The Cohesin Complex Prevents the End Joining of Distant DNA Double-Strand Ends

Molecular Cell

Volumn 61, Issue 1, 2016, Pages 15-26

  Gelot, Camille ^a   Guirouilh Barbat, Josée ^a   Le Guen, Tangui ^a   Dardillac, Elodie ^a   Chailleux, Catherine ^b   Canitrot, Yvan ^b   Lopez, Bernard S ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Cohesin; Double strand break repair; Genome rearrangements; NHEJ; Replication stress

Indexed keywords

COHESIN; DOUBLE STRANDED DNA; PROTEIN; PROTEIN RAD21; SORORIN; UNCLASSIFIED DRUG; CDCA5 PROTEIN, HUMAN; CELL CYCLE PROTEIN; NONHISTONE PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; RAD21 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CHROMOSOME ABERRATION; CHROMOSOME ANALYSIS; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; EXOME; GENOME ANALYSIS; HUMAN; HUMAN CELL; PROTEIN DNA BINDING; SEQUENCE ANALYSIS; CELL LINE; DNA REPAIR; G2 PHASE CELL CYCLE CHECKPOINT; GENE REARRANGEMENT; GENETIC TRANSFECTION; GENETICS; METABOLISM; RNA INTERFERENCE; S PHASE CELL CYCLE CHECKPOINT; TIME FACTOR;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CYCLE PROTEINS; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME ABERRATIONS; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPLICATION; G2 PHASE CELL CYCLE CHECKPOINTS; GENE REARRANGEMENT; HUMANS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; RNA INTERFERENCE; S PHASE CELL CYCLE CHECKPOINTS; TIME FACTORS; TRANSFECTION;

EID: 84953636418     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.11.002     Document Type: Article

References (39)

