Nucleotide excision repair and photolyase repair of UV photoproducts in nucleosomes: Assessing the existence of nucleosome and non-nucleosome rDNA chromatin in vivo

Biochemistry and Cell Biology

Volumn 87, Issue 1, 2009, Pages 337-346

  Tremblay, Maxime ^a   Toussaint, Martin ^a   D'Amours, Annie ^a   Conconi, Antonio ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Chromatin; Cyclobutane pyrimidine dimer; Nucleosome; Nucleotide excision repair; Photolyase; Psoralen cross linking; rDNA; Ribosomal genes; RNA polymerase I; UV

Indexed keywords

CHROMATIN; CYCLOBUTANE PYRIMIDINE DIMER; NUCLEOSOME; NUCLEOTIDE EXCISION REPAIR; PHOTOLYASE; PSORALEN CROSS-LINKING; RDNA; RIBOSOMAL GENES; RNA POLYMERASE I; UV;

BUTANE; DNA; GENES; GENETIC ENGINEERING; NUCLEIC ACIDS; NUCLEOTIDES; POLYMERS; RNA; TRANSCRIPTION; ULTRAVIOLET DEVICES;

REPAIR;

DEOXYRIBODIPYRIMIDINE PHOTOLYASE; RIBOSOME DNA;

CHROMATIN; DNA DAMAGE; DNA PACKAGING; DNA REPAIR; DNA STRUCTURE; EXCISION REPAIR; GENE EXPRESSION; HUMAN; IN VIVO STUDY; NONHUMAN; NUCLEOSOME; PROTEIN FUNCTION; REVIEW; ULTRAVIOLET RADIATION;

ANIMALS; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DNA DAMAGE; DNA REPAIR; DNA, RIBOSOMAL; HUMANS; NUCLEOSOMES; ULTRAVIOLET RAYS;

EID: 65249147157     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O08-128     Document Type: Review

References (128)

1. Aboussekhra, A., and Thoma, F. 1998. Nucleotide excision repair and photolyase preferentially repair the nontranscribed strand of RNA polymerase III-transcribed genes in Saccharomyces cerevisiae. Genes Dev. 12: 411-421. doi:10.1101/gad.12.3.411. PMID:9450934.
2. Araki, M., Masutani, C., Maekawa, T., Watanabe, Y., Yamada, A., Kusumoto, R., et al. 2000. Reconstitution of damage DNA excision reaction from SV40 minichromosomes with purified nucleotide excision repair proteins. Mutat. Res. 459: 147-160. PMID:10725665.
3. Banditt, M., Koller, T., and Sogo, J.M. 1999. Transcriptional activity and chromatin structure of enhancer-deleted rRNA genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 4953-4960. PMID:10373545.
4. Bohr, V.A., Smith, C.A., Okumoto, D.S., and Hanawalt, P.C. 1985. DNA repair in an active gene: removal of pyrimidine dimmers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell, 40: 359-369. doi:10.1016/0092-8674(85)90150-3. PMID:3838150.
5. Brown, D.W., Libertini, L.J., Suquet, C., Small, E.W., and Smerdon, M.J. 1993. Unfolding of nucleosome cores dramatically changes the distribution of ultraviolet photoproducts in DNA. Biochemistry, 32: 10527-10531. doi:10.1021/bi00091a001. PMID:8399198.
6. Bucceri, A., Kapitza, K., and Thoma, F. 2006. Rapid accessibility of nucleosomal DNA in yeast on a second time scale. EMBO J. 25: 3123-3132. doi:10.1038/sj.emboj.7601196. PMID:16778764.
7. Carell, T., Burgdorf, L.T., Kundu, L.M., and Cichon, M. 2001. The mechanism of action of DNA photolyases. Curr. Opin. Chem. Biol. 5: 491-498. doi:10.1016/S1367-5931(00)00239-8. PMID:11578921.
8. Cavalli, G., and Thoma, F. 1993. Chromatin transitions during activation and repression of galactose-regulated genes in yeast. EMBO J. 12: 4603-4613. PMID:8223470.
9. Cavalli, G., Bachmann, D., and Thoma, F. 1996. Inactivation of to-poisomerases affects transcription-dependent chromatin transitions in rDNA but not in a gene transcribed by RNA polymerase II. EMBO J. 15: 590-597. PMID:8599942.
10. Citterio, E., Van Den Boom, V., Schnitzler, G., Kanaar, R., Bonte, E., Kingston, R.E., et al. 2000. ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol. Cell. Biol. 20: 7643-7653. doi:10.1128/ MCB.20.20.7643-7653.2000. PMID:11003660.
