Menin is required for optimal processing of the microRNA let-7a

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 9902-9908

  Gurung, Buddha ^a   Muhammad, Abdul Bari ^a   Hua, Xianxin ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; CELLS; CYTOLOGY; GENE EXPRESSION; INSULIN; PROTEINS; RNA;

CAP-BINDING COMPLEXES; INSULIN RECEPTOR SUBSTRATE 2; INSULIN SIGNALING; MICRORNAS; NUCLEAR RNA; OPTIMAL PROCESSING; PANCREATIC ISLET; WILD-TYPE CELLS;

CELL SIGNALING;

ARSENITE RESISTANT PROTEIN 2; CAP BINDING PROTEIN; DROSHA PROTEIN; INSULIN RECEPTOR SUBSTRATE 2; LET 7A; MENIN PROTEIN; MICRORNA; MICRORNA 155; NUCLEAR PROTEIN; RIBONUCLEASE III; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INSR GENE; IRS2 GENE; MEN1 GENE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

BETA CELL; CANCER BIOLOGY; IRS2; LET-7A; MENIN; MICRORNA; PANCREAS; PANCREATIC ISLETS; TUMOR SUPPRESSOR GENE;

ANIMALS; ANTIGENS, CD; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; MICE; MICRORNAS; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1; NEOPLASM PROTEINS; NUCLEAR CAP-BINDING PROTEIN COMPLEX; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; RECEPTOR, INSULIN; RIBONUCLEASE III; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, NEOPLASM; TRANSCRIPTION FACTORS;

EID: 84898063109     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.520692     Document Type: Article

References (56)

