DNA damage-induced activation of ATM promotes β-TRCPmediated Mdm2 ubiquitination and destruction

Oncotarget

Volumn 3, Issue 9, 2012, Pages 1026-1035

  Wang, Zhiwei ^a   Inuzuka, Hiroyuki ^a   Zhong, Jiateng ^a,b   Fukushima, Hidefumi ^a   Wan, Lixin ^a   Liu, Pengda ^a   Wei, Wenyi ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Basic Medical College   (China)

Author keywords

And cancer; ATM; CKId; Destruction; DNA damage; Mdm2; Ubiquitination; TRCP

Indexed keywords

ATM PROTEIN; BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; CASEIN KINASE IDELTA; PROTEIN MDM2; PROTEIN P53;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DNA DAMAGE; ENZYME INACTIVATION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DESTRUCTION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UBIQUITINATION;

EID: 84868623430     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.640     Document Type: Article

References (44)

1. Siegel R, Naishadham D and Jemal A. Cancer statistics, 2012. CA Cancer J Clin. 2012; 62(1):10-29.
2. Freed-Pastor WA and Prives C. Mutant p53: one name, many proteins. Genes Dev. 2012; 26(12):1268-1286.
3. Menendez D, Inga A and Resnick MA. The expanding universe of p53 targets. Nat Rev Cancer. 2009; 9(10):724-737.
4. Meek DW. Tumour suppression by p53: a role for the DNA damage response? Nat Rev Cancer. 2009; 9(10):714-723.
5. Toledo F and Wahl GM. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer. 2006; 6(12):909-923.
6. Oliner JD, Pietenpol JA, Thiagalingam S, Gyuris J, Kinzler KW and Vogelstein B. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature. 1993; 362(6423):857-860.
7. Rolfe M, Beer-Romero P, Glass S, Eckstein J, Berdo I, Theodoras A, Pagano M and Draetta G. Reconstitution of p53-ubiquitinylation reactions from purified components: the role of human ubiquitin-conjugating enzyme UBC4 and E6-associated protein (E6AP). Proc Natl Acad Sci U S A. 1995; 92(8):3264-3268.
8. Yang X, Li H, Zhou Z, Wang WH, Deng A, Andrisani O and Liu X. Plk1-mediated phosphorylation of Topors regulates p53 stability. J Biol Chem. 2009; 284(28):18588-18592.
9. Coumailleau F, Das V, Alcover A, Raposo G, Vandormael-Pournin S, Le Bras S, Baldacci P, Dautry-Varsat A, Babinet C and Cohen-Tannoudji M. Over-expression of Rififylin, a new RING finger and FYVE-like domain-containing protein, inhibits recycling from the endocytic recycling compartment. Mol Biol Cell. 2004; 15(10):4444-4456.
10. Dornan D, Wertz I, Shimizu H, Arnott D, Frantz GD, Dowd P, O'Rourke K, Koeppen H and Dixit VM. The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature. 2004; 429(6987):86-92.
11. Jung YS, Qian Y and Chen X. Pirh2 RING-finger E3 ubiquitin ligase: its role in tumorigenesis and cancer therapy. FEBS Lett. 2012; 586(10):1397-1402.
12. Montes de Oca Luna R, Wagner DS and Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature. 1995; 378(6553):203-206.
13. Jones SN, Roe AE, Donehower LA and Bradley A. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature. 1995; 378(6553):206-208.
14. Manfredi JJ. The Mdm2-p53 relationship evolves: Mdm2 swings both ways as an oncogene and a tumor suppressor. Genes Dev. 2010; 24(15):1580-1589.
15. Miliani de Marval PL and Zhang Y. The RP-Mdm2-p53 pathway and tumorigenesis. Oncotarget. 2011; 2(3):234-238.
16. Azmi AS, Banerjee S, Ali S, Wang Z, Bao B, Beck FW, Maitah M, Choi M, Shields TF, Philip PA, Sarkar FH and Mohammad RM. Network modeling of MDM2 inhibitoroxaliplatin combination reveals biological synergy in wtp53 solid tumors. Oncotarget. 2011; 2(5):378-392.
17. Inuzuka H, Fukushima H, Shaik S and Wei W. Novel insights into the molecular mechanisms governing Mdm2 ubiquitination and destruction. Oncotarget. 2010; 1(7):685-690.
18. Inuzuka H, Tseng A, Gao D, Zhai B, Zhang Q, Shaik S, Wan L, Ang XL, Mock C, Yin H, Stommel JM, Gygi S, Lahav G, Asara J, Xiao ZX, Kaelin WG, Jr., et al. Phosphorylation by casein kinase I promotes the turnover of the Mdm2 oncoprotein via the SCF(beta-TRCP) ubiquitin ligase. Cancer Cell. 2010; 18(2):147-159.
19. Taira N, Yamamoto H, Yamaguchi T, Miki Y and Yoshida K. ATM augments nuclear stabilization of DYRK2 by inhibiting MDM2 in the apoptotic response to DNA damage. J Biol Chem. 2010; 285(7):4909-4919.
20. Cheng Q, Chen L, Li Z, Lane WS and Chen J. ATM activates p53 by regulating MDM2 oligomerization and E3 processivity. EMBO J. 2009; 28(24):3857-3867.
