Men1 is a melanoma tumor suppressor that preserves genomic integrity by stimulating transcription of genes that promote homologous recombination-directed dna repair

Molecular and Cellular Biology

Volumn 33, Issue 13, 2013, Pages 2635-2647

  Fang, Minggang ^a   Xia, Fen ^b   Mahalingam, Meera ^c   Virbasius, Ching Man ^a   Wajapeyee, Narendra ^d   Green, Michael R ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; HISTONE H3; LYSINE; RAD51 PROTEIN;

ARTICLE; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MELANOCYTE; MELANOMA; MELANOMA CELL; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1 GENE; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE;

BRCA1 PROTEIN; CELL CYCLE PROTEINS; CELL LINE; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA END-JOINING REPAIR; DNA-BINDING PROTEINS; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; MYELOID-LYMPHOID LEUKEMIA PROTEIN; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RAD51 RECOMBINASE; RECOMBINATIONAL DNA REPAIR; TUMOR SUPPRESSOR PROTEINS;

EID: 84880684921     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00167-13     Document Type: Article

References (50)

1. Poisson A, Zablewska B, Gaudray P. 2003. Menin interacting proteins as clues toward the understanding of multiple endocrine neoplasia type 1. Cancer Lett. 189:1-10.
2. Guru SC, Goldsmith PK, Burns AL, Marx SJ, Spiegel AM, Collins FS, Chandrasekharappa SC. 1998. Menin, the product of the MEN1 gene, is a nuclear protein. Proc. Natl. Acad. Sci. U. S. A. 95:1630-1634.
3. Kim H, Lee JE, Cho EJ, Liu JO, Youn HD. 2003. Menin, a tumor suppressor, represses JunD-mediated transcriptional activity by association with an mSin3A-histone deacetylase complex. Cancer Res. 63:6135-6139.
4. Heppner C, Bilimoria KY, Agarwal SK, Kester M, Whitty LJ, Guru SC, Chandrasekharappa SC, Collins FS, Spiegel AM, Marx SJ, Burns AL. 2001. The tumor suppressor protein menin interacts with NF-kappaB proteins and inhibits NF-kappaB-mediated transactivation. Oncogene 20: 4917-4925.
5. Kaji H, CanaffL, Lebrun JJ, Goltzman D, Hendy GN. 2001. Inactivation of menin, a Smad3-interacting protein, blocks transforming growth factor type beta signaling. Proc. Natl. Acad. Sci. U. S. A. 98:3837-3842.
6. Hughes CM, Rozenblatt-Rosen O, Milne TA, Copeland TD, Levine SS, Lee JC, Hayes DN, Shanmugam KS, Bhattacharjee A, Biondi CA, Kay GF, Hayward NK, Hess JL, Meyerson M. 2004. Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol. Cell 13:587-597.
7. Karnik SK, Hughes CM, Gu X, Rozenblatt-Rosen O, McLean GW, Xiong Y, Meyerson M, Kim SK. 2005. Menin regulates pancreatic islet growth by promoting histone methylation and expression of genes encoding p27Kip1 and p18INK4c. Proc. Natl. Acad. Sci. U. S. A. 102:14659-14664.
8. Kottemann MC, Bale AE. 2009. Characterization of DNA damagedependent cell cycle checkpoints in a menin-deficient model. DNARepair (Amst.) 8:944-952.
9. Yokoyama A, Wang Z, Wysocka J, Sanyal M, Aufiero DJ, Kitabayashi I, Herr W, Cleary ML. 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.
10. Hessman O, Skogseid B, Westin G, Akerstrom G. 2001. Multiple allelic deletions and intratumoral genetic heterogeneity in men1 pancreatic tumors. J. Clin. Endocrinol. Metab. 86:1355-1361.
