An epigenetic code for DNA damage repair pathways?

Biochemistry and Cell Biology

Volumn 83, Issue 3, 2005, Pages 270-285

  Hassa, Paul O ^a   Hottiger, Michael O ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Acetylation; ChiP; DNA repair pathways; Epigenetic code; Histone modifications; Methylation; MS MS; Phosphorylation and mono(ADP ribosyl)ation

Indexed keywords

ACETYLATION; CELLS; GENES; HISTOLOGY; MUTAGENS;

CHIP; DNA REPAIR PATHWAYS; EPIGENETIC CODE; HISTONE MODIFICATIONS; METHYLATION; MS/MS; PHOSPHORYLATION AND MONO(ADP-RIBOSYL)ATION;

DNA;

ARGININE; BUTYRIC ACID; DNA DEPENDENT PROTEIN KINASE; DOUBLE STRANDED DNA; HISTONE; HISTONE DEACETYLASE; LYSINE; METHYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3 KINASE; SERINE;

ACETYLATION; CELL INTERACTION; CHROMATIN STRUCTURE; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA STRAND BREAKAGE; DRUG MECHANISM; EPIGENETICS; EXCISION REPAIR; GENE INTERACTION; GENETIC CODE; HUMAN; IMMUNOPRECIPITATION; METHYLATION; MISMATCH REPAIR; MOLECULAR INTERACTION; NONHUMAN; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; UBIQUITINATION;

ADENOSINE DIPHOSPHATE RIBOSE; ANIMALS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; FUNGAL PROTEINS; HISTONES; HUMANS; LYSINE; MACROMOLECULAR SUBSTANCES; MASS SPECTROMETRY; METHYLATION; PHOSPHORYLATION; RECOMBINATION, GENETIC; RIBOSE;

EUKARYOTA;

EID: 24744436674     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o05-034     Document Type: Review

References (172)

1. Adamietz, P., and Rudolph, A. 1984. ADP-ribosylation of nuclear proteins in vivo. Identification of histone H2B as a major acceptor for mono- and poly(ADP-ribose) in dimethyl sulfate-treated hepatoma AH 7974 cells. J Biol Chem. 259: 6841-6846.
2. Agresti, A., and Bianchi, M.E. 2003. HMGB proteins and gene expression. Curr. Opin. Genet. Dev. 13: 170-178.
3. Allison, S.J., and Milner, J. 2003. Loss of p53 has site-specific effects on histone H3 modification, including serine 10 phosphorylation important for maintenance of ploidy. Cancer Res. 63: 6674-6679.
4. Ame, J.C., Spenlehauer, C., and de Murcia, G. 2004. The PARP superfamily. Bioessays, 26: 882-893.
5. An, W., Kim, J., and Roeder, R.G. 2004. Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell, 117: 735-748.
6. Ausio, J., Abbott, D.W., Wang, X., and Moore, S.C. 2001. Histone variants and histone modifications: a structural perspective. Biochem. Cell Biol. 79: 693-708.
7. Bannister, A.J., Schneider, R., and Kouzarides, T. 2002. Histone methylation: dynamic or static? Cell, 109: 801-806.
8. Bassing, C.H., Chua, K.F., Sekiguchi, J., Suh, H., Whitlow, S.R., Fleming, J.C. et al. 2002. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. U.S.A. 99: 8173-8178.
9. Bauer, U.M., Daujat, S., Nielsen, S.J., Nightingale, K., and Kouzarides, T. 2002. Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Rep. 3: 39-44.
10. Bednar, J., Horowitz, R.A., Dubochet, J., and Woodcock, C.L. 1995. Chromatin conformation and salt-induced compaction: three-dimensional structural information from cryoelectron microscopy. J. Cell Biol. 131: 1365-1376.
11. Belmont, A.S., and Bruce, K. 1994. Visualization of G1 chromosomes: a folded, twisted, supercoiled chromonema model of interphase chromatid structure. J. Cell Biol. 127: 287-302.
12. Bernstein, C., Bernstein, H., Payne, C.M., and Garewal, H. 2002. DNA repair/pro-apoptotic dual-role proteins in five major DNA repair pathways: fail-safe protection against carcinogenesis. Mutat. Res. 511: 145-178.
13. Bhakat, K.K., Hazra, T.K., and Mitra, S. 2004. Acetylation of the human DNA glycosylase NEIL2 and inhibition of its activity. Nucleic Acids Res. 32: 3033-3039.
