Advertisement

Journal of Molecular Histology

, Volume 37, Issue 5–7, pp 225–238 | Cite as

Nucleotide excision repair and cancer

  • Diana Leibeling
  • Petra Laspe
  • Steffen Emmert
Original Paper

Abstract

Nucleotide excision repair (NER) is the most versatile and best studied DNA repair system in humans. NER can repair a variety of bulky DNA damages including UV-light induced DNA photoproducts. NER consists of a multistep process in which the DNA lesion is recognized and demarcated by DNA unwinding. Then, a ~28 bp DNA damage containing oligonucleotide is excised followed by gap filling using the undamaged DNA strand as a template. The consequences of defective NER are demonstrated by three rare autosomal-rezessive NER-defective syndromes: xeroderma pigmentosum (XP), Cockayne syndrome (CS), and trichothiodystrophy (TTD). XP patients show severe sun sensitivity, freckling in sun exposed skin, and develop skin cancers already during childhood. CS patients exhibit sun sensitivity, severe neurologic abnormalities, and cachectic dwarfism. Clinical symptoms of TTD patients include sun sensitivity, freckling in sun exposed skin areas, and brittle sulfur-deficient hair. In contrast to XP patients, CS and TTD patients are not skin cancer prone. Studying these syndromes can increase the knowledge of skin cancer development including cutaneous melanoma as well as basal and squamous cell carcinoma in general that may lead to new preventional and therapeutic anticancer strategies in the normal population.

Keywords

DNA repair Nucleotide excision repair Xeroderma pigmentosum Cockayne syndrome Trichothiodystrophy COFS syndrome Skin cancer Topical therapy with DNA repair enzymes 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgments

D.L. and S.E. are supported by the Deutsche Forschungsgemeinschaft DFG (GRK 1034).

References

  1. Blankenburg S, Konig IR, Moessner R, Laspe P, Thoms KM, Krueger U, Khan SG, Westphal G, Berking C, Volkenandt M, Reich K, Neumann C, Ziegler A, Kraemer KH, Emmert S (2005a) Assessment of 3 xeroderma pigmentosum group C gene polymorphisms and risk of cutaneous melanoma: a case-control study. Carcinogenesis 26:1085–1090CrossRefGoogle Scholar
  2. Blankenburg S, Konig IR, Moessner R, Laspe P, Thoms KM, Krueger U, Khan SG, Westphal G, Volkenandt M, Neumann C, Ziegler A, Kraemer KH, Reich K, Emmert S (2005b) No association between three xeroderma pigmentosum group C and one group G gene polymorphisms and risk of cutaneous melanoma. Eur J Hum Genet 13:253–255CrossRefGoogle Scholar
  3. Bootsma D, Hoeijmakers JH (1993) DNA repair. Engagement with transcription. Nature 363:114–115PubMedCrossRefGoogle Scholar
  4. Bootsma D, Kraemer KH, Cleaver JE, Hoeijmakers JH (2002) Nucleotide excision repair syndromes: xeroderma pigmentosum, Cockayne syndrome, and trichothiodystrophy. In: Vogelstein B, Kinzler KW (eds) The genetic basis of human cancer. McGraw-Hill, New York, pp 211–237Google Scholar
  5. Broughton BC, Berneburg M, Fawcett H, Taylor EM, Arlett CF, Nardo T, Stefanini M, Menefee E, Price VH, Queille S, Sarasin A, Bohnert E, Krutmann J, Davidson R, Kraemer KH, Lehmann AR (2001) Two individuals with features of both xeroderma pigmentosum and trichothiodystrophy highlight the complexity of the clinical outcomes of mutations in the XPD gene. Hum Mol Genet 10:2539–2547PubMedCrossRefGoogle Scholar
  6. Broughton BC, Cordonnier A, Kleijer WJ, Jaspers NG, Fawcett H, Raams A, Garritsen VH, Stary A, Avril MF, Boudsocq F, Masutani C, Hanaoka F, Fuchs RP, Sarasin A, Lehmann AR (2002) Molecular analysis of mutations in DNA polymerase eta in xeroderma pigmentosum-variant patients. Proc Natl Acad Sci U S A 99:815–820PubMedCrossRefGoogle Scholar
