Stochastic and reversible assembly of a multiprotein DNA repair complex ensures accurate target site recognition and efficient repair

Journal of Cell Biology

Volumn 189, Issue 3, 2010, Pages 445-463

  Luijsterburg, Martijn S ^a,c,f   Von Bornstaedt, Gesa ^b,d   Gourdin, Audrey M ^e   Politi, Antonio Z ^f   Moné, Martijn J ^a,c   Warmerdam, Daniël O ^a,e   Goedhart, Joachim ^a   Vermeulen, Wim ^e   Van Driel, Roel ^a,c   Höfer, Thomas ^b,d  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c Department of Clinical and Molecular Ophthalmogenetics   (Netherlands)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MULTIPROTEIN COMPLEX; NUCLEOTIDE BINDING PROTEIN; NUCLEOTIDE EXCISION REPAIR PROTEIN; UNCLASSIFIED DRUG;

ACCURACY; ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DIFFUSION; DNA DAMAGE; DNA REPAIR; ENZYME MODIFICATION; EXCISION REPAIR; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KINETICS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; STOCHASTIC MODEL;

ANIMALS; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; DNA; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; KINETICS;

MAMMALIA;

EID: 77951819090     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200909175     Document Type: Article

References (79)

1. Aboussekhra, A., M. Biggerstaff, M.K. Shivji, J.A. Vilpo, V. Moncollin, V.N. Podust, M. Protic, U. Hübscher, J.M. Egly, and R.D. Wood. 1995. Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell. 80:859-868. doi:10.1016/0092-8674(95)90289-9
2. Araújo, S.J., E.A. Nigg, and R.D. Wood. 2001. Strong functional interactions of TFIIH with XPC and XPG in human DNA nucleotide excision repair, without a preassembled repairosome. Mol. Cell. Biol. 21:2281-2291. doi:10.1128/MCB.21.7.2281-2291.2001
3. Black, J.C., J.E. Choi, S.R. Lombardo, and M. Carey. 2006. A mechanism for coordinating chromatin modification and preinitiation complex assembly. Mol. Cell. 23:809-818. doi:10.1016/j.molcel.2006.07.018
4. Blackwell, L.J., and J.A. Borowiec. 1994. Human replication protein A binds single-stranded DNA in two distinct complexes. Mol. Cell. Biol. 14:3993-4001.
5. Camenisch, U., R. Dip, S.B. Schumacher, B. Schuler, and H. Naegeli. 2006. Recognition of helical kinks by xeroderma pigmentosum group A protein triggers DNA excision repair. Nat. Struct. Mol. Biol. 13:278-284. doi:10.1038/nsmb1061 (Pubitemid 43348515)
6. Camenisch, U., R. Dip, M. Vitanescu, and H. Naegeli. 2007. Xeroderma pigmentosum complementation group A protein is driven to nucleotide excision repair sites by the electrostatic potential of distorted DNA. DNA Repair (Amst.). 6:1819-1828. doi:10.1016/j.dnarep.2007.07.011 (Pubitemid 350052729)
7. Coin, F., V. Oksenych, and J.M. Egly. 2007. Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol. Cell. 26:245-256. doi:10.1016/j.molcel.2007.03. 009 (Pubitemid 46656218)
