Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1

Nature. 2005 Mar 3;434(7029):108-13. doi: 10.1038/nature03314.

Abstract

Spinocerebellar ataxia with axonal neuropathy-1 (SCAN1) is a neurodegenerative disease that results from mutation of tyrosyl phosphodiesterase 1 (TDP1). In lower eukaryotes, Tdp1 removes topoisomerase 1 (top1) peptide from DNA termini during the repair of double-strand breaks created by collision of replication forks with top1 cleavage complexes in proliferating cells. Although TDP1 most probably fulfils a similar function in human cells, this role is unlikely to account for the clinical phenotype of SCAN1, which is associated with progressive degeneration of post-mitotic neurons. In addition, this role is redundant in lower eukaryotes, and Tdp1 mutations alone confer little phenotype. Moreover, defects in processing or preventing double-strand breaks during DNA replication are most probably associated with increased genetic instability and cancer, phenotypes not observed in SCAN1 (ref. 8). Here we show that in human cells TDP1 is required for repair of chromosomal single-strand breaks arising independently of DNA replication from abortive top1 activity or oxidative stress. We report that TDP1 is sequestered into multi-protein single-strand break repair (SSBR) complexes by direct interaction with DNA ligase IIIalpha and that these complexes are catalytically inactive in SCAN1 cells. These data identify a defect in SSBR in a neurodegenerative disease, and implicate this process in the maintenance of genetic integrity in post-mitotic neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Axons / metabolism
  • Axons / pathology*
  • Camptothecin / pharmacology
  • Catalysis / drug effects
  • Cell Line
  • Comet Assay
  • DNA Damage* / drug effects
  • DNA Ligase ATP
  • DNA Ligases / metabolism
  • DNA Repair* / drug effects
  • DNA Replication / drug effects
  • DNA Topoisomerases, Type I / metabolism
  • DNA, Single-Stranded / genetics
  • DNA, Single-Stranded / metabolism*
  • Humans
  • Multiprotein Complexes / chemistry
  • Multiprotein Complexes / metabolism
  • Mutation
  • Oxidative Stress / physiology
  • Phosphoric Diester Hydrolases / genetics
  • Phosphoric Diester Hydrolases / metabolism
  • Poly-ADP-Ribose Binding Proteins
  • Protein Binding
  • Spinocerebellar Ataxias / genetics*
  • Spinocerebellar Ataxias / pathology*
  • Topoisomerase I Inhibitors
  • Xenopus Proteins

Substances

  • DNA, Single-Stranded
  • Multiprotein Complexes
  • Poly-ADP-Ribose Binding Proteins
  • Topoisomerase I Inhibitors
  • Xenopus Proteins
  • Phosphoric Diester Hydrolases
  • TDP1 protein, human
  • tyrosyl-DNA phosphodiesterase
  • DNA Topoisomerases, Type I
  • DNA Ligases
  • DNA Ligase ATP
  • DNA ligase III alpha protein, Xenopus
  • Camptothecin