DNA Dynamics during Early Double-Strand Break Processing Revealed by Non-Intrusive Imaging of Living Cells

PLoS Genetics

Volumn 10, Issue 3, 2014, Pages

  Saad, Hicham ^a,b   Gallardo, Franck ^a,b,c   Dalvai, Mathieu ^a,b   Tanguy le Gac, Nicolas ^a,d   Lane, David ^a,b   Bystricky, Kerstin ^a,b,c  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b CNRS   (France)

^c UPS   (France)

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

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BINDING SITE; CELL FUNCTION; CHROMATIN; CONTROLLED STUDY; DNA STRUCTURE; DOUBLE STRANDED DNA BREAK; GENE FUNCTION; GENE LOCUS; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULAR MECHANICS; NONHUMAN; OLIGOMERIZATION; PROTEIN BINDING; RECOMBINATION REPAIR; SACCHAROMYCES CEREVISIAE; CHROMOSOME; DNA DAMAGE; DNA REPAIR; FUNGAL GENOME; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM;

CHROMATIN; DNA BINDING PROTEIN;

CHROMATIN; CHROMOSOMES, FUNGAL; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; GENOME, FUNGAL; HOMOLOGOUS RECOMBINATION; SACCHAROMYCES CEREVISIAE;

EID: 84897424193     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004187     Document Type: Article

References (70)

