Skip to main content
SpringerLink
Log in

Molecular Mechanism of DNA Damage Recognition for Global Genomic Nucleotide Excision Repair: A Defense System Against UV-Induced Skin Cancer

  • Chapter
  • First Online:
DNA Repair Disorders

Abstract

Nucleotide excision repair (NER) is a versatile DNA repair pathway responsible for removal of ultraviolet light (UV)-induced DNA photolesions from the genome. In mammals, NER operating throughout the genome decreases the risk of UV-induced mutagenesis arising due to DNA translesion synthesis across photolesions on template DNA strands and thereby contributes to suppression of skin cancer. Lesion recognition for global genomic NER relies on multiple xeroderma pigmentosum (XP)-related protein factors, XPC, UV-DDB, TFIIH, and XPA, each of which probes for a different aspect of abnormal DNA structure. A combination of diverse strategies is likely required to achieve the broad substrate specificity, efficiency, and accuracy of this DNA repair system. To regulate this elaborate system in vivo, post-translational protein modifications, such as ubiquitination, and higher-order chromatin structures also play important roles.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 139.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Kraemer KH, Lee MM, Andrews AD, Lambert WC. The role of sunlight and DNA repair in melanoma and nonmelanoma skin cancer. The xeroderma pigmentosum paradigm. Arch Dermatol. 1994;130:1018–21. https://doi.org/10.1001/archderm.1994.01690080084012.

    Article  CAS  PubMed  Google Scholar 

  2. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T, editors. DNA repair and mutagenesis. 2nd ed. Washington: ASM Press; 2006.

    Google Scholar 

  3. Gillet LCJ, Schärer OD. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev. 2006;106:253–76. https://doi.org/10.1021/cr040483f.

    Article  CAS  PubMed  Google Scholar 

  4. Cleaver JE, Crowley E. UV damage, DNA repair and skin carcinogenesis. Front Biosci. 2002;7:d1024–43. https://doi.org/10.2741/A829.

    Article  CAS  PubMed  Google Scholar 

  5. Friedberg EC. How nucleotide excision repair protects against cancer. Nat Rev Cancer. 2001;1:22–33. https://doi.org/10.1038/35094000.

    Article  CAS  PubMed  Google Scholar 

  6. Schärer OD. Nucleotide excision repair in eukaryotes. Cold Spring Harb Perspect Biol. 2013;5:a012609. https://doi.org/10.1101/cshperspect.a012609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Brooks PJ, Wise DS, Berry DA, Kosmoski JV, Smerdon MJ, Somers RL, Mackie H, Spoonde AY, Ackerman EJ, Coleman K, Tarone RE, Robbins JH. The oxidative DNA lesion 8,5′-(S)-cyclo-2′-deoxyadenosine is repaired by the nucleotide excision repair pathway and blocks gene expression in mammalian cells. J Biol Chem. 2000;275:22355–62. https://doi.org/10.1074/jbc.M002259200.

    Article  CAS  PubMed  Google Scholar 

  8. Kuraoka I, Bender C, Romieu A, Cadet J, Wood RD, Lindahl T. Removal of oxygen free-radical-induced 5′,8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc Natl Acad Sci U S A. 2000;97:3832–7. https://doi.org/10.1073/pnas.070471597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wood RD. Mammalian nucleotide excision repair proteins and interstrand crosslink repair. Environ Mol Mutagen. 2010;51:520–6. https://doi.org/10.1002/em.20569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Langevin F, Crossan GP, Rosado IV, Arends MJ, Patel KJ. Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature. 2011;475:53–8. https://doi.org/10.1038/nature10192.

    Article  CAS  PubMed  Google Scholar 

  11. Noll DM, Mason TM, Miller PS. Formation and repair of interstrand cross-links in DNA. Chem Rev. 2006;106:277–301. https://doi.org/10.1021/cr040478b.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Riedl T, Hanaoka F, Egly JM. The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J. 2003;22:5293–303. https://doi.org/10.1093/emboj/cdg489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Sugasawa K, Ng JMY, Masutani C, Iwai S, van der Spek PJ, Eker APM, Hanaoka F, Bootsma D, Hoeijmakers JHJ. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell. 1998;2:223–32. https://doi.org/10.1016/S1097-2765(00)80132-X.

    Article  CAS  PubMed  Google Scholar 

  14. Volker M, Moné MJ, Karmakar P, van Hoffen A, Schul W, Vermeulen W, Hoeijmakers JHJ, van Driel R, van Zeeland AA, Mullenders LHF. Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell. 2001;8:213–24. https://doi.org/10.1016/s1097-2765(01)00281-7.

    Article  CAS  PubMed  Google Scholar 

  15. Fujiwara Y, Masutani C, Mizukoshi T, Kondo J, Hanaoka F, Iwai S. Characterization of DNA recognition by the human UV-damaged DNA-binding protein. J Biol Chem. 1999;274:20027–33. https://doi.org/10.1074/jbc.274.28.20027.

    Article  CAS  PubMed  Google Scholar 

  16. Sugasawa K, Okuda Y, Saijo M, Nishi R, Matsuda N, Chu G, Mori T, Iwai S, Tanaka K, Tanaka K, Hanaoka F. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell. 2005;121:387–400. https://doi.org/10.1016/j.cell.2005.02.035.

    Article  CAS  PubMed  Google Scholar 

  17. Wittschieben BØ, Iwai S, Wood RD. DDB1-DDB2 (xeroderma pigmentosum group E) protein complex recognizes a cyclobutane pyrimidine dimer, mismatches, apurinic/apyrimidinic sites, and compound lesions in DNA. J Biol Chem. 2005;280:39982–9. https://doi.org/10.1074/jbc.M507854200.

    Article  CAS  PubMed  Google Scholar 

  18. Hanawalt PC, Spivak G. Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol. 2008;9:958–70. https://doi.org/10.1038/nrm2549.

    Article  CAS  PubMed  Google Scholar 

  19. Compe E, Egly JM. TFIIH: when transcription met DNA repair. Nat Rev Mol Cell Biol. 2012;13:343–54. https://doi.org/10.1038/nrm3350.

    Article  CAS  PubMed  Google Scholar 

  20. Araújo SJ, Nigg EA, Wood RD. Strong functional interactions of TFIIH with XPC and XPG in human DNA nucleotide excision repair, without a preassembled repairosome. Mol Cell Biol. 2001;21:2281–91. https://doi.org/10.1128/MCB.21.7.2281-2291.2001.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Li RY, Calsou P, Jones CJ, Salles B. Interactions of the transcription/DNA repair factor TFIIH and XP repair proteins with DNA lesions in a cell-free repair assay. J Mol Biol. 1998;281:211–8. https://doi.org/10.1006/jmbi.1998.1949.

