Mechanisms of p53 degradation

Clinica Chimica Acta

Volumn 438, Issue , 2014, Pages 139-147

  Chao, Chuck C K ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

De ubiquitinating enzyme; E3 ligase; Mdm2; P53; Proteasome; Ubiquitin

Indexed keywords

ARF BINDING PROTEIN 1; ARF PROTEIN; CULLIN; DNA DAMGAGE BINDING PROTEIN 1; E1A ASSOCIATED P300 PROTEIN; MAKORIN RING FINGER PROTEIN 1; PROTEIN CARP1; PROTEIN CARP2; PROTEIN MDM2; PROTEIN P53; PROTEIN SYNOVIOLIN; RING FINGER PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE COP1; UBIQUITIN PROTEIN LIGASE CUL4A; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE ROC; UBIQUITIN PROTEIN LIGASE UBE4B; UNCLASSIFIED DRUG;

CARBOXY TERMINAL SEQUENCE; GENE; GENE ACTIVITY; GENE MUTATION; HUMAN; NEDDYLATION; NONHUMAN; P53 GENE; PIRH2 GENE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SUMOYLATION; UBIQUITINATION; ANIMAL; METABOLISM;

ANIMALS; HUMANS; PROTEOLYSIS; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITINATION;

EID: 84907185306     PISSN: 00098981     EISSN: 18733492     Source Type: Journal    
DOI: 10.1016/j.cca.2014.08.015     Document Type: Review

References (112)

