Somatostatin stimulates menin gene expression by inhibiting protein kinase A

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 295, Issue 4, 2008, Pages

  Mensah Osman, Edith ^a   Zavros, Yana ^a   Merchant, Juanita L ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b BSRB 2051 ^*  (United States)

Author keywords

Forskolin; Gastrin; MEN1; Octreotide; SSTR2A

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; MESSENGER RNA; METHIONINE; OCTREOTIDE; SOMATOSTATIN; SOMATOSTATIN RECEPTOR;

ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CELL LINE; CONTROLLED STUDY; DUODENUM; ENZYME ACTIVITY; GENE EXPRESSION; HORMONE RELEASE; HUMAN; HUMAN CELL; HYPERGASTRINEMIA; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STOMACH ANTRUM; WILD TYPE;

ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DUODENUM; GASTRINS; GENE EXPRESSION; MICE; MICE, INBRED C57BL; OCTREOTIDE; PROTO-ONCOGENE PROTEINS; PYLORIC ANTRUM; RECEPTORS, SOMATOSTATIN; SOMATOSTATIN;

EID: 57349200454     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00607.2007     Document Type: Article

References (58)

1. Agarwal SK, Guru SC, Heppner C, Erdos MR, Collins RM, Park SY, Saggar S, Chandrasekharappa SC, Collins FS, Spiegel AM, Marx SJ, Burns AL. Menin interacts with the AP1 transcription factor JunD and represses JunD-activated transcription. Cell 96: 143-152, 1999.
2. Agarwal SK, Novotny EA, Crabtree JS, Weitzman JB, Yaniv M, Burns AL, Chandrasekharappa SC, Collins FS, Spiegel AM, Marx SJ. Transcription factor JunD, deprived of menin, switches from growth suppressor to growth promoter. Proc Natl Acad Sci USA 100: 10770-10775, 2003.
3. Alderton F, Humphrey PP, Sellers LA. High-intensity p38 kinase activity is critical for p21(cip1) induction and the antiproliferative function of G(i) protein-coupled receptors. Mol Pharmacol 59: 1119-1128, 2001.
4. Anlauf M, Perren A, Henopp T, Rudolf T, Garbrecht N, Schmitt A, Raffel A, Gimm O, Weihe E, Knoefel WT, Dralle H, Heitz PU, Komminoth P, Kloppel G. Allelic deletion of the MEN1 gene in duodenal gastrin and somatostatin cell neoplasms and their precursor lesions. Gut 56: 637-644, 2007.
5. Anlauf M, Perren A, Meyer CL, Schmid S, Saremaslani P, Kruse ML, Weihe E, Komminoth P, Heitz PU, Kloppel G. Precursor lesions in patients with multiple endocrine neoplasia type 1-associated duodenal gastrinomas. Gastroenterology 128: 1187-1198, 2005.
6. Arnold R, Simon B, Wied M. Treatment of neuroendocrine GEP tumours with somatostatin analogues: a review. Digestion 62, Suppl 1: 84-91, 2000.
7. Bachwich D, Merchant J, Brand SJ. Identification of a cis-regulatory element mediating somatostatin inhibition of epidermal growth factor-stimulated gastrin gene transcription. Mol Endocrinol 6: 1175-1184, 1992.
8. Biondi CA, Gartside MG, Waring P, Loffler KA, Stark MS, Magnuson MA, Kay GF, Hayward NK. Conditional inactivation of the MEN1 gene leads to pancreatic and pituitary tumorigenesis but does not affect normal development of these tissues. Mol Cell Biol 24: 3125-3131, 2004.
9. Brand SJ, Fuller PJ. Differential gastrin gene expression in rat gastrointestinal tract and pancreas during neonatal development. J Biol Chem 263: 5341-5347, 1988.