11. Conconi, A. 2005. The yeast rDNA locus: a model system to study DNA repair in chromatin. DNA Repair (Amst.), 4: 897-908. doi:10.1016/j. dnarep.2005.04.008. PMID:15996904.
12. Conconi, A., Widmer, R.M., Koller, T., and Sogo, J.M. 1989. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell, 57: 753-776. doi:10.1016/0092-8674(89)90790-3. PMID:2720786.
13. Conconi, A., Sogo, J.M., and Ryan, C.A. 1992. Ribosomal gene clusters are uniquely proportioned between open and closed chromatin structures in both tomato leaf cells and exponentially growing suspension cultures. Proc. Natl. Acad. Sci. U.S.A. 89: 5256-5260. doi:10.1073/pnas.89.12.5256. PMID:11607297.
14. Conconi, A., Bespalov, V., and Smerdon, M.J. 2002. Transcription coupled repair in RNA polymerase I transcribed genes of yeast. Proc. Natl. Acad. Sci. U.S.A. 99: 649-654. doi:10.1073/pnas. 022373099. PMID:11782531.
15. Conconi, A., Paquette, M., Fahy, D., Bespalov, V.A., and Smerdon, M.J. 2005a. Repair-independent chromatin assembly onto active ribosomal genes in yeast after UV irradiation. Mol. Cell. Biol. 25: 9773-9783. doi:10.1128/MCB.25.22.9773-9783.2005. PMID: 16260595.
16. Conconi, A., Bespalov, V.A., Fahy, D., and Smerdon, J.M. 2005b. DNA repair in RNA Polymerase-I transcribed genes. In From DNA photolesions to mutations, skin cancer and cell death. Edited by R. Drouin, E. Sage, and M. Rouabhia. RSC Publishing. Cambridge, U.K. pp. 123-147.
17. Dammann, R., Lucchini, R., Koller, T., and Sogo, J.M. 1993. Chromatin structures and transcription of rDNA in yeast Saccharo-myces cerevisiae. Nucleic Acids Res. 21: 2331-2338. doi:10. 1093/nar/21.10.2331. PMID:8506130.
18. Dammann, R., Lucchini, R., Koller, T., and Sogo, J.M. 1995. Transcription in the yeast rRNA gene locus: distribution of the active gene copies and chromatin structure of their flanking regulatory sequences. Mol. Cell. Biol. 15: 5294-5303. PMID:7565678.
19. De Bernardin, W., Koller, T., and Sogo, J.M. 1986. Structure of in-vivo transcribing chromatin as studied in simian virus 40 mini- chromosomes. J. Mol. Biol. 191: 469-482. doi:10.1016/0022-2836(86)90142-7. PMID:3029385.
20. Donahue, B.A., Yin, S., Taylor, J.-S., Reines, D., and Hanawalt, P.C. 1994. Transcript cleavage by RNA polymerase II arrested by a cyclobutane pyrimidine dimmer in the DNA template. Proc. Natl. Acad. Sci. U.S.A. 91: 8502-8506. doi:10.1073/pnas. 91.18.8502. PMID:8078911.
21. Fahy, D., Conconi, A., and Smerdon, M.J. 2005. Rapid changes in transcription and chromatin structure of ribosomal genes in yeast during growth phase transitions. Exp. Cell Res. 305: 365-373. doi:10.1016/j.yexcr.2005. 01.016. PMID:15817161.
22. Ferreiro, J.A., Powell, N.G., Karabetsou, N., Kent, N.A., Mellor, J., and Water, R. 2004. Cbf1p modulates chromatin structure, transcription and repair at the Saccharomyces cerevisiae MET16 locus. Nucleic Acids Res. 32: 1617-1626. doi:10.1093/nar/ gkh324. PMID:15007107.
23. French, S.L., Osheim, Y.N., Cioci, F., Nomura, M., and Beyer, A.L. 2003. In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes. Mol. Cell. Biol. 23: 1558-1568. doi:10.1128/MCB.23.5.1558-1568.2003. PMID:12588976.
24. Friedberg, E.C., Wood, R.D., Walker, G.C., Schultz, R.A., Siede, W., and Ellenberger, T. 2006. DNA repair and mutagenesis. 2nd ed. ASM Press, Washington, DC.
25. Frit, P., Kwon, K., Coin, F., Auriol, J., Dubaele, S., Salles, B., and Egly, J.M. 2002. Transcriptional activators stimulate DNA repair. Mol. Cell, 10: 1391-1401. doi:10.1016/S1097-2765(02) 00732-3. PMID:12504014.
