Pirh2 RING-finger E3 ubiquitin ligase: Its role in tumorigenesis and cancer therapy

FEBS Letters

Volumn 586, Issue 10, 2012, Pages 1397-1402

  Jung, Yong Sam ^a   Qian, Yingjuan ^a   Chen, Xinbin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer therapy; E3 ligase; Pirh2; Tumorigenesis

Indexed keywords

CELL PROTEIN; MEMBRANE PROTEIN; MYC PROTEIN; P53 INDUCED RING H2 PROTEIN; PROTEASOME; PROTEIN MDM2; PROTEIN P53; PROTEIN P73; PROTEIN POLH; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CANCER GROWTH; CANCER THERAPY; CARCINOGENESIS; CELL TRANSFORMATION; DNA DAMAGE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASMS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-MDM2; RING FINGER DOMAINS; SEQUENCE HOMOLOGY, AMINO ACID; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASES;

EID: 84861194412     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.03.052     Document Type: Review

References (75)

1. A.M. Weissman Themes and variations on ubiquitylation Nat. Rev. Mol. Cell Biol. 2 2001 169 178 (Pubitemid 33675741)
2. S. Lipkowitz, and A.M. Weissman RINGs of good and evil: RING finger ubiquitin ligases at the crossroads of tumour suppression and oncogenesis Nat. Rev. Cancer 11 2011 629 643
3. D. Dornan COP1, the negative regulator of p53, is overexpressed in breast and ovarian adenocarcinomas Cancer Res. 64 2004 7226 7230 (Pubitemid 39372056)
4. J.J. Manfredi The Mdm2-p53 relationship evolves: Mdm2 swings both ways as an oncogene and a tumor suppressor Genes Dev. 24 2010 1580 1589
5. S. Shangary Temporal activation of p53 by a specific MDM2 inhibitor is selectively toxic to tumors and leads to complete tumor growth inhibition Proc. Natl. Acad. Sci. USA 105 2008 3933 3938 (Pubitemid 351723502)
6. N. Issaeva, P. Bozko, M. Enge, M. Protopopova, L.G. Verhoef, M. Masucci, A. Pramanik, and G. Selivanova Small molecule RITA binds to p53, blocks p53-HDM-2 interaction and activates p53 function in tumors Nat. Med. 10 2004 1321 1328 (Pubitemid 40022713)
7. L.T. Vassilev In vivo activation of the p53 pathway by small-molecule antagonists of MDM2 Science 303 2004 844 848 (Pubitemid 38174664)
8. A. Hakem Role of Pirh2 in mediating the regulation of p53 and c-Myc PLoS Genet. 7 2011 e1002360
9. T. Hattori, T. Isobe, K. Abe, H. Kikuchi, K. Kitagawa, T. Oda, C. Uchida, and M. Kitagawa Pirh2 promotes ubiquitin-dependent degradation of the cyclin-dependent kinase inhibitor p27Kip1 Cancer Res. 67 2007 10789 10795 (Pubitemid 350145907)
10. Y.S. Jung, A. Hakem, R. Hakem, and X. Chen Pirh2 E3 ubiquitin ligase monoubiquitinates DNA polymerase eta to suppress translesion DNA synthesis Mol. Cell. Biol. 31 2011 3997 4006
11. Y.S. Jung, G. Liu, and X. Chen Pirh2 E3 ubiquitin ligase targets DNA polymerase eta for 20S proteasomal degradation Mol. Cell. Biol. 30 2010 1041 1048
12. Y.S. Jung, Y. Qian, and X. Chen The p73 tumor suppressor is targeted by Pirh2 RING finger E3 ubiquitin ligase for the proteasome-dependent degradation J. Biol. Chem. 286 2011 35388 35395
13. R.P. Leng Pirh2, a p53-induced ubiquitin-protein ligase, promotes p53 degradation Cell 112 2003 779 791 (Pubitemid 36378882)
14. J. Zhu, J. Jiang, W. Zhou, and X. Chen The potential tumor suppressor p73 differentially regulates cellular p53 target genes Cancer Res. 58 1998 5061 5065 (Pubitemid 28521161)
15. K. Harms, S. Nozell, and X. Chen The common and distinct target genes of the p53 family transcription factors Cell. Mol. Life Sci. 61 2004 822 842 (Pubitemid 38651002)