1. Everett R.D., 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 herpes virus regulatory protein. EMBO J 1997, 16:1519-1530.
2. Brooks C.L., Gu W. p53 regulation by ubiquitin. FEBS Lett 2011, 585:2803-2809.
3. Love I.M., Grossman S.R. It takes 15 to tango: making sense of the many ubiquitin ligases of p53. Genes Cancer 2012, 3:249-263.
4. Satija Y.K., Bhardwaj A., Das S. A portrayal of E3 ubiquitin ligases and deubiquitylases in cancer. Int J Cancer 2013, 133:2759-2768.
5. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002, 82:373-428.
6. Ciechanover A. Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ 2005, 12:1178-1190.
7. Catic A., Ploegh H.L. Ubiquitin-conserved protein or selfish gene?. Trends Biochem Sci 2005, 30:600-604.
8. Kundrat L., Regan L. Identification of residues on Hsp70 and Hsp90 ubiquitinated by the cochaperone CHIP. J Mol Biol 2010, 395:587-594.
9. Hofmann R.M., Pickart C.M. In vitro assembly and recognition of Lys-63 polyubiquitin chains. J Biol Chem 2001, 276:27936-27943.
10. Kravtsova-Ivantsiv Y., Ciechanover A. Non-canonical ubiquitin-based signals for proteasomal degradation. J Cell Sci 2012, 125:539-548.
11. Toledo F., Wahl G.M. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 2006, 6:909-923.
12. Ringshausen I., O'Shea C.C., Finch A.J., Swigart L.B., Evan G.I. Mdm2 is critically and continuously required to suppress lethal p53 activity in vivo. Cancer Cell 2006, 10:501-514.
13. Maki C.G., Huibregtse J.M., Howley P.M. In vivo ubiquitination and proteasome-mediated degradation of p53(1). Cancer Res 1996, 56:2649-2654.
14. Maki C.G., Howley P.M. Ubiquitination of p53 and p21 is differentially affected by ionizing and UV radiation. Mol Cell Biol 1997, 17:355-363.
15. Li M., Brooks C.L., Wu-Baer F., Chen D., Baer R., Gu W. Mono-versus polyubiquitination: differential control of p53 fate by Mdm2. Science 2003, 302:1972-1975.
16. Lee J.T., Gu W. The multiple levels of regulation by p53 ubiquitination. Cell Death Differ 2010, 17:86-92.
17. Levine A.J., Oren M. The first 30years of p53: growing ever more complex. Nat Rev Cancer 2009, 9:749-758.
18. Momand J., Zambetti G.P., Olson D.C., George D., Levine A.J. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992, 69:1237-1245.
19. Kussie P.H., Gorina S., Marechal V., et al. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 1996, 274:948-953.
20. Haupt Y., Maya R., Kazaz A., Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997, 387:296-299.
21. Kubbutat M.H., Jones S.N., Vousden K.H. Regulation of p53 stability by Mdm2. Nature 1997, 387:299-303.
22. Honda R., Tanaka H., Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 1997, 420:25-27.
23. Fang S., Jensen J.P., Ludwig R.L., Vousden K.H., Weissman A.M. Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J Biol Chem 2000, 275:8945-8951.
24. Montes de Oca Luna R., Wagner D.S., Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 1995, 378:203-206.
25. Jain A.K., Barton M.C. Making sense of ubiquitin ligases that regulate p53. Cancer Biol Ther 2010, 10:665-672.
26. Wang X. p53 regulation: teamwork between RING domains of Mdm2 and MdmX. Cell Cycle 2011, 10:4225-4229.
27. Wang X., Jiang X. Mdm2 and MdmX partner to regulate p53. FEBS Lett 2012, 586:1390-1396.
28. Marine J.C., Jochemsen A.G. Mdmx as an essential regulator of p53 activity. Biochem Biophys Res Commun 2005, 331:750-760.
29. Marine J.C., 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, 13:927-934.
30. Wahl G.M. Mouse bites dogma: how mouse models are changing our views of how P53 is regulated in vivo. Cell Death Differ 2006, 13:973-983.
31. Iwakuma T., Lozano G. Crippling p53 activities via knock-in mutations in mouse models. Oncogene 2007, 26:2177-2184.
32. Barboza J.A., Iwakuma T., Terzian T., El-Naggar A.K., Lozano G. Mdm2 and Mdm4 loss regulates distinct p53 activities. Mol Cancer Res 2008, 6:947-954.
33. Minsky N., Oren M. The RING domain of Mdm2 mediates histone ubiquitylation and transcriptional repression. Mol Cell 2004, 16:631-639.
