The deubiquitylating enzyme USP44 counteracts the DNA double-strand break response mediated by the RNF8 and RNF168 ubiquitin ligases

Journal of Biological Chemistry

Volumn 288, Issue 23, 2013, Pages 16579-16587

  Mosbech, Anna ^a   Lukas, Claudia ^a   Bekker Jensen, Simon ^a   Mailand, Niels ^a  

^a University of Copenhagen   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR RESPONSE; DNA DOUBLE-STRAND BREAKS; FUNCTIONAL REDUNDANCY; OVER-EXPRESSION; PROTEIN ASSEMBLY; RING FINGER; UBIQUITIN LIGASES; UBIQUITYLATION;

ENZYMES;

PROTEINS;

HISTONE H2A; PROTEIN RNF168; PROTEIN RNF8; PROTEINASE; REGULATOR PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN SPECIFIC PROTEASE 26; UBIQUITIN SPECIFIC PROTEASE 29; UBIQUITIN SPECIFIC PROTEASE 44; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SUBSTRATE; HISTONE UBIQUITINATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

DEUBIQUITYLATION; DNA DAMAGE RESPONSE; DNA REPAIR; SIGNALING; UBIQUITIN;

CELL LINE; CYSTEINE ENDOPEPTIDASES; DNA BREAKS, DOUBLE-STRANDED; DNA-BINDING PROTEINS; ENDOPEPTIDASES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84878758649     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.459917     Document Type: Article

References (42)

