Implication of posttranslational histone modifications in nucleotide excision repair

International Journal of Molecular Sciences

Volumn 13, Issue 10, 2012, Pages 12461-12486

  Li, Shisheng ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Acetylation; Global genomic repair; Histone modifications; Methylation; Nucleotide excision repair; Phosphorylation; Ubiquitination

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; E1A ASSOCIATED P300 PROTEIN; FUNGAL PROTEIN; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE GCN5; HISTONE H2AX; HISTONE H3; MITOGEN ACTIVATED PROTEIN KINASE P38; NUCLEOTIDE; PROTEIN TIP60; UBIQUITIN; UNCLASSIFIED DRUG; CHROMATIN; HISTONE ACETYLTRANSFERASE PCAF;

DNA DAMAGE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME MECHANISM; ENZYME SPECIFICITY; EXCISION REPAIR; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HISTONE PHOSPHORYLATION; HISTONE UBIQUITINATION; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PROCESSING; REVIEW; ULTRAVIOLET RADIATION; CHROMATIN; DNA REPAIR; HUMAN; METABOLISM;

CHROMATIN; DNA REPAIR; HISTONE ACETYLTRANSFERASES; HISTONES; HUMANS; P300-CBP TRANSCRIPTION FACTORS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84867767219     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms131012461     Document Type: Review

References (139)

1. Luger, K.; Mader, A.W.; Richmond, R.K.; Sargent, D.F.; Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389, 251-260.
2. Kouzarides, T. Chromatin modifications and their function. Cell 2007, 128, 693-705.
3. Reardon, J.T.; Sancar, A. Nucleotide excision repair. Prog. Nucleic Acid Res. Mol. Biol. 2005, 79, 183-235.
4. Gillet, L.C.; Scharer, O.D. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem. Rev. 2006, 106, 253-276.
5. Nouspikel, T. DNA repair in mammalian cells: Nucleotide excision repair: Variations on versatility. Cell. Mol. Life Sci. 2009, 66, 994-1009.
6. Tatum, D.; Li, S. Nucleotide Excision Repair in S. cerevisiae. In DNA Repair/Book 1; Storici, F., Ed.; InTech Open Access Publisher, 2011; available online: http://www.intechopen.com/books/ dna-repair-on-the-pathways-to-fixing-dna-damage-and-errors/nucleotide-excision-repair-in-s-cerevisiae (accessed on 28 September 2012).
7. Waters, R.; Teng, Y.; Yu, Y.; Yu, S.; Reed, S.H. Tilting at windmills? The nucleotide excision repair of chromosomal DNA. DNA Repair (Amst.) 2009, 8, 146-152.
8. Fousteri, M.; Mullenders, L.H. Transcription-coupled nucleotide excision repair in mammalian cells: Molecular mechanisms and biological effects. Cell Res. 2008, 18, 73-84.
9. Hanawalt, P.C.; Spivak, G. Transcription-coupled DNA repair: Two decades of progress and surprises. Nat. Rev. Mol. Cell Biol. 2008, 9, 958-970.
10. Nag, R.; Smerdon, M.J. Altering the chromatin landscape for nucleotide excision repair. Mutat. Res. 2009, 682, 13-20.
11. Reed, S.H. Nucleotide excision repair in chromatin: Damage removal at the drop of a HAT. DNA Repair (Amst.) 2011, 10, 734-742.
12. Zhang, L.; Jones, K.; Gong, F. The molecular basis of chromatin dynamics during nucleotide excision repair. Biochem. Cell Biol. 2009, 87, 265-272.
13. Cao, J.; Yan, Q. Histone ubiquitination and deubiquitination in transcription, DNA damage response, and cancer. Front. Oncol. 2012, 2, 26.
14. Chatterjee, S.; Senapati, P.; Kundu, T.K. Post-translational modifications of lysine in DNA-damage repair. Essays Biochem. 2012, 52, 93-111.
15. Dinant, C.; Houtsmuller, A.B.; Vermeulen, W. Chromatin structure and DNA damage repair. Epigenet. Chromatin 2008, 1, 9.
16. Escargueil, A.E.; Soares, D.G.; Salvador, M.; Larsen, A.K.; Henriques, J.A. What histone code for DNA repair? Mutat. Res. 2008, 658, 259-270.
