Positive feedback regulation of p53 transactivity by DNA damage-induced ISG15 modification

Nature Communications

Volumn 7, Issue , 2016, Pages

  Park, Jong Ho ^a   Yang, Seung Wook ^a   Park, Jung Mi ^a   Ka, Seung Hyeun ^a   Kim, Ji Hoon ^a   Kong, Young Yun ^a   Jeon, Young Joo ^b   Seol, Jae Hong ^a   Chung, Chin Ha ^a,c  

^a Seoul National University   (South Korea)

^b Chungnam National University   (South Korea)

^c National Academy of Sciences   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; DOXORUBICIN; EFP PROTEIN; ISG15 PROTEIN; PROTEIN BAX; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; UBCH8 PROTEIN; UBE1L PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; BAX PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYTOKINE; ISG15 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN; UBE1L PROTEIN, HUMAN; UBE2L6 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

DNA; GENE EXPRESSION; PROTEIN; TUMOR; ULTRAVIOLET RADIATION;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING SITE; CARCINOGENESIS; CELL GROWTH; COLON CARCINOMA; CONJUGATION; CONTROLLED STUDY; DNA DAMAGE; DNA MODIFICATION; DNA RESPONSIVE ELEMENT; FEMALE; HCT116 CELL LINE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PROMOTER REGION; PROTEIN ACETYLATION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; TRANSACTIVATION; UBIQUITINATION; ACETYLATION; CELL PROLIFERATION; DRUG EFFECT; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RADIATION RESPONSE; TUMOR CELL LINE; ULTRAVIOLET RADIATION;

ACETYLATION; BCL-2-ASSOCIATED X PROTEIN; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYTOKINES; DNA DAMAGE; DOXORUBICIN; HUMANS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINS; ULTRAVIOLET RAYS;

EID: 84984623404     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12513     Document Type: Article

References (68)