14. Bird, A.W., Yu, D.Y., Pray-Grant, M.G., Qiu, Q., Harmon, K.E., Megee, P.C. et al. 2002. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature (London), 419: 411-415.
15. Birger, Y., West, K.L., Postnikov, Y.V., Lim, J.H., Furusawa, T., Wagner, J.P. et al. 2003. Chromosomal protein HMGN1 enhances the rate of DNA repair in chromatin. EMBO J. 22: 1665-1675.
16. Blander, G., and Guarente, L. 2004. The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73: 417-435.
17. Bohm, L., Schneeweiss, F.A., Sharan, R.N., and Feinendegen, L.E. 1997. Influence of histone acetylation on the modification of cytoplasmic and nuclear proteins by ADP-ribosylation in response to free radicals. Biochim. Biophys. Acta, 1334: 149-154.
18. Bonaldi, T., Imhof, A., and Regula, J.T. 2004a. A combination of different mass spectroscopic techniques for the analysis of dynamic changes of histone modifications. Proteomics, 4: 1382-1396.
19. Bonaldi, T., Regula, J.T., and Imhof, A. 2004b The use of mass spectrometry for the analysis of histone modifications. Methods Enzymol. 377: 111-130.
20. Brand, M., Moggs, J.G., Oulad-Abdelghani, M., Lejeune, F., Dilworth, F.J., Stevenin, J. et al. 2001. UV-damaged DNA-binding protein in the TFTC complex links DNA damage recognition to nucleosome acetylation. EMBO J. 20: 3187-3196.
21. Brand, M., Yamamoto, K., Staub, A., and Tora, L. 1999. Identification of TATA-binding protein-free TAFII-containing complex subunits suggests a role in nucleosome acetylation and signal transduction. J. Biol. Chem. 274: 18285-18289.
22. Brehm, A., Tufteland, K.R., Aasland, R., and Becker, RB. 2004. The many colours of chromodomains. Bioessays, 26: 133-140.
23. Burma, S., Chen, B.P., Murphy, M., Kurimasa, A., and Chen, D.J. 2001. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276: 42462-42467.
24. Burzio, L.O., Riquelme, P.T., and Koide, S.S. 1979. ADP ribosylation of rat liver nucleosomal core histones. J. Biol. Chem. 254: 3029-3037.
25. Camporeale, G., Shubert, E.E., Sarath, G., Cerny, R., and Zempleni, J. 2004. K8 and K12 are biotinylated in human histone H4. Eur. J. Biochem. 271: 2257-2263.
26. Carrozza, M.J., Utley, R.T., Workman, J.L., and Cote, J. 2003. The diverse functions of histone acetyltransferase complexes. Trends Genet. 19: 321-329.
27. Catez, F., Lim, J.H., Hock, R., Postnikov, Y.V., and Bustin, M. 2003. HMGN dynamics and chromatin function. Biochem. Cell Biol. 81: 113-122.
28. Celeste, A., Petersen, S., Romanienko, P.J., Fernandez-Capetillo, O., Chen, H.T., Sedelnikova, O.A. et al. 2002. Genomic instability in mice lacking histone H2AX. Science (Wash.), 296: 922-927.
29. Chen, H.Y., Sun, J.M., Zhang, Y., Davie, J.R., and Meistrich, M.L. 1998. Ubiquitination of histone H3 in elongating spermatids of rat testes. J. Biol. Chem. 273: 13165-13169.
30. Cheung, P., Tanner, K.G., Cheung, W.L., Sassone-Corsi, P., Denu, J.M., and Allis, C.D. 2000. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell, 5: 905-915.
31. Clarke, A.S., Lowell, J.E., Jacobson, S.J., and Pillus, L. 1999. Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol. Cell. Biol. 19: 2515-2526.
32. Clements, A., Poux, A.N., Lo, W.S., Pillus, L., Berger, S.L., and Marmorstein, R. 2003. Structural basis for histone and phosphohistone binding by the GCN5 histone acetyltransferase. Mol. Cell, 12: 461-473.
33. Cline, S.D., and Hanawalt, P.C. 2003. Who's on first in the cellular response to DNA damage? Nat. Rev. Mol. Cell Biol. 4: 361-372.
