Animal cells and systems

The Korean Society for Integrative Biology (한국통합생물학회)
권호 표지
DOI QR코드

DOI QR Code

Ubiquitin E3 ligases controlling p53 stability

  • Lee, Seong-Won (School of Biological Sciences, Seoul National University) ;
  • Seong, Min-Woo (School of Biological Sciences, Seoul National University) ;
  • Jeon, Young-Joo (School of Biological Sciences, Seoul National University) ;
  • Chung, Chin-Ha (School of Biological Sciences, Seoul National University)
  • Received : 2012.03.13
  • Accepted : 2012.04.23
  • Published : 2012.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

The p53 protein plays a pivotal role in tumor suppression. The cellular level of p53 is normally kept low by proteasome-mediated degradation, allowing cell cycle progression and cell proliferation. Under stress conditions, such as DNA damage, p53 is stabilized and activated through various post-translational modifications of itself as well as of its regulatory proteins for induction of the downstream genes responsible for cell cycle arrest, DNA repair, and apoptosis. Therefore, the level of p53 should be tightly regulated for normal cell growth and for prevention of the accumulation of mutations in DNA under stress conditions, which otherwise would lead to tumorigenesis. Since the discovery of Mdm2, a critical ubiquitin E3 ligase that destabilizes p53 in mammalian cells, nearly 20 different E3 ligases have been identified and shown to function in the control of stability, nuclear export, translocation to chromatin or nuclear foci, and oligomerization of p53. So far, a large number of excellent reviews have been published on the control of p53 function in various aspects. Therefore, this review will focus only on mammalian ubiquitin E3 ligases that mediate proteasome-dependent degradation of p53.

Keywords

References

  1. Adhikary S, Marinoni F, Hock A, Hulleman E, Popov N, Beier R, Bernard S, Quarto M, Capra M, Goettig S, et al. 2005. The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell. 123:409-421. https://doi.org/10.1016/j.cell.2005.08.016
  2. Amano T, Yamasaki S, Yagishita N, Tsuchimochi K, Shin H, Kawahara K, Aratani S, Fujita H, Zhang L, Ikeda R, et al. 2003. Synoviolin/Hrd1, an E3 ubiquitin ligase, as a novel pathogenic factor for arthropathy. Genes Dev. 17:2436-2449. https://doi.org/10.1101/gad.1096603
  3. Anderson CW, Appella E. 2010. Signaling to the p53 tumor suppressor through pathways activated by genotoxic and non-genotoxic stresses. In Ralph AB, Edward AD, editors. Handbook of cell signaling. 2nd ed. San Die-go(CA): Academic Press. p. chapter 264, 2185-2204. Available from: http://www.sciencedirect.com/science/article/pii/B9780123741455002643
  4. Ashcroft M, Taya Y, Vousden KH. 2000. Stress signals utilize multiple pathways to stabilize p53. Mol Cell Biol. 20:3224-3233. https://doi.org/10.1128/MCB.20.9.3224-3233.2000
  5. Baert JL, Monte D, Verreman K, Degerny C, Coutte L, de Launoit Y. 2010. The E3 ubiquitin ligase complex component COP1 regulates PEA3 group member stability and transcriptional activity. Oncogene. 29:1810-1820. https://doi.org/10.1038/onc.2009.471
  6. Barboza JA, Iwakuma T, Terzian T, El-Naggar AK, Lozano G. 2008. Mdm2 and Mdm4 loss regulates distinct p53 activities. Mol Cancer Res. 6:947-954. https://doi.org/10.1158/1541-7786.MCR-07-2079
  7. Bargonetti J, Manfredi JJ, Chen X, Marshak DR, Prives C. 1993. A proteolytic fragment from the central region of p53 has marked sequence-specific DNA-binding activity when generated from wild-type but not from oncogenic mutant p53 protein. Genes Dev. 7:2565-2574. https://doi.org/10.1101/gad.7.12b.2565
  8. Beitel LK, Elhaji YA, Lumbroso R, Wing SS, Panet- Raymond V, Gottlieb B, Pinsky L, Trifiro MA. 2002. Cloning and characterization of an androgen receptor Nterminal- interacting protein with ubiquitin-protein ligase activity. J Mol Endocrinol. 29:41-60. https://doi.org/10.1677/jme.0.0290041
  9. Bianchi E, Denti S, Catena R, Rossetti G, Polo S, Gasparian S, Putignano S, Rogge L, Pardi R. 2003. Characterization of human constitutive photomorphogenesis protein 1, a RING finger ubiquitin ligase that interacts with Jun transcription factors and modulates their transcriptional activity. J Biol Chem. 278:19682-19690. https://doi.org/10.1074/jbc.M212681200
  10. Blagosklonny MV, Toretsky J, Neckers L. 1995. Geldanamycin selectively destabilizes and conformationally alters mutated p53. Oncogene 11:933-939.
