Systematic identification of fragile sites via genome-wide location analysis of γ-H2AX

Nature Structural and Molecular Biology

Volumn 17, Issue 3, 2010, Pages 299-305

  Szilard, Rachel K ^a   Jacques, Pierre Tienne ^b   Laramée, Louise ^b   Cheng, Benjamin ^a   Galicia, Sarah ^a   Bataille, Alain R ^b   Yeung, Mantek ^a,c   Mendez, Megan ^a   Bergeron, Maxime ^b   Robert, François ^b,d   Durocher, Daniel ^a,c  

^a MOUNT SINAI HOSPITAL   (Canada)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA HISTONE H2AX; HISTONE DEACETYLASE; HISTONE H2AX; MEC1 PROTEIN; PROTEIN; TEL1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE LOCUS; GENE MAPPING; GENETIC CODE; GENOME; GENOME ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; YEAST;

CELL CYCLE; CELL CYCLE PROTEINS; CHROMATIN IMMUNOPRECIPITATION; GENOME, FUNGAL; HISTONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 77949275845     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1754     Document Type: Article

References (60)

1. Labib, K. & Hodgson, B. Replication fork barriers: pausing for a break or stalling for time? EMBO Rep. 8, 346-353 (2007).
2. Durkin, S.G. & Glover, T.W. Chromosome fragile sites. Annu. Rev. Genet. 41, 169-192 (2007).
3. Ivessa, A.S. et al. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol. Cell 12, 1525-1536 (2003).
4. Ivessa, A.S., Zhou, J.Q., Schulz, V.P., Monson, E.K. & Zakian, V.A. Saccharomyces Rrm3p, a 5′ to 3′ DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 16, 1383-1396 (2002).
5. Deshpande, A.M. & Newlon, C.S. DNA replication fork pause sites dependent on transcription. Science 272, 1030-1033 (1996).
6. Greenfeder, S.A. & Newlon, C.S. Replication forks pause at yeast centromeres. Mol. Cell. Biol. 12, 4056-4066 (1992).
7. Cha, R.S. & Kleckner, N. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297, 602-606 (2002).
8. Raveendranathan, M. et al. Genome-wide replication profles of S-phase checkpoint mutants reveal fragile sites in yeast. EMBO J. 25, 3627-3639 (2006).
9. Rothstein, R. Deletions of a tyrosine tRNA gene in S. cerevisiae. Cell 17, 185-190 (1979).
10. Admire, A. et al. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes Dev. 20, 159-173 (2006).
11. Roeder, G.S. & Fink, G.R. DNA rearrangements associated with a transposable element in yeast. Cell 21, 239-249 (1980).
12. Lemoine, F.J., Degtyareva, N.P., Lobachev, K. & Petes, T.D. Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 120, 587-598 (2005).
13. Cliby, W.A. et al. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17, 159-169 (1998).
14. Brown, E.J. & Baltimore, D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14, 397-402 (2000).
15. Weinert, T.A., Kiser, G.L. & Hartwell, L.H. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 8, 652-665 (1994).
16. Paulovich, A.G. & Hartwell, L.H. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82, 841-847 (1995).
17. Sun, Z., Fay, D.S., Marini, F., Foiani, M. & Stern, D.F. Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes Dev. 10, 395-406 (1996).
18. Desany, B.A., Alcasabas, A.A., Bachant, J.B. & Elledge, S.J. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12, 2956-2970 (1998).
19. Lopes, M. et al. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412, 557-561 (2001).
20. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S. & Bonner, W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868 (1998).
21. Downs, J.A., Lowndes, N.F. & Jackson, S.P. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408, 1001-1004 (2000).
22. Foster, E.R. & Downs, J.A. Histone H2A phosphorylation in DNA double-strand break repair. FEBS J. 272, 3231-3240 (2005).
23. Fernandez-Capetillo, O., Lee, A., Nussenzweig, M. & Nussenzweig, A. H2AX: the histone guardian of the genome. DNA Repair (Amst.) 3, 959-967 (2004).
24. Cobb, J.A. et al. Replisome instability, fork collapse, and gross chromosomal rearrangements arise synergistically from Mec1 kinase and RecQ helicase mutations. Genes Dev. 19, 3055-3069 (2005).
25. Ward, I.M. & Chen, J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276, 47759-47762 (2001).
26. Redon, C. et al. Yeast histone 2A serine 129 is essential for the effcient repair of checkpoint-blind DNA damage. EMBO Rep. 4, 678-684 (2003).
27. Ren, B. et al. Genome-wide location and function of DNA binding proteins. Science 290, 2306-2309 (2000).
28. Shroff, R. et al. Distribution and dynamics of chromatin modifcation induced by a defned DNA double-strand break. Curr. Biol. 14, 1703-1711 (2004).
29. Kim, J.A., Kruhlak, M., Dotiwala, F., Nussenzweig, A. & Haber, J.E. Heterochromatin is refractory to gamma-H2AX modifcation in yeast and mammals. J. Cell Biol. 178, 209-218 (2007).
