Methylmalonyl-CoA mutase induction by cerebral ischemia and neurotoxicity of the mitochondrial toxin methylmalonic acid

J Neurosci. 1996 Nov 15;16(22):7336-46. doi: 10.1523/JNEUROSCI.16-22-07336.1996.

Abstract

Differential screening of gerbil brain hippocampal cDNA libraries was used to search for genes expressed in ischemic, but not normal, brain. The methylmalonyl-CoA mutase (MCM) cDNA was highly expressed after ischemia and showed a 95% similarity to mouse and 91% similarity to the human MCM cDNAs. Transient global ischemia induced a fourfold increase in MCM mRNA on Northern blots from both hippocampus and whole forebrain. MCM protein exhibited a similar induction on Western blots of gerbil cerebral cortex 8 and 24 hr after ischemia. Treatment of primary brain astrocytes with either the branched-chain amino acid (BCAA) isoleucine or the BCAA metabolite, propionate, induced MCM mRNA fourfold. Increased concentrations of BCAAs and odd-chain fatty acids, both of which are metabolized to propionate, may contribute to inducing the MCM gene during ischemia. Methylmalonic acid, which is formed from the MCM substrate methylmalonyl-CoA and which inhibits succinate dehydrogenase (SDH), produced dose-related cell death when injected into the basal ganglia of adult rat brain. This neurotoxicity is similar to that of structurally related mitochondrial SDH inhibitors, malonate and 3-nitropropionic acid. Methylmalonic acid may contribute to neuronal injury in human conditions in which it accumulates, including MCM mutations and B12 deficiency. This study shows that methylmalonyl-CoA mutase is induced by several stresses, including ischemia, and would serve to decrease the accumulation of an endogenous cellular mitochondrial inhibitor and neurotoxin, methylmalonic acid.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Basal Ganglia / blood supply
  • Basal Ganglia / cytology
  • Basal Ganglia / metabolism
  • Base Sequence
  • Blotting, Northern
  • Blotting, Western
  • Brain Chemistry / physiology
  • Brain Ischemia / physiopathology*
  • Cell Death / drug effects
  • DNA, Complementary / analysis
  • Gene Expression Regulation, Developmental / drug effects
  • Gene Expression Regulation, Developmental / physiology
  • Gene Expression Regulation, Enzymologic / drug effects
  • Gene Expression Regulation, Enzymologic / physiology
  • Gerbillinae
  • Isoleucine / pharmacology
  • Male
  • Methylmalonic Acid / toxicity*
  • Methylmalonyl-CoA Mutase / genetics*
  • Methylmalonyl-CoA Mutase / metabolism
  • Microinjections
  • Mitochondria / chemistry
  • Mitochondria / drug effects
  • Molecular Sequence Data
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / enzymology
  • Neurotoxins / pharmacology*
  • Oxidative Stress / physiology
  • Propionates / pharmacology
  • RNA, Messenger / analysis
  • Sequence Homology, Amino Acid

Substances

  • DNA, Complementary
  • Neurotoxins
  • Propionates
  • RNA, Messenger
  • Isoleucine
  • Methylmalonic Acid
  • Methylmalonyl-CoA Mutase
  • propionic acid