  11. Brooks CL, Gu W. 2011. p53 regulation by ubiquitin. FEBS Lett. 585:2803-2809. https://doi.org/10.1016/j.febslet.2011.05.022
  12. Bueso-Ramos CE, Yang Y, deLeon E, McCown P, Stass SA, Albitar M. 1993. The human MDM-2 oncogene is overexpressed in leukemias. Blood. 82:2617-2623.
  13. Chavez-Reyes A, Parant JM, Amelse LL, de Oca Luna RM, Korsmeyer SJ, Lozano G. 2003. Switching mechanisms of cell death in mdm2- and mdm4-null mice by deletion of p53 downstream targets. Cancer Res. 63:8664-8669.
  14. Chen D, Kon N, Li M, Zhang W, Qin J, Gu W. 2005. ARFBP1/ Mule is a critical mediator of the ARF tumor suppressor. Cell. 121:1071-1083. https://doi.org/10.1016/j.cell.2005.03.037
  15. Chen D, Brooks CL, Gu W. 2006. ARF-BP1 as a potential therapeutic target. Br J Cancer. 94:1555-1558. https://doi.org/10.1038/sj.bjc.6603119
  16. Chu D, Kakazu N, Gorrin-Rivas MJ, Lu HP, Kawata M, Abe T, Ueda K, Adachi Y. 2001. Cloning and characterization of LUN, a novel ring finger protein that is highly expressed in lung and specifically binds to a palindromic sequence. J Biol Chem. 276:14004-14013. https://doi.org/10.1074/jbc.M010262200
  17. Connell P, Ballinger CA, Jiang J, Wu Y, Thompson LJ, Hohfeld J, Patterson C. 2001. The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol. 3:93-96. https://doi.org/10.1038/35050618
  18. Coumailleau F, Das V, Alcover A, Raposo G, Vandormael- Pournin S, Le Bras S, Baldacci P, Dautry-Varsat A, Babinet C, Cohen-Tannoudji M. 2004. Over-expression of Rififylin, a new RING finger and FYVE-like domain-containing protein, inhibits recycling from the endocytic recycling compartment. Mol Biol Cell. 15: 4444-4456. https://doi.org/10.1091/mbc.E04-04-0274
  19. Davidoff AM, Iglehart JD, Marks JR. 1992. Immune response to p53 is dependent upon p53/HSP70 complexes in breast cancers. Proc Natl Acad Sci USA. 89: 3439-3442. https://doi.org/10.1073/pnas.89.8.3439
  20. Demand J, Alberti S, Patterson C, Hohfeld J. 2001. Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling. Curr Biol. 11:1569-1577. https://doi.org/10.1016/S0960-9822(01)00487-0
  21. Deng XW, Caspar T, Quail PH. 1991. cop1: a regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev. 5:1172-1182. https://doi.org/10.1101/gad.5.7.1172
  22. Dornan D, Bheddah S, Newton K, Ince W, Frantz GD, Dowd P, Koeppen H, Dixit VM, French DM. 2004a. COP1, the negative regulator of p53, is overexpressed in breast and ovarian adenocarcinomas. Cancer Res. 64:7226-7230. https://doi.org/10.1158/0008-5472.CAN-04-2601
  23. Dornan D, Wertz I, Shimizu H, Arnott D, Frantz GD, Dowd P, O'Rourke K, Koeppen H, Dixit VM. 2004b. The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature. 429:86-92. https://doi.org/10.1038/nature02514
  24. Dornan D, Shimizu H, Mah A, Dudhela T, Eby M, O'Rourke K, Seshagiri S, Dixit VM. 2006. ATM engages autodegradation of the E3 ubiquitin ligase COP1 after DNA damage. Science. 313:1122-1126. https://doi.org/10.1126/science.1127335
  25. Duan W, Gao L, Wu X, Zhang Y, Otterson GA, Villalona- Calero MA. 2006. Differential response between the p53 ubiquitin-protein ligases Pirh2 and MdM2 following DNA damage in human cancer cells. Exp Cell Res. 312:3370-3378. https://doi.org/10.1016/j.yexcr.2006.07.005