34. Covic, M., Hassa, P.O., Saccani, S., Buerki, C., Meier, N.I., Lombardi, C. et al. 2005. Arginine methyltransferase CARM1 is a promo ter-specific regulator of NF-kappaB-dependent gene expression. EMBO J. 24: 85-96.
35. Cuthbert, G.L., Daujat, S., Snowden, A.W., Erdjument-Bromage, H., Hagiwara, T., Yamada, M. et al. 2004. Histone deimination antagonizes arginine methylation. Cell, 118: 545-553.
36. D'Amours, D., Desnoyers, S., D'Silva, I., and Poirier, G.G. 1999. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 342(2): 249-268.
37. de Ruijter, A.J., van Gennip, A.H., Caron, H.N., Kemp, S., and van Kuilenburg, A.B. 2003. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J. 370: 737-749.
38. Downs, J.A., Allard, S., Jobin-Robitaille, O., Javaheri, A., Auger, A., Bouchard, N. et al. 2004. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell, 16: 979-990.
39. Dresler, S.L. 1985. Stimulation of deoxyribonucleic acid excision repair in human fibroblasts pretreated with sodium butyrate. Biochemistry, 24: 6861-6869.
40. Dudas, A., and Chovanec, M. 2004. DNA double-strand break repair by homologous recombination. Mutat. Res. 566: 131-167.
41. Ehrenhofer-Murray, A.E. 2004. Chromatin dynamics at DNA replication, transcription and repair. Eur. J. Biochem. 271: 2335-2349.
42. Fernandez-Capetillo, O., Celeste, A., and Nussenzweig, A. 2003. Focusing on foci: H2AX and the recruitment of DNA-damage response factors. Cell Cycle, 2: 426-427.
43. Fernandez-Capetillo, O., Lee, A., Nussenzweig, M., and Nussenzweig, A. 2004a. H2AX: the histone guardian of the genome. DNA Repair (Amst.), 3: 959-967.
44. Fernandez-Capetillo, O., Allis, C.D., and Nussenzweig, A. 2004b. Phosphorylation of histone H2B at DNA double-strand breaks. J. Exp. Med. 199: 1671-1677.
45. Fischle, W., Wang, Y., and Allis, C.D. 2003. Histone and chromatin cross-talk. Curr. Opin. Cell Biol. 15: 172-183.
46. Fletcher, T.M., and Hansen, J.C. 1995. Core histone tail domains mediate oligonucleosome folding and nucleosomal DNA organization through distinct molecular mechanisms. J. Biol. Chem. 270: 25359-25362.
47. Fortini, P., Pascucci, B., Parlanti, E., D'Errico, M., Simonelli, V., and Dogliotti, E. 2003. 8-Oxoguanine DNA damage: at the crossroad of alternative repair pathways. Mutat. Res. 531: 127-139.
48. Friedberg, E.C., Hanaoka, F., Tanaka, K., Yasui, A., and Wilson, S.H. 2004. Report on the 2nd US-Japan DNA Repair Meeting. Honolulu, Hawai, 4-8 June 2004. DNA Repair (Amst.), 3: 1661-1674.
49. Furuta, T., Takemura, H., Liao, Z.Y., Aune, G.J., Redon, C., Sedelnikova, O.A. et al. 2003. Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replication-dependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J. Biol. Chem. 278: 20303-20312.
50. Game, J.C., Williamson, M.S., and Baccari, C. 2005. X-ray survival characteristics and genetic analysis for nine Saccharomyces deletion mutants that affect radiation sensitivity. Genetics, 169(1): 51-63. Available from http://www.genetics.org/cgi/ rapidpdf/genetics.104.028613v1 [accessed 15 September 2004].
51. Garcia-Salcedo, J.A., Gijon, P., Nolan, D.P., Tebabi, P., and Pays, E. 2003. A chromosomal SIR2 homologue with both histone NAD-dependent ADP-ribosyltransferase and deacetylase activities is involved in DNA repair in Trypanosoma brucei. EMBO J. 22: 5851-5862.
52. Gill, G. 2004. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18: 2046-2059.
53. Golderer, G., and Grobner, P. 1991. ADP-ribosylation of core histones and their acetylated subspecies. Biochem. J. 277(3): 607-610.
54. Gros, L., Delaporte, C., Frey, S., Decesse, J., de Saint-Vincent, B.R., Cavarec, L. et al. 2003. Identification of new drug sensitivity genes using genetic suppressor elements: protein arginine N-methyltransferase mediates cell sensitivity to DNA-damaging agents. Cancer Res. 63: 164-171.
