Increased sister chromatid cohesion and DNA damage response factor localization at an enzyme-induced DNA double-strand break in vertebrate cells

Nucleic Acids Research

Volumn 37, Issue 18, 2009, Pages 6054-6063

  Dodson, Helen ^a   Morrison, Ciaran G ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CELL PROTEIN; COHESIN; ENDONUCLEASE; GREEN FLUORESCENT PROTEIN; KU ANTIGEN; PROTEIN TET; RAD51 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL KINETICS; CHICKEN; CONTROLLED STUDY; CYTOGENETICS; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; SISTER CHROMATID;

ANIMALS; ANTIGENS, NUCLEAR; CELL CYCLE PROTEINS; CELL LINE; CHICKENS; CHROMATIDS; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; HISTONES; HUMANS; OVALBUMIN; PROTEIN-SERINE-THREONINE KINASES; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE PROTEINS; TUMOR SUPPRESSOR PROTEINS;

VERTEBRATA;

EID: 70350674207     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp684     Document Type: Article

References (43)

1. Khanna,K.K. and Jackson,S.P. (2001) DNA double-strand breaks: Signaling, repair and the cancer connection. Nat. Genet., 27, 247-254.
2. Jackson,S.P. (2002) Sensing and repairing DNA double-strand breaks. Carcinogenesis, 23, 687-696.
3. Shiloh,Y. (2003) ATM and related protein kinases: Safeguarding genome integrity. Nat. Rev. Cancer, 3, 155-168.
4. Zhou,B.B. and Elledge,S.J. (2000) The DNA damage response: Putting checkpoints in perspective. Nature, 408, 433-439.
5. Lavin,M.F. (2007) ATM and the Mre11 complex combine to recognize and signal DNA double-strand breaks. Oncogene, 26, 7749-7758.
6. DiTullio,R.A. Jr, Mochan,T.A., Venere,M., Bartkova,J., Sehested,M., Bartek,J. and Halazonetis,T.D. (2002) 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol., 4, 998-1002.
7. Rogakou,E.P., Boon,C., Redon,C. and Bonner,W.M. (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol., 146, 905-916.
8. Stucki,M., Clapperton,J.A., Mohammad,D., Yaffe,M.B., Smerdon,S.J. and Jackson,S.P. (2005) MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell, 123, 1213-1226.
9. Kim,J.S., Krasieva,T.B., LaMorte,V., Taylor,A.M. and Yokomori,K. (2002) Specific recruitment of human cohesin to laser-induced DNA damage. J. Biol. Chem., 277, 45149-45153.
10. Strom,L., Lindroos,H.B., Shirahige,K. and Sjogren,C. (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell, 16, 1003-1015.
11. Unal,E., Arbel-Eden,A., Sattler,U., Shroff,R., Lichten,M., Haber,J.E. and Koshland,D. (2004) DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell, 16, 991-1002.
12. Haaf,T., Golub,E.I., Reddy,G., Radding,C.M. and Ward,D.C. (1995) Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl Acad. Sci. USA, 92, 2298-2302.
13. Maser,R.S., Monsen,K.J., Nelms,B.E. and Petrini,J.H. (1997) hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol. Cell Biol., 17, 6087-6096.
14. Nelms,B.E., Maser,R.S., MacKay,J.F., Lagally,M.G. and Petrini,J.H. (1998) In situ visualization of DNA double-strand break repair in human fibroblasts. Science, 280, 590-592.
15. Lukas,C., Falck,J., Bartkova,J., Bartek,J. and Lukas,J. (2003) Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol., 5, 255-260.
16. Paques,F. and Haber,J.E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 63, 349-404.
17. Richardson,C., Moynahan,M.E. and Jasin,M. (1998) Double-strand break repair by interchromosomal recombination: Suppression of chromosomal translocations. Genes Dev., 12, 3831-3842.
18. Rodrigue,A., Lafrance,M., Gauthier,M.C., McDonald,D., Hendzel,M., West,S.C., Jasin,M. and Masson,J.Y. (2006) Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J., 25, 222-231.
19. Berkovich,E., Monnat,R.J. Jr. and Kastan,M.B. (2007) Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol., 9, 683-690.
20. Soutoglou,E., Dorn,J.F., Sengupta,K., Jasin,M., Nussenzweig,A., Ried,T., Danuser,G. and Misteli,T. (2007) Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol., 9, 675-682.