10. De Jong M, Valkema R, Jamar F, Kvols LK, Kwekkeboom DJ, Breeman WA, Bakker WH, Smith C, Pauwels S, Krenning EP. Somatostatin receptor-targeted radionuclide therapy of tumors: preclinical and clinical findings. Semin Nucl Med 32: 133-140, 2002.
11. Dockray GJ. The G. W. Harris Prize Lecture. The gut endocrine system and its control. Exp Physiol 79: 607-634, 1994.
12. Florio T. Molecular mechanisms of the antiproliferative activity of somatostatin receptors (SSTRs) in neuroendocrine tumors. Front Biosci 13: 822-840, 2008.
13. Ford MG, Valle JD, Soroka CJ, Merchant JL. EGF receptor activation stimulates endogenous gastrin gene expression in canine G cells and human gastric cell cultures. J Clin Invest 99: 2762-2771, 1997.
14. Fougner SL, Borota OC, Berg JP, Hald JK, Ramm-Pettersen J, Bollerslev J. The clinical response to somatostatin analogues in acromegaly correlates to the somatostatin receptor subtype 2a protein expression of the adenoma. Clin Endocrinol (Oxf) 68: 458-465, 2008.
15. Franklin DS, Godfrey VL, O'Brien DA, Deng C, Xiong Y. Functional collaboration between different cyclin-dependent kinase inhibitors suppresses tumor growth with distinct tissue specificity. Mol Cell Biol 20: 6147-6158, 2000.
16. Gibril F, Jensen RT. Zollinger-Ellison syndrome revisited: diagnosis, biologic markers, associated inherited disorders, and acid hypersecretion. Curr Gastroenterol Rep 6: 454-463, 2004.
17. Gobl AE, Berg M, Lopez-Egido JR, Oberg K, Skogseid B, Westin G. Menin represses JunD-activated transcription by a histone deacetylase-dependent mechanism. Biochim Biophys Acta 1447: 51-56, 1999.
18. Godley-Merchant J, Brand SJ. Regulation of the gastrin promoter by epidermal growth factor and neuropeptides. Proc Natl Acad Sci USA 86: 3036-3040, 1989.
19. Gugger M, Waser B, Kappeler A, Schonbrunn A, Reubi JC. Cellular detection of sst2A receptors in human gastrointestinal tissue. Gut 53: 1431-1436, 2004.
20. Gugger M, Waser B, Kappeler A, Schonbrunn A, Reubi JC. Immunohistochemical localization of somatostatin receptor sst2A in human gut and lung tissue: possible implications for physiology and carcinogenesis. Ann NY Acad Sci 1014: 132-136, 2004.
21. Guillermet-Guibert J, Lahlou H, Cordelier P, Bousquet C, Pyronnet S, Susini C. Physiology of somatostatin receptors. J Endocrinol Invest 28: 5-9, 2005.
22. Heppner C, Bilimoria KY, Agarwal SK, Kester M, Whitty LJ, Guru SC, Chandrasekharappa SC, Collins FS, Spiegel AM, Marx SJ, Burns AL. The tumor suppressor protein menin interacts with NF-kappaB proteins and inhibits NF-kappaB-mediated transactivation. Oncogene 20: 4917-4925, 2001.
23. Hofland LJ, Lamberts SW. Somatostatin receptors and disease: role of receptor subtypes. Baillieres Clin Endocrinol Metab 10: 163-176, 1996.
24. Hou W, Schubert ML. Gastric secretion. Curr Opin Gastroenterol 22: 593-598, 2006.
25. Hubina E, Nanzer AM, Hanson MR, Ciccarelli E, Losa M, Gaia D, Papotti M, Terreni MR, Khalaf S, Jordan S, Czirjak S, Hanzely Z, Nagy GM, Goth MI, Grossman AB, Korbonits M. Somatostatin analogues stimulate p27 expression and inhibit the MAP kinase pathway in pituitary tumours. Eur J Endocrinol 155: 371-379, 2006.
26. Jensen RT, Gibril F, Termanini B. Definition of the role of somatostatin receptor scintigraphy in gastrointestinal neuroendocrine tumor localization. Yale J Biol Med 70: 481-500, 1997.