55. Hanawalt, P.C. 1998. Genomic instability: environmental invasion and the enemies within. Mutat. Res. 400: 117-125.
56. Hanawalt, P.C., Crowley, D.J., Ford, J.M., Ganesan, A.K., Lloyd, D.R., Nouspikel, T. et al. 2000. Regulation of nucleotide excision repair in bacteria and mammalian cells. Cold Spring Harbor Symp. Quant. Biol. 65: 183-191.
57. Hasan, S., El-Andaloussi, N., Hardeland, U., Hassa, P.O., Burki, C., Imhof, R. et al. 2002. Acetylation regulates the DNA end-trimming activity of DNA polymerase beta. Mol. Cell, 10: 1213-1222.
58. Hasan, S., and Hottiger, M.O. 2002. Histone acetyl transferases: a role in DNA repair and DNA replication. J. Mol. Med. 80: 463-474.
59. Hasan, S., Stucki, M., Hassa, P.O., Imhof, R., Gehrig, P., Hunziker, P. et al. 2001. Regulation of human flap endonuclease-1 activity by acetylation through the transcriptional coactivator p300. Mol. Cell, 7: 1221-1231.
60. Hassa, P.O., and Hottiger, M.O. 2002. The functional role of poly(ADP-ribose)polymerase 1 as novel coactivator of NF-kappaB in inflammatory disorders. Cell Mol. Life Sci. 59: 1534-1553.
61. Hassa, P.O., Buerki, C., Lombardi, C., Imhof, R., and Hottiger, M.O. 2003. Transcriptional coactivation of nuclear factor-kappaB-dependent gene expression by p300 is regulated by poly(ADP)-ribose polymerase-1. J. Biol. Chem. 278: 45145-45153.
62. Haushalter, K.A., and Kadonaga, J.T. 2003. Chromatin assembly by DNA-translocating motors. Nat. Rev. Mol. Cell Biol. 4: 613-620.
63. He, S., Bauman, D., Davis, J.S., Loyola, A., Nishioka, K., Gronlund, J.L. et al. 2003. Facile synthesis of site-specifically acetylated and methylated histone proteins: reagents for evaluation of the histone code hypothesis. Proc. Natl. Acad. Sci. U.S.A. 100: 12033-12038.
64. Henneke, G., Koundrioukoff, S., and Hubscher, U. 2003. Phosphorylation of human Fen1 by cyclin-dependent kinase modulates its role in replication fork regulation. Oncogene, 22: 4301-4313.
65. Hsieh, P. 2001. Molecular mechanisms of DNA mismatch repair. Mutat. Res. 486: 71-87.
66. Hubscher, U., Maga, G., and Spadari, S. 2002. Eukaryotic DNA polymerases. Annu. Rev. Biochem. 71: 133-163.
67. Hung, C.M., and Li, C. 2004. Identification and phylogenetic analyses of the protein arginine methyltransferase gene family in fish and ascidians. Gene, 340: 179-187.
68. Huyen, Y., Zgheib, O., Ditullio, R.A., Jr., Gorgoulis, V.G., Zacharatos, P., Petty, T.J. et al. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature (London), 432: 406-411.
69. Ikura, T., Ogryzko, V.V., Grigoriev, M., Groisman, R., Wang, J., Horikoshi, M. et al. 2000. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell, 102: 463-473.
70. Jackson, S.P. 2002. Sensing and repairing DNA double-strand breaks. Carcinogenesis, 23: 687-696.
71. Jacobs, S.A., and Khorasanizadeh, S. 2002. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science (Wash.), 295: 2080-2083.
72. Jason, L.J., Moore, S.C., Lewis, J.D., Lindsey, G., and Ausio, J. 2002. Histone ubiquitination: a tagging tail unfolds? Bioessays, 24: 166-174.
73. Jazayeri, A., McAinsh, A.D., and Jackson, S.P. 2004. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc. Natl. Acad. Sci. U.S.A. 101: 1644-1649.