    Article  CAS  PubMed  Google Scholar 

  22. Yokoi M, Masutani C, Maekawa T, Sugasawa K, Ohkuma Y, Hanaoka F. 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. 2000;275:9870–5.

    Article  CAS  PubMed  Google Scholar 

  23. Evans E, Moggs JG, Hwang JR, Egly JM, Wood RD. Mechanism of open complex and dual incision formation by human nucleotide excision repair factors. EMBO J. 1997;16:6559–73. https://doi.org/10.1093/emboj/16.21.6559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mu D, Wakasugi M, Hsu DS, Sancar A. Characterization of reaction intermediates of human excision repair nuclease. J Biol Chem. 1997;272:28971–9. https://doi.org/10.1074/jbc.272.46.28971.

    Article  CAS  PubMed  Google Scholar 

  25. Tapias A, Auriol J, Forget D, Enzlin JH, Schärer OD, Coin F, Coulombe B, Egly JM. Ordered conformational changes in damaged DNA induced by nucleotide excision repair factors. J Biol Chem. 2004;279:19074–83. https://doi.org/10.1074/jbc.M312611200.

    Article  CAS  PubMed  Google Scholar 

  26. Li C-L, Golebiowski FM, Onishi Y, Samara NL, Sugasawa K, Yang W. Tripartite DNA lesion recognition and verification by XPC, TFIIH, and XPA in nucleotide excision repair. Mol Cell. 2015;59:1025–34. https://doi.org/10.1016/j.molcel.2015.08.012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. de Laat WL, Appeldoorn E, Sugasawa K, Weterings E, Jaspers NGJ, Hoeijmakers JHJ. DNA-binding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev. 1998;12:2598–609. https://doi.org/10.1101/gad.12.16.2598.

    Article  PubMed  PubMed Central  Google Scholar 

  28. He Z, Henricksen LA, Wold MS, Ingles CJ. RPA involvement in the damage-recognition and incision steps of nucleotide excision repair. Nature. 1995;374:566–9. https://doi.org/10.1038/374566a0.

    Article  CAS  PubMed  Google Scholar 

  29. Li L, Lu X, Peterson CA, Legerski RJ. An interaction between the DNA repair factor XPA and replication protein A appears essential for nucleotide excision repair. Mol Cell Biol. 1995;15:5396–402. https://doi.org/10.1128/MCB.15.10.5396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Matsuda T, Saijo M, Kuraoka I, Kobayashi T, Nakatsu Y, Nagai A, Enjoji T, Masutani C, Sugasawa K, Hanaoka F. DNA repair protein XPA binds replication protein A (RPA). J Biol Chem. 1995;270:4152–7. https://doi.org/10.1074/jbc.270.8.4152.

    Article  CAS  PubMed  Google Scholar 

  31. Patrick SM, Turchi JJ. Xeroderma pigmentosum complementation group a protein (XPA) modulates RPA-DNA interactions via enhanced complex stability and inhibition of strand separation activity. J Biol Chem. 2002;277:16096–101. https://doi.org/10.1074/jbc.M200816200.

    Article  CAS  PubMed  Google Scholar 

  32. Matsunaga T, Mu D, Park CH, Reardon JT, Sancar A. Human DNA repair excision nuclease. Analysis of the roles of the subunits involved in dual incisions by using anti-XPG and anti-ERCC1 antibodies. J Biol Chem. 1995;270:20862–9. https://doi.org/10.1074/jbc.270.35.20862.

    Article  CAS  PubMed  Google Scholar 

  33. Moggs JG, Yarema KJ, Essigmann JM, Wood RD. Analysis of incision sites produced by human cell extracts and purified proteins during nucleotide excision repair of a 1,3-intrastrand d(GpTpG)-cisplatin adduct. J Biol Chem. 1996;271:7177–86. https://doi.org/10.1074/jbc.271.12.7177.

    Article  CAS  PubMed  Google Scholar 

  34. O’Donovan A, Davies AA, Moggs JG, West SC, Wood RD. XPG endonuclease makes the 3′ incision in human DNA nucleotide excision repair. Nature. 1994;371:432–5. https://doi.org/10.1038/371432a0.

    Article  PubMed  Google Scholar 

  35. Sijbers AM, de Laat WL, Ariza RR, Biggerstaff M, Wei YF, Moggs JG, Carter KC, Shell BK, Evans E, de Jong MC, Rademakers S, de Rooij J, Jaspers NGJ, Hoeijmakers JHJ, Wood RD. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell. 1996;86:811–22. https://doi.org/10.1016/S0092-8674(00)80155-5.

    Article  CAS  PubMed  Google Scholar 

  36. Ito S, Kuraoka I, Chymkowitch P, Compe E, Takedachi A, Ishigami C, Coin F, Egly JM, Tanaka K. XPG stabilizes TFIIH, allowing transactivation of nuclear receptors: implications for Cockayne syndrome in XP-G/CS patients. Mol Cell. 2007;26:231–43. https://doi.org/10.1016/j.molcel.2007.03.013.

    Article  CAS  PubMed  Google Scholar 

  37. Zotter A, Luijsterburg MS, Warmerdam DO, Ibrahim S, Nigg A, van Cappellen WA, Hoeijmakers JHJ, van Driel R, Vermeulen W, Houtsmuller AB. Recruitment of the nucleotide excision repair endonuclease XPG to sites of UV-induced DNA damage depends on functional TFIIH. Mol Cell Biol. 2006;26:8868–79. https://doi.org/10.1128/MCB.00695-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Li L, Elledge SJ, Peterson CA, Bales ES, Legerski RJ. Specific association between the human DNA repair proteins XPA and ERCC1. Proc Natl Acad Sci U S A. 1994;91:5012–6. https://doi.org/10.1073/pnas.91.11.5012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Li L, Peterson CA, Lu X, Legerski RJ. Mutations in XPA that prevent association with ERCC1 are defective in nucleotide excision repair. Mol Cell Biol. 1995;15:1993–8. https://doi.org/10.1128/MCB.15.4.1993.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Park CH, Sancar A. Formation of a ternary complex by human XPA, ERCC1, and ERCC4(XPF) excision repair proteins. Proc Natl Acad Sci U S A. 1994;91:5017–21. https://doi.org/10.1073/pnas.91.11.5017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Staresincic L, Fagbemi AF, Enzlin JH, Gourdin AM, Wijgers N, Dunand-Sauthier I, Giglia-Mari G, Clarkson SG, Vermeulen W, Schärer OD. Coordination of dual incision and repair synthesis in human nucleotide excision repair. EMBO J. 2009;28:1111–20. https://doi.org/10.1038/emboj.2009.49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Constantinou A, Gunz D, Evans E, Lalle P, Bates PA, Wood RD, Clarkson SG. Conserved residues of human XPG protein important for nuclease activity and function in nucleotide excision repair. J Biol Chem. 1999;274:5637–48. https://doi.org/10.1074/jbc.274.9.5637.

