Enrichment of Cdk1-cyclins at DNA double-strand breaks stimulates Fun30 phosphorylation and DNA end resection

Nucleic Acids Research

Volumn 44, Issue 6, 2016, Pages 2742-2753

  Chen, Xuefeng ^a   Niu, Hengyao ^b   Yu, Yang ^c   Wang, Jingjing ^a   Zhu, Shuangyi ^a   Zhou, Jianjie ^a   Papusha, Alma ^c   Cui, Dandan ^c   Pan, Xuewen ^c   Kwon, Youngho ^b   Sung, Patrick ^b   Ira, Grzegorz ^c  

^a WUHAN UNIVERSITY   (China)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CDK1 CYCLIN COMPLEX; CLB2 PROTEIN; CLB5 PROTEIN; CYCLIN DEPENDENT KINASE 1; CYCLINE; FUN30 PROTEIN; HYBRID PROTEIN; REGULATOR PROTEIN; SERINE; UNCLASSIFIED DRUG; CHROMATIN; CLB2 PROTEIN, S CEREVISIAE; CLB5 PROTEIN, S CEREVISIAE; CYCLIN B; FUN30 PROTEIN, S CEREVISIAE; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; DNA END RESECTION; DOUBLE STRANDED DNA BREAK; FUN30 GENE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; AMINO ACID SEQUENCE; CHEMISTRY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA END JOINING REPAIR; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; CDC2 PROTEIN KINASE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYCLIN B; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, FUNGAL; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SERINE; TRANSCRIPTION FACTORS;

EID: 84964335156     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1544     Document Type: Article

References (60)

1. Bonilla, C.Y., Melo, J.A. and Toczyski, D.P. (2008) Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Mol. Cell, 30, 267-276.
2. Enserink, J.M. and Kolodner, R.D. (2010) An overview of Cdk1-controlled targets and processes. Cell Div., 5, 11.
3. Koivomagi, M., Valk, E., Venta, R., Iofik, A., Lepiku, M., Morgan, D.O. and Loog, M. (2011) Dynamics of Cdk1 substrate specificity during the cell cycle. Mol. Cell, 42, 610-623.
4. Loog, M. and Morgan, D.O. (2005) Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature, 434, 104-108.
5. Koivomagi, M., Ord, M., Iofik, A., Valk, E., Venta, R., Faustova, I., Kivi, R., Balog, E.R., Rubin, S.M. and Loog, M. (2013) Multisite phosphorylation networks as signal processors for Cdk1. Nat. Struct. Mol. Biol., 20, 1415-1424.
6. McGrath, D.A., Balog, E.R., Koivomagi, M., Lucena, R., Mai, M.V., Hirschi, A., Kellogg, D.R., Loog, M. and Rubin, S.M. (2013) Cks confers specificity to phosphorylation-dependent CDK signaling pathways. Nat. Struct. Mol. Biol., 20, 1407-1414.
7. Holt, L.J., Tuch, B.B., Villen, J., Johnson, A.D., Gygi, S.P. and Morgan, D.O. (2009) Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science, 325, 1682-1686.
8. Aylon, Y., Liefshitz, B. and Kupiec, M. (2004) The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J., 23, 4868-4875.
9. Ira, G., Pellicioli, A., Balijja, A., Wang, X., Fiorani, S., Carotenuto, W., Liberi, G., Bressan, D., Wan, L., Hollingsworth, N.M. et al. (2004) DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature, 431, 1011-1017.
10. Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G.C., Lukas, J. and Jackson, S.P. (2006) ATM-and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol., 8, 37-45.
11. Barlow, J.H., Lisby, M. and Rothstein, R. (2008) Differential regulation of the cellular response to DNA double-strand breaks in G1. Mol. Cell, 30, 73-85.
12. Janke, R., Herzberg, K., Rolfsmeier, M., Mar, J., Bashkirov, V.I., Haghnazari, E., Cantin, G., Yates, J.R. 3rd and Heyer, W.D. (2010) A truncated DNA-damage-signaling response is activated after DSB formation in the G1 phase of Saccharomyces cerevisiae. Nucleic Acids Res., 38, 2302-2313.
13. Aparicio, T., Baer, R. and Gautier, J. (2014) DNA double-strand break repair pathway choice and cancer. DNA Repair (Amst.), 19, 169-175.
14. Chung, W.H., Zhu, Z., Papusha, A., Malkova, A. and Ira, G. (2010) Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet., 6, e1000948.
15. Zakharyevich, K., Ma, Y., Tang, S., Hwang, P.Y., Boiteux, S. and Hunter, N. (2010) Temporally and biochemically distinct activities of Exo1 during meiosis: Double-strand break resection and resolution of double Holliday junctions. Mol. Cell, 40, 1001-1015.
16. Aboussekhra, A., Chanet, R., Adjiri, A. and Fabre, F. (1992) Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Mol. Cell. Biol., 12, 3224-3234.
17. Cejka, P., Cannavo, E., Polaczek, P., Masuda-Sasa, T., Pokharel, S., Campbell, J.L. and Kowalczykowski, S.C. (2010) DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature, 467, 112-116.
18. Mimitou, E.P. and Symington, L.S. (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature, 455, 770-774.
19. Niu, H., Chung, W.H., Zhu, Z., Kwon, Y., Zhao, W., Chi, P., Prakash, R., Seong, C., Liu, D., Lu, L. et al. (2010) Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature, 467, 108-111.
20. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E. and Ira, G. (2008) Sgs1 helicase and two nucleases dna2 and exo1 resect DNA double-strand break ends. Cell, 134, 981-994.
21. Nicolette, M.L., Lee, K., Guo, Z., Rani, M., Chow, J.M., Lee, S.E. and Paull, T.T. (2010) Mre11-Rad50-Xrs2 and Sae2 promote 5-strand resection of DNA double-strand breaks. Nat. Struct. Mol. Biol., 17, 1478-1485.
22. Chen, X., Niu, H., Chung, W.H., Zhu, Z., Papusha, A., Shim, E.Y., Lee, S.E., Sung, P. and Ira, G. (2011) Cell cycle regulation of DNA double-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat. Struct. Mol. Biol., 18, 1015-1019.
23. Huertas, P., Cortes-Ledesma, F., Sartori, A.A., Aguilera, A. and Jackson, S.P. (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature, 455, 689-692.
24. Tomimatsu, N., Mukherjee, B., Catherine Hardebeck, M., Ilcheva, M., Vanessa Camacho, C., Louise Harris, J., Porteus, M., Llorente, B., Khanna, K.K. and Burma, S. (2014) Phosphorylation of EXO1 by CDKs 1 and 2 regulates DNA end resection and repair pathway choice. Nat. Commun., 5, 3561.
25. Huertas, P. and Jackson, S.P. (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem., 284, 9558-9565.
26. Falck, J., Forment, J.V., Coates, J., Mistrik, M., Lukas, J., Bartek, J. and Jackson, S.P. (2012) CDK targeting of NBS1 promotes DNA-end resection, replication restart and homologous recombination. EMBO Rep., 13, 561-568.
27. Wohlbold, L., Merrick, K.A., De, S., Amat, R., Kim, J.H., Larochelle, S., Allen, J.J., Zhang, C., Shokat, K.M., Petrini, J.H. et al. (2012) Chemical genetics reveals a specific requirement for Cdk2 activity in the DNA damage response and identifies Nbs1 as a Cdk2 substrate in human cells. PLoS Genet., 8, e1002935.
28. Peterson, S.E., Li, Y., Chait, B.T., Gottesman, M.E., Baer, R. and Gautier, J. (2011) Cdk1 uncouples CtIP-dependent resection and Rad51 filament formation during M-phase double-strand break repair. J. Cell Biol., 194, 705-720.
29. Trovesi, C., Falcettoni, M., Lucchini, G., Clerici, M. and Longhese, M.P. (2011) Distinct Cdk1 requirements during single-strand annealing, noncrossover, and crossover recombination. PLoS Genet., 7, e1002263.
30. Pfander, B. and Diffley, J.F. (2011) Dpb11 coordinates Mec1 kinase activation with cell cycle-regulated Rad9 recruitment. EMBO J., 30, 4897-4907.
31. Granata, M., Lazzaro, F., Novarina, D., Panigada, D., Puddu, F., Abreu, C.M., Kumar, R., Grenon, M., Lowndes, N.F., Plevani, P. et al. (2010) Dynamics of Rad9 chromatin binding and checkpoint function are mediated by its dimerization and are cell cycle-regulated by CDK1 activity. PLoS Genet., 6, e1001047.
32. Abreu, C.M., Kumar, R., Hamilton, D., Dawdy, A.W., Creavin, K., Eivers, S., Finn, K., Balsbaugh, J.L., O'Connor, R., Kiely, P.A. et al. (2013) Site-specific phosphorylation of the DNA damage response mediator rad9 by cyclin-dependent kinases regulates activation of checkpoint kinase 1. PLoS Genet., 9, e1003310.
33. Wang, G., Tong, X., Weng, S. and Zhou, H. (2012) Multiple phosphorylation of Rad9 by CDK is required for DNA damage checkpoint activation. Cell Cycle, 11, 3792-3800.
34. Gallo-Fernandez, M., Saugar, I., Ortiz-Bazan, M.A., Vazquez, M.V. and Tercero, J.A. (2012) Cell cycle-dependent regulation of the nuclease activity of Mus81-Eme1/Mms4. Nucleic Acids Res., 40, 8325-8335.
35. Saugar, I., Vazquez, M.V., Gallo-Fernandez, M., Ortiz-Bazan, M.A., Segurado, M., Calzada, A. and Tercero, J.A. (2013) Temporal regulation of the Mus81-Mms4 endonuclease ensures cell survival under conditions of DNA damage. Nucleic Acids Res., 41, 8943-8958.
36. Szakal, B. and Branzei, D. (2013) Premature Cdk1/Cdc5/Mus81 pathway activation induces aberrant replication and deleterious crossover. EMBO J., 32, 1155-1167.
37. Saponaro, M., Callahan, D., Zheng, X., Krejci, L., Haber, J.E., Klein, H.L. and Liberi, G. (2010) Cdk1 targets Srs2 to complete synthesis-dependent strand annealing and to promote recombinational repair. PLoS Genet., 6, e1000858.
38. Dehe, P.M., Coulon, S., Scaglione, S., Shanahan, P., Takedachi, A., Wohlschlegel, J.A., Yates, J.R. 3rd, Llorente, B., Russell, P. and Gaillard, P.H. (2013) Regulation of Mus81-Eme1 Holliday junction resolvase in response to DNA damage. Nat. Struct. Mol. Biol., 20, 598-603.
39. Chen, X., Cui, D., Papusha, A., Zhang, X., Chu, C.D., Tang, J., Chen, K., Pan, X. and Ira, G. (2012) The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature, 489, 576-580.
40. Church, G.M. and Gilbert, W. (1984) Genomic sequencing. Proc. Natl. Acad. Sci. U.S.A., 81, 1991-1995.
41. Vaze, M., Pellicioli, A., Lee, S., Ira, G., Liberi, G., Arbel-Eden, A., Foiani, M. and Haber, J. (2002) Recovery from checkpoint-mediated arrest after repair of a double-strand break requires srs2 helicase. Mol. Cell, 10, 373-385.
42. Costelloe, T., Louge, R., Tomimatsu, N., Mukherjee, B., Martini, E., Khadaroo, B., Dubois, K., Wiegant, W.W., Thierry, A., Burma, S. et al. (2012) The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature, 489, 581-584.
43. Eapen, V.V., Sugawara, N., Tsabar, M., Wu, W.H. and Haber, J.E. (2012) The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation. Mol. Cell. Biol., 32, 4727-4740.
44. Ubersax, J.A., Woodbury, E.L., Quang, P.N., Paraz, M., Blethrow, J.D., Shah, K., Shokat, K.M. and Morgan, D.O. (2003) Targets of the cyclin-dependent kinase Cdk1. Nature, 425, 859-864.
45. Neves-Costa, A., Will, W.R., Vetter, A.T., Miller, J.R. and Varga-Weisz, P. (2009) The SNF2-family member Fun30 promotes gene silencing in heterochromatic loci. PLoS One, 4, e8111.
46. Yu, Q., Zhang, X. and Bi, X. (2011) Roles of chromatin remodeling factors in the formation and maintenance of heterochromatin structure. J. Biol. Chem., 286, 14659-14669.
47. Durand-Dubief, M., Will, W.R., Petrini, E., Theodorou, D., Harris, R.R., Crawford, M.R., Paszkiewicz, K., Krueger, F., Correra, R.M., Vetter, A.T. et al. (2012) SWI/SNF-like chromatin remodeling factor Fun30 supports point centromere function in S. cerevisiae. PLoS Genet., 8, e1002974.
48. Steglich, B., Stralfors, A., Khorosjutina, O., Persson, J., Smialowska, A., Javerzat, J.P. and Ekwall, K. (2015) The Fun30 chromatin remodeler Fft3 controls nuclear organization and chromatin structure of insulators and subtelomeres in fission yeast. PLoS Genet., 11, e1005101.
49. Stralfors, A., Walfridsson, J., Bhuiyan, H. and Ekwall, K. (2011) The FUN30 chromatin remodeler, Fft3, protects centromeric and subtelomeric domains from euchromatin formation. PLoS Genet., 7, e1001334.
50. Rowbotham, S.P., Barki, L., Neves-Costa, A., Santos, F., Dean, W., Hawkes, N., Choudhary, P., Will, W.R., Webster, J., Oxley, D. et al. (2011) Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol. Cell, 42, 285-296.
51. Bishop, A.C., Ubersax, J.A., Petsch, D.T., Matheos, D.P., Gray, N.S., Blethrow, J., Shimizu, E., Tsien, J.Z., Schultz, P.G., Rose, M.D. et al. (2000) A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature, 407, 395-401.
52. Clerici, M., Trovesi, C., Galbiati, A., Lucchini, G. and Longhese, M.P. (2014) Mec1/ATR regulates the generation of single-stranded DNA that attenuates Tel1/ATM signaling at DNA ends. EMBO J., 33, 198-216.
53. Takizawa, C.G. and Morgan, D.O. (2000) Control of mitosis by changes in the subcellular location of cyclin-B1-Cdk1 and Cdc25C. Curr. Opin. Cell Biol., 12, 658-665.
54. Wilmes, G.M., Archambault, V., Austin, R.J., Jacobson, M.D., Bell, S.P. and Cross, F.R. (2004) Interaction of the S-phase cyclin Clb5 with an 'RXL' docking sequence in the initiator protein Orc6 provides an origin-localized replication control switch. Genes Dev., 18, 981-991.
55. Buis, J., Stoneham, T., Spehalski, E. and Ferguson, D.O. (2012) Mre11 regulates CtIP-dependent double-strand break repair by interaction with CDK2. Nat. Struct. Mol. Biol., 19, 246-252.
56. Jirawatnotai, S., Hu, Y., Michowski, W., Elias, J.E., Becks, L., Bienvenu, F., Zagozdzon, A., Goswami, T., Wang, Y.E., Clark, A.B. et al. (2011) A function for cyclin D1 in DNA repair uncovered by protein interactome analyses in human cancers. Nature, 474, 230-234.
57. Enserink, J.M., Hombauer, H., Huang, M.E. and Kolodner, R.D. (2009) Cdc28/Cdk1 positively and negatively affects genome stability in S. cerevisiae. J. Cell Biol., 185, 423-437.
58. Kosugi, S., Hasebe, M., Tomita, M. and Yanagawa, H. (2009) Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. U.S.A., 106, 10171-10176.
59. Lazzaro, F., Sapountzi, V., Granata, M., Pellicioli, A., Vaze, M., Haber, J.E., Plevani, P., Lydall, D. and Muzi-Falconi, M. (2008) Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J., 27, 1502-1512.
60. Panier, S. and Boulton, S.J. (2014) Double-strand break repair: 53BP1 comes into focus. Nat. Rev. Mol. Cell. Biol., 15, 7-18.