Xeroderma pigmentosum group A protein loads as a separate factor onto DNA lesions

Molecular and Cellular Biology

Volumn 23, Issue 16, 2003, Pages 5755-5767

  Rademakers, Suzanne ^a   Volker, Marcel ^c   Hoogstraten, Deborah ^a   Nigg, Alex L ^b   Moné, Martijn J ^d   Van Zeeland, Albert A ^c   Hoeijmakers, Jan H J ^a   Houtsmuller, Adriaan B ^b   Vermeulen, Wim ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; POLYPEPTIDE; PROTEIN; REPLICATION PROTEIN A; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

ARTICLE; CELL LINE; CONTROLLED STUDY; DIFFUSION; DNA DAMAGE; DNA REPAIR; EXCISION REPAIR; HUMAN; HUMAN CELL; IMMOBILIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; ULTRAVIOLET IRRADIATION; XERODERMA PIGMENTOSUM;

CELL LINE; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, RADIATION; FIBROBLASTS; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOBLOTTING; LIGHT; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MODELS, GENETIC; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; TIME FACTORS; TRANSFECTION; ULTRAVIOLET RAYS; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

MAMMALIA;

EID: 0042632884     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.16.5755-5767.2003     Document Type: Article

References (64)

1. Aboussekhra, A., M. Biggerstaff, M. K. K. Shivji, J. A. Vilpo, V. Moncollin, V. N. Podust, M. Protic, U. Hubscher, J.-M. Egly, and R. D. Wood. 1995. Mammalian DNA nucleotide excision repair reconstituted with purified components. Cell 80:859-868.
2. Araki, M., C. Masutani, M. Takemura, A. Uchida, K. Sugasawa, J. Kondoh, Y. Ohkuma, and F. Hanaoka. 2001. Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J. Biol. Chem. 276:18665-18672.
3. Araujo, 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.
4. Araujo, S. J., F. Tirode, F. Coin, H. Pospiech, J. E. Syvaoja, M. Stucki, U. Hubscher, J. M. Egly, and R. D. Wood. 2000. Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK. Genes Dev. 14:349-359.
5. Araujo, S. J., and R. D. Wood. 1999. Protein complexes in nucleotide excision repair. Mutat. Res. 435:23-33.
6. Batty, D., V. Rapic'-Otrin, A. S. Levine, and R. D. Wood. 2000. Stable binding of human XPC complex to irradiated DNA confers strong discrimination for damaged sites. J. Mol. Biol. 300:275-290.
7. Bootsma, D., K. H. Kraemer, J. E. Cleaver, and J. H. J. Hoeijmakers. 2001. Nucleotide excision repair syndromes: xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy, p. 677-703. In B. Vogelstein and K. W. Kinzler (ed.), The genetic basis of human cancer, 8th ed. McGraw-Hill, New York, N.Y.
8. Bowman, K. K., D. M. Sicard, J. M. Ford, and P. C. Hanawalt. 2000. Reduced global genomic repair of ultraviolet light-induced cyclobutane pyrimidine dimers in simian virus 40-transformed human cells. Mol. Carcinog. 29:17-24.
9. Chu, G., and E. Chang. 1988. Xeroderma pigmentosum group E cells lack a nuclear factor that binds to damaged DNA. Science 242:564-567.
10. Citterio, E., W. Vermeulen, and J. H. J. Hoeijmakers. 2000. Transcriptional healing. Cell 101:447-450.
11. Cook, P. R. 1999. The organization of replication and transcription. Science 284:1790-1795.
12. Cooper, P. K., T. Nouspikel, S. G. Clarkson, and S. A. Leadon. 1997. Defective transcription-coupled repair of oxidative base damage in Cockayne syndrome patients from XP group G. Science 275:990-993.
