Cohesin and the nucleolus constrain the mobility of spontaneous repair foci

EMBO Reports

Volumn 14, Issue 11, 2013, Pages 984-991

  Dion, Vincent ^a   Kalck, Véronique ^a   Seeber, Andrew ^a,b   Schleker, Thomas ^a,c   Gasser, Susan M ^a,b  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c St Elisabeth Straubing GmbH   (Germany)

Author keywords

chromatin dynamics; cohesin; DNA damage; nucleolus; Rad52 foci

Indexed keywords

COHESIN; RAD52 PROTEIN;

ARTICLE; CELL CYCLE S PHASE; CHROMATIN; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; YEAST;

CELL CYCLE PROTEINS; CELL NUCLEOLUS; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA DAMAGE; DNA REPAIR; HOMOLOGOUS RECOMBINATION; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84887064569     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/embor.2013.142     Document Type: Article

References (37)

1. Alt FW, Zhang Y, Meng FL, Guo C, Schwer B (2013) Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell 152: 417-429
2. Gehlen LR, Gasser SM, Dion V (2011) How broken DNA finds its template for repair: a computational approach. Prog Theoret Physics Suppl 191: 20-29
3. Heyer WD, Ehmsen KT, Liu J (2010) Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44: 113-139
4. Finn K, Lowndes NF, Grenon M (2012) Eukaryotic DNA damage checkpoint activation in response to double-strand breaks. Cell Mol Life Sci 69: 1447-1473
5. Lisby M, Barlow JH, Burgess RC, Rothstein R (2004) Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118: 699-713
6. Mine-Hattab J, Rothstein R (2012) Increased chromosome mobility facilitates homology search during recombination. Nat Cell Biol 14: 510-517
7. Lisby M, Rothstein R, Mortensen UH (2001) Rad52 forms DNA repair and recombination centers during S phase. Proc Natl Acad Sci USA 98: 8276-8282
8. Dion V, Kalck V, Horigome C, Towbin BD, Gasser SM (2012) Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery. Nat Cell Biol 14: 502-509
9. Neumann FR, Dion V, Gehlen LR, Tsai-Pflugfelder M, Schmid R, Taddei A, Gasser SM (2012) Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Genes Dev 26: 369-383
10. Agmon N, Liefshitz B, Zimmer C, Fabre E, Kupiec M (2013) Effect of nuclear architecture on the efficiency of double-strand break repair. Nat Cell Biol 15: 694-699
11. Torres-Rosell J et al (2007) The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat Cell Biol 9: 923-931
12. Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144: 732-744
13. Jakob B, Splinter J, Conrad S, Voss KO, Zink D, Durante M, Lobrich M, Taucher-Scholz G (2011) DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res 39: 6489-6499
14. Nagai S et al (2008) Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322: 597-602
15. Dion V, Gasser SM (2013) Chromatin movement in the maintenance of genome stability. Cell 152: 1355-1364
16. Nielsen I, Bentsen IB, Lisby M, Hansen S, Mundbjerg K, Andersen AH, Bjergbaek L (2009) A Flp-nick system to study repair of a single protein-bound nick in vivo. Nat Methods 6: 753-757
17. Gonzalez-Prieto R, Munoz-Cabello AM, Cabello-Lobato MJ, Prado F (2013) Rad51 replication fork recruitment is required for DNA damage tolerance. EMBO J 32: 1307-1321
18. Oza P, Jaspersen SL, Miele A, Dekker J, Peterson CL (2009) Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev 23: 912-927
19. Bystricky K, Van Attikum H, Montiel MD, Dion V, Gehlen L, Gasser SM (2009) Regulation of nuclear positioning and dynamics of the silent mating type loci by the yeast Ku70/Ku80 complex. Mol Cell Biol 29: 835-848
20. Povirk LF (1996) DNA damage and mutagenesis by radiomimetic DNA-cleaving agents: bleomycin, neocarzinostatin and other enediynes. Mutat Res 355: 71-89
21. Fung CW, Mozlin AM, Symington LS (2009) Suppression of the double-strand-break-repair defect of the Saccharomyces cerevisiae rad57 mutant. Genetics 181: 1195-1206
22. Lobachev K, Vitriol E, Stemple J, Resnick MA, Bloom K (2004) Chromosome fragmentation after induction of a double-strand break is an active process prevented by the RMX repair complex. Curr Biol 14: 2107-2112
23. Kaye JA, Melo JA, Cheung SK, Vaze MB, Haber JE, Toczyski DP (2004) DNA breaks promote genomic instability by impeding proper chromosome segregation. Curr Biol 14: 2096-2106
24. Heun P, Laroche T, Shimada K, Furrer P, Gasser SM (2001) Chromosome dynamics in the yeast interphase nucleus. Science 294: 2181-2186
25. Heun P, Laroche T, Raghuraman MK, Gasser SM (2001) The positioning and dynamics of origins of replication in the budding yeast nucleus. J Cell Biol 152: 385-400
26. Meister P, Gehlen LR, Varela E, Kalck V, Gasser SM (2010) Visualizing yeast chromosomes and nuclear architecture. Methods Enzymol 470: 535-567
27. Chubb JR, Boyle S, Perry P, Bickmore WA (2002) Chromatin motion is constrained by association with nuclear compartments in human cells. Curr Biol 12: 439-445
28. Johzuka K, Horiuchi T (2009) The cis element and factors required for condensin recruitment to chromosomes. Mol Cell 34: 26-35
29. Nasmyth K, Haering CH (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43: 525-558
30. Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K (2000) Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103: 375-386
31. Lopez-Serra L, Lengronne A, Borges V, Kelly G, Uhlmann F (2013) Budding yeast Wapl controls sister chromatid cohesion maintenance and chromosome condensation. Curr Biol 23: 64-69
32. Mayer ML et al (2004) Identification of protein complexes required for efficient sister chromatid cohesion. Mol Biol Cell 15: 1736-1745
33. Tittel-Elmer M, Lengronne A, Davidson MB, Bacal J, Francois P, Hohl M, Petrini JH, Pasero P, Cobb JA (2012) Cohesin association to replication sites depends on rad50 and promotes fork restart. Mol Cell 48: 98-108
34. De Piccoli G et al (2006) Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat Cell Biol 8: 1032-1034
35. Cortes-Ledesma F, Aguilera A (2006) Double-strand breaks arising by replication through a nick are repaired by cohesin-dependent sister-chromatid exchange. EMBO Rep 7: 919-926
36. Wurtele H et al (2012) Histone H3 lysine 56 acetylation and the response to DNA replication fork damage. Mol Cell Biol 32: 154-172
37. Munoz-Galvan S, Jimeno S, Rothstein R, Aguilera A (2013) Histone H3K56 acetylation, Rad52, and non-DNA repair factors control double-strand break repair choice with the sister chromatid. PLoS Genet 9: e1003237