SIRT6 recruits SNF2H to DNA break sites, preventing genomic instability through chromatin remodeling

Molecular Cell

Volumn 51, Issue 4, 2013, Pages 454-468

  Toiber, Debra ^a   Erdel, Fabian ^b   Bouazoune, Karim ^c   Silberman, DafneM ^a,d   Zhong, Lei ^a   Mulligan, Peter ^a   Sebastian, Carlos ^a   Cosentino, Claudia ^a   Martinez Pastor, Barbara ^a   Giacosa, Sofia ^a   D'Urso, Agustina ^a,e   Näär, AndersM ^a   Kingston, Robert ^c   Rippe, Karsten ^b   Mostoslavsky, Raul ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d Centre de Estudios Farmacologicos y Botanicos   (Argentina)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; H3K56 PROTEIN; HISTONE; PROTEIN; SIRTUIN 6; SNF2H PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DEACETYLATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; GENOMIC INSTABILITY; GENOTOXICITY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PHENOTYPE; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA DAMAGE; DNA REPAIR; GENOMIC INSTABILITY; HIPPOCAMPUS; HISTONES; HUMANS; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; NUCLEOSOMES; SIRTUINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

MUS;

EID: 84882630603     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.06.018     Document Type: Article

References (45)

1. Bunting S.F., Callén E., Wong N., Chen H.T., Polato F., Gunn A., Bothmer A., Feldhahn N., Fernandez-Capetillo O., Cao L., et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010, 141:243-254.
2. Chapman J.R., Taylor M.R., Boulton S.J. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 2012, 47:497-510.
3. Chen C.C., Carson J.J., Feser J., Tamburini B., Zabaronick S., Linger J., Tyler J.K. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 2008, 134:231-243.
4. Chen X., Cui D., Papusha A., Zhang X., Chu C.D., Tang J., Chen K., Pan X., Ira G. The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 2012, 489:576-580.
5. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
6. Costelloe T., Louge R., Tomimatsu N., Mukherjee B., Martini E., Khadaroo B., Dubois K., Wiegant W.W., Thierry A., Burma S., et al. The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 2012, 489:581-584.
7. Das C., Lucia M.S., Hansen K.C., Tyler J.K. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 2009, 459:113-117.
8. Erdel F., Rippe K. Chromatin remodelling in mammalian cells by ISWI-type complexes-where, when and why?. FEBS J. 2011, 278:3608-3618.
9. Erdel F., Schubert T., Marth C., Längst G., Rippe K. Human ISWI chromatin-remodeling complexes sample nucleosomes via transient binding reactions and become immobilized at active sites. Proc. Natl. Acad. Sci. USA 2010, 107:19873-19878.
10. Finkel T., Deng C.X., Mostoslavsky R. Recent progress in the biology and physiology of sirtuins. Nature 2009, 460:587-591.
11. Gospodinov A., Vaissiere T., Krastev D.B., Legube G., Anachkova B., Herceg Z. Mammalian Ino80 mediates double-strand break repair through its role in DNA end strand resection. Mol. Cell. Biol. 2011, 31:4735-4745.
12. Kaidi A., Weinert B.T., Choudhary C., Jackson S.P. Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 2010, 329:1348-1353.
13. Kanfi Y., Naiman S., Amir G., Peshti V., Zinman G., Nahum L., Bar-Joseph Z., Cohen H.Y. The sirtuin SIRT6 regulates lifespan in male mice. Nature 2012, 483:218-221.
14. Kashiwaba S., Kitahashi K., Watanabe T., Onoda F., Ohtsu M., Murakami Y. The mammalian INO80 complex is recruited to DNA damage sites in an ARP8 dependent manner. Biochem. Biophys. Res. Commun. 2010, 402:619-625.
15. Kielbassa C., Roza L., Epe B. Wavelength dependence of oxidative DNA damage induced by UV and visible light. Carcinogenesis 1997, 18:811-816.
16. Lan L., Ui A., Nakajima S., Hatakeyama K., Hoshi M., Watanabe R., Janicki S.M., Ogiwara H., Kohno T., Kanno S., Yasui A. The ACF1 complex is required for DNA double-strand break repair in human cells. Mol. Cell 2010, 40:976-987.
17. Larsen D.H., Poinsignon C., Gudjonsson T., Dinant C., Payne M.R., Hari F.J., Rendtlew Danielsen J.M., Menard P., Sand J.C., Stucki M., et al. The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J.Cell Biol. 2010, 190:731-740.
18. 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 double-strand break repair. EMBO J. 2010, 29:1434-1445.
19. Liszt G., Ford E., Kurtev M., Guarente L. Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J.Biol. Chem. 2005, 280:21313-21320.
20. Lukas J., Lukas C., Bartek J. More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat. Cell Biol. 2011, 13:1161-1169.
