Recognition of DNA damage by XPC coincides with disruption of the XPC-RAD23 complex

Journal of Cell Biology

Volumn 196, Issue 6, 2012, Pages 681-688

  Bergink, Steven ^a,c   Toussaint, Wendy ^a,d   Luijsterburg, Martijn S ^b   Dinant, Christoffel ^a,e   Alekseev, Sergey ^a   Hoeijmakers, Jan H J ^a   Dantuma, Nico P ^b   Houtsmuller, Adriaan B ^a   Vermeulen, Wim ^a  

^a JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

^b KAROLINSKA INSTITUTE   (Sweden)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d GHENT UNIVERSITY   (Belgium)

^e DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME; PROTEIN; RAD23A PROTEIN; RAD23B PROTEIN; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP C PROTEIN;

ANIMAL CELL; ARTICLE; CELL MOTILITY; CHROMATIN; CONTROLLED STUDY; DISSOCIATION; DNA DAMAGE; EXCISION REPAIR; IN VITRO STUDY; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ULTRAVIOLET IRRADIATION;

ANIMALS; CELL LINE; CELL NUCLEUS; DNA; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; MICE;

EID: 84860339685     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201107050     Document Type: Article

References (41)

1. Alekseev, S., M.S. Luijsterburg, A. Pines, B. Geverts, P.O. Mari, G. Giglia-Mari, H. Lans, A.B. Houtsmuller, L.H. Mullenders, J.H. Hoeijmakers, and W. Vermeulen. 2008. Cellular concentrations of DDB2 regulate dynamic binding of DDB1 at UV-induced DNA damage. Mol. Cell. Biol. 28:7402-7413. http://dx.doi.org/10.1128/MCB.01108-08
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. http://dx.doi.org/10.1074/jbc.M100855200
3. Camenisch, U., D. Träutlein, F.C. Clement, J. Fei, A. Leitenstorfer, E. Ferrando-May, and H. Naegeli. 2009. Two-stage dynamic DNA quality check by xeroderma pigmentosum group C protein. EMBO J. 28:2387-2399. http://dx.doi.org/10.1038/emboj.2009.187
4. Cheo, D.L., H.J. Ruven, L.B. Meira, R.E. Hammer, D.K. Burns, N.J. Tappe, A.A. van Zeeland, L.H. Mullenders, and E.C. Friedberg. 1997. Characterization of defective nucleotide excision repair in XPC mutant mice. Mutat. Res. 374:1-9. http://dx.doi.org/10.1016/S0027-5107(97)00046-8
5. Cleaver, J.E. 2005. Cancer in xeroderma pigmentosum and related disorders of DNA repair. Nat. Rev. Cancer. 5:564-573. http://dx.doi.org/10.1038/nrc1652
6. Datsenko, K.A., and B.L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA. 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297
7. Dinant, C., M. de Jager, J. Essers, W.A. van Cappellen, R. Kanaar, A.B. Houtsmuller, and W. Vermeulen. 2007. Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J. Cell Sci. 120:2731-2740. http://dx.doi.org/10.1242/jcs.004523
8. Dundr, M., and T. Misteli. 2003. Measuring dynamics of nuclear proteins by photobleaching. Curr. Protoc. Cell Biol. Chapter 13:Unit 13.5.
9. Fei, J., N. Kaczmarek, A. Luch, A. Glas, T. Carell, and H. Naegeli. 2011. Regulation of nucleotide excision repair by UV-DDB: Prioritization of damage recognition to internucleosomal DNA. PLoS Biol. 9:e1001183. http://dx.doi.org/10.1371/journal.pbio.1001183
10. Fousteri, M., W. Vermeulen, A.A. van Zeeland, and L.H. Mullenders. 2006. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell. 23:471-482. http://dx.doi.org/10.1016/j.molcel.2006.06.029