11. Itakura Y, Sakurai A, Katai M, Ikeo Y, Hashizume K. 2000. Enhanced sensitivity to alkylating agent in lymphocytes from patients with multiple endocrine neoplasia type 1. Biomed. Pharmacother. 54(Suppl 1):187s-190s.
12. Busygina V, Suphapeetiporn K, Marek LR, Stowers RS, Xu T, Bale AE. 2004. Hypermutability in a Drosophila model for multiple endocrine neoplasia type 1. Hum. Mol. Genet. 13:2399-2408.
13. Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR. 2008. Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 132:363-374.
14. Campisi J. 2005. Suppressing cancer: the importance of being senescent. Science 309:886-887.
15. Won J, Kim M, Kim N, Ahn JH, Lee WG, Kim SS, Chang KY, Yi YW, Kim TK. 2006. Small molecule-based reversible reprogramming of cellular lifespan. Nat. Chem. Biol. 2:369-374.
16. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, Appella E, Kastan MB, Siliciano JD. 1998. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281:1677-1679.
17. Gazin C, Wajapeyee N, Gobeil S, Virabasius CM, Green MR. 2007. An elaborate pathway required for Ras-mediated epigenetic silencing. Nature 449:1073-1077.
18. SØrensen CS, Hansen LT, Dziegielewski J, Syljuasen RG, Lundin C, Bartek J, Helleday T. 2005. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat. Cell Biol. 7:195-201.
19. Thyagarajan B, McCormick-Graham M, Romero DP, Campbell C. 1996. Characterization of homologousDNArecombination activity in normal and immortal mammalian cells. Nucleic Acids Res. 24:4084-4091.
20. Mohindra A, Bolderson E, Stone J, Wells M, Helleday T, Meuth M. 2004. A tumour-derived mutant allele of XRCC2 preferentially suppresses homologous recombination at DNA replication forks. Hum. Mol. Genet. 13:203-212.
21. Wen Q, Scorah J, Phear G, Rodgers G, Rodgers S, Meuth M. 2008. A mutant allele of MRE11 found in mismatch repair-deficient tumor cells suppresses the cellular response to DNA replication fork stress in a dominantnegative manner. Mol. Biol. Cell 19:1693-1705.
22. Wilson S, Warr N, Taylor DL, Watts FZ. 1999. The role of Schizosaccharomyces pombe Rad32, the Mre11 homologue, and other DNA damage response proteins in non-homologous end joining and telomere length maintenance. Nucleic Acids Res. 27:2655-2661.
23. Zhuang J, Jiang G, Willers H, Xia F. 2009. Exonuclease function of human Mre11 promotes deletional nonhomologous end joining. J. Biol. Chem. 284:30565-30573.
24. Raha T, Cheng SW, Green MR. 2005. HIV-1 Tat stimulates transcription complex assembly through recruitment of TBP in the absence of TAFs. PLoS Biol. 3:e44. doi:10.1371/journal.pbio.0030044.
25. Ihaka R, Gentleman R. 1996. R: a language for data analysis and graphics. J. Comput. Graph. Stat. 5:299-314.
26. Herman JG, Baylin SB. 2003. Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349:2042-2054.
27. Weinberg RA. 2006. The biology of cancer. Garland Science, New York, NY.
28. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, Pommier Y. 2008. GammaH2AX and cancer. Nat. Rev. Cancer 8:957-967.
29. Moynahan ME, Jasin M. 2010. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 11:196-207.
30. Shrivastav M, De Haro LP, NickoloffJA. 2008. Regulation of DNA double-strand break repair pathway choice. Cell Res. 18:134-147.
31. Sonoda E, Hochegger H, Saberi A, Taniguchi Y, Takeda S. 2006. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst.) 5:1021-1029.
32. Lieber MR, Ma Y, Pannicke U, Schwarz K. 2003. Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell Biol. 4:712-720.