8. Darzacq, X., and R.H. Singer. 2008. The dynamic range of transcription. Mol. Cell. 30:545-546. doi:10.1016/j.molcel.2008.05.009
9. Darzacq, X., Y. Shav-Tal, V. de Turris, Y. Brody, S.M. Shenoy, R.D. Phair, and R.H. Singer. 2007. In vivo dynamics of RNA polymerase II transcription. Nat. Struct. Mol. Biol. 14:796-806. doi:10.1038/nsmb1280 (Pubitemid 47373828)
10. de Laat, W.L., E. Appeldoorn, K. Sugasawa, E. Weterings, N.G. Jaspers, and J.H. Hoeijmakers. 1998. DNA-binding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev. 12:2598-2609. doi:10.1101/gad.12.16.2598 (Pubitemid 28406961)
11. Dinant, C., M.S. Luijsterburg, T. Höfer, G. von Bornstaedt, W. Vermeulen, A.B. Houtsmuller, and R. van Driel. 2009. Assembly of multiprotein complexes that control genome function. J. Cell Biol. 185:21-26. doi:10.1083/jcb.200811080
12. Dip, R., U. Camenisch, and H. Naegeli. 2004. Mechanisms of DNA damage recognition and strand discrimination in human nucleotide excision repair. DNA Repair (Amst.). 3:1409-1423. doi:10.1016/j.dnarep.2004.05.005 (Pubitemid 39221739)
13. Dundr, M., U. Hoffmann-Rohrer, Q. Hu, I. Grummt, L.I. Rothblum, R.D. Phair, and T. Misteli. 2002. A kinetic framework for a mammalian RNA polymerase in vivo. Science. 298:1623-1626. doi:10.1126/science.1076164 (Pubitemid 35387201)
14. Essers, J., A.F. Theil, C. Baldeyron, W.A. van Cappellen, A.B. Houtsmuller, R. Kanaar, and W. Vermeulen. 2005. Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol. 25:9350-9359. doi:10.1128/MCB.25.21. 9350-9359.2005 (Pubitemid 41507836)
15. Evans, E., J.G. Moggs, J.R. Hwang, J.M. Egly, and R.D. Wood. 1997. Mechanism of open complex and dual incision formation by human nucleotide excision repair factors. EMBO J. 16:6559-6573. doi:10.1093/emboj/16.21.6559 (Pubitemid 27483280)
16. Giglia-Mari, G., C. Miquel, A.F. Theil, P.O. Mari, D. Hoogstraten, J.M. Ng, C. Dinant, J.H. Hoeijmakers, and W. Vermeulen. 2006. Dynamic interaction of TTDA with TFIIH is stabilized by nucleotide excision repair in living cells. PLoS Biol. 4:e156. doi:10.1371/journal.pbio.0040156
17. Gillet, L.C., and O.D. Schärer. 2006. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem. Rev. 106:253-276. doi:10.1021/cr040483f (Pubitemid 43316557)
18. Gorski, S.A., S.K. Snyder, S. John, I. Grummt, and T. Misteli. 2008. Modulation of RNA polymerase assembly dynamics in transcriptional regulation. Mol. Cell. 30:486-497. doi:10.1016/j.molcel.2008.04.021
19. Green, C.M., and G. Almouzni. 2003. Local action of the chromatin assembly factor CAF-1 at sites of nucleotide excision repair in vivo. EMBO J. 22:5163-5174. doi:10.1093/emboj/cdg478
20. Hall, H., J. Gurský, A. Nicodemou, I. Rybanská, E. Kimlícková, and M. Pirsel. 2006. Characterization of ERCC3 mutations in the Chinese hamster ovary 27-1, UV24 and MMC-2 cell lines. Mutat. Res. 593:177-186. (Pubitemid 43113373)
21. Henricksen, L.A., C.B. Umbricht, and M.S. Wold. 1994. Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem. 269:11121-11132.