34. Ohkubo S., Tanaka T., Taya Y., Kitazato K., Prives C. Excess HDM2 impacts cell cycle and apoptosis and has a selective effect on p53-dependent transcription. J Biol Chem 2006, 281:16943-16950.
35. Tang Y., Zhao W., Chen Y., Zhao Y., Gu W. Acetylation is indispensable for p53 activation. Cell 2008, 133:612-626.
36. Francoz S., Froment P., Bogaerts S., et al. Mdm4 and Mdm2 cooperate to inhibit p53 activity in proliferating and quiescent cells in vivo. Proc Natl Acad Sci U S A 2006, 103:3232-3237.
37. Xiong S., Van Pelt C.S., Elizondo-Fraire A.C., Liu G., Lozano G. Synergistic roles of Mdm2 and Mdm4 for p53 inhibition in central nervous system development. Proc Natl Acad Sci U S A 2006, 103:3226-3231.
38. Rodriguez M.S., Desterro J.M., Lain S., Lane D.P., Hay R.T. Multiple C-terminal lysine residues target p53 for ubiquitin-proteasome-mediated degradation. Mol Cell Biol 2000, 20:8458-8467.
39. Lohrum M.A., Woods D.B., Ludwig R.L., Balint E., Vousden K.H. C-terminal ubiquitination of p53 contributes to nuclear export. Mol Cell Biol 2001, 21:8521-8532.
40. 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, 25:5389-5395.
41. Krummel K.A., Lee C.J., Toledo F., Wahl G.M. 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 U S A 2005, 102:10188-10193.
42. Chan W.M., Mak M.C., Fung T.K., Lau A., Siu W.Y., Poon R.Y. Ubiquitination of p53 at multiple sites in the DNA-binding domain. Mol Cancer Res 2006, 4:15-25.
43. Wade M., Wang Y.V., Wahl G.M. The p53 orchestra: Mdm2 and Mdmx set the tone. Trends Cell Biol 2010, 20:299-309.
44. Itahana K., Mao H., Jin A., et al. Targeted inactivation of Mdm2 RING finger E3 ubiquitin ligase activity in the mouse reveals mechanistic insights into p53 regulation. Cancer Cell 2007, 12:355-366.
45. Clegg H.V., Itahana K., Zhang Y. Unlocking the Mdm2-p53 loop: ubiquitin is the key. Cell Cycle 2008, 7:287-292.
46. Marchenko N.D., Moll U.M. The role of ubiquitination in the direct mitochondrial death program of p53. Cell Cycle 2007, 6:1718-1723.
47. Marchenko N.D., Wolff S., Erster S., Becker K., Moll U.M. Monoubiquitylation promotes mitochondrial p53 translocation. EMBO J 2007, 26:923-934.
48. Chipuk J.E., Kuwana T., Bouchier-Hayes L., et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004, 303:1010-1014.
49. Leng R.P., Lin Y., Ma W., et al. Pirh2, a p53-induced ubiquitin-protein ligase, promotes p53 degradation. Cell 2003, 112:779-791.
50. Lee J., Zhou P. Cullins and cancer. Genes Cancer 2010, 1:690-699.
51. Sun L., Shi L., Li W., et al. JFK, a Kelch domain-containing F-box protein, links the SCF complex to p53 regulation. Proc Natl Acad Sci U S A 2009, 106:10195-10200.
52. Verma S., Ali A., Arora S., Banerjea A.C. Inhibition of beta-TrcP-dependent ubiquitination of p53 by HIV-1 Vpu promotes p53-mediated apoptosis in human T cells. Blood 2011, 117:6600-6607.
53. Nag A., Bagchi S., Raychaudhuri P. Cul4A physically associates with MDM2 and participates in the proteolysis of p53. Cancer Res 2004, 64:8152-8155.
54. Banks D., Wu M., Higa L.A., et al. L2DTL/CDT2 and PCNA interact with p53 and regulate p53 polyubiquitination and protein stability through MDM2 and CUL4A/DDB1 complexes. Cell Cycle 2006, 5:1719-1729.
55. Aggarwal P., Lessie M.D., Lin D.I., et al. Nuclear accumulation of cyclin D1 during S phase inhibits Cul4-dependent Cdt1 proteolysis and triggers p53-dependent DNA rereplication. Genes Dev 2007, 21:2908-2922.
56. Kopanja D., Stoyanova T., Okur M.N., Huang E., Bagchi S., Raychaudhuri P. Proliferation defects and genome instability in cells lacking Cul4A. Oncogene 2009, 28:2456-2465.
57. Querido E., Blanchette P., Yan Q., 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.
58. Andrews P., He Y.J., Xiong Y. Cytoplasmic localized ubiquitin ligase cullin 7 binds to p53 and promotes cell growth by antagonizing p53 function. Oncogene 2006, 25:4534-4548.
59. Cang Y., Zhang J., Nicholas S.A., et al. Deletion of DDB1 in mouse brain and lens leads to p53-dependent elimination of proliferating cells. Cell 2006, 127:929-940.