26. Fritz, L.K., and Smerdon, M.J. 1995. Repair of UV damage in actively transcribed ribosomal genes. Biochemistry, 34: 13117-13124. doi:10.1021/bi00040a024. PMID:7548072.
27. Gaillard, P.-H.L., Martini, E.M.-D., Kaufman, P.D., Stillman, B., Moustacchi, E., and Almouzni, G. 1996. Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell, 86: 887-896. doi:10.1016/S0092-8674(00)80164-6. PMID:8808624.
28. Gaillard, P.-H.L., Moggs, J.G., Roche, D.M.J., Quivy, J.-P., Becker, P.B., Wood, R.D., and Almouzni, G. 1997. Initiation and bidirectional propagation of chromatin assembly from a target site for nucleotide excision repair. EMBO J. 16: 6281-6289. doi:10.1093/emboj/16.20.6281. PMID:9321407.
29. Gaillard, H., Fitzgerald, D.J., Smith, C.L., Peterson, C.L., Richmond, T.J., and Thoma, F. 2003. Chromatin remodeling activities act on UV-damaged nucleosomes and modulate DNA damage accessibility to photolyase. J. Biol. Chem. 278: 17655-17663. doi:10.1074/jbc.M300770200. PMID:12637512.
30. Gale, J.M., and Smerdon, M.J. 1988. Photofootprint of nucleosome core DNA in intact chromatin having different structural states. J. Mol. Biol. 204: 949-958. doi:10.1016/0022-2836(88)90054-X. PMID:3221402.
31. Gale, J.M., and Smerdon, M.J. 1990. UV induced (6-4) photoproducts are distributed differently than cyclobutane dimers in nucleosomes. Photochem. Photobiol. 51: 411-417. doi:10.1111/j. 1751-1097.1990.tb01732.x. PMID:2160660.
32. Gale, J.M., Nissen, K.A., and Smerdon, M.J. 1987. UV-induced formation of pyrimidine dimers in nucleosome core DNA is strongly modulated with a period of 10.3 bases. Proc. Natl. Acad. Sci. U.S.A. 84: 6644-6648. doi:10.1073/pnas.84.19.6644. PMID:3477794.
33. Gong, F., Fahy, D., and Smerdon, M.J. 2006. Rad4-Rad23 interaction with SWI/SNF links ATP-dependent chromatin remodeling with nucleotide excision repair. Nat. Struct. Mol. Biol. 13: 902-907. doi:10.1038/nsmb1152. PMID:17013386.
34. Green, C.M., and Almouzni, G. 2002. When repair meets chromatin. First in series on chromatin dynamics. EMBO Rep. 3: 28-33. doi:10.1093/embo- reports/kvf005. PMID:11799057.
35. Green, C.M., and Almouzni, G. 2003. Local action of the chroma-tin assembly factor CAF-1 at sites of nucleotide excision repair in vivo. EMBO J. 22: 5163-5174. doi:10.1093/emboj/cdg478. PMID:14517254.
36. Groth, A., Roccha, W., Verreault, A., and Almouzni, G. 2007. Chromatin challenges during DNA replication and repair. Cell, 128: 721-733. doi:10.1016/j.cell.2007.01.030. PMID:17320509.
37. Grummt, I. 1999. Regulation of mammalian ribosomal gene transcription by RNA polymerase I. Prog. Nucleic Acid Res. Mol. Biol. 62: 109-154. doi:10.1016/S0079-6603(08)60506-1. PMID:9932453.
38. Grummt, I., and Pikaard, C.S. 2003. Epigenetic silencing of RNA polymerase I transcription. Nat. Rev. Mol. Cell Biol. 4: 641-649. doi:10.1038/nrm1171. PMID:12923526.
39. Hara, R., and Sancar, A. 2002. The SWI/SNF chromatin-remodeling factor stimulates repair by human excision nuclease in the mononucleosome core particle. Mol. Cell. Biol. 22: 6779-6787. doi:10.1128/MCB.22.19.6779- 6787.2002. PMID:12215535.
40. Hara, R., and Sancar, A. 2003. Effect of damage type on stimulation of human excision nuclease by SWI/SNF chromatin remodelling factor. Mol. Cell. Biol. 23: 4121-4125. doi:10.1128/ MCB.23.12.4121-4125.2003. PMID:12773556.
41. Hara, R., Shelby, C.P., Liu, M., Price, D.H., and Sancar, A. 1999. Human transcription release factor 2 dissociates RNA polymerases I and II stalled at a cyclobutane thymine dimer. J. Biol. Chem. 274: 24779-24786. doi:10.1074/jbc.274.35.24779. PMID:10455150.