    Article  CAS  PubMed  Google Scholar 

  43. Wakasugi M, Reardon JT, Sancar A. The non-catalytic function of XPG protein during dual incision in human nucleotide excision repair. J Biol Chem. 1997;272:16030–4. https://doi.org/10.1074/jbc.272.25.16030.

    Article  CAS  PubMed  Google Scholar 

  44. Aboussekhra A, Biggerstaff M, Shivji MKK, Vilpo JA, Moncollin V, Podust VN, Protić M, Hübscher U, Egly JM, Wood RD. Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell. 1995;80:859–68. https://doi.org/10.1016/0092-8674(95)90289-9.

    Article  CAS  PubMed  Google Scholar 

  45. Araújo SJ, Tirode F, Coin F, Pospiech H, Syväoja JE, Stucki M, Hübscher U, Egly JM, Wood RD. 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. 2000;14:349–59. https://doi.org/10.1101/gad.14.3.349.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Shivji MK, Podust VN, Hübscher U, Wood RD. Nucleotide excision repair DNA synthesis by DNA polymerase epsilon in the presence of PCNA, RFC, and RPA. Biochemistry. 1995;34:5011–7. https://doi.org/10.1021/bi00015a012.

    Article  CAS  PubMed  Google Scholar 

  47. Gary R, Ludwig DL, Cornelius HL, MacInnes MA, Park MS. The DNA repair endonuclease XPG binds to proliferating cell nuclear antigen (PCNA) and shares sequence elements with the PCNA-binding regions of FEN-1 and cyclin-dependent kinase inhibitor p21. J Biol Chem. 1997;272:24522–9. https://doi.org/10.1074/jbc.272.39.24522.

    Article  CAS  PubMed  Google Scholar 

  48. Ogi T, Lehmann AR. The Y-family DNA polymerase k (pol k) functions in mammalian nucleotide-excision repair. Nat Cell Biol. 2006;8:640–2. https://doi.org/10.1038/ncb1417.

    Article  CAS  PubMed  Google Scholar 

  49. Ogi T, Limsirichaikul S, Overmeer RM, Volker M, Takenaka K, Cloney R, Nakazawa Y, Niimi A, Miki Y, Jaspers NG, Mullenders LHF, Yamashita S, Fousteri MI, Lehmann AR. Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol Cell. 2010;37:714–27. https://doi.org/10.1016/j.molcel.2010.02.009.

    Article  CAS  PubMed  Google Scholar 

  50. Moser J, Kool H, Giakzidis I, Caldecott K, Mullenders LHF, Fousteri MI. Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III alpha in a cell-cycle-specific manner. Mol Cell. 2007;27:311–23. https://doi.org/10.1016/j.molcel.2007.06.014.

    Article  CAS  PubMed  Google Scholar 

  51. Legerski R, Peterson C. Expression cloning of a human DNA repair gene involved in xeroderma pigmentosum group C. Nature. 1992;359:70–3. https://doi.org/10.1038/359070a0.

    Article  CAS  PubMed  Google Scholar 

  52. Masutani C, Sugasawa K, Yanagisawa J, Sonoyama T, Ui M, Enomoto T, Takio K, Tanaka K, van der Spek PJ, Bootsma D, Hoeijmakers JHJ, Hanaoka F. 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. 1994;13:1831–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Shivji MKK, Eker APM, Wood RD. DNA repair defect in xeroderma pigmentosum group C and complementing factor from HeLa cells. J Biol Chem. 1994;269:22749–57.

    CAS  PubMed  Google Scholar 

  54. Min J-H, Pavletich NP. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature. 2007;449:570–5. https://doi.org/10.1038/nature06155.

    Article  CAS  PubMed  Google Scholar 

  55. Anantharaman V. Peptide-N-glycanases and DNA repair proteins, Xp-C/Rad4, are, respectively, active and inactivated enzymes sharing a common transglutaminase fold. Hum Mol Genet. 2001;10:1627–30. https://doi.org/10.1093/hmg/10.16.1627.

    Article  CAS  PubMed  Google Scholar 

  56. Lee J-H, Choi JM, Lee C, Yi KJ, Cho Y. Structure of a peptide:N-glycanase-Rad23 complex: insight into the deglycosylation for denatured glycoproteins. Proc Natl Acad Sci U S A. 2005;102:9144–9. https://doi.org/10.1073/pnas.0502082102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Miller RD, Prakash L, Prakash S. Defective excision of pyrimidine dimers and interstrand DNA crosslinks in rad7 and rad23 mutants of Saccharomyces cerevisiae. Mol Gen Genet. 1982;188:235–9. https://doi.org/10.1007/BF00332681.

    Article  CAS  PubMed  Google Scholar 

  58. Sugasawa K, Ng JMY, Masutani C, Maekawa T, Uchida A, van der Spek PJ, Eker APM, Rademakers S, Visser C, Aboussekhra A, Wood RD, Hanaoka F, Bootsma D, Hoeijmakers JHJ. Two human homologs of Rad23 are functionally interchangeable in complex formation and stimulation of XPC repair activity. Mol Cell Biol. 1997;17:6924–31. https://doi.org/10.1128/MCB.17.12.6924.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Ng JMY, Vermeulen W, van der Horst GTJ, Bergink S, Sugasawa K, Vrieling H, Hoeijmakers JHJ. A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev. 2003;17:1630–45. https://doi.org/10.1101/gad.260003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Okuda Y, Nishi R, Ng JMY, Vermeulen W, van der Horst GTJ, Mori T, Hoeijmakers JHJ, Hanaoka F, Sugasawa K. Relative levels of the two mammalian Rad23 homologs determine composition and stability of the xeroderma pigmentosum group C protein complex. DNA Repair (Amst). 2004;3:1285–95. https://doi.org/10.1016/j.dnarep.2004.06.010.

    Article  CAS  Google Scholar 

  61. van der Spek PJ, Visser CE, Hanaoka F, Smit B, Hagemeijer A, Bootsma D, Hoeijmakers JHJ. Cloning, comparative mapping, and RNA expression of the mouse homologues of the Saccharomyces cerevisiae nucleotide excision repair gene RAD23. Genomics. 1996;31:20–7. https://doi.org/10.1006/geno.1996.0004.

