Signaling from Mus81-Eme2-Dependent DNA Damage Elicited by Chk1 Deficiency Modulates Replication Fork Speed and Origin Usage

Cell Reports

Volumn 14, Issue 5, 2016, Pages 1114-1127

  Técher, Hervé ^a,b,d   Koundrioukoff, Stéphane ^a,b   Carignon, Sandra ^a,b   Wilhelm, Therese ^a,b,e   Millot, Gaël A ^a,b   Lopez, Bernard S ^c   Brison, Olivier ^a,b   Debatisse, Michelle ^a,b  

^a INSTITUT CURIE   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c Gustave Roussy Comprehensive Cancer Institute   (France)

^d FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^e UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; HISTONE H2AX; MRE11 PROTEIN; NUCLEASE; PROTEIN MUS81; PROTEIN P53; UNCLASSIFIED DRUG; ATM PROTEIN; ATR PROTEIN, HUMAN; CHEK1 PROTEIN, HUMAN; DEOXYRIBONUCLEASE; DEOXYRIBONUCLEOSIDE; DNA BINDING PROTEIN; EME2 PROTEIN, HUMAN; ENDONUCLEASE; MRE11A PROTEIN, HUMAN; MUS81 PROTEIN, HUMAN; PROTEIN KINASE;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL CYCLE S PHASE; CELL DIVISION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CELL PROLIFERATION; DEFICIENCY; DNA REPLICATION ORIGIN; METABOLISM; TUMOR CELL LINE;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; CHECKPOINT KINASE 1; DEOXYRIBONUCLEOSIDES; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; HUMANS; PROTEIN KINASES; REPLICATION ORIGIN; SIGNAL TRANSDUCTION;

EID: 84957933027     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.12.093     Document Type: Article

References (64)

