Preserved striatal innervation maintains motor function despite severe loss of nigral dopaminergic neurons

Brain. 2024 Sep 3;147(9):3189-3203. doi: 10.1093/brain/awae089.

Abstract

Degeneration of dopaminergic neurons in the substantia nigra and their striatal axon terminals causes cardinal motor symptoms of Parkinson's disease. In idiopathic cases, high levels of mitochondrial DNA alterations, leading to mitochondrial dysfunction, are a central feature of these vulnerable neurons. Here we present a mouse model expressing the K320E variant of the mitochondrial helicase Twinkle in dopaminergic neurons, leading to accelerated mitochondrial DNA mutations. These K320E-TwinkleDaN mice showed normal motor function at 20 months of age, although ∼70% of nigral dopaminergic neurons had perished. Remaining neurons still preserved ∼75% of axon terminals in the dorsal striatum and enabled normal dopamine release. Transcriptome analysis and viral tracing confirmed compensatory axonal sprouting of the surviving neurons. We conclude that a small population of substantia nigra dopaminergic neurons is able to adapt to the accumulation of mitochondrial DNA mutations and maintain motor control.

Keywords: Parkinson’s disease; axonal sprouting; dopaminergic neurons; mitochondrial DNA; motor symptoms; neurodegeneration.

MeSH terms

  • Animals
  • Corpus Striatum* / metabolism
  • Corpus Striatum* / pathology
  • DNA Helicases / genetics
  • DNA, Mitochondrial / genetics
  • Dopamine / metabolism
  • Dopaminergic Neurons* / metabolism
  • Dopaminergic Neurons* / pathology
  • Male
  • Mice
  • Mice, Transgenic
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Motor Activity / physiology
  • Mutation
  • Substantia Nigra* / metabolism
  • Substantia Nigra* / pathology

Substances

  • DNA, Mitochondrial
  • DNA Helicases
  • Mitochondrial Proteins
  • Dopamine