42. Hara, R., Mo, J., and Sancar, A. 2000. DNA damage in the nucleosome core is refractory to repair by human excision nuclease. Mol. Cell. Biol. 20: 9173-9181. doi:10.1128/MCB.20.24.9173-9181.2000. PMID:11094069.
43. Hoeijmakers, J.H. 2001. Genome maintenance mechanism for preventing cancer. Nature, 411: 366-374. doi:10.1038/35077232. PMID:11357144.
44. Hunting, D.J., Dresler, S.L., and Lieberman, M.W. 1985. Multiple conformational states of repair patches in chromatin during DNA excision repair. Biochemistry, 24: 3219-3226. doi:10. 1021/bi00334a022. PMID:3927974.
45. Jensen, K.A., and Smerdon, J.M. 1990. DNA repair within nucleosome cores of UV-irradiated human cells. Biochemistry, 29: 4773-4782. doi:10.1021/bi00472a005. PMID:2364058.
46. Jones, H.S., Kawauchi, J., Braglia, P., Alen, C.M., Kent, N.A., and Proudfoot, N.J. 2007. RNA polymerase I in yeast transcribes dynamic nucleosomal rDNA. Nat. Struct. Mol. Biol. 14: 123-130. doi:10.1038/nsmb1199. PMID:17259992.
47. Kao, Y.T., Saxena, C., Wang, L., Sancar, A., and Zhong, D. 2005. Direct observation of thymine dimer repair in DNA by photolyase. Proc. Natl. Acad. Sci. U.S.A. 102: 16128-16132. doi:10. 1073/pnas.0506586102. PMID:16169906.
48. Kosmoski, J.V., and Smerdon, M.J. 1999. Synthesis and nucleosome structure of DNA containing a UV photoproduct at a specific site. Biochemistry, 38: 9485-9494. doi:10.1021/bi990297h. PMID:10413526.
49. Kosmoski, J.V., Ackerman, E.J., and Smerdon, M.J. 2001. DNA repair of a single UV photoproduct in a designed nucleosome. Proc. Natl. Acad. Sci. U.S.A. 98: 10113-10118. doi:10.1073/ pnas.181073398. PMID:11517308.
50. Lainé, J.P., and Egly, J.M. 2006. When transcription and repair meet: a complex system. Trends Genet. 22: 430-436. doi:10. 1016/j.tig.2006.06.006. PMID:16797777.
51. Lan, S.Y., and Smerdon, J.M. 1985. A nonuniform distribution of excision repair synthesis in nucleosome core DNA. Biochemistry, 24: 7771-7783. doi:10.1021/bi00347a041. PMID:4092038.
52. Liu, X., and Smerdon, M.J. 2000. Nucleotide excision repair of the 5 S ribosomal RNA gene assembled into a nucleosome. J. Biol. Chem. 275: 23729-23735. doi:10.1074/jbc.M002206200. PMID:10821833.
53. Livingstone-Zatchej, M., Meier, A., Suter, B., and Thoma, F. 1997. RNA polymerase II transcription inhibits DNA repair by photolyase in the transcribed strand of active yeast genes. Nucleic Acids Res. 25: 3795-3800. doi:10.1093/nar/25.19.3795. PMID:9380500.
54. Livingstone-Zatchej, M., Marcionelli, R., Möller, K., de Pril, R., and Thoma, F. 2003. Repair of UV lesions in silenced chromatin provides in vivo evidence for a compact chromatin structure. J. Biol. Chem. 278: 37471-37479. doi:10.1074/jbc.M306335200. PMID:12882973.
55. Lucchini, R., and Sogo, J.M. 1992. Different chromatin structures along the spacers flanking active and inactive Xenopus rRNA genes. Mol. Cell. Biol. 12: 4288-4296. PMID:1406621.
56. Lucchini, R., and Sogo, J.M. 1998. The dynamic structure of ribosomal RNA gene chromatin. In Transcription of ribosomal RNA genes by eukaryotic RNA polymerase I. Edited by M.R. Paule. M.R. R.G. Landes Company, Austin, Texas. pp. 254-276.
57. Lucchini, R., Pauli, U., Braun, R., Koller, T., and Sogo, J.M. 1987. Structure of the extrachromosomal ribosomal RNA chromatin of Physarum polycephalum. J. Mol. Biol. 196: 829-843. doi:10. 1016/0022-2836(87)90408-6. PMID:3681980.
58. Luger, K., Mäder, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. 1997. Crystal structure of the nucleosome core particle at 2.8A resolution. Nature, 389: 251-260. doi:10.1038/ 38444. PMID:9305837.
