The multiple endocrine neoplasia type 1 (MEN1) tumor suppressor regulates peroxisome proliferator-activated receptor γ-dependent adipocyte differentiation

Molecular and Cellular Biology

Volumn 29, Issue 18, 2009, Pages 5060-5069

  Dreijerink, Koen M A ^a   Varier, Radhika A ^a   Van Beekum, Olivier ^a   Jeninga, Ellen H ^a   Höppener, Jo W M ^a   Lips, Cornelis J M ^a   Kummer, J Alain ^a   Kalkhoven, Eric ^a   Timmers, H T Marc ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID BINDING PROTEIN 4; HISTONE; HISTONE H3K4; METHIONINE; METHYLTRANSFERASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; UNCLASSIFIED DRUG; FABP4 PROTEIN, HUMAN; FATTY ACID BINDING PROTEIN; LIGAND; LYSINE; MEN1 PROTEIN, HUMAN; MEN1 PROTEIN, MOUSE; ONCOPROTEIN;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN TISSUE; METHYLATION; MOUSE; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; TRANSCRIPTION INITIATION; TUMOR SUPPRESSOR GENE; ANIMAL; CELL STRAIN 3T3; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE;

MURINAE;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CELL DIFFERENTIATION; FATTY ACID-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HISTONES; HUMANS; LIGANDS; LYSINE; METHYLATION; MICE; PPAR GAMMA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS; TRANSCRIPTION, GENETIC;

EID: 70249113378     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01001-08     Document Type: Article

References (55)