1. Adamo A., Collis S.J., Adelman C.A., Silva N., Horejsi Z., Ward J.D., Martinez-Perez E., Boulton S.J., La Volpe A. Preventing nonhomologous end joining suppresses DNA repair defects of Fanconi anemia. Mol. Cell 2010, 39:25-35.
2. Atienza J.M., Roth R.B., Rosette C., Smylie K.J., Kammerer S., Rehbock J., Ekblom J., Denissenko M.F. Suppression of RAD21 gene expression decreases cell growth and enhances cytotoxicity of etoposide and bleomycin in human breast cancer cells. Mol. Cancer Ther. 2005, 4:361-368.
3. Bauerschmidt C., Arrichiello C., Burdak-Rothkamm S., Woodcock M., Hill M.A., Stevens D.L., Rothkamm K. Cohesin promotes the repair of ionizing radiation-induced DNA double-strand breaks in replicated chromatin. Nucleic Acids Res. 2010, 38:477-487.
4. Bétermier M., Bertrand P., Lopez B.S. Is non-homologous end-joining really an inherently error-prone process?. PLoS Genet. 2014, 10:e1004086.
5. Caron P., Aymard F., Iacovoni J.S., Briois S., Canitrot Y., Bugler B., Massip L., Losada A., Legube G. Cohesin protects genes against γH2AX induced by DNA double-strand breaks. PLoS Genet. 2012, 8:e1002460.
6. Delacôte F., Lopez B.S. Importance of the cell cycle phase for the choice of the appropriate DSB repair pathway, for genome stability maintenance: the trans-S double-strand break repair model. Cell Cycle 2008, 7:33-38.
7. Deng Z., Wang Z., Stong N., Plasschaert R., Moczan A., Chen H.-S., Hu S., Wikramasinghe P., Davuluri R.V., Bartolomei M.S., et al. A role for CTCF and cohesin in subtelomere chromatin organization, TERRA transcription, and telomere end protection. EMBO J. 2012, 31:4165-4178.
8. Dion V., Kalck V., Seeber A., Schleker T., Gasser S.M. Cohesin and the nucleolus constrain the mobility of spontaneous repair foci. EMBO Rep. 2013, 14:984-991.
9. Enervald E., Du L., Visnes T., Björkman A., Lindgren E., Wincent J., Borck G., Colleaux L., Cormier-Daire V., van Gent D.C., et al. A regulatory role for the cohesin loader NIPBL in nonhomologous end joining during immunoglobulin class switch recombination. J. Exp. Med. 2013, 210:2503-2513.
10. Grabarz A., Barascu A., Guirouilh-Barbat J., Lopez B.S. Initiation of DNA double strand break repair: signaling and single-stranded resection dictate the choice between homologous recombination, non-homologous end-joining and alternative end-joining. Am. J. Cancer Res. 2012, 2:249-268.
11. Guacci V., Koshland D., Strunnikov A. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 1997, 91:47-57.
12. Guirouilh-Barbat J., Huck S., Bertrand P., Pirzio L., Desmaze C., Sabatier L., Lopez B.S. Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells. Mol. Cell 2004, 14:611-623.
13. Guirouilh-Barbat J., Rass E., Plo I., Bertrand P., Lopez B.S. Defects in XRCC4 and KU80 differentially affect the joining of distal nonhomologous ends. Proc. Natl. Acad. Sci. USA 2007, 104:20902-20907.
14. Guirouilh-Barbat J., Huck S., Lopez B.S. S-phase progression stimulates both the mutagenic KU-independent pathway and mutagenic processing of KU-dependent intermediates, for nonhomologous end joining. Oncogene 2008, 27:1726-1736.
15. Guirouilh-Barbat J., Lambert S., Bertrand P., Lopez B.S. Is homologous recombination really an error-free process?. Front. Genet. 2014, 5:175.
16. Jeppsson K., Kanno T., Shirahige K., Sjögren C. The maintenance of chromosome structure: positioning and functioning of SMC complexes. Nat. Rev. Mol. Cell Biol. 2014, 15:601-614.
17. Klein F., Mahr P., Galova M., Buonomo S.B., Michaelis C., Nairz K., Nasmyth K. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 1999, 98:91-103.
18. Kong X., Ball A.R., Pham H.X., Zeng W., Chen H.-Y., Schmiesing J.A., Kim J.S., Berns M., Yokomori K. Distinct functions of human cohesin-SA1 and cohesin-SA2 in double-strand break repair. Mol. Cell. Biol. 2014, 34:685-698.
19. Liang F., Han M., Romanienko P.J., Jasin M. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl. Acad. Sci. USA 1998, 95:5172-5177.
20. Magdalou I., Lopez B.S., Pasero P., Lambert S.A. The causes of replication stress and their consequences on genome stability and cell fate. Semin. Cell Dev. Biol. 2014, 30:154-164.
21. Musio A., Montagna C., Mariani T., Tilenni M., Focarelli M.L., Brait L., Indino E., Benedetti P.A., Chessa L., Albertini A., et al. SMC1 involvement in fragile site expression. Hum. Mol. Genet. 2005, 14:525-533.
22. Oka Y., Suzuki K., Yamauchi M., Mitsutake N., Yamashita S. Recruitment of the cohesin loading factor NIPBL to DNA double-strand breaks depends on MDC1, RNF168 and HP1γ in human cells. Biochem. Biophys. Res. Commun. 2011, 411:762-767.
23. Pace P., Mosedale G., Hodskinson M.R., Rosado I.V., Sivasubramaniam M., Patel K.J. Ku70 corrupts DNA repair in the absence of the Fanconi anemia pathway. Science 2010, 329:219-223.
24. Petersen S., Casellas R., Reina-San-Martin B., Chen H.T., Difilippantonio M.J., Wilson P.C., Hanitsch L., Celeste A., Muramatsu M., Pilch D.R., et al. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 2001, 414:660-665.
25. Potts P.R., Porteus M.H., Yu H. Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J. 2006, 25:3377-3388.
26. Rass E., Grabarz A., Plo I., Gautier J., Bertrand P., Lopez B.S. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol. 2009, 16:819-824.
27. Remeseiro S., Cuadrado A., Losada A. Cohesin in development and disease. Development 2013, 140:3715-3718.
28. Rothkamm K., Krüger I., Thompson L.H., Löbrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 2003, 23:5706-5715.
29. Saintigny Y., Delacôte F., Varès G., Petitot F., Lambert S., Averbeck D., Lopez B.S. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 2001, 20:3861-3870.
30. Schrader C.E., Guikema J.E.J., Linehan E.K., Selsing E., Stavnezer J. Activation-induced cytidine deaminase-dependent DNA breaks in class switch recombination occur during G1 phase of the cell cycle and depend upon mismatch repair. J. Immunol. 2007, 179:6064-6071.
31. Simsek D., Brunet E., Wong S.Y., Katyal S., Gao Y., McKinnon P.J., Lou J., Zhang L., Li J., Rebar E.J., et al. DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet. 2011, 7:e1002080.
32. Sofueva S., Yaffe E., Chan W.-C., Georgopoulou D., Vietri Rudan M., Mira-Bontenbal H., Pollard S.M., Schroth G.P., Tanay A., Hadjur S. Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J. 2013, 32:3119-3129.
33. Soutoglou E., Dorn J.F., Sengupta K., Jasin M., Nussenzweig A., Ried T., Danuser G., Misteli T. Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 2007, 9:675-682.
34. Ström L., Lindroos H.B., Shirahige K., Sjögren C. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell 2004, 16:1003-1015.
35. Thomas-Claudepierre A.-S., Schiavo E., Heyer V., Fournier M., Page A., Robert I., Reina-San-Martin B. The cohesin complex regulates immunoglobulin class switch recombination. J. Exp. Med. 2013, 210:2495-2502.
36. Tittel-Elmer M., Lengronne A., Davidson M.B., Bacal J., François P., Hohl M., Petrini J.H., Pasero P., Cobb J.A. Cohesin association to replication sites depends on rad50 and promotes fork restart. Mol. Cell 2012, 48:98-108.
37. Ünal E., Arbel-Eden A., Sattler U., Shroff R., Lichten M., Haber J.E., Koshland D. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 2004, 16:991-1002.
38. Xie A., Kwok A., Scully R. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. 2009, 16:814-818.
39. Zucman-Rossi J., Legoix P., Victor J.M., Lopez B., Thomas G. Chromosome translocation based on illegitimate recombination in human tumors. Proc. Natl. Acad. Sci. USA 1998, 95:11786-11791.