Making sense of ubiquitin ligases that regulate p53

Cancer Biology and Therapy

Volumn 10, Issue 7, 2010, Pages 665-672

  Jain, Abhinav K ^a   Barton, Michelle Craig ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Cancer; Developmental expression; E3 ligase; Proteasome; Protein degradation; Tissue specificity; Tumor suppressor

Indexed keywords

PROTEIN MDM2; PROTEIN P53; UBIQUITIN PROTEIN LIGASE E3;

APOPTOSIS; CANCER INHIBITION; CELL CYCLE ARREST; HUMAN; NONHUMAN; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN STABILITY; REVIEW; UBIQUITINATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; HUMANS; MODELS, BIOLOGICAL; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 77957558627     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.10.7.13445     Document Type: Review

References (88)

1. Soussi T, Beroud C. Assessing TP53 status in human tumours to evaluate clinical outcome. Nat Rev Cancer 2001; 1:233-40. (Pubitemid 33741898)
2. Hainaut P, Hollstein M. p53 and human cancer: The first ten thousand mutations. Adv Cancer Res 2000; 77:81-137. (Pubitemid 29439303)
3. Vousden KH, Prives C. Blinded by the Light: The Growing Complexity of p53. Cell 2009; 137:413-31.
4. Loewer A, Batchelor E, Gaglia G, Lahav G. Basal dynamics of p53 reveal transcriptionally attenuated pulses in cycling cells. Cell 142:89-100.
5. Hu W, Chan CS, Wu R, Zhang C, Sun Y, Song JS, et al. Negative Regulation of Tumor Suppressor p53 by MicroRNA miR-504. Mol Cell 38:689-99.
6. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408:307-10.
7. Horn HF, Vousden KH. Coping with stress: multiple ways to activate p53. Oncogene 2007; 26:1306-16.
8. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008; 9:402-12. (Pubitemid 351574202)
9. Laptenko O, Prives C. Transcriptional regulation by p53: one protein, many possibilities. Cell Death Differ 2006; 13:951-61.
10. Carter S, Vousden KH. Modifications of p53: competing for the lysines. Curr Opin Genet Dev 2009; 19:18-24.
11. Kruse JP, Gu W. Modes of p53 regulation. Cell 2009; 137:609-22.
12. Deshaies RJ, Joazeiro CA. RING domain E3 ubiquitin ligases. Annu Rev Biochem 2009; 78:399-434.
13. Chen ZJ, Sun LJ. Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell 2009; 33:275-86.
14. Brooks CL, Gu W. p53 ubiquitination: Mdm2 and beyond. Mol Cell 2006; 21:307-15.
15. Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007; 315:201-5.
16. Jain AK, Barton MC. Regulation of p53: TRIM24 enters the RING. Cell Cycle 2009; 8:3668-74.
17. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997; 387:296-9. (Pubitemid 27220766)
18. Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 1997; 420:25-7. (Pubitemid 28037193)
19. Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature 1997; 387:299-303.
20. Jones SN, Roe AE, Donehower LA, Bradley A. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature 1995; 378:206-8.
21. Montes de Oca Luna R, Wagner DS, Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 1995; 378:203-6.
22. Lu WJ, Abrams JM. Lessons from p53 in non-mammalian models. Cell Death Differ 2006; 13:909-12.
23. Wu X, Bayle JH, Olson D, Levine AJ. The p53-mdm-2 autoregulatory feedback loop. Genes Dev 1993; 7:1126-32.
24. Stommel JM, Wahl GM. Accelerated MDM2 auto-degradation induced by DNA-damage kinases is required for p53 activation. EMBO J 2004; 23:1547-56.
