Identification of RNF168 as a PML nuclear body regulator

Journal of Cell Science

Volumn 129, Issue 3, 2016, Pages 580-591

  Shire, Kathy ^a   Wong, Andrew I ^a   Tatham, Michael H ^b   Anderson, Oliver F ^b   Ripsman, David ^a   Gulstene, Stephanie ^a   Moffat, Jason ^a   Hay, Ronald T ^b   Frappier, Lori ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

PML nuclear bodies; RNF168; RNF8; SUMO

Indexed keywords

LYSINE; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN RNF168; PROTEIN RNF8; SHORT HAIRPIN RNA; SUMO 2 PROTEIN; SUMO 3 PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; ISOPROTEIN; NUCLEAR PROTEIN; PML PROTEIN, HUMAN; PROTEIN BINDING; RNF168 PROTEIN, HUMAN; SUMO PROTEIN; TRANSCRIPTION FACTOR; TUMOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE;

AMINO ACID SEQUENCE; ARTICLE; CELL NUCLEUS INCLUSION BODY; COMPLEX FORMATION; CONTROLLED STUDY; CORRELATION ANALYSIS; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; PLASMID; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SUMOYLATION; U2OS CELL LINE; UBIQUITINATION; WESTERN BLOTTING; HUMAN; METABOLISM; MYELOID LEUKEMIA; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; HUMANS; INTRANUCLEAR INCLUSION BODIES; LEUKEMIA, MYELOID; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN BINDING; PROTEIN ISOFORMS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84957697039     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.176446     Document Type: Article

References (61)