59. Mees, A., Klar, T., Gnau, P., Hennecke, U., Eker, A.P., Carell, T., and Essen, L.O. 2004. Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science, 306: 1789-1793. doi:10.1126/science.1101598. PMID:15576622.
60. Meier, A., and Thoma, F. 2005. RNA polymerase I transcription factors in active yeast rRNA gene promoters enhance UV damage formation and inhibit repair. Mol. Cell. Biol. 25: 1586-1595. doi:10.1128/MCB.25.5.1586-1595.2005. PMID:15713619.
61. Meier, A., Livingstone-Zatchej, M., and Thoma, F. 2002. Repair of active and silenced rDNA in yeast. J. Biol. Chem. 277: 11845-11852. doi:10.1074/jbc.M110941200. PMID:11805105.
62. Mello, J.A., and Almouzni, G. 2001. The ins and outs of nucleosome assembly. Curr. Opin. Genet. Dev. 11: 136-141. doi:10. 1016/S0959-437X(00)00170-2. PMID:11250135.
63. Mello, J.A., Silljé, H.H., Roche, D.M., Kirschner, D.B., Nigg, E.A., and Almouzni, G. 2002. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3: 329-334. doi:10.1093/embo-reports/kvf068. PMID:11897662.
64. Mellon, I. 2005. Transcription-coupled repair: a complex affair. Mutat. Res. 577: 155-161. PMID:15913669.
65. Mellon, I., and Hanawalt, P.C. 1989. Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand. Nature, 342: 95-98. doi:10.1038/342095a0. PMID:2554145.
66. Mellon, I., Bohr, V.A., Smith, C.A., and Hanawalt, P.C. 1986. Preferential DNA repair of an active gene in human cells. Proc. Natl. Acad. Sci. U.S.A. 83: 8878-8882. doi:10.1073/pnas.83.23. 8878. PMID:3466163.
67. Mellon, I., Spivak, G., and Hanawalt, P.C. 1987. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell, 51: 241-249. doi:10.1016/0092-8674(87)90151-6. PMID:3664636.
68. Merz, K., Hondele, M., Goetze, H., Gmelch, K., Stoeckl, U., and Griesenbeck, J. 2008. Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules. Genes Dev. 22: 1190-1204. doi:10. 1101/gad.466908. PMID:18451108.
69. Mitchell, D.L., Nguyen, T.D., and Cleaver, J.E. 1990. Non-random induction of pyrimidine-pyrimidone (6-4) photoproducts in ultraviolet-irradiated human chromatin. J. Biol. Chem. 265: 5353-5356. PMID:2318816.
70. Moggs, J.G., Grandi, P., Quivy, J.P., Jonsson, Z.O., Hubscher, U., Becker, P.B., and Almouzni, G. 2000. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol. Cell. Biol. 20: 1206-1218. doi:10.1128/ MCB.20.4.1206-1218.2000. PMID:10648606.
71. Morse, N.R., Meniel, V., and Waters, R. 2002. Photoreactivation of UV-induced cyclobutane pyrimidine dimers in the MFA2 gene of Saccharomyces cerevisiae. Nucleic Acids Res. 30: 1799-1807. doi:10.1093/nar/30.8. 1799. PMID:11937634.
72. Moss, T. 2004. At the crossroads of growth control; making ribosomal RNA. Curr. Opin. Genet. Dev. 14: 210-217. doi:10.1016/j. gde.2004.02.005. PMID:15196469.
73. Moss, T., Langlois, F., Gagnon-Kugler, T., and Stefanovsky, V. 2007. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci. 64: 29-49. doi:10. 1007/s00018-006-6278-1. PMID:17171232.
74. Muller, M., Lucchini, R., and Sogo, J.M. 2000. Replication of yeast rDNA initiates downstream of transcriptionally active genes. Mol. Cell, 5: 767-777. doi:10.1016/S1097-2765(00)80317-2. PMID:10882113.
75. Nag, R., Gong, F., Fahy, D., and Smerdon, M.J. 2008. A single amino acid change in histone H4 enhances UV survival and DNA repair in yeast. Nucleic Acids Res. 36: 3857-3866. PMID:18508805.
76. Ness, P.J., Labhart, P., Banz, E., Koller, T., and Parish, R.W. 1983. Chromatin structure along the ribosomal DNA of Dictyostelium. Regional differences and changes accompanying cell differentiation. J. Mol. Biol. 166: 361-381. doi:10.1016/S0022-2836(83) 80090-4. PMID:6304325.
77. Niggli, H.J., and Cerutti, P. 1982. Nucleosomal distribution of thymine photodimers following far- and near-ultraviolet irradiation. Biochem. Biophys. Res. Commun. 105: 1215-1223. doi:10. 1016/0006-291X(82)91098-1. PMID:7092895.