    Article  PubMed  Google Scholar 

  62. Watkins JF, Sung P, Prakash L, Prakash S. The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function. Mol Cell Biol. 1993;13:7757–65. https://doi.org/10.1128/MCB.13.12.7757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sugasawa K, Masutani C, Uchida A, Maekawa T, van der Spek PJ, Bootsma D, Hoeijmakers JHJ, Hanaoka F. HHR23B, a human Rad23 homolog, stimulates XPC protein in nucleotide excision repair in vitro. Mol Cell Biol. 1996;16:4852–61. https://doi.org/10.1128/MCB.16.9.4852.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Masutani C, Araki M, Sugasawa K, van der Spek PJ, Yamada A, Uchida A, Maekawa T, Bootsma D, Hoeijmakers JHJ, Hanaoka F. Identification and characterization of XPC-binding domain of hHR23B. Mol Cell Biol. 1997;17:6915–23. https://doi.org/10.1128/MCB.17.12.6915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Araki M, Masutani C, Takemura M, Uchida A, Sugasawa K, Kondoh J, Ohkuma Y, Hanaoka F. 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. 2001;276:18665–72. https://doi.org/10.1074/jbc.M100855200.

    Article  CAS  PubMed  Google Scholar 

  66. Nishi R, Okuda Y, Watanabe E, Mori T, Iwai S, Masutani C, Sugasawa K, Hanaoka F. Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol Cell Biol. 2005;25:5664–74. https://doi.org/10.1128/MCB.25.13.5664-5674.2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Mu D, Park CH, Matsunaga T, Hsu DS, Reardon JT, Sancar A. Reconstitution of human DNA repair excision nuclease in a highly defined system. J Biol Chem. 1995;270:2415–8. https://doi.org/10.1074/jbc.270.6.2415.

    Article  CAS  PubMed  Google Scholar 

  68. Errabolu R, Sanders MA, Salisbury JL. Cloning of a cDNA encoding human centrin, an EF-hand protein of centrosomes and mitotic spindle poles. J Cell Sci. 1994;107(Pt 1):9–16.

    CAS  PubMed  Google Scholar 

  69. Salisbury JL, Suino KM, Busby R, Springett M. Centrin-2 is required for centriole duplication in mammalian cells. Curr Biol. 2002;12:1287–92. https://doi.org/10.1016/S0960-9822(02)01019-9.

    Article  CAS  PubMed  Google Scholar 

  70. Batty D, Rapic’-Otrin V, Levine AS, Wood RD. Stable binding of human XPC complex to irradiated DNA confers strong discrimination for damaged sites. J Mol Biol. 2000;300:275–90. https://doi.org/10.1006/jmbi.2000.3857.

    Article  CAS  PubMed  Google Scholar 

  71. Hey T, Lipps G, Sugasawa K, Iwai S, Hanaoka F, Krauss G. The XPC-HR23B complex displays high affinity and specificity for damaged DNA in a true-equilibrium fluorescence assay. Biochemistry. 2002;41:6583–7. https://doi.org/10.1021/bi012202t.

    Article  CAS  PubMed  Google Scholar 

  72. Kusumoto R, Masutani C, Sugasawa K, Iwai S, Araki M, Uchida A, Mizukoshi T, Hanaoka F. Diversity of the damage recognition step in the global genomic nucleotide excision repair in vitro. Mutat Res. 2001;485:219–27. https://doi.org/10.1016/S0921-8777(00)00082-3.

    Article  CAS  PubMed  Google Scholar 

  73. Sugasawa K, Okamoto T, Shimizu Y, Masutani C, Iwai S, Hanaoka F. A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 2001;15:507–21. https://doi.org/10.1101/gad.866301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Sugasawa K, Shimizu Y, Iwai S, Hanaoka F. A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair (Amst). 2002;1:95–107. https://doi.org/10.1016/S1568-7864(01)00008-8.

    Article  CAS  Google Scholar 

  75. Buterin T, Meyer C, Giese B, Naegeli H. DNA quality control by conformational readout on the undamaged strand of the double helix. Chem Biol. 2005;12:913–22. https://doi.org/10.1016/j.chembiol.2005.06.011.

    Article  CAS  PubMed  Google Scholar 

  76. Sugasawa K, Akagi J-I, Nishi R, Iwai S, Hanaoka F. Two-step recognition of DNA damage for mammalian nucleotide excision repair: directional binding of the XPC complex and DNA strand scanning. Mol Cell. 2009;36:642–53. https://doi.org/10.1016/j.molcel.2009.09.035.

    Article  CAS  PubMed  Google Scholar 

  77. Kong M, Liu L, Chen X, Driscoll KI, Mao P, Böhm S, Kad NM, Watkins SC, Bernstein KA, Wyrick JJ, Min J-H, Van Houten B. Single-molecule imaging reveals that Rad4 employs a dynamic DNA damage recognition process. Mol Cell. 2016;64:376–87. https://doi.org/10.1016/j.molcel.2016.09.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Camenisch U, Träutlein D, Clement FC, Fei J, Leitenstorfer A, Ferrando-May E, Naegeli H. Two-stage dynamic DNA quality check by xeroderma pigmentosum group C protein. EMBO J. 2009;28:2387–99. https://doi.org/10.1038/emboj.2009.187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Chen X, Velmurugu Y, Zheng G, Park B, Shim Y, Kim Y, Liu L, Van Houten B, He C, Ansari A, Min J-H. Kinetic gating mechanism of DNA damage recognition by Rad4/XPC. Nat Commun. 2015;6:5849. https://doi.org/10.1038/ncomms6849.

    Article  PubMed  Google Scholar 

  80. Hess MT, Schwitter U, Petretta M, Giese B, Naegeli H. Bipartite substrate discrimination by human nucleotide excision repair. Proc Natl Acad Sci U S A. 1997;94:6664–9. https://doi.org/10.1016/0092-8674(95)90289-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. McAteer K, Jing Y, Kao J, Taylor JS, Kennedy MA. Solution-state structure of a DNA dodecamer duplex containing a Cis-syn thymine cyclobutane dimer, the major UV photoproduct of DNA. J Mol Biol. 1998;282:1013–32. https://doi.org/10.1006/jmbi.1998.2062.

    Article  CAS  PubMed  Google Scholar 

  82. Coin F, Marinoni JC, Rodolfo C, Fribourg S, Pedrini AM, Egly JM. Mutations in the XPD helicase gene result in XP and TTD phenotypes, preventing interaction between XPD and the p44 subunit of TFIIH. Nat Genet. 1998;20:184–8. https://doi.org/10.1038/2491.

    Article  CAS  PubMed  Google Scholar 

  83. Schaeffer L, Moncollin V, Roy R, Staub A, Mezzina M, Sarasin A, Weeda G, Hoeijmakers JHJ, Egly JM. The ERCC2/DNA repair protein is associated with the class II BTF2/TFIIH transcription factor. EMBO J. 1994;13:2388–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Mathieu N, Kaczmarek N, Naegeli H. Strand- and site-specific DNA lesion demarcation by the xeroderma pigmentosum group D helicase. Proc Natl Acad Sci U S A. 2010;107:17545–50. https://doi.org/10.1073/pnas.1004339107.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Naegeli H, Bardwell L, Friedberg EC. The DNA helicase and adenosine triphosphatase activities of yeast Rad3 protein are inhibited by DNA damage. A potential mechanism for damage-specific recognition. J Biol Chem. 1992;267:392–8.

