Intracellular pH reduction prevents excitotoxic and ischemic neuronal death by inhibiting NADPH oxidase

Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):E4362-8. doi: 10.1073/pnas.1313029110. Epub 2013 Oct 25.

Abstract

Sustained activation of N-methyl-d-aspartate (NMDA) -type glutamate receptors leads to excitotoxic neuronal death in stroke, brain trauma, and neurodegenerative disorders. Superoxide production by NADPH oxidase is a requisite event in the process leading from NMDA receptor activation to excitotoxic death. NADPH oxidase generates intracellular H(+) along with extracellular superoxide, and the intracellular H(+) must be released or neutralized to permit continued NADPH oxidase function. In cultured neurons, NMDA-induced superoxide production and neuronal death were prevented by intracellular acidification by as little as 0.2 pH units, induced by either lowered medium pH or by inhibiting Na(+)/H(+) exchange. In mouse brain, superoxide production induced by NMDA injections or ischemia-reperfusion was likewise prevented by inhibiting Na(+)/H(+) exchange and by reduced expression of the Na(+)/H(+) exchanger-1 (NHE1). Neuronal intracellular pH and neuronal Na(+)/H(+) exchange are thus potent regulators of excitotoxic superoxide production. These findings identify a mechanism by which cell metabolism can influence coupling between NMDA receptor activation and superoxide production.

Keywords: Hv1; NOX2; acidosis; cariporide.

Publication types

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

MeSH terms

  • Analysis of Variance
  • Animals
  • Brain / cytology
  • Brain / metabolism*
  • Cation Transport Proteins / metabolism
  • Cell Death / physiology*
  • Cells, Cultured
  • DNA Primers / genetics
  • Fluorescence
  • Hydrogen-Ion Concentration
  • Intracellular Fluid / chemistry*
  • Mice
  • NADPH Oxidases / metabolism*
  • Neurons / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Sodium-Hydrogen Exchanger 1
  • Sodium-Hydrogen Exchangers / metabolism
  • Superoxides / metabolism

Substances

  • Cation Transport Proteins
  • DNA Primers
  • Receptors, N-Methyl-D-Aspartate
  • Slc9a1 protein, mouse
  • Sodium-Hydrogen Exchanger 1
  • Sodium-Hydrogen Exchangers
  • Superoxides
  • NADPH Oxidases