Reduced histone biosynthesis and chromatin changes arising from a damage signal at telomeres

Nature Structural and Molecular Biology

Volumn 17, Issue 10, 2010, Pages 1218-1225

  O'Sullivan, Roderick J ^a   Kubicek, Stefan ^b,e   Schreiber, Stuart L ^b,c,d   Karlseder, Jan ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c HARVARD UNIVERSITY   (United States)

^d HARVARD UNIVERSITY   (United States)

^e ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HISTONE; HISTONE H3; HISTONE H4;

ARTICLE; CELL AGING; CELL CYCLE; CELLULAR DISTRIBUTION; CHROMATIN; CHROMOSOMAL INSTABILITY; CHROMOSOME DAMAGE; CHROMOSOME REPLICATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; DNA DAMAGE RESPONSE; EPIGENETICS; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; TELOMERE;

BLEOMYCIN; CELL AGING; CELL LINE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA DAMAGE; DNA REPLICATION; EPIGENESIS, GENETIC; FIBROBLASTS; HISTONES; HUMANS; METHYLATION; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; NUCLEAR PROTEINS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS E7 PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; REPRESSOR PROTEINS; RETINOBLASTOMA PROTEIN; TELOMERE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77957814604     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1897     Document Type: Article

References (56)

1. Kaygun, H. & Marzluff, W.F. Translation termination is involved in histone mRNA degradation when DNA replication is inhibited. Mol. Cell. Biol. 25, 6879-6888 (2005).
2. Su, C. et al. DNA damage induces downregulation of histone gene expression through the G1 checkpoint pathway. EMBO J. 23, 1133-1143 (2004).
3. Groth, A. et al. Human Asf1 regulates the fow of S phase histones during replicational stress. Mol. Cell 17, 301-311 (2005).
4. Hoek, M. & Stillman, B. Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc. Natl. Acad. Sci. USA 100, 12183-12188 (2003).
5. Das, C., Lucia, M.S., Hansen, K.C. & Tyler, J.K. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459, 113-117 (2009).
6. Tjeertes, J.V., Miller, K.M. & Jackson, S.P. Screen for DNA-damage-responsive histone modifcations identifes H3K9Ac and H3K56Ac in human cells. EMBO J. 28, 1878-1889 (2009).
7. Bunz, F. et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282, 1497-1501 (1998).
8. Wang, Z.F., Whitfeld, M.L., Ingledue, T.C. III, Dominski, Z. & Marzluff, W.F. The protein that binds the 3′ end of histone mRNA: a novel RNA-binding protein required for histone pre-mRNA processing. Genes Dev. 10, 3028-3040 (1996).
9. Whitfeld, M.L. et al. Stem-loop binding protein, the protein that binds the 3′ end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms. Mol. Cell. Biol. 20, 4188-4198 (2000).
10. Zhang, Z., Shibahara, K. & Stillman, B. PCNA connects DNA replication to epigenetic inheritance in yeast. Nature 408, 221-225 (2000).
11. Gérard, A. et al. The replication kinase Cdc7-Dbf4 promotes the interaction of the p150 subunit of chromatin assembly factor 1 with proliferating cell nuclear antigen. EMBO Rep. 7, 817-823 (2006).
12. Juan, G., Hernando, E. & Cordon-Cardo, C. Separation of live cells in different phases of the cell cycle for gene expression analysis. Cytometry 49, 170-175 (2002).
13. Kouzarides, T. Chromatin modifcations and their function. Cell 128, 693-705 (2007).
14. Bernstein, B.E. et al. Genomic maps and comparative analysis of histone modifcations in human and mouse. Cell 120, 169-181 (2005).
15. Fischle, W. et al. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17, 1870-1881 (2003).
16. Francis, N.J., Follmer, N.E., Simon, M.D., Aghia, G. & Butler, J.D. Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro. Cell 137, 110-122 (2009).
17. Goldstein, S. Replicative senescence: the human fbroblast comes of age. Science 249, 1129-1133 (1990).
18. Chen, E.S. et al. Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451, 734-737 (2008).
19. Kloc, A., Zaratiegui, M., Nora, E. & Martienssen, R. RNA interference guides histone modifcation during the S phase of chromosomal replication. Curr. Biol. 18, 490-495 (2008).
20. Peters, A.H. et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12, 1577-1589 (2003).
21. Imai, S., Armstrong, C.M., Kaeberlein, M. & Guarente, L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403, 795-800 (2000).