74. Jenuwein, T. 2001. Re-SET-ting heterochromatin by histone methyl-transferases. Trends Cell Biol. 11: 266-273.
75. Jenuwein, T., and Allis, C.D. 2001. Translating the histone code. Science (Wash.), 293: 1074-1080.
76. Kalkhoven, E. 2004. CBP and p300: HATs for different occasions. Biochem. Pharmacol. 68: 1145-1155.
77. Kanai, Y., Miwa, M., Matsushima, T., and Sugimura, T. 1978. Comparative studies on antibody and antibody production to poly(ADP-ribose) in mice. Immunology, 34: 501-508.
78. Kanai, Y., Moroi, Y., Yokohari, R., and Goto, S. 1983. Profiles of antibodies to poly(ADP-ribose), left-handed Z-DNA, and other nuclear constituents in systemic lupus erythematosus and progressive systemic sclerosis. Princess Takamatsu Symp. 13: 93-100.
79. Kanai, Y., Akatsuka, T., Kubota, T., Goto, S., and Stollar, B.D. 1985. MRL/Mp-lpr/lpr mouse derived monoclonal antibodies that recognise determinants shared by poly (ADP-ribose), single stranded DNA and left handed Z-DNA. Clin. Exp. Immunol. 59: 139-145.
80. Khorasanizadeh, S. 2004. The nucleosome: from genomic organization to genomic regulation. Cell, 116: 259-272.
81. Kim, M.Y., Mauro, S., Gevry, N., Lis, J.T., and Kraus, W.L. 2004. NAD(+)-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell, 119: 803-814.
82. Kobayashi, J., Tauchi, H., Sakamoto, S., Nakamura, A., Morishima, K., Matsuura, S. et al. 2002. NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12: 1846-1851.
83. Kreimeyer, A., Wielckens, K., Adamietz, P., and Hilz, H. 1984. DNA repair-associated ADP-ribosylation in vivo. Modification of histone H1 differs from that of the principal acceptor proteins. J. Biol. Chem. 259: 890-896.
84. Kurdistani, S.K., and Grunstein, M. 2003. Histone acetylation and deacetylation in yeast. Nat. Rev. Mol. Cell. Biol. 4: 276-284.
85. Kusch, T., Florens, L., Macdonald, W.H., Swanson, S.K., Glaser, R.L., Yates, J.R. III et al. 2004. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science (Wash.), 306: 2084-2087.
86. Lachner, M., and Jenuwein, T. 2002. The many faces of histone lysine methylation. Curr. Opin. Cell Biol. 14: 286-298.
87. Lachner, M., O'Sullivan, R.J., and Jenuwein, T. 2003. An epigenetic road map for histone lysine methylation. J. Cell Sci. 116: 2117-2124.
88. Lee, J.S., Latimer, L.J., and Sibley, J.T. 1989. Detection of unusual nucleic acids with monoclonal antibodies specific for triplexes, poly(ADP-ribose), DNA-RNA hybrids, and Z-DNA. Anal. Biochem. 178: 373-377.
89. Lindahl, T., and Barnes, D.E. 2000. Repair of endogenous DNA damage. Cold Spring Harb. Symp. Quant. Biol. 65: 127-133.
90. Lindahl, T., and Wood, R.D. 1999. Quality control by DNA repair. Science (Wash.), 286: 1897-1905.
91. Lindahl, T., Satoh, M.S., Poirier, G.G., and Klungland, A. 1995. Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem. Sci. 20: 405-411.
92. Ljungman, M., and Lane, D.P. 2004. Transcription -guarding the genome by sensing DNA damage. Nat. Rev. Cancer, 4: 727-737.
93. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature (London), 389: 251-260.
94. Lukas, J., Lukas, C., and Bartek, J. 2004. Mammalian cell cycle checkpoints: signalling pathways and their organization in space and time. DNA Repair (Amst.), 3: 997-1007.
95. Lusser, A., and Kadonaga, J.T. 2003. Chromatin remodeling by ATP-dependent molecular machines. Bioessays, 25: 1192-1200.
96. Malanga, M., and Farina, B. 2000. Noncovalent binding of poly(ADP-ribose) to nuclear matrix proteins: developmental changes and tissue specificity. Biol. Chem. 381: 1047-1053.
97. Malik, H.S., and Henikoff, S. 2003. Phylogenomics of the nucleosome. Nat. Struct. Biol. 10: 882-891.
98. Manke, I.A., Lowery, D.M., Nguyen, A., and Yaffe, M.B. 2003. BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science (Wash.), 302: 636-639.