1. Agarwal, S. K., S. Impey, S. McWeeney, P. C. Scacheri, F. S. Collins, R. H. Goodman, A. M. Spiegel, and S. J. Marx. 2007. Distribution of meninoccupied regions in chromatin specifies a broad role of menin in transcriptional regulation. Neoplasia 9:101-107.
2. Albert, T. K., H. Hanzawa, Y. I. Legtenberg, M. J. de Ruwe, F. A. van den Heuvel, M. A. Collart, R. Boelens, and H. T. Timmers. 2002. Identification of a ubiquitin-protein ligase subunit within the CCR4-NOT transcription repressor complex. EMBO J. 21:355-364.
3. Altiok, S., M. Xu, and B. M. Spiegelman. 1997. PPARgamma induces cell cycle withdrawal: inhibition of E2F/DP DNA-binding activity via downregulation of PP2A. Genes Dev. 11:1987-1998. (Pubitemid 27332985)
4. Bertolino, P., I. Radovanovic, H. Casse, A. Aguzzi, Z. Q. Wang, and C. X. Zhang. 2003. Genetic ablation of the tumor suppressor menin causes lethality at mid-gestation with defects in multiple organs. Mech. Dev. 120:549-560. (Pubitemid 36623317)
5. Brandi, M. L., R. F. Gagel, A. Angeli, J. P. Bilezikian, P. Beck-Peccoz, C. Bordi, B. Conte-Devolx, A. Falchetti, R. G. Gheri, A. Libroia, C. J. Lips, G. Lombardi, M. Mannelli, F. Pacini, B. A. Ponder, F. Raue, B. Skogseid, G. Tamburrano, R. V. Thakker, N. W. Thompson, P. Tomassetti, F. Tonelli, S. A. Wells, Jr., and S. J. Marx. 2001. Guidelines for diagnosis and therapy of MEN type 1 and type 2. J. Clin. Endocrinol. Metab. 86:5658-5671. (Pubitemid 33152604)
6. Brelivet, Y., S. Kammerer, N. Rochel, O. Poch, and D. Moras. 2004. Signature of the oligomeric behaviour of nuclear receptors at the sequence and structural level. EMBO Rep. 5:423-429. (Pubitemid 38618287)
7. Chen, D., H. Ma, H. Hong, S. S. Koh, S. M. Huang, B. T. Schurter, D. W. Aswad, and M. R. Stallcup. 1999. Regulation of transcription by a protein methyltransferase. Science 284:2174-2177.
8. Darling, T. N., M. C. Skarulis, S. M. Steinberg, S. J. Marx, A. M. Spiegel, and M. Turner. 1997. Multiple facial angiofibromas and collagenomas in patients with multiple endocrine neoplasia type 1. Arch. Dermatol. 133:853-857. (Pubitemid 27337545)
9. Dreijerink, K. M., K. W. Mulder, G. S. Winkler, J. W. Hoppener, C. J. Lips, and H. T. Timmers. 2006. Menin links estrogen receptor activation to histone H3K4 trimethylation. Cancer Res. 66:4929-4935.
10. Dubois, M., F. Pattou, J. Kerr-Conte, V. Gmyr, B. Vandewalle, P. Desreumaux, J. Auwerx, K. Schoonjans, and J. Lefebvre. 2000. Expression of peroxisome proliferator-activated receptor gamma (PPARgamma) in normal human pancreatic islet cells. Diabetologia 43:1165-1169. (Pubitemid 30702940)
11. Franklin, D. S., V. L. Godfrey, D. A. O'Brien, C. Deng, and Y. Xiong. 2000. Functional collaboration between different cyclin-dependent kinase inhibitors suppresses tumor growth with distinct tissue specificity. Mol. Cell. Biol. 20:6147-6158.
12. Ge, K., M. Guermah, C. X. Yuan, M. Ito, A. E. Wallberg, B. M. Spiegelman, and R. G. Roeder. 2002. Transcription coactivator TRAP220 is required for PPAR gamma 2-stimulated adipogenesis. Nature 417:563-567. (Pubitemid 34595925)
13. Goke, R., A. Goke, B. Goke, W. S. El-Deiry, and Y. Chen. 2001. Pioglitazone inhibits growth of carcinoid cells and promotes TRAIL-induced apoptosis by induction of p21waf1/cip1. Digestion 64:75-80. (Pubitemid 34701873)
14. Gurnell, M., J. M. Wentworth, M. Agostini, M. Adams, T. N. Collingwood, C. Provenzano, P. O. Browne, O. Rajanayagam, T. P. Burris, J. W. Schwabe, M. A. Lazar, and V. K. Chatterjee. 2000. A dominant-negative peroxisome proliferator-activated receptor gamma (PPARgamma) mutant is a constitutive repressor and inhibits PPARgamma-mediated adipogenesis. J. Biol. Chem. 275:5754-5759. (Pubitemid 30115218)
15. Heaney, A. P., M. Fernando, and S. Melmed. 2003. PPAR-gamma receptor ligands: novel therapy for pituitary adenomas. J. Clin. Investig. 111:1381-1388. (Pubitemid 36554709)
16. Heery, D. M., E. Kalkhoven, S. Hoare, and M. G. Parker. 1997. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387:733-736.
17. Hughes, C. M., O. Rozenblatt-Rosen, T. A. Milne, T. D. Copeland, S. S. Levine, J. C. Lee, D. N. Hayes, K. S. Shanmugam, A. Bhattacharjee, C. A. Biondi, G. F. Kay, N. K. Hayward, J. L. Hess, and M. Meyerson. 2004. Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol. Cell 13:587-597.
