Regulation of tolerance to DNA alkylating damage by Dot1 and Rad53 in Saccharomyces cerevisiae

DNA Repair

Volumn 9, Issue 10, 2010, Pages 1038-1049

  Conde, Francisco ^a   Ontoso, David ^a   Acosta, Isabel ^a   Gallego Sánchez, Alfonso ^a   Bueno, Avelino ^a   San Segundo, Pedro A ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

DNA damage tolerance; Dot1; Histone modification; Rad53; TLS

Indexed keywords

CHECKPOINT KINASE 2; CYCLINE; DNA POLYMERASE REV1; HISTONE H3; HISTONE H3 LYSINE 79; HISTONE METHYLTRANSFERASE; MESYLIC ACID METHYL ESTER; PROTEIN DOT1; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CHROMOSOME; CONTROLLED STUDY; DNA ALKYLATION; DNA DAMAGE; DNA REPLICATION; ENZYME ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN METHYLATION; SACCHAROMYCES CEREVISIAE; TRANSLESION SYNTHESIS; UBIQUITINATION;

ALKYLATING AGENTS; CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; METHYL METHANESULFONATE; MUTAGENESIS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 77957321478     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2010.07.003     Document Type: Article

References (79)

1. Aguilera A., Gomez-Gonzalez B. Genome instability: a mechanistic view of its causes and consequences. Nat. Rev. Genet. 2008, 9:204-217.
2. Kastan M.B., Bartek J. Cell-cycle checkpoints and cancer. Nature 2004, 432:316-323.
3. Kerzendorfer C., O'Driscoll M. Human DNA damage response and repair deficiency syndromes: linking genomic instability and cell cycle checkpoint proficiency. DNA Repair 2009, 8:1139-1152.
4. Harrison J.C., Haber J.E. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 2006, 40:209-235.
5. Branzei D., Foiani M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell. Biol. 2010, 11:208-219.
6. Friedel A.M., Pike B.L., Gasser S.M. ATR/Mec1: coordinating fork stability and repair. Curr. Opin. Cell Biol. 2009, 21:237-244.
7. Ulrich H.D. The RAD6 pathway: control of DNA damage bypass and mutagenesis by ubiquitin and SUMO. Chembiochem 2005, 6:1735-1743.
8. Kunz B.A., Straffon A.F., Vonarx E.J. DNA damage-induced mutation: tolerance via translesion synthesis. Mutat. Res. 2000, 451:169-185.
9. Andersen P.L., Xu F., Xiao W. Eukaryotic DNA damage tolerance and translesion synthesis through covalent modifications of PCNA. Cell. Res. 2008, 18:162-173.
10. Waters L.S., Minesinger B.K., Wiltrout M.E., D'Souza S., Woodruff R.V., Walker G.C. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev. 2009, 73:134-154.
11. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002, 419:135-141.
12. Gallego-Sanchez A., Conde F., San Segundo P., Bueno A. Control of PCNA deubiquitylation in yeast. Biochem. Soc. Trans. 2010, 38:104-109.
13. Klein H.L. Reversal of fortune: Rad5 to the rescue. Mol. Cell 2007, 28:181-183.
14. Prakash S., Johnson R.E., Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 2005, 74:317-353.
15. Bao Y., Shen X. Chromatin remodeling in DNA double-strand break repair. Curr. Opin. Genet. Dev. 2007, 17:126-131.
16. Downey M., Durocher D. γH2AX as a checkpoint maintenance signal. Cell Cycle 2006, 5:1376-1381.
17. Downs J.A., Nussenzweig M.C., Nussenzweig A. Chromatin dynamics and the preservation of genetic information. Nature 2007, 447:951-958.
18. Peterson C.L., Cote J. Cellular machineries for chromosomal DNA repair. Genes Dev. 2004, 18:602-616.
19. Schleker T., Nagai S., Gasser S.M. Posttranslational modifications of repair factors and histones in the cellular response to stalled replication forks. DNA Repair 2009, 8:1089-1100.
20. van Attikum H., Gasser S.M. The histone code at DNA breaks: a guide to repair?. Nat. Rev. Mol. Cell. Biol. 2005, 6:757-765.