  26. Duan S, Yao Z, Hou D, Wu Z, Zhu WG, Wu M. 2007. Phosphorylation of Pirh2 by calmodulin-dependent kinase II impairs its ability to ubiquitinate p53. EMBO J. 26:3062-3074. https://doi.org/10.1038/sj.emboj.7601749
  27. Esser C, Scheffner M, Hohfeld J. 2005. The chaperoneassociated ubiquitin ligase CHIP is able to target p53 for proteasomal degradation. J Biol Chem. 280: 27443-27448. https://doi.org/10.1074/jbc.M501574200
  28. Fang S, Jensen JP, Ludwig RL, Vousden KH, Weissman AM. 2000. Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J Biol Chem. 275:8945-8951. https://doi.org/10.1074/jbc.275.12.8945
  29. Feng Z, Hu W, de Stanchina E, Teresky AK, Jin S, Lowe S, Levine AJ. 2007. The regulation of AMPK beta1, TSC2, and PTEN expression by p53: stress, cell and tissue specificity, and the role of these gene products in modulating the IGF-1-AKT-mTOR pathways. Cancer Res. 67:3043-3053. https://doi.org/10.1158/0008-5472.CAN-06-4149
  30. Finch RA, Donoviel DB, Potter D, Shi M, Fan A, Freed DD, Wang CY, Zambrowicz BP, Ramirez-Solis R, Sands AT, et al. 2002. mdmx is a negative regulator of p53 activity in vivo. Cancer Res. 62:3221-3225.
  31. Froyen G, Corbett M, Vandewalle J, Jarvela I, Lawrence O, Meldrum C, Bauters M, Govaerts K, Vandeleur L, Van Esch H, et al. 2008. Submicroscopic duplications of the hydroxysteroid dehydrogenase HSD17B10 and the E3 ubiquitin ligase HUWE1 are associated with mental retardation. Am J Hum Genet. 82:432-443. https://doi.org/10.1016/j.ajhg.2007.11.002
  32. Gannon JV, Greaves R, Iggo R, Lane DP. 1990. Activating mutations in p53 produce a common conformational effect. A monoclonal antibody specific for the mutant form. EMBO J. 9:1595-1602.
  33. Girnita L, Girnita A, Larsson O. 2003. Mdm2-dependent ubiquitination and degradation of the insulin-like growth factor 1 receptor. Proc Natl Acad Sci USA. 100: 8247-8252. https://doi.org/10.1073/pnas.1431613100
  34. Grossman SR, Deato ME, Brignone C, Chan HM, Kung AL, Tagami H, Nakatani Y, Livingston DM. 2003. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science. 300:342-344. https://doi.org/10.1126/science.1080386
  35. Hall JR, Kow E, Nevis KR, Lu CK, Luce KS, Zhong Q, Cook JG. 2007. Cdc6 stability is regulated by the Huwe1 ubiquitin ligase after DNA damage. Mol Biol Cell. 18:3340-3350. https://doi.org/10.1091/mbc.E07-02-0173
  36. Haluska P, Jr., Saleem A, Rasheed Z, Ahmed F, Su EW, Liu LF, Rubin EH. 1999. Interaction between human topoisomerase I and a novel RING finger/arginine-serine protein. Nucleic Acids Res. 27:2538-2544. https://doi.org/10.1093/nar/27.12.2538
  37. Hattori T, Isobe T, Abe K, Kikuchi H, Kitagawa K, Oda T, Uchida C, Kitagawa M. 2007. Pirh2 promotes ubiquitindependent degradation of the cyclin-dependent kinase inhibitor p27Kip1. Cancer Res. 67:10789-10795. https://doi.org/10.1158/0008-5472.CAN-07-2033
  38. Haupt Y, Maya R, Kazaz A, Oren M. 1997. Mdm2 promotes the rapid degradation of p53. Nature. 387:296-299. https://doi.org/10.1038/387296a0
  39. Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu Rev Biochem. 67:425-479. https://doi.org/10.1146/annurev.biochem.67.1.425
  40. Hinds PW, Finlay CA, Quartin RS, Baker SJ, Fearon ER, Vogelstein B, Levine AJ. 1990. Mutant p53 DNA clones from human colon carcinomas cooperate with ras in transforming primary rat cells: a comparison of the ''hot spot'' mutant phenotypes. Cell Growth Differ. 1:571-580.