18. Jeninga, E. H., O. van Beekum, A. D. van Dijk, N. Hamers, B. I. Hendriks-Stegeman, A. M. Bonvin, R. Berger, and E. Kalkhoven. 2007. Impaired peroxisome proliferator-activated receptor gamma function through mutation of a conserved salt bridge (R425C) in familial partial lipodystrophy. Mol. Endocrinol. 21:1049-1065.
19. Kalkhoven, E., J. E. Valentine, D. M. Heery, and M. G. Parker. 1998. Isoforms of steroid receptor co-activator 1 differ in their ability to potentiate transcription by the oestrogen receptor. EMBO J. 17:232-243. (Pubitemid 28041064)
20. Karnik, S. K., H. Chen, G. W. McLean, J. J. Heit, X. Gu, A. Y. Zhang, M. Fontaine, M. H. Yen, and S. K. Kim. 2007. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 318:806-809.
21. Kim, H., J. E. Lee, E. J. Cho, J. O. Liu, and H. D. Youn. 2003. Menin, a tumor suppressor, represses JunD-mediated transcriptional activity by association with an mSin3A-histone deacetylase complex. Cancer Res. 63:6135-6139. (Pubitemid 37255151)
22. Kishida, K., I. Shimomura, H. Nishizawa, N. Maeda, H. Kuriyama, H. Kondo, M. Matsuda, H. Nagaretani, N. Ouchi, K. Hotta, S. Kihara, T. Kadowaki, T. Funahashi, and Y. Matsuzawa. 2001. Enhancement of the aquaporin adipose gene expression by a peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 276:48572-48579. (Pubitemid 37370773)
23. Klein, F. A., R. A. Atkinson, N. Potier, D. Moras, and J. Cavarelli. 2005. Biochemical and NMR mapping of the interface between CREB-binding protein and ligand binding domains of nuclear receptor: beyond the LXXLL motif. J. Biol. Chem. 280:5682-5692.
24. La, P., A. C. Silva, Z. Hou, H. Wang, R. W. Schnepp, N. Yan, Y. Shi, and X. Hua. 2004. Direct binding of DNA by tumor suppressor menin. J. Biol. Chem. 279:49045-49054. (Pubitemid 39625786)
25. Lee, J., P. K. Saha, Q. H. Yang, S. Lee, J. Y. Park, Y. Suh, S. K. Lee, L. Chan, R. G. Roeder, and J. W. Lee. 2008. Targeted inactivation of MLL3 histone H3-Lys-4 methyltransferase activity in the mouse reveals vital roles for MLL3 in adipogenesis. Proc. Natl. Acad. Sci. USA 105:19229-19234.
26. Lee, S., D. K. Lee, Y. Dou, J. Lee, B. Lee, E. Kwak, Y. Y. Kong, S. K. Lee, R. G. Roeder, and J. W. Lee. 2006. Coactivator as a target gene specificity determinant for histone H3 lysine 4 methyltransferases. Proc. Natl. Acad. Sci. USA 103:15392-15397. (Pubitemid 44625602)
27. Lee, S., J. Lee, S. K. Lee, and J. W. Lee. 2008. Activating signal cointegrator-2 is an essential adaptor to recruit histone H3 lysine 4 methyltransferases MLL3 and MLL4 to the liver X receptors. Mol. Endocrinol. 22:1312-1319.
28. Lehrke, M., and M. A. Lazar. 2005. The many faces of PPARgamma. Cell 123:993-999.
29. Lemos, M. C., and R. V. Thakker. 2008. Multiple endocrine neoplasia type 1 (MEN1): analysis of 1336 mutations reported in the first decade following identification of the gene. Hum. Mutat. 29:22-32.
30. Lin, S. Y., and S. J. Elledge. 2003. Multiple tumor suppressor pathways negatively regulate telomerase. Cell 113:881-889.
31. Messager, M., C. Carriere, X. Bertagna, and Y. de Keyzer. 2006. RT-PCR analysis of corticotroph-associated genes expression in carcinoid tumours in the ectopic-ACTH syndrome. Eur. J. Endocrinol. 154:159-166. (Pubitemid 43250750)
32. Milne, T. A., C. M. Hughes, R. Lloyd, Z. Yang, O. Rozenblatt-Rosen, Y. Dou, R. W. Schnepp, C. Krankel, V. A. Livolsi, D. Gibbs, X. Hua, R. G. Roeder, M. Meyerson, and J. L. Hess. 2005. Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors. Proc. Natl. Acad. Sci. USA 102:749-754.
33. Mo, R., S. M. Rao, and Y. J. Zhu. 2006. Identification of the MLL2 complex as a coactivator for estrogen receptor alpha. J. Biol. Chem. 281:15714-15720 (Pubitemid 43848459)
34. Morrison, R. F., and S. R. Farmer. 1999. Role of PPARgamma in regulating a cascade expression of cyclin-dependent kinase inhibitors, p18(INK4c) and p21(Waf1/Cip1), during adipogenesis. J. Biol. Chem. 274:17088-17097. (Pubitemid 129519039)
35. Nolte, R. T., G. B. Wisely, S. Westin, J. E. Cobb, M. H. Lambert, R. Kurokawa, M. G. Rosenfeld, T. M. Willson, C. K. Glass, and M. V. Milburn. 1998. Ligand binding and co-activator assembly of the peroxisome proliferatoractivated receptor-gamma. Nature 395:137-143.
36. Occhi, G., N. Albiger, S. Berlucchi, M. Gardiman, M. Scanarini, R. Scienza, A. Fassina, F. Mantero, and C. Scaroni. 2007. Peroxisome proliferatoractivated receptor gamma in the human pituitary gland: expression and splicing pattern in adenomas versus normal pituitary. J. Neuroendocrinol. 19:552-559. (Pubitemid 47189000)