22. Hey, T., G. Lipps, K. Sugasawa, S. Iwai, F. Hanaoka, and G. Krauss. 2002. The XPC-HR23B complex displays high affinity and specificity for damaged DNA in a true-equilibrium fluorescence assay. Biochemistry. 41:6583-6587. doi:10.1021/bi012202t (Pubitemid 34547348)
23. Hoeijmakers, J.H. 2001. Genome maintenance mechanisms for preventing cancer. Nature. 411:366-374. doi:10.1038/35077232
24. Hoogstraten, D., A.L. Nigg, H. Heath, L.H. Mullenders, R. van Driel, J.H. Hoeijmakers, W. Vermeulen, and A.B. Houtsmuller. 2002. Rapid switching of TFIIH between RNA polymerase I and II transcription and DNA repair in vivo. Mol. Cell. 10:1163-1174. doi:10.1016/S1097-2765(02)00709-8 (Pubitemid 35453833)
25. Hoogstraten, D., S. Bergink, J.M. Ng, V.H. Verbiest, M.S. Luijsterburg, B. Geverts, A. Raams, C. Dinant, J.H. Hoeijmakers, W. Vermeulen, and A.B. Houtsmuller. 2008. Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. J. Cell Sci. 121:2850-2859. doi:10.1242/jcs.031708
26. Hopfield, J.J. 1974. Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. Natl. Acad. Sci. USA. 71:4135-4139. doi:10.1073/pnas.71.10.4135
27. Houtsmuller, A.B., S. Rademakers, A.L. Nigg, D. Hoogstraten, J.H. Hoeijmakers, and W. Vermeulen. 1999. Action of DNA repair endonuclease ERCC1/XPF in living cells. Science. 284:958-961. doi:10.1126/science.284.5416.958
28. Karpova, T.S., M.J. Kim, C. Spriet, K. Nalley, T.J. Stasevich, Z. Kherrouche, L. Heliot, and J.G. McNally. 2008. Concurrent fast and slow cycling of a transcriptional activator at an endogenous promoter. Science. 319:466-469. doi:10.1126/science.1150559
29. Kaufmann, W.K., and S.J. Wilson. 1990. DNA repair endonuclease activity during synchronous growth of diploid human fibroblasts. Mutat. Res. 236:107-117.
30. Kesseler, K.J., W.K. Kaufmann, J.T. Reardon, T.C. Elston, and A. Sancar. 2007. A mathematical model for human nucleotide excision repair: damage recognition by random order assembly and kinetic proofreading. J. Theor. Biol. 249:361-375. doi:10.1016/j.jtbi.2007.07.025
31. Kimura, H., and P.R. Cook. 2001. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol. 153:1341-1353. doi:10.1083/jcb.153.7.1341 (Pubitemid 34286121)
32. Kremers, G.J., J. Goedhart, E.B. van Munster, and T.W. Gadella Jr. 2006. Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Förster radius. Biochemistry. 45:6570-6580. doi:10.1021/bi0516273
33. Kremers, G.J., K.L. Hazelwood, C.S. Murphy, M.W. Davidson, and D.W. Piston. 2009. Photoconversion in orange and red fluorescent proteins. Nat. Methods. 6:355-358. doi:10.1038/nmeth.1319
34. Kunkel, T.A., and K. Bebenek. 2000. DNA replication fidelity. Annu. Rev. Biochem. 69:497-529. doi:10.1146/annurev.biochem.69.1.497
35. Luijsterburg, M.S., J. Goedhart, J. Moser, H. Kool, B. Geverts, A.B. Houtsmuller, L.H. Mullenders, W. Vermeulen, and R. van Driel. 2007. Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC. J. Cell Sci. 120:2706-2716. doi:10.1242/jcs.008367
36. MacInnes, M.A., J.A. Dickson, R.R. Hernandez, D. Learmonth, G.Y. Lin, J.S. Mudgett, M.S. Park, S. Schauer, R.J. Reynolds, G.F. Strniste, et al. 1993. Human ERCC5 cDNA-cosmid complementation for excision repair and bipartite amino acid domains conserved with RAD proteins of Saccharomyces cerevisiae and Schizosaccharomyces pombe. Mol. Cell. Biol. 13:6393-6402.