1. Ablain, J., Rice, K., Soilihi, H., de Reynies, A., Minucci, S. and de Thé, H. (2014). Activation of a promyelocytic leukemia-tumor protein 53 axis underlies acute promyelocytic leukemia cure. Nat. Med. 20, 167-174.
2. Al-Hakim, A., Escribano-Diaz, C., Landry, M.-C., O'Donnell, L., Panier, S., Szilard, R. K. and Durocher, D. (2010). The ubiquitous role of ubiquitin in the DNA damage response. DNA Repair 9, 1229-1240.
3. Bartocci, C. and Denchi, E. L. (2013). Put a RING on it: regulation and inhibition of RNF8 and RNF168 RING finger E3 ligases at DNA damage sites. Front. Genet. 4, 128.
4. Bernardi, R. and Pandolfi, P. P. (2007). Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell Biol. 8, 1006-1016.
5. Bischof, O., Kim, S.-H., Irving, J., Beresten, S., Ellis, N. A. and Campisi, J. (2001). Regulation and localization of the Bloom syndrome protein in response to DNA damage. J. Cell Biol. 153, 367-380.
6. Bøe, S. O., Haave, M., Jul-Larsen, A., Grudic, A., Bjerkvig, R. and Lønning, P. E. (2006). Promyelocytic leukemia nuclear bodies are predetermined processing sites for damaged DNA. J. Cell Sci. 119, 3284-3295.
7. Boichuk, S., Hu, L., Makielski, K., Pandolfi, P. P. and Gjoerup, O. V. (2011). Functional connection between Rad51 and PML in homology-directed repair. PLoS ONE 6, e25814.
8. Branigan, E., Plechanovová, A., Jaffray, E. G., Naismith, J. H. and Hay, R. T. (2015). Structural basis for the RING-catalyzed synthesis of K63-linked ubiquitin chains. Nat. Struct. Mol. Biol. 22, 597-602.
9. Condemine, W., Takahashi, Y., Zhu, J., Puvion-Dutilleul, F., Guegan, S., Janin, A. and de Thé, H. (2006). Characterization of endogenous human promyelocytic leukemia isoforms. Cancer Res. 66, 6192-6198.
10. Cuchet, D., Sykes, A., Nicolas, A., Orr, A., Murray, J., Sirma, H., Heeren, J., Bartelt, A. and Everett, R. D. (2011). PML isoforms I and II participate in PMLdependent restriction of HSV-1 replication. J. Cell Sci. 124, 280-291.
11. Cuchet-Lourenco, D., Vanni, E., Glass, M., Orr, A. and Everett, R. D. (2012). Herpes simplex virus 1 ubiquitin ligase ICP0 interacts with PML isoform I and induces its SUMO-independent degradation. J. Virol. 86, 11209-11222.
12. Danielsen, J. R., Povlsen, L. K., Villumsen, B. H., Streicher, W., Nilsson, J., Wikstrom, M., Bekker-Jensen, S. and Mailand, N. (2012). DNA damageinducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMObinding Zinc finger. J. Cell Biol. 197, 179-187.
13. de The, H., Le Bras, M. and Lallemand-Breitenbach, V. (2012). The cell biology of disease: acute promyelocytic leukemia, arsenic, and PML bodies. J. Cell Biol. 198, 11-21.
14. Dellaire, G. and Bazett-Jones, D. P. (2004). PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays 26, 963-977.
15. Dellaire, G., Ching, R. W., Ahmed, K., Jalali, F., Tse, K. C. K., Bristow, R. G. and Bazett-Jones, D. P. (2006). Promyelocytic leukemia nuclear bodies behave as DNA damage sensors whose response to DNA double-strand breaks is regulated by NBS1 and the kinases ATM, Chk2, and ATR. J. Cell Biol. 175, 55-66.
16. Doil, C., Mailand, N., Bekker-Jensen, S., Menard, P., Larsen, D. H., Pepperkok, R., Ellenberg, J., Panier, S., Durocher, D., Bartek, J. et al. (2009). RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435-446.
17. Erker, Y., Neyret-Kahn, H., Seeler, J. S., Dejean, A., Atfi, A. and Levy, L. (2013). Arkadia, a novel SUMO-targeted ubiquitin ligase involved in PML degradation. Mol. Cell. Biol. 33, 2163-2177.
18. Everett, R. D. and Chelbi-Alix, M. K. (2007). PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89, 819-830.
19. Fanelli, M., Fantozzi, A., De Luca, P., Caprodossi, S., Matsuzawa, S.-i., Lazar, M. A., Pelicci, P. G. and Minucci, S. (2004). The coiled-coil domain is the structural determinant for mammalian homologues of Drosophila Sina-mediated degradation of promyelocytic leukemia protein and other tripartite motif proteins by the proteasome. J. Biol. Chem. 279, 5374-5379.
20. Galanty, Y., Belotserkovskaya, R., Coates, J., Polo, S., Miller, K. M. and Jackson, S. P. (2009). Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-939.
