Molecular Basis of DNA Repair Mechanisms and Syndromes

  • G. Weeda
  • J. de Boer
  • I. Donker
  • J. de Wit
  • S. B. Winkler
  • G. T. J. van der Horst
  • W. Vermeulen
  • D. Bootsma
  • J. H. J. Hoeijmakers
Part of the Recent Results in Cancer Research book series (RECENTCANCER, volume 154)

Abstract

Numerous chemical agents and various types of radiation (e.g. UV-light, X-rays) induce a wide range of lesions in DNA. Such damage can lead to changes in the nucleotide sequence varying from point mutations to gross chromosomal aberrations which can alter the expression or functioning of genes implicated in regulation of cell proliferation and differentiation, thereby forwarding the cell in the multistep process of carcinogenesis. To prevent these and other deleterious consequences of DNA injury, all living organisms are equipped with a complex network of DNA repair systems. One of the best studied repair processes is the nucleotide excision repair (NER) pathway which removes a wide diversity of DNA lesions including cyclobutane pyrimidine dimers and (6–4) photoproducts as well as chemical adducts and cross-links. In most — if not all — organisms two NER subpathways operate. One deals with the rapid and efficient removal of lesions that block transcription and thus need to be eliminated urgently (transcription-coupled repair, TCR). The other accomplishes the slower and less efficient global genome repair (GGR) of bulk DNA, including the nontranscribed strand of active genes.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aboussekhra A, Biggerstaff M, Shivji MKK, Vilpo JA, Moncollin V, Podust VN, Protic M, Hubscher U, Egly J-M, Wood RD (1995) Mammalian excision repair reconstituted with purified components. Cell 80: 859–868PubMedCrossRefGoogle Scholar
  2. Adamczewski JPA, Rossignol M, Tassan J-P, Nigg EA, Moncollin V, Egly J-M (1996) MAT1, cdk7 and cyclin H form a kinase complex which is UV light-sensitive upon association with TFIIH. EMBO J 15: 1877–1884PubMedGoogle Scholar
  3. Bootsma D, Kraemer KH, Cleaver JE, Hoeijmakers JHJ (1997) Nucleotide excision repair syndromes: xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. In: Vogelstein B, Kinzler K (eds) The genetic basis of human cancer. McGraw-Hill, New YorkGoogle Scholar
  4. Chu G, Chang E (1988) Xeroderma pigmentosum group E lacks a nuclear factor that binds to damaged DNA. Science 242: 564–567Google Scholar
  5. De Boer J, Donker I, de Wit J, Hoeijmakers JHJ, Weeda G (1998) Disruption of the mouse XPD DNA repair/basal transcription gene results in preimplantation lethality. Cancer Res 1998.Google Scholar
  6. De Vries A, van Oostrom CThM, Hofhuis FMA, Dortant PM, Berg RJW, de Gruijl FR, Wester PW, van Kreijl CF, Capel PJA, van Steeg H, Verbeek SJ (1995) Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 377: 169–173Google Scholar
  7. Donahue BA, Yin S, Taylor J-S, Reines D, Hanawalt PC (1994) Transcript cleavage by RNA polymerase II arrested by a cylobutane pyrimidine dimer in the DNA template. Proc Natl Acad Sci USA 91: 8502–8506PubMedCrossRefGoogle Scholar
  8. Friedberg EC, Walker GC, Siede W (1995) DNA repair and mutagenesis. ASM, Washington, DCGoogle Scholar