  41. Hirao A, Kong YY, Matsuoka S, Wakeham A, Ruland J, Yoshida H, Liu D, Elledge SJ, Mak TW. 2000. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science. 287:1824-1827. https://doi.org/10.1126/science.287.5459.1824
  42. Honda R, Tanaka H, Yasuda H. 1997. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420:25-27. https://doi.org/10.1016/S0014-5793(97)01480-4
  43. Jain AK, Barton MC. 2010. Making sense of ubiquitin ligases that regulate p53. Cancer Biol Ther. 10:665-672. https://doi.org/10.4161/cbt.10.7.13445
  44. Jones SN, Roe AE, Donehower LA, Bradley A. 1995. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature. 378:206-208. https://doi.org/10.1038/378206a0
  45. Jung YS, Liu G, Chen X. 2010. Pirh2 E3 ubiquitin ligase targets DNA polymerase eta for 20S proteasomal degradation. Mol Cell Biol. 30:1041-1048. https://doi.org/10.1128/MCB.01198-09
  46. Jung YS, Qian Y, Chen X. 2011. The p73 tumor suppressor is targeted by Pirh2 RING finger E3 ubiquitin ligase for the proteasome-dependent degradation. J Biol Chem. 286:35388-35395. https://doi.org/10.1074/jbc.M111.261537
  47. Kaneko M, Ishiguro M, Niinuma Y, Uesugi M, Nomura Y. 2002. Human HRD1 protects against ER stress-induced apoptosis through ER-associated degradation. FEBS Lett. 532:147-152. https://doi.org/10.1016/S0014-5793(02)03660-8
  48. Kato S, Ding J, Pisck E, Jhala US, Du K. 2008. COP1 functions as a FoxO1 ubiquitin E3 ligase to regulate FoxO1-mediated gene expression. J Biol Chem. 283:35464-35473. https://doi.org/10.1074/jbc.M801011200
  49. Kim JH, Park SM, Kang MR, Oh SY, Lee TH, Muller MT, Chung IK. 2005. Ubiquitin ligase MKRN1 modulates telomere length homeostasis through a proteolysis of hTERT. Genes Dev. 19:776-781. https://doi.org/10.1101/gad.1289405
  50. Kruse JP, Gu W. 2009. MSL2 promotes Mdm2-independent cytoplasmic localization of p53. J Biol Chem. 284: 3250-3263. https://doi.org/10.1074/jbc.M805658200
  51. Kubbutat MH, Jones SN, Vousden KH. 1997. Regulation of p53 stability by Mdm2. Nature. 387:299-303. https://doi.org/10.1038/387299a0
  52. Kuo ML, Duncavage EJ, Mathew R, den Besten W, Pei D, Naeve D, Yamamoto T, Cheng C, Sherr CJ, Roussel MF. 2003. Arf induces p53-dependent and -independent antiproliferative genes. Cancer Res. 63:1046-1053.
  53. Laine A, Topisirovic I, Zhai D, Reed JC, Borden KL, Ronai Z. 2006. Regulation of p53 localization and activity by Ubc13. Mol Cell Biol. 26:8901-8913. https://doi.org/10.1128/MCB.01156-06
  54. Laine A, Ronai Z. 2007. Regulation of p53 localization and transcription by the HECT domain E3 ligase WWP1. Oncogene. 26:1477-1483. https://doi.org/10.1038/sj.onc.1209924
  55. Le Cam L, Linares LK, Paul C, Julien E, Lacroix M, Hatchi E, Triboulet R, Bossis G, Shmueli A, Rodriguez MS, et al. 2006. E4F1 is an atypical ubiquitin ligase that modulates p53 effector functions independently of degradation. Cell. 127:775-788. https://doi.org/10.1016/j.cell.2006.09.031
  56. Lee EW, Lee MS, Camus S, Ghim J, Yang MR, Oh W, Ha NC, Lane DP, Song J. 2009. Differential regulation of p53 and p21 by MKRN1 E3 ligase controls cell cycle arrest and apoptosis. EMBO J. 28:2100-2113. https://doi.org/10.1038/emboj.2009.164
  57. Leng RP, Lin Y, Ma W, Wu H, Lemmers B, Chung S, Parant JM, Lozano G, Hakem R, Benchimol S. 2003. Pirh2, a p53-induced ubiquitin-protein ligase, promotes p53 degradation. Cell. 112:779-791. https://doi.org/10.1016/S0092-8674(03)00193-4