60. Hu R., Aplin A.E. Skp2 regulates G2/M progression in a p53-dependent manner. Mol Biol Cell 2008, 19:4602-4610.
61. Higa L.A., Banks D., Wu M., Kobayashi R., Sun H., Zhang H. L2DTL/CDT2 interacts with the CUL4/DDB1 complex and PCNA and regulates CDT1 proteolysis in response to DNA damage. Cell Cycle 2006, 5:1675-1680.
62. Jackson S., Xiong Y. CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem Sci 2009, 34:562-570.
63. Yamasaki S., Yagishita N., Sasaki T., et al. Cytoplasmic destruction of p53 by the endoplasmic reticulum-resident ubiquitin ligase 'Synoviolin'. EMBO J 2007, 26:113-122.
64. Wu Z.Z., Sun N.K., Chien K.Y., Chao C.C. Silencing of the SNARE protein NAPA sensitizes cancer cells to cisplatin by inducing ERK1/2 signaling, synoviolin ubiquitination and p53 accumulation. Biochem Pharmacol 2011, 82:1630-1640.
65. Dornan D., Wertz I., Shimizu H., et al. The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature 2004, 429:86-92.
66. Yang W., Rozan L.M., McDonald E.R., et al. CARPs are ubiquitin ligases that promote MDM2-independent p53 and phospho-p53ser20 degradation. J Biol Chem 2007, 282:3273-3281.
67. Lee E.W., Lee M.S., Camus S., et al. Differential regulation of p53 and p21 by MKRN1 E3 ligase controls cell cycle arrest and apoptosis. EMBO J 2009, 28:2100-2113.
68. 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.
69. Zhong Q., Gao W., Du F., Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 2005, 121:1085-1095.
70. Zhang X., Berger F.G., Yang J., Lu X. USP4 inhibits p53 through deubiquitinating and stabilizing ARF-BP1. EMBO J 2011, 30:2177-2189.
71. Kon N., Zhong J., Qiang L., Accili D., Gu W. Inactivation of arf-bp1 induces p53 activation and diabetic phenotypes in mice. J Biol Chem 2012, 287:5102-5111.
72. Verdecia M.A., Joazeiro C.A., Wells N.J., et al. Conformational flexibility underlies ubiquitin ligation mediated by the WWP1 HECT domain E3 ligase. Mol Cell 2003, 11:249-259.
73. Huibregtse J.M., Scheffner M., Beaudenon S., Howley P.M. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc Natl Acad Sci U S A 1995, 92:2563-2567.
74. Bernassola F., Karin M., Ciechanover A., Melino G. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 2008, 14:10-21.
75. Cheng Q., Cao X., Yuan F., Li G., Tong T. Knockdown of WWP1 inhibits growth and induces apoptosis in hepatoma carcinoma cells through the activation of caspase3 and p53. Biochem Biophys Res Commun 2014, 448:248-254.
76. Hatakeyama S., Nakayama K.I. U-box proteins as a new family of ubiquitin ligases. Biochem Biophys Res Commun 2003, 302:635-645.
77. 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.
78. Muller P., Hrstka R., Coomber D., Lane D.P., Vojtesek B. Chaperone-dependent stabilization and degradation of p53 mutants. Oncogene 2008, 27:3371-3383.
79. Wu H., Pomeroy S.L., Ferreira M., et al. UBE4B promotes Hdm2-mediated degradation of the tumor suppressor p53. Nat Med 2011, 17:347-355.
80. Shi D., Pop M.S., Kulikov R., Love I.M., Kung A.L., Grossman S.R. CBP and p300 are cytoplasmic E4 polyubiquitin ligases for p53. Proc Natl Acad Sci U S A 2009, 106:16275-16280.
81. Grossman S.R., Deato M.E., Brignone C., et al. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science 2003, 300:342-344.
82. Lai Z., Ferry K.V., Diamond M.A., et al. Human mdm2 mediates multiple mono-ubiquitination of p53 by a mechanism requiring enzyme isomerization. J Biol Chem 2001, 276:31357-31367.
83. D'Andrea A., Pellman D. Deubiquitinating enzymes: a new class of biological regulators. Crit Rev Biochem Mol Biol 1998, 33:337-352.
84. Wilkinson K.D. Signal transduction: aspirin, ubiquitin and cancer. Nature 2003, 424:738-739.
85. Hu M., Li P., Li M., et al. Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 2002, 111:1041-1054.
86. Li M., Chen D., Shiloh A., et al. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 2002, 416:648-653.