27. Ji Y, Prasad NB, Novotny EA, Kaur S, Elkahloun A, Chen Y, Zhang RZ, Chu ML, Agarwal SK, Marx SJ, Collins FS, Chandrasekharappa SC. Mouse embryo fibroblasts lacking the tumor suppressor menin show altered expression of extracellular matrix protein genes. Mol Cancer Res 5: 1041-1051, 2007.
28. Kaji H, Canaff L, Lebrun JJ, Goltzman D, Hendy GN. Inactivation of menin, a Smad3-interacting protein, blocks transforming growth factor type beta signaling. Proc Natl Acad Sci USA 98: 3837-3842, 2001.
29. Karnik SK, Hughes CM, Gu X, Rozenblatt-Rosen O, McLean GW, Xiong Y, Meyerson M, Kim SK. Menin regulates pancreatic islet growth by promoting histone methylation and expression of genes encoding p27Kip1 and p18INK4c. Proc Natl Acad Sci USA 102: 14659-14664, 2005.
30. Kim H, Lee JE, Cho EJ, Liu JO, Youn HD. Menin, a tumor suppressor, represses JunD-mediated transcriptional activity by association with an mSin3A-histone deacetylase complex. Cancer Res 63: 6135-6139, 2003.
31. La P, Desmond A, Hou Z, Silva AC, Schnepp RW, Hua X. Tumor suppressor menin: the essential role of nuclear localization signal domains in coordinating gene expression. Oncogene 25: 3537-3546, 2006.
32. Lahlou H, Saint-Laurent N, Esteve JP, Eychene A, Pradayrol L, Pyronnet S, Susini C. sst2 Somatostatin receptor inhibits cell proliferation through Ras-, Rap1-, and B-Raf-dependent ERK2 activation. J Biol Chem 278: 39356-39371, 2003.
33. Lay JM, Bane G, Brunkan CS, Davis J, Lopez-Diaz L, Samuelson LC. Enteroendocrine cell expression of a cholecystokinin gene construct in transgenic mice and cultured cells. Am J Physiol Gastrointest Liver Physiol 288: G354-G361, 2005.
34. Low MJ. Clinical endocrinology and metabolism. The somatostatin neuroendocrine system: physiology and clinical relevance in gastrointestinal and pancreatic disorders. Best Pract Res Clin Endocrinol Metab 18: 607-622, 2004.
35. Low MJ, Otero-Corchon V, Parlow AF, Ramirez JL, Kumar U, Patel YC, Rubinstein M. Somatostatin is required for masculinization of growth hormone-regulated hepatic gene expression but not of somatic growth. J Clin Invest 107: 1571-1580, 2001.
36. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 277: 33275-33283, 2002.
37. Martinez V, Curi AP, Torkian B, Schaeffer JM, Wilkinson HA, Walsh JH, Tache Y. High basal gastric acid secretion in somatostatin receptor subtype 2 knockout mice. Gastroenterology 114: 1125-1132, 1998.
38. Mensah-Osman E, Labut E, Zavros Y, El-Zaatari M, Law DJ, Merchant JL. Regulated expression of the human gastrin gene in mice. Regul Pept. In Press.
39. Milne TA, Hughes CM, Lloyd R, Yang Z, Rozenblatt-Rosen O, Dou Y, Schnepp RW, Krankel C, Livolsi VA, Gibbs D, Hua X, Roeder RG, Meyerson M, Hess JL. Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors. Proc Natl Acad Sci USA 102: 749-754, 2005.
40. Mould AW, Duncan R, Serewko-Auret M, Loffler KA, Biondi C, Gartside M, Kay GF, Hayward NK. Global expression profiling of murine MEN1-associated tumors reveals a regulatory role for menin in transcription, cell cycle and chromatin remodelling. Int J Cancer 121: 776-783, 2007.
41. Patel YC. Somatostatin and its receptor family. Front Neuroendocrinol 20: 157-198, 1999.
42. Patel YC, Greenwood MT, Panetta R, Demchyshyn L, Niznik H, Srikant CB. The somatostatin receptor family. Life Sci 57: 1249-1265, 1995.
