Obligatory role for complex I inhibition in the dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)

Toxicol Sci. 2007 Jan;95(1):196-204. doi: 10.1093/toxsci/kfl133. Epub 2006 Oct 12.

Abstract

Administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) to mice and nonhuman primates causes a parkinsonian disorder characterized by a loss of dopamine-producing neurons in the substantia nigra and corresponding motor deficits. MPTP has been proposed to exert its neurotoxic effects through a variety of mechanisms, including inhibition of complex I of the mitochondrial respiratory chain, displacement of dopamine from vesicular stores, and formation of reactive oxygen species from mitochondrial or cytosolic sources. However, the mechanism of MPTP-induced neurotoxicity is still a matter of debate. Recently, we reported that the yeast single-subunit nicotinamide adenine dinucleotide (reduced) dehydrogenase (NDI1) is resistant to rotenone, a complex I inhibitor that produces a parkinsonian syndrome in rats, and that overexpression of NDI1 in SK-N-MC cells prevents the toxicity of rotenone. In this study, we used viral-mediated overexpression of NDI1 in SK-N-MC cells and animals to determine the relative contribution of complex I inhibition in the toxicity of MPTP. In cell culture, NDI1 overexpression abolished the toxicity of 1-methyl-4-phenylpyridinium, the active metabolite of MPTP. Overexpression of NDI1 through stereotactic administration of a viral vector harboring the NDI1 gene into the substantia nigra protected mice from both the neurochemical and behavioral deficits elicited by MPTP. These data identify inhibition of complex I as a requirement for dopaminergic neurodegeneration and subsequent behavioral deficits produced by MPTP. Furthermore, combined with reports of a complex I defect in Parkinson's disease (PD) patients, the present study affirms the utility of MPTP in understanding the molecular mechanisms underlying dopaminergic neurodegeneration in PD.

Publication types

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

MeSH terms

  • 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine / adverse effects*
  • 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine / metabolism
  • Animals
  • Behavior, Animal
  • Brain / drug effects
  • Brain / metabolism
  • Brain / pathology
  • Cell Death / drug effects
  • Cell Line, Tumor
  • Dependovirus / genetics
  • Disease Models, Animal
  • Dopamine / metabolism*
  • Dopamine Plasma Membrane Transport Proteins / genetics
  • Dopamine Plasma Membrane Transport Proteins / metabolism
  • Electron Transport Complex I / antagonists & inhibitors*
  • Electron Transport Complex I / metabolism
  • Genetic Therapy
  • Genetic Vectors
  • Humans
  • MPTP Poisoning / chemically induced
  • MPTP Poisoning / metabolism*
  • MPTP Poisoning / pathology
  • MPTP Poisoning / prevention & control
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Microglia / drug effects
  • Microglia / metabolism
  • Motor Activity / drug effects
  • Motor Skills Disorders / chemically induced
  • Motor Skills Disorders / metabolism*
  • Motor Skills Disorders / pathology
  • Motor Skills Disorders / prevention & control
  • NADH Dehydrogenase / biosynthesis*
  • NADH Dehydrogenase / genetics
  • Neuroglia / drug effects
  • Neuroglia / metabolism
  • Neurons / drug effects
  • Neurons / metabolism
  • Saccharomyces cerevisiae Proteins / biosynthesis*
  • Saccharomyces cerevisiae Proteins / genetics
  • Transfection

Substances

  • Dopamine Plasma Membrane Transport Proteins
  • Ndi1 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine
  • NADH Dehydrogenase
  • Electron Transport Complex I
  • Dopamine