The multiple levels of regulation by p53 ubiquitination

Cell Death and Differentiation

Volumn 17, Issue 1, 2010, Pages 86-92

  Lee, J T ^a   Gu, W ^a  

^a Columbia University ^*  (United States)

Author keywords

apoptosis; HAUSP; Mdm2; Mdmx; p53; ubiquitination

Indexed keywords

ONCOPROTEIN; PROTEASOME; PROTEIN MDM2; PROTEIN P53; UBIQUITIN PROTEIN LIGASE; UBIQUITIN THIOLESTERASE; USP7 PROTEIN, HUMAN;

CANCER INHIBITION; CELL DEATH; CELL NUCLEUS; CELL PROLIFERATION; CELLULAR STRESS RESPONSE; CYTOSOL; DEATH; DEGRADATION; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; STRESS; UBIQUITINATION; ANIMAL; APOPTOSIS; HUMAN; METABOLISM; MOUSE;

MUS;

ANIMALS; APOPTOSIS; HUMANS; MICE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN THIOLESTERASE; UBIQUITINATION;

EID: 77449155637     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2009.77     Document Type: Review

References (68)

1. Kruse JP, Gu W. SnapShot: p53 posttranslational modifications. Cell 2008; 133: 930 e931.
2. Scoumanne A, Chen X. Protein methylation: a new mechanism of p53 tumor suppressor regulation. Histol Histopathol 2008; 23: 1143-1149.
3. Haglund K, Dikic I. Ubiquitylation and cell signaling. EMBO J 2005; 24: 3353-3359. (Pubitemid 41486773)
4. Lee JT, Wheeler TC, Li L, Chin LS. Ubiquitination of alpha-synuclein by Siah-1 promotes alpha-synuclein aggregation and apoptotic cell death. Hum Mol Genet 2008; 17: 906-917. (Pubitemid 351359706)
5. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997; 387: 296-299. (Pubitemid 27220766)
6. Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 1997; 420: 25-27. (Pubitemid 28037193)
7. Brooks CL, Gu W. p53 ubiquitination: Mdm2 and beyond. Mol Cell 2006; 21: 307-315. (Pubitemid 43163526)
8. Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature 1997; 387: 299-303. (Pubitemid 27220767)
9. Rodriguez MS, Desterro JM, Lain S, Lane DP, Hay RT. Multiple C-terminal lysine residues target p53 for ubiquitin-proteasome-mediated degradation. Mol Cell Biol 2000; 20: 8458-8467.
10. Chan WM, Mak MC, Fung TK, Lau A, Siu WY, Poon RY. Ubiquitination of p53 at multiple sites in the DNA-binding domain. Mol Cancer Res 2006; 4: 15-25. (Pubitemid 43259886)
11. Ito A, Lai CH, Zhao X, Saito S, Hamilton MH, Appella E et al. p300/CBP-mediated p53 acetylation is commonly induced by p53-activating agents and inhibited by MDM2. EMBO J 2001; 20: 1331-1340. (Pubitemid 32233973)
12. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W. Acetylation is indispensable for p53 activation. Cell 2008; 133: 612-626. (Pubitemid 351636297)
13. Wang X, Taplick J, Geva N, Oren M. Inhibition of p53 degradation by Mdm2 acetylation. FEBS Lett 2004; 561: 195-201. (Pubitemid 38317321)
14. Wu X, Bayle JH, Olson D, Levine AJ. The p53-mdm-2 autoregulatory feedback loop. Genes Dev 1993; 7: 1126-1132. (Pubitemid 23207405)
15. Clegg HV, Itahana K, Zhang Y. Unlocking the Mdm2-p53 loop: ubiquitin is the key. Cell Cycle 2008; 7: 287-292. (Pubitemid 351366489)
16. Toledo F, Wahl GM. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 2006; 6: 909-923. (Pubitemid 44862676)
17. Kruse JP, GU W. Modes of p53 regulation. Cell 2009; 137: 609-622.
18. Li M, Brooks CL, Wu-Baer F, Chen D, Baer R, Gu W. Mono- versus polyubiquitination: differential control of p53 fate by Mdm2. Science 2003; 302: 1972-1975. (Pubitemid 37523506)
19. Lohrum MA, Ashcroft M, Kubbutat MH, Vousden KH. Contribution of two independent MDM2-binding domains in p14(ARF) to p53 stabilization. Curr Biol 2000; 10: 539-542. (Pubitemid 30308313)
20. Gallagher SJ, Kefford RF, Rizos H. The ARF tumour suppressor. Int J Biochem Cell Biol 2006; 38: 1637-1641. (Pubitemid 43947645)
21. Chen D, Kon N, Li M, Zhang W, Qin J, Gu W. ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell 2005; 121: 1071-1083. (Pubitemid 40884397)
22. Honda R, Yasuda H. Association of p19(ARF) with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53. EMBO J 1999; 18: 22-27. (Pubitemid 29005019)