78. Noll, M. 1974. Internal structure of the chromatin subunit. Nucleic Acids Res. 1: 1573-1578. doi:10.1093/nar/1.11.1573. PMID:10793712.
79. Park, J.S., Marr, M.T., and Roberts, J.W. 2002. E. coli transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell, 109: 757-767. doi:10. 1016/S0092-8674(02)00769-9. PMID:12086674.
80. Pehrson, J.R., and Cohen, L.H. 1992. Effects of DNA looping on pyrimidine dimer formation. Nucleic Acids Res. 20: 1321-1324. doi:10.1093/nar/20.6. 1321. PMID:1561089.
81. Prakash, S., and Prakash, L. 2000. Nucleotide excision repair in yeast. Mutat. Res. 451: 13-24. PMID:10915862.
82. Ramanathan, B., and Smerdon, M.J. 1989. Enhanced DNA repair synthesis in hyperacetylated nucleosomes. J. Biol. Chem. 264: 11026-11034. PMID:2738057.
83. Reeder, R.H. 1999. Regulation of RNA polymerase I transcription in yeast and vertebrates. Prog. Nucleic Acid Res. Mol. Biol. 62: 293-327. doi:10.1016/S0079-6603(08)60511-5. PMID:9932458.
84. Sancar, A. 2003. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103: 2203-2237. doi:10.1021/cr0204348. PMID:12797829.
85. Sanz, C., Gorab, E., Ruiz, M.F., Sogo, J.M., and Díez, J.L. 2007. Chromatin structure of ribosomal genes in Chironomus thummi (Diptera: Chironomidae): tissue specificity and behaviour under drug treatment. Chromosome Res. 15: 429-438. doi:10.1007/ s10577-007-1134-1. PMID:17487564.
86. Sarker, A.H., Tsutakawa, S.E., Kostek, S., Ng, C., Shin, D.S., Peris, M., et al. 2005. Recognition of RNA polymerase II and transcription bubbles by XPG, CSB, and TFIIH: insights for transcription-coupled repair and Cockayne Syndrome. Mol. Cell, 20: 187-198. PMID:16246722.
87. Schieferstein, U., and Thoma, F. 1998. Site-specific repair of cyclobutane pyrimidine dimers in a positioned nucleosome by photolyase and T4 endonuclease V in vitro. EMBO J. 17: 306-316. doi:10.1093/emboj/17.1.306. PMID:9427764.
88. Schmid, M., Durussel, T., and Laemmli, U.K. 2004. ChIC and ChEC; genomic mapping of chromatin proteins. Mol. Cell, 16: 147-157. PMID:15469830.
89. Smerdon, M.J. 1986. Completion of excision repair in human cells. Relationship between ligation and nucleosome formation. J. Biol. Chem. 261: 244-252. PMID:3941074.
90. Smerdon, M.J., and Conconi, A. 1999. Modulation of DNA damage and DNA repair in chromatin. Prog. Nucleic Acid Res. Mol. Biol. 62: 227-255. doi:10.1016/S0079-6603(08)60509-7. PMID:9932456.
91. Smerdon, M.J., and Lieberman, M.W. 1978. Nucleosome rearrangement in human chromatin during UV-induced DNA-repair synthesis. Proc. Natl. Acad. Sci. U.S.A. 75: 4238-4241. doi:10. 1073/pnas.75.9.4238. PMID:279912.
92. Smerdon, M.J., and Lieberman, M.W. 1980. Distribution within chromatin of deoxyribonucleic acid repair synthesis occurring at different times after ultraviolet radiation. Biochemistry, 19: 2992-3000. doi:10.1021/ bi00554a025. PMID:7397113.
93. Smerdon, M.J., and Thoma, F. 1990. Site-specific DNA repair at the nucleosome level in a yeast minichromosome. Cell, 61: 675-684. doi:10.1016/0092-8674(90)90479-X. PMID:2188732.
94. Smerdon, M.J., Kastan, M.B., and Lieberman, M.W. 1979. Distribution of repair-incorporated nucleotides and nucleosome rearrangement in the chromatin of normal and xeroderma pigmentosum human fibroblasts. Biochemistry, 18: 3732-3739. doi:10.1021/bi00584a014. PMID:476082.
95. Smith, J.S., and Boeke, J.D. 1997. An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev. 11: 241-254. doi:10.1101/gad.11.2.241. PMID:9009206.
96. Smith, J.S., Caputo, E., and Boeke, J.D. 1999. A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors. Mol. Cell. Biol. 19: 3184-3197. PMID:10082585.
