Histone H3 K79 methylation states play distinct roles in UV-induced sister chromatid exchange and cell cycle checkpoint arrest in Saccharomyces cerevisiae

Nucleic Acids Research

Volumn 42, Issue 10, 2014, Pages 6286-6299

  Rossodivita, Alyssa A ^a   Boudoures, Anna L ^a   Mecoli, Jonathan P ^a   Steenkiste, Elizabeth M ^a   Karl, Andrea L ^a   Vines, Eudora M ^a   Cole, Arron M ^a   Ansbro, Megan R ^a   Thompson, Jeffrey S ^a  

^a DENISON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; HEME OXYGENASE ENDONUCLEASE; HISTONE H3; HYDROXYUREA; UNCLASSIFIED DRUG;

ADE2 GENE; ARTICLE; BRE1 GENE; CELL CYCLE REGULATION; CELL SURVIVAL; CELL SYNCHRONIZATION; COMPARATIVE STUDY; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DOT1 GENE; DOUBLE STRANDED DNA BREAK; EPISTASIS; FUNGAL GENE; FUNGUS MUTANT; G1 PHASE CELL CYCLE CHECKPOINT; GENE CONVERSION; GENE MUTATION; HISTONE DIMETHYLATION; HISTONE METHYLATION; HISTONE TRIMETHYLATION; HISTONE UBIQUITINATION; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RAD5 GENE; RADIATION EXPOSURE; RADIOSENSITIVITY; RECOMBINATION REPAIR; SACCHAROMYCES CEREVISIAE; SENSITIVITY ANALYSIS; SISTER CHROMATID EXCHANGE; SURVIVAL RATE; TRP1 GENE; ULTRAVIOLET RADIATION;

DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; G1 PHASE CELL CYCLE CHECKPOINTS; HISTONES; HYDROXYUREA; METHYLATION; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID EXCHANGE; UBIQUITINATION; ULTRAVIOLET RAYS;

EID: 84903181716     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku242     Document Type: Article

References (49)