23. Sharpless NE. INK4a/ARF: a multifunctional tumor suppressor locus. Mutat Res 2005; 576: 22-38. (Pubitemid 40982680)
24. Korgaonkar C, Hagen J, Tompkins V, Frazier AA, Allamargot C, Quelle FW et al. Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function. Mol Cell Biol 2005; 25: 1258-1271. (Pubitemid 40204905)
25. Sharp DA, Kratowicz SA, Sank MJ, George DL. Stabilization of the MDM2 oncoprotein by interaction with the structurally related MDMX protein. J Biol Chem 1999; 274: 38189-38196. (Pubitemid 30026893)
26. Tanimura S, Ohtsuka S, Mitsui K, Shirouzu K, Yoshimura A, Ohtsubo M. MDM2 interacts with MDMX through their RING finger domains. FEBS Lett 1999; 447: 5-9. (Pubitemid 29134936)
27. Ghosh M, Huang K, Berberich SJ. Overexpression of Mdm2 and MdmX fusion proteins alters p53 mediated transactivation, ubiquitination, and degradation. Biochemistry 2003; 42: 2291-2299. (Pubitemid 36255203)
28. Pan Y, Chen J. MDM2 promotes ubiquitination and degradation of MDMX. Mol Cell Biol 2003; 23: 5113-5121. (Pubitemid 36950868)
29. Linares LK, Hengstermann A, Ciechanover A, Muller S, Scheffner M. HdmX stimulates Hdm2-mediated ubiquitination and degradation of p53. Proc Natl Acad Sci USA 2003; 100: 12009-12014. (Pubitemid 37271506)
30. Parant J, Chavez-Reyes A, Little NA, Yan W, Reinke V, Jochemsen AG et al. Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53. Nat Genet 2001; 29: 92-95. (Pubitemid 32801817)
31. Jones SN, Roe AE, Donehower LA, Bradley A. Rescue of embryonic lethality in Mdm2- deficient mice by absence of p53. Nature 1995; 378: 206-208.
32. Montes de Oca Luna R, Wagner DS, Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 1995; 378: 203-206.
33. Francoz S, Froment P, Bogaerts S, De Clercq S, Maetens M, Doumont G et al. Mdm4 and Mdm2 cooperate to inhibit p53 activity in proliferating and quiescent cells in vivo. Proc Natl Acad Sci USA 2006; 103: 3232-3237. (Pubitemid 43346453)
34. Xiong S, Van Pelt CS, Elizondo-Fraire AC, Liu G, Lozano G. Synergistic roles of Mdm2 and Mdm4 for p53 inhibition in central nervous system development. Proc Natl Acad Sci USA 2006; 103: 3226-3231. (Pubitemid 43346452)
35. Li M, Chen D, Shiloh A, Luo J, Nikolaev AY, Qin J et al. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 2002; 416: 648-653. (Pubitemid 34406767)
36. Marchenko ND, Wolff S, Erster S, Becker K, Moll UM. Monoubiquitylation promotes mitochondrial p53 translocation. EMBO J 2007; 26: 923-934.
37. Brooks CL, Li M, Hu M, Shi Y, Gu W. The p53 - Mdm2 - HAUSP complex is involved in p53 stabilization by HAUSP. Oncogene 2007; 26: 7262-7266. (Pubitemid 350085320)
38. Meulmeester E, Maurice MM, Boutell C, Teunisse AF, Ovaa H, Abraham TE et al. Loss of HAUSP-mediated deubiquitination contributes to DNA damage-induced destabilization of Hdmx and Hdm2. Mol Cell 2005; 18: 565-576. (Pubitemid 40726233)
39. Ringshausen I, O'Shea CC, Finch AJ, Swigart LB, Evan GI. Mdm2 is critically and continuously required to suppress lethal p53 activity in vivo. Cancer Cell 2006; 10: 501-514. (Pubitemid 44854749)
40. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993; 75: 495-505. (Pubitemid 23335075)
41. Leng RP, Lin Y, Ma W, Wu H, Lemmers B, Chung S et al. Pirh2, a p53-induced ubiquitinprotein ligase, promotes p53 degradation. Cell 2003; 112: 779-791. (Pubitemid 36378882)
42. Aylon Y, Oren M. Living with p53, dying of p53. Cell 2007; 130: 597-600. (Pubitemid 47268063)
43. Horn HF, Vousden KH. Coping with stress: multiple ways to activate p53. Oncogene 2007; 26: 1306-1316. (Pubitemid 46328472)
44. Rajendra R, Malegaonkar D, Pungaliya P, Marshall H, Rasheed Z, Brownell J et al. Topors functions as an E3 ubiquitin ligase with specific E2 enzymes and ubiquitinates p53. J Biol Chem 2004; 279: 36440-36444. (Pubitemid 39128984)
45. Dornan D, Wertz I, Shimizu H, Arnott D, Frantz GD, Dowd P et al. The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature 2004; 429: 86-92. (Pubitemid 38620556)