13. de Boer, J., and J. H. Hoeijmakers. 2000. Nucleotide excision repair and human syndromes. Carcinogenesis 21:453-460.
14. 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.
15. de Laat, W. L., N. G. Jaspers, and J. H. Hoeijmakers. 1999. Molecular mechanism of nucleotide excision repair. Genes Dev. 13:768-785.
16. Drapkin, R., J. T. Reardon, A. Ansari, J. C. Huang, L. Zawel, K. Ahn, A. Sancar, and D. Reinberg. 1994. Dual role of TFIIH in DNA excision repair and in transcription by RNA polymerase II. Nature 368:769-772.
17. Eker, A. P. M., W. Vermeulen, N. Miura, K. Tanaka, N. G. J. Jaspers, J. H. J. Hoeijmakers, and D. Bootsma. 1992. Xeroderma pigmentosum group A correcting protein from calf thymus. Mutat. Res. 274:211-224.
18. Ellenberg, J., E. D. Siggia, J. E. Moreira, C. L. Smith, J. F. Presley, H. J. Worman, and J. Lippincott-Schwartz. 1997. Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J. Cell Biol. 138:1193-1206.
19. Essers, J., A. B. Houtsmuller, L. van Veelen, C. Paulusma, A. L. Nigg, A. Pastink, W. Vermeulen, J. H. J. Hoeijmakers, and R. Kanaar. 2002. Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J. 21:2030-2037.
20. 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.
21. Friedberg, E. C., G. C. Walker, and W. Siede. 1995. DNA repair and mutagenesis, ASM Press, Washington, D.C.
22. Frit, P., E. Bergmann, and J. M. Egly. 1999. Transcription factor IIH: a key player in the cellular response to DNA damage. Biochimie 81:27-38.
23. Guzder, S. N., P. Sung, L. Prakash, and S. Prakash. 1996. Nucleotide excision repair in yeast is mediated by sequential assembly of repair factors and not by a pre-assembled repairosome. J. Biol. Chem. 271:8903-8910.
24. Hamel, B. C., A. Raams, A. R. Schuitema-Dijkstra, P. Simons, I. van der Burgt, N. G. Jaspers, and W. J. Kleijer. 1996. Xeroderma pigmentosum-Cockayne syndrome complex: a further case. J. Med. Genet. 33:607-610.
25. Hanawalt, P., and G. Spivak. 1999. Transcription-coupled DNA repair. In M. Dizdaroglu and A. E. Karakaya (ed.), Advances in DNA damage and repair. Kluwer Academic/Plenum Publishers, New York, N.Y.
26. He, Z., L. A. Henricksen, M. S. Wold, and C. J. Ingles. 1995. RPA involvement in the damage-recognition and incision steps of nucleotide excision repair. Nature 374:566-569.
27. Hoeijmakers, J. H. 2001. Genome maintenance mechanisms for preventing cancer. Nature 411:366-374.
28. 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.
29. Houtsmuller, A. B., S. Rademakers, A. L. Nigg, D. Hoogstraten, J. H. J. Hoeijmakers, and W. Vermeulen. 1999. Action of DNA repair endonuclease ERCC1/XPF in living cells. Science 284:958-961.
30. Houtsmuller, A. B., and W. Vermeulen. 2001. Macromolecular dynamics in living cell nuclei revealed by fluorescence redistribution after photobleaching. Histochem. Cell Biol. 115:13-21.
31. Hwang, B. J., J. M. Ford, P. C. Hanawalt, and G. Chu. 1999. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl. Acad. Sci. USA 96:424-428.
32. Iyer, N., M. S. Reagan, K.-J. Wu, B. Canagarajah, and E. C. Friedberg. 1996. Interactions involving the human RNA polymerase II transcription/nucleotide excision repair complex TFIIH, the nucleotide excision repair protein XPG, and Cockayne syndrome group B (CSB) protein. Biochemistry 35:2157-2167.