1. Libé, R., and Bertherat, J. (2005) Molecular genetics of adrenocortical tumours, from familial tosporadic diseases.Eur. J. Endocrinol. 153, 477-487
2. Burgess, J. R., Nord, B., David, R., Greenaway, T. M., Parameswaran, V., Larsson, C., Shepherd, J. J., and Teh, B. T. (2000) Phenotype and pheno-copy: the relationship between genotype and clinical phenotypein a single large family with multiple endocrine neoplasia type 1 (MEN 1). Clin. En-docrinol. 53, 205-211
3. Marx, S. J. (2005) Molecular genetics of multiple endocrine neoplasia types 1 and 2. Nat. Rev. Cancer 5, 367-375
4. Bertolino, P., Radovanovic, I., Casse, H., Aguzzi, A., Wang, Z. Q., and Zhang, C. X. (2003) Genetic ablation of the tumor suppressor menin causes lethality at mid-gestation with defects in multiple organs. Mech. Dev. 120, 549-560
5. Chandrasekharappa, S. C., Guru, S. C., Manickam, P., Olufemi, S. E., Collins, F. S., Emmert-Buck, M. R., Debelenko, L. V., Zhuang, Z., Lubensky, I. A., Liotta, L. A., Crabtree, J. S., Wang, Y., Roe, B. A., Weisemann, J., Boguski, M. S., Agarwal, S. K., Kester, M.B., Kim, Y. S., Heppner, C., Dong, Q., Spiegel, A. M., Burns, A. L., and Marx, S. J. (1997) Positional cloning of the gene for multiple endocrine neoplasia-type 1. Science 276, 404-407
6. Lemmens, I., Van de Ven, W. J., Kas, K., Zhang, C. X., Giraud, S., Wautot, V., Buisson, N., De Witte, K., Salandre, J., Lenoir, G., Pugeat, M., Calender, A., Parente, F., Quincey, D., Gaudray, P., De Wit, M. J., Lips, C. J., Höp-pener, J. W., Khodaei, S., Grant, A. L., Weber, G., Kytölä, S., Teh, B. T., Farnebo, F., and Thakker, R. V. (1997) Identification of the multiple endocrine neoplasia type 1 (MEN1) gene. The European Consortium on MEN1. Hum Mol. Genet. 6, 1177-1183
7. Agarwal, S. K., Guru, S. C., Heppner, C., Erdos, M. R., Collins, R. M., Park, S. Y., Saggar, S., Chandrasekharappa, S. C., Collins, F. S., Spiegel, A. M., Marx, S. J., and Burns, A. L. (1999) Menin interacts with the AP1 transcription factor JunD and represses JunD-activated transcription. Cell 96, 143-152
8. Hughes, C. M., Rozenblatt-Rosen, O., Milne, T. A., Copeland, T. D., Levine, S. S., Lee, J. C., Hayes, D. N., Shanmugam, K. S., Bhattacharjee, A., Biondi, C. A., Kay, G. F., Hayward, N. K., Hess, J. L., and Meyerson, M. (2004) Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol. Cell 13, 587-597
9. Jin, S., Mao, H., Schnepp, R. W., Sykes, S. M., Silva, A. C., D'Andrea, A. D., and Hua, X. (2003) Menin associates with FANCD2, a protein involved in repair of DNA damage. Cancer Res. 63, 4204-4210
10. Yang, Y., and Hua, X. (2007) In search of tumor suppressing functions of menin. Mol. Cell. Endocrinol. 265-266, 34-41
11. Chen, G., A. J., Wang, M., Farley, S., Lee, L. Y., Lee, L.C., and Sawicki, M. P. (2008) Menin promotes the Wnt signaling pathway in pancreatic endocrine cells. Mol. Cancer Res. 6, 1894-1907
12. Gurung, B., Feng, Z., Iwamoto, D.V., Thiel, A., Jin, G., Fan, C.M., Ng, J.M., Curran, T., and Hua, X. (2013) Menin epigenetically represses Hedgehog signaling in MEN1 tumor syndrome. Cancer Res. 73, 2650-2658
13. Huang, J., Gurung, B., Wan, B., Matkar, S., Veniaminova, N. A., Wan, K., Merchant, J. L., Hua, X., and Lei, M. (2012) The same pocket in menin binds both MLL and JunD but has opposite effects on transcription. Nature 482, 542-546
14. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233
15. Kusenda, B., Mraz, M., Mayer, J., and Pospisilova, S. (2006) MicroRNA biogenesis, functionality and cancer relevance. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 150, 205-215
16. Denli, A. M., Tops, B. B., Plasterk, R. H., Ketting, R. F., and Hannon, G. J. (2004) Processing of primary microRNAs by the Microprocessor complex. Nature 432, 231-235
17. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Rådmark, O., Kim, S., and Kim, V. N. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419
18. Gregory, R. I., Yan, K. P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N., and Shiekhattar, R. (2004) The Microprocessor complex mediates the genesis of microRNAs. Nature 432, 235-240
19. Hutvágner, G., McLachlan, J., Pasquinelli, A. E., Bálint, E., Tuschl, T., and Zamore, P.D.(2001) A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834-838