  58. Li M, Brooks CL, Wu-Baer F, Chen D, Baer R, Gu W. 2003. Mono- versus polyubiquitination: differential control of p53 fate by Mdm2. Science. 302:1972-1975. https://doi.org/10.1126/science.1091362
  59. Li M, Brooks CL, Kon N, Gu W. 2004. A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol Cell. 13: 879-886. https://doi.org/10.1016/S1097-2765(04)00157-1
  60. Li DQ, Ohshiro K, Reddy SD, Pakala SB, Lee MH, Zhang Y, Rayala SK, Kumar R. 2009. E3 ubiquitin ligase COP1 regulates the stability and functions of MTA1. Proc Natl Acad Sci USA. 106:17493-17498. https://doi.org/10.1073/pnas.0908027106
  61. Lin HK, Wang L, Hu YC, Altuwaijri S, Chang C. 2002. Phosphorylation-dependent ubiquitylation and degradation of androgen receptor by Akt require Mdm2 E3 ligase. EMBO J. 21:4037-4048. https://doi.org/10.1093/emboj/cdf406
  62. Lin L, Ozaki T, Takada Y, Kageyama H, Nakamura Y, Hata A, Zhang JH, Simonds WF, Nakagawara A, Koseki H. 2005. Topors, a p53 and topoisomerase I-binding RING finger protein, is a coactivator of p53 in growth suppression induced by DNA damage. Oncogene. 24:3385-3396. https://doi.org/10.1038/sj.onc.1208554
  63. Liu Z, Oughtred R, Wing SS. 2005. Characterization of E3Histone, a novel testis ubiquitin protein ligase which ubiquitinates histones. Mol Cell Biol. 25:2819-2831. https://doi.org/10.1128/MCB.25.7.2819-2831.2005
  64. Logan IR, Gaughan L, McCracken SR, Sapountzi V, Leung HY, Robson CN. 2006. Human PIRH2 enhances androgen receptor signaling through inhibition of histone deacetylase 1 and is overexpressed in prostate cancer. Mol Cell Biol. 26:6502-6510. https://doi.org/10.1128/MCB.00147-06
  65. Maruyama S, Miyajima N, Bohgaki M, Tsukiyama T, Shigemura M, Nonomura K, Hatakeyama S. 2008. Ubiquitylation of epsilon-COP by PIRH2 and regulation of the secretion of PSA. Mol Cell Biochem. 307:73-82.
  66. McDonald ER, 3rd, El-Deiry WS. 2004. Suppression of caspase-8- and -10-associated RING proteins results in sensitization to death ligands and inhibition of tumor cell growth. Proc Natl Acad Sci USA. 101:6170-6175. https://doi.org/10.1073/pnas.0307459101
  67. Meacham GC, Patterson C, Zhang W, Younger JM, Cyr DM. 2001. The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat Cell Biol. 3:100-105. https://doi.org/10.1038/35050509
  68. Meek DW, Anderson CW. 2009. Posttranslational modification of p53: cooperative integrators of function. Cold Spring Harb Perspect Biol. 1:a000950.
  69. Meek DW, Knippschild U. 2003. Posttranslational modification of MDM2. Mol Cancer Res. 1:1017-1026.
  70. Michael D, Oren M. 2003. The p53-Mdm2 module and the ubiquitin system. Semin Cancer Biol. 13:49-58. https://doi.org/10.1016/S1044-579X(02)00099-8
  71. Migliorini D, Lazzerini Denchi E, Danovi D, Jochemsen A, Capillo M, Gobbi A, Helin K, Pelicci PG, Marine JC. 2002. Mdm4 (Mdmx) regulates p53-induced growth arrest and neuronal cell death during early embryonic mouse development. Mol Cell Biol. 22:5527-5538. https://doi.org/10.1128/MCB.22.15.5527-5538.2002
  72. Migliorini D, Bogaerts S, Defever D, Vyas R, Denecker G, Radaelli E, Zwolinska A, Depaepe V, Hochepied T, Skarnes WC, et al. 2011. Cop1 constitutively regulates c-Jun protein stability and functions as a tumor suppressor in mice. J Clin Invest. 121:1329-1343. https://doi.org/10.1172/JCI45784
  73. Min JN,Whaley RA, Sharpless NE, Lockyer P, Portbury AL, Patterson C. 2008. CHIP deficiency decreases longevity, with accelerated aging phenotypes accompanied by altered protein quality control. Mol Cell Biol. 28: 4018-4025. https://doi.org/10.1128/MCB.00296-08