  7. Broughton BC, Steingrimsdottir H, Lehmann AR (1996) Five polymorphisms in the coding sequence of the xeroderma pigmentosum group D gene. Mutat Res 362:209–211PubMedGoogle Scholar
  8. Broughton BC, Steingrimsdottir H, Weber CA, Lehmann AR (1994) Mutations in the xeroderma pigmentosum group D DNA repair/transcription gene in patients with trichothiodystrophy. Nat Genet 7:189–194PubMedCrossRefGoogle Scholar
  9. Buschta-Hedayat N, Buterin T, Hess MT, Missura M, Naegeli H (1999) Recognition of nonhybridizing base pairs during nucleotide excision repair of DNA. Proc Natl Acad Sci U S A 96:6090–6095PubMedCrossRefGoogle Scholar
  10. Cheng L, Eicher SA, Guo Z, Hong WK, Spitz MR, Wei Q (1998) Reduced DNA repair capacity in head and neck cancer patients. Cancer Epidemiol Biomarkers Prev 7:465–468PubMedGoogle Scholar
  11. Cleaver JE (1972) Xeroderma pigmentosum: variants with normal DNA repair and normal sensitivity to ultraviolet light. J Invest Dermatol 58:124–128PubMedCrossRefGoogle Scholar
  12. Cooper PK, Nouspikel T, Clarkson SG, Leadon SA (1997) Defective transcription-coupled repair of oxidative base damage in Cockayne syndrome patients from XP group G. Science 275:990–993PubMedCrossRefGoogle Scholar
  13. de Boer J, Hoeijmakers JH (2000) Nucleotide excision repair and human syndromes. Carcinogenesis 21:453–460PubMedCrossRefGoogle Scholar
  14. Dianov GL, Kuzminov AV, Mazin AV, Salganik RI (1991) Molecular mechanisms of deletion formation in Escherichia coli plasmids. I. Deletion formation mediated by long direct repeats. Mol Gen Genet 228:153–159PubMedCrossRefGoogle Scholar
  15. Dodson ML, Michaels ML, Lloyd RS (1994) Unified catalytic mechanism for DNA glycosylases. J Biol Chem 269:32709–32712PubMedGoogle Scholar
  16. Dybdahl M, Vogel U, Frentz G, Wallin H, Nexo BA (1999) Polymorphisms in the DNA repair gene XPD: correlations with risk and age at onset of basal cell carcinoma. Cancer Epidemiol Biomarkers Prev 8:77–81PubMedGoogle Scholar
  17. Emmert S, Kobayashi N, Khan SG, Kraemer KH (2000) The xeroderma pigmentosum group C gene leads to selective repair of cyclobutane pyrimidine dimers rather than 6–4 photoproducts. Natl Acad Sci U S A 97:2151–2156CrossRefGoogle Scholar
  18. Emmert S, Leibeling D, Runger TM (2006) Syndromes with genetic instability: Model diseases for (skin) cancerogenesis. J Dtsch Dermatol Ges (in press)Google Scholar
  19. Emmert S, Schneider TD, Khan SG, Kraemer KH (2001) The human XPG gene: gene architecture, alternative splicing and single nucleotide polymorphisms. Nucleic Acids Res 29:1443–1452PubMedCrossRefGoogle Scholar
  20. Emmert S, Slor H, Busch DB, Batko S, Albert RB, Coleman D, Khan SG, Abu-Libdeh B, DiGiovanna JJ, Cunningham BB, Lee MM, Crollick J, Inui H, Ueda T, Hedayati M, Grossman L, Shahlavi T, Cleaver JE, Kraemer KH (2002) Relationship of neurologic degeneration to genotype in three Xeroderma Pigmentosum Group G patients. J Invest Dermatol 118:972–982PubMedCrossRefGoogle Scholar
  21. Gasparro FP, Mitchnick M, Nash JF (1998) A review of sunscreen safety and efficacy. Photochem Photobiol 68:243–256PubMedCrossRefGoogle Scholar
  22. Gerard M, Fischer L, Moncollin V, Chipoulet JM, Chambon P, Egly JM (1991) Purification and interaction properties of the human RNA polymerase B(II) general transcription factor BTF2. J Biol Chem 266:20940–20945PubMedGoogle Scholar
  23. Giglia-Mari G, Coin F, Ranish JA, Hoogstraten D, Theil A, Wijgers N, Jaspers NG, Raams A, Argentini M, van der Spek PJ, Botta E, Stefanini M, Egly JM, Aebersold R, Hoeijmakers JH, Vermeulen W (2004) A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat Genet 36:714–719PubMedCrossRefGoogle Scholar
