1985.
46. Waldum HL, Brenna E, Kleveland PM, Sandvik AK. Gastrin-physiological and pathophysiological role: clinical consequences. Dig Dis 13: 25-38, 1995.
47. Waldum HL, Haugen OA, Isaksen C, Mecsei R, Sandvik AK. Enterochromaffin-like tumour cells in the diffuse but not the intestinal type of gastric carcinomas. Scand J Gastroenterol Suppl 180: 165-169, 1991.
48. Waldum HL, Sandvik AK, Brenna E, Petersen H. Gastrin-histamine sequence in the regulation of gastric acid secretion. Gut 32: 698-701, 1991.
49. Waldum HL, Aase S, Kvetnoi I, Brenna E, Sandvik AK, Syversen U, Johnsen G, Vatten L, Polak JM. Neuroendocrine differentiation in human gastric carcinoma. Cancer 83: 435-444, 1998.
50. Wang TC, Bonner-Weir S, Oates PS, Chulak M, Simon B, Merlino GT, Schmidt EV, Brand SJ. Pancreatic gastrin stimulates islet differentiation of transforming growth factor alpha-induced ductular precursor cells. J Clin Invest 92: 1349-1356, 1993.
51. Wang TC, Koh TJ, Varro A, Cahill RJ, Dangler CA, Fox JG, Dockray GJ. Processing and proliferative effects of human progastrin in transgenic mice. J Clin Invest 98: 1918-1929, 1996.
52. Watanabe G, Howe A, Lee RJ, Albanese C, Shu IW, Karnezis AN, Zon L, Kyriakis J, Rundell K, Pestell RG. Induction of cyclin D1 by simian virus 40 small tumor antigen. Proc Natl Acad Sci USA 93: 12861-12866, 1996.
53. Watson SA, Clarke PA, Smith AM, Varro A, Michaeli D, Grimes S, Caplin M, Hardcastle JD. Expression of CCKB/gastrin receptor isoforms in gastro-intestinal tumour cells. Int J Cancer 77: 572-577, 1998.
54. Yehia G, Razavi R, Memin E, Schlotter F, Molina CA. The expression of inducible cAMP early repressor (ICER) is altered in prostate cancer cells and reverses the transformed phenotype of the LNCaP prostate tumor cell line. Cancer Res 61: 6055-6059, 2001.
55. Yehia G, Schlotter F, Razavi R, Alessandrini A, Molina CA. Mitogen-activated protein kinase phosphorylates and targets inducible cAMP early repressor to ubiquitin-mediated destruction. J Biol Chem 276: 35272-35279, 2001.
56. Zhukova E, Sinnett-Smith J, Wong H, Chiu T, Rozengurt E. CCK(B)/gastrin receptor mediates synergistic stimulation of DNA synthesis and cyclin D1, D3, and E expression in Swiss 3T3 cells. J Cell Physiol 189: 291-305, 2001.