1. Aguilera A., Gómez-González B. Genome instability: a mechanistic view of its causes and consequences. Nat. Rev. Genet. 2008, 9:204-217.
2. Alabert C., Bukowski-Wills J.C., Lee S.B., Kustatscher G., Nakamura K., de Lima Alves F., Menard P., Mejlvang J., Rappsilber J., Groth A. Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat. Cell Biol. 2014, 16:281-293.
3. Altmeyer M., Neelsen K.J., Teloni F., Pozdnyakova I., Pellegrino S., Grøfte M., Rask M.B., Streicher W., Jungmichel S., Nielsen M.L., Lukas J. Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose). Nat. Commun. 2015, 6:8088.
4. Beck H., Nähse V., Larsen M.S., Groth P., Clancy T., Lees M., Jørgensen M., Helleday T., Syljuåsen R.G., Sørensen C.S. Regulators of cyclin-dependent kinases are crucial for maintaining genome integrity in S phase. J. Cell Biol. 2010, 188:629-638.
5. Beck H., Nähse-Kumpf V., Larsen M.S., O'Hanlon K.A., Patzke S., Holmberg C., Mejlvang J., Groth A., Nielsen O., Syljuåsen R.G., Sørensen C.S. Cyclin-dependent kinase suppression by WEE1 kinase protects the genome through control of replication initiation and nucleotide consumption. Mol. Cell. Biol. 2012, 32:4226-4236.
6. Bester A.C., Roniger M., Oren Y.S., Im M.M., Sarni D., Chaoat M., Bensimon A., Zamir G., Shewach D.S., Kerem B. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 2011, 145:435-446.
7. Buis J., Stoneham T., Spehalski E., Ferguson D.O. Mre11 regulates CtIP-dependent double-strand break repair by interaction with CDK2. Nat. Struct. Mol. Biol. 2012, 19:246-252.
8. Buisson R., Boisvert J.L., Benes C.H., Zou L. Distinct but concerted roles of ATR, DNA-PK, and Chk1 in countering replication stress during S phase. Mol. Cell 2015, 59:1011-1024.
9. Burrell R.A., McClelland S.E., Endesfelder D., Groth P., Weller M.C., Shaikh N., Domingo E., Kanu N., Dewhurst S.M., Gronroos E., et al. Replication stress links structural and numerical cancer chromosomal instability. Nature 2013, 494:492-496.
10. Chabosseau P., Buhagiar-Labarchède G., Onclercq-Delic R., Lambert S., Debatisse M., Brison O., Amor-Guéret M. Pyrimidine pool imbalance induced by BLM helicase deficiency contributes to genetic instability in Bloom syndrome. Nat. Commun. 2011, 2:368.
11. Choi H.J., Lin J.R., Vannier J.B., Slaats G.G., Kile A.C., Paulsen R.D., Manning D.K., Beier D.R., Giles R.H., Boulton S.J., Cimprich K.A. NEK8 links the ATR-regulated replication stress response and S phase CDK activity to renal ciliopathies. Mol. Cell 2013, 51:423-439.
12. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
13. Couch F.B., Bansbach C.E., Driscoll R., Luzwick J.W., Glick G.G., Bétous R., Carroll C.M., Jung S.Y., Qin J., Cimprich K.A., Cortez D. ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev. 2013, 27:1610-1623.
14. Courbet S., Gay S., Arnoult N., Wronka G., Anglana M., Brison O., Debatisse M. Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 2008, 455:557-560.
15. D'Angiolella V., Donato V., Forrester F.M., Jeong Y.T., Pellacani C., Kudo Y., Saraf A., Florens L., Washburn M.P., Pagano M. Cyclin F-mediated degradation of ribonucleotide reductase M2 controls genome integrity and DNA repair. Cell 2012, 149:1023-1034.
16. Domínguez-Kelly R., Martín Y., Koundrioukoff S., Tanenbaum M.E., Smits V.A., Medema R.H., Debatisse M., Freire R. Wee1 controls genomic stability during replication by regulating the Mus81-Eme1 endonuclease. J. Cell Biol. 2011, 194:567-579.
17. Eykelenboom J.K., Harte E.C., Canavan L., Pastor-Peidro A., Calvo-Asensio I., Llorens-Agost M., Lowndes N.F. ATR activates the S-M checkpoint during unperturbed growth to ensure sufficient replication prior to mitotic onset. Cell Rep. 2013, 5:1095-1107.
18. Forment J.V., Blasius M., Guerini I., Jackson S.P. Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation. PLoS ONE 2011, 6:e23517.
19. Gallo-Fernández M., Saugar I., Ortiz-Bazán M.A., Vázquez M.V., Tercero J.A. Cell cycle-dependent regulation of the nuclease activity of Mus81-Eme1/Mms4. Nucleic Acids Res. 2012, 40:8325-8335.
20. González Besteiro M.A., Gottifredi V. The fork and the kinase: a DNA replication tale from a CHK1 perspective. Mutat. Res. Rev. Mutat. Res. 2015, 763:168-180.