  74. Nadav E, Shmueli A, Barr H, Gonen H, Ciechanover A, Reiss Y. 2003. A novel mammalian endoplasmic reticulum ubiquitin ligase homologous to the yeast Hrd1. Biochem Biophys Res Commun. 303:91-97. https://doi.org/10.1016/S0006-291X(03)00279-1
  75. Noy T, Suad O, Taglicht D, Ciechanover A. 2012. HUWE1 ubiquitinates MyoD and targets it for proteasomal degradation. Biochem Biophys Res Commun. 418: 408-413. https://doi.org/10.1016/j.bbrc.2012.01.045
  76. Oliner JD, Kinzler KW, Meltzer PS, George DL, Vogelstein B. 1992. Amplification of a gene encoding a p53- associated protein in human sarcomas. Nature. 358: 80-83. https://doi.org/10.1038/358080a0
  77. Oyanagi H, Takenaka K, Ishikawa S, Kawano Y, Adachi Y, Ueda K, Wada H, Tanaka F. 2004. Expression of LUN gene that encodes a novel RING finger protein is correlated with development and progression of nonsmall cell lung cancer. Lung Cancer 46:21-28. https://doi.org/10.1016/j.lungcan.2004.03.009
  78. Parant J, Chavez-Reyes A, Little NA, Yan W, Reinke V, Jochemsen AG, Lozano G. 2001. Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53. Nat Genet. 29:92-95. https://doi.org/10.1038/ng714
  79. Parsons JL, Tait PS, Finch D, Dianova II, Edelmann MJ, Khoronenkova SV, Kessler BM, Sharma RA, McKenna WG, Dianov GL. 2009. Ubiquitin ligase ARF-BP1/Mule modulates base excision repair. EMBO J. 28:3207-3215. https://doi.org/10.1038/emboj.2009.243
  80. Petrucelli L, Dickson D, Kehoe K, Taylor J, Snyder H, Grover A, De Lucia M, McGowan E, Lewis J, Prihar G, et al. 2004. CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum Mol Genet. 13: 703-714. https://doi.org/10.1093/hmg/ddh083
  81. Pickart CM. 2001. Mechanisms underlying ubiquitination. Annu Rev Biochem. 70:503-533. https://doi.org/10.1146/annurev.biochem.70.1.503
  82. Qi L, Heredia JE, Altarejos JY, Screaton R, Goebel N, Niessen S, Macleod IX, Liew CW, Kulkarni RN, Bain J, et al. 2006. TRB3 links the E3 ubiquitin ligase COP1 to lipid metabolism. Science. 312:1763-1766. https://doi.org/10.1126/science.1123374
  83. Rajendra R, Malegaonkar D, Pungaliya P, Marshall H, Rasheed Z, Brownell J, Liu LF, Lutzker S, Saleem A, Rubin EH. 2004. Topors functions as an E3 ubiquitin ligase with specific E2 enzymes and ubiquitinates p53. J Biol Chem. 279:36440-36444. https://doi.org/10.1074/jbc.C400300200
  84. Rasheed ZA, Saleem A, Ravee Y, Pandolfi PP, Rubin EH. 2002. The topoisomerase I-binding RING protein, topors, is associated with promyelocytic leukemia nuclear bodies. Exp Cell Res. 277:152-160. https://doi.org/10.1006/excr.2002.5550
  85. Renner F, Moreno R, Schmitz ML. 2010. SUMOylationdependent localization of IKKepsilon in PML nuclear bodies is essential for protection against DNA-damagetriggered cell death. Mol Cell. 37:503-515. https://doi.org/10.1016/j.molcel.2010.01.018
  86. Saleem A, Dutta J, Malegaonkar D, Rasheed F, Rasheed Z, Rajendra R, Marshall H, Luo M, Li H, Rubin EH. 2004. The topoisomerase I- and p53-binding protein topors is differentially expressed in normal and malignant human tissues and may function as a tumor suppressor. Oncogene. 23:5293-5300. https://doi.org/10.1038/sj.onc.1207700
  87. Sasaki S, Nakamura T, Arakawa H, Mori M, Watanabe T, Nagawa H, Croce CM. 2002. Isolation and characterization of a novel gene, hRFI, preferentially expressed in esophageal cancer. Oncogene. 21:5024-5030. https://doi.org/10.1038/sj.onc.1205627
  88. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505. https://doi.org/10.1016/0092-8674(93)90384-3