17. Greenberg, R.A. Histone tails: Directing the chromatin response to DNA damage. FEBS Lett. 2011, 585, 2883-2890.
18. Mendez-Acuna, L.; Di Tomaso, M.V.; Palitti, F.; Martinez-Lopez, W. Histone post-translational modifications in DNA damage response. Cytogenet. Genome Res. 2010, 128, 28-36.
19. Thomson, T.M.; Guerra-Rebollo, M. Ubiquitin and SUMO signalling in DNA repair. Biochem. Soc. Trans. 2010, 38, 116-131.
20. Zhu, Q.; Wani, A.A. Histone modifications: Crucial elements for damage response and chromatin restoration. J. Cell. Physiol. 2010, 223, 283-288.
21. Smerdon, M.J.; Lan, S.Y.; Calza, R.E.; Reeves, R. Sodium butyrate stimulates DNA repair in UV-irradiated normal and xeroderma pigmentosum human fibroblasts. J. Biol. Chem. 1982, 257, 13441-13447.
22. Ramanathan, B.; Smerdon, M.J. Changes in nuclear protein acetylation in u.v.-damaged human cells. Carcinogenesis 1986, 7, 1087-1094.
23. Ramanathan, B.; Smerdon, M.J. Enhanced DNA repair synthesis in hyperacetylated nucleosomes. J. Biol. Chem. 1989, 264, 11026-11034.
24. Lee, K.K.; Workman, J.L. Histone acetyltransferase complexes: One size doesn't fit all. Nat. Rev. Mol. Cell Biol. 2007, 8, 284-295.
25. Hodawadekar, S.C.; Marmorstein, R. Chemistry of acetyl transfer by histone modifying enzymes: Structure, mechanism and implications for effector design. Oncogene 2007, 26, 5528-5540.
26. Berton, T.R.; Mitchell, D.L.; Guo, R.; Johnson, D.G. Regulation of epidermal apoptosis and DNA repair by E2F1 in response to ultraviolet B radiation. Oncogene 2005, 24, 2449-2460.
27. Guo, R.; Chen, J.; Mitchell, D.L.; Johnson, D.G. GCN5 and E2F1 stimulate nucleotide excision repair by promoting H3K9 acetylation at sites of damage. Nucleic Acids Res. 2011, 39, 1390-1397.
28. Guo, R.; Chen, J.; Zhu, F.; Biswas, A.K.; Berton, T.R.; Mitchell, D.L.; Johnson, D.G. E2F1 localizes to sites of UV-induced DNA damage to enhance nucleotide excision repair. J. Biol. Chem. 2010, 285, 19308-19315.
29. Brand, M.; Moggs, J.G.; Oulad-Abdelghani, M.; Lejeune, F.; Dilworth, F.J.; Stevenin, J.; Almouzni, G.; Tora, L. UV-damaged DNA-binding protein in the TFTC complex links DNA damage recognition to nucleosome acetylation. EMBO J. 2001, 20, 3187-3196.
30. Martinez, E.; Palhan, V.B.; Tjernberg, A.; Lymar, E.S.; Gamper, A.M.; Kundu, T.K.; Chait, B.T.; Roeder, R.G. Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol. Cell. Biol. 2001, 21, 6782-6795.
31. Teng, Y.; Liu, H.; Gill, H.W.; Yu, Y.; Waters, R.; Reed, S.H. Saccharomyces cerevisiae Rad16 mediates ultraviolet-dependent histone H3 acetylation required for efficient global genome nucleotide-excision repair. EMBO Rep. 2008, 9, 97-102.
32. Yu, S.; Teng, Y.; Waters, R.; Reed, S.H. How chromatin is remodelled during DNA repair of UV-induced DNA damage in Saccharomyces cerevisiae. PLoS Genet. 2011, 7, e1002124.
33. Yu, Y.; Teng, Y.; Liu, H.; Reed, S.H.; Waters, R. UV irradiation stimulates histone acetylation and chromatin remodeling at a repressed yeast locus. Proc. Natl. Acad. Sci. USA 2005, 102, 8650-8655.