  24. Graham JM Jr, Anyane-Yeboa K, Raams A, Appeldoorn E, Kleijer WJ, Garritsen VH, Busch D, Edersheim TG, Jaspers NG (2001) Cerebro-oculo-facio-skeletal syndrome with a nucleotide excision-repair defect and a mutated XPD gene, with prenatal diagnosis in a triplet pregnancy. Am J Hum Genet 69:291–300PubMedCrossRefGoogle Scholar
  25. Graham JM Jr, Hennekam R, Dobyns WB, Roeder E, Busch D (2004) MICRO syndrome: an entity distinct from COFS syndrome. Am J Med Genet A 128:235–245PubMedCrossRefGoogle Scholar
  26. Gratchev A, Strein P, Utikal J, Sergij G (2003) Molecular genetics of Xeroderma pigmentosum variant. Exp Dermatol 12:529–536PubMedCrossRefGoogle Scholar
  27. Hadshiew IM, Eller MS, Moll I, Gilchrest BA (2002) Photoprotective mechanisms of human skin. Modulation by oligonucleotides. Hautarzt 53:167–173PubMedCrossRefGoogle Scholar
  28. Harris AL (1985) DNA repair and resistance to chemotherapy. Cancer Surv 4:601–624PubMedGoogle Scholar
  29. Hays JB, Hoffman P (1999) Measurement of activities of cyclobutane-pyrimidine-dimer and (6–4)- photoproduct photolyases. Methods Mol Biol 113:133–146PubMedGoogle Scholar
  30. Hitomi K, Nakamura H, Kim ST, Mizukoshi T, Ishikawa T, Iwai S, Todo T (2001) Role of two histidines in the (6–4) photolyase reaction. J Biol Chem 276:10103–10109PubMedCrossRefGoogle Scholar
  31. Hoeijmakers JH (2001) Genome maintenance mechanisms for preventing cancer. Nature 411:366–374PubMedCrossRefGoogle Scholar
  32. Holstege FC, van der Vliet PC, Timmers HT (1996) Opening of an RNA polymerase II promoter occurs in two distinct steps and requires the basal transcription factors IIE and IIH. EMBO J 15:1666–1677PubMedGoogle Scholar
  33. Hori N, Doi T, Karaki Y, Kikuchi M, Ikehara M, Ohtsuka E (1992) Participation of glutamic acid 23 of T4 endonuclease V in the beta- elimination reaction of an abasic site in a synthetic duplex DNA. Nucleic Acids Res 20:4761–4764PubMedCrossRefGoogle Scholar
  34. Itin PH, Sarasin A, Pittelkow MR (2001) Trichothiodystrophy: update on the sulfur-deficient brittle hair syndromes. J Am Acad Dermatol 44:891–920PubMedCrossRefGoogle Scholar
  35. Johnson RE, Kondratick CM, Prakash S, Prakash L (1999) hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285:263–265PubMedCrossRefGoogle Scholar
  36. Keeney S, Chang GJ, Linn S (1993) Characterization of a human DNA damage binding protein implicated in xeroderma pigmentosum E. J Biol Chem 268:21293–21300PubMedGoogle Scholar
  37. Khan SG, Levy HL, Legerski R, Quackenbush E, Reardon JT, Emmert S, Sancar A, Li L, Schneider TD, Cleaver JE, Kraemer KH (1998) Xeroderma pigmentosum group C splice mutation associated with autism and hypoglycinemia. J Invest Dermatol 111:791–796PubMedCrossRefGoogle Scholar
  38. Khan SG, Muniz-Medina V, Shahlavi T, Baker CC, Inui H, Ueda T, Emmert S, Schneider TD, Kraemer KH (2002) The human XPC DNA repair gene: arrangement, splice site information content and influence of a single nucleotide polymorphism in a splice acceptor site on alternative splicing and function. Nucleic Acids Res 30:3624–3631PubMedCrossRefGoogle Scholar
  39. Khan SG, Oh KS, Shahlavi T, Ueda T, Busch DB, Inui H, Emmert S, Imoto K, Muniz-Medina V, Baker CC, DiGiovanna JJ, Schmidt D, Khadavi A, Metin A, Gozukara E, Slor H, Sarasin A, Kraemer KH (2006) Reduced XPC DNA repair gene mRNA levels in clinically normal parents of xeroderma pigmentosum patients. Carcinogenesis 27:84–94PubMedCrossRefGoogle Scholar
  40. Kibitel JT, Yee V, Yarosh DB (1991) Enhancement of ultraviolet-DNA repair in denV gene transfectants and T4 endonuclease V-liposome recipients. Photochem Photobiol 54:753–760PubMedCrossRefGoogle Scholar