21. Mao Z., Hine C., Tian X., Van Meter M., Au M., Vaidya A., Seluanov A., Gorbunova V. SIRT6 promotes DNA repair under stress by activating PARP1. Science 2011, 332:1443-1446.
22. McCord R.A., Michishita E., Hong T., Berber E., Boxer L.D., Kusumoto R., Guan S., Shi X., Gozani O., Burlingame A.L., et al. SIRT6 stabilizes DNA-dependent protein kinase at chromatin for DNA double-strand break repair. Aging (Albany NY) 2009, 1:109-121.
23. Michishita E., McCord R.A., Boxer L.D., Barber M.F., Hong T., Gozani O., Chua K.F. Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6. Cell Cycle 2009, 8:2664-2666.
24. Miller K.M., Tjeertes J.V., Coates J., Legube G., Polo S.E., Britton S., Jackson S.P. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat. Struct. Mol. Biol. 2010, 17:1144-1151.
25. Mostoslavsky R., Chua K.F., Lombard D.B., Pang W.W., Fischer M.R., Gellon L., Liu P., Mostoslavsky G., Franco S., Murphy M.M., et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 2006, 124:315-329.
26. Murr R., Loizou J.I., Yang Y.G., Cuenin C., Li H., Wang Z.Q., Herceg Z. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol. 2006, 8:91-99.
27. Nakamura K., Kato A., Kobayashi J., Yanagihara H., Sakamoto S., Oliveira D.V., Shimada M., Tauchi H., Suzuki H., Tashiro S., et al. Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol. Cell 2011, 41:515-528.
28. Neumann F.R., Dion V., Gehlen L.R., Tsai-Pflugfelder M., Schmid R., Taddei A., Gasser S.M. Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Genes Dev. 2012, 26:369-383.
29. Papamichos-Chronakis M., Peterson C.L. Chromatin and the genome integrity network. Nat. Rev. Genet. 2013, 14:62-75.
30. Papamichos-Chronakis M., Watanabe S., Rando O.J., Peterson C.L. Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 2011, 144:200-213.
31. 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. 2001, 15:3237-3242.
32. Polo S.E., Kaidi A., Baskcomb L., Galanty Y., Jackson S.P. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J. 2010, 29:3130-3139.
33. Schwer B., Schumacher B., Lombard D.B., Xiao C., Kurtev M.V., Gao J., Schneider J.I., Chai H., Bronson R.T., Tsai L.H., et al. Neural sirtuin 6 (Sirt6) ablation attenuates somatic growth and causes obesity. Proc. Natl. Acad. Sci. USA 2010, 107:21790-21794.
34. Sebastián C., Zwaans B.M., Silberman D.M., Gymrek M., Goren A., Zhong L., Ram O., Truelove J., Guimaraes A.R., Toiber D., et al. The histone deacetylase SIRT6 is a tumor suppressor that controls cancer metabolism. Cell 2012, 151:1185-1199.
35. Smeenk G., Wiegant W.W., Vrolijk H., Solari A.P., Pastink A., van Attikum H. The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J.Cell Biol. 2010, 190:741-749.
36. Smeenk G., Wiegant W.W., Marteijn J.A., Luijsterburg M.S., Sroczynski N., Costelloe T., Romeijn R.J., Pastink A., Mailand N., Vermeulen W., et al. Poly(ADP-ribosyl)ation links the chromatin remodeler SMARCA5/SNF2H to RNF168-dependent DNA damage signaling. J.Cell Sci. 2013, 126:889-903. Published online December 21, 2012. 10.1242/jcs.109413.
37. Tennen R.I., Berber E., Chua K.F. Functional dissection of SIRT6: identification of domains that regulate histone deacetylase activity and chromatin localization. Mech. Ageing Dev. 2010, 131:185-192.
38. Tjeertes J.V., Miller K.M., Jackson S.P. Screen for DNA-damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J. 2009, 28:1878-1889.
39. Toiber D., Sebastian C., Mostoslavsky R. Characterization of nuclear sirtuins: molecular mechanisms and physiological relevance. Handb Exp Pharmacol 2011, 206:189-224.
40. Wang J.H., Gostissa M., Yan C.T., Goff P., Hickernell T., Hansen E., Difilippantonio S., Wesemann D.R., Zarrin A.A., Rajewsky K., et al. Mechanisms promoting translocations in editing and switching peripheral Bcells. Nature 2009, 460:231-236.
41. Xu Y., Sun Y., Jiang X., Ayrapetov M.K., Moskwa P., Yang S., Weinstock D.M., Price B.D. The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J.Cell Biol. 2010, 191:31-43.
42. Xu Y., Ayrapetov M.K., Xu C., Gursoy-Yuzugullu O., Hu Y., Price B.D. Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol. Cell 2012, 48:723-733.
43. Yang B., Zwaans B.M., Eckersdorff M., Lombard D.B. The sirtuin SIRT6 deacetylates H3 K56Ac invivo to promote genomic stability. Cell Cycle 2009, 8:2662-2663.
44. Yuan J., Pu M., Zhang Z., Lou Z. Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle 2009, 8:1747-1753.
45. Zhong L., D'Urso A., Toiber D., Sebastian C., Henry R.E., Vadysirisack D.D., Guimaraes A., Marinelli B., Wikstrom J.D., Nir T., et al. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 2010, 140:280-293.