34. Battu, A.; Ray, A.; Wani, A.A. ASF1A and ATM regulate H3K56-mediated cell-cycle checkpoint recovery in response to UV irradiation. Nucleic Acids Res. 2011, 39, 7931-7945.
35. Cazzalini, O.; Perucca, P.; Savio, M.; Necchi, D.; Bianchi, L.; Stivala, L.A.; Ducommun, B.; Scovassi, A.I.; Prosperi, E. Interaction of p21(CDKN1A) with PCNA regulates the histone acetyltransferase activity of p300 in nucleotide excision repair. Nucleic Acids Res. 2008, 36, 1713-1722.
36. Hasan, S.; Hassa, P.O.; Imhof, R.; Hottiger, M.O. Transcription coactivator p300 binds PCNA and may have a role in DNA repair synthesis. Nature 2001, 410, 387-391.
37. Kuo, W.H.; Wang, Y.; Wong, R.P.; Campos, E.I.; Li, G. The ING1b tumor suppressor facilitates nucleotide excision repair by promoting chromatin accessibility to XPA. Exp. Cell Res. 2007, 313, 1628-1638.
38. Pedeux, R.; Sengupta, S.; Shen, J.C.; Demidov, O.N.; Saito, S.; Onogi, H.; Kumamoto, K.; Wincovitch, S.; Garfield, S.H.; McMenamin, M.; et al. ING2 regulates the onset of replicative senescence by induction of p300-dependent p53 acetylation. Mol. Cell. Biol. 2005, 25, 6639-6648.
39. Rubbi, C.P.; Milner, J. p53 is a chromatin accessibility factor for nucleotide excision repair of DNA damage. EMBO J. 2003, 22, 975-986.
40. Scott, M.; Bonnefin, P.; Vieyra, D.; Boisvert, F.M.; Young, D.; Bazett-Jones, D.P.; Riabowol, K. UV-induced binding of ING1 to PCNA regulates the induction of apoptosis. J. Cell Sci. 2001, 114, 3455-3462.
41. Vieyra, D.; Loewith, R.; Scott, M.; Bonnefin, P.; Boisvert, F.M.; Cheema, P.; Pastyryeva, S.; Meijer, M.; Johnston, R.N.; Bazett-Jones, D.P.; et al. Human ING1 proteins differentially regulate histone acetylation. J. Biol. Chem. 2002, 277, 29832-29839.
42. Wang, J.; Chin, M.Y.; Li, G. The novel tumor suppressor p33ING2 enhances nucleotide excision repair via inducement of histone H4 acetylation and chromatin relaxation. Cancer Res. 2006, 66, 1906-1911.
43. Driscoll, R.; Hudson, A.; Jackson, S.P. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 2007, 315, 649-652.
44. Han, J.; Zhou, H.; Horazdovsky, B.; Zhang, K.; Xu, R.M.; Zhang, Z. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 2007, 315, 653-655.
45. Schneider, J.; Bajwa, P.; Johnson, F.C.; Bhaumik, S.R.; Shilatifard, A. Rtt109 is required for proper H3K56 acetylation: A chromatin mark associated with the elongating RNA polymerase II. J. Biol. Chem. 2006, 281, 37270-37274.
46. Tsubota, T.; Berndsen, C.E.; Erkmann, J.A.; Smith, C.L.; Yang, L.; Freitas, M.A.; Denu, J.M.; Kaufman, P.D. Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol. Cell 2007, 25, 703-712.
47. Cheng, Z.; Ke, Y.; Ding, X.; Wang, F.; Wang, H.; Wang, W.; Ahmed, K.; Liu, Z.; Xu, Y.; Aikhionbare, F.; et al. Functional characterization of TIP60 sumoylation in UV-irradiated DNA damage response. Oncogene 2008, 27, 931-941.
48. Decker, P.V.; Yu, D.Y.; Iizuka, M.; Qiu, Q.; Smith, M.M. Catalytic-site mutations in the MYST family histone Acetyltransferase Esa1. Genetics 2008, 178, 1209-1220.
49. Campi, M.; D'Andrea, L.; Emiliani, J.; Casati, P. Participation of chromatin-remodeling proteins in the repair of ultraviolet-B-damaged DNA. Plant Physiol. 2012, 158, 981-995.
50. 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 (Amst.) 2007, 6, 383-395.