33. Keeney, S., G. J. Chang, and S. Linn. 1993. Characterization of human DNA damage binding protein implicated in xeroderma pigmentosum E. J. Biol. Chem. 268:21293-21300.
34. Kowalczykowski, S. C. 2000. Some assembly required. Nat. Struct. Biol. 7:1087-1089.
35. Kusumoto, R., C. Masutani, K. Sugasawa, S. Iwai, M. Araki, A. Uchida, T. Mizukoshi, and F. Hanaoka. 2001. Diversity of the damage recognition step in the global genomic nucleotide excision repair in vitro. Mutat. Res. 485:219-227.
36. Le Page, F., E. E. Kwoh, A. Avrutskaya, A. Gentil, S. A. Leadon, A. Sarasin, and P. K. Cooper. 2000. Transcription-coupled repair of 8-oxoguanine: requirement for XPG, TFIIH, and CSB and implications for Cockayne syndrome. Cell 101:159-171.
37. Li, L., X. Lu, C. A. Peterson, and R. J. Legerski. 1995. An interaction between the DNA repair factor XPA and replication protein A appears essential for nucleotide excision repair. Mol. Cell. Biol. 15:5396-5402.
38. Lindahl, T., and R. D. Wood. 1999. Quality control by DNA repair. Science 286:1897-1905.
39. Matsuda, T., M. Saijo, I. Kuraoka, T. Kobayashi, Y. Nahatssu, A. Nagai, T. Enjoji, C. Masutani, K. Sugasawa, F. Hanaoka, A. Yasui, and K. Tanaka. 1995. DNA repair protein XPA binds to replication protein A (RPA). J. Biol. Chem. 270:4152-4157.
40. Mer, G., A. Bochkarev, R. Gupta, E. Bochkareva, L. Frappier, C. J. Ingles, A. M. Edwards, and W. J. Chazin. 2000. Structural basis for the recognition of DNA repair proteins UNG2, XPA, and RAD52 by replication factor RPA. Cell 103:449-456.
41. Missura, M., T. Buterin, R. Hindges, U. Hubscher, J. Kasparkova, V. Brabec, and H. Naegeli. 2001. Double-check probing of DNA bending and unwinding by XPA-RPA: an architectural function in DNA repair. EMBO J. 20:3554-3564.
42. Miura, N., I. Miyamoto, H. Asahina, I. Satokata, K. Tanaka, and Y. Okada. 1991. Identification and characterization of XPAC protein, the gene product of the human XPAC (xeroderma pigmentosum group A complementing) gene. J. Biol. Chem. 266:19786-19789.
43. Mone, 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.
44. Mu, D., C. H. Park, T. Matsunaga, D. S. Hsu, J. T. Reardon, and A. Sancar. 1995. Reconstitution of human DNA repair excision nuclease in a highly defined system. J. Biol. Chem. 270:2415-2418.
45. Nakatsu, Y., H. Asahina, E. Citterio, S. Rademakers, W. Vermeulen, S. Kamiuchi, J. P. Yeo, M. C. Khaw, M. Saijo, N. Kodo, T. Matsuda, J. H. Hoeijmakers, and K. Tanaka. 2000. XAB2, a novel tetratricopeptide repeat protein involved in transcription-coupled DNA repair and transcription. J. Biol. Chem. 275:34931-34937.
46. Niedernhofer, L. J., J. Essers, G. Weeda, B. Beverloo, J. de Wit, M. Muijtjens, H. Odijk, J. H. Hoeijmakers, and R. Kanaar. 2001. The structure-specific endonuclease Ercc1-Xpf is required for targeted gene replacement in embryonic stem cells. EMBO J. 20:6540-6549.
47. Patrick, S. M., and J. J. Turchi. 2002. Xeroderma pigmentosum complementation group A protein (XPA) modulates RPA-DNA interactions via enhanced complex stability and inhibition of strand separation activity. J. Biol. Chem. 277:16096-16101.
48. Reardon, J. T., and A. Sancar. 2002. Molecular anatomy of the human excision nuclease assembled at sites of DNA damage. Mol. Cell. Biol. 22:5938-5945.