  41. King JS, Valcarcel ER, Rufer JT, Phillips JW, Morgan WF (1993) Noncomplementary DNA double-strand-break rejoining in bacterial and human cells. Nucleic Acids Res 21:1055–1059PubMedCrossRefGoogle Scholar
  42. Klungland A, Hoss M, Gunz D, Constantinou A, Clarkson SG, Doetsch PW, Bolton PH, Wood RD, Lindahl T (1999) Base excision repair of oxidative DNA damage activated by XPG protein. Mol Cell 3:33–42PubMedCrossRefGoogle Scholar
  43. Koberle B, Masters JR, Hartley JA, Wood RD (1999) Defective repair of cisplatin-induced DNA damage caused by reduced XPA protein in testicular germ cell tumours. Curr Biol 9:273–276PubMedCrossRefGoogle Scholar
  44. Kraemer KH, Lee MM, Scotto J (1987) Xeroderma pigmentosum. Cutaneous, ocular, and neurologic abnormalities in 830 published cases. Arch Dermatol 123:241–250PubMedCrossRefGoogle Scholar
  45. Kraemer KH, Levy DD, Parris CN, Gozukara EM, Moriwaki S, Adelberg S, Seidman MM (1994) Xeroderma pigmentosum and related disorders examining: the linkage between defective DNA repair and cancer. J Invest Dermatol 103:96S–101SPubMedCrossRefGoogle Scholar
  46. Kraemer KH, Slor H (1985) Xeroderma pigmentosum. Clin Dermatol 3:33–69PubMedCrossRefGoogle Scholar
  47. Kripke ML, Cox PA, Bucana C, Vink AA, Alas L, Yarosh DB (1996) Role of DNA damage in local suppression of contact hypersensitivity in mice by UV radiation.Exp Dermatol 5:173–180PubMedCrossRefGoogle Scholar
  48. Kulaksiz G, Reardon JT, Sancar A (2005) Xeroderma pigmentosum complementation group E protein (XPE/DDB2): purification of various complexes of XPE and analyses of their damaged DNA binding and putative DNA repair properties. Mol Cell Biol 25:9784–9792PubMedCrossRefGoogle Scholar
  49. Kusewitt DF, Budge CL, Anderson MM, Ryan SL, Ley RD (1993) Frequency of ultraviolet radiation-induced mutation at the hprt locus in repair-proficient murine fibroblasts transfected with the denV gene of bacteriophage T4. Photochem Photobiol 58:450–454PubMedCrossRefGoogle Scholar
  50. Kusewitt DF, Budge CL, Ley RD (1994) Enhanced pyrimidine dimer repair in cultured murine epithelial cells transfected with the denV gene of bacteriophage T4. J Invest Dermatol 102:485–489PubMedCrossRefGoogle Scholar
  51. Kusewitt DF, Ley RD, Henderson EE (1991) Enhanced pyrimidine dimer removal in repair-proficient murine fibroblasts transformed with the denV gene of bacteriophage T4. Mutat Res 255:1–9PubMedGoogle Scholar
  52. Lalle P, Nouspikel T, Constantinou A, Thorel F, Clarkson SG (2002) The founding members of xeroderma pigmentosum group G produce XPG protein with severely impaired endonuclease activity. J Invest Dermatol 118:344–351PubMedCrossRefGoogle Scholar
  53. Le Page F, Kwoh EE, Avrutskaya A, Gentil A, Leadon SA, Sarasin A, Cooper PK (2000) Transcription-coupled repair of 8-oxoguanine: requirement for XPG, TFIIH, and CSB and implications for Cockayne syndrome. Cell 101:159–171PubMedCrossRefGoogle Scholar
  54. Lehmann AR (1982) Three complementation groups in Cockayne syndrome. Mutat Res 106:347–356PubMedGoogle Scholar
  55. Lehmann AR (1987) Cockayne‘s syndrome and trichothiodystrophy: defective repair without cancer. Cancer Rev 7:82–103Google Scholar
  56. Lehmann AR (2001) The xeroderma pigmentosum group D (XPD) gene: one gene, two functions, three diseases. Genes Dev 15:15–23PubMedCrossRefGoogle Scholar
  57. Licht CL, Stevnsner T, Bohr VA (2003) Cockayne syndrome group B cellular and biochemical functions. Am J Hum Genet 73:1217–1239PubMedCrossRefGoogle Scholar
  58. Lindahl T, Wood RD (1999) Quality control by DNA repair. Science 286:1897–1905PubMedCrossRefGoogle Scholar
  59. Magnaldo T, Sarasin A (2004) Xeroderma pigmentosum: from symptoms and genetics to gene-based skin therapy. Cells Tissues Organs 177:189–198PubMedCrossRefGoogle Scholar
