ABRO1 suppresses tumourigenesis and regulates the DNA damage response by stabilizing p53

Nature Communications

Volumn 5, Issue , 2014, Pages

  Zhang, Jianhong ^a   Cao, Mengmeng ^b   Dong, Jiahong ^c   Li, Changyan ^a   Xu, Wangxiang ^a   Zhan, Yiqun ^a   Wang, Xiaohui ^a   Yu, Miao ^a   Ge, Changhui ^a   Ge, Zhiqiang ^b   Yang, Xiaoming ^a,b  

^a BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^b TIANJIN UNIVERSITY   (China)

^c CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ABRAXAS BROTHER 1 PROTEIN; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CAMPTOTHECIN; DOXORUBICIN; ETOPOSIDE; LEPTOMYCIN B; PROTEIN; PROTEIN MDM2; PROTEIN P53; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; USP7 PROTEIN; DEUBIQUITINASE; FAM175B PROTEIN, HUMAN; MESSENGER RNA; NUCLEAR MATRIX PROTEIN; TP53 PROTEIN, HUMAN; UBIQUITIN; UBIQUITIN THIOLESTERASE; USP7 PROTEIN, HUMAN;

DNA; GENE EXPRESSION; GERM CELL; TUMOR;

A549 CELL LINE; AMINO TERMINAL SEQUENCE; ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CARCINOMA; CANCER CELL LINE; CANCER INHIBITION; CANCER SURVIVAL; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CELL PROLIFERATION; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; CLONOGENESIS; DNA DAMAGE; DOWN REGULATION; EXPRESSION VECTOR; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; GENE OVEREXPRESSION; GENE SILENCING; HISTOPATHOLOGY; HT 29 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; IONIZING RADIATION; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; LUNG CANCER CELL LINE; MAJOR CLINICAL STUDY; MCF 7 CELL LINE; MOUSE; NEUROBLASTOMA CELL LINE; NONHUMAN; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RNA INTERFERENCE; THYROID TUMOR; UBIQUITINATION; UPREGULATION; CARCINOGENESIS; CELL NUCLEUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; NEOPLASM; TUMOR CELL LINE;

APOPTOSIS; CARCINOGENESIS; CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; DNA DAMAGE; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; NUCLEAR MATRIX-ASSOCIATED PROTEINS; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN; UBIQUITIN THIOLESTERASE; UBIQUITIN-SPECIFIC PROTEASES;

EID: 84923287176     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6059     Document Type: Article

References (65)