    CAS  PubMed  Google Scholar 

  86. Naegeli H, Sugasawa K. The xeroderma pigmentosum pathway: decision tree analysis of DNA quality. DNA Repair (Amst). 2011;10:673–83. https://doi.org/10.1016/j.dnarep.2011.04.019.

    Article  CAS  Google Scholar 

  87. Hwang JR, Moncollin V, Vermeulen W, Seroz T, van Vuuren H, Hoeijmakers JHJ, Egly JM. A 3′→5′ XPB helicase defect in repair/transcription factor TFIIH of xeroderma pigmentosum group B affects both DNA repair and transcription. J Biol Chem. 1996;271:15898–904. https://doi.org/10.1074/jbc.271.27.15898.

    Article  CAS  PubMed  Google Scholar 

  88. Tirode F, Busso D, Coin F, Egly JM. Reconstitution of the transcription factor TFIIH: assignment of functions for the three enzymatic subunits, XPB, XPD, and cdk7. Mol Cell. 1999;3:87–95. https://doi.org/10.1016/S1097-2765(00)80177-X.

    Article  CAS  PubMed  Google Scholar 

  89. Coin F, Oksenych V, Egly JM. Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol Cell. 2007;26:245–56. https://doi.org/10.1016/j.molcel.2007.03.009.

    Article  CAS  PubMed  Google Scholar 

  90. Oksenych V, Bernardes de Jesus B, Zhovmer A, Egly JM, Coin F. Molecular insights into the recruitment of TFIIH to sites of DNA damage. EMBO J. 2009;28:2971–80. https://doi.org/10.1038/emboj.2009.230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Tanaka K, Miura N, Satokata I, Miyamoto I, Yoshida MC, Satoh Y, Kondo S, Yasui A, Okayama H, Okada Y. Analysis of a human DNA excision repair gene involved in group A xeroderma pigmentosum and containing a zinc-finger domain. Nature. 1990;348:73–6. https://doi.org/10.1038/348073a0.

    Article  CAS  PubMed  Google Scholar 

  92. Bunick CG, Miller MR, Fuller BE, Fanning E, Chazin WJ. Biochemical and structural domain analysis of xeroderma pigmentosum complementation group C protein. Biochemistry. 2006;45:14965–79. https://doi.org/10.1021/bi061370o.

    Article  CAS  PubMed  Google Scholar 

  93. Nishi R, Sakai W, Tone D, Hanaoka F, Sugasawa K. Structure-function analysis of the EF-hand protein centrin-2 for its intracellular localization and nucleotide excision repair. Nucleic Acids Res. 2013;41:6917–29. https://doi.org/10.1093/nar/gkt434.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Nocentini S, Coin F, Saijo M, Tanaka K, Egly JM. DNA damage recognition by XPA protein promotes efficient recruitment of transcription factor II H. J Biol Chem. 1997;272:22991–4. https://doi.org/10.1074/jbc.272.37.22991.

    Article  CAS  PubMed  Google Scholar 

  95. Park CH, Mu D, Reardon JT, Sancar A. The general transcription-repair factor TFIIH is recruited to the excision repair complex by the XPA protein independent of the TFIIE transcription factor. J Biol Chem. 1995;270:4896–902. https://doi.org/10.1074/jbc.270.9.4896.

    Article  CAS  PubMed  Google Scholar 

  96. You J-S, Wang M, Lee S-H. Biochemical analysis of the damage recognition process in nucleotide excision repair. J Biol Chem. 2003;278:7476–85. https://doi.org/10.1074/jbc.M210603200.

    Article  CAS  PubMed  Google Scholar 

  97. Asahina H, Kuraoka I, Shirakawa M, Morita EH, Miura N, Miyamoto I, Ohtsuka E, Okada Y, Tanaka K. The XPA protein is a zinc metalloprotein with an ability to recognize various kinds of DNA damage. Mutat Res. 1994;315:229–37. https://doi.org/10.1016/0921-8777(94)90034-5.

    Article  CAS  PubMed  Google Scholar 

  98. Jones CJ, Wood RD. Preferential binding of the xeroderma pigmentosum group A complementing protein to damaged DNA. Biochemistry. 1993;32:12096–104. https://doi.org/10.1021/bi00096a021.

    Article  CAS  PubMed  Google Scholar 

  99. Missura M, Buterin T, Hindges R, Hübscher U, Kaspárková J, Brabec V, Naegeli H. Double-check probing of DNA bending and unwinding by XPA-RPA: an architectural function in DNA repair. EMBO J. 2001;20:3554–64. https://doi.org/10.1093/emboj/20.13.3554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Krasikova YS, Rechkunova NI, Maltseva EA, Petruseva IO, Lavrik OI. Localization of xeroderma pigmentosum group A protein and replication protein A on damaged DNA in nucleotide excision repair. Nucleic Acids Res. 2010;38:8083–94. https://doi.org/10.1093/nar/gkq649.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Coin F, Oksenych V, Mocquet V, Groh S, Blattner C, Egly JM. Nucleotide excision repair driven by the dissociation of CAK from TFIIH. Mol Cell. 2008;31:9–20. https://doi.org/10.1016/j.molcel.2008.04.024.

    Article  CAS  PubMed  Google Scholar 

  102. Goosen N, Moolenaar GF. Role of ATP hydrolysis by UvrA and UvrB during nucleotide excision repair. Res Microbiol. 2001;152:401–9. https://doi.org/10.1016/S0923-2508(01)01211-6.

    Article  CAS  PubMed  Google Scholar 

  103. Kad NM, Wang H, Kennedy GG, Warshaw DM, Van Houten B. Collaborative dynamic DNA scanning by nucleotide excision repair proteins investigated by single- molecule imaging of quantum-dot-labeled proteins. Mol Cell. 2010;37:702–13. https://doi.org/10.1016/j.molcel.2010.02.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Selby CP, Sancar A. Structure and function of the (A) BC excinuclease of Escherichia coli. Mutat Res. 1990;236:203–11. https://doi.org/10.1016/0921-8777(90)90005-P.

    Article  CAS  PubMed  Google Scholar 

  105. Van Houten B, Croteau DL, DellaVecchia MJ, Wang H, Kisker C. “Close-fitting sleeves”: DNA damage recognition by the UvrABC nuclease system. Mutat Res. 2005;577:92–117. https://doi.org/10.1016/j.mrfmmm.2005.03.013.

    Article  CAS  PubMed  Google Scholar 

  106. Peng W, Shaw BR. Accelerated deamination of cytosine residues in UV-induced cyclobutane pyrimidine dimers leads to CC→TT transitions. Biochemistry. 1996;35:10172–81. https://doi.org/10.1021/bi960001x.