21. Falbo K.B., Alabert C., Katou Y., Wu S., Han J., Wehr T., Xiao J., He X., Zhang Z., Shi Y., Shirahige K., Pasero P., Shen X. Involvement of a chromatin remodeling complex in damage tolerance during DNA replication. Nat. Struct. Mol. Biol. 2009, 16:1167-1172.
22. Feng Q., Wang H., Ng H.H., Erdjument-Bromage H., Tempst P., Struhl K., Zhang Y. Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr. Biol. 2002, 12:1052-1058.
23. Lacoste N., Utley R.T., Hunter J.M., Poirier G.G., Cote J. Disruptor of telomeric silencing-1 is a chromatin-specific histone H3 methyltransferase. J. Biol. Chem. 2002, 277:30421-30424.
24. Ng H.H., Feng Q., Wang H., Erdjument-Bromage H., Tempst P., Zhang Y., Struhl K. Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev. 2002, 16:1518-1527.
25. van Leeuwen F., Gafken P.R., Gottschling D.E. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 2002, 109:745-756.
26. San-Segundo P.A., Roeder G.S. Role for the silencing protein Dot1 in meiotic checkpoint control. Mol. Biol. Cell 2000, 11:3601-3615.
27. Conde F., Refolio E., Cordon-Preciado V., Cortes-Ledesma F., Aragon L., Aguilera A., San-Segundo P.A. 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 2009, 182:437-446.
28. Bostelman L.J., Keller A.M., Albrecht A.M., Arat A., Thompson J.S. Methylation of histone H3 lysine-79 by Dot1p plays multiple roles in the response to UV damage in Saccharomyces cerevisiae. DNA Repair 2007, 6:383-395.
29. Game J.C., Williamson M.S., Baccari C. X-ray survival characteristics and genetic analysis for nine Saccharomyces deletion mutants that show altered radiation sensitivity. Genetics 2005, 169:51-63.
30. Game J.C., Williamson M.S., Spicakova T., Brown J.M. The RAD6/BRE1 histone modification pathway in Saccharomyces confers radiation resistance through a RAD51-dependent process that is independent of RAD18. Genetics 2006, 173:1951-1968.
31. Toh G.W., O'Shaughnessy A.M., Jimeno S., Dobbie I.M., Grenon M., Maffini S., O'Rorke A., Lowndes N.F. Histone H2A phosphorylation and H3 methylation are required for a novel Rad9 DSB repair function following checkpoint activation. DNA Repair 2006, 5:693-703.
32. Giannattasio M., Lazzaro F., Plevani P., Muzi-Falconi M. The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J. Biol. Chem. 2005, 280:9879-9886.
33. Wysocki R., Javaheri A., Allard S., Sha F., Cote J., Kron S.J. Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell. Biol. 2005, 25:8430-8443.
34. Conde F., San-Segundo P.A. Role of Dot1 in the response to alkylating DNA damage in Saccharomyces cerevisiae: regulation of DNA damage tolerance by the error-prone polymerases Polζ/Rev1. Genetics 2008, 179:1197-1210.
35. Guenther M.G., Lawton L.N., Rozovskaia T., Frampton G.M., Levine S.S., Volkert T.L., Croce C.M., Nakamura T., Canaani E., Young R.A. Aberrant chromatin at genes encoding stem cell regulators in human mixed-lineage leukemia. Genes Dev. 2008, 22:3403-3408.
36. Krivtsov A.V., Feng Z., Lemieux M.E., Faber J., Vempati S., Sinha A.U., Xia X., Jesneck J., Bracken A.P., Silverman L.B., Kutok J.L., Kung A.L., Armstrong S.A. H3K79 methylation profiles define murine and human MLL-AF4 leukemias. Cancer Cell 2008, 14:355-368.
37. Lin Y.H., Kakadia P.M., Chen Y., Li Y.Q., Deshpande A.J., Buske C., Zhang K.L., Zhang Y., Xu G.L., Bohlander S.K. Global reduction of the epigenetic H3K79 methylation mark and increased chromosomal instability in CALM-AF10-positive leukemias. Blood 2009, 114:651-658.
38. Okada Y., Feng Q., Lin Y., Jiang Q., Li Y., Coffield V.M., Su L., Xu G., Zhang Y. hDOT1L links histone methylation to leukemogenesis. Cell 2005, 121:167-178.