11. Guzder, S.N., P. Sung, L. Prakash, and S. Prakash. 1998. Affinity of yeast nucleotide excision repair factor 2, consisting of the Rad4 and Rad23 proteins, for ultraviolet damaged DNA. J. Biol. Chem. 273:31541-31546. http://dx.doi.org/10.1074/jbc.273.47.31541
12. Hoeijmakers, J.H. 2001. Genome maintenance mechanisms for preventing cancer. Nature. 411:366-374. http://dx.doi.org/10.1038/35077232
13. 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. (published erratum appears in J. Cell Sci. 2008. 121:3991) http://dx.doi.org/10.1242/jcs.031708
14. 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.
15. Imam, A.M., G.P. Patrinos, M. de Krom, S. Bottardi, R.J. Janssens, E. Katsantoni, A.W. Wai, D.J. Sherratt, and F.G. Grosveld. 2000. Modification of human beta-globin locus PAC clones by homologous recombination in Escherichia coli. Nucleic Acids Res. 28:E65. http://dx.doi.org/10.1093/nar/28.12.e65
16. Janićijević, A., K. Sugasawa, Y. Shimizu, F. Hanaoka, N. Wijgers, M. Djurica, J.H. Hoeijmakers, and C. Wyman. 2003. DNA bending by the human damage recognition complex XPC-HR23B. DNA Repair (Amst.). 2:325-336. http://dx.doi.org/10.1016/S1568-7864(02)00222-7
17. Lommel, L., T. Ortolan, L. Chen, K. Madura, and K.S. Sweder. 2002. Proteolysis of a nucleotide excision repair protein by the 26 S proteasome. Curr. Genet. 42:9-20. http://dx.doi.org/10.1007/s00294-002-0332-9
18. Luijsterburg, M.S., G. von Bornstaedt, A.M. Gourdin, A.Z. Politi, M.J. Moné, D.O. Warmerdam, J. Goedhart, W. Vermeulen, R. van Driel, and T. Höfer. 2010. Stochastic and reversible assembly of a multiprotein DNA repair complex ensures accurate target site recognition and efficient repair. J. Cell Biol. 189:445-463. http://dx.doi.org/10.1083/jcb.200909175
19. Masutani, C., K. Sugasawa, J. Yanagisawa, T. Sonoyama, M. Ui, T. Enomoto, K. Takio, K. Tanaka, P.J. van der Spek, D. Bootsma, et al. 1994. Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homologue of yeast RAD23. EMBO J. 13:1831-1843.
20. Min, J.H., and N.P. Pavletich. 2007. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature. 449:570-575. http://dx.doi.org/10.1038/nature06155
21. 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 UVinduced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep. 2:1013-1017. http://dx.doi.org/10.1093/emboreports/kve224
22. 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. http://dx.doi.org/10.1016/j.dnarep.2005.01.001
23. 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. http://dx.doi.org/10.1016/j.molcel.2007.06.014
24. Ng, J.M., W. Vermeulen, G.T. van der Horst, S. Bergink, K. Sugasawa, H. Vrieling, and J.H. Hoeijmakers. 2003. A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev. 17:1630-1645. http://dx.doi.org/10.1101/gad.260003
25. Nishi, R., Y. Okuda, E. Watanabe, T. Mori, S. Iwai, C. Masutani, K. Sugasawa, and F. Hanaoka. 2005. Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol. Cell. Biol. 25:5664-5674. http://dx.doi.org/10.1128/MCB.25.13.5664-5674.2005
26. Ogi, T., S. Limsirichaikul, R.M. Overmeer, M. Volker, K. Takenaka, R. Cloney, Y. Nakazawa, A. Niimi, Y. Miki, N.G. Jaspers, et al. 2010. Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol. Cell. 37:714-727. http://dx.doi.org/10.1016/j.molcel.2010.02.009
27. Okuda, Y., R. Nishi, J.M. Ng, W. Vermeulen, G.T. van der Horst, T. Mori, J.H. Hoeijmakers, F. Hanaoka, and K. Sugasawa. 2004. Relative levels of the two mammalian Rad23 homologs determine composition and stability of the xeroderma pigmentosum group C protein complex. DNA Repair (Amst.). 3:1285-1295. http://dx.doi.org/10.1016/j.dnarep.2004.06.010