    Article  CAS  PubMed  Google Scholar 

  107. Stary A, Sarasin A. Molecular mechanisms of UV-induced mutations as revealed by the study of DNA polymerase h in human cells. Res Microbiol. 2002;153:441–5. https://doi.org/10.1016/S0923-2508(02)01343-8.

    Article  CAS  PubMed  Google Scholar 

  108. You YH, Lee DH, Yoon JH, Nakajima S, Yasui A, Pfeifer GP. Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells. J Biol Chem. 2001;276:44688–94. https://doi.org/10.1074/jbc.M107696200.

    Article  CAS  PubMed  Google Scholar 

  109. Keeney S, Chang GJ, Linn S. Characterization of a human DNA damage binding protein implicated in xeroderma pigmentosum E. J Biol Chem. 1993;268:21293–300.

    CAS  PubMed  Google Scholar 

  110. Nichols AF, Itoh T, Graham JA, Liu W, Yamaizumi M, Linn S. Human damage-specific DNA-binding protein p48. Characterization of XPE mutations and regulation following UV irradiation. J Biol Chem. 2000;275:21422–8. https://doi.org/10.1074/jbc.M000960200.

    Article  CAS  PubMed  Google Scholar 

  111. Rapić-Otrin V, Navazza V, Nardo T, Botta E, McLenigan M, Bisi DC, Levine AS, Stefanini M. True XP group E patients have a defective UV-damaged DNA binding protein complex and mutations in DDB2 which reveal the functional domains of its p48 product. Hum Mol Genet. 2003;12:1507–22. https://doi.org/10.1093/hmg/ddg174.

    Article  PubMed  Google Scholar 

  112. Dualan R, Brody T, Keeney S, Nichols AF, Admon A, Linn S. Chromosomal localization and cDNA cloning of the genes (DDB1 and DDB2) for the p127 and p48 subunits of a human damage-specific DNA binding protein. Genomics. 1995;29:62–9. https://doi.org/10.1006/geno.1995.1215.

    Article  CAS  PubMed  Google Scholar 

  113. Scrima A, Konícková R, Czyzewski BK, Kawasaki Y, Jeffrey PD, Groisman R, Nakatani Y, Iwai S, Pavletich NP, Thomä NH. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell. 2008;135:1213–23. https://doi.org/10.1016/j.cell.2008.10.045.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Payne A, Chu G. Xeroderma pigmentosum group E binding factor recognizes a broad spectrum of DNA damage. Mutat Res. 1994;310:89–102. https://doi.org/10.1016/0027-5107(94)90012-4.

    Article  CAS  PubMed  Google Scholar 

  115. Reardon JT, Nichols AF, Keeney S, Smith CA, Taylor JS, Linn S, Sancar A. Comparative analysis of binding of human damaged DNA-binding protein (XPE) and Escherichia coli damage recognition protein (UvrA) to the major ultraviolet photoproducts: T[c,s]T, T[t,s]T, T[6-4]T, and T[Dewar]T. J Biol Chem. 1993;268:21301–8.

    CAS  PubMed  Google Scholar 

  116. Fitch ME, Nakajima S, Yasui A, Ford JM. In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product. J Biol Chem. 2003;278:46906–10. https://doi.org/10.1074/jbc.M307254200.

    Article  CAS  PubMed  Google Scholar 

  117. Moser J, Volker M, Kool H, Alekseev S, Vrieling H, Yasui A, Van Zeeland AA, Mullenders LHF. The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair (Amst). 2005;4:571–82. https://doi.org/10.1016/j.dnarep.2005.01.001.

    Article  CAS  Google Scholar 

  118. Nishi R, Alekseev S, Dinant C, Hoogstraten D, Houtsmuller AB, Hoeijmakers JHJ, Vermeulen W, Hanaoka F, Sugasawa K. UV-DDB-dependent regulation of nucleotide excision repair kinetics in living cells. DNA Repair (Amst). 2009;8:767–76. https://doi.org/10.1016/j.dnarep.2009.02.004.

    Article  CAS  Google Scholar 

  119. Wang Q-E, Zhu Q, Wani G, Chen J, Wani AA. UV radiation-induced XPC translocation within chromatin is mediated by damaged-DNA binding protein, DDB2. Carcinogenesis. 2004;25:1033–43. https://doi.org/10.1093/carcin/bgh085.

    Article  CAS  PubMed  Google Scholar 

  120. Hwang BJ, Ford JM, Hanawalt PC, Chu G. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc Natl Acad Sci U S A. 1999;96:424–8. https://doi.org/10.1073/pnas.96.2.424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Tang JY, Hwang BJ, Ford JM, Hanawalt PC, Chu G. Xeroderma pigmentosum p48 gene enhances global genomic repair and suppresses UV-induced mutagenesis. Mol Cell. 2000;5:737–44. https://doi.org/10.1016/S1097-2765(00)80252-X.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Adimoolam S, Ford JM. p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc Natl Acad Sci U S A. 2002;99:12985–90. https://doi.org/10.1073/pnas.202485699.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Itoh T, O’Shea C, Linn S. Impaired regulation of tumor suppressor p53 caused by mutations in the xeroderma pigmentosum DDB2 gene: mutual regulatory interactions between p48(DDB2) and p53. Mol Cell Biol. 2003;23:7540–53. https://doi.org/10.1128/MCB.23.21.7540-7553.2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Bagchi S, Raychaudhuri P. Damaged-DNA binding protein-2 drives apoptosis following DNA damage. Cell Div. 2010;5:3. https://doi.org/10.1186/1747-1028-5-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Itoh T, Iwashita S, Cohen MB, Meyerholz DK, Linn S. Ddb2 is a haploinsufficient tumor suppressor and controls spontaneous germ cell apoptosis. Hum Mol Genet. 2007;16:1578–86. https://doi.org/10.1093/hmg/ddm107.

    Article  CAS  PubMed  Google Scholar 

  126. Stoyanova T, Roy N, Kopanja D, Bagchi S, Raychaudhuri P. DDB2 decides cell fate following DNA damage. Proc Natl Acad Sci U S A. 2009;106:10690–5. https://doi.org/10.1073/pnas.0812254106.

    Article  PubMed  PubMed Central  Google Scholar 

  127. Stubbert LJ, Smith JM, Hamill JD, Arcand TL, McKay BC. The anti-apoptotic role for p53 following exposure to ultraviolet light does not involve DDB2. Mutat Res. 2009;663:69–76. https://doi.org/10.1016/j.mrfmmm.2009.01.010.