21. Gorrini C., Squatrito M., Luise C., Syed N., Perna D., Wark L., Martinato F., Sardella D., Verrecchia A., Bennett S., et al. Tip60 is a haplo-insufficient tumour suppressor required for an oncogene-induced DNA damage response. Nature 2007, 448:1063-1067.
22. Håkansson P., Hofer A., Thelander L. Regulation of mammalian ribonucleotide reduction and dNTP pools after DNA damage and in resting cells. J. Biol. Chem. 2006, 281:7834-7841.
23. Hu C.M., Yeh M.T., Tsao N., Chen C.W., Gao Q.Z., Chang C.Y., Lee M.H., Fang J.M., Sheu S.Y., Lin C.J., et al. Tumor cells require thymidylate kinase to prevent dUTP incorporation during DNA repair. Cancer Cell 2012, 22:36-50.
24. Huertas P., Jackson S.P. Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem. 2009, 284:9558-9565.
25. Kaidi A., Jackson S.P. KAT5 tyrosine phosphorylation couples chromatin sensing to ATM signalling. Nature 2013, 498:70-74.
26. Katsuno Y., Suzuki A., Sugimura K., Okumura K., Zineldeen D.H., Shimada M., Niida H., Mizuno T., Hanaoka F., Nakanishi M. Cyclin A-Cdk1 regulates the origin firing program in mammalian cells. Proc. Natl. Acad. Sci. USA 2009, 106:3184-3189.
27. Koundrioukoff S., Carignon S., Técher H., Letessier A., Brison O., Debatisse M. Stepwise activation of the ATR signaling pathway upon increasing replication stress impacts fragile site integrity. PLoS Genet. 2013, 9:e1003643.
28. Marheineke K., Hyrien O. Control of replication origin density and firing time in Xenopus egg extracts: role of a caffeine-sensitive, ATR-dependent checkpoint. J. Biol. Chem. 2004, 279:28071-28081.
29. Mathews C.K. Deoxyribonucleotide metabolism, mutagenesis and cancer. Nat. Rev. Cancer 2015, 15:528-539.
30. Mathews C.K., Sinha N.K. Are DNA precursors concentrated at replication sites?. Proc. Natl. Acad. Sci. USA 1982, 79:302-306.
31. Matos J., Blanco M.G., West S.C. Cell-cycle kinases coordinate the resolution of recombination intermediates with chromosome segregation. Cell Rep. 2013, 4:76-86.
32. Maya-Mendoza A., Petermann E., Gillespie D.A., Caldecott K.W., Jackson D.A. Chk1 regulates the density of active replication origins during the vertebrate S phase. EMBO J. 2007, 26:2719-2731.
33. Merrick C.J., Jackson D., Diffley J.F. Visualization of altered replication dynamics after DNA damage in human cells. J. Biol. Chem. 2004, 279:20067-20075.
34. Miotto B., Chibi M., Xie P., Koundrioukoff S., Moolman-Smook H., Pugh D., Debatisse M., He F., Zhang L., Defossez P.A. The RBBP6/ZBTB38/MCM10 axis regulates DNA replication and common fragile site stability. Cell Rep. 2014, 7:575-587.
35. Murfuni I., Basile G., Subramanyam S., Malacaria E., Bignami M., Spies M., Franchitto A., Pichierri P. Survival of the replication checkpoint deficient cells requires MUS81-RAD52 function. PLoS Genet. 2013, 9:e1003910.
36. Niida H., Katsuno Y., Sengoku M., Shimada M., Yukawa M., Ikura M., Ikura T., Kohno K., Shima H., Suzuki H., et al. Essential role of Tip60-dependent recruitment of ribonucleotide reductase at DNA damage sites in DNA repair during G1 phase. Genes Dev. 2010, 24:333-338.
37. Pepe A., West S.C. MUS81-EME2 promotes replication fork restart. Cell Rep. 2014, 7:1048-1055.
38. Petermann E., Helleday T., Caldecott K.W. Claspin promotes normal replication fork rates in human cells. Mol. Biol. Cell 2008, 19:2373-2378.
39. Petermann E., Woodcock M., Helleday T. Chk1 promotes replication fork progression by controlling replication initiation. Proc. Natl. Acad. Sci. USA 2010, 107:16090-16095.
40. Peterson S.E., Li Y., Chait B.T., Gottesman M.E., Baer R., Gautier J. Cdk1 uncouples CtIP-dependent resection and Rad51 filament formation during M-phase double-strand break repair. J. Cell Biol. 2011, 194:705-720.
41. Pontarin G., Fijolek A., Pizzo P., Ferraro P., Rampazzo C., Pozzan T., Thelander L., Reichard P.A., Bianchi V. Ribonucleotide reduction is a cytosolic process in mammalian cells independently of DNA damage. Proc. Natl. Acad. Sci. USA 2008, 105:17801-17806.
42. Saldivar J.C., Miuma S., Bene J., Hosseini S.A., Shibata H., Sun J., Wheeler L.J., Mathews C.K., Huebner K. Initiation of genome instability and preneoplastic processes through loss of Fhit expression. PLoS Genet. 2012, 8:e1003077.