20. Ketting, R. F., Fischer, S. E., Bernstein, E., Sijen, T., Hannon, G. J., and Plasterk, R.H. (2001) Dicer functions inRNA interference andin synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 15, 2654-2659
21. Knight, S. W., and Bass, B. L. (2001) A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabdi-tis elegans. Science 293, 2269-2271
22. Krol, J., Loedige, I., and Filipowicz, W. (2010) The widespread regulation of microRNA biogenesis, function and decay.Nat. Rev. Genet11, 597-610
23. Gregory, R. I., Chendrimada, T. P., Cooch, N., and Shiekhattar, R. (2005) Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123, 631-640
24. Sayed, D., and Abdellatif, M. (2011) MicroRNAs in development and disease. Physiol. Rev. 91, 827-887
25. Small, E. M., and Olson, E. N. (2011) Pervasive roles of microRNAs in cardiovascular biology. Nature 469, 336-342
26. Fernandez-Valverde, S. L., Taft, R. J., and Mattick, J. S. (2011) MicroRNAs in beta-cell biology, insulin resistance, diabetes and its complications. Diabetes 60, 1825-1831
27. Poy, M. N., Eliasson, L., Krutzfeldt, J., Kuwajima, S., Ma, X., Macdonald, P. E., Pfeffer, S., Tuschl, T., Rajewsky, N., Rorsman, P., and Stoffel, M. (2004) A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432, 226-230
28. Trajkovski, M., Hausser, J., Soutschek, J., Bhat, B., Akin, A., Zavolan, M., Heim, M. H., and Stoffel, M. (2011) MicroRNAs 103 and 107 regulate insulin sensitivity. Nature 474, 649-653
29. Caldas, C., and Brenton, J. D. (2005) Sizing up miRNAs as cancer genes. Nat. Med. 11, 712-714
30. Di Leva, G., and Croce, C. M. (2013) miRNA profiling of cancer. Curr. Opin. Genet. Dev. 23, 3-11
31. Lynn, F. C., Skewes-Cox, P., Kosaka, Y., McManus, M. T., Harfe, B. D., and German, M. S. (2007) MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes 56, 2938-2945
32. Melkman-Zehavi, T., Oren, R., Kredo-Russo, S., Shapira, T., Mandelbaum, A. D., Rivkin, N., Nir, T., Lennox, K. A., Behlke, M. A., Dor, Y., and Horn-stein, E. (2011) miRNAs control insulin content in pancreatic beta-cells via down-regulation of transcriptional repressors. EMBO J. 30, 835-845
33. Wang, Y., Liu, J., Liu, C., Naji, A., and Stoffers, D. A. (2013) MicroRNA-7 regulates the mTOR pathway and proliferation in adult pancreatic beta-cells. Diabetes 62, 887-895
34. Roldo, C., Missiaglia, E., Hagan, J. P., Falconi, M., Capelli, P., Bersani, S., Calin, G. A., Volinia, S., Liu, C. G., Scarpa, A., and Croce, C. M. (2006) MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. J. Clin. Oncol. 24, 4677-4684
35. Perren, A., Komminoth, P., and Heitz, P. U. (2004) Molecular genetics of gastroenteropancreatic endocrine tumors. Ann. N.Y. Acad. Sci. 1014, 199-208
36. Schnepp, R. W., Chen, Y. X., Wang, H., Cash, T., Silva, A., Diehl, J. A., Brown, E., and Hua, X. (2006) Mutation of tumor suppressor gene Men1 acutely enhances proliferation of pancreatic islet cells. Cancer Res. 66, 5707-5715
37. Gruber, J. J., Zatechka, D. S., Sabin, L. R., Yong, J., Lum, J. J., Kong, M., Zong, W. X., Zhang, Z., Lau, C. K., Rawlings, J., Cherry, S., Ihle, J. N., Dreyfuss, G., and Thompson, C. B. (2009) Ars2 links the nuclear cap-binding complex to RNA interference and cell proliferation. Cell 138, 328-339
38. Yokoyama, A., and Cleary, M. L. (2008) Menin critically links MLL proteins with LEDGF on cancer-associated target genes. Cancer Cell 14, 36-46
39. Sabin, L. R., Zhou, R., Gruber, J. J., Lukinova, N., Bambina, S., Berman, A., Lau, C. K., Thompson, C. B., and Cherry, S. (2009) Ars2 regulates both miRNA-and siRNA-dependent silencing and suppresses RNA virus infection in Drosophila. Cell 138, 340-351
40. Stålberg, P., Grimfjärd, P., Santesson, M., Zhou, Y., Lindberg, D., Gobl, A., Oberg, K., Westin, G., Rastad, J., Wang, S., and Skogseid, B. (2004) Trans-fection of the multiple endocrine neoplasia type 1 gene to a human endocrine pancreatic tumor cell line inhibits cell growth and affects expression of JunD, delta-like protein 1/preadipocyte factor-1, proliferating cell nuclear antigen, and QM/Jif-1. J. Clin. Endocrinol. Metab. 89, 2326-2337
41. Frost, R. J., and Olson, E. N. (2011) Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs. Proc. Natl. Acad. Sci. U.S.A. 108, 21075-21080