51. Chaudhuri, S.; Wyrick, J.J.; Smerdon, M.J. Histone H3 Lys79 methylation is required for efficient nucleotide excision repair in a silenced locus of Saccharomyces cerevisiae. Nucleic Acids Res. 2009, 37, 1690-1700.
52. Tatum, D.; Li, S. Evidence that the histone methyltransferase Dot1 mediates global genomic repair by methylating histone H3 on lysine 79. J. Biol. Chem. 2011, 286, 17530-17535.
53. Palomera-Sanchez, Z.; Bucio-Mendez, A.; Valadez-Graham, V.; Reynaud, E.; Zurita, M. Drosophila p53 is required to increase the levels of the dKDM4B demethylase after UV-induced DNA damage to demethylate histone H3 lysine 9. J. Biol. Chem. 2010, 285, 31370-31379.
54. Sanders, S.L.; Portoso, M.; Mata, J.; Bahler, J.; Allshire, R.C.; Kouzarides, T. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 2004, 119, 603-614.
55. Schotta, G.; Sengupta, R.; Kubicek, S.; Malin, S.; Kauer, M.; Callen, E.; Celeste, A.; Pagani, M.; Opravil, S.; De La Rosa-Velazquez, I.A.; et al. A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev. 2008, 22, 2048-2061.
56. Hanasoge, S.; Ljungman, M. H2AX phosphorylation after UV irradiation is triggered by DNA repair intermediates and is mediated by the ATR kinase. Carcinogenesis 2007, 28, 2298-2304.
57. Marti, T.M.; Hefner, E.; Feeney, L.; Natale, V.; Cleaver, J.E. H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 2006, 103, 9891-9896.
58. Matsumoto, M.; Yaginuma, K.; Igarashi, A.; Imura, M.; Hasegawa, M.; Iwabuchi, K.; Date, T.; Mori, T.; Ishizaki, K.; Yamashita, K.; et al. Perturbed gap-filling synthesis in nucleotide excision repair causes histone H2AX phosphorylation in human quiescent cells. J. Cell Sci. 2007, 120, 1104-1112.
59. Stiff, T.; Walker, S.A.; Cerosaletti, K.; Goodarzi, A.A.; Petermann, E.; Concannon, P.; O'Driscoll, M.; Jeggo, P.A. ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J. 2006, 25, 5775-5782.
60. Sen, S.P.; De Benedetti, A. TLK1B promotes repair of UV-damaged DNA through chromatin remodeling by Asf1. BMC Mol. Biol. 2006, 7, 37.
61. Shimada, M.; Niida, H.; Zineldeen, D.H.; Tagami, H.; Tanaka, M.; Saito, H.; Nakanishi, M. Chk1 is a histone H3 threonine 11 kinase that regulates DNA damage-induced transcriptional repression. Cell 2008, 132, 221-232.
62. Moore, J.D.; Yazgan, O.; Ataian, Y.; Krebs, J.E. Diverse roles for histone H2A modifications in DNA damage response pathways in yeast. Genetics 2007, 176, 15-25.
63. Tatum, D.; Li, W.; Placer, M.; Li, S. Diverse roles of RNA polymerase II-associated factor 1 complex in different subpathways of nucleotide excision repair. J. Biol. Chem. 2011, 286, 30304-30313.
64. Guerrero-Santoro, J.; Kapetanaki, M.G.; Hsieh, C.L.; Gorbachinsky, I.; Levine, A.S.; Rapic-Otrin, V. The cullin 4B-based UV-damaged DNA-binding protein ligase binds to UV-damaged chromatin and ubiquitinates histone H2A. Cancer Res. 2008, 68, 5014-5022.
65. Kapetanaki, M.G.; Guerrero-Santoro, J.; Bisi, D.C.; Hsieh, C.L.; Rapic-Otrin, V.; Levine, A.S. The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc. Natl. Acad. Sci. USA 2006, 103, 2588-2593.
66. Takedachi, A.; Saijo, M.; Tanaka, K. DDB2 complex-mediated ubiquitylation around DNA damage is oppositely regulated by XPC and Ku and contributes to the recruitment of XPA. Mol. Cell. Biol. 2010, 30, 2708-2723.