1. Milne GT, Jin S, Shannon KB, Weaver DT, (1996) Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol Cell Biol 16: 4189-4198.
2. Ivankovic S, Dermic D, (2012) DNA end resection controls the balance between homologous and illegitimate recombination in Escherichia coli. PLoS One 7: e39030.
3. Krogh BO, Symington LS, (2004) Recombination proteins in yeast. Annu Rev Genet 38: 233-271.
4. Huertas P, (2010) DNA resection in eukaryotes: deciding how to fix the break. Nat Struct Mol Biol 17: 11-16.
5. Mimitou EP, Symington LS, (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455: 770-774.
6. Symington LS, Gautier J, (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45: 247-271.
7. Lisby M, Rothstein R, Mortensen UH, (2001) Rad52 forms DNA repair and recombination centers during S phase. Proc Natl Acad Sci U S A 98: 8276-8282.
8. Nagai S, Dubrana K, Tsai-Pflugfelder M, Davidson MB, Roberts TM, et al. (2008) Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322: 597-602.
9. 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.
10. Lisby M, Mortensen UH, Rothstein R, (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 5: 572-577.
11. Hicks WM, Yamaguchi M, Haber JE, (2011) Real-time analysis of double-strand DNA break repair by homologous recombination. Proc Natl Acad Sci U S A 108: 3108-3115.
12. Jiang L, Nagai H, Ohara H, Hara S, Tachibana M, et al. (2008) Characteristics and modifying factors of asbestos-induced oxidative DNA damage. Cancer Sci 99: 2142-2151.
13. 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.
14. Mine-Hattab J, Rothstein R, (2012) Increased chromosome mobility facilitates homology search during recombination. Nat Cell Biol 14: 510-517.
15. Houston PL, Broach JR, (2006) The dynamics of homologous pairing during mating type interconversion in budding yeast. PLoS Genet 2: e98.
16. Michaelis C, Ciosk R, Nasmyth K, (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91: 35-45.
17. Fuchs J, Lorenz A, Loidl J, (2002) Chromosome associations in budding yeast caused by integrated tandemly repeated transgenes. J Cell Sci 115: 1213-1220.
18. Lassadi I, Bystricky K, (2011) Tracking of single and multiple genomic loci in living yeast cells. Methods Mol Biol 745: 499-522.
19. Straight AF, Belmont AS, Robinett CC, Murray AW, (1996) GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol 6: 1599-1608.
20. Possoz C, Filipe SR, Grainge I, Sherratt DJ, (2006) Tracking of controlled Escherichia coli replication fork stalling and restart at repressor-bound DNA in vivo. Embo J 25: 2596-2604.
21. Sofueva S, Osman F, Lorenz A, Steinacher R, Castagnetti S, et al. (2011) Ultrafine anaphase bridges, broken DNA and illegitimate recombination induced by a replication fork barrier. Nucleic Acids Res 39: 6568-6584.
22. Jacome A, Fernandez-Capetillo O, (2011) Lac operator repeats generate a traceable fragile site in mammalian cells. EMBO Rep 12: 1032-1038.
23. Dubarry M, Loiodice I, Chen CL, Thermes C, Taddei A, (2011) Tight protein-DNA interactions favor gene silencing. Genes Dev 25: 1365-1370.
24. Dubarry N, Pasta F, Lane D, (2006) ParABS systems of the four replicons of Burkholderia cenocepacia: new chromosome centromeres confer partition specificity. J Bacteriol 188: 1489-1496.
25. Khare D, Ziegelin G, Lanka E, Heinemann U, (2004) Sequence-specific DNA binding determined by contacts outside the helix-turn-helix motif of the ParB homolog KorB. Nat Struct Mol Biol 11: 656-663.
26. Thorn K, (2010) Spinning-disk confocal microscopy of yeast. Methods Enzymol 470: 581-602.
27. Haber JE, (2000) Lucky breaks: analysis of recombination in Saccharomyces. Mutat Res 451: 53-69.
28. Connolly B, White CI, Haber JE, (1988) Physical monitoring of mating type switching in Saccharomyces cerevisiae. Mol Cell Biol 8: 2342-2349.
29. Stracker TH, Petrini JH, (2011) The MRE11 complex: starting from the ends. Nat Rev Mol Cell Biol 12: 90-103.
30. Langerak P, Mejia-Ramirez E, Limbo O, Russell P, (2011) Release of Ku and MRN from DNA ends by Mre11 nuclease activity and Ctp1 is required for homologous recombination repair of double-strand breaks. PLoS Genet 7: e1002271.
31. Frank-Vaillant M, Marcand S, (2002) Transient stability of DNA ends allows nonhomologous end joining to precede homologous recombination. Mol Cell 10: 1189-1199.
32. Lee SE, Pellicioli A, Demeter J, Vaze MP, Gasch AP, et al. (2000) Arrest, adaptation, and recovery following a chromosome double-strand break in Saccharomyces cerevisiae. Cold Spring Harb Symp Quant Biol 65: 303-314.
33. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G, (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134: 981-994.
34. Mimitou EP, Symington LS, (2010) Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. Embo J 29: 3358-3369.
35. Shim EY, Chung WH, Nicolette ML, Zhang Y, Davis M, et al. (2010) Saccharomyces cerevisiae Mre11/Rad50/Xrs2 and Ku proteins regulate association of Exo1 and Dna2 with DNA breaks. Embo J 29: 3370-3380.
36. Hajjoul H, Kocanova S, Lassadi I, Bystricky K, Bancaud A, (2009) Lab-on-Chip for fast 3D particle tracking in living cells. Lab Chip 9: 3054-3058.
