E3 ubiquitin ligase TRIM32 negatively regulates tumor suppressor p53 to promote tumorigenesis

Cell Death and Differentiation

Volumn 21, Issue 11, 2014, Pages 1792-1804

  Liu, Ju ^a   Zhang, C ^a   Wang, X L ^a,b   Ly, P ^a   Belyi, V ^a   Xu Monette, Z Y ^c   Young, K H ^c   Hu, W ^a   Feng, Z ^a  

^a RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^b SHANDONG UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; DOXORUBICIN; DOXYCYCLINE; E3 UBIQUITIN LIGASE TRIM32; ETOPOSIDE; FLUOROURACIL; MESSENGER RNA; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; PROTEIN P73; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; TRANSCRIPTION FACTOR; TRIM32 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ALGORITHM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BINDING AFFINITY; CARCINOGENESIS; CELL AGING; CELL TRANSFORMATION; CELLULAR STRESS RESPONSE; COLONY FORMATION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; G1 PHASE CELL CYCLE CHECKPOINT; GENE IDENTIFICATION; HUMAN; HUMAN CELL; INTRON; MALE; MALIGNANT TRANSFORMATION; MCF 7 CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; UPREGULATION; ANIMAL; GENETICS; METABOLISM; TUMOR CELL LINE;

MUS;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DNA DAMAGE; HUMANS; MICE; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84961324372     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.121     Document Type: Article

References (54)

1. Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell 2009; 137: 413-431.
2. Levine AJ, Oren M. The first 30 years of p53: growing ever more complex. Nat Rev Cancer 2009; 9: 749-758.
3. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408: 307-310.
4. Feng Z, Levine AJ. The regulation of energy metabolism and the IGF-1/mTOR pathways by the p53 protein. Trends Cell Biol 2010; 20: 427-434.
5. Brooks CL, Gu W. p53 ubiquitination: Mdm2 and beyond. Mol Cell 2006; 21: 307-315.
6. Harris SL, Levine AJ. The p53 pathway: positive and negative feedback loops. Oncogene 2005; 24: 2899-2908.
7. 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: 1237-1245.
8. Oliner JD, Kinzler KW, Meltzer PS, George DL, Vogelstein B. Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 1992; 358: 80-83.
9. 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: 779-791.
10. 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.
11. Meroni G. Genomics and evolution of the TRIM gene family. Adv Exp Med Biol 2012; 770: 1-9.
12. Cambiaghi V, Giuliani V, Lombardi S, Marinelli C, Toffalorio F, Pelicci PG. TRIM proteins in cancer. Adv Exp Med Biol 2012; 770: 77-91.
13. Nicklas S, Otto A, Wu X, Miller P, Stelzer S, Wen Y et al. TRIM32 regulates skeletal muscle stem cell differentiation and is necessary for normal adult muscle regeneration. PloS One 2012; 7: e30445.
14. Schwamborn JC, Berezikov E, Knoblich JA. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 2009; 136: 913-925.
15. Horn EJ, Albor A, Liu Y, El-Hizawi S, Vanderbeek GE, Babcock M et al. RING protein Trim32 associated with skin carcinogenesis has anti-apoptotic and E3-ubiquitin ligase properties. Carcinogenesis 2004; 25: 157-167.
16. Kano S, Miyajima N, Fukuda S, Hatakeyama S. Tripartite motif protein 32 facilitates cell growth and migration via degradation of Abl-interactor 2. Cancer Res 2008; 68: 5572-5580.
17. Locke M, Tinsley CL, Benson MA, Blake DJ. TRIM32 is an E3 ubiquitin ligase for dysbindin. Hum Mol Genet 2009; 18: 2344-2358.
18. Albor A, El-Hizawi S, Horn EJ, Laederich M, Frosk P, Wrogemann K et al. The interaction of Piasy with Trim32, an E3-ubiquitin ligase mutated in limb-girdle muscular dystrophy type 2H, promotes Piasy degradation and regulates UVB-induced keratinocyte apoptosis through NFkappaB. J Biol Chem 2006; 281: 25850-25866.
19. el-Deiry WS, Kern SE, Pietenpol JA, Kinzler KW, Vogelstein B. Definition of a consensus binding site for p53. Nat Genet 1992; 1: 45-49.
20. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008; 9: 402-412.
21. Hoh J, Jin S, Parrado T, Edington J, Levine AJ, Ott J. The p53MH algorithm and its application in detecting p53-responsive genes. Proc Natl Acad Sci USA 2002; 99: 8467-8472.
22. Hu W, Feng Z, Teresky AK, Levine AJ. p53 regulates maternal reproduction through LIF. Nature 2007; 450: 721-724.
23. Hu W, Zhang C, Wu R, Sun Y, Levine A, Feng Z. Glutaminase 2, a novel p53 target gene regulating energy metabolism and antioxidant function. Proc Natl Acad Sci USA 2010; 107: 7455-7460.
24. Zhang C, Lin M, Wu R, Wang X, Yang B, Levine AJ et al. Parkin, a p53 target gene, mediates the role of p53 in glucose metabolism and the Warburg effect. Proc Natl Acad Sci USA 2011; 108: 16259-16264.
25. Albertoni M, Shaw PH, Nozaki M, Godard S, Tenan M, Hamou MF et al. Anoxia induces macrophage inhibitory cytokine-1 (MIC-1) in glioblastoma cells independently of p53 and HIF-1. Oncogene 2002; 21: 4212-4219.
26. Khwaja FW, Svoboda P, Reed M, Pohl J, Pyrzynska B, Van Meir EG. Proteomic identification of the wt-p53-regulated tumor cell secretome. Oncogene 2006; 25: 7650-7661.
27. Kim E, Gunther W, Yoshizato K, Meissner H, Zapf S, Nusing RM et al. Tumor suppressor p53 inhibits transcriptional activation of invasion gene thromboxane synthase mediated by the proto-oncogenic factor ets-1. Oncogene 2003; 22: 7716-7727.
28. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 1998; 282: 1497-1501.
29. Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, Gavrilova O et al. p53 regulates mitochondrial respiration. Science 2006; 312: 1650-1653.
30. Jung YS, Qian Y, Yan W, Chen X. Pirh2 E3 ubiquitin ligase modulates keratinocyte differentiation through p63. J Invest Dermatol 2013; 133: 1178-1187.
31. Urist M, Tanaka T, Poyurovsky MV, Prives C. p73 induction after DNA damage is regulated by checkpoint kinases Chk1 and Chk2. Genes Dev 2004; 18: 3041-3054.
32. Vilgelm AE, Washington MK, Wei J, Chen H, Prassolov VS, Zaika AI. Interactions of the p53 protein family in cellular stress response in gastrointestinal tumors. Mol Cancer Ther 2010; 9: 693-705.
33. Weisz L, Oren M, Rotter V. Transcription regulation by mutant p53. Oncogene 2007; 26: 2202-2211.
34. Zhang J, Hu MM, Wang YY, Shu HB. TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination. J Biol Chem 2012; 287: 28646-28655.
35. Hock A, Vousden KH. Regulation of the p53 pathway by ubiquitin and related proteins. Int J Biochem Cell Biol 2010; 42: 1618-1621.
36. Lukashchuk N, Vousden KH. Ubiquitination and degradation of mutant p53. Mol Cell Biol 2007; 27: 8284-8295.
37. Zheng T, Wang J, Zhao Y, Zhang C, Lin M, Wang X et al. Spliced MDM2 isoforms promote mutant p53 accumulation and gain-of-function in tumorigenesis. Nat Commun 2013; 4: 2996.
38. Hwang PM, Bunz F, Yu J, Rago C, Chan TA, Murphy MP et al. Ferredoxin reductase affects p53-dependent, 5-fluorouracil-induced apoptosis in colorectal cancer cells. Nat Med 2001; 7: 1111-1117.
39. Amundson SA, Myers TG, Fornace Jr AJ. Roles for p53 in growth arrest and apoptosis: putting on the brakes after genotoxic stress. Oncogene 1998; 17: 3287-3299.
40. Elmore LW, Rehder CW, Di X, McChesney PA, Jackson-Cook CK, Gewirtz DA et al. Adriamycin-induced senescence in breast tumor cells involves functional p53 and telomere dysfunction. J Biol Chem 2002; 277: 35509-35515.
41. Gonzalez-Cano L, Hillje AL, Fuertes-Alvarez S, Marques MM, Blanch A, Ian RW et al. Regulatory feedback loop between TP73 and TRIM32. Cell Death Dis 2013; 4: e704.
42. Lowe SW, Jacks T, Housman DE, Ruley HE. Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells. Proc Natl Acad Sci USA 1994; 91: 2026-2030.
43. Buzzai M, Jones RG, Amaravadi RK, Lum JJ, DeBerardinis RJ, Zhao F et al. Systemic treatment with the antidiabetic drug metformin selectively impairs p53-deficient tumor cell growth. Cancer Res 2007; 67: 6745-6752.
44. Yoon CH, Lee ES, Lim DS, Bae YS. PKR, a p53 target gene, plays a crucial role in the tumor-suppressor function of p53. Proc Natl Acad Sci USA 2009; 106: 7852-7857.
45. 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 2010; 38: 689-699.
46. Montes deOca Luna R, Wagner DS, Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 1995; 378: 203-206.
47. 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.
48. Wade M, Li YC, Wahl GM. MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat Rev Cancer 2013; 13: 83-96.
49. Levine AJ, Hu W, Feng Z. The P53 pathway: what questions remain to be explored? Cell Death Differ 2006; 13: 1027-1036.
50. Chen J. The Roles of MDM2 and MDMX phosphorylation in stress signaling to p53. Genes Cancer 2012; 3: 274-282.
51. Zhang C, Liu J, Liang Y, Wu R, Zhao Y, Hong X et al. Tumour-associated mutant p53 drives the Warburg effect. Nature Commun 2013; 4: 2935.
52. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT et al. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 1999; 398: 714-718.
53. Yang A, Walker N, Bronson R, Kaghad M, Oosterwegel M, Bonnin J et al. p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature 2000; 404: 99-103.
54. Sun XX, Challagundla KB, Dai MS. Positive regulation of p53 stability and activity by the deubiquitinating enzyme Otubain 1. EMBO J 2012; 31(3): 576-592.