37. Maillard, O., S. Solyom, and H. Naegeli. 2007. An aromatic sensor with aversion to damaged strands confers versatility to DNA repair. PLoS Biol. 5:e79. doi:10.1371/journal.pbio.0050079
38. Michelman-Ribeiro, A., D. Mazza, T. Rosales, T.J. Stasevich, H. Boukari, V. Rishi, C. Vinson, J.R. Knutson, and J.G. McNally. 2009. Direct measurement of association and dissociation rates of DNA binding in live cells by fluorescence correlation spectroscopy. Biophys. J. 97:337-346. doi:10.1016/j.bpj.2009.04.027
39. Min, J.H., and N.P. Pavletich. 2007. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature. 449:570-575. doi:10.1038/nature06155 (Pubitemid 47525148)
40. Misteli, T. 2007. Beyond the sequence: cellular organization of genome function. Cell. 128:787-800. doi:10.1016/j.cell.2007.01.028 (Pubitemid 46273571)
41. Mocquet, V., J.P. Lainé, T. Riedl, Z. Yajin, M.Y. Lee, and J.M. Egly. 2008. Sequential recruitment of the repair factors during NER: the role of XPG in initiating the resynthesis step. EMBO J. 27:155-167. doi:10.1038/sj.emboj.7601948
42. Moné, M.J., M. Volker, O. Nikaido, L.H. Mullenders, A.A. van Zeeland, P.J. Verschure, E.M. Manders, and R. van Driel. 2001. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep. 2:1013-1017. doi:10.1093/embo-reports/kve224
43. Moné, M.J., T. Bernas, C. Dinant, F.A. Goedvree, E.M. Manders, M. Volker, A.B. Houtsmuller, J.H. Hoeijmakers, W. Vermeulen, and R. van Driel. 2004. In vivo dynamics of chromatin-associated complex formation in mammalian nucleotide excision repair. Proc. Natl. Acad. Sci. USA. 101:15933-15937. doi:10.1073/pnas.0403664101
44. Moser, J., M. Volker, H. Kool, S. Alekseev, H. Vrieling, A. Yasui, A.A. van Zeeland, and L.H. Mullenders. 2005. The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair (Amst.). 4:571-582. doi:10.1016/j.dnarep. 2005.01.001 (Pubitemid 40462045)
45. Moser, J., H. Kool, I. Giakzidis, K. Caldecott, L.H. Mullenders, and M.I. Fousteri. 2007. Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III alpha in a cell-cycle-specific manner. Mol. Cell. 27:311-323. doi:10.1016/j.molcel.2007.06.014 (Pubitemid 47058307)
46. Mu, D., D.S. Hsu, and A. Sancar. 1996. Reaction mechanism of human DNA repair excision nuclease. J. Biol. Chem. 271:8285-8294. doi:10.1074/jbc.271.32. 19451 (Pubitemid 26108661)
47. Mullenders, L.H., A.A. van Zeeland, and A.T. Natarajan. 1987. The localization of ultraviolet-induced excision repair in the nucleus and the distribution of repair events in higher order chromatin loops in mammalian cells. J. Cell Sci. Suppl. 6:243-262.
48. Nishi, R., S. Alekseev, C. Dinant, D. Hoogstraten, A.B. Houtsmuller, J.H. Hoeijmakers, W. Vermeulen, F. Hanaoka, and K. Sugasawa. 2009. UV-DDB-dependent regulation of nucleotide excision repair kinetics in living cells. DNA Repair (Amst.). 8:767-776. doi:10.1016/j.dnarep.2009.02.004
49. O'Donovan, A., A.A. Davies, J.G. Moggs, S.C. West, and R.D. Wood. 1994. XPG endonuclease makes the 3′ incision in human DNA nucleotide excision repair. Nature. 371:432-435. doi:10.1038/371432a0 (Pubitemid 24302560)
50. Park, C.J., and B.S. Choi. 2006. The protein shuffle. Sequential interactions among components of the human nucleotide excision repair pathway. FEBS J. 273:1600-1608. doi:10.1111/j.1742-4658.2006.05189.x
51. Perdiz, D., P. Grof, M. Mezzina, O. Nikaido, E. Moustacchi, and E. Sage. 2000. Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. Possible role of Dewar photoproducts in solar mutagenesis. J. Biol. Chem. 275:26732-26742.
52. Politi, A., M.J. Moné, A.B. Houtsmuller, D. Hoogstraten, W. Vermeulen, R. Heinrich, and R. van Driel. 2005. Mathematical modeling of nucleotide excision repair reveals efficiency of sequential assembly strategies. Mol. Cell. 19:679-690. doi:10.1016/j.molcel.2005.06.036 (Pubitemid 41219443)
53. Polo, S.E., D. Roche, and G. Almouzni. 2006. New histone incorporation marks sites of UV repair in human cells. Cell. 127:481-493. doi:10.1016/j.cell. 2006.08.049
54. Press, W., S. Teukolsky, W. Vetterling, and B. Flannery. 2007. Numerical Recipes: The Art of Scientific Computing. Third edition. Cambridge University Press, Cambridge/New York. 1235 pp.