33. Smith J, Tho LM, Xu N, Gillespie DA. 2010. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv. Cancer Res. 108:73-112.
34. Francis J, Lin W, Rozenblatt-Rosen O, Meyerson M. 2011. The menin tumor suppressor protein is phosphorylated in response to DNA damage. PLoS One 6:e16119. doi:10.1371/journal.pone.0016119.
35. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, III, Hurov KE, Luo J, Bakalarski CE, Zhao Z, Solimini N, Lerenthal Y, Shiloh Y, Gygi SP, Elledge SJ. 2007. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316:1160-1166.
36. Shiloh Y. 2006. The ATM-mediated DNA-damage response: taking shape. Trends Biochem. Sci. 31:402-410.
37. Scacheri PC, Davis S, Odom DT, Crawford GE, Perkins S, Halawi MJ, Agarwal SK, Marx SJ, Spiegel AM, Meltzer PS, Collins FS. 2006. Genome-wide analysis of menin binding provides insights into MEN1 tumorigenesis. PLoS Genet. 2:e51. doi:10.1371/journal.pgen.0020051.
38. Dreijerink KM, Lips CJ, Timmers HT. 2009. Multiple endocrine neoplasia type 1: a chromatin writer's block. J. Intern. Med. 266:53-59.
39. Gertz J, Reddy TE, Varley KE, Garabedian MJ, Myers RM. 2012. Genistein and bisphenol A exposure cause estrogen receptor 1 to bind thousands of sites in a cell type-specific manner. Genome Res. 22:2153-2162.
40. Dreijerink KM, Mulder KW, Winkler GS, Hoppener JW, Lips CJ, Timmers HT. 2006. Menin links estrogen receptor activation to histone H3K4 trimethylation. Cancer Res. 66:4929-4935.
41. Wakeling AE, Dukes M, Bowler J. 1991. A potent specific pure antiestrogen with clinical potential. Cancer Res. 51:3867-3873.
42. Nord B, Platz A, Smoczynski K, Kytola S, Robertson G, Calender A, Murat A, Weintraub D, Burgess J, Edwards M, Skogseid B, Owen D, Lassam N, Hogg D, Larsson C, Teh BT. 2000. Malignant melanoma in patients with multiple endocrine neoplasia type 1 and involvement of the MEN1 gene in sporadic melanoma. Int. J. Cancer 87:463-467.
43. Cruz C, Teule A, Caminal JM, Blanco I, Piulats JM. 2011. Uveal melanoma and BRCA1/BRCA2 genes: a relationship that needs further investigation. J. Clin. Oncol. 29:e827-829.
44. Deng H, Liu J, Deng Y, Han G, Shellman YG, Robinson SE, Tentler JJ, Robinson WA, Norris DA, Wang XJ, Zhang Q. 2013. CtBP1 is expressed in melanoma and represses the transcription of p16INK4a and Brca1. J. Investig. Dermatol. 133:1294-1301.
45. Jin S, Mao H, Schnepp RW, Sykes SM, Silva AC, D'Andrea AD, Hua X. 2003. Menin associates with FANCD2, a protein involved in repair of DNA damage. Cancer Res. 63:4204-4210.
46. Gallo A, Agnese S, Esposito I, Galgani M, Avvedimento VE. 2010. Menin stimulates homology-directed DNA repair. FEBS Lett. 584:4531-4536.
47. Paulsen RD, Soni DV, Wollman R, Hahn AT, Yee MC, Guan A, Hesley JA, Miller SC, Cromwell EF, Solow-Cordero DE, Meyer T, Cimprich KA. 2009. A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol. Cell 35:228-239.
48. Kennedy RD, Quinn JE, Mullan PB, Johnston PG, Harkin DP. 2004. The role of BRCA1 in the cellular response to chemotherapy. J. Natl. Cancer Inst. 96:1659-1668.
49. Lai D, Visser-Grieve S, Yang X. 2012. Tumour suppressor genes in chemotherapeutic drug response. Biosci. Rep. 32:361-374.
50. Mullan PB, Gorski JJ, Harkin DP. 2006. BRCA1-a good predictive arker of drug sensitivity in breast cancer treatment? Biochim. Biophys. Acta 1766:205-216.