42. Withers, D. J., Gutierrez, J. S., Towery, H., Burks, D. J., Ren, J. M., Previs, S., Zhang, Y., Bernal, D., Pons, S., Shulman, G.I., Bonner-Weir, S., and White, M. F. (1998) Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391, 900-904
43. Yang, Y., Gurung, B., Wu, T., Wang, H., Stoffers, D. A., and Hua, X. (2010) Reversalof preexisting hyperglycemia in diabetic mice byacute deletion of the Men1 gene. Proc. Natl. Acad. Sci. U.S.A. 107, 20358-20363
44. Johnson, S. M., Grosshans, H., Shingara, J., Byrom, M., Jarvis, R., Cheng, A., Labourier, E., Reinert, K. L., Brown, D., and Slack, F. J. (2005) RAS is regulated by the let-7 microRNA family. Cell 120, 635-647
45. Heppner, C., Bilimoria, K. Y., Agarwal, S. K., Kester, M., Whitty, L. J., Guru, S. C, Chandrasekharappa, S. C, Collins, F. S., Spiegel, A. M., Marx, S. J., and Burns, A. L. (2001) The tumor suppressor protein menin interacts with NF-KB proteins and inhibits NF-mediated transactivation. Oncogene 20, 4917-4925
46. Dreijerink, K. M., Varier, R. A., van Beekum, O., Jeninga, E. H., Höppener, J. W., Lips, C. J., Kummer, J. A., Kalkhoven, E., and Timmers, H. T. (2009) The multiple endocrine neoplasia type 1 (MEN1) tumor suppressor regulates peroxisome proliferator-activated receptor 7-dependent adipocyte differentiation. Mol. Cell. Biol. 29, 5060-5069
47. Milne, T. A., Hughes, C. M., Lloyd, R., Yang, Z., Rozenblatt-Rosen, O., Dou, Y., Schnepp, R. W., Krankel, C, Livolsi, V. A., Gibbs, D., Hua, X., Roeder, R. G., Meyerson, M., and Hess, J. L. (2005) Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors. Proc. Natl. Acad. Sci. U.S.A. 102, 749-754
48. Yokoyama, A., Wang, Z., Wysocka, J., Sanyal, M., Aufiero, D. J., Ki-tabayashi, I., Herr, W., and Cleary, M. L. (2004) Leukemia proto-oncopro-tein MLL forms a SET1-like histone methyltransferase complex with menin to regulateHox gene expression. Mol. Cell. Biol. 24, 5639-5649
49. Thiel, A. T., Feng, Z., Pant, D. K., Chodosh, L. A., and Hua, X. (2013) The trithorax protein partner menin acts in tandem with EZH2 to suppress C/EBPa and differentiation in MLL-AF9 leukemia. Haematologica 98, 918-927
50. Gobl, A. E., Berg, M., Lopez-Egido, J. R., Oberg, K., Skogseid, B., and Westin, G. (1999) Menin represses JunD-activated transcription by a histone deacetylase-dependent mechanism. Biochim. Biophys. Acta 1447, 51-56
51. Luzi, E., Marini, F., Tognarini, I., Galli, G., Falchetti, A., and Brandi, M. L. (2012) The regulatory network menin-microRNA 26a as a possible target for RNA-based therapy of bone diseases. Nucleic Acid Ther. 22, 103-108
52. Schuppin, G. T., Pons, S., Hügl, S., Aiello, L. P., King, G. L., White, M., and Rhodes, C. J. (1998) A specific increased expression of insulin receptor substrate 2 in pancreatic beta-cell lines is involved in mediating serum-stimulated beta-cell growth. Diabetes 47, 1074-1085
53. Kubota, N., Tobe, K., Terauchi, Y., Eto, K., Yamauchi, T., Suzuki, R., Tsub-amoto, Y., Komeda, K., Nakano, R., Miki, H., Satoh, S., Sekihara, H., Sci-acchitano, S., Lesniak, M., Aizawa, S., Nagai, R., Kimura, S., Akanuma, Y., Taylor, S. I., and Kadowaki, T. (2000) Disruption of insulin receptor substrate 2 causes type 2 diabetes because of liver insulin resistance and lack of compensatory beta-cell hyperplasia. Diabetes 49, 1880-1889
54. Crabtree, J. S., Scacheri, P. C, Ward, J. M., McNally, S. R., Swain, G. P., Montagna, C, Hager, J. H, Hanahan, D., Edlund, H., Magnuson, M. A., Garrett-Beal, L., Burns, A. L., Ried, T., Chandrasekharappa, S. C, Marx, S. J., Spiegel, A. M., and Collins, F. S. (2003) Of mice and MEN1: insulinomas in a conditional mouse knockout. Mol. Cell. Biol. 23, 6075-6085
55. Wuescher, L., Angevine, K., Hinds, T., Ramakrishnan, S., Najjar, S. M., and Mensah-Osman, E. J. (2011) Insulin regulates menin expression, cytoplasmic localization, and interaction with FOXO1.Am. J. Physiol. Endocrinol. Metab. 301, E474-483
56. Jiao, Y., Shi, C, Edil, B. H, de Wilde, R. F., Klimstra, D. S., Maitra, A., Schulick, R. D., Tang, L. H., Wolfgang, C. L., Choti, M. A., Velculescu, V. E., Diaz, L. A., Jr., Vogelstein, B., Kinzler, K. W., Hruban, R. H, and Papadopoulos, N. (2011) DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 331, 1199-1203