99. Marmorstein, R. 2001. Protein modules that manipulate histone tails for chromatin regulation. Nat. Rev. Mol. Cell Biol. 2: 422-432.
100. Min, J., Zhang, Y., and Xu, R.M. 2003. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev. 17: 1823-1828.
101. Moore, J.D., and Krebs, J.E. 2004. Histone modifications and DNA double-strand break repair. Biochem. Cell Biol. 82: 446-452.
102. Mutskov, V., Gerber, D., Angelov, D., Ausio, J., Workman, J., and Dimitrov, S. 1998. Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding. Mol. Cell. Biol. 18: 6293-6304.
103. Narang, M.A., Dumas, R., Ayer, L.M., and Gravel, R.A. 2004. Reduced histone biotinylation in multiple carboxylase deficiency patients: a nuclear role for holocarboxylase synthetase. Hum. Mol. Genet. 13: 15-23.
104. Narlikar, G.J., Fan, H.Y., and Kingston, R.E. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell, 108: 475-487.
105. 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.
106. Nielsen, P.R., Nietlispach, D., Mott, H.R., Callaghan, J., Bannister, A., Kouzarides, T. et al. 2002. Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature (London), 416: 103-107.
107. Nowak, S.J., and Corces, V.G. 2004. Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet. 20: 214-220.
108. Ogata, N., Ueda, K., and Hayaishi, O. 1980a. ADP-ribosylation of histone H2B. Identification of glutamic acid residue 2 as the modification site. J. Biol. Chem. 255: 7610-7615.
109. Ogata, N., Ueda, K., Kagamiyama, H., and Hayaishi, O. 1980b. ADP-ribosylation of histone H1. Identification of glutamic acid residues 2, 14, and the COOH-terminal lysine residue as modification sites. J. Biol. Chem. 255: 7616-7620.
110. Okayama, H., Edson, C.M., Fukushima, M., Ueda, K., and Hayaishi, O. 1977. Purification and properties of poly(adenosine diphosphate ribose) synthetase. J. Biol. Chem. 252: 7000-7005.
111. Okayama, H., Ueda, K., and Hayaishi, O. 1978. Purification of ADP-ribosylated nuclear proteins by covalent chromatography on dihydroxyboryl polyacrylamide beads and their characterization. Proc. Natl. Acad. Sci. U.S.A. 75: 1111-1115.
112. Osley, M.A. 2004. H2B ubiquitylation: the end is in sight. Biochim. Biophys. Acta, 1677: 74-78.
113. Pal, S., Vishwanath, S.N., Erdjument-Bromage, H., Tempst, P., and Sif, S. 2004. Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes. Mol. Cell Biol. 24: 9630-9645.
114. Park, E.J., Chan, D.W., Park, J.H., Oettinger, M.A., and Kwon, J. 2003. DNA-PK is activated by nucleosomes and phosphorylates H2AX within the nucleosomes in an acetylation-dependent manner. Nucleic Acids Res. 31: 6819-6827.
115. Paull, T.T., Rogakou, E.P., Yamazaki, V., Kirchgessner, C.U., Gellert, M., and Bonner, W.M. 2000. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10: 886-895.
116. Peters, D.M., Griffin, J.B., Stanley, J.S., Beck, M.M., and Zempleni, J. 2002. Exposure to UV light causes increased biotinylation of histones in Jurkat cells. Am. J. Physiol. Cell Physiol. 283: C878-C884.
117. Peterson, C.L. 2002. Chromatin remodeling enzymes: taming the machines. Third in review series on chromatin dynamics. EMBO Rep. 3: 319-322.
118. Peterson, C.L., and Cote, J. 2004. Cellular machineries for chromosomal DNA repair. Genes Dev. 18: 602-616.
119. Peterson, C.L., and Laniel, M.A. 2004. Histones and histone modifications. Curr. Biol. 14: R546-R551.
120. Pham, A.D., and Sauer, F. 2000. Ubiquitin-activating/conjugating activity of TAFII250, a mediator of activation of gene expression in Drosophila. Science (Wash.), 289: 2357-2360.
121. Pleschke, J.M., Kleczkowska, H.E., Strohm, M., and Althaus, F.R. 2000. Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem. 275: 40974-40980.
122. Prigent, C., and Dimitrov, S. 2003. Phosphorylation of serine 10 in histone H3, what for? J. Cell Sci. 116: 3677-3685.