22. Michishita, E. et al. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452, 492-496 (2008).
23. Chen, C.C. et al. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134, 231-243 (2008).
24. Hayashi, R. et al. Transcriptional regulation of human chromatin assembly factor ASF1. DNA Cell Biol. 26, 91-99 (2007).
25. Jasencakova, Z. et al. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 37, 736-743 (2010).
26. Harper, J.W. & Elledge, S.J. The DNA damage response: ten years after. Mol. Cell 28, 739-745 (2007).
27. Petrini, J.H. & Stracker, T.H. The cellular response to DNA double-strand breaks: defning the sensors and mediators. Trends Cell Biol. 13, 458-462 (2003).
28. Stracker, T.H., Couto, S.S., Cordon-Cardo, C., Matos, T. & Petrini, J.H. Chk2 suppresses the oncogenic potential of DNA replication-associated DNA damage. Mol. Cell 31, 21-32 (2008).
29. Scaffdi, P. & Misteli, T. Lamin A-dependent nuclear defects in human aging. Science 312, 1059-1063 (2006).
30. Stewart, S.A. et al. Telomerase contributes to tumorigenesis by a telomere length-independent mechanism. Proc. Natl. Acad. Sci. USA 99, 12606-12611 (2002).
31. Blasco, M.A. The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 8, 299-309 (2007).
32. Grunstein, M. Yeast heterochromatin: Regulation of its assembly and inheritance by histones. Cell 93, 325-328 (1998).
33. Bianchi, A. & Shore, D. Early replication of short telomeres in budding yeast. Cell 128, 1051-1062 (2007).
34. Meeks-Wagner, D. & Hartwell, L.H. Normal stoichiometry of histone dimer sets is necessary for high fdelity of mitotic chromosome transmission. Cell 44, 43-52 (1986).
35. Steger, D.J. & Workman, J.L. Transcriptional analysis of purifed histone acetyltransferase complexes. Methods 19, 410-416 (1999).
36. Harris, M.E. et al. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol. Cell. Biol. 11, 2416-2424 (1991).
37. Dominski, Z., Zheng, L.X., Sanchez, R. & Marzluff, W.F. Stem-loop binding protein facilitates 3′-end formation by stabilizing U7 snRNP binding to histone pre-mRNA. Mol. Cell. Biol. 19, 3561-3570 (1999).
38. Groth, A. et al. Regulation of replication fork progression through histone supply and demand. Science 318, 1928-1931 (2007).
39. Dang, W. et al. Histone H4 lysine 16 acetylation regulates cellular lifespan. Nature 459, 802-807 (2009).
40. Michishita, E. et al. Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6. Cell Cycle 8, 2664-2666 (2009).
41. Recht, J. et al. Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modifcation associated with S phase in mitosis and meiosis. Proc. Natl. Acad. Sci. USA 103, 6988-6993 (2006).
42. Li, Q. et al. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134, 244-255 (2008).
43. Maas, N.L., Miller, K.M., DeFazio, L.G. & Toczyski, D.P. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol. Cell 23, 109-119 (2006).
44. Schotta, G. et al. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18, 1251-1262 (2004).
45. Feng, Q. et al. Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr. Biol. 12, 1052-1058 (2002).
46. van Leeuwen, F., Gafken, P.R. & Gottschling, D.E. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109, 745-756 (2002).
47. Nishioka, K. et al. PR-Set7 is a nucleosome-specifc methyltransferase that modifes lysine 20 of histone H4 and is associated with silent chromatin. Mol. Cell 9, 1201-1213 (2002).
48. Altaf, M. et al. Interplay of chromatin modifers on a short basic patch of histone H4 tail defnes the boundary of telomeric heterochromatin. Mol. Cell 28, 1002-1014 (2007).
49. d'Adda di Fagagna,F. et al., A DNA damage checkpoint response in telomere-initiated senescence, Nature, 426, 194-198, 2003
50. Denchi, E.L. & de Lange, T. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448, 1068-1071 (2007).
51. Takai, H., Smogorzewska, A. & de Lange, T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13, 1549-1556 (2003).
52. 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).
53. Crabbe, L., Verdun, R.E., Haggblom, C.I. & Karlseder, J. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306, 1951-1953 (2004).
54. Fodor, B.D. et al. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev. 20, 1557-1562 (2006).
55. Verdun, R.E. & Karlseder, J. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127, 709-720 (2006).
56. Azuara, V. Profling of DNA replication timing in unsynchronized cell populations. Nat. Protoc. 1, 2171-2177 (2006).