Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery

Nature Cell Biology

Volumn 14, Issue 5, 2012, Pages 502-509

  Dion, Vincent ^a   Kalck, Véronique ^a   Horigome, Chihiro ^a   Towbin, Benjamin D ^a,b   Gasser, Susan M ^a,b  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; FUNGAL DNA; PROTEIN MEC1; PROTEIN RAD9; RAD51 PROTEIN; RAD52 PROTEIN; RAD54 PROTEIN; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN;

ARTICLE; BUDDING; CELL NUCLEUS; CONTROLLED STUDY; DNA ADDUCT; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; HOMOLOGOUS RECOMBINATION; MUTANT; NONHUMAN; NUCLEAR SIZE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DNA BINDING; PROTEIN TRANSPORT; TIME LAPSE IMAGING; YEAST;

CELL CYCLE PROTEINS; CHROMATIN; DNA DAMAGE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROSCOPY, FLUORESCENCE; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 84860500314     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2465     Document Type: Article

References (43)

1. Gehlen, L., Gasser, S. M. & Dion, V. How broken DNA-nds a template for repair: a computational approach. Prog. Theor. Phys. Suppl. 191, 20-29 (2011).
2. Savage, J. R. Insight into sites. Mutat. Res. 366, 81-95 (1996). (Pubitemid 27008348)
3. Dimitrova, N., Chen, Y. C., Spector, D. L. & de Lange, T. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524-528 (2008). (Pubitemid 50304845)
4. Noon, A. T. & Goodarzi, A. A. 53BP1-mediated DNA double strand break repair: insert bad pun here. DNA Repair (Amst) 10, 1071-1076 (2011).
5. Aten, J. A. et al. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303, 92-95 (2004). (Pubitemid 38055778)
6. Lisby, M., Mortensen, U. H. & Rothstein, R. Colocalization of multiple DNA doublestrand breaks at a single Rad52 repair centre. Nat. Cell Biol. 5, 572-577 (2003). (Pubitemid 36781093)
7. Jakob, B., Splinter, J., Durante, M. & Taucher-Scholz, G. Live cell microscopy analysis of radiation-induced DNA double-strand break motion. Proc. Natl Acad. Sci. USA 106, 3172-3177 (2009).
8. Jakob, B., Splinter, J. & Taucher-Scholz, G. Positional stability of damaged chromatin domains along radiation tracks in mammalian cells. Radiat. Res. 171, 405-418 (2009).
9. Kruhlak, M. J. et al. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 172, 823-834 (2006).
10. Soutoglou, E. et al. Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 9, 675-682 (2007). (Pubitemid 47214730)
11. Nelms, B. E., Maser, R. S., MacKay, J. F., Lagally, M. G. & Petrini, J. H. In situ visualization of DNA double-strand break repair in human-broblasts. Science 280, 590-592 (1998). (Pubitemid 28227762)
12. Gartenberg, M. R., Neumann, F. R., Laroche, T., Blaszczyk, M. & Gasser, S. M. Sir-mediated repression can occur independently of chromosomal and subnuclear contexts. Cell 119, 955-967 (2004). (Pubitemid 40037609)
13. Meister, P., Gehlen, L. R., Varela, E., Kalck, V. & Gasser, S. M. Visualizing yeast chromosomes and nuclear architecture. Methods Enzymol. 470, 535-567 (2010).
14. Neumann, F. R. et al. INO80 promotes chromatin movement and functionally impacts homologous recombination. Genes Dev. 26, 369-383 (2012).
15. Straight, A. F., Belmont, A. S., Robinett, C. C. & Murray, A. W. GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr. Biol. 6, 1599-1608 (1996). (Pubitemid 27050227)
16. Lisby, M., Barlow, J. H., Burgess, R. C. & Rothstein, R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118, 699-713 (2004). (Pubitemid 39221730)
17. Heun, P., Laroche, T., Shimada, K., Furrer, P. & Gasser, S. M. Chromosome dynamics in the yeast interphase nucleus. Science 294, 2181-2186 (2001). (Pubitemid 33150678)
18. Povirk, L. F. DNA damage and mutagenesis by radiomimetic DNA-cleaving agents: bleomycin, neocarzinostatin and other enediynes. Mutat. Res. 355, 71-89 (1996). (Pubitemid 26275505)
19. Mazin, A. V., Mazina, O. M., Bugreev, D. V. & Rossi, M. J. Rad54, the motor of homologous recombination. DNA Repair (Amst) 9, 286-302 (2010).