30. Wang, Y., Vujcic, M. & Kowalski, D. DNA replication forks pause at silent origins near the HML locus in budding yeast. Mol. Cell. Biol. 21, 4938-4948 (2001).
31. Azvolinsky, A., Dunaway, S., Torres, J.Z., Bessler, J.B. & Zakian, V.A. The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes. Genes Dev. 20, 3104-3116 (2006).
32. Torres, J.Z., Schnakenberg, S.L. & Zakian, V.A. Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol. Cell. Biol. 24, 3198-3212 (2004).
33. Rothstein, R., Helms, C. & Rosenberg, N. Concerted deletions and inversions are caused by mitotic recombination between δ sequences in Saccharomyces cerevisiae. Mol. Cell. Biol. 7, 1198-1207 (1987).
34. Melo, J.A., Cohen, J. & Toczyski, D.P. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15, 2809-2821 (2001).
35. Lisby, M., Rothstein, R. & Mortensen, U.H. Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl. Acad. Sci. USA 98, 8276-8282 (2001).
36. Kanellis, P. et al. A screen for suppressors of gross chromosomal rearrangements identifes a conserved role for PLP in preventing DNA lesions. PLoS Genet. 3, e134 (2007).
37. Sollier, J. et al. The Saccharomyces cerevisiae Esc2 and Smc5-6 proteins promote sister chromatid junction-mediated intra-S repair. Mol. Biol. Cell 20, 1671-1682 (2009).
38. Mankouri, H.W., Ngo, H.P. & Hickson, I.D. Esc2 and Sgs1 act in functionally distinct branches of the homologous recombination repair pathway in Saccharomyces cerevisiae. Mol. Biol. Cell 20, 1683-1694 (2009).
39. Myung, K., Pennaneach, V., Kats, E.S. & Kolodner, R.D. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc. Natl. Acad. Sci. USA 100, 6640-6645 (2003).
40. Hackett, J.A., Feldser, D.M. & Greider, C.W. Telomere dysfunction increases mutation rate and genomic instability. Cell 106, 275-286 (2001).
41. Kraus, E., Leung, W.Y. & Haber, J.E. Break-induced replication: a review and an example in budding yeast. Proc. Natl. Acad. Sci. USA 98, 8255-8262 (2001).
42. Tercero, J.A., Longhese, M.P. & Diffey, J.F. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 11, 1323-1336 (2003).
43. Myung, K. & Kolodner, R.D. Induction of genome instability by DNA damage in Saccharomyces cerevisiae. DNA Repair (Amst.) 2, 243-258 (2003).
44. Lee, K., Zhang, Y. & Lee, S.E. Saccharomyces cerevisiae ATM ortholog suppresses break-induced chromosome translocations. Nature 454, 543-546 (2008).
45. Azvolinsky, A., Giresi, P.G., Lieb, J.D. & Zakian, V.A. Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol. Cell 34, 722-734 (2009).
46. Broach, J.R. Galactose regulation in Saccharomyces cerevisiae. The enzymes encoded by the GAL7, 10, 1 cluster are co-ordinately controlled and separately translated. J. Mol. Biol. 131, 41-53 (1979).
47. MacIsaac, K.D. et al. An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7, 113 (2006).
48. Xie, J. et al. Sum1 and Hst1 repress middle sporulation-specifc gene expression during mitosis in Saccharomyces cerevisiae. EMBO J. 18, 6448-6454 (1999).
49. Kadosh, D. & Struhl, K. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89, 365-371 (1997).
50. Robert, F. et al. Global position and recruitment of HATs and HDACs in the yeast genome. Mol. Cell 16, 199-209 (2004).
51. Ashburner, M. et al. Gene ontology: tool for the unifcation of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29 (2000).
52. Inai, T., Yukawa, M. & Tsuchiya, E. Interplay between chromatin and trans-acting factors on the IME2 promoter upon induction of the gene at the onset of meiosis. Mol. Cell. Biol. 27, 1254-1263 (2007).
53. Veis, J., Klug, H., Koranda, M. & Ammerer, G. Activation of the G2/M-specifc gene CLB2 requires multiple cell cycle signals. Mol. Cell. Biol. 27, 8364-8373 (2007).
54. Aparicio, J.G., Viggiani, C.J., Gibson, D.G. & Aparicio, O.M. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol. Cell. Biol. 24, 4769-4780 (2004).
55. Vogelauer, M., Rubbi, L., Lucas, I., Brewer, B.J. & Grunstein, M. Histone acetylation regulates the time of replication origin fring. Mol. Cell 10, 1223-1233 (2002).
56. Guillemette, B. et al. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol. 3, e384 (2005).
57. Pfaff, M.W. A new mathematical model for relative quantifcation in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001).
58. Pokholok, D.K. et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122, 517-527 (2005).
59. Rufange, A., Jacques, P.E., Bhat, W., Robert, F. & Nourani, A. Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol. Cell 27, 393-405 (2007).
60. Nieduszynski, C.A., Hiraga, S., Ak, P., Benham, C.J. & Donaldson, A.D. OriDB: a DNA replication origin database. Nucleic Acids Res. 35, D40-D46 (2007).