21. Chang L, Zhou B, Hu S, Guo R, Liu X, Jones SN and Yen Y. ATM-mediated serine 72 phosphorylation stabilizes ribonucleotide reductase small subunit p53R2 protein against MDM2 to DNA damage. Proc Natl Acad Sci U S A. 2008; 105(47):18519-18524.
22. Derheimer FA and Kastan MB. Multiple roles of ATM in monitoring and maintaining DNA integrity. FEBS Lett. 2010; 584(17):3675-3681.
23. Maya R, Balass M, Kim ST, Shkedy D, Leal JF, Shifman O, Moas M, Buschmann T, Ronai Z, Shiloh Y, Kastan MB, Katzir E and Oren M. ATM-dependent phosphorylation of Mdm2 on serine 395: role in p53 activation by DNA damage. Genes Dev. 2001; 15(9):1067-1077.
24. Gannon HS, Woda BA and Jones SN. ATM phosphorylation of Mdm2 Ser394 regulates the amplitude and duration of the DNA damage response in mice. Cancer Cell. 2012; 21(5):668-679.
25. Fang S, Jensen JP, Ludwig RL, Vousden KH and Weissman AM. Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J Biol Chem. 2000; 275(12):8945-8951.
26. Stommel JM and Wahl GM. Accelerated MDM2 autodegradation induced by DNA-damage kinases is required for p53 activation. EMBO J. 2004; 23(7):1547-1556.
27. Itahana K, Mao H, Jin A, Itahana Y, Clegg HV, Lindstrom MS, Bhat KP, Godfrey VL, Evan GI and Zhang Y. Targeted inactivation of Mdm2 RING finger E3 ubiquitin ligase activity in the mouse reveals mechanistic insights into p53 regulation. Cancer Cell. 2007; 12(4):355-366.
28. Frescas D and Pagano M. Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat Rev Cancer. 2008; 8(6):438-449.
29. Pei D, Zhang Y and Zheng J. Regulation of p53: a collaboration between Mdm2 and Mdmx. Oncotarget. 2012; 3(3):228-235.
30. Meulmeester E, Pereg Y, Shiloh Y and Jochemsen AG. ATM-mediated phosphorylations inhibit Mdmx/Mdm2 stabilization by HAUSP in favor of p53 activation. Cell Cycle. 2005; 4(9):1166-1170.
31. Khosravi R, Maya R, Gottlieb T, Oren M, Shiloh Y and Shkedy D. Rapid ATM-dependent phosphorylation of MDM2 precedes p53 accumulation in response to DNA damage. Proc Natl Acad Sci U S A. 1999; 96(26):14973-14977.
32. Lu X, Ma O, Nguyen TA, Jones SN, Oren M and Donehower LA. The Wip1 Phosphatase acts as a gatekeeper in the p53-Mdm2 autoregulatory loop. Cancer Cell. 2007; 12(4):342-354.
33. Santos JA, Logarinho E, Tapia C, Allende CC, Allende JE and Sunkel CE. The casein kinase 1 alpha gene of Drosophila melanogaster is developmentally regulated and the kinase activity of the protein induced by DNA damage. J Cell Sci. 1996; 109 ( Pt 7):1847-1856.
34. Jin VX, Rabinovich A, Squazzo SL, Green R and Farnham PJ. A computational genomics approach to identify cisregulatory modules from chromatin immunoprecipitation microarray data--a case study using E2F1. Genome Res. 2006; 16(12):1585-1595.
35. Alsheich-Bartok O, Haupt S, Alkalay-Snir I, Saito S, Appella E and Haupt Y. PML enhances the regulation of p53 by CK1 in response to DNA damage. Oncogene. 2008; 27(26):3653-3661.
36. Fu D, Calvo JA and Samson LD. Balancing repair and tolerance of DNA damage caused by alkylating agents. Nat Rev Cancer. 2012; 12(2):104-120.
37. Smith J, Tho LM, Xu N and Gillespie DA. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Cancer Res. 2010; 108:73-112.
38. Khoronenkova SV, Dianova, II, Ternette N, Kessler BM, Parsons JL and Dianov GL. ATM-dependent downregulation of USP7/HAUSP by PPM1G activates p53 response to DNA damage. Mol Cell. 2012; 45(6):801-813.
39. Wang Z and Li B. Mdm2 links genotoxic stress and metabolism to p53. Protein Cell. 2010; 1(12):1063-1072.
40. Reinhardt HC, Aslanian AS, Lees JA and Yaffe MB. p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell. 2007; 11(2):175-189.
41. Pang LY, Scott M, Hayward RL, Mohammed H, Whitelaw CB, Smith GC and Hupp TR. p21(WAF1) is component of a positive feedback loop that maintains the p53 transcriptional program. Cell Cycle. 2011; 10(6):932-950.
42. Cheng Q and Chen J. Mechanism of p53 stabilization by ATM after DNA damage. Cell Cycle. 2010; 9(3):472-478.
43. Jin J, Shirogane T, Xu L, Nalepa G, Qin J, Elledge SJ and Harper JW. SCFbeta-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes Dev. 2003; 17(24):3062-3074.
44. Shirogane T, Jin J, Ang XL and Harper JW. SCFbeta-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein. J Biol Chem. 2005; 280(29):26863-26872.