25. Manfredi JJ. The Mdm2-p53 relationship evolves: Mdm2 swings both ways as an oncogene and a tumor suppressor. Genes Dev 24:1580-9.
26. Momand J, Zambetti GP, Olson DC, George D, Levine AJ. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992; 69:1237-45.
27. Chen J, Marechal V, Levine AJ. Mapping of the p53 and mdm-2 interaction domains. Mol Cell Biol 1993; 13:4107-14.
28. Yu GW, Rudiger S, Veprintsev D, Freund S, Fernandez-Fernandez MR, Fersht AR. The central region of HDM2 provides a second binding site for p53. Proc Natl Acad Sci USA 2006; 103:1227-32. (Pubitemid 43191147)
29. Shimizu H, Burch LR, Smith AJ, Dornan D, Wallace M, Ball KL, Hupp TR. The conformationally flexible S9-S10 linker region in the core domain of p53 contains a novel MDM2 binding site whose mutation increases ubiquitination of p53 in vivo. J Biol Chem 2002; 277:28446-58. (Pubitemid 41079269)
30. Marine JC, Francoz S, Maetens M, Wahl G, Toledo F, Lozano G. Keeping p53 in check: essential and synergistic functions of Mdm2 and Mdm4. Cell Death Differ 2006; 13:927-34. (Pubitemid 43346452)
31. Uldrijan S, Pannekoek WJ, Vousden KH. An essential function of the extreme C-terminus of MDM2 can be provided by MDMX. EMBO J 2007; 26:102-12.
32. Singh RK, Iyappan S, Scheffner M. Heterooligomerization with MdmX rescues the ubiquitin/Nedd8 ligase activity of RING finger mutants of Mdm2. J Biol Chem 2007; 282:10901-7.
33. Meek DW, Knippschild U. Posttranslational modification of MDM2. Mol Cancer Res 2003; 1:1017-26.
34. Kawai H, Wiederschain D, Kitao H, Stuart J, Tsai KK, Yuan ZM. DNA damage-induced MDMX degradation is mediated by MDM2. J Biol Chem 2003; 278:45946-53. (Pubitemid 37432741)
35. Li M, Brooks CL, Wu-Baer F, Chen D, Baer R, Gu W. Mono- versus poly-ubiquitination: differential control of p53 fate by Mdm2. Science 2003; 302:1972-5.
36. Nie L, Sasaki M, Maki CG. Regulation of p53 nuclear export through sequential changes in conformation and ubiquitination. J Biol Chem 2007; 282:14616-25.
37. Grossman SR, Deato ME, Brignone C, Chan HM, Kung AL, Tagami H, et al. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science 2003; 300:342-4.
38. Sui G, Affar el B, Shi Y, Brignone C, Wall NR, Yin P, et al. Yin Yang 1 is a negative regulator of p53. Cell 2004; 117:859-72.
39. Higashitsuji H, Itoh K, Sakurai T, Nagao T, Sumitomo Y, Masuda T, et al. The oncoprotein gankyrin binds to MDM2/HDM2, enhancing ubiquitylation and degradation of p53. Cancer Cell 2005; 8:75-87. (Pubitemid 40991816)
40. Wang C, Ivanov A, Chen L, Fredericks WJ, Seto E, Rauscher FJ, 3rd, Chen J. MDM2 interaction with nuclear corepressor KAP1 contributes to p53 inactivation. EMBO J 2005; 24:3279-90.
41. Du W, Jiang P, Li N, Mei Y, Wang X, Wen L, et al. Suppression of p53 activity by Siva1. Cell Death Differ 2009; 16:1493-504.
42. Xirodimas DP, Saville MK, Bourdon JC, Hay RT, Lane DP. Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell 2004; 118:83-97.
43. Carter S, Bischof O, Dejean A, Vousden KH. C-terminal modifications regulate MDM2 dissociation and nuclear export of p53. Nat Cell Biol 2007; 9:428-35. (Pubitemid 46511076)
44. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W. Acetylation is indispensable for p53 activation. Cell 2008; 133:612-26.