67. Wang, H.; Zhai, L.; Xu, J.; Joo, H.Y.; Jackson, S.; Erdjument-Bromage, H.; Tempst, P.; Xiong, Y.; Zhang, Y. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 2006, 22, 383-394.
68. Sugasawa, K.; Okuda, Y.; Saijo, M.; Nishi, R.; Matsuda, N.; Chu, G.; Mori, T.; Iwai, S.; Tanaka, K.; Tanaka, K.; et al. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 2005, 121, 387-400.
69. Groisman, R.; Polanowska, J.; Kuraoka, I.; Sawada, J.; Saijo, M.; Drapkin, R.; Kisselev, A.F.; Tanaka, K.; Nakatani, Y. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 2003, 113, 357-367.
70. Bergink, S.; Salomons, F.A.; Hoogstraten, D.; Groothuis, T.A.; de Waard, H.; Wu, J.; Yuan, L.; Citterio, E.; Houtsmuller, A.B.; Neefjes, J.; et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 2006, 20, 1343-1352.
71. Marteijn, J.A.; Bekker-Jensen, S.; Mailand, N.; Lans, H.; Schwertman, P.; Gourdin, A.M.; Dantuma, N.P.; Lukas, J.; Vermeulen, W. Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response. J. Cell Biol. 2009, 186, 835-847.
72. Zhu, Q.; Wani, G.; Arab, H.H.; El-Mahdy, M.A.; Ray, A.; Wani, A.A. Chromatin restoration following nucleotide excision repair involves the incorporation of ubiquitinated H2A at damaged genomic sites. DNA Repair (Amst.) 2009, 8, 262-273.
73. Grant, P.A.; Duggan, L.; Cote, J.; Roberts, S.M.; Brownell, J.E.; Candau, R.; Ohba, R.; Owen-Hughes, T.; Allis, C.D.; Winston, F.; et al. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: Characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev. 1997, 11, 1640-1650.
74. Ruiz-Garcia, A.B.; Sendra, R.; Pamblanco, M.; Tordera, V. Gcn5p is involved in the acetylation of histone H3 in nucleosomes. FEBS Lett. 1997, 403, 186-190.
75. Suka, N.; Suka, Y.; Carmen, A.A.; Wu, J.; Grunstein, M. Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol. Cell 2001, 8, 473-479.
76. Zhang, W.; Bone, J.R.; Edmondson, D.G.; Turner, B.M.; Roth, S.Y. Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase. EMBO J. 1998, 17, 3155-3167.
77. Ferreiro, J.A.; Powell, N.G.; Karabetsou, N.; Mellor, J.; Waters, R. Roles for Gcn5p and Ada2p in transcription and nucleotide excision repair at the Saccharomyces cerevisiae MET16 gene. Nucleic Acids Res. 2006, 34, 976-985.
78. Teng, Y.; Yu, Y.; Waters, R. The Saccharomyces cerevisiae histone acetyltransferase Gcn5 has a role in the photoreactivation and nucleotide excision repair of UV-induced cyclobutane pyrimidine dimers in the MFA2 gene. J. Mol. Biol. 2002, 316, 489-499.
79. Waters, R.; Evans, K.; Bennett, M.; Yu, S.; Reed, S.H. Nucleotide excision repair in cellular chromatin: Studies with yeast from nucleotide to gene to genome. Int. J. Mol. Sci. 2012, 13, 11141-11164.
80. Sterner, D.E.; Berger, S.L. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 2000, 64, 435-459.
81. Ogryzko, V.V.; Schiltz, R.L.; Russanova, V.; Howard, B.H.; Nakatani, Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996, 87, 953-959.
82. Zhao, Q.; Barakat, B.M.; Qin, S.; Ray, A.; El-Mahdy, M.A.; Wani, G.; Arafa el, S.; Mir, S.N.; Wang, Q.E.; Wani, A.A. The p38 mitogen-activated protein kinase augments nucleotide excision repair by mediating DDB2 degradation and chromatin relaxation. J. Biol. Chem. 2008, 283, 32553-32561.
83. Yin, D.T.; Wang, Q.; Chen, L.; Liu, M.Y.; Han, C.; Yan, Q.; Shen, R.; He, G.; Duan, W.; Li, J.J.; et al. Germline stem cell gene PIWIL2 mediates DNA repair through relaxation of chromatin. PLoS One 2011, 6, e27154.