37. Bystricky K, Van Attikum H, Montiel MD, Dion V, Gehlen L, et al. (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.
38. Hajjoul H, Mathon J, Ranchon H, Goiffon I, Mozziconacci J, et al. (2013) High-throughput chromatin motion tracking in living yeast reveals the flexibility of the fiber throughout the genome. Genome Res 23: 1829-1838.
39. Chen H, Symington LS, (2012) Overcoming the chromatin barrier to end resection. Cell Res 23 (3) (): 317-9.
40. Sharples GJ, Leach DR, (1995) Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast. Mol Microbiol 17: 1215-1217.
41. Johzuka K, Ogawa H, (1995) Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics 139: 1521-1532.
42. Varon R, Vissinga C, Platzer M, Cerosaletti KM, Chrzanowska KH, et al. (1998) Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 93: 467-476.
43. Ivanov EL, Sugawara N, White CI, Fabre F, Haber JE, (1994) Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol Cell Biol 14: 3414-3425.
44. Fiorentini P, Huang KN, Tishkoff DX, Kolodner RD, Symington LS, (1997) Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol Cell Biol 17: 2764-2773.
45. Gangloff S, McDonald JP, Bendixen C, Arthur L, Rothstein R, (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol Cell Biol 14: 8391-8398.
46. Budd ME, Choe W, Campbell JL, (2000) The nuclease activity of the yeast DNA2 protein, which is related to the RecB-like nucleases, is essential in vivo. J Biol Chem 275: 16518-16529.
47. Tsubouchi H, Ogawa H, (1998) A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol Cell Biol 18: 260-268.
48. 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.
49. Lisby M, Rothstein R, (2009) Choreography of recombination proteins during the DNA damage response. DNA Repair (Amst) 8: 1068-1076.
50. Soutoglou E, Dorn JF, Sengupta K, Jasin M, Nussenzweig A, et al. (2007) Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 9: 675-682.
51. de Jager M, van Noort J, van Gent DC, Dekker C, Kanaar R, et al. (2001) Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol Cell 8: 1129-1135.
52. Williams RS, Kunkel TA, (2011) FEN nucleases: bind, bend, fray, cut. Cell 145: 171-172.
53. Longhese MP, Bonetti D, Manfrini N, Clerici M, (2010) Mechanisms and regulation of DNA end resection. Embo J 29: 2864-2874.
54. Lazzaro F, Sapountzi V, Granata M, Pellicioli A, Vaze M, et al. (2008) Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. Embo J 27: 1502-1512.
55. Bennett G, Papamichos-Chronakis M, Peterson CL, (2013) DNA repair choice defines a common pathway for recruitment of chromatin regulators. Nat Commun 4: 2084.
56. Cannavo E, Cejka P, Kowalczykowski SC, (2013) Relationship of DNA degradation by Saccharomyces cerevisiae Exonuclease 1 and its stimulation by RPA and Mre11-Rad50-Xrs2 to DNA end resection. Proc Natl Acad Sci U S A 110: E1661-1668.
57. Adkins NL, Niu H, Sung P, Peterson CL, (2013) Nucleosome dynamics regulates DNA processing. Nat Struct Mol Biol 20 (7) (): 836-42.
58. Cejka P, Cannavo E, Polaczek P, Masuda-Sasa T, Pokharel S, et al. (2010) DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467: 112-116.
59. Chiolo I, Carotenuto W, Maffioletti G, Petrini JH, Foiani M, et al. (2005) Srs2 and Sgs1 DNA helicases associate with Mre11 in different subcomplexes following checkpoint activation and CDK1-mediated Srs2 phosphorylation. Mol Cell Biol 25: 5738-5751.
60. Chung WH, Zhu Z, Papusha A, Malkova A, Ira G, (2010) Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet 6: e1000948.
61. Zakharyevich K, Ma Y, Tang S, Hwang PY, Boiteux S, et al. (2010) Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions. Mol Cell 40: 1001-1015.
62. Hanai R, Liu R, Benedetti P, Caron PR, Lynch AS, et al. (1996) Molecular dissection of a protein SopB essential for Escherichia coli F plasmid partition. J Biol Chem 271: 17469-17475.
63. Surtees JA, Funnell BE, (1999) P1 ParB domain structure includes two independent multimerization domains. J Bacteriol 181: 5898-5908.
64. Guynet C, de la Cruz F, (2011) Plasmid segregation without partition. Mob Genet Elements 1: 236-241.
65. Morales VM, Backman A, Bagdasarian M, (1991) A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97: 39-47.
66. Goldstein AL, Pan X, McCusker JH, (1999) Heterologous URA3MX cassettes for gene replacement in Saccharomyces cerevisiae. Yeast 15: 507-511.
67. Gietz RD, Schiestl RH, (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 31-34.
68. Iacovoni JS, Caron P, Lassadi I, Nicolas E, Massip L, et al. (2010) High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. Embo J 29: 1446-1457.
69. Shen Z, St-Denis A, Chartrand P, (2010) Cotranscriptional recruitment of She2p by RNA pol II elongation factor Spt4-Spt5/DSIF promotes mRNA localization to the yeast bud. Genes Dev 24: 1914-1926.
70. Gallardo F, Laterreur N, Cusanelli E, Ouenzar F, Querido E, et al. (2011) Live cell imaging of telomerase RNA dynamics reveals cell cycle-dependent clustering of telomerase at elongating telomeres. Mol Cell 44: 819-827.