46. Yang W, Rozan LM, McDonald 3rd ER, Navaraj A, Liu JJ, Matthew EM et al. CARPs are ubiquitin ligases that promote MDM2-independent p53 and phospho-p53ser20 degradation. J Biol Chem 2007; 282: 3273-3281. (Pubitemid 47084358)
47. Yamasaki S, Yagishita N, Sasaki T, Nakazawa M, Kato Y, Yamadera T et al. Cytoplasmic destruction of p53 by the endoplasmic reticulum-resident ubiquitin ligase 'Synoviolin'. EMBO J 2007; 26: 113-122. (Pubitemid 46094704)
48. Esser C, Scheffner M, Hohfeld J. The chaperone-associated ubiquitin ligase CHIP is able to target p53 for proteasomal degradation. J Biol Chem 2005; 280: 27443-27448. (Pubitemid 41040787)
49. Querido E, Blanchette P, Yan Q, Kamura T, Morrison M, Boivin D et al. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev 2001; 15: 3104-3117. (Pubitemid 33115675)
50. Laine A, Topisirovic I, Zhai D, Reed JC, Borden KL, Ronai Z. Regulation of p53 localization and activity by Ubc13. Mol Cell Biol 2006; 26: 8901-8913. (Pubitemid 44851948)
51. Laine A, Ronai Z. Regulation of p53 localization and transcription by the HECT domain E3 ligase WWP1. Oncogene 2007; 26: 1477-1483. (Pubitemid 46340811)
52. Le Cam L, Linares LK, Paul C, Julien E, Lacroix M, Hatchi E et al. E4F1 is an atypical ubiquitin ligase that modulates p53 effector functions independently of degradation. Cell 2006; 127: 775-788. (Pubitemid 44716249)
53. Chao C, Wu Z, Mazur SJ, Borges H, Rossi M, Lin T et al. Acetylation of mouse p53 at lysine 317 negatively regulates p53 apoptotic activities after DNA damage. Mol Cell Biol 2006; 26: 6859-6869. (Pubitemid 44387635)
54. Kruse JP, Gu W. MSL2 Promotes Mdm2-independent cytoplasmic localization of p53. J Biol Chem 2009; 284: 3250-3263.
55. Lohrum MA, Woods DB, Ludwig RL, Balint E, Vousden KH. C-terminal ubiquitination of p53 contributes to nuclear export. Mol Cell Biol 2001; 21: 8521-8532. (Pubitemid 33108611)
56. Stommel JM, Marchenko ND, Jimenez GS, Moll UM, Hope TJ, Wahl GM. A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. EMBO J 1999; 18: 1660-1672. (Pubitemid 29127078)
57. Brooks CL, Li M, Gu W. Mechanistic studies of MDM2-mediated ubiquitination in p53 regulation. J Biol Chem 2007; 282: 22804-22815. (Pubitemid 47267318)
58. Nie L, Sasaki M, Maki CG. Regulation of p53 nuclear export through sequential changes in conformation and ubiquitination. J Biol Chem 2007; 282: 14616-14625. (Pubitemid 47100427)
59. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 11: 577-590. (Pubitemid 36385115)
60. Leu JI, Dumont P, Hafey M, Murphy ME, George DL. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat Cell Biol 2004; 6: 443-450. (Pubitemid 38607505)
61. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004; 303: 1010-1014. (Pubitemid 38209704)
62. Everett RD, Meredith M, Orr A, Cross A, Kathoria M, Parkinson J. A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein. EMBO J 1997; 16: 1519-1530. (Pubitemid 27151947)
63. Feng Z, Zhang H, Levine AJ, Jin S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci USA 2005; 102: 8204-8209. (Pubitemid 40800067)
64. Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri-Mergny M, D'Amelio M et al. Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 2008; 10: 676-687. (Pubitemid 351772933)
65. Fuchs SY, Adler V, Pincus MR, Ronai Z. MEKK1/JNK signaling stabilizes and activates p53. Proc Natl Acad Sci USA 1998; 95: 10541-10546. (Pubitemid 28413103)
66. Fuchs SY, Adler V, Buschmann T, Yin Z, Wu X, Jones SN et al. JNK targets p53 ubiquitination and degradation in nonstressed cells. Genes Dev 1998; 12: 2658-2663. (Pubitemid 28420646)
67. Brooks CL, Gu W. Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation. Curr Opin Cell Biol 2003; 15: 164-171. (Pubitemid 36332191)
68. Carter S, Vousden KH. p53-Ubl fusions as models of ubiquitination, sumoylation and neddylation of p53. Cell Cycle 2008; 7: 2519-2528.