    Article  CAS  PubMed  Google Scholar 

  128. Itoh T, Cado D, Kamide R, Linn S. DDB2 gene disruption leads to skin tumors and resistance to apoptosis after exposure to ultraviolet light but not a chemical carcinogen. Proc Natl Acad Sci U S A. 2004;101:2052–7. https://doi.org/10.1073/pnas.0306551101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Angers S, Li T, Yi X, MacCoss MJ, Moon RT, Zheng N. Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature. 2006;443:590–3. https://doi.org/10.1038/nature05175.

    Article  CAS  PubMed  Google Scholar 

  130. Higa LA, Wu M, Ye T, Kobayashi R, Sun H, Zhang H. CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat Cell Biol. 2006;8:1277–83. https://doi.org/10.1038/ncb1490.

    Article  CAS  PubMed  Google Scholar 

  131. Lee J, Zhou P. DCAFs, the missing link of the CUL4-DDB1 ubiquitin ligase. Mol Cell. 2007;26:775–80. https://doi.org/10.1016/j.molcel.2007.06.001.

    Article  CAS  PubMed  Google Scholar 

  132. Cavadini S, Fischer ES, Bunker RD, Potenza A, Lingaraju GM, Goldie KN, Mohamed WI, Faty M, Petzold G, Beckwith REJ, Tichkule RB, Hassiepen U, Abdulrahman W, Pantelic RS, Matsumoto S, Sugasawa K, Stahlberg H, Thomä NH. Cullin-RING ubiquitin E3 ligase regulation by the COP9 signalosome. Nature. 2016;531:598–603. https://doi.org/10.1038/nature17416.

    Article  CAS  PubMed  Google Scholar 

  133. Fischer ES, Scrima A, Böhm K, Matsumoto S, Lingaraju GM, Faty M, Yasuda T, Cavadini S, Wakasugi M, Hanaoka F, Iwai S, Gut H, Sugasawa K, Thomä NH. The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell. 2011;147:1024–39. https://doi.org/10.1016/j.cell.2011.10.035.

    Article  CAS  PubMed  Google Scholar 

  134. Groisman R, Polanowska J, Kuraoka I, Sawada J-I, Saijo M, Drapkin R, Kisselev AF, Tanaka K, Nakatani Y. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell. 2003;113:357–67. https://doi.org/10.1016/S0092-8674(03)00316-7.

    Article  CAS  PubMed  Google Scholar 

  135. Chen X, Zhang Y, Douglas L, Zhou P. UV-damaged DNA-binding proteins are targets of CUL-4A-mediated ubiquitination and degradation. J Biol Chem. 2001;276:48175–82. https://doi.org/10.1074/jbc.M106808200.

    Article  CAS  PubMed  Google Scholar 

  136. Kapetanaki MG, Guerrero-Santoro J, Bisi DC, Hsieh CL, Rapić-Otrin V, Levine AS. The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc Natl Acad Sci U S A. 2006;103:2588–93. https://doi.org/10.1073/pnas.0511160103.

    Article  CAS  PubMed  Google Scholar 

  137. Matsuda N, Azuma K, Saijo M, Iemura S-I, Hioki Y, Natsume T, Chiba T, Tanaka K, Tanaka K. DDB2, the xeroderma pigmentosum group E gene product, is directly ubiquitylated by Cullin 4A-based ubiquitin ligase complex. DNA Repair (Amst). 2005;4:537–45. https://doi.org/10.1016/j.dnarep.2004.12.012.

    Article  CAS  Google Scholar 

  138. Wang H, Zhai L, Xu J, Joo H-Y, Jackson S, Erdjument-Bromage H, Tempst P, Xiong Y, Zhang Y. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol Cell. 2006;22:383–94. https://doi.org/10.1016/j.molcel.2006.03.035.

    Article  CAS  PubMed  Google Scholar 

  139. Matsumoto S, Fischer ES, Yasuda T, Dohmae N, Iwai S, Mori T, Nishi R, Yoshino K-I, Sakai W, Hanaoka F, Thomä NH, Sugasawa K. Functional regulation of the DNA damage-recognition factor DDB2 by ubiquitination and interaction with xeroderma pigmentosum group C protein. Nucleic Acids Res. 2015;43:1700–13. https://doi.org/10.1093/nar/gkv038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Puumalainen M-R, Lessel D, Rüthemann P, Kaczmarek N, Bachmann K, Ramadan K, Naegeli H. Chromatin retention of DNA damage sensors DDB2 and XPC through loss of p97 segregase causes genotoxicity. Nat Commun. 2014;5:3695. https://doi.org/10.1038/ncomms4695.

    Article  PubMed  Google Scholar 

  141. Fitch ME, Cross IV, Turner SJ, Adimoolam S, Lin CX, Williams KG, Ford JM. The DDB2 nucleotide excision repair gene product p48 enhances global genomic repair in p53 deficient human fibroblasts. DNA Repair (Amst). 2003;2:819–26. https://doi.org/10.1016/S1568-7864(03)00066-1.

    Article  CAS  Google Scholar 

  142. Rapić-Otrin V, McLenigan MP, Bisi DC, Gonzalez M, Levine AS. Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res. 2002;30:2588–98. https://doi.org/10.1093/nar/30.11.2588.

    Article  PubMed  Google Scholar 

  143. Pines A, Vrouwe MG, Marteijn JA, Typas D, Luijsterburg MS, Cansoy M, Hensbergen P, Deelder A, de Groot A, Matsumoto S, Sugasawa K, Thoma N, Vermeulen W, Vrieling H, Mullenders L. PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J Cell Biol. 2012;199:235–49. https://doi.org/10.1083/jcb.201112132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Akita M, Tak Y-S, Shimura T, Matsumoto S, Okuda-Shimizu Y, Shimizu Y, Nishi R, Saitoh H, Iwai S, Mori T, Ikura T, Sakai W, Hanaoka F, Sugasawa K. SUMOylation of xeroderma pigmentosum group C protein regulates DNA damage recognition during nucleotide excision repair. Sci Rep. 2015;5:10984. https://doi.org/10.1038/srep10984.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. van Cuijk L, van Belle GJ, Turkyilmaz Y, Poulsen SL, Janssens RC, Theil AF, Sabatella M, Lans H, Mailand N, Houtsmuller AB, Vermeulen W, Marteijn JA. SUMO and ubiquitin-dependent XPC exchange drives nucleotide excision repair. Nat Commun. 2015;6:7499. https://doi.org/10.1038/ncomms8499.

    Article  PubMed  Google Scholar 

  146. Gale JM, Nissen KA, Smerdon MJ. 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. 1987;84:6644–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Gale JM, Smerdon MJ. UV induced (6-4) photoproducts are distributed differently than cyclobutane dimers in nucleosomes. Photochem Photobiol. 1990;51:411–7. https://doi.org/10.1111/j.1751-1097.1990.tb01732.x.