123. Qin, S., and Parthun, M.R. 2002. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol. Cell Biol. 22: 8353-8365.
124. Ramanathan, B., and Smerdon, M.J. 1989. Enhanced DNA repair synthesis in hyperacetylated nucleosomes. J. Biol. Chem. 264: 11026-11034.
125. Rea, S., Eisenhaber, F., O'Carroll, D., Strahl, B.D., Sun, Z.W., Schmid, M. et al. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature (London), 406: 593-599.
126. Reeves, R. 2001. Molecular biology of HMGA proteins: hubs of nuclear function. Gene, 277: 63-81.
127. Richmond, T.J., and Davey, C.A. 2003. The structure of DNA in the nucleosome core. Nature (London), 423: 145-150.
128. Richmond, T.J., Rechsteiner, T., and Luger, K. 1993. Studies of nucleosome structure. Cold Spring Harbor Symp. Quant. Biol. 58: 265-272.
129. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S., and Bonner, W.M. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273: 5858-5868.
130. Rogakou, E.P., Boon, C., Redon, C., and Bonner, W.M. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146: 905-916.
131. Sanders, S.L., Portoso, M., Mata, J., Bahler, J., Allshire, R.C., and Kouzarides, T. 2004. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell, 119: 603-614.
132. Scharer, O.D. 2003. Chemistry and biology of DNA repair. Angew Chem. Int. Ed. Engl. 42: 2946-2974.
133. Schreiber, S.L., and Bernstein, B.E. 2002. Signaling network model of chromatin. Cell, 111: 771-778.
134. Schurter, B.T., Koh, S.S., Chen, D., Bunick, G.J., Harp, J.M., Hanson, B.L. et al. 2001. Methylation of histone H3 by coactivator-associated arginine methyltransferase 1. Biochemistry, 40: 5747-5756.
135. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J.R., Cole, P.A. et al. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell, 119: 941-953.
136. Shiio, Y., and Eisenman, R.N. 2003. Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. U.S.A. 100: 13225-13230.
137. Shiloh, Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer, 3: 155-168.
138. Sibley, J.T., Braun, R.P., and Lee, J.S. 1986. The production of antibodies to DNA in normal mice following immunization with poly(ADP-ribose). Clin. Exp. Immunol. 64: 563-569.
139. Sibley, J.T., Latimer, L.J., and Lee, J.S. 1988. Shared idiotypes on anti-DNA and anti-poly (ADP-ribose) antibodies. J. Immunol. 140: 3502-3507.
140. Slupphaug, G., Kavli, B., and Krokan, H.E. 2003. The interacting pathways for prevention and repair of oxidative DNA damage. Mutat. Res. 531: 231-251.
141. Smerdon, M.J., Lan, S.Y., Calza, R.E., and Reeves, R. 1982. Sodium butyrate stimulates DNA repair in UV-irradiated normal and xeroderma pigmentosum human fibroblasts. J. Biol. Chem. 257: 13441-13447.
142. Stanley, J.S., Griffin, J.B., and Zempleni, J. 2001. Biotinylation of histones in human cells. Effects of cell proliferation. Eur. J. Biochem. 268: 5424-5429.
143. Stiff, T., O'Driscoll, M., Rief, N., Iwabuchi, K., Lobrich, M., and Jeggo, P.A. 2004. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64: 2390-2396.
144. Strahl, B.D., and Allis, C.D. 2000. The language of covalent histone modifications. Nature (London), 403: 41-45.
145. Strahl, B.D., Briggs, S.D., Brame, C.J., Caldwell, J.A., Koh, S.S., Ma, H. et al. 2001. Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr. Biol. 11: 996-1000.
146. Stucki, M., and Jackson, S.P. 2004. Tudor domains track down DNA breaks. Nat. Cell Biol. 6: 1150-1152.
147. Sugasawa, K., Ng, J.M., Masutani, C., Iwai, S., van der Spek, P.J., Eker, A.P. et al. 1998. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell, 2: 223-232.
148. Thomas, J.O. 2001. HMG1 and 2: architectural DNA-binding proteins. Biochem. Soc. Trans. 29: 395-401.
149. Thompson, L.H., and Schild, D. 2002. Recombinational DNA repair and human disease. Mutat. Res. 509: 49-78.
150. Tini, M., Benecke, A., Um, S.J., Torchia, J., Evans, R.M., and Chambon, P. 2002. Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol. Cell, 9: 265-277.
