Mitochondrial DNA Replication Defects Disturb Cellular dNTP Pools and Remodel One-Carbon Metabolism

Cell Metab. 2016 Apr 12;23(4):635-48. doi: 10.1016/j.cmet.2016.01.019. Epub 2016 Feb 25.

Abstract

Mitochondrial dysfunction affects cellular energy metabolism, but less is known about the consequences for cytoplasmic biosynthetic reactions. We report that mtDNA replication disorders caused by TWINKLE mutations-mitochondrial myopathy (MM) and infantile onset spinocerebellar ataxia (IOSCA)-remodel cellular dNTP pools in mice. MM muscle shows tissue-specific induction of the mitochondrial folate cycle, purine metabolism, and imbalanced and increased dNTP pools, consistent with progressive mtDNA mutagenesis. IOSCA-TWINKLE is predicted to hydrolyze dNTPs, consistent with low dNTP pools and mtDNA depletion in the disease. MM muscle also modifies the cytoplasmic one-carbon cycle, transsulfuration, and methylation, as well as increases glucose uptake and its utilization for de novo serine and glutathione biosynthesis. Our evidence indicates that the mitochondrial replication machinery communicates with cytoplasmic dNTP pools and that upregulation of glutathione synthesis through glucose-driven de novo serine biosynthesis contributes to the metabolic stress response. These results are important for disorders with primary or secondary mtDNA instability and offer targets for metabolic therapy.

Publication types

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

MeSH terms

  • Adult
  • Animals
  • Carbon / metabolism
  • DNA Helicases / genetics
  • DNA Helicases / metabolism
  • DNA Replication
  • DNA, Mitochondrial / genetics
  • DNA, Mitochondrial / metabolism*
  • Female
  • Folic Acid / metabolism
  • Glucose / metabolism
  • Glutathione / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mitochondria / pathology
  • Mitochondrial Myopathies / genetics
  • Mitochondrial Myopathies / metabolism*
  • Mitochondrial Myopathies / pathology
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Models, Molecular
  • Mutation
  • Nucleotides / metabolism*
  • Serine / metabolism
  • Spinocerebellar Degenerations / genetics
  • Spinocerebellar Degenerations / metabolism*
  • Spinocerebellar Degenerations / pathology

Substances

  • DNA, Mitochondrial
  • Mitochondrial Proteins
  • Nucleotides
  • Serine
  • Carbon
  • Folic Acid
  • Twnk protein, mouse
  • DNA Helicases
  • TWNK protein, human
  • Glutathione
  • Glucose

Supplementary concepts

  • Infantile onset spinocerebellar ataxia