55. Rademakers, S., M. Volker, D. Hoogstraten, A.L. Nigg, M.J. Moné, A.A. Van Zeeland, J.H. Hoeijmakers, A.B. Houtsmuller, and W. Vermeulen. 2003. Xeroderma pigmentosum group A protein loads as a separate factor onto DNA lesions. Mol. Cell. Biol. 23:5755-5767. doi:10.1128/MCB.23.16.5755-5767.2003 (Pubitemid 36951338)
56. Riedl, T., F. Hanaoka, and J.M. Egly. 2003. The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J. 22:5293-5303. doi:10.1093/emboj/cdg489 (Pubitemid 37222048)
57. Satokata, I., K. Tanaka, N. Miura, M. Narita, T. Mimaki, Y. Satoh, S. Kondo, and Y. Okada. 1992. Three nonsense mutations responsible for group A xeroderma pigmentosum. Mutat. Res. 273:193-202.
58. Schaeffer, L., R. Roy, S. Humbert, V. Moncollin, W. Vermeulen, J.H. Hoeijmakers, P. Chambon, and J.M. Egly. 1993. DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science. 260:58-63. doi:10.1126/science.8465201 (Pubitemid 23122745)
59. Shaner, N.C., R.E. Campbell, P.A. Steinbach, B.N. Giepmans, A.E. Palmer, and R.Y. Tsien. 2004. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22:1567-1572. doi:10.1038/nbt1037
60. Shivji, K.K., M.K. Kenny, and R.D. Wood. 1992. Proliferating cell nuclear antigen is required for DNA excision repair. Cell. 69:367-374. doi:10.1016/0092-8674(92)90416-A
61. Shivji, M.K., V.N. Podust, U. Hübscher, and R.D. Wood. 1995. Nucleotide excision repair DNA synthesis by DNA polymerase epsilon in the presence of PCNA, RFC, and RPA. Biochemistry. 34:5011-5017. doi:10.1021/ bi00015a012
62. Sijbers, A.M., W.L. de Laat, R.R. Ariza, M. Biggerstaff, Y.F. Wei, J.G. Moggs, K.C. Carter, B.K. Shell, E. Evans, M.C. de Jong, et al. 1996. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell. 86:811-822. doi:10.1016/S0092-8674(00)80155-5 (Pubitemid 26303449)
63. Smith, C.A., and D.S. Okumoto. 1984. Nature of DNA repair synthesis resistant to inhibitors of polymerase alpha in human cells. Biochemistry. 23:1383-1391. doi:10.1021/bi00302a008
64. Sugasawa, K., J.M. Ng, C. Masutani, S. Iwai, P.J. van der Spek, A.P. Eker, F. Hanaoka, D. Bootsma, and J.H. Hoeijmakers. 1998. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell. 2:223-232. doi:10.1016/S1097-2765(00)80132-X (Pubitemid 128373647)
65. Sugasawa, K., J. Akagi, R. Nishi, S. Iwai, and F. Hanaoka. 2009. Two-step recognition of DNA damage for mammalian nucleotide excision repair: Directional binding of the XPC complex and DNA strand scanning. Mol. Cell. 36:642-653. doi:10.1016/j.molcel.2009.09.035
66. Tapias, A., J. Auriol, D. Forget, J.H. Enzlin, O.D. Schärer, F. Coin, B. Coulombe, and J.M. Egly. 2004. Ordered conformational changes in damaged DNA induced by nucleotide excision repair factors. J. Biol. Chem. 279:19074-19083. doi:10.1074/jbc.M312611200 (Pubitemid 38623338)
67. Tsodikov, O.V., D. Ivanov, B. Orelli, L. Staresincic, I. Shoshani, R. Oberman, O.D. Schärer, G. Wagner, and T. Ellenberger. 2007. Structural basis for the recruitment of ERCC1-XPF to nucleotide excision repair complexes by XPA. EMBO J. 26:4768-4776. doi:10.1038/sj.emboj.7601894