  9. Gerard M, Fischer L, Moncollin V, Chipoulet M, Chambon P, Egly J-M (1991) Purification and interaction properties of the human RNA polymerase B (II) general transcription factor BTF2. J Biol Chem 266: 20940–20945PubMedGoogle Scholar
  10. Gorbalenya AE, Koonin EC (1993) Helicase: amino acid sequence comparison and structure-function relationships. Curr Biol 3: 419–429Google Scholar
  11. Hanawalt PC, Donahue BA, Sweder KS (1994) Collision or collusion? Curr Biol 4: 518–521PubMedCrossRefGoogle Scholar
  12. Henning KA, Li L, Iyer N, McDaniel LD, Reagan MS, Legerski R, Schultz RA, Stefanini M, Lehmann AR, Mayne L, Friedberg EC (1995) The Cockayne syndrome group A gene encodes a WD repeat protein that interacts with CSB protein and a subunit of RNA polymerase II TFIIH. Cell 82: 555–564PubMedCrossRefGoogle Scholar
  13. Hoeijmakers JHJ (1993) Nucleotide excision repair II: From yeast to mammals. Trends Genet 9: 211–217PubMedCrossRefGoogle Scholar
  14. Huang JR, Moncollin V, Vermeulen W, Seroz T, van Vuuren H, Hoeijmakers JHJ, Egly J-M (1996) 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 271: 15898–15904CrossRefGoogle Scholar
  15. Itin PH, Pittelkow MR (1990) Trichothiodystrophy: review of sulphur-deficient brittle hair syndromes and association with ectodermal dysplasias. J Am Acad Dermatol 22: 705–717PubMedCrossRefGoogle Scholar
  16. Jones CJ, Wood RD (1993) Preferential binding of xeroderma pigmentosum group A complementing protein to damaged DNA. Biochemistry 32: 12096–12104PubMedCrossRefGoogle Scholar
  17. Marinoni J-C, Roy R, Vermeulen W, Miniou P, Lutz Y, Weeda G, Seroz T, Gomez DM, Hoeijmakers JHJ, Egly J-M (1997) Cloning and characterization of p52, the fifth subunit of the core of the transcription/DNA repair factor TFIIH. EMBO J 16: 1093–1102PubMedCrossRefGoogle Scholar
  18. Masutani C, Sugasawa K, Yanagisawa J, Sonoyama T, Ui M, Enemoto T, Takio K, Tanaka K, van der Spek PJ, Bootsma D, Hoeijmakers JHJ, Hanaoka F (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: 1831–1843PubMedGoogle Scholar
  19. Mellon, I, Spivak G, Hanawalt PC (1997) Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51: 241–249CrossRefGoogle Scholar
  20. Nakane H, Takeuchi S, Yuba S, Saijo M, Nakatsu Y, Murai H, Nakatsuru Y, Ishikawa T, Hirota S, Kitamura Y, Kato Y, Tsunoda Y, Miyauchi H, Horio T, Tokunaga T, Matsunaga T, Nikaido O, Nishimune Y, Okada Y, Tanaka K (1995) High incidence of ultraviolet-B- or chemical-carcinogen-induced skin tumours in mice lacking the xeroderma pigmentosum group A gene. Nature 377: 165–168PubMedCrossRefGoogle Scholar
  21. Nance NA, Berry SA (1992) Cockayne syndrome. Review of 140 cases. Am J Med Genet 42: 68–84PubMedCrossRefGoogle Scholar
  22. O’Donovan A, Davies AA, Moggs J, West SC, Wood RD (1994) XPG endonuclease makes the 3’ incision in human DNA nucleotide excision repair. Nature 371: 432–435PubMedCrossRefGoogle Scholar
  23. Schaeffer L, Roy R, Humbert S, Moncollin V, Vermeulen W, Hoeijmakers JHJ, Chambon P, Egly J-M (1993) DNA repair helicase: a component of BTF2(TFIIH) transcription factor. Science 260: 58–63PubMedCrossRefGoogle Scholar
  24. Schaeffer L, Moncollin V, Roy R, Staub A, Mezzina M, Sarasin A, Weeda G, Hoeijmakers JHJ, Egly J-M (1994) The ERCC2/DNA repair protein is associated with the class II BTF2/TFIIH transcription factor EMBO J 13: 2388–2392PubMedGoogle Scholar