  89. Sdek P, Ying H, Chang DL, Qiu W, Zheng H, Touitou R, Allday MJ, Xiao ZX. 2005. MDM2 promotes proteasome- dependent ubiquitin-independent degradation of retinoblastoma protein. Mol Cell. 20:699-708. https://doi.org/10.1016/j.molcel.2005.10.017
  90. Sheng Y, Laister RC, Lemak A, Wu B, Tai E, Duan S, Lukin J, Sunnerhagen M, Srisailam S, Karra M, et al. 2008. Molecular basis of Pirh2-mediated p53 ubiquitylation. Nat Struct Mol Biol. 15:1334-1342. https://doi.org/10.1038/nsmb.1521
  91. Shenoy SK, McDonald PH, Kohout TA, Lefkowitz RJ. 2001. Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin. Science. 294:1307-1313. https://doi.org/10.1126/science.1063866
  92. Shi D, Pop MS, Kulikov R, Love IM, Kung AL, Grossman SR. 2009. CBP and p300 are cytoplasmic E4 polyubiquitin ligases for p53. Proc Natl Acad Sci USA. 106:16275- 16280. https://doi.org/10.1073/pnas.0904305106
  93. Shieh SY, Ikeda M, Taya Y, Prives C. 1997. DNA damageinduced phosphorylation of p53 alleviates inhibition by MDM2. Cell. 91:325-334. https://doi.org/10.1016/S0092-8674(00)80416-X
  94. Shieh SY, Taya Y, Prives C. 1999. DNA damage-inducible phosphorylation of p53 at N-terminal sites including a novel site, Ser20, requires tetramerization. EMBO J. 18:1815-1823. https://doi.org/10.1093/emboj/18.7.1815
  95. Shimura H, Schwartz D, Gygi SP, Kosik KS. 2004. CHIPHsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J Biol Chem. 279:4869-4876. https://doi.org/10.1074/jbc.M305838200
  96. Shvarts A, Steegenga WT, Riteco N, van Laar T, Dekker P, Bazuine M, van Ham RC, van der Houven van Oordt W, Hateboer G, van der Eb AJ, et al. 1996. MDMX: a novel p53-binding protein with some functional properties of MDM2. EMBO J. 15:5349-5357.
  97. Simelyte E, Rosengren S, Boyle DL, Corr M, Green DR, Firestein GS. 2005. Regulation of arthritis by p53: critical role of adaptive immunity. Arthriris Rheum. 52: 1876-1884. https://doi.org/10.1002/art.21099
  98. Stad R, Little NA, Xirodimas DP, Frenk R, van der Eb AJ, Lane DP, Saville MK, Jochemsen AG. 2001. Mdmx stabilizes p53 and Mdm2 via two distinct mechanisms. EMBO Rep. 2:1029-1034. https://doi.org/10.1093/embo-reports/kve227
  99. Sun L, Shi L, Li W, Yu W, Liang J, Zhang H, Yang X, Wang Y, Li R, Yao X, et al. 2009. JFK, a Kelch domaincontaining F-box protein, links the SCF complex to p53 regulation. Proc Natl Acad Sci USA. 106:10195-10200. https://doi.org/10.1073/pnas.0901864106
  100. Taira N, Yamamoto H, Yamaguchi T, Miki Y, Yoshida K. 2010. ATM augments nuclear stabilization of DYRK2 by inhibiting MDM2 in the apoptotic response to DNA damage. J Biol Chem. 285:4909-4919. https://doi.org/10.1074/jbc.M109.042341
  101. Tibbetts RS, Brumbaugh KM, Williams JM, Sarkaria JN, Cliby WA, Shieh SY, Taya Y, Prives C, Abraham RT. 1999. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13:152-157. https://doi.org/10.1101/gad.13.2.152
  102. Tombes RM, Mikkelsen RB, Jarvis WD, Grant S. 1999. Downregulation of delta CaM kinase II in human tumor cells. Biochim Biophys Acta. 1452:1-11. https://doi.org/10.1016/S0167-4889(99)00113-5
  103. Vitari AC, Leong KG, Newton K, Yee C, O'Rourke K, Liu J, Phu L, Vij R, Ferrando R, Couto SS, et al. 2011. COP1 is a tumour suppressor that causes degradation of ETS transcription factors. Nature. 474:403-406. https://doi.org/10.1038/nature10005
  104. Wang Z, Yang B, Dong L, Peng B, He X, Liu W. 2011. A novel oncoprotein Pirh2: rising from the shadow of MDM2. Cancer Sci. 102:909-917. https://doi.org/10.1111/j.1349-7006.2011.01899.x
