Menin and TGF-β superfamily member signaling via the Smad pathway in pituitary, parathyroid and osteoblast

Hormone and Metabolic Research

Volumn 37, Issue 6, 2005, Pages 375-379

  Hendy, C N ^a,b   Kaji, H ^c   Sowa, H ^c   Lebrun, J J ^a,b   Canaff, L ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b ROYAL VICTORIA HOSPITAL   (Canada)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Anterior pituitary; Menin; Osteoblast; Parathyroid

Indexed keywords

ACTIVIN; ANTISENSE OLIGONUCLEOTIDE; GROWTH INHIBITOR; METHIONINE; PARATHYROID HORMONE; PROLACTIN; SMAD1 PROTEIN; SMAD3 PROTEIN; SMAD5 PROTEIN; TRANSCRIPTION FACTOR PIT 1; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA;

ADENOHYPOPHYSIS; BONE DEVELOPMENT; CELL CULTURE; CELL MATURATION; CELL PROLIFERATION; HEMODIALYSIS; HEMOLYTIC UREMIC SYNDROME; HYPOPHYSIS CELL; MESENCHYME CELL; MULTIPLE ENDOCRINE NEOPLASIA; NONHUMAN; OSTEOBLAST; PARATHYROID CELL; PARATHYROID HORMONE RELEASE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DNA-BINDING PROTEINS; HUMANS; MICE; MICE, MUTANT STRAINS; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1; OSTEOBLASTS; PITUITARY GLAND; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD1 PROTEIN; THYROID GLAND; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 22444444114     PISSN: 00185043     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2005-870152     Document Type: Review

References (49)

