Involvement of mtDNA damage elicited by oxidative stress in the arsenical skin cancers

J Invest Dermatol. 2013 Jul;133(7):1890-900. doi: 10.1038/jid.2013.55. Epub 2013 Jan 31.

Abstract

Arsenic causes several human cancers. Arsenic-induced Bowen's disease (As-BD), the most common arsenical cancer, is characterized by increased proliferation, dysplasia, and individual cell apoptosis, all of which involve mitochondria. We reported that arsenic causes aberrant keratinocyte proliferation through mtTFA-mediated mitochondrial biogenesis in As-BD. Increasing mitochondrial biogenesis causes cells to undergo oxidative stress. However, how arsenic induces oxidative stress and causes mtDNA damage in arsenical cancers remains largely unknown. Using tissues from As-BD patients and arsenic-treated keratinocytes, we determined the oxidative stress, antioxidant enzymes, DNA-repair enzymes, and 8-hydroxy-2'-deoxyguanosine (8-OHdG) level in mtDNA by immunofluorescence, real-time PCR, and western blot. The results showed that oxidative stress was enhanced in both As-BD and arsenic-treated keratinocytes. Antioxidant enzymes including manganese-superoxide anion and copper/zinc-superoxide anion and DNA-repair enzymes were upregulated concomitantly in tissues and cells. In arsenic-treated keratinocytes, increased mitochondrial oxidative stress and the 8-OHdG level in mtDNA were attenuated by pretreatment with ascorbic acid, a potent antioxidant. Further, we found several somatic mutations in the ND4, ND5, and ND6 genes of mtDNA in lesional but not in perilesional skin from As-BD patients. Taken together, the results suggest that oxidative damage and mutations to mtDNA might be involved in the arsenical skin cancers in the context of mitochondrial biogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 8-Hydroxy-2'-Deoxyguanosine
  • Aged
  • Aged, 80 and over
  • Antioxidants / metabolism
  • Apoptosis / drug effects
  • Arsenic / adverse effects*
  • Arsenic / pharmacology
  • Bowen's Disease / chemically induced*
  • Bowen's Disease / genetics
  • Bowen's Disease / physiopathology*
  • Case-Control Studies
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • DNA Damage / physiology*
  • DNA Repair Enzymes / metabolism
  • DNA, Mitochondrial / genetics
  • DNA, Mitochondrial / physiology*
  • Deoxyguanosine / analogs & derivatives
  • Deoxyguanosine / metabolism
  • Humans
  • Keratinocytes / drug effects
  • Keratinocytes / metabolism
  • Keratinocytes / pathology
  • Middle Aged
  • Mutation / genetics
  • Oxidative Stress / physiology*
  • Skin Neoplasms / chemically induced*
  • Skin Neoplasms / genetics
  • Skin Neoplasms / physiopathology*
  • Superoxides / metabolism

Substances

  • Antioxidants
  • DNA, Mitochondrial
  • Superoxides
  • 8-Hydroxy-2'-Deoxyguanosine
  • DNA Repair Enzymes
  • Deoxyguanosine
  • Arsenic