ATM mediates prb function to control dnmt1 protein stability and dna methylation

Molecular and Cellular Biology

Volumn 33, Issue 16, 2013, Pages 3113-3124

  Shamma, Awad ^a   Suzuki, Misa ^a   Hayashi, Naoyuki ^a,b   Kobayashi, Masahiko ^b   Sasaki, Nobunari ^a   Nishiuchi, Takumi ^b   Doki, Yuichiro ^c   Okamoto, Takahiro ^d   Kohno, Susumu ^a   Muranaka, Hayato ^a   Kitajima, Shunsuke ^a   Yamamoto, Ken ichi ^b   Takahashi, Chiaki ^a  

^a Division of Molecular Pathology   (Japan)

^b KANAZAWA UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DNA METHYLTRANSFERASE 1; NOGGIN; RETINOBLASTOMA PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA METHYLATION; EPIGENETICS; GENE INTERACTION; GENETIC ANALYSIS; IN VIVO STUDY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; THYROID PARAFOLLICULAR CELL; THYROID TUMOR; UBIQUITINATION;

ANIMALS; CELL CYCLE PROTEINS; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; ENZYME STABILITY; GENE DELETION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; THYROID GLAND; THYROID NEOPLASMS; TUMOR SUPPRESSOR PROTEINS; UBIQUITINATION;

EID: 84881297457     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01597-12     Document Type: Article

References (42)