97. Smith, S., and Stillman, B. 1989. Purification and characterization of CAF-1, a human cell factor required for chromatin assembly during DNA replication. Cell, 58: 15-25. doi:10.1016/0092-8674(89)90398-X. PMID:2546672.
98. Sogo, J.M., and Thoma, F. 2003. The structure of rDNA chromatin. In The nucleolus. Edited by M.O.J. Olson. Kluwer Academic/ Plenum Publishers. New York. pp. 1-15.
99. Sogo, J.M., Ness, P.J., Widmer, R.M., Parish, R.W., and Koller, T. 1984. Psoralen-crosslinking of DNA as a probe for the structure of active nucleolar chromatin. J. Mol. Biol. 178: 897-919. doi:10.1016/0022-2836(84)90318-8. PMID:6092647.
100. Sollner-Webb, B., and Mougey, E.B. 1991. News from the nucleo-lus: rRNA gene expression. Trends Biochem. Sci. 16: 58-62. doi:10.1016/0968- 0004(91)90025-Q. PMID:1858134.
101. Stancheva, I., Lucchini, R., Koller, T., and Sogo, J.M. 1997. Chromatin structure and methylation of rat rRNA genes studied by formaldehyde fixation and psoralen cross-linking. Nucleic Acids Res. 25: 1727-1735. doi:10.1093/nar/25.9.1727. PMID:9108154.
102. Stefanovsky, V., Langlois, F., Gagnon-Kugler, T., Rothblum, L.I., and Moss, T. 2006. Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phos-phorylation and r-chromatin remodeling. Mol. Cell, 21: 629-639. doi:10.1016/j.molcel.2006.01.023. PMID:16507361.
103. Sugasawa, K., Masutani, C., and Hanaoka, F. 1993. Cell-free repair of UV-damaged simian virus 40 chromosomes in human cell extracts. I. Development of a cell-free system detecting excision repair of UV-irradiated SV40 chromosomes. J. Biol. Chem. 268: 9098-9104. PMID:8386176.
104. Suquet, C., Mitchell, D.L., and Smerdon, M.J. 1995. Repair of UV-induced (6-4) photoproducts in nucleosome core DNA. J. Biol. Chem. 270: 507-509. doi:10.1074/jbc.270.2.507. PMID:7822270.
105. Suter, B., and Thoma, F. 2002. DNA-repair by photolyase reveals dynamic properties of nucleosome positioning in vivo. J. Mol. Biol. 319: 395-406. doi:10.1016/S0022-2836(02)00291-7. PMID:12051916.
106. Suter, B., Livingstone-Zatchej, M., and Thoma, F. 1997. Chromatin structure modulates DNA repair by photolyase in vivo. EMBO J. 16: 2150-2160. doi:10.1093/emboj/16.8.2150. PMID:9155040.
107. Suter, B., Livingstone-Zatchej, M., and Thoma, F. 1999. Mapping cyclobutane-pyrimidine dimers in DNA and using DNA-repair by photolyase for chromatin analysis in yeast. Methods Enzy-mol. 304: 447-461. doi:10.1016/S0076-6879(99)04027-6. PMID:10372376.
108. Suter, B., Wellinger, R.E., and Thoma, F. 2000a. DNA repair in a yeast origin of replication: contributions of photolyase and nu-cleotide excision repair. Nucleic Acids Res. 28: 2060-2068. doi:10.1093/nar/28.10. 2060. PMID:10773073.
109. Suter, B., Schnappauf, G., and Thoma, F. 2000b. Poly(dA.dT) sequences exist as rigid DNA structures in nucleosome-free yeast promoters in vivo. Nucleic Acids Res. 28: 4083-4089. doi:10. 1093/nar/28.21.4083. PMID:11058103.
110. Teng, Y., Yu, Y., and Waters, R. 2002. The Saccharomyces cerevisiae histone acetyltransferase Gcn5 has a role in the photoreacti-vation and nucleotide excision repair of UV-induces cyclobutane pyrimidine dimmers in the MFA2 gene. J. Mol. Biol. 316: 489-499. doi:10.1006/jmbi.2001.5383. PMID:11866513.
111. Teng, Y., Yu, Y., Ferreiro, J.A., and Waters, R. 2005. Histone acetylation, chromatin remodelling, transcription and nucleotide excision repair in S. cerevisiae: studies with two model genes. DNA Repair (Amst.), 4: 870-883. doi:10.1016/j.dnarep.2005.04. 006. PMID:15950549.
112. Thoma, F. 1999. Light and dark in chromatin repair: repair of UV-induced DNA lesions by photolyase and nucleotide excision repair. EMBO J. 18: 6585-6598. doi:10.1093/emboj/18.23.6585. PMID:10581233.