16. M. Dohn, S. Zhang, and X. Chen P63alpha and DeltaNp63alpha can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes Oncogene 20 2001 3193 3205 (Pubitemid 32553672)
17. C.A. Corcoran, J. Montalbano, H. Sun, Q. He, Y. Huang, and M.S. Sheikh Identification and characterization of two novel isoforms of Pirh2 ubiquitin ligase that negatively regulate p53 independent of RING finger domains J. Biol. Chem. 284 2009 21955 21970
18. G. Wu, M. Sun, L. Zhang, J. Zhou, Y. Wang, and K. Huo A novel hPirh2 splicing variant without ubiquitin protein ligase activity interacts with p53 and is down-regulated in hepatocellular carcinoma FEBS Lett. 584 2010 2772 2778
19. J. Shi, Y. Huang, and M.S. Sheikh Identification of Pirh2D, an additional novel isoform of Pirh2 ubiquitin ligase Mol. Cell. Pharmacol. 2 2010 21 23
20. Y. Sheng Molecular basis of Pirh2-mediated p53 ubiquitylation Nat. Struct. Mol. Biol. 15 2008 1334 1342
21. L.K. Beitel, Y.A. Elhaji, R. Lumbroso, S.S. Wing, V. Panet-Raymond, B. Gottlieb, L. Pinsky, and M.A. Trifiro Cloning and characterization of an androgen receptor N-terminal-interacting protein with ubiquitin-protein ligase activity J. Mol. Endocrinol. 29 2002 41 60 (Pubitemid 34965745)
22. I.R. Logan, L. Gaughan, S.R. McCracken, V. Sapountzi, H.Y. Leung, and C.N. Robson Human PIRH2 enhances androgen receptor signaling through inhibition of histone deacetylase 1 and is overexpressed in prostate cancer Mol. Cell. Biol. 26 2006 6502 6510 (Pubitemid 44277889)
23. S. Maruyama, N. Miyajima, M. Bohgaki, T. Tsukiyama, M. Shigemura, K. Nonomura, and S. Hatakeyama Ubiquitylation of epsilon-COP by PIRH2 and regulation of the secretion of PSA Mol. Cell. Biochem. 307 2008 73 82 (Pubitemid 350238649)
24. I.R. Logan, V. Sapountzi, L. Gaughan, D.E. Neal, and C.N. Robson Control of human PIRH2 protein stability: involvement of TIP60 and the proteosome J. Biol. Chem. 279 2004 11696 11704 (Pubitemid 38401673)
25. G. Zheng, J. Ning, and Y.C. Yang PLAGL2 controls the stability of Pirh2, an E3 ubiquitin ligase for p53 Biochem. Biophys. Res. Commun. 364 2007 344 350 (Pubitemid 47633421)
26. L. Zhang, J. Li, C. Wang, Y. Ma, and K. Huo A new human gene hNTKL-BP1 interacts with hPirh2 Biochem. Biophys. Res. Commun. 330 2005 293 297 (Pubitemid 40394965)
27. J. Yan, D. Zhang, Y. Di, H. Shi, H. Rao, and K. Huo A newly identified Pirh2 substrate SCYL1-BP1 can bind to MDM2 and accelerate MDM2 self-ubiquitination FEBS Lett. 584 2010 3275 3278
28. L. Wang, G. He, P. Zhang, X. Wang, M. Jiang, and L. Yu Interplay between MDM2, MDMX, Pirh2 and COP1: the negative regulators of p53 Mol. Biol. Rep. 2010
29. Y.S. Jung, Y. Qian, and X. Chen Examination of the expanding pathways for the regulation of p21 expression and activity Cell. Signal. 22 2010 1003 1012
30. A.C. Joerger, S. Rajagopalan, E. Natan, D.B. Veprintsev, C.V. Robinson, and A.R. Fersht Structural evolution of p53, p63, and p73: implication for heterotetramer formation Proc. Natl. Acad. Sci. USA 106 2009 17705 17710
31. D. Coutandin Conformational stability and activity of p73 require a second helix in the tetramerization domain Cell Death Differ. 16 2009 1582 1589
32. E. Natan, and A.C. Joerger Structure and kinetic stability of the p63 tetramerization domain J. Mol. Biol. 415 2012 503 513
33. J. Momand, G.P. Zambetti, D.C. Olson, D. George, and A.J. Levine The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation Cell 69 1992 1237 1245
34. J.D. Oliner, J.A. Pietenpol, S. Thiagalingam, J. Gyuris, K.W. Kinzler, and B. Vogelstein Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53 Nature 362 1993 857 860 (Pubitemid 23132165)