87. Lim S.K., Shin J.M., Kim Y.S., Baek K.H. Identification and characterization of murine mHAUSP encoding a deubiquitinating enzyme that regulates the status of p53 ubiquitination. Int J Oncol 2004, 24:357-364.
88. Li M., Brooks C.L., Kon N., Gu W. A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol Cell 2004, 13:879-886.
89. Kon N., Kobayashi Y., Li M., Brooks C.L., Ludwig T., Gu W. Inactivation of HAUSP in vivo modulates p53 function. Oncogene 2010, 29:1270-1279.
90. Cummins J.M., Rago C., Kohli M., Kinzler K.W., Lengauer C., Vogelstein B. Tumour suppression: disruption of HAUSP gene stabilizes p53 2004, 428. [1 pp. following 486].
91. Kon N., Zhong J., Kobayashi Y., et al. Roles of HAUSP-mediated p53 regulation in central nervous system development. Cell Death Differ 2011, 18:1366-1375.
92. Meulmeester E., Pereg Y., Shiloh Y., Jochemsen A.G. ATM-mediated phosphorylations inhibit Mdmx/Mdm2 stabilization by HAUSP in favor of p53 activation. Cell Cycle 2005, 4:1166-1170.
93. Vucic D., Dixit V.M., Wertz I.E. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 2011, 12:439-452.
94. Jochemsen A.G., Shiloh Y. USP10: friend and foe. Cell 2010, 140:308-310.
95. Yuan J., Luo K., Zhang L., Cheville J.C., Lou Z. USP10 regulates p53 localization and stability by deubiquitinating p53. Cell 2010, 140:384-396.
96. Rabut G., Peter M. Function and regulation of protein neddylation. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep 2008, 9:969-976.
97. Xirodimas D.P., Saville M.K., Bourdon J.C., Hay R.T., Lane D.P. Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell 2004, 118:83-97.
98. Abida W.M., Nikolaev A., Zhao W., Zhang W., Gu W. FBXO11 promotes the neddylation of p53 and inhibits its transcriptional activity. J Biol Chem 2007, 282:1797-1804.
99. Liu G., Xirodimas D.P. NUB1 promotes cytoplasmic localization of p53 through cooperation of the NEDD8 and ubiquitin pathways. Oncogene 2010, 29:2252-2261.
100. Varadaraj A., Mattoscio D., Chiocca S. SUMO Ubc9 enzyme as a viral target. IUBMB Life 2014, 66:27-33.
101. Stehmeier P., Muller S. Regulation of p53 family members by the ubiquitin-like SUMO system. DNA Repair (Amst) 2009, 8:491-498.
102. Schmidt D., Muller S. PIAS/SUMO: new partners in transcriptional regulation. Cell Mol Life Sci 2003, 60:2561-2574.
103. Bischof O., Schwamborn K., Martin N., et al. The E3 SUMO ligase PIASy is a regulator of cellular senescence and apoptosis. Mol Cell 2006, 22:783-794.
104. Carter S., Bischof O., Dejean A., Vousden K.H. C-terminal modifications regulate MDM2 dissociation and nuclear export of p53. Nat Cell Biol 2007, 9:428-435.
105. Carter S., Vousden K.H. p53-Ubl fusions as models of ubiquitination, sumoylation and neddylation of p53. Cell Cycle 2008, 7:2519-2528.
106. Devine T., Dai M.S. Targeting the ubiquitin-mediated proteasome degradation of p53 for cancer therapy. Curr Pharm Des 2013, 19:3248-3262.
107. Hicke L., Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 2003, 19:141-172.
108. Christophorou M.A., Ringshausen I., Finch A.J., Swigart L.B., Evan G.I. The pathological response to DNA damage does not contribute to p53-mediated tumour suppression. Nature 2006, 443:214-217.
109. Jegga A.G., Inga A., Menendez D., Aronow B.J., Resnick M.A. Functional evolution of the p53 regulatory network through its target response elements. Proc Natl Acad Sci U S A 2008, 105:944-949.
110. Wu Z.Z., Sun N.K., Chao C.C. Knockdown of CITED2 using short-hairpin RNA sensitizes cancer cells to cisplatin through stabilization of p53 and enhancement of p53-dependent apoptosis. J Cell Physiol 2011, 226:2415-2428.
111. Kuo T.C., Chang P.Y., Huang S.F., Chou C.K., Chao C.C. Knockdown of HURP inhibits the proliferation of hepacellular carcinoma cells via downregulation of gankyrin and accumulation of p53. Biochem Pharmacol 2012, 83:758-768.
112. Sun N.K., Huang S.L., Chien K.Y., Chao C.C. Golgi-SNARE GS28 potentiates cisplatin-induced apoptosis by forming GS28-MDM2-p53 complexes and by preventing the ubiquitination and degradation of p53. Biochem J 2012, 444:303-314.