37. Pijnappel, W. W., H. F. Hendriks, G. E. Folkers, C. E. van den Brink, E. J. Dekker, C. Edelenbosch, P. T. van der Saag, and A. J. Durston. 1993. The retinoid ligand 4-oxo-retinoic acid is a highly active modulator of positional specification. Nature 366:340-344. (Pubitemid 23349360)
38. Rosen, E. D., R. N. Kulkarni, P. Sarraf, U. Ozcan, T. Okada, C.-H. Hsu, D. Eisenman, M. A. Magnuson, F. J. Gonzalez, C. R. Kahn, and B. M. Spiegelman. 2003. Targeted elimination of peroxisome proliferator-activated receptor γ in β cells leads to abnormalities in islet mass without compromising glucose homeostasis. Mol. Cell. Biol. 23:7222-7229.
39. Ruthenburg, A. J., C. D. Allis, and J. Wysocka. 2007. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell 25:15-30.
40. Scacheri, P. C., S. Davis, D. T. Odom, G. E. Crawford, S. Perkins, M. J. Halawi, S. K. Agarwal, S. J. Marx, A. M. Spiegel, P. S. Meltzer, and F. S. Collins. 2006. Genome-wide analysis of menin binding provides insights into MEN1 tumorigenesis. PLoS Genet. 2:e51.
41. Semple, R. K., V. K. Chatterjee, and S. O'Rahilly. 2006. PPAR gamma and human metabolic disease. J. Clin. Investig. 116:581-589. (Pubitemid 43326862)
42. Sierra, J., T. Yoshida, C. A. Joazeiro, and K. A. Jones. 2006. The APC tumor suppressor counteracts beta-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev. 20:586-600. (Pubitemid 43345324)
43. Sowa, H., H. Kaji, L. Canaff, G. N. Hendy, T. Tsukamoto, T. Yamaguchi, K. Miyazono, T. Sugimoto, and K. Chihara. 2003. 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. 278:21058-21069. (Pubitemid 36806417)
44. Steger, D. J., M. I. Lefterova, L. Ying, A. J. Stonestrom, M. Schupp, D. Zhuo, A. L. Vakoc, J.-E. Kim, J. Chen, M. A. Lazar, G. A. Blobel, and C. R. Vakoc. 2008. DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol. Cell. Biol. 28: 2825-2839.
45. Takada, I., M. Mihara, M. Suzawa, F. Ohtake, S. Kobayashi, M. Igarashi, M. Y. Youn, K. Takeyama, T. Nakamura, Y. Mezaki, S. Takezawa, Y. Yogiashi, H. Kitagawa, G. Yamada, S. Takada, Y. Minami, H. Shibuya, K. Matsumoto, and S. Kato. 2007. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat. Cell Biol. 9:1273-1285. (Pubitemid 350042359)
46. Tontonoz, P., E. Hu, R. A. Graves, A. I. Budavari, and B. M. Spiegelman. 1994. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 8:1224-1234. (Pubitemid 2102252)
47. Tontonoz, P., E. Hu, and B. M. Spiegelman. 1994. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79:1147-1156.
48. Tontonoz, P., S. Singer, B. M. Forman, P. Sarraf, J. A. Fletcher, C. D. Fletcher, R. P. Brun, E. Mueller, S. Altiok, H. Oppenheim, R. M. Evans, and B. M. Spiegelman. 1997. Terminal differentiation of human liposarcoma cells induced by ligands for peroxisome proliferator-activated receptor gamma and the retinoid X receptor. Proc. Natl. Acad. Sci. USA 94:237-241. (Pubitemid 27027193)
49. Tyagi, S., A. L. Chabes, J. Wysocka, and W. Herr. 2007. E2F activation of S phase promoters via association with HCF-1 and the MLL family of histone H3K4 methyltransferases. Mol. Cell 27:107-119. (Pubitemid 46991384)
50. Vermeulen, M., K. W. Mulder, S. Denissov, W. W. Pijnappel, F. M. van Schaik, R. A. Varier, M. P. Baltissen, H. G. Stunnenberg, M. Mann, and H. T. Timmers. 2007. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131:58-69. (Pubitemid 47498531)
51. Vortmeyer, A. O., R. Boni, E. Pak, S. Pack, and Z. Zhuang. 1998. Multiple endocrine neoplasia 1 gene alterations in MEN1-associated and sporadic lipomas. J. Natl. Cancer Inst. 90:398-399.
52. Winkler, G. S., K. W. Mulder, V. J. Bardwell, E. Kalkhoven, and H. T. Timmers. 2006. Human Ccr4-Not complex is a ligand-dependent repressor of nuclear receptor-mediated transcription. EMBO J. 25:3089-3099.
53. Wysocka, J., T. Swigut, H. Xiao, T. A. Milne, S. Y. Kwon, J. Landry, M. Kauer, A. J. Tackett, B. T. Chait, P. Badenhorst, C. Wu, and C. D. Allis. 2006. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442:86-90. (Pubitemid 44064214)
54. Yadav, N., D. Cheng, S. Richard, M. Morel, V. R. Iyer, C. M. Aldaz, and M. T. Bedford. 2008. CARM1 promotes adipocyte differentiation by coactivating PPARgamma. EMBO Rep. 9:193-198. (Pubitemid 351223458)
55. Yokoyama, A., Z. Wang, J. Wysocka, M. Sanyal, D. J. Aufiero, I. Kitabayashi, W. Herr, and M. L. Cleary. 2004. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol. Cell. Biol. 24:5639-5649. (Pubitemid 38787950)