151. Trievel, R.C. 2004. Structure and function of histone methyltransferases. Crit. Rev. Eukaryot. Gene. Expr. 14: 147-169.
152. Tsukiyama, T., and Wu, C. 1997. Chromatin remodeling and transcription. Curr. Opin. Genet. Dev. 7: 182-191.
153. Turner, B.M. 2000. Histone acetylation and an epigenetic code. Bioessays, 22: 836-845.
154. Turner, B.M. 2002. Cellular memory and the histone code. Cell, 111: 285-291.
155. Ushiroyama, T., Tanigawa, Y., Tsuchiya, M., Matsuura, R., Ueki, M., Sugimoto, O. et al. 1985. Amino acid sequence of histone H1 at the ADP-ribose-accepting site and ADP-ribose X histone-H1 adduct as an inhibitor of cyclic-AMP-dependent phosphorylation. Eur J. Biochem. 151: 173-177.
156. Utley, R.T., and Cote, J. 2003. The MYST family of histone acetyltransferases. Curr. Top. Microbiol. Immunol. 274: 203-236.
157. van Gool, A.J., Citterio, E., Rademakers, S., van Os, R., Vermeulen, W., Constantinou, A. et al. 1997. The Cockayne syndrome B protein, involved in transcription-coupled DNA repair, resides in an RNA polymerase II-containing complex. EMBO J. 16: 5955-5965.
158. Vaquero, A., Loyola, A., and Reinberg, D. 2003. The constantly changing face of chromatin. Sci. Aging Knowledge Environ. 2003: RE4.
159. Verdin, E., Dequiedt, F., and Kasler, H.G. 2003. Class II histone deacetylases: versatile regulators. Trends Genet. 19: 286-293.
160. Wang, H., Cao, R., Xia, L., Erdjument-Bromage, H., Borchers, C., Tempst, P. et al. 2001. Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol. Cell. 8: 1207-1217.
161. Wang, Y., Wysocka, J., Sayegh, J., Lee, Y.H., Perlin, J.R., Leonelli, L. et al. 2004. Human PAD4 regulates histone arginine methylation levels via demethylimination. Science (Wash.), 306: 279-283.
162. Wang, Z.Q., Auer, B., Stingl, L., Berghammer, H., Haidacher, D., Schweiger, M. et al. 1995. Mice lacking ADPRT and poly(ADP-ribosyl) ation develop normally but are susceptible to skin disease. Genes Dev. 9: 509-520.
163. Ward, I.M., and Chen, J. 2001. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276: 47759-47762.
164. Wielckens, K., Bredehorst, R., Adamietz, P., and Hilz, H. 1982. Mono ADP-ribosylation and poly ADP-ribosylation of proteins in normal and malignant tissues. Adv. Enzyme Regul. 20: 23-37.
165. Woodcock, C.L., and Dimitrov, S. 2001. Higher-order structure of chromatin and chromosomes. Curr. Opin. Genet. Dev. 11: 130-135.
166. Woodcock, C.L., and Horowitz, R.A. 1995. Chromatin organization re-viewed. Trends Cell Biol. 5: 272-277.
167. Woodcock, C.L., Grigoryev, S.A., Horowitz, R.A., and Whitaker, N. 1993. A chromatin folding model that incorporates linker variability generates fibers resembling the native structures. Proc. Natl. Acad. Sci. U.S.A. 90: 9021-9025.
168. Yoshihara, K., Hashida, T., Yoshihara, H., Tanaka, Y., and Ohgushi, H. 1977. Enzyme-bound early product of purified poly(ADP-ribose) polymerase. Biochem. Biophys. Res. Commun. 78: 1281-1288.
169. Yuan, F., Gu, L., Guo, S., Wang, C., and Li, G.M. 2004. Evidence for involvement of HMGB1 protein in human DNA mismatch repair. J. Biol. Chem. 279: 20935-20940.
170. Zeitlin, S.G., Shelby, R.D., and Sullivan, K.F. 2001. CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. J. Cell Biol. 155: 1147-1157.
171. Zeng, L., and Zhou, M.M. 2002. Bromodomain: an acetyl-lysine binding domain. FEBS Lett. 513: 124-128.
172. Zong, W.X., Ditsworth, D., Bauer, D.E., Wang, Z.Q., and Thompson, C.B. 2004. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev. 18: 1272-1282.