45. Itahana K, Mao H, Jin A, Itahana Y, Clegg HV, Lindstrom MS, et al. Targeted inactivation of Mdm2 RING finger E3 ubiquitin ligase activity in the mouse reveals mechanistic insights into p53 regulation. Cancer Cell 2007; 12:355-66. (Pubitemid 47539309)
46. 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; 10:501-14. (Pubitemid 44854749)
47. Feng L, Lin T, Uranishi H, Gu W, Xu Y. Functional analysis of the roles of posttranslational modifications at the p53 C terminus in regulating p53 stability and activity. Mol Cell Biol 2005; 25:5389-95. (Pubitemid 40853576)
48. Krummel KA, Lee CJ, Toledo F, Wahl GM. The C-terminal lysines fine-tune p53 stress responses in a mouse model but are not required for stability control or transactivation. Proc Natl Acad Sci USA 2005; 102:10188-93. (Pubitemid 41023347)
49. Leng RP, Lin Y, Ma W, Wu H, Lemmers B, Chung S, et al. Pirh2, a p53-induced ubiquitin-protein ligase, promotes p53 degradation. Cell 2003; 112:779-91. (Pubitemid 36378882)
50. Parant J, Chavez-Reyes A, Little NA, Yan W, Reinke V, Jochemsen AG, Lozano G. Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53. Nat Genet 2001; 29:92-5. (Pubitemid 32801817)
51. Daujat S, Neel H, Piette J. Preferential expression of Mdm2 oncogene during the development of neural crest and its derivatives in mouse early embryogenesis. Mech Dev 2001; 103:163-5. (Pubitemid 32457921)
52. Chavez-Reyes A, Parant JM, Amelse LL, de Oca Luna RM, Korsmeyer SJ, Lozano G. Switching mechanisms of cell death in mdm2- and mdm4-null mice by deletion of p53 downstream targets. Cancer Res 2003; 63:8664-9. (Pubitemid 38064041)
53. Bourdon JC. p53 and its isoforms in cancer. Br J Cancer 2007; 97:277-82.
54. Midgley CA, Owens B, Briscoe CV, Thomas DB, Lane DP, Hall PA. Coupling between gamma irradiation, p53 induction and the apoptotic response depends upon cell type in vivo. J Cell Sci 1995; 108:1843-8.
55. INK4a loss. Genes Dev 2008; 22:1337-44.
56. Laine A, Topisirovic I, Zhai D, Reed JC, Borden KL, Ronai Z. Regulation of p53 localization and activity by Ubc13. Mol Cell Biol 2006; 26:8901-13.
57. Khetchoumian K, Teletin M, Tisserand J, Mark M, Herquel B, Ignat M, et al. Loss of Trim24 (Tif1alpha) gene function confers oncogenic activity to retinoic acid receptor alpha. Nat Genet 2007; 39:1500-6.
58. Allton K, Jain AK, Herz HM, Tsai WW, Jung SY, Qin J, et al. Trim24 targets endogenous p53 for degradation. Proc Natl Acad Sci USA 2009; 106:11612-6.
59. Liu L, Scolnick DM, Trievel RC, Zhang HB, Marmorstein R, Halazonetis TD, Berger SL. p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol Cell Biol 1999; 19:1202-9. (Pubitemid 29046862)
60. Huang J, Perez-Burgos L, Placek BJ, Sengupta R, Richter M, Dorsey JA, et al. Repression of p53 activity by Smyd2-mediated methylation. Nature 2006; 444:629-32. (Pubitemid 44864441)
61. Huang J, Sengupta R, Espejo AB, Lee MG, Dorsey JA, Richter M, et al. p53 is regulated by the lysine demethylase LSD1. Nature 2007; 449:105-8. (Pubitemid 47373772)
62. Huang J, Dorsey J, Chuikov S, Perez-Burgos L, Zhang X, Jenuwein T, et al. G9a and Glp methylate lysine 373 in the tumor suppressor p53. J Biol Chem 285:9636-41.
63. Murray-Zmijewski F, Slee EA, Lu X. A complex barcode underlies the heterogeneous response of p53 to stress. Nat Rev Mol Cell Biol 2008; 9:702-12.
64. Bode AM, Dong Z. Post-translational modification of p53 in tumorigenesis. Nat Rev Cancer 2004; 4:793-805.