84. 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.
85. Tang, Y.; Holbert, M.A.; Wurtele, H.; Meeth, K.; Rocha, W.; Gharib, M.; Jiang, E.; Thibault, P.; Verreault, A.; Cole, P.A.; et al. Fungal Rtt109 histone acetyltransferase is an unexpected structural homolog of metazoan p300/CBP. Nat. Struct. Mol. Biol. 2008, 15, 738-745.
86. Tillhon, M.; Cazzalini, O.; Nardo, T.; Necchi, D.; Sommatis, S.; Stivala, L.A.; Scovassi, A.I.; Prosperi, E. p300/CBP acetyl transferases interact with and acetylate the nucleotide excision repair factor XPG. DNA Repair (Amst.) 2012, doi.org/10.1016/j.dnarep.2012.08.001.
87. Marmorstein, R. Structure and function of histone acetyltransferases. Cell. Mol. Life Sci. 2001, 58, 693-703.
88. Ikura, T.; Ogryzko, V.V.; Grigoriev, M.; Groisman, R.; Wang, J.; Horikoshi, M.; Scully, R.; Qin, J.; Nakatani, Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000, 102, 463-473.
89. Bird, A.W.; Yu, D.Y.; Pray-Grant, M.G.; Qiu, Q.; Harmon, K.E.; Megee, P.C.; Grant, P.A.; Smith, M.M.; Christman, M.F. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 2002, 419, 411-415.
90. Casati, P.; Campi, M.; Chu, F.; Suzuki, N.; Maltby, D.; Guan, S.; Burlingame, A.L.; Walbot, V. Histone acetylation and chromatin remodeling are required for UV-B-dependent transcriptional activation of regulated genes in maize. Plant Cell 2008, 20, 827-842.
91. Greer, E.L.; Shi, Y. Histone methylation: A dynamic mark in health, disease and inheritance. Nat. Rev. Genet. 2012, 13, 343-357.
92. Nguyen, A.T.; Zhang, Y. The diverse functions of Dot1 and H3K79 methylation. Genes Dev. 2011, 25, 1345-1358.
93. 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.
94. Shanower, G.A.; Muller, M.; Blanton, J.L.; Honti, V.; Gyurkovics, H.; Schedl, P. Characterization of the grappa gene, the Drosophila histone H3 lysine 79 methyltransferase. Genetics 2005, 169, 173-184.
95. Jones, B.; Su, H.; Bhat, A.; Lei, H.; Bajko, J.; Hevi, S.; Baltus, G.A.; Kadam, S.; Zhai, H.; Valdez, R.; et al. The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet. 2008, 4, e1000190.
96. Janzen, C.J.; Hake, S.B.; Lowell, J.E.; Cross, G.A. Selective di- or trimethylation of histone H3 lysine 76 by two DOT1 homologs is important for cell cycle regulation in Trypanosoma brucei. Mol. Cell 2006, 23, 497-507.
97. 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.
98. 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.
99. Shahbazian, M.D.; Zhang, K.; Grunstein, M. Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1. Mol. Cell 2005, 19, 271-277.
100. Altaf, M.; Utley, R.T.; Lacoste, N.; Tan, S.; Briggs, S.D.; Cote, J. Interplay of chromatin modifiers on a short basic patch of histone H4 tail defines the boundary of telomeric heterochromatin. Mol. Cell 2007, 28, 1002-1014.
101. Fingerman, I.M.; Li, H.C.; Briggs, S.D. A charge-based interaction between histone H4 and Dot1 is required for H3K79 methylation and telomere silencing: Identification of a new trans-histone pathway. Genes Dev. 2007, 21, 2018-2029.
102. Oh, S.; Jeong, K.; Kim, H.; Kwon, C.S.; Lee, D. A lysine-rich region in Dot1p is crucial for direct interaction with H2B ubiquitylation and high level methylation of H3K79. Biochem. Biophys. Res. Commun. 2010, 399, 512-517.
103. Robzyk, K.; Recht, J.; Osley, M.A. Rad6-dependent ubiquitination of histone H2B in yeast. Science 2000, 287, 501-504.