35. J.T. Lee, and W. Gu The multiple levels of regulation by p53 ubiquitination Cell Death Differ. 17 2010 86 92
36. Y. Haupt, R. Maya, A. Kazaz, and M. Oren Mdm2 promotes the rapid degradation of p53 Nature 387 1997 296 299 (Pubitemid 27220766)
37. M.H. Kubbutat, S.N. Jones, and K.H. Vousden Regulation of p53 stability by Mdm2 Nature 387 1997 299 303 (Pubitemid 27220767)
38. D. Michael, and M. Oren The p53 and Mdm2 families in cancer Curr. Opin. Genet. Dev. 12 2002 53 59 (Pubitemid 34094990)
39. Y. Barak, T. Juven, R. Haffner, and M. Oren Mdm2 expression is induced by wild type p53 activity EMBO J. 12 1993 461 468 (Pubitemid 23073692)
40. X. Wu, J.H. Bayle, D. Olson, and A.J. Levine The p53-mdm-2 autoregulatory feedback loop Genes Dev. 7 1993 1126 1132 (Pubitemid 23207405)
41. M. Li, C.L. Brooks, F. Wu-Baer, D. Chen, R. Baer, and W. Gu Mono- versus polyubiquitination: differential control of p53 fate by Mdm2 Science 302 2003 1972 1975 (Pubitemid 37523506)
42. R. Maya ATM-dependent phosphorylation of Mdm2 on serine 395: role in p53 activation by DNA damage Genes Dev. 15 2001 1067 1077 (Pubitemid 32417300)
43. C. Prives, and P.A. Hall The p53 pathway J. Pathol. 187 1999 112 126 (Pubitemid 29009841)
44. S.Y. Shieh, M. Ikeda, Y. Taya, and C. Prives DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2 Cell 91 1997 325 334 (Pubitemid 27467963)
45. Q. Li Axin determines cell fate by controlling the p53 activation threshold after DNA damage Nat. Cell Biol. 11 2009 1128 1134
46. D. Dornan The ubiquitin ligase COP1 is a critical negative regulator of p53 Nature 429 2004 86 92 (Pubitemid 38620556)
47. W.M. Ongkeko, X.Q. Wang, W.Y. Siu, A.W. Lau, K. Yamashita, A.L. Harris, L.S. Cox, and R.Y. Poon MDM2 and MDMX bind and stabilize the p53-related protein p73 Curr. Biol. 9 1999 829 832 (Pubitemid 29375186)
48. X. Zeng MDM2 suppresses p73 function without promoting p73 degradation Mol. Cell. Biol. 19 1999 3257 3266 (Pubitemid 29193787)
49. I.R. Watson, and M.S. Irwin Ubiquitin and ubiquitin-like modifications of the p53 family Neoplasia 8 2006 655 666 (Pubitemid 44379792)
50. W. Duan, L. Gao, L.J. Druhan, W.G. Zhu, C. Morrison, G.A. Otterson, and M.A. Villalona-Calero Expression of Pirh2, a newly identified ubiquitin protein ligase, in lung cancer J. Natl. Cancer Inst. 96 2004 1718 1721 (Pubitemid 39585640)
51. X.M. Wang, L.Y. Yang, L. Guo, C. Fan, and F. Wu P53-induced RING-H2 protein, a novel marker for poor survival in hepatocellular carcinoma after hepatic resection Cancer 115 2009 4554 4563
52. M. Shimada High expression of Pirh2, an E3 ligase for p27, is associated with low expression of p27 and poor prognosis in head and neck cancers Cancer Sci. 100 2009 866 872
53. K. Chin Genomic and transcriptional aberrations linked to breast cancer pathophysiologies Cancer Cell 10 2006 529 541 (Pubitemid 44854748)
54. A.H. Bild Oncogenic pathway signatures in human cancers as a guide to targeted therapies Nature 439 2006 353 357 (Pubitemid 43128862)
55. A. Berchuck Patterns of gene expression that characterize long-term survival in advanced stage serous ovarian cancers Clin. Cancer Res. 11 2005 3686 3696 (Pubitemid 40685585)
56. M. Raponi Gene expression signatures for predicting prognosis of squamous cell and adenocarcinomas of the lung Cancer Res. 66 2006 7466 7472 (Pubitemid 44289200)
57. C. Cao, E.T. Shinohara, T.K. Subhawong, L. Geng, K. Woon Kim, J.M. Albert, D.E. Hallahan, and B. Lu Radiosensitization of lung cancer by nutlin, an inhibitor of murine double minute 2 Mol. Cancer Ther. 5 2006 411 417