113. Thoma, F. 2005. Repair of UV lesions in nucleosomes-intrinsic properties and remodeling. DNA Repair (Amst.), 4: 855-869. doi:10.1016/j.dnarep. 2005.04.005. PMID:15925550.
114. Tijsterman, M., De Pril, R., Tasseron-De Jong, J.G., and Brouwer, J. 1999. RNA polymerase II transcription suppresses nucleosomal modulation of UV-induced (6-4) photoproduct and cyclobutane pyrimidine dimer repair in yeast. Mol. Cell. Biol. 19: 934-940. PMID:9858617.
115. Tornaletti, S., and Hanawalt, P.C. 1999. Effect of DNA lesions on transcription elongation. Biochimie, 81(1-2): 139-146. doi:10. 1016/S0300-9084(99)80046-7. PMID:10214918.
116. Tremblay, M., Teng, Y., Paquette, M., Waters, R., and Conconi, A. 2008. Complementary roles of yeast Rad4p and Rad34p in nucleotide excision repair of active and inactive rRNA gene chromatin. Mol. Cell. Biol. 28: 7504-7513.
117. Toussaint, M., Levasseur, G., Tremblay, M., Paquette, M., and Conconi, A. 2005. Psoralen photocrosslinking, a tool to study the chromatin structure of RNA polymerase I-transcribed ribosomal genes. Biochem. Cell Biol. 83: 449-459. doi:10.1139/ o05-141. PMID:16094448.
118. Ura, K., and Hayes, J.J. 2002. Nucleotide excision repair and chromatin remodeling. Eur. J. Biochem. 269: 2288-2293. doi:10. 1046/j.1432-1033. 2002.02888.x. PMID:11985610.
119. Ura, K., Araki, M., Saeki, H., Masutani, C., Ito, T., Iwai, S., et al. 2001. ATP-dependent chromatin remodeling facilitates nucleotide excision repair of UV-induced DNA lesions in synthetic dinucleosomes. EMBO J. 20: 2004-2014. doi:10.1093/emboj/20.8. 2004. PMID:11296233.
120. van Noort, J., Orsini, F., Eker, A., Wyman, C., de Grooth, B., and Greve, J. 1999. DNA bending by photolyase in specific and nonspecific complexes studied by atomic force microscopy. Nucleic Acids Res. 27: 3875-3880. doi:10.1093/nar/27.19.3875. PMID:10481027.
121. Verhage, R.A., Van De Putte, P., and Brouwer, J. 1996. Repair of rDNA in Saccharomyces cerevisiae: RAD4-independent strandspecific nucleotide excision repair of RNA polymeras I transcribed genes. Nucleic Acids Res. 24: 1020-1025. doi:10.1093/ nar/24.6.1020. PMID:8604332.
122. Verhage, R.A., Tijsterman, M., van de Putte, P., and Brouwer, J. 1998. Transcription-coupled and global genome nucleotide excision repair. In Nucleic acids and molecular biology. Vol. 12. Edited by F. Eckstein, D.M.J. Lilley. Springer-Verlag, New York. pp. 157-172.
123. Verreault, A. 2000. De novo nucleosome assembly: new pieces in an old puzzle. Genes Dev. 14: 1430-1438. PMID:10859162.
124. Wang, Z.G., Wu, X.H., and Friedberg, E.C. 1991. Nucleotide excision repair of DNA by human cell extracts is suppressed in reconstituted nucleosomes. J. Biol. Chem. 266: 22472-22478. PMID:1939267.
125. Waters, R., and Smerdon, M.J. 2005. Nucleotide excision repair in chromatin: searching for the key to enter. DNA Repair (Amst.), 4(Suppl): 853-950. doi:10.1016/j.dnarep.2005.04.004. PMID:15967734.
126. Weber, S. 2005. Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyase. Biochim. Biophys. Acta, 1707: 1-23. doi:10.1016/j.bbabio.2004.02.010. PMID:15721603.
127. Wellinger, R.E., and Thoma, F. 1997. Nucleosome structure and positioning modulate nucleotide excision repair in the non-transcribed strand of an active gene. EMBO J. 16: 5046-5056. doi:10.1093/emboj/16.16.5046. PMID:9305646.
128. Yu, Y., Teng, Y., Liu, H., Reed, S.H., and Waters, R. 2005. UV irradiation stimulates histone acetylation and chromatin remodeling at a repressed yeast locus. Proc. Natl. Acad. Sci. U.S.A. 102: 8650-8655. doi:10.1073/pnas.0501458102. PMID:15939881.