49. Robins, P., C. J. Jones, M. Biggerstaff, T. Lindahl, and R. D. Wood. 1991. Complementation of DNA repair in xeroderma pigmentosum group A cell extracts by a protein with affinity for damaged DNA. EMBO J. 10:3913-3921.
50. Schaeffer, L., R. Roy, S. Humbert, V. Moncollin, W. Vermeulen, J. H. J. Hoeijmakers, P. Chambon, and J. Egly. 1993. DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science 260:58-63.
51. Selby, C. P., and A. Sancar. 1997. Human transcription-repair coupling factor CSB/ERCC6 is a DNA-stimulated ATPase but is not a helicase and does not disrupt the ternary transcription complex of stalled RNA polymerase II. J. Biol. Chem. 272:1885-1890.
52. 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.
53. Sugasawa, K., T. Okamoto, Y. Shimizu, C. Masutani, S. Iwai, and F. Hanaoka. 2001. A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 15:507-521.
54. Svejstrup, J. Q., Z. G. Wang, W. J. Feaver, X. H. Wu, D. A. Bushnell, T. F. Donahue, E. C. Friedberg, and R. D. Kornberg. 1995. Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a nucleotide excision repairosome. Cell 80:21-28.
55. Svetlova, M., A. Nikiforov, L. Solovjeva, N. Pleskach, N. Tomilin, and P. C. Hanawalt. 1999. Reduced extractability of the XPA DNA repair protein in ultraviolet light-irradiated mammalian cells. FEBS Lett. 463:49-52.
56. Tang, J. Y., B. J. Hwang, J. M. Ford, P. C. Hanawalt, and G. Chu. 2000. Xeroderma pigmentosum p48 gene enhances global genomic repair and suppresses UV-induced mutagenesis. Mol. Cell 5:737-744.
57. Van der Spek, P. J., A. Eker, S. Rademakers, C. Visser, K. Sugasawa, C. Masutani, F. Hanaoka, D. Bootsma, and J. H. J. Hoeijmakers. 1996. XPC and human homologs of RAD23: intracellular localization and relationship to other nucleotide excision repair complexes. Nucleic Acids Res. 24:2551-2559.
58. Van Gool, A. J., G. T. J. Van der Horst, E. Citterio, and J. H. J. Hoeijmakers. 1997. Cockayne syndrome: defective repair of transcription? EMBO J. 16:4155-4162.
59. Vermeulen,W., A. J. Van Vuuren, M. Chipoulet, L. Schaeffer, E. Appeldoorn, G. Weeda, N. G. Jaspers, A. Priestley, C. F. Arlett, A. R. Lehmann, M. Stefeanini, M. Mezzina, A. Sarasin, D. Bootsma, J.-M. Egly, and J. H. J. Hoeijmakers. 1994. Three unusual repair deficiencies associated with transcription factor BTF2(TFIIH): evidence for the existence of a transcription syndrome. Cold Spring Harbor Symp. Quant. Biol. 59:317-329.
60. Volker, M., M. J. Moné, P. Karmakar, A. Hoffen, W. Schul, W. Vermeulen, J. H. J. Hoeijmakers, R. van Driel, A. A. van Zeeland, and L. H. F. Mullenders. 2001. Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8:213-224.
61. Wakasugi, M., and A. Sancar. 1999. Order of assembly of human DNA repair excision nuclease. J. Biol. Chem. 274:18759-18768.
62. Wakasugi, M., M. Shimizu, H. Morioka, S. Linn, O. Nikaido, and T. Matsunaga. 2001. Damaged DNA-binding protein DDB stimulates the excision of cyclobutane pyrimidine dimers in vitro in concert with XPA and replication protein A. J. Biol. Chem. 276:15434-15440.
63. Wansink, D. G., W. Schul, I. van der Kraan, B. van Steensel, R. van Driel, and L. de Jong. 1993. Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J. Cell Biol. 122:283-293.
64. 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.