  105. Weber JD, Jeffers JR, Rehg JE, Randle DH, Lozano G, Roussel MF, Sherr CJ, Zambetti GP. 2000. p53-independent functions of the p19(ARF) tumor suppressor. Genes Dev. 14:2358-2365. https://doi.org/10.1101/gad.827300
  106. Weger S, Hammer E, Heilbronn R. 2005. Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo. FEBS Lett. 579:5007-5012. https://doi.org/10.1016/j.febslet.2005.07.088
  107. Wei W, Kaelin WG, Jr. 2011. Good COP1 or bad COP1? In vivo veritas. J Clin Invest. 121:1263-1265. https://doi.org/10.1172/JCI57080
  108. Wertz IE, O'Rourke KM, Zhang Z, Dornan D, Arnott D, Deshaies RJ, Dixit VM. 2004. Human De-etiolated-1 regulates c-Jun by assembling a CUL4A ubiquitin ligase. Science. 303:1371-1374. https://doi.org/10.1126/science.1093549
  109. Whitesell L, Sutphin PD, Pulcini EJ, Martinez JD, Cook PH. 1998. The physical association of multiple molecular chaperone proteins with mutant p53 is altered by geldanamycin, an hsp90-binding agent. Mol Cell Biol. 18:1517-1524. https://doi.org/10.1128/MCB.18.3.1517
  110. Wu H, Zeinab RA, Flores ER, Leng RP. 2011. Pirh2, a ubiquitin E3 ligase, inhibits p73 transcriptional activity by promoting its ubiquitination. Mol Cancer Res. 9:1780-1790. https://doi.org/10.1158/1541-7786.MCR-11-0157
  111. Xu W, Marcu M, Yuan X, Mimnaugh E, Patterson C, Neckers L. 2002. Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu. Proc Natl Acad Sci USA. 99:12847-12852. https://doi.org/10.1073/pnas.202365899
  112. Yamasaki S, Yagishita N, Sasaki T, Nakazawa M, Kato Y, Yamadera T, Bae E, Toriyama S, Ikeda R, Zhang L, et al. 2007. Cytoplasmic destruction of p53 by the endoplasmic reticulum-resident ubiquitin ligase 'Synoviolin'. EMBO J. 26:113-122. https://doi.org/10.1038/sj.emboj.7601490
  113. Yang W, Rozan LM, McDonald ER, 3rd, Navaraj A, Liu JJ, Matthew EM, Wang W, Dicker DT, El-Deiry WS. 2007. CARPs are ubiquitin ligases that promote MDM2- independent p53 and phospho-p53ser20 degradation. J Biol Chem. 282:3273-3281. https://doi.org/10.1074/jbc.M610793200
  114. Yi C, Wang H, Wei N, Deng XW. 2002. An initial biochemical and cell biological characterization of the mammalian homologue of a central plant developmental switch, COP1. BMC Cell Biol. 3:30. https://doi.org/10.1186/1471-2121-3-30
  115. Yoon SY, Lee Y, Kim JH, Chung AS, Joo JH, Kim CN, Kim NS, Choe IS, Kim JW. 2005. Over-expression of human UREB1 in colorectal cancer: HECT domain of human UREB1 inhibits the activity of tumor suppressor p53 protein. Biochem Biophys Res Commun. 326:7-17.
  116. Zhang Y, Xiong Y, Yarbrough WG. 1998. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell. 92:725-734. https://doi.org/10.1016/S0092-8674(00)81401-4
  117. Zhang Z, Wang H, Li M, Agrawal S, Chen X, Zhang R. 2004. MDM2 is a negative regulator of p21WAF1/CIP1, independent of p53. J Biol Chem. 279:16000-16006. https://doi.org/10.1074/jbc.M312264200
  118. Zhong Q, Gao W, Du F, Wang X. 2005. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell. 121:1085-1095. https://doi.org/10.1016/j.cell.2005.06.009

Cited by

  1. Trb3 Regulates LR Axis formation in zebrafish embryos vol.36, pp.6, 2012, https://doi.org/10.1007/s10059-013-0237-0
  2. Ubiquitin proteasome system networks in the neurological disorders vol.17, pp.6, 2012, https://doi.org/10.1080/19768354.2013.855256
  3. p53 Acetylation: Regulation and Consequences vol.7, pp.1, 2015, https://doi.org/10.3390/cancers7010030
  4. The Ubiquitin Proteasome System in Genome Stability and Cancer vol.13, pp.9, 2012, https://doi.org/10.3390/cancers13092235