68. van Attikum, H., and S.M. Gasser. 2009. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol. 19:207-217. doi:10.1016/j.tcb.2009.03.001
69. van den Boom, V., E. Citterio, D. Hoogstraten, A. Zotter, J.M. Egly, W.A. van Cappellen, J.H. Hoeijmakers, A.B. Houtsmuller, and W. Vermeulen. 2004. DNA damage stabilizes interaction of CSB with the transcription elongation machinery. J. Cell Biol. 166:27-36. doi:10.1083/jcb.200401056
70. van Duin, M., J. de Wit, H. Odijk, A. Westerveld, A. Yasui, M.H. Koken, J.H. Hoeijmakers, and D. Bootsma. 1986. Molecular characterization of the human excision repair gene ERCC-1: cDNA cloning and amino acid homology with the yeast DNA repair gene RAD10. Cell. 44:913-923. doi:10.1016/0092-8674(86)90014-0
71. van Hoffen, A., J. Venema, R. Meschini, A.A. van Zeeland, and L.H. Mullenders. 1995. Transcription-coupled repair removes both cyclobutane pyrimidine dimers and 6-4 photoproducts with equal efficiency and in a sequential way from transcribed DNA in xeroderma pigmentosum group C fibroblasts. EMBO J. 14:360-367.
72. Vermeulen, W., R.J. Scott, S. Rodgers, H.J. Müller, J. Cole, C.F. Arlett, W.J. Kleijer, D. Bootsma, J.H. Hoeijmakers, and G. Weeda. 1994. Clinical heterogeneity within xeroderma pigmentosum associated with mutations in the DNA repair and transcription gene ERCC3. Am. J. Hum. Genet. 54:191-200. (Pubitemid 24046331)
73. Villani, G., and N. Tanguy Le Gac. 2000. Interactions of DNA helicases with damaged DNA: possible biological consequences. J. Biol. Chem. 275:33185-33188. doi:10.1074/jbc.R000011200
74. Volker, M., M.J. Moné, P. Karmakar, A. van Hoffen, W. Schul, W. Vermeulen, J.H. Hoeijmakers, R. van Driel, A.A. van Zeeland, and L.H. Mullenders. 2001. Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell. 8:213-224. doi:10.1016/S1097-2765(01)00281-7 (Pubitemid 32772919)
75. Wakasugi, M., and A. Sancar. 1999. Order of assembly of human DNA repair excision nuclease. J. Biol. Chem. 274:18759-18768. doi:10.1074/jbc.274.26.18759 (Pubitemid 129519286)
76. Yagi, T., J. Tatsumi-Miyajima, M. Sato, K.H. Kraemer, and H. Takebe. 1991. Analysis of point mutations in an ultraviolet-irradiated shuttle vector plasmid propagated in cells from Japanese xeroderma pigmentosum patients in complementation groups A and F. Cancer Res. 51:3177-3182.
77. Ye, N., M.S. Bianchi, N.O. Bianchi, and G.P. Holmquist. 1999. Adaptive enhancement and kinetics of nucleotide excision repair in humans. Mutat. Res. 435:43-61. (Pubitemid 29474946)
78. Yokoi, M., C. Masutani, T. Maekawa, K. Sugasawa, Y. Ohkuma, and F. Hanaoka. 2000. The xeroderma pigmentosum group C protein complex XPC-HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA. J. Biol. Chem. 275:9870-9875. doi:10.1074/jbc.275.13.9870 (Pubitemid 30185224)
79. Zotter, A., M.S. Luijsterburg, D.O. Warmerdam, S. Ibrahim, A. Nigg, W.A. van Cappellen, J.H. Hoeijmakers, R. van Driel, W. Vermeulen, and A.B. Houtsmuller. 2006. Recruitment of the nucleotide excision repair endonuclease XPG to sites of UV-induced dna damage depends on functional TFIIH. Mol. Cell. Biol. 26:8868-8879. doi:10.1128/MCB.00695-06 (Pubitemid 44851945)