1. Ciccia, A., and Elledge, S. J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204
2. Bekker-Jensen, S., and Mailand, N. (2010) Assembly and function of DNA double-strand break repair foci in mammalian cells. DNA Repair 9, 1219-1228
3. Lukas, J., Lukas, C., and Bartek, J. (2011) More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat. Cell Biol. 13, 1161-1169
4. Huen, M. S., Grant, R., Manke, I., Minn, K., Yu, X., Yaffe, M. B., and Chen, J. (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131, 901-914 (Pubitemid 350138083)
5. 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 (Pubitemid 350138084)
6. Mattiroli, F., Vissers, J. H., van Dijk, W. J., Ikpa, P., Citterio, E., Vermeulen, W., Marteijn, J. A., and Sixma, T. K. (2012) RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150, 1182-1195
7. Doil, C., Mailand, N., Bekker-Jensen, S., Menard, P., Larsen, D. H., Pepperkok, R., Ellenberg, J., Panier, S., Durocher, D., Bartek, J., Lukas, J., and Lukas, C. (2009) RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435-446
8. 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., Oldreive, C., Wildenhain, J., Tagliaferro, A., Pelletier, L., Taubenheim, N., Durandy, A., Byrd, P. J., Stankovic, T., Taylor, A. M., and Durocher, D. (2009) The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136, 420-434
9. Pinato, S., Gatti, M., Scandiuzzi, C., Confalonieri, S., and Penengo, L. (2011) UMI, a novel RNF168 ubiquitin binding domain involved in the DNA damage signaling pathway. Mol. Cell Biol. 31, 118-126
10. Bouwman, P., Aly, A., Escandell, J. M., Pieterse, M., Bartkova, J., van der Gulden, H., Hiddingh, S., Thanasoula, M., Kulkarni, A., Yang, Q., Haffty, B. G., Tommiska, J., Blomqvist, C., Drapkin, R., Adams, D. J., Nevanlinna, H., Bartek, J., Tarsounas, M., Ganesan, S., and Jonkers, J. (2010) 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 17, 688-695
11. Bunting, S. F., Callén, E., Wong, N., Chen, H. T., Polato, F., Gunn, A., Bothmer, A., Feldhahn, N., Fernandez-Capetillo, O., Cao, L., Xu, X., Deng, C. X., Finkel, T., Nussenzweig, M., Stark, J. M., and Nussenzweig, A. (2010) 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141, 243-254
12. Chapman, J. R., Taylor, M. R., and Boulton, S. J. (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 47, 497-510
13. Kim, H., Chen, J., and Yu, X. (2007) Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316, 1202-1205 (Pubitemid 46877484)
14. Sobhian, B., Shao, G., Lilli, D. R., Culhane, A. C., Moreau, L. A., Xia, B., Livingston, D. M., and Greenberg, R. A. (2007) RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316, 1198-1202 (Pubitemid 46877483)
15. Wang, B., Matsuoka, S., Ballif, B. A., Zhang, D., Smogorzewska, A., Gygi, S. P., and Elledge, S. J. (2007) Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316, 1194-1198 (Pubitemid 46877482)
16. Wu, J., Huen, M. S., Lu, L. Y., Ye, L., Dou, Y., Ljungman, M., Chen, J., and Yu, X. (2009) Histone ubiquitination associates with BRCA1-dependent DNA damage response. Mol. Cell Biol. 29, 849-860
17. Sato, Y., Yoshikawa, A., Mimura, H., Yamashita, M., Yamagata, A., and Fukai, S. (2009) Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by tandem UIMs of RAP80. EMBO J. 28, 2461-2468
18. Acs, K., Luijsterburg, M. S., Ackermann, L., Salomons, F. A., Hoppe, T., and Dantuma, N. P. (2011) The AAA-ATPase VCP/p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks. Nat. Struct. Mol. Biol. 18, 1345-1350
19. Mallette, F. A., Mattiroli, F., Cui, G., Young, L. C., Hendzel, M. J., Mer, G., Sixma, T. K., and Richard, S. (2012) RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J. 31, 1865-1878
20. Gudjonsson, T., Altmeyer, M., Savic, V., Toledo, L., Dinant, C., Grøfte, M., Bartkova, J., Poulsen, M., Oka, Y., Bekker-Jensen, S., Mailand, N., Neumann, B., Heriche, J. K., Shearer, R., Saunders, D., Bartek, J., Lukas, J., and Lukas, C. (2012) TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 150, 697-709
21. Nakada, S., Tai, I., Panier, S., Al-Hakim, A., Iemura, S., Juang, Y. C., O'Donnell, L., Kumakubo, A., Munro, M., Sicheri, F., Gingras, A. C., Natsume, T., Suda, T., and Durocher, D. (2010) Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466, 941-946
22. Shao, G., Lilli, D. R., Patterson-Fortin, J., Coleman, K. A., Morrissey, D. E., and Greenberg, R. A. (2009) The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc. Natl. Acad. Sci. U.S.A. 106, 3166-3171
23. Shanbhag, N. M., Rafalska-Metcalf, I. U., Balane-Bolivar, C., Janicki, S. M., and Greenberg, R. A. (2010) ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141, 970-981
24. Nicassio, F., Corrado, N., Vissers, J. H., Areces, L. B., Bergink, S., Marteijn, J. A., Geverts, B., Houtsmuller, A. B., Vermeulen, W., Di Fiore, P. P., and Citterio, E. (2007) Human USP3 is a chromatin modifier required for S phase progression and genome stability. Curr. Biol. 17, 1972-1977 (Pubitemid 350088491)
25. Butler, L. R., Densham, R. M., Jia, J., Garvin, A. J., Stone, H. R., Shah, V., Weekes, D., Festy, F., Beesley, J., and Morris, J. R. (2012) The proteasomal de-ubiquitinating enzyme POH1 promotes the double-strand DNA break response. EMBO J. 31, 3918-3934
26. Bekker-Jensen, S., Lukas, C., Melander, F., Bartek, J., and Lukas, J. (2005) Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J. Cell Biol. 170, 201-211 (Pubitemid 41043803)
27. Lukas, C., Melander, F., Stucki, M., Falck, J., Bekker-Jensen, S., Goldberg, M., Lerenthal, Y., Jackson, S. P., Bartek, J., and Lukas, J. (2004) Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23, 2674-2683 (Pubitemid 38988238)
28. Poulsen, M., Lukas, C., Lukas, J., Bekker-Jensen, S., and Mailand, N. (2012) Human RNF169 is a negative regulator of the ubiquitin-dependent response to DNA double-strand breaks. J. Cell Biol. 197, 189-199
29. Nijman, S. M., Luna-Vargas, M. P., Velds, A., Brummelkamp, T. R., Dirac, A. M., Sixma, T. K., and Bernards, R. (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786 (Pubitemid 41721026)
30. Wang, P. J., McCarrey, J. R., Yang, F., and Page, D. C. (2001) An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 27, 422-426 (Pubitemid 32268424)
31. Scheuermann, J. C., de Ayala Alonso, A. G., Oktaba, K., Ly-Hartig, N., McGinty, R. K., Fraterman, S., Wilm, M., Muir, T. W., and Müller, J. (2010) Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature 465, 243-247
32. Vissers, J. H., Nicassio, F., van Lohuizen, M., Di Fiore, P. P., and Citterio, E. (2008) The many faces of ubiquitinated histone H2A: insights from the DUBs. Cell Div. 3, 8
33. Bekker-Jensen, S., Rendtlew Danielsen, J., Fugger, K., Gromova, I., Nerstedt, A., Lukas, C., Bartek, J., Lukas, J., and Mailand, N. (2010) HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat. Cell Biol. 12, (suppl.) 80-86
34. 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
35. Morris, J. R., Boutell, C., Keppler, M., Densham, R., Weekes, D., Alamshah, A., Butler, L., Galanty, Y., Pangon, L., Kiuchi, T., Ng, T., and Solomon, E. (2009) The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886-890
36. Fuchs, G., Shema, E., Vesterman, R., Kotler, E., Wolchinsky, Z., Wilder, S., Golomb, L., Pribluda, A., Zhang, F., Haj-Yahya, M., Feldmesser, E., Brik, A., Yu, X., Hanna, J., Aberdam, D., Domany, E., and Oren, M. (2012) RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. Mol. Cell 46, 662-673
37. Brooks, C. L., and Gu, W. (2011) p53 regulation by ubiquitin. FEBS Lett. 585, 2803-2809
38. Stegmeier, F., Rape, M., Draviam, V. M., Nalepa, G., Sowa, M. E., Ang, X. L., McDonald, E. R., 3rd, Li, M. Z., Hannon, G. J., Sorger, P. K., Kirschner, M. W., Harper, J. W., and Elledge, S. J. (2007) Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature 446, 876-881
39. Zhang, Y., van Deursen, J., and Galardy, P. J. (2011) Overexpression of ubiquitin specific protease 44 (USP44) induces chromosomal instability and is frequently observed in human T-cell leukemia. PLoS One 6, e23389
40. Joo, H. Y., Zhai, L., Yang, C., Nie, S., Erdjument-Bromage, H., Tempst, P., Chang, C., and Wang, H. (2007) Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature 449, 1068-1072 (Pubitemid 350014605)
41. Cohn, M. A., Kee, Y., Haas, W., Gygi, S. P., and D'Andrea, A. D. (2009) UAF1 is a subunit of multiple deubiquitinating enzyme complexes. J. Biol. Chem. 284, 5343-5351
42. Zhang, Y., Foreman, O., Wigle, D. A., Kosari, F., Vasmatzis, G., Salisbury, J. L., van Deursen, J., and Galardy, P. J. (2012) USP44 regulates centrosome positioning to prevent aneuploidy and suppress tumorigenesis. J. Clin. Invest. 122, 4362-4374