39. Okada Y., Jiang Q., Lemieux M., Jeannotte L., Su L., Zhang Y. Leukaemic transformation by CALM-AF10 involves upregulation of Hoxa5 by hDOT1L. Nat. Cell. Biol. 2006, 8:1017-1024.
40. Cordon-Preciado V., Ufano S., Bueno A. Limiting amounts of budding yeast Rad53 S-phase checkpoint activity results in increased resistance to DNA alkylation damage. Nucleic Acids Res. 2006, 34:5852-5862.
41. Longtine M.S., McKenzie A., 3rd D.J., Demarini N.G., Shah A., Wach A., Brachat P., Philippsen J.R., Pringle Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
42. Frederiks F., Tzouros M., Oudgenoeg G., van Welsem T., Fornerod M., Krijgsveld J., van Leeuwen F. Nonprocessive methylation by Dot1 leads to functional redundancy of histone H3K79 methylation states. Nat. Struct. Mol. Biol. 2008, 15:550-557.
43. Sym M., Engebrecht J.A., Roeder G.S. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 1993, 72:365-378.
44. San-Segundo P.A., Roeder G.S. Pch2 links chromatin silencing to meiotic checkpoint control. Cell 1999, 97:313-324.
45. Sawada K., Yang Z., Horton J.R., Collins R.E., Zhang X., Cheng X. Structure of the conserved core of the yeast Dot1p, a nucleosomal histone H3 lysine 79 methyltransferase. J. Biol. Chem. 2004, 279:43296-43306.
46. Fleming A.B., Kao C.F., Hillyer C., Pikaart M., Osley M.A. H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol. Cell 2008, 31:57-66.
47. Bergink S., Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 2009, 458:461-467.
48. Hishida T., Ohya T., Kubota Y., Kamada Y., Shinagawa H. Functional and physical interaction of yeast Mgs1 with PCNA: impact on RAD6-dependent DNA damage tolerance. Mol. Cell. Biol. 2006, 26:5509-5517.
49. Pellicioli A., Lucca C., Liberi G., Marini F., Lopes M., Plevani P., Romano A., Di Fiore P.P., Foiani M. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 1999, 18:6561-6572.
50. Bienko M., Green C.M., Crosetto N., Rudolf F., Zapart G., Coull B., Kannouche P., Wider G., Peter M., Lehmann A.R., Hofmann K., Dikic I. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 2005, 310:1821-1824.
51. D'Souza S., Waters L.S., Walker G.C. Novel conserved motifs in Rev1 C-terminus are required for mutagenic DNA damage tolerance. DNA Repair 2008, 7:1455-1470.
52. Guo C., Fischhaber P.L., Luk-Paszyc M.J., Masuda Y., Zhou J., Kamiya K., Kisker C., Friedberg E.C. Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J. 2003, 22:6621-6630.
53. Acharya N., Johnson R.E., Prakash S., Prakash L. Complex formation with Rev1 enhances the proficiency of Saccharomyces cerevisiae DNA polymerase ζ for mismatch extension and for extension opposite from DNA lesions. Mol. Cell. Biol. 2006, 26:9555-9563.
54. Lehmann A.R., Niimi A., Ogi T., Brown S., Sabbioneda S., Wing J.F., Kannouche P.L., Green C.M. Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair 2007, 6:891-899.
55. Zhuang Z., Johnson R.E., Haracska L., Prakash L., Prakash S., Benkovic S.J. Regulation of polymerase exchange between Polη and Polδ by monoubiquitination of PCNA and the movement of DNA polymerase holoenzyme. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:5361-5366.
56. Daigaku Y., Davies A.A., Ulrich H.D. Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature 2010, 465:951-955.
57. Karras G.I., Jentsch S. The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell 2010, 141:255-267.
58. Lopes M., Foiani M., Sogo J.M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 2006, 21:15-27.
59. Waters L.S., Walker G.C. The critical mutagenic translesion DNA polymerase Rev1 is highly expressed during G(2)/M phase rather than S phase. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:8971-8976.
