Common pathways for ultraviolet skin carcinogenesis in the repair and replication defective groups of xeroderma pigmentosum

J Dermatol Sci. 2000 May;23(1):1-11. doi: 10.1016/s0923-1811(99)00088-2.

Abstract

The human disease xeroderma pigmentosum (XP) involves DNA repair and replication deficiencies that predispose homozygous individuals to a 1000-fold increase in nonmelanoma and melanoma skin cancers. Two major forms of XP are known with different biochemical defects: one form lacks nucleotide excision repair (NER); the other lacks the capacity to replicate damaged DNA. Since the clinical symptoms of both kinds of patients are almost the same, the different cellular defects must be reconciled with common clinical outcomes. An additional question among the NER defective patients is how to reconcile widely different skin and central nervous system symptoms with mutations in the same biochemical pathway. XP involves seven genes of the NER system (XPA through G). The XPA gene codes for a protein that is central to NER and binds to a variety of UV light and chemical damage to DNA. It also acts as a nucleation center for other repair proteins to attach and carry out excision and replacement synthesis. Mutations in XPA that are within the DNA binding site produce more severe CNS disorders, than mutations in the C-terminal region of the protein that interacts with the TFIIH complex. In contrast, mutations in two members of the TFIIH complex, the XPB and XPD genes are generally very severe with both skin and CNS disorders. Missense mutations within the helicase regions of these genes are associated with DNA repair deficiencies and XPD; mutations elsewhere in these genes are correlated with symptoms of XP and Cockayne syndrome and trichothiodystrophy. This raises the question whether the CNS disorders of XPA, XPB, and XPD patients are similar, or whether a careful clinical evaluation might reveal different mechanisms of development. The XP variant lacks the capacity to replicate damaged DNA due to mutations in hRad30, a damage-specific polymerase eta. The phenotype of XP variant cells becomes unstable and the cells become much more UV-sensitive when they are transformed by methods that inactivate p53. On a p53 negative background, the induction of recombination between sister chromatids occurs much more extensively than in normal cells, and we have evidence that DNA double strand breaks which trigger an apoptotic pathway involving caspase-3 are involved. The pathway for UV carcinogenesis may be the same for all XP patients if the ultimate cause of genomic instability is an increase in replication of damaged DNA by the error-prone polymerase zeta. The presence of unrepaired damage in the NER defective groups of XP would present more substrate for the error-prone system leading to increased mutation rates. The absence of pol eta would require cells to use the error-prone pol zeta pathway, also increasing mutation rates from UV damage. A common pathway for increased mutagenesis therefore underlies both forms of XP.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.
  • Review

MeSH terms

  • Animals
  • Central Nervous System Diseases / genetics
  • DNA Polymerase iota
  • DNA Repair / genetics
  • DNA Replication / genetics
  • DNA-Directed DNA Polymerase / genetics
  • Humans
  • Mutation
  • Neoplasms, Radiation-Induced / etiology*
  • Neoplasms, Radiation-Induced / genetics
  • Neoplasms, Radiation-Induced / metabolism
  • Skin Neoplasms / etiology*
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism
  • Ultraviolet Rays / adverse effects
  • Xeroderma Pigmentosum / complications*
  • Xeroderma Pigmentosum / genetics
  • Xeroderma Pigmentosum / metabolism*

Substances

  • DNA-Directed DNA Polymerase
  • Rad30 protein
  • DNA Polymerase iota
  • POLI protein, human