A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice

Nature Communications

Volumn 5, Issue , 2014, Pages

  Pai, Chen Chun ^a   Deegan, Rachel S ^a   Subramanian, Lakxmi ^b   Gal, Csenge ^c   Sarkar, Sovan ^a   Blaikley, Elizabeth J ^a   Walker, Carol ^a   Hulme, Lydia ^a   Bernhard, Eric ^a   Codlin, Sandra ^d   Bähler, Jürg ^d   Allshire, Robin ^b   Whitehall, Simon ^c   Humphrey, Timothy C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; HISTONE H3; HISTONE H3K36; UNCLASSIFIED DRUG; ACYLTRANSFERASE; CHROMATIN; FUNGAL DNA; GCN5 PROTEIN, S POMBE; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; SCHIZOSACCHAROMYCES POMBE PROTEIN; SET2 PROTEIN, S POMBE;

CHROMOSOME; DNA; HOMOLOGY; METHYLATION; PROTEIN; YEAST;

ACETYLATION; ARTICLE; CELL CYCLE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; HISTONE METHYLATION; HISTONE MODIFICATION; HOMOLOGOUS RECOMBINATION; IONIZING RADIATION; MICROARRAY ANALYSIS; MINICHROMOSOME; MOLECULAR WEIGHT; NONHUMAN; PHENOTYPE; SISTER CHROMATID; WESTERN BLOTTING; DNA REPAIR; GENETICS; METABOLISM; METHYLATION; RECOMBINATION REPAIR; SCHIZOSACCHAROMYCES;

ACETYLATION; ACETYLTRANSFERASES; CHROMATIN; DNA END-JOINING REPAIR; DNA REPAIR; DNA, FUNGAL; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; METHYLATION; RECOMBINATIONAL DNA REPAIR; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84902251340     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5091     Document Type: Article

References (59)

