Mitochondrial inhibitor models of Huntington's disease and Parkinson's disease induce zinc accumulation and are attenuated by inhibition of zinc neurotoxicity in vitro or in vivo

Neurodegener Dis. 2013;11(1):49-58. doi: 10.1159/000336558. Epub 2012 May 24.

Abstract

Background: Inhibition of mitochondrial function occurs in many neurodegenerative diseases, and inhibitors of mitochondrial complexes I and II are used to model them. The complex II inhibitor, 3-nitroproprionic acid (3-NPA), kills the striatal neurons susceptible in Huntington's disease. The complex I inhibitor N-methyl-4-phenylpyridium (MPP(+)) and 6-hydroxydopamine (6-OHDA) are used to model Parkinson's disease. Zinc (Zn(2+)) accumulates after 3-NPA, 6-OHDA and MPP(+) in situ or in vivo.

Objective: We will investigate the role of Zn(2+) neurotoxicity in 3-NPA, 6-OHDA and MPP(+).

Methods: Murine striatal/midbrain tyrosine hydroxylase positive, or near-pure cortical neuronal cultures, or animals were exposed to 3-NPA or MPP(+) and 6-OHDA with or without neuroprotective compounds. Intracellular zinc ([Zn(2+)](i)), nicotinamide adenine dinucleotide (NAD(+)), NADH, glycolytic intermediates and neurotoxicity were measured.

Results: We showed that compounds or genetics which restore NAD(+) and attenuate Zn(2+) neurotoxicity (pyruvate, nicotinamide, NAD(+), increased NAD(+) synthesis, sirtuin inhibition or Zn(2+) chelation) attenuated the neuronal death induced by these toxins. The increase in [Zn(2+)](i) preceded a reduction in the NAD(+)/NADH ratio that caused a reversible glycolytic inhibition. Pyruvate, nicotinamide and NAD(+) reversed the reductions in the NAD(+)/NADH ratio, glycolysis and neuronal death after challenge with 3-NPA, 6-OHDA or MPP(+), as was previously shown for exogenous Zn(2+). To test efficacy in vivo, we injected 3-NPA into the striatum of rats and systemically into mice, with or without pyruvate. We observed early striatal Zn(2+) fluorescence, and pyruvate significantly attenuated the 3-NPA-induced lesion and restored behavioral scores.

Conclusions: Together, these studies suggest that Zn(2+) accumulation caused by MPP(+) and 3-NPA is a novel preventable mechanism of the resultant neurotoxicity.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine / pharmacology
  • Animals
  • Carrier Proteins
  • Cation Transport Proteins
  • Cell Death / drug effects
  • Cells, Cultured
  • Cerebral Cortex / cytology
  • Dihydroxyacetone Phosphate / metabolism
  • Disease Models, Animal
  • Drug Interactions
  • Embryo, Mammalian
  • Fructose-Bisphosphatase / metabolism
  • Humans
  • Huntington Disease / chemically induced
  • Huntington Disease / drug therapy*
  • Huntington Disease / metabolism*
  • Huntington Disease / pathology
  • Male
  • Matrix Metalloproteinase 16 / deficiency
  • Membrane Proteins / deficiency
  • Membrane Transport Proteins
  • Mental Disorders / chemically induced
  • Mental Disorders / prevention & control
  • Mice
  • Mice, Inbred C57BL
  • Mice, Neurologic Mutants
  • Mice, Transgenic
  • NAD / metabolism
  • NAD / therapeutic use
  • Neurons / drug effects
  • Niacinamide / therapeutic use
  • Nitro Compounds / toxicity
  • Oxidopamine / toxicity
  • Parkinson Disease / drug therapy
  • Parkinson Disease / etiology
  • Parkinson Disease / metabolism*
  • Parkinson Disease / pathology
  • Propionates / toxicity
  • Pyruvic Acid / therapeutic use
  • Rats
  • Rats, Long-Evans
  • Tyrosine 3-Monooxygenase / metabolism
  • Zinc / metabolism*

Substances

  • Carrier Proteins
  • Cation Transport Proteins
  • Membrane Proteins
  • Membrane Transport Proteins
  • Nitro Compounds
  • Propionates
  • Slc30a3 protein, mouse
  • NAD
  • Niacinamide
  • Dihydroxyacetone Phosphate
  • Pyruvic Acid
  • Oxidopamine
  • 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine
  • Tyrosine 3-Monooxygenase
  • Fructose-Bisphosphatase
  • Matrix Metalloproteinase 16
  • Zinc
  • 3-nitropropionic acid