1. Lane, D. P. Cancer. p53, guardian of the genome. Nature 358, 15-16 (1992)
2. Levine, A. J. p53, the cellular gatekeeper for growth and division. Cell 88, 323-331 (1997)
3. Green, D. R. & Kroemer, G. Cytoplasmic functions of the tumour suppressor p53. Nature 458, 1127-1130 (2009)
4. Riley, T., Sontag, E., Chen, P. & Levine, A. Transcriptional control of human p53-regulated genes. Nat. Rev. Mol. Cell Biol. 9, 402-412 (2008)
5. Ashcroft, M. & Vousden, K. H. Regulation of p53 stability. Oncogene 18, 7637-7643 (1999)
6. Oliner, J. D., Kinzler, K. W., Meltzer, P. S., George, D. L. & Vogelstein, B. Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 358, 80-83 (1992)
7. Wu, X., Bayle, J. H., Olson, D. & Levine, A. J. The p53-mdm-2 autoregulatory feedback loop. Genes Dev. 7, 1126-1132 (1993)
8. el-Deiry, W. S. et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54, 1169-1174 (1994)
9. Miyashita, T. & Reed, J. C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293-299 (1995)
10. Nakano, K. & Vousden, K. H. PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell 7, 683-694 (2001)
11. Brooks, C. L. & Gu, W. Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation. Curr. Opin. Cell Biol 15, 164-171 (2003)
12. 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. 282, 1797-1804 (2007)
13. 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 118, 83-97 (2004)
14. Gostissa, M. et al. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J. 18, 6462-6471 (1999)
15. Rodriguez, M. S. et al. SUMO-1 modification activates the transcriptional response of p53. EMBO J. 18, 6455-6461 (1999)
16. Huang, Y. F., Wee, S., Gunaratne, J., Lane, D. P. & Bulavin, D. V. Isg15 controls p53 stability and functions. Cell Cycle 13, 2200-2210 (2014)
17. Haas, A. L., Ahrens, P., Bright, P. M. & Ankel, H. Interferon induces a 15- kilodalton protein exhibiting marked homology to ubiquitin. J. Biol. Chem. 262, 11315-11323 (1987)
18. Kim, M. J., Latham, A. G. & Krug, R. M. Human influenza viruses activate an interferon-independent transcription of cellular antiviral genes: outcome with influenza A virus is unique. Proc. Natl Acad. Sci. USA 99, 10096-10101 (2002)
19. Yuan, W. & Krug, R. M. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 20, 362-371 (2001)
20. Dastur, A., Beaudenon, S., Kelley, M., Krug, R. M. & Huibregtse, J. M. Herc5, an interferon-induced HECT E3 enzyme, is required for conjugation of ISG15 in human cells. J. Biol. Chem. 281, 4334-4338 (2006)
21. Kim, K. I., Giannakopoulos, N. V., Virgin, H. W. & Zhang, D. E. Interferoninducible ubiquitin E2, Ubc8, is a conjugating enzyme for protein ISGylation. Mol. Cell Biol. 24, 9592-9600 (2004)
22. Zou, W. & Zhang, D. E. The interferon-inducible ubiquitin-protein isopeptide ligase (E3) EFP also functions as an ISG15 E3 ligase. J. Biol. Chem. 281, 3989-3994 (2006)
23. Malakhov, M. P., Malakhova, O. A., Kim, K. I., Ritchie, K. J. & Zhang, D. E. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J. Biol. Chem. 277, 9976-9981 (2002)
24. DCunha, J., Knight, Jr E., Haas, A. L., Truitt, R. L. & Borden, E. C. Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc. Natl Acad. Sci. USA 93, 211-215 (1996)
25. Recht, M., Borden, E. C. & Knight, Jr E. A human 15-kDa IFN-induced protein induces the secretion of IFN-gamma. J. Immunol. 147, 2617-2623 (1991)
26. Lai, C. et al. Mice lacking the ISG15 E1 enzyme UbE1L demonstrate increased susceptibility to both mouse-adapted and non-mouse-adapted influenza B virus infection. J. Virol. 83, 1147-1151 (2009)
27. Lenschow, D. J. et al. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc. Natl Acad. Sci. USA 104, 1371-1376 (2007)
28. Dauphinee, S. M. et al. Contribution of increased ISG15, ISGylation and deregulated type I IFN signaling in Usp18 mutant mice during the course of bacterial infections. Genes Immun. 15, 282-292 (2014)
29. Bogunovic, D. et al. Mycobacterial disease and impaired IFN-gamma immunity in humans with inherited ISG15 deficiency. Science 337, 1684-1688 (2012)
30. Bogunovic, D., Boisson-Dupuis, S. & Casanova, J. L. ISG15: leading a double life as a secreted molecule. Exp. Mol. Med. 45, e18 (2013)
31. Zhang, X. et al. Human intracellular ISG15 prevents interferon-alpha/beta over-amplification and auto-inflammation. Nature 517, 89-93 (2015)
32. Jeon, Y. J. et al. Chemosensitivity is controlled by p63 modification with ubiquitin-like protein ISG15. J. Clin. Invest. 122, 2622-2636 (2012)
33. Park, J. M. et al. Modification of PCNA by ISG15 plays a crucial role in termination of error-prone translesion DNA synthesis. Mol. Cell 54, 626-638 (2014)
34. Sarkaria, J. N. et al. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59, 4375-4382 (1999)
35. el-Deiry, W. S., Kern, S. E., Pietenpol, J. A., Kinzler, K. W. & Vogelstein, B. Definition of a consensus binding site for p53. Nat. Genet. 1, 45-49 (1992)
36. Der, S. D., Zhou, A., Williams, B. R. & Silverman, R. H. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl Acad. Sci. USA 95, 15623-15628 (1998)