21. Michaelis,C., Ciosk,R. and Nasmyth,K. (1997) Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35-45.
22. Buerstedde,J.M. and Takeda,S. (1991) Increased ratio of targeted to random integration after transfection of chicken B cell lines. Cell 67, 179-188.
23. Takata,M., Sasaki,M.S., Sonoda,E., Morrison,C., Hashimoto,M., Utsumi,H., Yamaguchi-Iwai,Y., Shinohara,A. and Takeda,S. (1998) Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J., 17, 5497-5508.
24. Morrison,C., Sonoda,E., Takao,N., Shinohara,A., Yamamoto,K. and Takeda,S. (2000) The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J., 19, 463-471.
25. Sonoda,E., Zhao,G.Y., Kohzaki,M., Dhar,P.K., Kikuchi,K., Redon,C., Pilch,D.R., Bonner,W.M., Nakano,A., Watanabe,M. et al. (2007) Collaborative roles of gammaH2AX and the Rad51 paralog Xrcc3 in homologous recombinational repair. DNA Repair (Amst), 6, 280-292.
26. Dodson,H., Bourke,E., Jeffers,L.J., Vagnarelli,P., Sonoda,E., Takeda,S., Earnshaw,W.C., Merdes,A. and Morrison,C. (2004) Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. EMBO J., 23, 3864-3873.
27. Schultz,L.B., Chehab,N.H., Malikzay,A. and Halazonetis,T.D. (2000) p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol., 151, 1381-1390.
28. 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.
29. Walker,M., Black,E.J., Oehler,V., Gillespie,D.A. and Scott,M.T. (2009) Chk1 C-terminal regulatory phosphorylation mediates checkpoint activation by de-repression of Chk1 catalytic activity. Oncogene, 28, 2314-2323.
30. Paull,T.T., Rogakou,E.P., Yamazaki,V., Kirchgessner,C.U., Gellert,M. and Bonner,W.M. (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol., 10, 886-895.
31. Sonoda,E., Matsusaka,T., Morrison,C., Vagnarelli,P., Hoshi,O., Ushiki,T., Nojima,K., Fukagawa,T., Waizenegger,I.C., Peters,J.M. et al. (2001) Scc1/Rad21/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells. Dev. Cell, 1, 759-770.
32. Sjogren,C. and Nasmyth,K. (2001) Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr. Biol., 11, 991-995.
33. Strom,L., Karlsson,C., Lindroos,H.B., Wedahl,S., Katou,Y., Shirahige,K. and Sjogren,C. (2007) Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science, 317, 242-245.
34. Unal,E., Heidinger-Pauli,J.M. and Koshland,D. (2007) DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science, 317, 245-248.
35. Deckbar,D., Birraux,J., Krempler,A., Tchouandong,L., Beucher,A., Walker,S., Stiff,T., Jeggo,P. and Lobrich,M. (2007) Chromosome breakage after G2 checkpoint release. J. Cell Biol., 176, 749-755.
36. Heidinger-Pauli,J.M., Unal,E., Guacci,V. and Koshland,D. (2008) The kleisin subunit of cohesin dictates damage-induced cohesion. Mol. Cell, 31, 47-56.
37. Kim,S.T., Xu,B. and Kastan,M.B. (2002) Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev., 16, 560-570.
38. Yazdi,P.T., Wang,Y., Zhao,S., Patel,N., Lee,E.Y. and Qin,J. (2002) SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev., 16, 571-582.
39. Rogakou,E.P., Pilch,D.R., Orr,A.H., Ivanova,V.S. and Bonner,W.M. (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem., 273, 5858-5868.
40. Stiff,T., O'Driscoll,M., Rief,N., Iwabuchi,K., Lobrich,M. and Jeggo,P.A. (2004) ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res., 64, 2390-2396.
41. Burma,S., Chen,B.P., Murphy,M., Kurimasa,A. and Chen,D.J. (2001) ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem., 276, 42462-42467.
42. Celeste,A., Fernandez-Capetillo,O., Kruhlak,M.J., Pilch,D.R., Staudt,D.W., Lee,A., Bonner,R.F., Bonner,W.M. and Nussenzweig,A. (2003) Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol., 5, 675-679.
43. Celeste,A., Petersen,S., Romanienko,P.J., Fernandez-Capetillo,O., Chen,H.T., Sedelnikova,O.A., Reina-San-Martin,B., Coppola,V., Meffre,E., Difilippantonio,M.J. et al. (2002) Genomic instability in mice lacking histone H2AX. Science, 296, 922-927.