104. Wood, A.; Krogan, N.J.; Dover, J.; Schneider, J.; Heidt, J.; Boateng, M.A.; Dean, K.; Golshani, A.; Zhang, Y.; Greenblatt, J.F.; et al. Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol. Cell 2003, 11, 267-274.
105. Krogan, N.J.; Dover, J.; Wood, A.; Schneider, J.; Heidt, J.; Boateng, M.A.; Dean, K.; Ryan, O.W.; Golshani, A.; Johnston, M.; et al. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: Linking transcriptional elongation to histone methylation. Mol. Cell 2003, 11, 721-729.
106. Ng, H.H.; Dole, S.; Struhl, K. The Rtf1 component of the Paf1 transcriptional elongation complex is required for ubiquitination of histone H2B. J. Biol. Chem. 2003, 278, 33625-33628.
107. Wood, A.; Schneider, J.; Dover, J.; Johnston, M.; Shilatifard, A. The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J. Biol. Chem. 2003, 278, 34739-34742.
108. Piro, A.S.; Mayekar, M.K.; Warner, M.H.; Davis, C.P.; Arndt, K.M. Small region of Rtf1 protein can substitute for complete Paf1 complex in facilitating global histone H2B ubiquitylation in yeast. Proc. Natl. Acad. Sci. USA 2012, 109, 10837-10842.
109. 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.
110. Friedberg, E.C.; Walker, G.C.; Siede, W.; Wood, R.D.; Schultz, R.A.; Ellenberger, T. DNA Repair and Mutagenesis, 2nd ed.; ASM Press: Washington, DC, USA, 2006.
111. Struhl, K. Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat. Struct. Mol. Biol. 2007, 14, 103-105.
112. Li, S.; Ding, B.; Lejeune, D.; Ruggiero, C.; Chen, X.; Smerdon, M.J. The roles of Rad16 and Rad26 in repairing repressed and actively transcribed genes in yeast. DNA Repair (Amst.) 2007, 6, 1596-1606.
113. Ng, H.H.; Ciccone, D.N.; Morshead, K.B.; Oettinger, M.A.; Struhl, K. Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: A potential mechanism for position-effect variegation. Proc. Natl. Acad. Sci. USA 2003, 100, 1820-1825.
114. Hughes, T.R.; Marton, M.J.; Jones, A.R.; Roberts, C.J.; Stoughton, R.; Armour, C.D.; Bennett, H.A.; Coffey, E.; Dai, H.; He, Y.D.; et al. Functional discovery via a compendium of expression profiles. Cell 2000, 102, 109-126.
115. 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.
116. Siede, W.; Allen, J.B.; Elledge, S.J.; Friedberg, E.C. The Saccharomyces cerevisiae MEC1 gene, which encodes a homolog of the human ATM gene product, is required for G1 arrest following radiation treatment. J. Bacteriol. 1996, 178, 5841-5843.
117. Lu, X.; Simon, M.D.; Chodaparambil, J.V.; Hansen, J.C.; Shokat, K.M.; Luger, K. The effect of H3K79 dimethylation and H4K20 trimethylation on nucleosome and chromatin structure. Nat. Struct. Mol. Biol. 2008, 15, 1122-1124.
118. Fink, M.; Thompson, J.S.; Thoma, F. Contributions of histone H3 nucleosome core surface mutations to chromatin structures, silencing and DNA repair. PLoS One 2011, 6, e26210.
119. Fernandez-Capetillo, O.; Lee, A.; Nussenzweig, M.; Nussenzweig, A. H2AX: The histone guardian of the genome. DNA Repair (Amst.) 2004, 3, 959-967.
120. Zou, L.; Elledge, S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003, 300, 1542-1548.
121. Revet, I.; Feeney, L.; Bruguera, S.; Wilson, W.; Dong, T.K.; Oh, D.H.; Dankort, D.; Cleaver, J.E. Functional relevance of the histone gammaH2Ax in the response to DNA damaging agents. Proc. Natl. Acad. Sci. USA 2011, 108, 8663-8667.
122. Fink, M.; Imholz, D.; Thoma, F. Contribution of the serine 129 of histone H2A to chromatin structure. Mol. Cell. Biol. 2007, 27, 3589-3600.