  60. Mallery DL, Tanganelli B, Colella S, Steingrimsdottir H, van Gool AJ, Troelstra C, Stefanini M, Lehmann AR (1998) Molecular analysis of mutations in the CSB (ERCC6) gene in patients with Cockayne syndrome. Am J Hum Genet 62:77–85PubMedCrossRefGoogle Scholar
  61. Marti TM, Kunz C, Fleck O (2002) DNA mismatch repair and mutation avoidance pathways. J Cell Physiol 191:28–41PubMedCrossRefGoogle Scholar
  62. Masutani C, Araki M, Yamada A, Kusumoto R, Nogimori T, Maekawa T, Iwai S, Hanaoka F (1999a) Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J 18:3491–3501CrossRefGoogle Scholar
  63. Masutani C, Kusumoto R, Yamada A, Dohmae N, Yokoi M, Yuasa M, Araki M, Iwai S, Takio K, Hanaoka F (1999b) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 399:700–704CrossRefGoogle Scholar
  64. Meira LB, Graham JM, Jr., Greenberg CR, Busch DB, Doughty AT, Ziffer DW, Coleman DM, Savre-Train I, Friedberg EC (2000) Manitoba aboriginal kindred with original cerebro-oculo- facio-skeletal syndrome has a mutation in the Cockayne syndrome group B (CSB) gene. Am J Hum Genet 66:1221–1228PubMedCrossRefGoogle Scholar
  65. Mimaki T, Itoh N, Abe J, Tagawa T, Sato K, Yabuuchi H, Takebe H (1986) Neurological manifestations in xeroderma pigmentosum. Ann Neurol 20:70–75PubMedCrossRefGoogle Scholar
  66. Mitchell DL, Nairn RS (1989) The biology of the (6–4) photoproduct. Photochem Photobiol 49:805–819PubMedCrossRefGoogle Scholar
  67. Miyauchi H, Horio T, Akaeda T, Asada Y, Chang HR, Ishizaki K, Ikenaga M (1994) Cockayne syndrome in two adult siblings. J Am Acad Dermatol 30:329–335PubMedCrossRefGoogle Scholar
  68. Morikawa K, Matsumoto O, Tsujimoto M, Katayanagi K, Ariyoshi M, Doi T, Ikehara M, Inaoka T, Ohtsuka E (1992) X-ray structure of T4 endonuclease V: an excision repair enzyme specific for a pyrimidine dimer. Science 256:523–526PubMedCrossRefGoogle Scholar
  69. Moriwaki S, Stefanini M, Lehmann AR, Hoeijmakers JH, Robbins JH, Rapin I, Botta E, Tanganelli B, Vermeulen W, Broughton BC, Kraemer KH (1996) DNA repair and ultraviolet mutagenesis in cells from a new patient with xeroderma pigmentosum group G and cockayne syndrome resemble xeroderma pigmentosum cells. J Invest Dermatol 107:647–653PubMedCrossRefGoogle Scholar
  70. Mu D, Sancar A (1997) Model for XPC-independent transcription-coupled repair of pyrimidine dimers in humans. J Biol Chem 272:7570–7573PubMedCrossRefGoogle Scholar
  71. Mukhtar H, Elmets CA (1996) Photocarcinogenesis: mechanisms, models and human health implications. Photochem Photobiol 63:356–357PubMedCrossRefGoogle Scholar
  72. Nance MA, Berry SA (1992) Cockayne syndrome: review of 140 cases. Am J Med Genet 42:68–84PubMedCrossRefGoogle Scholar
  73. Nouspikel T, Clarkson SG (1994) Mutations that disable the DNA repair gene XPG in a xeroderma pigmentosum group G patient. Hum Mol Genet 3:963–967PubMedCrossRefGoogle Scholar
  74. Nouspikel T, Lalle P, Leadon SA, Cooper PK, Clarkson SG (1997) A common mutational pattern in Cockayne syndrome patients from xeroderma pigmentosum group G: implications for a second XPG function. Proc Natl Acad Sci U S A 94:3116–3121PubMedCrossRefGoogle Scholar
  75. Nuzzo F, Stefanini M (1989) The association of xeroderma pigmentosum with trichothiodystrophy: a clue to a better understanding of XP-D? In: Castellani A (ed) DNA damage and repair. Plenum Press, New York, London, pp 61–72Google Scholar
  76. Parris CN, Kraemer KH (1993) Ultraviolet-induced mutations in Cockayne syndrome cells are primarily caused by cyclobutane dimer photoproducts while repair of other photoproducts is normal. Proc Natl Acad Sci U S A 90:7260–7264PubMedCrossRefGoogle Scholar