28. Overmeer, R.M., A.M. Gourdin, A. Giglia-Mari, H. Kool, A.B. Houtsmuller, G. Siegal, M.I. Fousteri, L.H. Mullenders, and W. Vermeulen. 2010. Replication factor C recruits DNA polymerase delta to sites of nucleotide excision repair but is not required for PCNA recruitment. Mol. Cell. Biol. 30:4828-4839. http://dx.doi.org/10.1128/MCB.00285-10
29. Renaud, E., L. Miccoli, N. Zacal, D.S. Biard, C.T. Craescu, A.J. Rainbow, and J.F. Angulo. 2011. Differential contribution of XPC, RAD23A, RAD23B and CENTRIN 2 to the UV-response in human cells. DNA Repair (Amst.). 10:835-847. http://dx.doi.org/10.1016/j.dnarep.2011.05.003
30. Sands, A.T., A. Abuin, A. Sanchez, C.J. Conti, and A. Bradley. 1995. High susceptibility to ultraviolet-induced carcinogenesis in mice lacking XPC. Nature. 377:162-165. http://dx.doi.org/10.1038/377162a0
31. Soutoglou, E., and T. Misteli. 2008. Activation of the cellular DNA damage response in the absence of DNA lesions. Science. 320:1507-1510. http://dx.doi.org/10.1126/science.1159051
32. Soutoglou, E., J.F. Dorn, K. Sengupta, M. Jasin, A. Nussenzweig, T. Ried, G. Danuser, and T. Misteli. 2007. Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 9:675-682. http://dx.doi.org/10.1038/ncb1591
33. Staresincic, L., A.F. Fagbemi, J.H. Enzlin, A.M. Gourdin, N. Wijgers, I. Dunand-Sauthier, G. Giglia-Mari, S.G. Clarkson, W. Vermeulen, and O.D. Schärer. 2009. Coordination of dual incision and repair synthesis in human nucleotide excision repair. EMBO J. 28:1111-1120. http://dx.doi.org/10.1038/emboj.2009.49
34. Sugasawa, K., C. Masutani, A. Uchida, T. Maekawa, P.J. van der Spek, D. Bootsma, J.H. Hoeijmakers, and F. Hanaoka. 1996. HHR23B, a human Rad23 homolog, stimulates XPC protein in nucleotide excision repair in vitro. Mol. Cell. Biol. 16:4852-4861.
35. Sugasawa, K., Y. Okuda, M. Saijo, R. Nishi, N. Matsuda, G. Chu, T. Mori, S. Iwai, K. Tanaka, K. Tanaka, and F. Hanaoka. 2005. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell. 121:387-400. http://dx.doi.org/10.1016/j.cell.2005.02.035
36. 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. http://dx.doi.org/10.1016/j.molcel.2009.09.035
37. Uchida, A., K. Sugasawa, C. Masutani, N. Dohmae, M. Araki, M. Yokoi, Y. Ohkuma, and F. Hanaoka. 2002. The carboxy-terminal domain of the XPC protein plays a crucial role in nucleotide excision repair through interactions with transcription factor IIH. DNA Repair (Amst.). 1:449-461. http://dx.doi.org/10.1016/S1568-7864(02)00031-9
38. Vermeulen, W. 2011. Dynamics of mammalian NER proteins. DNA Repair (Amst.). 10:760-771. http://dx.doi.org/10.1016/j.dnarep.2011.04.015
39. Vermeulen, W., M. Stefanini, S. Giliani, J.H. Hoeijmakers, and D. Bootsma. 1991. Xeroderma pigmentosum complementation group H falls into complementation group D. Mutat. Res. 255:201-208.
40. Watkins, J.F., and M.J. Smerdon. 1985. Nucleosome rearrangement in vitro. 2. Formation of nucleosomes in newly repaired regions of DNA. Biochemistry. 24:7288-7295. http://dx.doi.org/10.1021/bi00346a040
41. Xie, Z., S. Liu, Y. Zhang, and Z. Wang. 2004. Roles of Rad23 protein in yeast nucleotide excision repair. Nucleic Acids Res. 32:5981-5990. http://dx.doi.org/10.1093/nar/gkh934