58. M. Wade, E.T. Wong, M. Tang, J.M. Stommel, and G.M. Wahl Hdmx modulates the outcome of p53 activation in human tumor cells J. Biol. Chem. 281 2006 33036 33044 (Pubitemid 46036686)
59. B. Hu, D.M. Gilkes, B. Farooqi, S.M. Sebti, and J. Chen MDMX overexpression prevents p53 activation by the MDM2 inhibitor nutlin J. Biol. Chem. 281 2006 33030 33035 (Pubitemid 46036685)
60. J.T. Patton, L.D. Mayo, A.D. Singhi, A.V. Gudkov, G.R. Stark, and M.W. Jackson Levels of HdmX expression dictate the sensitivity of normal and transformed cells to Nutlin-3 Cancer Res. 66 2006 3169 3176
61. E.R. Flores Tumor predisposition in mice mutant for p63 and p73: evidence for broader tumor suppressor functions for the p53 family Cancer Cell 7 2005 363 373 (Pubitemid 40544653)
62. R. Tomasini TAp73 knockout shows genomic instability with infertility and tumor suppressor functions Genes Dev. 22 2008 2677 2691
63. H. Wu, R.A. Zeinab, E.R. Flores, and R.P. Leng Pirh2, a ubiquitin E3 ligase, inhibits p73 transcriptional activity by promoting its ubiquitination Mol. Cancer Res. 9 2011 1780 1790
64. A. Alt, K. Lammens, C. Chiocchini, A. Lammens, J.C. Pieck, D. Kuch, K.P. Hopfner, and T. Carell Bypass of DNA lesions generated during anticancer treatment with cisplatin by DNA polymerase eta Science 318 2007 967 970 (Pubitemid 350098991)
65. J.E. Cleaver Cancer in xeroderma pigmentosum and related disorders of DNA repair Nat. Rev. Cancer 5 2005 564 573 (Pubitemid 40942832)
66. C.H. Wu, J. van Riggelen, A. Yetil, A.C. Fan, P. Bachireddy, and D.W. Felsher Cellular senescence is an important mechanism of tumor regression upon c-Myc inactivation Proc. Natl. Acad. Sci. USA 104 2007 13028 13033 (Pubitemid 351737587)
67. L.J. Crawford, B. Walker, and A.E. Irvine Proteasome inhibitors in cancer therapy J. Cell Commun. Signal. 5 2011 101 110
68. G. Wu, M. Sun, W. Zhang, and K. Huo AIG1 is a novel Pirh2-interacting protein that activates the NFAT signaling pathway Front. Biosci. (Elite Ed) 3 2011 834 842
69. W. Zhang, G. Wu, X. Yan, H. Shi, and K. Huo Preliminary study on the interaction between human PIRH2b and ARF4 J. Med. Mol. Biol. 4 2007 469 474
70. S. Duan, Z. Yao, D. Hou, Z. Wu, W.G. Zhu, and M. Wu Phosphorylation of Pirh2 by calmodulin-dependent kinase II impairs its ability to ubiquitinate p53 EMBO J. 26 2007 3062 3074 (Pubitemid 47057489)
71. S. Duan, Z. Yao, Y. Zhu, G. Wang, D. Hou, L. Wen, and M. Wu The Pirh2-keratin 8/18 interaction modulates the cellular distribution of mitochondria and UV-induced apoptosis Cell Death Differ. 16 2009 826 837
72. M. Chen, J.C. Cortay, I.R. Logan, V. Sapountzi, C.N. Robson, and D. Gerlier Inhibition of ubiquitination and stabilization of human ubiquitin E3 ligase PIRH2 by measles virus phosphoprotein J. Virol. 79 2005 11824 11836 (Pubitemid 41279300)
73. A.K. Karuppannan, S. Liu, Q. Jia, M. Selvaraj, and J. Kwang Porcine circovirus type 2 ORF3 protein competes with p53 in binding to Pirh2 and mediates the deregulation of p53 homeostasis Virology 398 2010 1 11
74. J. Liu The ORF3 protein of porcine circovirus type 2 interacts with porcine ubiquitin E3 ligase Pirh2 and facilitates p53 expression in viral infection J. Virol. 81 2007 9560 9567 (Pubitemid 47311501)
75. K. Abe, T. Hattori, T. Isobe, K. Kitagawa, T. Oda, C. Uchida, and M. Kitagawa Pirh2 interacts with and ubiquitylates signal recognition particle receptor beta subunit Biomed. Res. 29 2008 53 60 (Pubitemid 351425822)