1. Jackson, S.P. and Bartek, J. (2009) The DNA-damage response in human biology and disease. Nature, 461, 1071-1078.
2. Kupiec, M. (2000) Damage-induced recombination in the yeast Saccharomyces cerevisiae. Mutat. Res., 451, 91-105.
3. Thoma, F. (2005) Repair of UV lesions in nucleosomes-intrinsic properties and remodeling. DNA Repair (Amst), 4, 855-869.
4. Friedberg, E.C., Walker, G.C., Siede, W., Wood, R.D., Schultz, R.A. and Ellenberger, T. (2006) DNA Repair and Mutagenesis, 2nd edn. ASM Press, Washington, DC.
5. Prakash, S. and Prakash, L. (2000) Nucleotide excision repair in yeast. Mutat. Res., 451, 13-24.
6. Kadyk, L.C. and Hartwell, L.H. (1993) Replication-dependent sister chromatid recombination in rad1 mutants of Saccharomyces cerevisiae. Genetics, 133, 469-487.
7. Gangavarapu, V., Prakash, S. and Prakash, L. (2007) Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in saccharomyces cerevisiae. Mol. Cell. Biol., 27, 7758-7764.
8. Aboussekhra, A. and Al-Sharif, I.S. (2005) Homologous recombination is involved in transcription-coupled repair of UV damage in Saccharomyces cerevisiae. EMBO J., 24, 1999-2010.
9. Dinant, C., Houtsmuller, A.B. and Vermeulen, W. (2008) Chromatin structure and DNA damage repair. Epigenetics Chromatin, 1, doi:10.1186/1756- 8935-1-9.
10. van Attikum, H. and Gasser, S.M. (2005) The histone code at DNA breaks: a guide to repair? Nat. Rev. Mol. Cell Biol., 6, 757-765.
11. Bostelman, L.J., Keller, A.M., Albrecht, A.M., Arat, A. and Thompson, J.S. (2007) Methylation of histone H3 lysine-79 by Dot1p plays multiple roles in the response to UV damage in Saccharomyces cerevisiae. DNA Repair (Amst.), 6, 383-395.
12. Evans, M.L., Bostelman, L.J., Albrecht, A.M., Keller, A.M., Strande, N.T. and Thompson, J.S. (2008) UV sensitive mutations in histone H3 in Saccharomyces cerevisiae that alter specific K79 methylation states genetically act through distinct DNA repair pathways. Curr. Genet., 53, 259-274.
13. Conde, F. and San-Segundo, P.A. (2008) Role of Dot1 in the response to alkylating DNA damage in Saccharomyces cerevisiae: regulation of DNA damage tolerance by the error-prone polymerases Polzeta/Rev1. Genetics, 179, 1197-1210.
14. Toh, G.W., O'Shaughnessy, A.M., Jimeno, S., Dobbie, I.M., Grenon, M., Maffini, S., O'Rorke, A. and Lowndes, N.F. (2006) Histone H2A phosphorylation and H3 methylation are required for a novel Rad9 DSB repair function following checkpoint activation. DNA Repair (Amst.), 5, 693-703.
15. Giannattasio, M., Lazzaro, F., Plevani, P. and Muzi-Falconi, M. (2005) The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J. Biol. Chem., 280, 9879-9886.
16. Wysocki, R., Javaheri, A., Allard, S., Sha, F., Cote, J. and Kron, S.J. (2005) Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell. Biol., 25, 8430-8443.
17. Huyen, Y., Zgheib, O., Ditullio, R.A. Jr, Gorgoulis, V.G., Zacharatos, P., Petty, T.J., Sheston, E.A., Mellert, H.S., Stavridi, E.S. and Halazonetis, T.D. (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature, 432, 406-411.
18. Lazzaro, F., Sapountzi, V., Granata, M., Pellicioli, A., Vaze, M., Haber, J.E., Plevani, P., Lydall, D. and Muzi-Falconi, M. (2008) Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J., 27, 1502-1512.
19. Kim, W., Choi, M. and Kim, J.E. (2014) The histone methyltransferase Dot1/DOT1L as a critical regulator of the cell cycle. Cell Cycle, 13, 726-738.
20. Chaudhuri, S., Wyrick, J.J. and Smerdon, M.J. (2009) Histone H3 Lys79 methylation is required for efficient nucleotide excision repair in a silenced locus of Saccharomyces cerevisiae. Nucleic Acids Res., 37, 1690-1700.
21. Tatum, D. and Li, S. (2011) Evidence that the histone methyltransferase Dot1 mediates global genomic repair by methylating histone H3 on lysine 79. J. Biol. Chem., 286, 17530-17535.
22. Fink, M., Thompson, J.S. and Thoma, F. (2011) Contributions of histone H3 nucleosome core surface mutations to chromatin structures, silencing and DNA repair. PLoS One, 6, e26210.
23. Game, J.C., Williamson, M.S., Spicakova, T. and Brown, J.M. (2006) The RAD6/BRE1 histone modification pathway in Saccharomyces confers radiation resistance through a RAD51-dependent process that is independent of RAD18. Genetics, 173, 1951-1968.
24. Conde, F., Refolio, E., Cordon-Preciado, V., Cortes-Ledesma, F., Aragon, L., Aguilera, A. and San-Segundo, P.A. (2009) The Dot1 histone methyltransferase and the Rad9 checkpoint adaptor contribute to cohesin-dependent double-strand break repair by sister chromatid recombination in Saccharomyces cerevisiae. Genetics, 182, 437-446.
25. Ng, H.H., Feng, Q., Wang, H., Erdjument-Bromage, H., Tempst, P., Zhang, Y. and Struhl, K. (2002) Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev., 16, 1518-1527.