43. Patel YC, Greenwood MT, Warszynska A, Panetta R, Srikant CB. All five cloned human somatostatin receptors (hSSTR1-5) are functionally coupled to adenylyl cyclase. Biochem Biophys Res Commun 198: 605-612, 1994.
44. Portela-Gomes GM, Stridsberg M, Johansson H, Grimelius L. Colocalization of synaptophysin with different neuroendocrine hormones in the human gastrointestinal tract. Histochem Cell Biol 111: 49-54, 1999.
45. Ratineau C, Bernard C, Poncet G, Blanc M, Josso C, Fontaniere S, Calender A, Chayvialle JA, Zhang CX, Roche C. Reduction of menin expression enhances cell proliferation and is tumorigenic in intestinal epithelial cells. J Biol Chem 279: 24477-24484, 2004.
46. Reubi JC, Laissue J, Waser B, Horisberger U, Schaer JC. Expression of somatostatin receptors in normal, inflamed, and neoplastic human gastrointestinal tissues. Ann NY Acad Sci 733: 122-137, 1994.
47. Schmid HA. Pasireotide (SOM230): development, mechanism of action and potential applications. Mol Cell Endocrinol 286: 69-74, 2007.
48. Schonhoff SE, Giel-Moloney M, Leiter AB. Neurogenin 3-expressing progenitor cells in the gastrointestinal tract differentiate into both endocrine and non-endocrine cell types. Dev Biol 270: 443-454, 2004.
49. Shimon I. Somatostatin receptors in pituitary and development of somatostatin receptor subtype-selective analogs. Endocrine 20: 265-269, 2003.
50. Shimon I, Yan X, Taylor JE, Weiss MH, Culler MD, Melmed S. Somatostatin receptor (SSTR) subtype-selective analogues differentially suppress in vitro growth hormone and prolactin in human pituitary adenomas. Novel potential therapy for functional pituitary tumors. J Clin Invest 100: 2386-2392, 1997.
51. Shiotani A, Merchant JL. cAMP regulates gastrin gene expression. Am J Physiol Gastrointest Liver Physiol 269: G458-G464, 1995.
52. Stephen AE, Hodin RA. Neuroendocrine tumors of the pancreas, excluding gastrinoma. Surg Oncol Clin N Am 15: 497-510, 2006.
53. Theodoropoulou M, Zhang J, Laupheimer S, Paez-Pereda M, Erneux C, Florio T, Pagotto U, Stalla GK. Octreotide, a somatostatin analogue, mediates its antiproliferative action in pituitary tumor cells by altering phosphatidylinositol 3-kinase signaling and inducing Zac1 expression. Cancer Res 66: 1576-1582, 2006.
54. Wang Y, Giel-Moloney M, Rindi G, Leiter AB. Enteroendocrine precursors differentiate independently of Wnt and form serotonin expressing adenomas in response to active beta-catenin. Proc Natl Acad Sci USA 104: 11328-11333, 2007.
55. Zablewska B, Bylund L, Mandic SA, Fromaget M, Gaudray P, Weber G. Transcription regulation of the multiple endocrine neoplasia type 1 gene in human and mouse. J Clin Endocrinol Metab 88: 3845-3851, 2003.
56. Zavros Y, Eaton KA, Kang W, Rathinavelu S, Katukuri V, Kao JY, Samuelson LC, Merchant JL. Chronic gastritis in the hypochlorhydric gastrin-deficient mouse progresses to adenocarcinoma. Oncogene 24: 2354-2366, 2005.
57. Zavros Y, Kao JY, Merchant JL. Inflammation and cancer III. Somatostatin and the innate immune system. Am J Physiol Gastrointest Liver Physiol 286: G698-G701, 2004.
58. Zavros Y, Rieder G, Ferguson A, Samuelson LC, Merchant JL. Hypergastrinemia in response to gastric inflammation suppresses somatostatin. Am J Physiol Gastrointest Liver Physiol 282: G175-G183, 2002.