43. Scorah J., McGowan C.H. Claspin and Chk1 regulate replication fork stability by different mechanisms. Cell Cycle 2009, 8:1036-1043.
44. Seiler J.A., Conti C., Syed A., Aladjem M.I., Pommier Y. The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses. Mol. Cell. Biol. 2007, 27:5806-5818.
45. Shechter D., Costanzo V., Gautier J. ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell Biol. 2004, 6:648-655.
46. Sherman P.A., Fyfe J.A. Enzymatic assay for deoxyribonucleoside triphosphates using synthetic oligonucleotides as template primers. Anal. Biochem. 1989, 180:222-226.
47. Shibata A., Moiani D., Arvai A.S., Perry J., Harding S.M., Genois M.M., Maity R., van Rossum-Fikkert S., Kertokalio A., Romoli F., et al. DNA double-strand break repair pathway choice is directed by distinct MRE11 nuclease activities. Mol. Cell 2014, 53:7-18.
48. Shimura T., Toyoshima M., Adiga S.K., Kunoh T., Nagai H., Shimizu N., Inoue M., Niwa O. Suppression of replication fork progression in low-dose-specific p53-dependent S-phase DNA damage checkpoint. Oncogene 2006, 25:5921-5932.
49. Skoog L., Nordenskjöld B. Effects of hydroxyurea and 1-beta-D-arabinofuranosyl-cytosine on deoxyribonucleotide pools in mouse embryo cells. Eur. J. Biochem. 1971, 19:81-89.
50. Sørensen C.S., Syljuåsen R.G., Falck J., Schroeder T., Rönnstrand L., Khanna K.K., Zhou B.B., Bartek J., Lukas J. Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell 2003, 3:247-258.
51. Speroni J., Federico M.B., Mansilla S.F., Soria G., Gottifredi V. Kinase-independent function of checkpoint kinase 1 (Chk1) in the replication of damaged DNA. Proc. Natl. Acad. Sci. USA 2012, 109:7344-7349.
52. Stillman B. Deoxynucleoside triphosphate (dNTP) synthesis and destruction regulate the replication of both cell and virus genomes. Proc. Natl. Acad. Sci. USA 2013, 110:14120-14121.
53. Sun Y., Jiang X., Chen S., Fernandes N., Price B.D. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc. Natl. Acad. Sci. USA 2005, 102:13182-13187.
54. Syljuåsen R.G., Sørensen C.S., Hansen L.T., Fugger K., Lundin C., Johansson F., Helleday T., Sehested M., Lukas J., Bartek J. Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol. Cell. Biol. 2005, 25:3553-3562.
55. Tanaka H., Arakawa H., Yamaguchi T., Shiraishi K., Fukuda S., Matsui K., Takei Y., Nakamura Y. A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature 2000, 404:42-49.
56. Taricani L., Shanahan F., Malinao M.C., Beaumont M., Parry D. A functional approach reveals a genetic and physical interaction between ribonucleotide reductase and CHK1 in mammalian cells. PLoS ONE 2014, 9:e111714.
57. Técher H., Koundrioukoff S., Azar D., Wilhelm T., Carignon S., Brison O., Debatisse M., Le Tallec B. Replication dynamics: biases and robustness of DNA fiber analysis. J. Mol. Biol. 2013, 425:4845-4855.
58. Thompson R., Montano R., Eastman A. The Mre11 nuclease is critical for the sensitivity of cells to Chk1 inhibition. PLoS ONE 2012, 7:e44021.
59. Toledo L.I., Altmeyer M., Rask M.B., Lukas C., Larsen D.H., Povlsen L.K., Bekker-Jensen S., Mailand N., Bartek J., Lukas J. ATR prohibits replication catastrophe by preventing global exhaustion of RPA. Cell 2013, 155:1088-1103.
60. Wilhelm T., Magdalou I., Barascu A., Técher H., Debatisse M., Lopez B.S. Spontaneous slow replication fork progression elicits mitosis alterations in homologous recombination-deficient mammalian cells. Proc. Natl. Acad. Sci. USA 2014, 111:763-768.
61. Yekezare M., Gómez-González B., Diffley J.F. Controlling DNA replication origins in response to DNA damage - inhibit globally, activate locally. J. Cell Sci. 2013, 126:1297-1306.
62. Zeman M.K., Cimprich K.A. Causes and consequences of replication stress. Nat. Cell Biol. 2014, 16:2-9.
63. Zhang Y.W., Jones T.L., Martin S.E., Caplen N.J., Pommier Y. Implication of checkpoint kinase-dependent up-regulation of ribonucleotide reductase R2 in DNA damage response. J. Biol. Chem. 2009, 284:18085-18095.
64. Zhao H., Watkins J.L., Piwnica-Worms H. Disruption of the checkpoint kinase 1/cell division cycle 25A pathway abrogates ionizing radiation-induced S and G2 checkpoints. Proc. Natl. Acad. Sci. USA 2002, 99:14795-14800.