1. Chandrasekharappa SC, Guru SC, Manickam P, Olufemi SE, Collins FS, Emmert-Buck MR, Debelenko LV, Zhuang Z, Lubensky IA, Liotta LA, Crabtree JS, Wang Y, Roe BA, Weisemann J, Boguski MS, Agarwal SK, Rester MB, Kim YS, Heppner C, Dong Q, Spiegel AM, Burns AL, Marx SJ. Positional cloning of the gene for multiple endocrine neoplasia type 1. Science (Wash. DC) 1997; 276: 404-407
2. Guru SC, Goldsmith PK, Burns AL, Marx SJ, Spiegel AM, Collins FS, Chandrasekharappa SC. Menin, the product of the MEN1 gene, is a nuclear protein. Proc Natl Acad Sci USA 1998; 95: 1630-1634
3. Kaji H, Canaff L, Goltzman D, Hendy GN. Cell cycle regulation of menin expression. Cancer Res 1999; 59: 5097-5101
4. The European Consortium on MEN1. Identification of the multiple endocrine neoplasia type 1 (MEN1) gene. Hum Mol Genet 1997; 6: 1177-1183
5. Crabtree JS, Scachetti PC, Ward JM, Garrett-Beal L, Emmert-Buck MR, Edgemon KA, Lorang D, Libutti SK, Chandrasekharappa SC, Marx SJ, Spiegel AM, Collins FS. A mouse model of multiple endocrine neoplasia type 1 develops multiple endocrine tumors. Proc Natl Acad Sci USA 2001; 98: 1118-1123
6. Bertolino P, Tong WM, Galendo D, Wang ZQ Zhang CX. Heterozygous Men1 mutant mice develop a range of endocrine tumors mimicking multiple endocrine neoplasia type 1. Mol Endocrinol 2003; 17: 1880-1892
7. Bertolino P, Radovanovic I, Casse H, Aguzzi A, Wang ZQ, Zhang CX. Genetic ablation of the tumor suppressor menin causes lethality at mid-gestation ith defects in multiple organs. Mech Dev 2003; 120: 549-560
8. Hughes CM, Rozenblatt-Rosen O, Milne TA, Copeland TD, Levine SS, Lee JC, Hayes DN, Shanmugan KS, Bhattachariee A, Biondi CA, Kay GF, Hayward NK, Hess JL, Meyerson M. Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol Cell 2004; 13:587-597
9. Yokoyama A, Wang Z, Wysocka J, Sanyal M, Aufiero DJ, Kitabayushi I, Herr W, Cleary ML Leukemia proto-oncogene MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol 2004; 24: 5639-5649
10. Suphapeetiporn K, Greally JM, Walpita D, Ashley T, Bale AE. MEN1 tumor-suppressor protein localizes to telomeres during meiosis. Gene Chromosome Cancer 2002; 35: 81-85
11. Lin SY, Elledge SJ. Multiple tumor suppressor pathways negatively regulate telomerase. Cell 2003; 113: 881-889
12. Sukhodolets KE, Hickman AB, Agarwal SK, Sukhodolets MV, Obungu VH, Novotny EA, Crabtree JS, Chandrasekharappa SC, Collins FS, Spiegel AM, Burns AL, Marx SJ. The 32-kilodalton subunit of replication protein A interacts with menin, the product of the MEN1 tumor suppressor gene. Mol Cell Biol 2003; 23: 493-509
13. Jin S, Mao H, Schnepp RW, Sykes SM, Silva AC, D'Andrea AD, Hua X. Menin associates with FANCD2, a protein involved in repair of DNA damage. Cancer Res 2003; 63: 4204-4210
14. Poisson A, Zablewska B, Gaudray P. Menin interacting proteins as clues toward the understanding of multiple endocrine neoplasia type 1. Cancer Lett 2003; 189: 1-10
15. Dockray GJ. Keeping neuroendocrine cells in check: roles for TGFβ, Smads, and menin? Gut 2003; 52: 1237-1239
16. Shi Y, Massaque J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 2003; 113: 685-700
17. ten Dijke P, Miyazono K, Heldin CH. Signaling inputs converge on nuclear effectors in TGF-β signaling. Trends biochem Sci 2000; 25: 64-70
18. Markowitz S, Wag J, Myeroff L, Parsons R, Sun L, Lutterbaugh J, Fan RS, Zborowska E, Kinzler KW, Vogelstein B et al. Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science 1995; 268: 1336-1338
19. Goggins M, Shekher M, Turnacioglu K, Yeo CJ, Hruban RH, Kern SE. Genetic alterations of the transforming growth factor beta receptor genes in pancreatic and biliary adenocarcinomas. Cancer Res 1998; 58: 5329-5332
20. Chen T, de Vries EGE, Hollema H, Yegen HA, Vellucci VF, Strickler HD, Hildesheim A, Reiss M. Structural alterations of transforming growth factor-beta receptor genes in human cervical carcinoma. Int J Cancer 1999; 82: 43-51
21. Pasche B, Kolachana P, Nafa K, Satagopan J, Chen YG, Lo RS, Brener D, Yang D, Kirstein L, Oddoux C, Ostrer H, Vineis P, Varesco L, Jhanwar S, Luzzatto L, Massague J, Offit K. TbetaR-I(6A) is a candidate tumor susceptibility allele. Cancer Res 1999; 59: 5678-5682
22. Chen T, Carter D, Garrigue-Antar I, Reiss M. Transforming growth factor beta type I receptor kinase mutant associated with metastatic breast cancer. Cancer Res 1998; 58: 4805-4810
23. Hahn SA, Schutte M, Hoque AT, Moskaluk Ca, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH, Kern SE. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 1996; 271: 350-353
24. Barrett MT, Schutte M, Kern SE, Reid BJ. Allelic loss and mutational analysis of the DPC4 gene in esophageal adenocarcinoma. Cancer Res 1996; 56: 4351-4353
25. Kim SK, Fan Y, Papadimitrakopoulou V, Clayman G, Hittelman WN, Hong WK, Lotan R, Mao L. DPC4, a candidate tumor suppressor gene, is altered infrequently in head and neck squamous cell carcinoma. Cancer Res 1996; 56: 2519-2521
26. Kawate S, Takenoshita S, Ohwada S, Mogi A, Fukusato T, Makita F, Kuwano H, Morishita Y. Mutation analysis of transforming growth factor beta type II receptor, Smad2, and Smad4 in hepatocellular carcinoma. Int J Oncol 1999; 14: 127-131