20. Clever, B., Schmuckli-Maurer, J., Sigrist, M., Glassner, B. J. & Heyer, W. D. Speci-c negative effects resulting from elevated levels of the recombinational repair protein Rad54p in Saccharomyces cerevisiae. Yeast 15, 721-740 (1999). (Pubitemid 29308796)
21. Nielsen, I. et al. A Flp-nick system to study repair of a single protein-bound nick in vivo. Nat. Methods 6, 753-757 (2009).
22. Mochan, T. A., Venere, M., DiTullio, R. A. Jr & Halazonetis, T. D. 53BP1, an activator of ATM in response to DNA damage. DNA Repair (Amst) 3, 945-952 (2004). (Pubitemid 38997936)
23. Nyberg, K. A., Michelson, R. J., Putnam, C. W. & Weinert, T. A. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36, 617-656 (2002). (Pubitemid 36109200)
24. Stucki, M. & Jackson, S.P. MDC1/NFBD1: a key regulator of the DNA damage response in higher eukaryotes. DNA Repair (Amst) 3, 953-957 (2004). (Pubitemid 38997937)
25. Vialard, J. E., Gilbert, C. S., Green, C. M. & Lowndes, N. F. The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J. 17, 5679-5688 (1998). (Pubitemid 28445979)
26. Sweeney, F. D. et al. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr. Biol. 15, 1364-1375 (2005). (Pubitemid 41097540)
27. Usui, T., Foster, S. S. & Petrini, J. H. Maintenance of the DNA-damage checkpoint requires DNA-damage-induced mediator protein oligomerization. Mol. Cell 33, 147-159 (2009).
28. Conde, F. et al. The Dot1 histone methyltransferase and the Rad9 checkpoint adaptor contribute to cohesin-dependent double-strand break repair by sister chromatid recombination in Saccharomyces cerevisiae. Genetics 182, 437-446 (2009).
29. Zhao, X., Muller, E. G. & Rothstein, R. A suppressor of two essential checkpoint genes identi-es a novel protein that negatively affects dNTP pools. Mol Cell 2, 329-340 (1998). (Pubitemid 128379273)
30. Barlow, J. H. & Rothstein, R. Rad52 recruitment is DNA replication independent and regulated by Cdc28 and the Mec1 kinase. EMBO J. 28, 1121-1130 (2009).
31. White, C. I. & Haber, J. E. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9, 663-673 (1990).
32. Frank-Vaillant, M. & Marcand, S. Transient stability of DNA ends allows nonhomologous end joining to precede homologous recombination. Mol. Cell 10, 1189-1199 (2002). (Pubitemid 35453835)
33. Nagai, S. et al. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322, 597-602 (2008).
34. Pellicioli, A., Lee, S. E., Lucca, C., Foiani, M. & Haber, J. E. Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damageinduced G2/M arrest. Mol. Cell 7, 293-300 (2001). (Pubitemid 32206497)
35. Miné-Hattab, J. & Rothstein, R. Increased chromosome mobility: a model for homology search during homologous recombination. Nat. Cell Biol. http://dx.doi.org/10.1038/ncb2472 (2012).
36. Dubrana, K., van Attikum, H., Hediger, F. & Gasser, S. M. The processing of doublestrand breaks and binding of single-strand-binding proteins RPA and Rad51 modulate the formation of ATR-kinase foci in yeast . J. Cell Sci. 120, 4209-4220 (2007).
37. Zou, L. & Elledge, S. J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548 (2003). (Pubitemid 36682880)
38. Bennett, C. B., Lewis, A. L., Baldwin, K. K. & Resnick, M. A. Lethality induced by a single site-speci-c double-strand break in a dispensable yeast plasmid. Proc. Natl Acad. Sci. USA 90, 5613-5617 (1993). (Pubitemid 23176211)
39. Chiolo, I. et al. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144, 732-744 (2011).
40. Torres-Rosell, J. et al. The Smc5-Smc6 complex and SUMO modi-cation of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 9, 923-931 (2007). (Pubitemid 47190447)
41. Ponti, A., Gulati, A., Bäcker, V. & Schwarb, P. Huygens Remote Manager: a web interface for high-volume batch deconvolution . Imaging Microscopy 9, 57-58 (2007).
42. Sage, D., Neumann, F. R., Hediger, F., Gasser, S. M. & Unser, M. Automatic tracking of individual-uorescence particles: application to the study of chromosome dynamics. IEEE Trans. Image Process 14, 1372-1383 (2005). (Pubitemid 41430899)
43. Kim, Y. H. et al. Chromosome XII context is important for rDNA function in yeast. Nucleic Acids Res. 34, 2914-2924 (2006).