65. Olsson A, Manzl C, Strasser A, Villunger A. How important are post-translational modifications in p53 for selectivity in target-gene transcription and tumour suppression? Cell Death Differ 2007; 14:1561-75.
66. Toledo F, Wahl GM. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 2006; 6:909-23. (Pubitemid 44862676)
67. Yang WH, Kim JE, Nam HW, Ju JW, Kim HS, Kim YS, Cho JW. Modification of p53 with O-linked N-acetylglucosamine regulates p53 activity and stability. Nat Cell Biol 2006; 8:1074-83.
68. Meek DW, Anderson CW. Posttranslational Modification of p53: cooperative integrators of function. Cold Spring Harb Perspect Biol 2009; 1:000950.
69. Harris SL, Levine AJ. The p53 pathway: positive and negative feedback loops. Oncogene 2005; 24:2899-908.
70. Donehower LA, Lozano G. 20 years studying p53 functions in genetically engineered mice. Nat Rev Cancer 2009; 9:831-41.
71. Shi D, Pop MS, Kulikov R, Love IM, Kung AL, Grossman SR. CBP and p300 are cytoplasmic E4 polyubiquitin ligases for p53. Proc Natl Acad Sci USA 2009; 106:16275-80.
72. Gu W, Roeder RG. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 1997; 90:595-606.
73. Sato Y, Kamura T, Shirata N, Murata T, Kudoh A, Iwahori S, et al. Degradation of phosphorylated p53 by viral protein-ECS E3 ligase complex. PLoS Pathog 2009; 5:1000530.
74. Sheng Y, Laister RC, Lemak A, Wu B, Tai E, Duan S, et al. Molecular basis of Pirh2-mediated p53 ubiquitylation. Nat Struct Mol Biol 2008; 15:1334-42.
75. 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.
76. 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; 279:36440-4.
77. 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; 121:1071-83. (Pubitemid 40884397)
78. Laine A, Ronai Z. Regulation of p53 localization and transcription by the HECT domain E3 ligase WWP1. Oncogene 2007; 26:1477-83. (Pubitemid 46340811)
79. Boutell C, Everett RD. The herpes simplex virus type 1 (HSV-1) regulatory protein ICP0 interacts with and Ubiquitinates p53. J Biol Chem 2003; 278:36596-602. (Pubitemid 37139991)
80. Andrews P, He YJ, Xiong Y. Cytoplasmic localized ubiquitin ligase cullin 7 binds to p53 and promotes cell growth by antagonizing p53 function. Oncogene 2006; 25:4534-48. (Pubitemid 44175113)
81. Yang W, Rozan LM, McDonald ER, 3rd, Navaraj A, Liu JJ, Matthew EM, et al. CARPs are ubiquitin ligases that promote MDM2-independent p53 and phosphop53ser20 degradation. J Biol Chem 2007; 282:3273-81.
82. 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; 26:113-22.
83. Esser C, Scheffner M, Hohfeld J. The chaperone-associated ubiquitin ligase CHIP is able to target p53 for proteasomal degradation. J Biol Chem 2005; 280:27443-8. (Pubitemid 41040787)
84. 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; 127:775-88. (Pubitemid 44716249)
85. 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; 15:3104-17.
86. Kruse JP, Gu W. MSL2 promotes Mdm2-independent cytoplasmic localization of p53. J Biol Chem 2009; 284:3250-63.
87. Sun L, Shi L, Li W, Yu W, Liang J, Zhang H, et al. JFK, a Kelch domain-containing F-box protein, links the SCF complex to p53 regulation. Proc Natl Acad Sci USA 2009; 106:10195-200.
88. Lee EW, Lee MS, Camus S, Ghim J, Yang MR, Oh W, et al. Differential regulation of p53 and p21 by MKRN1 E3 ligase controls cell cycle arrest and apoptosis. EMBO J 2009; 28:2100-13.