  77. Petit C, Sancar A (1999) Nucleotide excision repair: from E. coli to man. Biochimie 81:15–25PubMedCrossRefGoogle Scholar
  78. Price VH, Odom RB, Ward WH, Jones FT (1980) Trichothiodystrophy: sulfur-deficient brittle hair as a marker for a neuroectodermal symptom complex. Arch Dermatol 116:1375–1384PubMedCrossRefGoogle Scholar
  79. Qiao Y, Spitz MR, Shen H, Guo Z, Shete S, Hedayati M, Grossman L, Mohrenweiser H, Wei Q (2002) Modulation of repair of ultraviolet damage in the host-cell reactivation assay by polymorphic XPC and XPD/ERCC2 genotypes. Carcinogenesis 23:295–299PubMedCrossRefGoogle Scholar
  80. Radany EH, Naumovski L, Love JD, Gutekunst KA, Hall DH, Friedberg EC (1984) Physical mapping and complete nucleotide sequence of the denV gene of bacteriophage T4. J Virol 52:846–856PubMedGoogle Scholar
  81. Rapin I, Lindenbaum Y, Dickson DW, Kraemer KH, Robbins JH (2000) Cockayne syndrome and xeroderma pigmentosum. Neurology 55:1442–1449PubMedGoogle Scholar
  82. Reardon JT, Bessho T, Kung HC, Bolton PH, Sancar A (1997) In vitro repair of oxidative DNA damage by human nucleotide excision repair system: possible explanation for neurodegeneration in xeroderma pigmentosum patients. Proc Natl Acad Sci U S A 94:9463–9468PubMedCrossRefGoogle Scholar
  83. Richards FM, Goudie DR, Cooper WN, Jene Q, Barroso I, Wicking C, Wainwright BJ, Ferguson-Smith MA (1997) Mapping the multiple self-healing squamous epithelioma (MSSE) gene and investigation of xeroderma pigmentosum group A (XPA) and PATCHED (PTCH) as candidate genes. Hum Genet 101:317–322PubMedCrossRefGoogle Scholar
  84. Robbins JH (1988) Xeroderma pigmentosum. Defective DNA repair causes skin cancer and neurodegeneration. JAMA 260:384–388PubMedCrossRefGoogle Scholar
  85. Robbins JH, Brumback RA, Mendiones M, Barrett SF, Carl JR, Cho S, Denckla MB, Ganges MB, Gerber LH, Guthrie RA (1991) Neurological disease in xeroderma pigmentosum. Documentation of a late onset type of the juvenile onset form. Brain 114(Pt 3):1335–1361Google Scholar
  86. Robbins JH, Kraemer KH, Lutzner MA, Festoff BW, Coon HG (1974) Xeroderma pigmentosum. An inherited diseases with sun sensitivity, multiple cutaneous neoplasms, and abnormal DNA repair. Ann Intern Med 80:221–248PubMedGoogle Scholar
  87. Runger TM, Emmert S, Schadendorf D, Diem C, Epe B, Hellfritsch D (2000) Alterations of DNA repair in melanoma cell lines resistant to cisplatin, fotemustine, or etoposide. J Invest Dermatol 114:34–39PubMedCrossRefGoogle Scholar
  88. Smith JR, Pereira-Smith OM (1996) Replicative senescence: implications for in vivo aging and tumor suppression. Science 273:63–67PubMedCrossRefGoogle Scholar
  89. Spivak G, Hanawalt PC (1992) Translesion DNA synthesis in the dihydrofolate reductase domain of UV- irradiated CHO cells. Biochemistry 31:6794–6800PubMedCrossRefGoogle Scholar
  90. Stefanini M, Fawcett H, Botta E, Nardo T, Lehmann AR (1996) Genetic analysis of twenty-two patients with Cockayne syndrome. Hum Genet 97:418–423PubMedCrossRefGoogle Scholar
  91. Stefanini M, Lagomarsini P, Arlett CF, Marinoni S, Borrone C, Crovato F, Trevisan G, Cordone G, Nuzzo F (1986) Xeroderma pigmentosum (complementation group D) mutation is present in patients affected by trichothiodystrophy with photosensitivity. Hum Genet 74:107–112PubMedCrossRefGoogle Scholar
  92. Stefanini M, Vermeulen W, Weeda G, Giliani S, Nardo T, Mezzina M, Sarasin A, Harper JI, Arlett CF, Hoeijmakers JH (1993) A new nucleotide-excision-repair gene associated with the disorder trichothiodystrophy. Am J Hum Genet 53:817–821PubMedGoogle Scholar
  93. Stege H, Roza L, Vink AA, Grewe M, Ruzicka T, Grether-Beck S, Krutmann J (2000) Enzyme plus light therapy to repair DNA damage in ultraviolet-B- irradiated human skin. Proc Natl Acad Sci U S A 97:1790–1795PubMedCrossRefGoogle Scholar