27. Kong XT, Choi SH, Inoue A, Xu F, Chen T, Takita J, Yokota J, Bessho F, Yanagisawa M, Hanada R, Yamamoto K, Hayashi Y. Expression and mutational analysis of the DCC, DPC4, and MADR2/JV18-1 genes in neuroblastoma. Cancer Res 1997; 57: 3772-3778
28. Yokota T, Matsumoto S, Yoshimoto M, Kasumi F, Akiyama F, Sakamoto G, Nakamura Y, Emi M. Mapping of a breast cancer tumor suppressor gene locus to a 4-cM interval on chromosome 18q21. Jpn J Cancer Res 1997; 88: 959-964
29. Nagatake M, Takagi Y, Osada H, Uchida K, Mitsudomi T, Saji S, Shimokata K, Takahashi T, Takahashi T. Somatic in vivo alterations of the DPC4 gene at 18q21 in human lung cancers. Cancer Res 1996; 56: 2718-2720
30. Eppert K, Scherer SW, Ozcelik H, Pirone R, Hoodless P, Kim H, Tsui LC, Bapat B, Gallinger S, Andrulis IL, Thomsen GH, Wrana JL, Attisano L MADR1 maps to 18q21 and encodes a TGFbeta-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 1996;86:543-552
31. Takagi Y, Koumura H, Futamura M, Aoki S, Yamaguchi K, Kida H, Tanemura H, Shimokawa K, Saji S. Somatic alterations of the SMAD-2 gene in human colorectal cancers. Br J Cancer 1998; 78: 1152-1155
32. Riggins GJ, Thiagalingam S, Rozenblum E, Weinstein CL, Kern SE, Hamilton SR, Willson JK, Markowitz SD, Kinzler KW, Vogelstein B. Mad-related genes in the human. Nat Genet 1996; 13: 347-349
33. Kaji H, Canaff L, Lebrun J-J, Goltzman D, Hendy GN. Inactivation of menin, a Smad3-interacting protein, blocks transforming growth factor type β signaling. Proc Natl Acad Sci USA 2001; 98: 3837-3842
34. Canaff L, Hendy GN. Menin interacts directly with the TGF-β signaling molecule Smad3 and MEN1 missense mutations within the interacting region have impaired TGF-β transcriptional activity. J Int Med 2004; 255: 721-722, Abs 7004
35. Stroschein SL, Wang W, Zhou S, Zhou Q, Luo K. Negative feedback regulation of TGF-beta signaling by the SnoN oncoprotein. Science 1999; 286:771-774
36. Luo K, Stroschein SL, Wang W, Chen D, Martens E, Zhou S, Zhou Q. The Ski oncoprotein interacts with the Smad proteins to repress TGF-β signaling. Genes Dev 1999; 13: 2196-2206
37. Theodoropoulou M, Cavallari I, Barzon L, D'Agostino DM, Ferro T, Arzberger T, Grubler Y, Schaaf L, Losa M, Fallo F, Ciminale V, Stalla GK, Pagotto U. Differential expression of menin in sporadic pituitary adenomas. Endocrine-Related Cancer 2004; 11: 333-344
38. Murata T, Ying S. Transforming growth factor-β and activin inhibit basal secretion of prolactin in a pituitary monolayer culture system. Proc Soc Exp Biol Med 1991; 198: 599-605
39. Lacerte A, Lee E-H, Reynaud R, Canaff L, De Guise C, Devost D, Ali S, Hendy GN, Lebrun J-J. Activin inhibits prolactin expression and cell growth through Smads, Pit-1 and Menin. Molec Endocrinol 2004; 18: 1558-1569
40. Sowa H, Kaji H, Kitazawa R, Kitazawa S, Tsukamoto T, Yano S, Tsukada T, Canaff L, Hendy GN, Sugimoto T, Chihara K. Menin inactivation leads to loss to transforming growth factor β inhibition of parathyroid cell proliferation and parathyroid hormone secretion. Cancer Res 2004; 64: 2223-2228
41. Shattuck TM, Costa J, Bernstein M, Jensen RT, Chung DC, Arnold A. Mutational analysis of Smad3, a candidate tumor suppressor implicated in TGF-β and menin pathways, in parathyroid adenomas and entero-pancreatic endocrine tumors. J Clin Endocrineol Metab 2002; 87: 3911-3914
42. Yanagisawa J , Yanagi Y, Masuhiro Y, Suzawa M, Wantanabe M, Kashiwagi K, Toriyabe T, Kawabata M, Miyazone K, Kato S. Convergence of transforming growth factor β and vitamin D signaling pathways on Smad transcriptional coactivators. Science 1999; 283: 1317-1321
43. 3 and transforming growth factor-β signaling requires binding of VDR and Smad3 proteins to their cognate DNA recognition elements. J Biol Chem 2001; 276: 15741-15746
44. Kremer R, Bolivar I, Goltzman D, Hendy GN. Influence of calcium and 1,25-dihydroxycholecalciferol on proliferation and proto-oncogene expression in primary cultures of bovine parathyroid cells. Endocrinology 1989; 125: 935-941
45. Otto WR, Rao J. Tomorrow's skeleton staff: mesenchymal stem cells and the repair of bone and cartilage. Cell Prolif 2004; 37: 97-110
46. Sowa H, Kaji H, Canaff L, Hendy GN, Tsukamoto T, Yamaguchi T, Miyazono K, Sugimoto T, Chihara K. Inactivation of menin, the product of the multiple endocrine neoplasia type 1 gene, inhibits the commitment of multipotential mesenchymal stem cells into the osteoblast lineage. J Biol Chem 2003; 278: 21058-21069
47. Sowa H, Kaji H, Hendy GN, Canaff L, Komori T, Sugimoto T, Chihara K. Menin is required for bone morphogenetic protein 2- and transforming growth factor β-regulated osteoblastic differentiation through interaction with Smads and Runx2. J Biol Chem 2004; 279: 40267-40275
48. Naito J, Kaji H, Sowa H, Hendy GN, Sugimoto T, Chihara K. Menin suppresses osteoblast differentiation by antagonizing the AP-1 factor, JunD. J Biol Chem 2005; 280: 4785-4791
49. -/- cell lines established to study the function of menin. Eighth International Workshop on Multiple Endocrine Neoplasia. Van Andel Institute, Grand Rapids, Michigan, USA: June 15-18, 2002: Abs. 24