1. Burkhart DL, Sage J. 2008. Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat. Rev. Cancer 8:671-682.
2. Viatour P, Sage J. 2011. Newly identified aspects of tumor suppression by RB. Dis. Model. Mech. 4:581-585.
3. Takahashi C, Sasaki N, Kitajima S. 2012. Twists in views on RB functions in cellular signaling, metabolism and stem cells. Cancer Sci. 103:1182- 1188.
4. Robertson KD, Ait-Si-Ali S, Yokochi T, Wade PA, Jones PL, Wolffe AP. 2000. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet. 25:338-342.
5. Dick FA. 2007. Structure-function analysis of the retinoblastoma tumor suppressor protein-is the whole a sum of its parts? Cell Div. 2:26. doi:10 .1186/1747-1028-2-26.
6. Lin W, Cao J, Liu J, Beshiri ML, Fujiwara Y, Francis J, Cherniack AD, Geisen C, Blair LP, Zou MR, Shen X, Kawamori D, Liu Z, Grisanzio C, Watanabe H, Minamishima YA, Zhang Q, Kulkarni RN, Signoretti S, Rodig SJ, Bronson RT, Orkin SH, Tuck DP, Benevolenskaya EV, Meyerson M, Kaelin WG, Jr, Yan Q. 2011. Loss of the retinoblastoma binding protein 2 (RBP2) histone demethylase suppresses tumorigenesis in mice lacking Rb1 or Men1. Proc. Natl. Acad. Sci. U. S. A. 108:13379- 13386.
7. Lopez-Bigas N, Kisiel AT, DeWaal DC, Holmes KB, Volkert TL, Love J, Murray HL, Young RA, Benevolenskaya EV. 2008. Genome-wide analysis of the H3K4 histone demethylase RBP2 reveals a transcriptional program controlling differentiation. Mol. Cell 31:520-530.
8. Li F, He Z, Shen J, Huang Q, Li W, Lui X, He Y, Wolf F, Li CY. 2010. Apoptotic caspases regulate induction of iPSCs from human fibroblasts. Cell Stem Cell 7:508-520.
9. Liu Y, Clem B, Zuba-Surma EK, El-Naggar S, Telang S, Jenson AB, Wang Y, Shao H, Ratajczak MZ, Chesney J, Dean DC. 2009. Mouse fibroblasts lacking RB1 function form spheres and undergo reprogramming to a cancer stem cell phenotype. Cell Stem Cell 4:336-347.
10. Sage J. 2012. The retinoblastoma tumor suppressor and stem cell biology. Genes Dev. 26:1409-1420.
11. Zhang J, Benavente CA, McEvoy J, Flores-Otero J, Ding L, Chen X, Ulyanov A, Wu G, Wilson M, Wang J, Brennan R, Rusch M, Manning AL, Ma J, Easton J, Shurtleff S, Mullighan C, Pounds S, Mukatira S, Gupta P, Neale G, Zhao D, Lu C, Fulton RS, Fulton LL, Hong X, Dooling DJ, Ochoa K, Naeve C, Dyson NJ, Mardis ER, Bahrami A, Ellison D, Wilson RK, Downing JR, Dyer MA. 2012. A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature 481:329- 334.
12. Duensing S, Munger K. 2002. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res. 62:7075-7082.
13. Pickering MT, Kowalik TF. 2006. Rb inactivation leads to E2F1-mediated DNA double-strand break accumulation. Oncogene 25:746-755.
14. Frame FM, Rogoff HA, Pickering MT, Cress WD, Kowalik TF. 2006. E2F1 induces MRN foci formation and a cell cycle checkpoint response in human fibroblasts. Oncogene 25:3258-3266.
15. Shamma A, Takegami Y, Miki T, Kitajima S, Noda M, Obara T, Okamoto T, Takahashi C. 2009. Rb regulates DNA damage response and cellular senescence through E2F-dependent suppression of N-ras isoprenylation. Cancer Cell 15:255-269.
16. van Harn T, Foijer F, van Vugt M, Banerjee R, Yang F, Oostra A, Joenje H, te Riele H. 2010. Loss of Rb proteins causes genomic instability in the absence of mitogenic signaling. Genes Dev. 24:1377-1388.
17. Sage J, Straight AF. 2010. RB's original CIN? Genes Dev. 24:1329-1333.
18. Polo SE, Jackson SP. 2011. Dynamics of DNA damage response proteins atDNAbreaks: a focus on protein modifications. Genes Dev. 25:409-433.
19. Bensimon A, Aebersold R, Shiloh Y. 2011. Beyond ATM: the protein kinase landscape of theDNAdamage response. FEBS Lett. 585:1625-1639.
20. Lukas J, Bartek J. 2009. DNA repair: new tales of an old tail. Nature 458:581-583.
21. Takahashi C, Bronson RT, Socolovsky M, Contreras B, Lee KY, Jacks T, Noda M, Kucherlapati R, Ewen ME. 2003. Rb and N-ras function together to control differentiation in the mouse. Mol. Cell. Biol. 23:5256- 5268.
22. Takahashi C, Contreras B, Bronson RT, Loda M, Ewen ME. 2004. Genetic interaction between Rb and K-ras in the control of differentiation and tumor suppression. Mol. Cell. Biol. 24:10406-10415.