  94. Sutherland BM, Hacham H, Bennett P, Sutherland JC, Moran M, Gange RW (2002) Repair of cyclobutyl pyrimidine dimers in human skin: variability among normal humans in nucleotide excision and in photorepair. Photodermatol Photoimmunol Photomed 18:109–116PubMedCrossRefGoogle Scholar
  95. Sutherland BM, Hacham H, Gange RW, Maytum D, Sutherland JC (1990) DNA damage and repair in human skin: pathways and questions. Basic Life Sci 53:149–160PubMedGoogle Scholar
  96. Swift M, Chase C (1979) Cancer in families with xeroderma pigmentosum. J Natl Cancer Inst 62:1415–1421PubMedGoogle Scholar
  97. Taieb A, Van Neste D, Lacombe D, Mezzina M, Sarasin A (1994) Bébé collodion d’ évolution favorable définissant un nouveau groupe génétique de trichothiodystrophie. Ann Dermatol Venereol S80Google Scholar
  98. Takebayashi Y, Pourquier P, Zimonjic DB, Nakayama K, Emmert S, Ueda T, Urasaki Y, Kanzaki A, Akiyama SI, Popescu N, Kraemer KH, Pommier Y (2001) Antiproliferative activity of ecteinascidin 743 is dependent upon transcription-coupled nucleotide-excision repair. Nat Med 7:961–966PubMedCrossRefGoogle Scholar
  99. Takebe H, Nishigori C, Satoh Y (1987) Genetics and skin cancer of xeroderma pigmentosum in Japan. Jpn J Cancer Res 78:1135–1143PubMedGoogle Scholar
  100. Tanaka K, Sekiguchi M, Okada Y (1975) Restoration of ultraviolet-induced unscheduled DNA synthesis of xeroderma pigmentosum cells by the concomitant treatment with bacteriophage T4 endonuclease V and HVJ (Sendai virus). Proc Natl Acad Sci U S A 72:4071–4075PubMedCrossRefGoogle Scholar
  101. Taylor EM, Broughton BC, Botta E, Stefanini M, Sarasin A, Jaspers NG, Fawcett H, Harcourt SA, Arlett CF, Lehmann AR (1997) Xeroderma pigmentosum and trichothiodystrophy are associated with different mutations in the XPD (ERCC2) repair/transcription gene. Proc Natl Acad Sci U S A 94:8658–8663PubMedCrossRefGoogle Scholar
  102. Tomescu D, Kavanagh G, Ha T, Campbell H, Melton DW (2001) Nucleotide excision repair gene XPD polymorphisms and genetic predisposition to melanoma. Carcinogenesis 22:403–408PubMedCrossRefGoogle Scholar
  103. Tsambaos D, Nikiforidis G, Balas C, Marinoni S (1994) Trichothiodystrophic hair reveals an abnormal pattern of viscoelastic parameters. Skin Pharmacol 7:257–261PubMedCrossRefGoogle Scholar
  104. Van Neste DJ, Gillespie JM, Marshall RC, Taieb A, De Brouwer B (1993) Morphological and biochemical characteristics of trichothiodystrophy- variant hair are maintained after grafting of scalp specimens on to nude mice. Br J Dermatol 128:384–387PubMedCrossRefGoogle Scholar
  105. van Steeg H, Kraemer KH (1999) Xeroderma pigmentosum and the role of UV-induced DNA damage in skin cancer. Mol Med Today 5:86–94PubMedCrossRefGoogle Scholar
  106. Venema J, van Hoffen A, Karcagi V, Natarajan AT, van Zeeland AA, Mullenders LH (1991) Xeroderma pigmentosum complementation group C cells remove pyrimidine dimers selectively from the transcribed strand of active genes. Mol Cell Biol 11:4128–4134PubMedGoogle Scholar
  107. Vermeulen W, van Vuuren AJ, Chipoulet M, Schaeffer L, Appeldoorn E, Weeda G, Jaspers NG, Priestley A, Arlett CF, Lehmann AR (1994) Three unusual repair deficiencies associated with transcription factor BTF2(TFIIH): evidence for the existence of a transcription syndrome. Cold Spring Harb Symp Quant Biol 59:317–329PubMedGoogle Scholar
  108. Vilpo JA, Vilpo LM, Szymkowski DE, O’Donovan A, Wood RD (1995) An XPG DNA repair defect causing mutagen hypersensitivity in mouse leukemia L1210 cells. Mol Cell Biol 15:290–297PubMedGoogle Scholar
  109. von Hebra F, Kaposi M (1874) On diseases of the skin, including the exanthema. In Tay W, 3 edn. p. 252. New Sydenham Society, LondonGoogle Scholar