1. Lane, D. P. Cancer. p53, guardian of the genome. Nature 35, 15-16 (1992).
2. Kruse, J. P. & Gu, W. Models of p53 regulation. Cell 137, 609-622 (2009).
3. Vousden, K. H. & Prives, C. Blinded by the light: the growing complexity of p53. Cell 137, 413-431 (2009).
4. Geyer, R. K., Yu, Z. K. & Maki, C. G. The MDM2 RING-finger domain is required to promote p53 nuclear export. Nat. Cell Biol. 2, 569-5739 (2000).
5. 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. 275, 8945-8951 (2000).
6. Brooks, C. L. & Gu, W. p53 ubiquitination: MDM2 and beyond. Mol. Cell 21, 307-315 (2006).
7. Marine, J. C. & Lozano, G. MDM2-mediated ubiquitylation: p53 and beyong. Cell Death Differ. 17, 93-1029 (2010).
8. Haupt, Y., Maya, R., Kazaz, A. & Oren, M. MDM2 promotes the rapid degradation of p53. Nature 387, 296-299 (1997).
9. Honda, R., Tanaka, H. & Yasuda, H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420, 25-27 (1997).
10. Appella, E. & Anderson, C. W. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268, 2764-2772 (2001).
11. Ashcroft, M., Kubbutat, M. H. & Vousden, K. H. Regulation of p53 function and stability by phosphorylation. Mol. Cell Biol. 19, 1751-1758 (1999).
12. Brooks, C. L. & Gu, W. Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation. Curr. Opin. Cell Biol. 15, 164-171 (2003).
13. Boyd, S. D., Tsai, K. Y. & Jacks, T. An intact HDM2 RING-finger domain is required for nuclear exclusion of p53. Nat. Cell Biol. 2, 563-568 (2000).
14. Freedman, D. A. & Levine, A. J. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell Biol. 18, 7288-7293 (1998).
15. Ventii, K. H. & Wilkinson, K. D. Protein partners of deubiquitinating enzymes. Biochem. J. 414, 161-175 (2008).
16. Nijman, S. M. et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786 (2005).
17. Allende-Vega, N., Sparks, A., Lane, D. P. & Saville, M. K. MdmX is a substrate for the deubiquitinating enzyme USP2a. Oncogene 29, 432-441 (2010).
18. Yuan, J., Luo, K., Zhang, L., Cheville, J. C. & Lou, Z. USP10 regulates p53 localization and stability by deubiquitinating p53. Cell 140, 384-396 (2010).
19. Li, M. et al. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416, 648-6539 (2002).
20. Li, M., Brooks, C. L., Kon, N. & Gu, W. A dynamic role of HAUSP in the p53-MDM2 pathway. Mol. Cell. 13, 879-886 (2004).
21. Brooks, C. L., Li, M., Hu, M., Shi, Y. & Gu, W. The p53-MDM2-HAUSP complex is involved in p53 stabilization by HAUSP. Oncogene 26, 7262-7266 (2007).
22. Hu, M. et al. Structural basis of competitive recognition of p53 and MDM2 by HAUSP/USP7: implications for the regulation of the p53-MDM2 pathway. PLoS Biol. 4, e27 (2006).
23. 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 4, 1166-1170 (2005).
24. Dayal, S. et al. Suppression of the deubiquitinating enzyme USP5 causes the accumulation of unanchored polyubiquitin and the activation of p53. J. Biol. Chem. 284, 5030-5041 (2009).
25. Nicholson, B. & Suresh Kumar, K. G. The multifaceted roles of USP7: new therapeutic opportunities. Cell. Biochem. Biophys. 60, 61-68 (2011).
26. Epping, M. T. et al. TSPYL5 suppresses p53 levels and function by physical interaction with USP7. Nat. Cell Biol. 13, 102-108 (2011).
27. Priolo, C. et al. The isopeptidase USP2a protects human prostate cancer from apoptosis. Cancer Res. 66, 8625-8632 (2006).
28. Graner, E. et al. The isopeptidase USP2a regulates the stability of fatty acid synthase in prostate cancer. Cancer Cell 5, 253-261 (2004).
29. Zhi, Y. et al. STAT3 repressed USP7 expression is crucial for colon cancer development. FEBS Lett. 586, 3013-3017 (2012).
30. Tang, J. et al. Critical role for Daxx in regulating MDM2. Nat. Cell Biol. 8, 855-862 (2006).
31. Ronai, Z. Balancing MDM2 - a Daxx-HAUSP matter. Nat. Cell Biol. 8, 790-791 (2006).
32. Song, M. S., Song, S. J., Kim, S. Y., Oh, H. J. & Lim, D. S. The tumour suppressor RASSF1A promotes MDM2 self-ubiquitination by disrupting the MDM2-DAXX-HAUSP complex. EMBO J. 27, 1863-1874 (2008).
33. Saridakis, V. et al. Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein-Barr nuclear antigen 1 implications for EBV-mediated immortalization. Mol. Cell 18, 25-36 (2005).
34. Kim, H. et al. DNA damage-induced RORa is crucial for p53 stabilization and increased apoptosis. Mol. Cell 44, 797-810 (2011).
35. Wang, Y., Solt, L. A., Kojetin, D. J. & Burris, T. P. Regulation of p53 stability and apoptosis by a ROR agonist. PLoS One 7, e34921 (2012).
36. Xiong, G., Wang, C., Evers, B. M., Zhou, B. P. & Xu, R. RORa suppresses breast tumor invasion by inducing SEMA3F expression. Cancer Res. 72, 1728-1739 (2012).
37. Michaelson, J. S. & Leder, P. RNAi reveals anti-apoptotic and transcriptionally repressive activities of DAXX. J. Cell Sci. 116, 345-352 (2003).
38. Kamranvar, S. A. & Masucci, M. G. The Epstein-Barr virus nuclear antigen-1 promotes telomere dysfunction via induction of oxidative stress. Leukemia 25, 1017-1025 (2011).
39. Cheng, T. C. et al. Expression of Epstein-Barr nuclear antigen 1 in gastric carcinoma cells is associated with enhanced tumorigenicity and reduced cisplatin sensitivity. Int. J. Oncol. 36, 151-160 (2010).
40. Sivachandran, N., Sarkari, F. & Frappier, L. Epstein-Barr nuclear antigen 1 contributes to nasopharyngeal carcinoma through disruption of PML nuclear bodies. PLoS Pathog. 4, e1000170 (2008).
41. Feng, L., Wang, J. & Chen, J. The Lys63-specific deubiquitinating enzyme BRCC36 is regulated by two scaffold proteins localizing in different subcellular compartments. J. Biol. Chem. 285, 30982-30988 (2010).
42. Patterson-Fortin, J., Shao, G., Bretscher, H., Messick, T. E. & Greenberg, R. A. Differential regulation of JAMM domain deubiquitinating enzyme activity within the RAP80 complex. J. Biol. Chem. 285, 30971-30981 (2010).
43. Hu, X. et al. NBA1/MERIT40 and BRE interaction is required for the integrity of two distinct deubiquitinating enzyme BRCC36-containing complexes. J. Biol. Chem. 286, 11734-11745 (2011).
44. Cooper, E. M. et al. K63-specific deubiquitination by two JAMM/MPN+ complexes: BRISC-associated Brcc36 and proteasomal Poh1. EMBO J. 28, 621-631 (2009).
45. Cilenti, L. et al. Regulation of ABRO1/KIAA0157 during myocardial infarction and cell death reveals a novel cardioprotective mechanism for Lys63-specific deubiquitination. J. Mol. Cell Cardiol. 50, 652-661 (2011).
46. Zheng, H. et al. A BRISC-SHMT complex deubiquitinates IFNAR1 and regulates interferon responses. Cell Rep. 17, 180-193 (2013).
47. Feng, L., Huang, J. & Chen, J. MERIT40 facilitates BRCA1 localization and DNA damage repair. Genes Dev. 23, 719-728 (2009).
48. Cooper, E. M., Boeke, J. D. & Cohen, R. E. Specificity of the BRISC deubiquitinating enzyme is not due to selective binding to Lys63-linked polyubiquitin. J. Biol. Chem. 285, 10344-10352 (2010).
49. Kim, H., Huang, J. & Chen, J. CCDC98 is a BRCA1-BRCT domain-binding protein involved in the DNA damage response. Nat. Struct. Mol. Biol. 14, 710-715 (2007).
50. Ambivero, C. T., Cilenti, L. & Zervos, A. S. ATF4 interacts with ABRO1/ KIAA0157 scaffold protein and participates in a cytoprotective pathway. Biochim. Biophys. Acta 1823, 2149-2156 (2012).
51. Sowa, M. E., Bennett, E. J., Gygi, S. P. & Harper, J. W. Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403 (2009).
52. Muller, P. A. & Vousden, K. H. Mutant p53 in cancer: new functions and therapeutic opportunities. Cancer Cell 25, 304-317 (2014).
53. Tang, M. K. et al. Comparative proteomic analysis reveals a function of the novel death receptor-associated protein BRE in the regulation of prohibitin and p53 expression and proliferation. Proteomics 6, 2376-2385 (2006).
54. Wang, B., Hurov, K., Hofmann, K. & Elledge, S. J. NBA1, a new player in the Brca1 A complex, is required for DNA damage resistance and checkpoint control. Genes Dev. 23, 729-739 (2009).
55. Soussi, T., Dehouche, K. & Bé roud, C. p53 website and analysis of p53 gene mutations in human cancer: forging a link between epidemiology and carcinogenesis. Hum. Mutat. 15, 105-113 (2000).
56. Pan, X. et al. Elevated expression of CUEDC2 protein confers endocrine resistance in breast cancer. Nat. Med. 17, 708-714 (2011).
57. Zhu, C. Y. et al. Cell growth suppression by thanatos-associated protein 11(THAP11) is mediated by transcriptional downregulation of c-Myc. Cell Death Differ. 16, 395-405 (2009).
58. Yu, M. et al. Proteomic screen defines the hepatocyte nuclear factor 1alphabinding partners and identifies HMGB1 as a new cofactor of HNF1alpha. Nucleic Acids Res. 36, 1209-1219 (2008).
59. Feng, L., Wang, J. & Chen, J. The Lys63-specific deubiquitinating enzyme BRCC36 is regulated by two scaffold proteins localizing in different subcellular compartments. J. Biol. Chem. 285, 30982-30988 (2010).
60. Patterson-Fortin, J., Shao, G., Bretscher, H., Messick, T. E. & Greenberg, R. A. Differential regulation of JAMM domain deubiquitinating enzyme activity within the RAP80 complex. J. Biol. Chem. 285, 30971-30981 (2010).
61. Liu, J. et al. Lentivirus-delivered short hairpin RNA targeting SNAIL inhibits HepG2 cell growth. Oncol. Rep. 30, 1483-1487 (2013).
62. Li, C. Y. et al. Overexpression of a hematopoietic transcriptional regulator EDAG induces myelopoiesis and suppresses lymphopoiesis in transgenic mice. Leukemia 21, 2277-2286 (2007).
63. Li, C. Y. et al. EDAG regulates the proliferation and differentiation of hematopoietic cells and resists cell apoptosis through the activation of nuclear factor-kappa B. Cell Death Differ. 11, 1299-1308 (2004).
64. Crescenzi, M., Soddu, S. & Tato', F. Mitotic cycle reactivation in terminally differentiated by adenovirus infection. J. Cell. Physiol. 162, 26-35 (1995).
65. Yuan, J., Luo, K., Zhang, L., Cheville, J. C. & Lou, Z. USP10 regulates p53 localization and stability by deubiquitinating p53. Cell 140, 384-396 (2010).