1. Symington, L. S. & Gautier, J. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45, 247-271 (2011).
2. Lieber, M. R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79, 181-211 (2010).
3. Heyer, W. D., Ehmsen, K. T. & Liu, J. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 44, 113-139 (2010).
4. Aylon, Y., Liefshitz, B. & Kupiec, M. The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J. 23, 4868-4875 (2004). (Pubitemid 40069716)
5. Ira, G. et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431, 1011-1017 (2004). (Pubitemid 39434425)
6. Ferreira, M. G. & Cooper, J. P. Two modes of DNA double-strand break repair are reciprocally regulated through the fission yeast cell cycle. Genes Dev. 18, 2249-2254 (2004). (Pubitemid 39209573)
7. Wagner, E. J. & Carpenter, P. B. Understanding the language of Lys36 methylation at histone H3. Nat. Rev. Mol. Cell Biol. 13, 115-126 (2012).
8. Strahl, B. D. et al. Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol. Cell Biol. 22, 1298-1306 (2002). (Pubitemid 34150767)
9. Edmunds, J. W., Mahadevan, L. C. & Clayton, A. L. Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J. 27, 406-420 (2008). (Pubitemid 351161656)
10. Al Sarakbi, W. et al. The mRNA expression of SETD2 in human breast cancer: correlation with clinico-pathological parameters. BMC Cancer 9, 290 (2009).
11. Dalgliesh, G. L. et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature 463, 360-363 (2010).
12. Newbold, R. F. & Mokbel, K. Evidence for a tumour suppressor function of SETD2 in human breast cancer: a new hypothesis. Anticancer Res. 30, 3309-3311 (2010).
13. Zhang, J. et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157-163 (2012).
14. Fontebasso, A. M. et al. Mutations in SETD2 and genes affecting histone H3K36 methylation target hemispheric high-grade gliomas. Acta Neuropathol. 125, 659-669 (2013).
15. Jazayeri, A., McAinsh, A. D. & Jackson, S. P. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc. Natl Acad. Sci. USA 101, 1644-1649 (2004). (Pubitemid 38234208)
16. Merker, J. D. et al. The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae. DNA. Repair 7, 1298-1308 (2008).
17. Fnu, S. et al. Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining. Proc. Natl Acad. Sci. USA 108, 540-545 (2011).
18. Daugaard, M. et al. LEDGF (p75) promotes DNA-end resection and homologous recombination. Nat. Struct. Mol. Biol. 19, 803-810 (2012).
19. Morris, S. A. et al. Identification of histone H3 lysine 36 acetylation as a highly conserved histone modification. J. Biol. Chem. 282, 7632-7640 (2007). (Pubitemid 47093631)
20. Daniel, J. A. & Grant, P. A. Multi-tasking on chromatin with the SAGA coactivator complexes. Mutat. Res. 618, 135-148 (2007). (Pubitemid 46574741)
21. Barlev, N. A. et al. Repression of GCN5 histone acetyltransferase activity via bromodomain-mediated binding and phosphorylation by the Ku-DNAdependent protein kinase complex. Mol. Cell Biol. 18, 1349-1358 (1998). (Pubitemid 28100899)
22. Tamburini, B. A. & Tyler, J. K. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol. Cell Biol. 25, 4903-4913 (2005). (Pubitemid 40781092)
23. Oishi, H. et al. An hGCN5/TRRAP histone acetyltransferase complex coactivates BRCA1 transactivation function through histone modification. J. Biol. Chem. 281, 20-26 (2006). (Pubitemid 43671158)
24. Lee, H. S., Park, J. H., Kim, S. J., Kwon, S. J. & Kwon, J. A cooperative activation loop among SWI/SNF, gamma-H2AX and H3 acetylation for DNA doublestrand break repair. EMBO J. 29, 1434-1445 (2010).
25. Lee, S. E. et al. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94, 399-409 (1998). (Pubitemid 28376083)
26. Pierce, A. J., Hu, P., Han, M., Ellis, N. & Jasin, M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15, 3237-3242 (2001). (Pubitemid 34008189)
27. Rea, S. et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593-599 (2000). (Pubitemid 30641039)
28. Morris, S. A. et al. Histone H3 K36 methylation is associated with transcription elongation in Schizosaccharomyces pombe. Eukaryot. Cell 4, 1446-1454 (2005). (Pubitemid 41176698)
29. Tinline-Purvis, H. et al. Failed gene conversion leads to extensive end processing and chromosomal rearrangements in fission yeast. EMBO J. 28, 3400-3412 (2009).
30. Keogh, M. C. et al. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123, 593-605 (2005).
31. Nakayama, J. et al. Alp13, an MRG family protein, is a component of fission yeast Clr6 histone deacetylase required for genomic integrity. EMBO J. 22, 2776-2787 (2003). (Pubitemid 36712373)
32. Nicolas, E. et al. Distinct roles of HDAC complexes in promoter silencing, antisense suppression and DNA damage protection. Nat. Struct. Mol. Biol. 14, 372-380 (2007). (Pubitemid 46685888)
33. Carneiro, T. et al. Telomeres avoid end detection by severing the checkpoint signal transduction pathway. Nature 467, 228-232 (2010).
34. Barlow, J. H., Lisby, M. & Rothstein, R. Differential regulation of the cellular response to DNA double-strand breaks in G1. Mol. Cell 30, 73-85 (2008). (Pubitemid 351470149)
35. Wang, Y. et al. Histone H3 lysine 14 acetylation is required for activation of a DNA damage checkpoint in fission yeast. J. Biol. Chem. 287, 4386-4393 (2012).
36. Johnsson, A., Xue-Franzen, Y., Lundin, M. & Wright, A. P. Stress-specific role of fission yeast Gcn5 histone acetyltransferase in programming a subset of stress response genes. Eukaryot. Cell 5, 1337-1346 (2006).
37. Benson, L. J. et al. Properties of the type B histone acetyltransferase Hat1: H4 tail interaction, site preference, and involvement in DNA repair. J. Biol. Chem. 282, 836-842 (2007). (Pubitemid 47076534)
38. Mitchell, L. et al. Functional dissection of the NuA4 histone acetyltransferase reveals its role as a genetic hub and that Eaf1 is essential for complex integrity. Mol. Cell Biol. 28, 2244-2256 (2008). (Pubitemid 351429971)
39. Qin, S. & Parthun, M. R. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol. Cell Biol. 22, 8353-8365 (2002). (Pubitemid 35304066)
40. Shim, E. Y., Ma, J. L., Oum, J. H., Yanez, Y. & Lee, S. E. The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell Biol. 25, 3934-3944 (2005). (Pubitemid 40617645)
41. 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).
42. Blier, P. R., Griffith, A. J., Craft, J. & Hardin, J. A. Binding of Ku protein to DNA. Measurement of affinity for ends and demonstration of binding to nicks. J. Biol. Chem. 268, 7594-7601 (1993). (Pubitemid 23105662)
43. Venkatesh, S. et al. Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489, 452-455 (2012).
44. Smolle, M. et al. Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat. Struct. Mol. Biol. 19, 884-892 (2012).
45. Adkins, N. L., Niu, H., Sung, P. & Peterson, C. L. Nucleosome dynamics regulates DNA processing. Nat. Struct. Mol. Biol. 20, 836-842 (2013).
46. Bird, A. W. et al. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419, 411-415 (2002).
47. Bennett, G., Papamichos-Chronakis, M. & Peterson, C. L. DNA repair choice defines a common pathway for recruitment of chromatin regulators. Nat. Commun. 4, 2084 (2013).
48. Jha, D. K. & Strahl, B. D. An RNA polymerase II-coupled function for histone H3K36 methylation in checkpoint activation and DSB repair. Nat. Commun. 5, 3965 doi:10.1038/ncomms4965 (2014).
49. Aymard, F. et al. Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks. Nat. Struct. Mol. Biol. 21, 366-374 (2014).
50. Pfister, S. X. et al. ETD2-dependent histone H3K36 trimethylation is required for homologous recombination repair and genome stability. Cell Reports (in press, 2014).
51. Faucher, D. & Wellinger, R. J. Methylated H3K4, a transcription-associated histone modification, is involved in the DNA damage response pathway. PLoS Genet. 6 pii e1001082 (2010).
52. Li, F. et al. The Histone Mark H3K36me3 Regulates Human DNA Mismatch Repair through Its Interaction with MutSalpha. Cell 153, 590-600 (2013).
53. Moreno, S., Klar, A. & Nurse, P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823 (1991).
54. Subramanian, L. & Nakamura, T. M. A kinase-independent role for the Rad3(ATR)-Rad26(ATRIP) complex in recruitment of Tel1(ATM) to telomeres in fission yeast. PLoS Genet. 6, e1000839 (2010).
55. Manolis, K. G. et al. Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J. 20, 210-221 (2001). (Pubitemid 32099117)
56. Rallis, C., Codlin, S. & Bahler, J. TORC1 signaling inhibition by rapamycin and caffeine affect lifespan, global gene expression, and cell proliferation of fission yeast. Aging Cell 12, 563-573 (2013).
57. Nurse, P. & Bissett, Y. Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature 292, 558-560 (1981). (Pubitemid 11023994)
58. Shechter, D., Dormann, H. L., Allis, C. D. & Hake, S. B. Extraction, purification and analysis of histones. Nat. Protoc. 2, 1445-1457 (2007). (Pubitemid 46952324)
59. Watson, A. T., Werler, P. & Carr, A. M. Regulation of gene expression at the fission yeast Schizosaccharomyces pombe urg1 locus. Gene 484, 75-85 (2011).