  110. Weeda G, Eveno E, Donker I, Vermeulen W, Chevallier- Lagente O, Taieb A, Stary A, Hoeijmakers JH, Mezzina M, Sarasin A (1997) A mutation in the XPB/ERCC3 DNA repair transcription gene, associated with trichothiodystrophy. Am J Hum Genet 60:320–329PubMedGoogle Scholar
  111. Wei Q, Cheng L, Hong WK, Spitz MR (1996) Reduced DNA repair capacity in lung cancer patients. Cancer Res 56:4103–4107PubMedGoogle Scholar
  112. Wei Q, Lee JE, Gershenwald JE, Ross MI, Mansfield PF, Strom SS, Wang LE, Guo Z, Qiao Y, Amos CI, Spitz MR, Duvic M (2003) Repair of UV light-induced DNA damage and risk of cutaneous malignant melanoma. J Natl Cancer Inst 95:308–315PubMedCrossRefGoogle Scholar
  113. Wei Q, Matanoski GM, Farmer ER, Hedayati MA, Grossman L (1993) DNA repair and aging in basal cell carcinoma: a molecular epidemiology study. Proc Natl Acad Sci U S A 90:1614–1618PubMedCrossRefGoogle Scholar
  114. Wei Q, Matanoski GM, Farmer ER, Hedayati MA, Grossman L (1995) DNA repair capacity for ultraviolet light-induced damage is reduced in peripheral lymphocytes from patients with basal cell carcinoma. J Invest Dermatol 104:933–936PubMedCrossRefGoogle Scholar
  115. Wood RD (1999) DNA damage recognition during nucleotide excision repair in mammalian cells. Biochimie 81:39–44PubMedCrossRefGoogle Scholar
  116. Wood RD, Mitchell M, Sgouros J, Lindahl T (2001) Human DNA repair genes. Science 291:1284–1289PubMedCrossRefGoogle Scholar
  117. Wu X, Zhao H, Wei Q, Amos CI, Zhang K, Guo Z, Qiao Y, Hong WK, Spitz MR (2003) XPA polymorphism associated with reduced lung cancer risk and a modulating effect on nucleotide excision repair capacity. Carcinogenesis 24:505–509PubMedCrossRefGoogle Scholar
  118. Yarosh D, Alas LG, Yee V, Oberyszyn A, Kibitel JT, Mitchell D, Rosenstein R, Spinowitz A, Citron M (1992a) Pyrimidine dimer removal enhanced by DNA repair liposomes reduces the incidence of UV skin cancer in mice. Cancer Res 52:4227–4231Google Scholar
  119. Yarosh D, Bucana C, Cox P, Alas L, Kibitel J, Kripke M (1994) Localization of liposomes containing a DNA repair enzyme in murine skin. J Invest Dermatol 103:461–468PubMedCrossRefGoogle Scholar
  120. Yarosh D, Klein J, Kibitel J, Alas L, O’Connor A, Cummings B, Grob D, Gerstein D, Gilchrest BA, Ichihashi M, Ogoshi M, Ueda M, Fernandez V, Chadwick C, Potten CS, Proby CM, Young AR, Hawk JL (1996) Enzyme therapy of xeroderma pigmentosum: safety and efficacy testing of T4N5 liposome lotion containing a prokaryotic DNA repair enzyme. Photodermatol Photoimmunol Photomed 12:122–130PubMedGoogle Scholar
  121. Yarosh D, Klein J, O’Connor A, Hawk J, Rafal E, Wolf P (2001) Effect of topically applied T4 endonuclease V in liposomes on skin cancer in xeroderma pigmentosum: a randomised study. Xeroderma Pigmentosum Study Group. Lancet 357:926–929PubMedCrossRefGoogle Scholar
  122. Yarosh D, Tsimis J, Yee V (1992b) Enhancement of DNA repair of UVR damage in mouse and human skin by liposomes containing a DNA repair enzyme. J Soc Cosmet Chem 41:85–92Google Scholar
  123. Yarosh DB (2001) Liposomes in investigative dermatology. Photodermatol Photoimmunol Photomed 17:203–212PubMedCrossRefGoogle Scholar
  124. Yarosh DB (2004) DNA repair, immunosuppression, and skin cancer. Cutis 74:10–13PubMedGoogle Scholar
  125. Yuasa M, Masutani C, Eki T, Hanaoka F (2000) Genomic structure, chromosomal localization and identification of mutations in the xeroderma pigmentosum variant (XPV) gene. Oncogene 19:4721–4728PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  1. 1.Department of Dermatology and VenerologyGeorg-August-University GoettingenGoettingenGermany

Personalised recommendations