37. Ritchie, K. J. & Zhang, D. E. ISG15: the immunological kin of ubiquitin. Semin. Cell Dev. Biol. 15, 237-246 (2004)
38. Lee, E. W. et al. Differential regulation of p53 and p21 by MKRN1 E3 ligase controls cell cycle arrest and apoptosis. EMBO J. 28, 2100-2113 (2009)
39. Gu, W. & Roeder, R. G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90, 595-606 (1997)
40. Luo, J. et al. Acetylation of p53 augments its site-specific DNA binding both in vitro and in vivo. Proc. Natl Acad. Sci. USA 101, 2259-2264 (2004)
41. Dornan, D. & Hupp, T. R. Inhibition of p53-dependent transcription by BOX-I phospho-peptide mimetics that bind to p300. EMBO Rep. 2, 139-144 (2001)
42. Maclaine, N. J. & Hupp, T. R. The regulation of p53 by phosphorylation: a model for how distinct signals integrate into the p53 pathway. Aging 1, 490-502 (2009)
43. Durfee, L. A., Lyon, N., Seo, K. & Huibregtse, J. M. The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol. Cell 38, 722-732 (2010)
44. Leong, C. O., Vidnovic, N., DeYoung, M. P., Sgroi, D. & Ellisen, L. W. The p63/ p73 network mediates chemosensitivity to cisplatin in a biologically defined subset of primary breast cancers. J. Clin. Invest. 117, 1370-1380 (2007)
45. Patturajan, M. et al. DeltaNp63 induces beta-catenin nuclear accumulation and signaling. Cancer Cell 1, 369-379 (2002)
46. Dohn, M., Zhang, S. & Chen, X. p63alpha and DeltaNp63alpha can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes. Oncogene 20, 3193-3205 (2001)
47. Duijf, P. H. et al. Gain-of-function mutation in ADULT syndrome reveals the presence of a second transactivation domain in p63. Hum. Mol. Genet. 11, 799-804 (2002)
48. Candi, E. et al. Differential roles of p63 isoforms in epidermal development: selective genetic complementation in p63 null mice. Cell Death Differ. 13, 1037-1047 (2006)
49. Serber, Z. et al. A C-terminal inhibitory domain controls the activity of p63 by an intramolecular mechanism. Mol. Cell. Biol. 22, 8601-8611 (2002)
50. Deutsch, G. B. et al. DNA damage in oocytes induces a switch of the quality control factor TAp63alpha from dimer to tetramer. Cell 144, 566-576 (2011)
51. Jeon, Y. J., Yoo, H. M. & Chung, C. H. ISG15 and immune diseases. Biochim. Biophys. Acta 1802, 485-496 (2010)
52. Andersen, J. B. et al. Stage-associated overexpression of the ubiquitin-like protein, ISG15, in bladder cancer. Br. J. Cancer 94, 1465-1471 (2006)
53. Bektas, N. et al. The ubiquitin-like molecule interferon-stimulated gene 15 (ISG15) is a potential prognostic marker in human breast cancer. Breast Cancer Res. 10, R58 (2008)
54. Desai, S. D. et al. Elevated expression of ISG15 in tumor cells interferes with the ubiquitin/26S proteasome pathway. Cancer Res. 66, 921-928 (2006)
55. Kiessling, A. et al. Expression, regulation and function of the ISGylation system in prostate cancer. Oncogene 28, 2606-2620 (2009)
56. Satake, H. et al. The ubiquitin-like molecule interferon-stimulated gene 15 is overexpressed in human prostate cancer. Oncol. Rep. 23, 11-16 (2010)
57. Huang, Y. F. & Bulavin, D. V. Oncogene-mediated regulation of p53 ISGylation and functions. Oncotarget 5, 5808-5818 (2014)
58. Chinyengetere, F. et al. Mice null for the deubiquitinase USP18 spontaneously develop leiomyosarcomas. BMC Cancer 15, 886 (2015)
59. Guo, Y. et al. Blockade of the ubiquitin protease UBP43 destabilizes transcription factor PML/RARalpha and inhibits the growth of acute promyelocytic leukemia. Cancer Res. 70, 9875-9885 (2010)
60. Guo, Y. et al. Evidence for the ubiquitin protease UBP43 as an antineoplastic target. Mol. Cancer Ther. 11, 1968-1977 (2012)
61. Shahidul Makki, M., Cristy Ruteshouser, E. & Huff, V. Ubiquitin specific protease 18 (Usp18) is a WT1 transcriptional target. Exp. Cell Res. 319, 612-622 (2013)
62. Feng, Q. et al. UBE1L causes lung cancer growth suppression by targeting cyclin D1. Mol. Cancer Ther. 7, 3780-3788 (2008)
63. Kitareewan, S. et al. UBE1L is a retinoid target that triggers PML/RARalpha degradation and apoptosis in acute promyelocytic leukemia. Proc. Natl Acad. Sci. USA 99, 3806-3811 (2002)
64. McLaughlin, P. M. et al. The ubiquitin-activating enzyme E1-like protein in lung cancer cell lines. Int. J. Cancer 85, 871-876 (2000)
65. Pitha-Rowe, I., Hassel, B. A. & Dmitrovsky, E. Involvement of UBE1L in ISG15 conjugation during retinoid-induced differentiation of acute promyelocytic leukemia. J. Biol. Chem. 279, 18178-18187 (2004)
66. Shah, S. J. et al. UBE1L represses PML/RAR{alpha} by targeting the PML domain for ISG15ylation. Mol. Cancer Ther. 7, 905-914 (2008)
67. Lee, S. W. et al. SUMOylation of hnRNP-K is required for p53-mediated cell-cycle arrest in response to DNA damage. EMBO J. 31, 4441-4452 (2012)
68. Jeon, Y. J. et al. Regulation of glutamine carrier proteins by RNF5 determines breast cancer response to ER stress-inducing chemotherapies. Cancer Cell 27, 354-369 (2015)