26. van Leeuwen, F., Gafken, P.R. and Gottschling, D.E. (2002) Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell, 109, 745-756.
27. Ng, H.H., Xu, R.M., Zhang, Y. and Struhl, K. (2002) Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J. Biol. Chem., 277, 34655-34657.
28. Sun, Z.W. and Allis, C.D. (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature, 418, 104-108.
29. Shahbazian, M.D., Zhang, K. and Grunstein, M. (2005) Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1. Mol. Cell, 19, 271-277.
30. Johnson, R.E., Henderson, S.T., Petes, T.D., Prakash, S., Bankmann, M. and Prakash, L. (1992) Saccharomyces cerevisiae RAD5-encoded DNA repair protein contains DNA helicase and zinc-binding sequence motifs and affects the stability of simple repetitive sequences in the genome. Mol. Cell. Biol., 12, 3807-3818.
31. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P. and Boeke, J.D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast, 14, 115-132.
32. Mozlin, A.M., Fung, C.W. and Symington, L.S. (2008) Role of the Saccharomyces cerevisiae Rad51 paralogs in sister chromatid recombination. Genetics, 178, 113-126.
33. Pringle, J.R. and Hartwell, L.H. (1981) The Saccharomyces cerevisiae cell cycle. In: Strathern, JN, Jones, EW and Broach, JR (eds.) The Molecular Biology of the Yeast Saccharomyces. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 97-142.
34. Lea, D.E. and Coulson, C.A. (1949) The distribution of the numbers of mutants in bacterial populations. J. Genet., 49, 264-285.
35. Spell, R.M. and Jinks-Robertson, S. (2004) Determination of mitotic recombination rates by fluctuation analysis in Saccharomyces cerevisiae. Methods Mol. Biol., 262, 3-12.
36. Glowczewski, L., Waterborg, J.H. and Berman, J.G. (2004) Yeast chromatin assembly complex 1 protein excludes nonacetylatable forms of histone H4 from chromatin and the nucleus. Mol. Cell. Biol., 24, 10180-10192.
37. Herskowitz, I. and Jensen, R.E. (1991) Putting the HO gene to work: practical uses for mating-type switching. Meth. Enzymol., 194, 132-146.
38. Elvers, I., Johansson, F., Groth, P., Erixon, K. and Helleday, T. (2011) UV stalled replication forks restart by re-priming in human fibroblasts. Nucleic Acids Res., 39, 7049-7057.
39. Fasullo, M. and Sun, M. (2008) UV but not X rays stimulate homologous recombination between sister chromatids and homologs in a Saccharomyces cerevisiae mec1 (ATR) hypomorphic mutant. Mutat. Res., 648, 73-81.
40. Friedl, A.A., Liefshitz, B., Steinlauf, R. and Kupiec, M. (2001) Deletion of the SRS2 gene suppresses elevated recombination and DNA damage sensitivity in rad5 and rad18 mutants of Saccharomyces cerevisiae. Mutat. Res., 486, 137-146.
41. Blastyak, A., Pinter, L., Unk, I., Prakash, L., Prakash, S. and Haracska, L. (2007) Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol. Cell, 28, 167-175.
42. Haber, J.E. (2012) Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics, 191, 33-64.
43. Nakanishi, S., Lee, J.S., Gardner, K.E., Gardner, J.M., Takahashi, Y.H., Chandrasekharan, M.B., Sun, Z.W., Osley, M.A., Strahl, B.D., Jaspersen, S.L. et al. (2009) Histone H2BK123 monoubiquitination is the critical determinant for H3K4 and H3K79 trimethylation by COMPASS and Dot1. J. Cell Biol., 186, 371-377.
44. Siede, W., Friedberg, A.S. and Friedberg, E.C. (1993) RAD9-dependent G1 arrest defines a second checkpoint for damaged DNA in the cell cycle of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A., 90, 7985-7989.
45. de la Torre-Ruiz, M.A., Green, C.M. and Lowndes, N.F. (1998) RAD9 and RAD24 define two additive, interacting branches of the DNA damage checkpoint pathway in budding yeast normally required for Rad53 modification and activation. EMBO J., 17, 2687-2698.
46. Schulze, J.M., Jackson, J., Nakanishi, S., Gardner, J.M., Hentrich, T., Haug, J., Johnston, M., Jaspersen, S.L., Kobor, M.S. and Shilatifard, A. (2009) Linking cell cycle to histone modifications: SBF and H2B monoubiquitination machinery and cell-cycle regulation of H3K79 dimethylation. Mol. Cell, 35, 626-641.
47. Game, J.C., Williamson, M.S. and Baccari, C. (2005) X-ray survival characteristics and genetic analysis for nine Saccharomyces deletion mutants that show altered radiation sensitivity. Genetics, 169, 51-63.
48. Thompson, J.S., Ling, X. and Grunstein, M. (1994) Histone H3 amino terminus is required for telomeric and silent mating locus repression in yeast. Nature, 369, 245-247.
49. Thompson, J.S., Snow, M.L., Giles, S., McPherson, L.E. and Grunstein, M. (2003) Identification of a functional domain within the essential core of histone H3 that is required for telomeric and HM silencing in Saccharomyces cerevisiae. Genetics, 163, 447-452.