Nucleosome dynamics regulates DNA processing

Nature Structural and Molecular Biology

Volumn 20, Issue 7, 2013, Pages 836-842

  Adkins, Nicholas L ^a   Niu, Hengyao ^b   Sung, Patrick ^b   Peterson, Craig L ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; HISTONE H2A; HISTONE H2AZ; HISTONE H2B; PHLEOMYCIN; RESTRICTION ENDONUCLEASE; SINGLE STRANDED DNA BINDING PROTEIN; STREPTAVIDIN;

ARTICLE; BINDING ASSAY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVE SITE; GENE INTERACTION; HOMOLOGOUS RECOMBINATION; IN VITRO STUDY; IN VIVO STUDY; INSECT CELL; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; SURGERY;

ADENOSINE TRIPHOSPHATASES; CHROMATIN; DIMERIZATION; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA HELICASES; DNA, FUNGAL; EXODEOXYRIBONUCLEASES; HISTONES; NUCLEOSOMES; RECQ HELICASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 84880154076     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2585     Document Type: Article

References (45)

1. Khanna, K.K. & Jackson, S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27, 247-254 (2001).
2. Zou, L. & Elledge, S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548 (2003).
3. Krogh, B.O. & Symington, L.S. Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271 (2004).
4. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E. & Ira, G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134, 981-994 (2008).
5. Mimitou, E.P. & Symington, L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770-774 (2008).
6. Gravel, S., Chapman, J.R., Magill, C. & Jackson, S.P. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22, 2767-2772 (2008).
7. Budd, M.E., Choe, W.C. & Campbell, J.L. DNA2 encodes a DNA helicase essential for replication of eukaryotic chromosomes. J. Biol. Chem. 270, 26766-26769 (1995).
8. Szankasi, P. & Smith, G.R. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267, 1166-1169 (1995).
9. Tsubouchi, H. & Ogawa, H. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerecisiae. Mol. Biol. Cell 11, 2221-2233 (2000).
10. Cotta-Ramusino, C. et al. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17, 153-159 (2005).
11. Hackett, J.A. & Greider, C.W. End resection initiates genomic instability in the absence of telomerase. Mol. Cell Biol. 23, 8450-8461 (2003).
12. Bertuch, A.A. & Lundblad, V. EXO1 contributes to telomere maintenance in both telomerase-proficient and telomerase-deficient Saccharomyces cerevisiae. Genetics 166, 1651-1659 (2004).
13. Niu, H. et al. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467, 108-111 (2010).
14. Szankasi, P. & Smith, G.R.A. DNA exonuclease induced during meiosis of Schizosaccharomyces pombe. J. Biol. Chem. 267, 3014-3023 (1992).
15. Tran, P.T., Erdeniz, N., Dudley, S. & Liskay, R.M. Characterization of nuclease-dependent functions of Exo1p in Saccharomyces cerevisiae. DNA Repair (Amst.) 1, 895-912 (2002).
16. Chu, W.K. & Hickson, I.D. RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer 9, 644-654 (2009).
17. Chai, B., Huang, J., Cairns, B.R. & Laurent, B.C. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19, 1656-1661 (2005).
18. Shim, E.Y. et al. RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell Biol. 27, 1602-1613 (2007).
19. Osley, M.A., Tsukuda, T. & Nickoloff, J.A. ATP-dependent chromatin remodeling factors and DNA damage repair. Mutat. Res. 618, 65-80 (2007).
20. Tsukuda, T. et al. INO80-dependent chromatin remodeling regulates early and late stages of mitotic homologous recombination. DNA Repair (Amst.) 8, 360-369 (2009).
21. Kalocsay, M., Hiller, N.J. & Jentsch, S. Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol. Cell 33, 335-343 (2009).
22. Chen, X. et al. The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489, 576-580 (2012).
23. Costelloe, T. et al. The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489, 581-584 (2012).
24. Papamichos-Chronakis, M., Krebs, J.E. & Peterson, C.L. Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev. 20, 2437-2449 (2006).
25. Morillo-Huesca, M., Clemente-Ruiz, M., Andjar, E. & Prado, F. The SWR1 histone replacement complex causes genetic instability and genome-wide transcription misregulation in the absence of H2A.Z. PLoS ONE 5, e12143 (2010).
26. Halley, J.E., Kaplan, T., Wang, A.Y., Kobor, M.S. & Rine, J. Roles for H2A.Z and its acetylation in GAL1 transcription and gene induction, but not GAL1-transcriptional memory. PLoS Biol. 8, e1000401 (2010).
27. Zhang, H., Roberts, D.N. & Cairns, B.R. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123, 219-231 (2005).
28. Watanabe, S., Radman-Livaja, M., Rando, O. & Peterson, C.L. A histone acetylation switch regulates H2A.Z deposition by the SWR-C remodeling enzyme. Science 340, 195-199 (2013).
29. Mizuguchi, G. et al. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303, 343-348 (2004).
30. Nishimura, K., Fukagawa, T., Takisawa, H., Kakimoto, T. & Kanemaki, M. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods 6, 917-922 (2009).
31. Shim, E.Y. et al. RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell Biol. 27, 1602-1613 (2007).
32. Eggleston, A.K., O'Neill, T.E., Bradbury, E.M. & Kowalczykowski, S.C. Unwinding of nucleosomal DNA by a DNA helicase. J. Biol. Chem. 270, 2024-2031 (1995).
33. Finkelstein, I.J., Visnapuu, M.L. & Greene, E.C. Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase. Nature 468, 983-987 (2010).
34. Nimonkar, A.V. et al. BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev. 25, 350-362 (2011).
35. Wei, K. et al. Inactivation of Exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev. 17, 603-614 (2003).
36. Giannattasio, M. et al. Exo1 competes with repair synthesis, converts NER intermediates to long ssDNA gaps, and promotes checkpoint activation. Mol. Cell 40, 50-62 (2010).
37. Hombauer, H., Campbell, C.S., Smith, C.E., Desai, A. & Kolodner, R.D. Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates. Cell 147, 1040-1053 (2011).
38. Hombauer, H., Srivatsan, A., Putnam, C.D. & Kolodner, R.D. Mismatch repair, but not heteroduplex rejection, is temporally coupled to DNA replication. Science 334, 1713-1716 (2011).
39. Xu, Y. et al. Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol. Cell 48, 723-733 (2012).
40. Rangasamy, D. Histone variant H2A.Z can serve as a new target for breast cancer therapy. Curr. Med. Chem. 17, 3155-3161 (2010).
41. Sigurdsson, S., Trujillo, K., Song, B., Stratton, S. & Sung, P. Basis for avid homologous DNA strand exchange by human Rad51 and RPA. J. Biol. Chem. 276, 8798-8806 (2001).
42. Raynard, S., Bussen, W. & Sung, P.A. A double Holliday junction dissolvasome comprising BLM, topoisomerase III, and BLAP75. J. Biol. Chem. 281, 13861-13864 (2006).
43. Luger, K., Rechsteiner, T.J. & Richmond, T.J. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 304, 3-19 (1999).
44. Smith, C.L., Horowitz-Scherer, R., Flanagan, J.F., Woodcock, C.L. & Peterson, C.L. Structural analysis of the yeast SWI/SNF chromatin remodeling complex. Nat. Struct. Biol. 10, 141-145 (2003).
45. Goldstein, A.L. & McCusker, J.H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553 (1999).