23. Takahashi C, Contreras B, Iwanaga T, Takegami Y, Bakker A, Bronson RT, Noda M, Loda M, Hunt JL, Ewen ME. 2006. Nras loss induces metastatic conversion of Rb1-deficient neuroendocrine thyroid tumor. Nat. Genet. 38:118-123.
24. Sharpless NE, Bardeesy N, Lee KH, Carrasco D, Castrillon DH, Aguirre AJ, Wu EA, Horner JW, DePinho RA. 2001. Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature 413:86 -91.
25. Herzog KH, Chong MJ, Kapsetaki M, Morgan JI, McKinnon PJ. 1998. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 280:1089-1091.
26. So S, Davis AJ, Chen DJ. 2009. Autophosphorylation at serine 1981 stabilizes ATM at DNA damage sites. J. Cell Biol. 187:977-990.
27. Ikura T, Ogryzko VV, Grigoriev M, Groisman R, Wang J, Horikoshi M, Scully R, Qin J, Nakatani Y. 2000. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102:463-473.
28. Lim KL, Chew KC, Tan JM, Wang C, Chung KK, Zhang Y, Tanaka Y, Smith W, Engelender S, Ross CA, Dawson VL, Dawson TM. 2005. Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation. J. Neurosci. 25:2002- 2009.
29. Kobayashi M, Ono H, Mihara K, Tauchi H, Komatsu K, Shibata T, Shimizu H, Uchida K, Yamamoto K. 2006. ATM activation by a sulfhydryl- reactive inflammatory cyclopentenone prostaglandin. Genes Cells 11:779-789.
30. Abe K, Naruse C, Kato T, Nishiuchi T, Saitou M, Asano M. 2011. Loss of heterochromatin protein 1 gamma reduces the number of primordial germ cells via impaired cell cycle progression in mice. Biol. Reprod. 85: 1013-1024.
31. Patel AC, Anna CH, Foley JF, Stockton PS, Tyson FL, Barrett JC, Devereux TR. 2000. Hypermethylation of the p16 (Ink4a) promoter in B6C3F1 mouse primary lung adenocarcinomas and mouse lung cell lines. Carcinogenesis 21:1691-1700.
32. McCabe MT, Davis JN, Day ML. 2005. Regulation of DNA methyltransferase 1 by the pRb/E2F1 pathway. Cancer Res. 65:3624-3632.
33. Qin W, Leonhardt H, Pichler G. 2011. Regulation of DNA methyltransferase 1 by interactions and modifications. Nucleus 2:392-402.
34. Bronner C. 2011. Control of DNMT1 abundance in epigenetic inheritance by acetylation, ubiquitylation, and the histone code. Sci. Signal. 4:pe3. doi:10.1126/scisignal.2001764.
35. Du Z, Song J, Wang Y, Zhao Y, Guda K, Yang S, Kao HY, Xu Y, Willis J, Markowitz SD, Sedwick D, Ewing RM, Wang Z. 2010. DNMT1 stability is regulated by proteins coordinating deubiquitination and acetylation- driven ubiquitination. Sci. Signal. 3:ra80. doi:10.1126/scisignal .2001462.
36. Sun Y, Jiang X, Price BD. 2010. Tip60: connecting chromatin to DNA damage signaling. Cell Cycle 9:930-936.
37. Rhee I, Jair KW, Yen RW, Lengauer C, Herman JG, Kinzler KW, Vogelstein B, Baylin SB, Schuebel KE. 2000. CpG methylation is maintained in human cancer cells lacking DNMT1. Nature 404:1003-1007.
38. Rhee I, Bachman KE, Park BH, Jair KW, Yen RW, Schuebel KE, Cui H, Feinberg AP, Lengauer C, Kinzler KW, Baylin SB, Vogelstein B. 2002. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 416:552-556.
39. Fournel M, Sapieha P, Beaulieu N, Besterman JM, MacLeod AR. 1999. Down-regulation of human DNA-(cytosine-5) methyltransferase induces cell cycle regulators p16ink4A and p21WAF/Cip1 by distinct mechanisms. J. Biol. Chem. 274:24250-24256.
40. Robert MF, Morin S, Beaulieu N, Gauthier F, Chute IC, Barsalou A, MacLeod AR. 2003. DNMT1 is required to maintain CpG methylation and aberrant gene silencing in human cancer cells. Nat. Genet. 33:61-65.
41. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre' M, Nuciforo PG, Bensimon A, Maestro R, Pelicci PG, d'Adda di Fagagna F. 2006. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444:638- 642.
42. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, Sougnez C, Greulich H, Muzny DM, Morgan MB, Fulton L, Fulton RS, Zhang Q, Wendl MC, Lawrence MS, Larson DE, Chen K, Dooling DJ, Sabo A, Hawes AC, Shen H, Jhangiani SN, Lewis LR, Hall O, Zhu Y, Mathew T, Ren Y, Yao J, Scherer SE, Clerc K, Metcalf GA, Ng B, Milosavljevic A, Gonzalez-Garay ML, Osborne JR, Meyer R, Shi X, Tang Y, Koboldt DC, Lin L, Abbott R, Miner TL, Pohl C, Fewell G, Haipek C, Schmidt H, Dunford-Shore BH, Kraja A, Crosby SD, Sawyer CS, et al. 2008. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455:1069-1075.