21. Geoffroy, M.-C. and Chelbi-Alix, M. K. (2011). Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. 31, 145-158.
22. Geoffroy, M.-C. and Hay, R. T. (2009). An additional role for SUMO in ubiquitinmediated proteolysis. Nat. Rev. Mol. Cell Biol. 10, 564-568.
23. Guzzo, C. M., Berndsen, C. E., Zhu, J., Gupta, V., Datta, A., Greenberg, R. A., Wolberger, C. and Matunis, M. J. (2012). RNF4-dependent hybrid SUMOubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci. Signal. 5, ra88.
24. Hu, X., Paul, A. and Wang, B. (2012). Rap80 protein recruitment to DNA doublestrand breaks requires binding to both small ubiquitin-like modifier (SUMO) and ubiquitin conjugates. J. Biol. Chem. 287, 25510-25519.
25. Lallemand-Breitenbach, V. and de The, H. (2010). PML nuclear bodies. Cold Spring Harb. Perspect. Biol. 2, a000661.
26. Lallemand-Breitenbach, V., Zhu, J., Puvion, F., Koken, M., Honore, N., Doubeikovsky, A., Duprez, E., Pandolfi, P. P., Puvion, E., Freemont, P. et al. (2001). Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-inducedPML or PML/retinoic acid receptor alpha degradation. J. Exp. Med. 193, 1361-1372.
27. Lallemand-Breitenbach, V., Jeanne, M., Benhenda, S., Nasr, R., Lei, M., Peres, L., Zhou, J., Zhu, J., Raught, B. and de Thé, H. (2008). Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 10, 547-555.
28. MacPherson, M. J., Beatty, L. G., Zhou, W., Du, M. and Sadowski, P. D. (2009). The CTCF insulator protein is posttranslationally modified by SUMO. Mol. Cell. Biol. 29, 714-725.
29. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C. and Lukas, J. (2007). RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887-900.
30. Moffat, J., Grueneberg, D. A., Yang, X., Kim, S. Y., Kloepfer, A. M., Hinkle, G., Piqani, B., Eisenhaure, T. M., Luo, B., Grenier, J. K. et al. (2006). A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298.
31. Nisole, S., Maroui, M. A., Mascle, X. H., Aubry, M. and Chelbi-Alix, M. K. (2013). Differential Roles of PML Isoforms. Front. Oncol. 3, 125.
32. Panier, S. and Durocher, D. (2009). Regulatory ubiquitylation in response to DNA double-strand breaks. DNA Repair 8, 436-443.
33. Panier, S., Ichijima, Y., Fradet-Turcotte, A., Leung, C. C. Y., Kaustov, L., Arrowsmith, C. H. and Durocher, D. (2012). Tandemprotein interaction modules organize the ubiquitin-dependent response to DNA double-strand breaks. Mol. Cell 47, 383-395.
34. Pinato, S., Scandiuzzi, C., Arnaudo, N., Citterio, E., Gaudino, G. and Penengo, L. (2009). RNF168, a new RING finger, MIU-containing protein that modifies chromatin by ubiquitination of histones H2A and H2AX. BMC Mol. Biol. 10, 55.
35. Rabellino, A. and Scaglioni, P. P. (2013). PML degradation: multiple ways to eliminate PML. Front. Oncol. 3, 60.
36. Salomoni, P., Ferguson, B. J., Wyllie, A. H. and Rich, T. (2008). New insights into the role of PML in tumour suppression. Cell Res. 18, 622-640.
37. Sarkari, F., Wang, X., Nguyen, T. and Frappier, L. (2011). The herpesvirus associated ubiquitin specific protease, USP7, is a negative regulator of PML proteins and PML nuclear bodies. PLoS ONE 6, e16598.
38. Scaglioni, P. P., Yung, T. M., Cai, L. F., Erdjument-Bromage, H., Kaufman, A. J., Singh, B., Teruya-Feldstein, J., Tempst, P. and Pandolfi, P. P. (2006). A CK2-dependent mechanism for degradation of the PML tumor suppressor. Cell 126, 269-283.
39. Scaglioni, P. P., Yung, T. M., Choi, S. C., Baldini, C., Konstantinidou, G. and Pandolfi, P. P. (2008). CK2 mediates phosphorylation and ubiquitin-mediated degradation of the PML tumor suppressor. Mol. Cell. Biochem. 316, 149-154.
40. Seeler, J.-S. and Dejean, A. (2001). SUMO: of branched proteins and nuclear bodies. Oncogene 20, 7243-7249.
41. Seifert, A., Schofield, P., Barton, G. J. and Hay, R. T. (2015). Proteotoxic stress reprograms the chromatin landscape of SUMO modification. Sci. Signal. 8, rs7.