    Article  CAS  PubMed  Google Scholar 

  148. Pehrson JR. Thymine dimer formation as a probe of the path of DNA in and between nucleosomes in intact chromatin. Proc Natl Acad Sci U S A. 1989;86:9149–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Pehrson JR. Probing the conformation of nucleosome linker DNA in situ with pyrimidine dimer formation. J Biol Chem. 1995;270:22440–4. https://doi.org/10.1038/311532a0.

    Article  CAS  PubMed  Google Scholar 

  150. Hara R, Mo J, Sancar A. DNA damage in the nucleosome core is refractory to repair by human excision nuclease. Mol Cell Biol. 2000;20:9173–81. https://doi.org/10.1128/MCB.20.24.9173-9181.2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Yasuda T, Sugasawa K, Shimizu Y, Iwai S, Shiomi T, Hanaoka F. Nucleosomal structure of undamaged DNA regions suppresses the non-specific DNA binding of the XPC complex. DNA Repair (Amst). 2005;4:389–95. https://doi.org/10.1016/j.dnarep.2004.10.008.

    Article  CAS  Google Scholar 

  152. Osakabe A, Tachiwana H, Kagawa W, Horikoshi N, Matsumoto S, Hasegawa M, Matsumoto N, Toga T, Yamamoto J, Hanaoka F, Thomä NH, Sugasawa K, Iwai S, Kurumizaka H. Structural basis of pyrimidine-pyrimidone (6-4) photoproduct recognition by UV-DDB in the nucleosome. Sci Rep. 2015;5:16330. https://doi.org/10.1038/srep16330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Hara R, Sancar A. The SWI/SNF chromatin-remodeling factor stimulates repair by human excision nuclease in the mononucleosome core particle. Mol Cell Biol. 2002;22:6779–87. https://doi.org/10.1128/MCB.22.19.6779-6787.2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Hara R, Sancar A. Effect of damage type on stimulation of human excision nuclease by SWI/SNF chromatin remodeling factor. Mol Cell Biol. 2003;23:4121–5. https://doi.org/10.1128/MCB.23.12.4121-4125.2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Ura K, Araki M, Saeki H, Masutani C, Ito T, Iwai S, Mizukoshi T, Kaneda Y, Hanaoka F. ATP-dependent chromatin remodeling facilitates nucleotide excision repair of UV-induced DNA lesions in synthetic dinucleosomes. EMBO J. 2001;20:2004–14. https://doi.org/10.1093/emboj/20.8.2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Datta A, Bagchi S, Nag A, Shiyanov P, Adami GR, Yoon T, Raychaudhuri P. The p48 subunit of the damaged-DNA binding protein DDB associates with the CBP/p300 family of histone acetyltransferase. Mutat Res. 2001;486:89–97. https://doi.org/10.1016/S0921-8777(01)00082-9.

    Article  CAS  PubMed  Google Scholar 

  157. Martinez E, Palhan VB, Tjernberg A, Lymar ES, Gamper AM, Kundu TK, Chait BT, Roeder RG. Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol Cell Biol. 2001;21:6782–95. https://doi.org/10.1128/MCB.21.20.6782-6795.2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Matsunuma R, Niida H, Ohhata T, Kitagawa K, Sakai S, Uchida C, Shiotani B, Matsumoto M, Nakayama KI, Ogura H, Shiiya N, Kitagawa M. UV damage-induced phosphorylation of HBO1 triggers CRL4DDB2-mediated degradation to regulate cell proliferation. Mol Cell Biol. 2015;36:394–406. https://doi.org/10.1128/MCB.00809-15.

    Article  CAS  PubMed  Google Scholar 

  159. Adam S, Dabin J, Chevallier O, Leroy O, Baldeyron C, Corpet A, Lomonte P, Renaud O, Almouzni G, Polo SE. Real-time tracking of parental histones reveals their contribution to chromatin integrity following DNA damage. Mol Cell. 2016;64:65–78. https://doi.org/10.1016/j.molcel.2016.08.019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Luijsterburg MS, Lindh M, Acs K, Vrouwe MG, Pines A, van Attikum H, Mullenders LH, Dantuma NP. DDB2 promotes chromatin decondensation at UV-induced DNA damage. J Cell Biol. 2012;197:267–81. https://doi.org/10.1083/jcb.201106074.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Kakumu E, Nakanishi S, Shiratori HM, Kato A, Kobayashi W, Machida S, Yasuda T, Adachi N, Saito N, Ikura T, Kurumizaka H, Kimura H, Yokoi M, Sakai W, Sugasawa K. Xeroderma pigmentosum group C protein interacts with histones: regulation by acetylated states of histone H3. Genes Cells. 2017;22:310–27. https://doi.org/10.1111/gtc.12479.

    Article  CAS  PubMed  Google Scholar 

  162. Luijsterburg MS, Dinant C, Lans H, Stap J, Wiernasz E, Lagerwerf S, Warmerdam DO, Lindh M, Brink MC, Dobrucki JW, Aten JA, Fousteri MI, Jansen G, Dantuma NP, Vermeulen W, Mullenders LHF, Houtsmuller AB, Verschure PJ, van Driel R. Heterochromatin protein 1 is recruited to various types of DNA damage. J Cell Biol. 2009;185:577–86. https://doi.org/10.1083/jcb.200810035.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Guo R, Chen J, Mitchell DL, Johnson DG. GCN5 and E2F1 stimulate nucleotide excision repair by promoting H3K9 acetylation at sites of damage. Nucleic Acids Res. 2011;39:1390–7. https://doi.org/10.1093/nar/gkq983.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The author’s work was supported by Grants-in-Aid from the Japan Society for the Promotion of Science (JSPS KAKENHI Grant Numbers JP23116008, JP16H06307, and JP16H01311) to K.S.

Author information

Authors and Affiliations

  1. Biosignal Research Center, Kobe University, Kobe, Hyogo, Japan

    Kaoru Sugasawa

Authors
  1. Kaoru Sugasawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kaoru Sugasawa .

Editor information

Editors and Affiliations

  1. Department of Dermatology, Graduate School of Medicine, Kobe University, Kobe, Japan

    Chikako Nishigori

  2. Biosignal Research Center, Kobe University, Kobe, Japan

    Kaoru Sugasawa

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sugasawa, K. (2019). Molecular Mechanism of DNA Damage Recognition for Global Genomic Nucleotide Excision Repair: A Defense System Against UV-Induced Skin Cancer. In: Nishigori, C., Sugasawa, K. (eds) DNA Repair Disorders. Springer, Singapore. https://doi.org/10.1007/978-981-10-6722-8_1

Download citation

  • DOI: https://doi.org/10.1007/978-981-10-6722-8_1

  • Published:

  • Publisher Name: Springer, Singapore

  • Print ISBN: 978-981-10-6721-1

  • Online ISBN: 978-981-10-6722-8

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation