Polo-like kinase 1 mediates BRCA1 phosphorylation and recruitment at DNA double-strand breaks

Oncotarget

Volumn 7, Issue 3, 2016, Pages 2269-2283

  Chabalier Taste, Corinne ^b   Brichese, Laetitia ^b   Racca, Carine ^a,b   Canitrot, Yvan ^b,c   Calsou, Patrick ^a,b,d   Larminat, Florence ^a,b  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c Laboratoire de Biologie Cellulaire et Moleculaire du Controle de la Proliferation   (France)

^d Equipe 'Labellisée LA LIGUE CONTRE LE CANCER 2013'   (France)

Author keywords

BRCA1; Chromosome Section; DNA double strand break; Homologous recombination; Plk1; Rad51

Indexed keywords

BRCA1 PROTEIN; POLO LIKE KINASE 1; SERINE; BRCA1 PROTEIN, HUMAN; CELL CYCLE PROTEIN; DNA; DNA BINDING PROTEIN; ONCOPROTEIN; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INHIBITION KINETICS; IONIZING RADIATION; MUTATIONAL ANALYSIS; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; DNA REPLICATION; GENETICS; HELA CELL LINE; MCF-7 CELL LINE; METABOLISM; MUTATION; PHOSPHORYLATION; TUMOR CELL LINE;

BRCA1 PROTEIN; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; HELA CELLS; HOMOLOGOUS RECOMBINATION; HUMANS; MCF-7 CELLS; MUTATION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RADIATION, IONIZING;

EID: 84962269049     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6825     Document Type: Article

References (57)

1. Barr FA, Sillje HH and Nigg EA. Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol. 2004; 5:429-440.
2. van Vugt MA and Medema RH. Getting in and out of mitosis with Polo-like kinase-1. Oncogene. 2005; 24:2844-2859.
3. Lowery DM, Clauser KR, Hjerrild M, Lim D, Alexander J, Kishi K, Ong SE, Gammeltoft S, Carr SA and Yaffe MB. Proteomic screen defines the Polo-box domain interactome and identifies Rock2 as a Plk1 substrate. Embo J. 2007; 26:2262-2273.
4. Elia AE, Rellos P, Haire LF, Chao JW, Ivins FJ, Hoepker K, Mohammad D, Cantley LC, Smerdon SJ and Yaffe MB. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell. 2003; 115:83-95.
5. Strebhardt K and Ullrich A. Targeting polo-like kinase 1 for cancer therapy. Nat Rev Cancer. 2006; 6:321-330.
6. Louwen F and Yuan J. Battle of the eternal rivals: restoring functional p53 and inhibiting Polo-like kinase 1 as cancer therapy. Oncotarget. 2013; 4:958-971. doi: 10.18632/oncotarget.1096.
7. Benada J, Burdova K, Lidak T, von Morgen P and Macurek L. Polo-like kinase 1 inhibits DNA damage response during mitosis. Cell Cycle. 2015; 14:219-231.
8. Song B, Liu XS, Davis K and Liu X. Plk1 phosphorylation of Orc2 promotes DNA replication under conditions of stress. Mol Cell Biol. 2011; 31:4844-4856.
9. Macurek L, Lindqvist A, Lim D, Lampson MA, Klompmaker R, Freire R, Clouin C, Taylor SS, Yaffe MB and Medema RH. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature. 2008; 455:119-123.
10. Yata K, Lloyd J, Maslen S, Bleuyard JY, Skehel M, Smerdon SJ and Esashi F. Plk1 and CK2 act in concert to regulate Rad51 during DNA double strand break repair. Mol Cell. 2012; 45:371-383.
11. Moynahan ME and Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol. 2010; 11:196-207.
12. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J and Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol. 2006; 173:195-206.
13. Wyman C and Kanaar R. DNA double-strand break repair: all's well that ends well. Annu Rev Genet. 2006; 40:363-383.
14. Cao L, Xu X, Bunting SF, Liu J, Wang RH, Cao LL, Wu JJ, Peng TN, Chen J, Nussenzweig A, Deng CX and Finkel T. A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency. Mol Cell. 2009; 35(4):534-541.
15. Chapman JR, Sossick AJ, Boulton SJ and Jackson SP. BRCA1-associated exclusion of 53BP1 from DNA damage sites underlies temporal control of DNA repair. J Cell Sci. 2012; 125(Pt 15):3529-3534.
16. Cruz-Garcia A, Lopez-Saavedra A and Huertas P. BRCA1 accelerates CtIP-mediated DNA-end resection. Cell Rep. 2014; 9:451-459.
17. Bhattacharyya A, Ear US, Koller BH, Weichselbaum RR and Bishop DK. The breast cancer susceptibility gene BRCA1 is required for subnuclear assembly of Rad51 and survival following treatment with the DNA cross-linking agent cisplatin. J Biol Chem. 2000; 275:23899-23903.
18. Moynahan ME, Chiu JW, Koller BH and Jasin M. Brca1 controls homology-directed DNA repair. Mol Cell. 1999; 4:511-518.
19. Bunting SF and Nussenzweig A. End-joining, translocations and cancer. Nat Rev Cancer. 2013; 13:443-454.
20. Cortez D, Wang Y, Qin J and Elledge SJ. Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science. 1999; 286:1162-1166.
21. Lee JS, Collins KM, Brown AL, Lee CH and Chung JH. hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature. 2000; 404:201-204.
22. Johnson N, Li YC, Walton ZE, Cheng KA, Li D, Rodig SJ, Moreau LA, Unitt C, Bronson RT, Thomas HD, Newell DR, D'Andrea AD, Curtin NJ, Wong KK and Shapiro GI. Compromised CDK1 activity sensitizes BRCA-proficient cancers to PARP inhibition. Nat Med. 2011; 17:875-882.
23. Lenart P, Petronczki M, Steegmaier M, Di Fiore B, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N and Peters JM. The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr Biol. 2007; 17:304-315.
24. Rothkamm K, Kruger I, Thompson LH and Lobrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol. 2003; 23:5706-5715.
25. Stark JM, Pierce AJ, Oh J, Pastink A and Jasin M. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol Cell Biol. 2004; 24:9305-9316.
26. Bennardo N, Cheng A, Huang N and Stark JM. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 2008; 4:e1000110.
27. Puget N, Knowlton M and Scully R. Molecular analysis of sister chromatid recombination in mammalian cells. DNA Repair (Amst). 2005; 4:149-161.
28. Scully R, Ganesan S, Vlasakova K, Chen J, Socolovsky M and Livingston DM. Genetic analysis of BRCA1 function in a defined tumor cell line. Mol Cell. 1999; 4:1093-1099.
29. Zein N, Sinha AM, McGahren WJ and Ellestad GA. Calicheamicin gamma 1I: an antitumor antibiotic that cleaves double-stranded DNA site specifically. Science. 1988; 240:1198-1201.
30. Elmroth K, Nygren J, Martensson S, Ismail IH and Hammarsten O. Cleavage of cellular DNA by calicheamicin gamma1. DNA Repair (Amst). 2003; 2:363-374.
31. Scully R, Chen J, Ochs RL, Keegan K, Hoekstra M, Feunteun J and Livingston DM. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell. 1997; 90:425-435.
32. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M and Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol. 2000; 10:886-895.
33. Zou J, Rezvani K, Wang H, Lee KS and Zhang D. BRCA1 downregulates the kinase activity of Polo-like kinase 1 in response to replication stress. Cell Cycle. 2013; 12:2255-2265.
34. Park JE, Soung NK, Johmura Y, Kang YH, Liao C, Lee KH, Park CH, Nicklaus MC and Lee KS. Polo-box domain: a versatile mediator of polo-like kinase function. Cell Mol Life Sci. 2010; 67:1957-1970.
35. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, Carotenuto W, Liberi G, Bressan D, Wan L, Hollingsworth NM, Haber JE and Foiani M. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature. 2004; 431:1011-1017.
36. Johnson N, Cai D, Kennedy RD, Pathania S, Arora M, Li YC, D'Andrea AD, Parvin JD and Shapiro GI. Cdk1 participates in BRCA1-dependent S phase checkpoint control in response to DNA damage. Mol Cell. 2009; 35:327-339.
37. Vassilev LT, Tovar C, Chen S, Knezevic D, Zhao X, Sun H, Heimbrook DC and Chen L. Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci U S A. 2006; 103:10660-10665.
38. Alexander J, Lim D, Joughin BA, Hegemann B, Hutchins JR, Ehrenberger T, Ivins F, Sessa F, Hudecz O, Nigg EA, Fry AM, Musacchio A, Stukenberg PT, Mechtler K, Peters JM, Smerdon SJ, et al. Spatial exclusivity combined with positive and negative selection of phosphorylation motifs is the basis for context-dependent mitotic signaling. Sci Signal. 2011; 4:ra42.
39. Hamanaka R, Smith MR, O'Connor PM, Maloid S, Mihalic K, Spivak JL, Longo DL and Ferris DK. Polo-like kinase is a cell cycle-regulated kinase activated during mitosis. J Biol Chem. 1995; 270:21086-21091.
40. Scully R, Chen J, Plug A, Xiao Y, Weaver D, Feunteun J, Ashley T and Livingston DM. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell. 1997; 88:265-275.
41. Tomlinson GE, Chen TT, Stastny VA, Virmani AK, Spillman MA, Tonk V, Blum JL, Schneider NR, Wistuba, II, Shay JW, Minna JD and Gazdar AF. Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res. 1998; 58:3237-3242.
42. Lee KS, Grenfell TZ, Yarm FR and Erikson RL. Mutation of the polo-box disrupts localization and mitotic functions of the mammalian polo kinase Plk. Proc Natl Acad Sci U S A. 1998; 95:9301-9306.
43. Greenberg RA, Sobhian B, Pathania S, Cantor SB, Nakatani Y and Livingston DM. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev. 2006; 20:34-46.
44. Zhang F, Ma J, Wu J, Ye L, Cai H, Xia B and Yu X. PALB2 links BRCA1 and BRCA2 in the DNA-damage response. Curr Biol. 2009; 19:524-529.
45. Sy SM, Huen MS and Chen J. PALB2 is an integral component of the BRCA complex required for homologous recombination repair. Proc Natl Acad Sci U S A. 2009; 106:7155-7160.
46. Yata K, Bleuyard JY, Nakato R, Ralf C, Katou Y, Schwab RA, Niedzwiedz W, Shirahige K and Esashi F. BRCA2 coordinates the activities of cell-cycle kinases to promote genome stability. Cell Rep. 2014; 7:1547-1559.
47. Sharma K, D'Souza RC, Tyanova S, Schaab C, Wisniewski JR, Cox J and Mann M. Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Rep. 2014; 8:1583-1594.
48. Caligo MA, Bonatti F, Guidugli L, Aretini P and Galli A. A yeast recombination assay to characterize human BRCA1 missense variants of unknown pathological significance. Hum Mutat. 2009; 30:123-133.
49. D'Argenio V, Esposito MV, Telese A, Precone V, Starnone F, Nunziato M, Cantiello P, Iorio M, Evangelista E, D'Aiuto M, Calabrese A, Frisso G, D'Aiuto G and Salvatore F. The molecular analysis of BRCA1 and BRCA2: Next-generation sequencing supersedes conventional approaches. Clin Chim Acta. 2015; 446:221-225.
50. Kumar P, HenikoffS and Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc. 2009; 4:1073-1081.
51. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS and Sunyaev SR. A method and server for predicting damaging missense mutations. Nat Methods. 2010; 7:248-249.
52. Rodel F, Keppner S, Capalbo G, Bashary R, Kaufmann M, Rodel C, Strebhardt K and Spankuch B. Polo-like kinase 1 as predictive marker and therapeutic target for radiotherapy in rectal cancer. Am J Pathol. 2010; 177:918-929.
53. Lund-Andersen C, Patzke S, Nahse-Kumpf V and Syljuasen RG. PLK1-inhibition can cause radiosensitization or radioresistance dependent on the treatment schedule. Radiother Oncol. 2014; 110:355-361.
54. Gunn A and Stark JM. I-SceI-based assays to examine distinct repair outcomes of mammalian chromosomal double strand breaks. Methods Mol Biol. 2012; 920:379-391.
55. Chabalier-Taste C, Racca C, Dozier C and Larminat F. BRCA1 is regulated by Chk2 in response to spindle damage. Biochim Biophys Acta. 2008; 1783:2223-2233.
56. Courilleau C, Chailleux C, Jauneau A, Grimal F, Briois S, Boutet-Robinet E, Boudsocq F, Trouche D and Canitrot Y. The chromatin remodeler p400 ATPase facilitates Rad51-mediated repair of DNA double-strand breaks. J Cell Biol. 2012; 199:1067-1081.
57. Di Paolo A, Racca C, Calsou P and Larminat F. Loss of BRCA1 impairs centromeric cohesion and triggers chromosomal instability. Faseb J. 2014; 28:5250-5261.