42. Shen, L., Tatham, M. H., Dong, C., Zagórska, A., Naismith, J. H. and Hay, R. T. (2006a). SUMO protease SENP1 induces isomerization of the scissile peptide bond. Nat. Struct. Mol. Biol. 13, 1069-1077.
43. Shen, T. H., Lin, H.-K., Scaglioni, P. P., Yung, T. M. and Pandolfi, P. P. (2006b). The mechanisms of PML-nuclear body formation. Mol. Cell 24, 331-339.
44. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V. and Mann, M. (2007). In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860.
45. Sivachandran, N., Sarkari, F. and Frappier, L. (2008). Epstein-Barr nuclear antigen 1 contributes to nasopharyngeal carcinoma through disruption of PML nuclear bodies. PLoS Pathog. 4, e1000170.
46. Sivachandran, N., Cao, J. Y. and Frappier, L. (2010). Epstein-Barr virus nuclear antigen 1 Hijacks the host kinase CK2 to disrupt PML nuclear bodies. J. Virol. 84, 11113-11123.
47. Sivachandran, N., Dawson, C. W., Young, L. S., Liu, F.-F., Middeldorp, J. and Frappier, L. (2012a). Contributions of the Epstein-Barr virus EBNA1 protein to gastric carcinoma. J. Virol. 86, 60-68.
48. Sivachandran, N., Wang, X. and Frappier, L. (2012b). Functions of the Epstein-Barr virus EBNA1 protein in viral reactivation and lytic infection. J. Virol. 86, 6146-6158.
49. Stewart, G. S., Panier, S., Townsend, K., Al-Hakim, A. K., Kolas, N. K., Miller, E. S., Nakada, S., Ylanko, J., Olivarius, S., Mendez, M. et al. (2009). The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136, 420-434.
50. Sun, Y., Hegamyer, G., Cheng, Y. J., Hildesheim, A., Chen, J. Y., Chen, I. H., Cao, Y., Yao, K. T. and Colburn, N. H. (1992). An infrequent point mutation of the p53 gene in human nasopharyngeal carcinoma. Proc. Natl. Acad. Sci. USA 89, 6516-6520.
51. Tatham, M. H., Geoffroy, M.-C., Shen, L., Plechanovova, A., Hattersley, N., Jaffray, E. G., Palvimo, J. J. and Hay, R. T. (2008). RNF4 is a poly-SUMOspecific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10, 538-546.
52. Tatham, M. H., Matic, I., Mann, M. and Hay, R. T. (2011). Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci. Signal. 4, rs4.
53. Tatham, M. H., Plechanovová, A., Jaffray, E. G., Salmen, H. and Hay, R. T. (2013). Ube2W conjugates ubiquitin to alpha-amino groups of protein N-termini. Biochem. J. 453, 137-145.
54. Tavalai, N. and Stamminger, T. (2009). Interplay between Herpesvirus infection and host defense by PML nuclear bodies. Viruses 1, 1240-1264.
55. Tavalai, N. and Stamminger, T. (2011). Intrinsic cellular defense mechanisms targeting human cytomegalovirus. Virus Res. 157, 128-133.
56. Tikoo, S., Madhavan, V., Hussain, M., Miller, E. S., Arora, P., Zlatanou, A., Modi, P., Townsend, K., Stewart, G. S. and Sengupta, S. (2013). Ubiquitin-dependent recruitment of the Bloom syndrome helicase upon replication stress is required to suppress homologous recombination. EMBO J. 32, 1778-1792.
57. Wolyniec, K., Shortt, J., de Stanchina, E., Levav-Cohen, Y., Alsheich-Bartok, O., Louria-Hayon, I., Corneille, V., Kumar, B., Woods, S. J., Opat, S. et al. (2012). E6AP ubiquitin ligase regulates PML-induced senescence in Myc-driven lymphomagenesis. Blood 120, 822-832.
58. Wu, H.-C., Lin, Y.-C., Liu, C.-H., Chung, H.-C., Wang, Y.-T., Lin, Y.-W., Ma, H.-I., Tu, P.-H., Lawler, S. E. and Chen, R.-H. (2014). USP11 regulates PML stability to control Notch-induced malignancy in brain tumours. Nat. Commun. 5, 3214.
59. Yeung, P. L., Denissova, N. G., Nasello, C., Hakhverdyan, Z., Chen, J. D. and Brenneman, M. A. (2012). Promyelocytic leukemia nuclear bodies support a late step in DNA double-strand break repair by homologous recombination. J. Cell Biochem. 113, 1787-1799.
60. Yuan, W.-C., Lee, Y.-R., Huang, S.-F., Lin, Y.-M., Chen, T.-Y., Chung, H.-C., Tsai, C.-H., Chen, H.-Y., Chiang, C.-T., Lai, C.-K. et al. (2011). A Cullin3-KLHL20 Ubiquitin ligase-dependent pathway targets PML to potentiate HIF-1 signaling and prostate cancer progression. Cancer Cell 20, 214-228.
61. Zhong, S., Hu, P., Ye, T.-Z., Stan, R., Ellis, N. A. and Pandolfi, P. P. (2000). A role for PML and the nuclear body in genomic stability. Oncogene 18, 7941-7947.