Spinocerebellar ataxia with axonal neuropathy: consequence of a Tdp1 recessive neomorphic mutation?

EMBO J. 2007 Nov 14;26(22):4732-43. doi: 10.1038/sj.emboj.7601885. Epub 2007 Oct 18.

Abstract

Tyrosyl-DNA phosphodiesterase 1 (Tdp1) cleaves the phosphodiester bond between a covalently stalled topoisomerase I (Topo I) and the 3' end of DNA. Stalling of Topo I at DNA strand breaks is induced by endogenous DNA damage and the Topo I-specific anticancer drug camptothecin (CPT). The H493R mutation of Tdp1 causes the neurodegenerative disorder spinocerebellar ataxia with axonal neuropathy (SCAN1). Contrary to the hypothesis that SCAN1 arises from catalytically inactive Tdp1, Tdp1-/- mice are indistinguishable from wild-type mice, physically, histologically, behaviorally, and electrophysiologically. However, compared to wild-type mice, Tdp1-/- mice are hypersensitive to CPT and bleomycin but not to etoposide. Consistent with earlier in vitro studies, we show that the H493R Tdp1 mutant protein retains residual activity and becomes covalently trapped on the DNA after CPT treatment of SCAN1 cells. This result provides a direct demonstration that Tdp1 repairs Topo I covalent lesions in vivo and suggests that SCAN1 arises from the recessive neomorphic mutation H493R. This is a novel mechanism for disease since neomorphic mutations are generally dominant.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Axons
  • Bleomycin / pharmacology
  • Brain / metabolism
  • Camptothecin / analogs & derivatives
  • Camptothecin / pharmacology
  • Cells, Cultured
  • Comet Assay
  • Embryo, Mammalian / cytology
  • Etoposide / pharmacology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Genes, Recessive
  • Humans
  • Irinotecan
  • Mice
  • Mice, Knockout
  • Mutation
  • Phosphoric Diester Hydrolases / deficiency
  • Phosphoric Diester Hydrolases / genetics
  • Phosphoric Diester Hydrolases / metabolism*
  • Polyneuropathies / genetics
  • Polyneuropathies / metabolism
  • RNA, Messenger / metabolism
  • Spinocerebellar Ataxias / genetics*
  • Spinocerebellar Ataxias / metabolism
  • Topotecan / pharmacology

Substances

  • Antineoplastic Agents
  • RNA, Messenger
  • Bleomycin
  • Etoposide
  • Irinotecan
  • Topotecan
  • Phosphoric Diester Hydrolases
  • Tdp1 protein, mouse
  • Camptothecin