60. Guo C., Tang T.S., Bienko M., Parker J.L., Bielen A.B., Sonoda E., Takeda S., Ulrich H.D., Dikic I., Friedberg E.C. Ubiquitin-binding motifs in REV1 protein are required for its role in the tolerance of DNA damage. Mol. Cell. Biol. 2006, 26:8892-8900.
61. Sabbioneda S., Bortolomai I., Giannattasio M., Plevani P., Muzi-Falconi M. Yeast Rev1 is cell cycle regulated, phosphorylated in response to DNA damage and its binding to chromosomes is dependent upon MEC1. DNA Repair 2007, 6:121-127.
62. Evans M.L., Bostelman L.J., Albrecht A.M., Keller A.M., Strande N.T., Thompson J.S. UV sensitive mutations in histone H3 in Saccharomyces cerevisiae that alter specific K79 methylation states genetically act through distinct DNA repair pathways. Curr. Genet. 2008, 53:259-274.
63. O'Neill B.M., Szyjka S.J., Lis E.T., Bailey A.O., Yates J.R., 3rd O.M., Aparicio F.E., Romesberg Pph3-Psy2 is a phosphatase complex required for Rad53 dephosphorylation and replication fork restart during recovery from DNA damage. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:9290-9295.
64. Szyjka S.J., Aparicio J.G., Viggiani C.J., Knott S., Xu W., Tavare S., Aparicio O.M. Rad53 regulates replication fork restart after DNA damage in Saccharomyces cerevisiae. Genes Dev. 2008, 22:1906-1920.
65. Segurado M., Tercero J.A. The S-phase checkpoint: targeting the replication fork. Biol. Cell 2009, 101:617-627.
66. Vazquez M.V., Rojas V., Tercero J.A. Multiple pathways cooperate to facilitate DNA replication fork progression through alkylated DNA. DNA Repair 2008, 7:1693-1704.
67. Tercero J.A., Diffley J.F. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 2001, 412:553-557.
68. Tercero J.A., Longhese M.P., Diffley J.F. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 2003, 11:1323-1336.
69. Bomar M.G., D'Souza S., Bienko M., Dikic I., Walker G.C., Zhou P. Unconventional ubiquitin recognition by the ubiquitin-binding motif within the Y family DNA polymerases ι and Rev1. Mol. Cell 2010, 37:408-417.
70. Guo C., Sonoda E., Tang T.S., Parker J.L., Bielen A.B., Takeda S., Ulrich H.D., Friedberg E.C. REV1 protein interacts with PCNA: significance of the REV1 BRCT domain in vitro and in vivo. Mol. Cell 2006, 23:265-271.
71. Edmunds C.E., Simpson L.J., Sale J.E. PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Mol. Cell 2008, 30:519-529.
72. Pages V., Santa Maria S.R., Prakash L., Prakash S. Role of DNA damage-induced replication checkpoint in promoting lesion bypass by translesion synthesis in yeast. Genes Dev. 2009, 23:1438-1449.
73. Dumstorf C.A., Mukhopadhyay S., Krishnan E., Haribabu B., McGregor W.G. REV1 is implicated in the development of carcinogen-induced lung cancer. Mol. Cancer Res. 2009, 7:247-254.
74. Frederiks F., Heynen G.J., van Deventer S.J., Janssen H., van Leeuwen F. Two Dot1 isoforms in Saccharomyces cerevisiae as a result of leaky scanning by the ribosome. Nucleic Acids Res. 2009, 37:7047-7058.
75. Rockmill B., Roeder G.S. Meiosis in asynaptic yeast. Genetics 1990, 126:563-574.
76. Zhao X., Muller E.G., Rothstein R. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 1998, 2:329-340.
77. Brachmann C.B., Davies A., Cost G.J., Caputo E., Li J., Hieter P., Boeke J.D. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 1998, 14:115-132.
78. Sikorski R.S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 1989, 122:19-27.
79. Christianson T.W., Sikorski R.S., Dante M., Shero J.H., Hieter P. Multifunctional yeast high-copy-number shuttle vectors. Gene 1992, 110:119-122.