  25. Sijbers AM, de Laat WL, Ariza RR, Biggerstaff M, Wei YF, Moggs JG, Carter KC, Shell BK, Evans, de Jong MC, Rademakers S, de Rooij J, Jaspers NGJ, Hoeijmakers JHJ, Wood RD (1996) Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell 86: 811–822Google Scholar
  26. Van der Horst GTJ, van Steeg H, Berg RJW, van Gool AJ, de Wit J, Weeda G, Morreau H, Seems RB, van Kreijl CF, de Gruijl FR, Bootsma D, Hoeijmakers JHJ (1997) Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell 89: 425–435Google Scholar
  27. Van Gool AJ, Citterio E, Rademakers S, van Os R, Vermeulen W, Constantinou A, Egly J-M, Bootsma D, Hoeijmakers JHJ (1997) The Cockayne syndrome B protein, involved in transcription-coupled DNA repair resides in an RNA polymerase II-containing complex. EMBO J 16: 5955–5956PubMedCrossRefGoogle Scholar
  28. Van Vuuren AJ, Vermeulen W, Ma L, Weeda G, Appeldoorn E, Jaspers NGJ, van der Eb AJ, Bootsma D, Hoeijmakers JHJ, Humbert S, Schaeffer L, Egly J-M (1994) Correction of xeroderma pigmentosum repair defect by basal transcription factor BTF2 ( TFIIH ). EMBO J 13: 1645–1653PubMedGoogle Scholar
  29. Venema J, van Hoffen A, Karcagi V, Natarajan AT, van Zeeland AA, Mullenders LHF (1991) Xeroderma pigmentosum complementation group C cells remove pyrimidine selectively from the transcribed strand of active genes. Mol Cell Biol 11: 4128–4134PubMedGoogle Scholar
  30. Vermeulen W, van Vuuren AJ, Chipoulet M, Schaeffer L, Appeldoorn E, Weeda G, Jaspers NGJ, Priestley A, Arlett CF, Lehmann AR, Stefanini M, Mezzina M, Sarasin A, Bootsma D, Egly J-M, Hoeijmakers JHJ (1994) Three unusual repair deficiencies associated with transcription factor BTF2(TFIIH): evidence for the existence of a transcription syndrome. Cold Spring Harbor Symp Quant Biol 59: 317–329PubMedCrossRefGoogle Scholar
  31. Weeda G, van Ham RCA, Vermeulen W, Bootsma D, van der Eb AJ, Hoeijmakers JHJ (1990) A presumed DNA helicase encoded by ERCC-3 is involved in the human repair disorders xeroderma pigmentosum and Cockayne’s syndrome. Cell 62: 777–791PubMedCrossRefGoogle Scholar
  32. Weeda G, Rossignol M, Fraser RA, Winkler GS, Vermeulen W, van’t Veer LJ, Ma L, Hoeijmakers JHJ, Egly J-M (1997a) The XPB subunit of repair/transcription factor TFIIH directly interacts with SUG1, a subunit of the 26S proteasome and putative transcription factor. Nucleic Acids Res 25: 2274–2283PubMedCrossRefGoogle Scholar
  33. Weeda G, Donker I, de Wit J, Morreau H, Janssens R, Vissers CJ, Nigg A, van Steeg H, Bootsma D, Hoeijmakers JHJ (1997b) Disruption of the mouse ERCCI results in a novel repair syndrome with growth failure, nuclear abnormalities and senescence. Curr Biol 7: 427–439Google Scholar
  34. Winkler SB, Vermeulen W, Coin F, Egly J-M, Hoeijmakers JHJ, Weeda G (1998) Affinity purification of human DNA repair/transcription factor TFIIH using epitope tagged XPB protein. J Biol Chem.Google Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1998

Authors and Affiliations

  • G. Weeda
    • 1
  • J. de Boer
    • 1
  • I. Donker
    • 1
  • J. de Wit
    • 1
  • S. B. Winkler
    • 1
  • G. T. J. van der Horst
    • 1
  • W. Vermeulen
    • 1
  • D. Bootsma
    • 1
  • J. H. J. Hoeijmakers
    • 1
  1. 1.Department of Cell Biology and Genetics, Medical Genetic CentreErasmus UniversityRotterdamThe Netherlands

Personalised recommendations