123. Oh, K.S.; Bustin, M.; Mazur, S.J.; Appella, E.; Kraemer, K.H. UV-induced histone H2AX phosphorylation and DNA damage related proteins accumulate and persist in nucleotide excision repair-deficient XP-B cells. DNA Repair (Amst.) 2011, 10, 5-15.
124. Vrouwe, M.G.; Pines, A.; Overmeer, R.M.; Hanada, K.; Mullenders, L.H. UV-induced photolesions elicit ATR-kinase-dependent signaling in non-cycling cells through nucleotide excision repair-dependent and -independent pathways. J. Cell Sci. 2011, 124, 435-446.
125. Fernandez-Capetillo, O.; Chen, H.T.; Celeste, A.; Ward, I.; Romanienko, P.J.; Morales, J.C.; Naka, K.; Xia, Z.; Camerini-Otero, R.D.; Motoyama, N.; et al. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 2002, 4, 993-997.
126. Clements, A.; Poux, A.N.; Lo, W.S.; Pillus, L.; Berger, S.L.; Marmorstein, R. Structural basis for histone and phosphohistone binding by the GCN5 histone acetyltransferase. Mol. Cell 2003, 12, 461-473.
127. Ivaldi, M.S.; Karam, C.S.; Corces, V.G. Phosphorylation of histone H3 at Ser10 facilitates RNA polymerase II release from promoter-proximal pausing in Drosophila. Genes Dev. 2007, 21, 2818-2831.
128. Welchman, R.L.; Gordon, C.; Mayer, R.J. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol. 2005, 6, 599-609.
129. Sun, Z.W.; Allis, C.D. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 2002, 418, 104-108.
130. Chandrasekharan, M.B.; Huang, F.; Sun, Z.W. Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc. Natl. Acad. Sci. USA 2009, 106, 16686-16691.
131. Chandrasekharan, M.B.; Huang, F.; Sun, Z.W. Histone H2B ubiquitination and beyond: Regulation of nucleosome stability, chromatin dynamics and the trans-histone H3 methylation. Epigenetics 2010, 5, 460-468.
132. Hannah, J.; Zhou, P. Regulation of DNA damage response pathways by the cullin-RING ubiquitin ligases. DNA Repair (Amst.) 2009, 8, 536-543.
133. Sugasawa, K. UV-DDB: A molecular machine linking DNA repair with ubiquitination. DNA Repair (Amst.) 2009, 8, 969-972.
134. Lan, L.; Nakajima, S.; Kapetanaki, M.G.; Hsieh, C.L.; Fagerburg, M.; Thickman, K.; Rodriguez-Collazo, P.; Leuba, S.H.; Levine, A.S.; Rapic-Otrin, V. Monoubiquitinated histone H2A destabilizes photolesion-containing nucleosomes with concomitant release of UV-damaged DNA-binding protein E3 ligase. J. Biol. Chem. 2012, 287, 12036-12049.
135. Bertolaet, B.L.; Clarke, D.J.; Wolff, M.; Watson, M.H.; Henze, M.; Divita, G.; Reed, S.I. UBA domains of DNA damage-inducible proteins interact with ubiquitin. Nat. Struct. Boil. 2001, 8, 417-422.
136. Ryu, K.S.; Lee, K.J.; Bae, S.H.; Kim, B.K.; Kim, K.A.; Choi, B.S. Binding surface mapping of intra- and interdomain interactions among hHR23B, ubiquitin, and polyubiquitin binding site 2 of S5a. J. Biol. Chem. 2003, 278, 36621-36627.
137. Parada, L.A.; McQueen, P.G.; Misteli, T. Tissue-specific spatial organization of genomes. Genome Biol. 2004, 5, R44.
138. Ernst, J.; Kheradpour, P.; Mikkelsen, T.S.; Shoresh, N.; Ward, L.D.; Epstein, C.B.; Zhang, X.; Wang, L.; Issner, R.; Coyne, M.; et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 2011, 473, 43-49.
139. Teng, Y.; Bennett, M.; Evans, K.E.; Zhuang-Jackson, H.; Higgs, A.; Reed, S.H.; Waters, R. A novel method for the genome-wide high resolution analysis of DNA damage. Nucleic Acids Res. 2011, 39, e10.