Neuronal selenoprotein expression is required for interneuron development and prevents seizures and neurodegeneration

FASEB J. 2010 Mar;24(3):844-52. doi: 10.1096/fj.09-143974. Epub 2009 Nov 4.

Abstract

Cerebral selenium (Se) deficiency is associated with neurological phenotypes including seizures and ataxia. We wanted to define whether neurons require selenoprotein expression and which selenoproteins are most important, and explore the possible pathomechanism. Therefore, we abrogated the expression of all selenoproteins in neurons by genetic inactivation of the tRNA[Ser](Sec) gene. Cerebral expression of selenoproteins was significantly diminished in the mutants, and histological analysis revealed progressive neurodegeneration. Developing interneurons failed to specifically express parvalbumin (PV) in the mutants. Electrophysiological recordings, before overt cell death, showed normal excitatory transmission, but revealed spontaneous epileptiform activity consistent with seizures in the mutants. In developing cortical neuron cultures, the number of PV(+) neurons was reduced on combined Se and vitamin E deprivation, while other markers, such as calretinin (CR) and GAD67, remained unaffected. Because of the synergism between Se and vitamin E, we analyzed mice lacking neuronal expression of the Se-dependent enzyme glutathione peroxidase 4 (GPx4). Although the number of CR(+) interneurons remained normal in Gpx4-mutant mice, the number of PV(+) interneurons was reduced. Since these mice similarly exhibit seizures and ataxia, we conclude that GPx4 is a selenoenzyme modulating interneuron function and PV expression. Cerebral SE deficiency may thus act via reduced GPx4 expression.-Wirth, E. K., Conrad, M., Winterer, J., Wozny, C., Carlson, B. A., Roth, S., Schmitz, D., Bornkamm, G. W., Coppola, V., Tessarollo, L., Schomburg, L., Köhrle, J., Hatfield, D. L., Schweizer, U. Neuronal selenoprotein expression is required for interneuron development and prevents seizures and neurodegeneration.

Publication types

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

MeSH terms

  • Animals
  • Blotting, Western
  • Calbindin 2
  • Cell Differentiation / drug effects
  • Cells, Cultured
  • Electrophysiology
  • Glutathione Peroxidase / metabolism
  • Glutathione Peroxidase / physiology
  • Immunohistochemistry
  • Interneurons / drug effects
  • Interneurons / metabolism
  • Interneurons / physiology*
  • Mice
  • Mice, Knockout
  • Nerve Degeneration / metabolism*
  • Nerve Degeneration / prevention & control*
  • Parvalbumins / metabolism
  • Parvalbumins / physiology
  • Phospholipid Hydroperoxide Glutathione Peroxidase
  • RNA, Transfer, Amino Acyl / genetics
  • RNA, Transfer, Amino Acyl / physiology
  • S100 Calcium Binding Protein G / metabolism
  • S100 Calcium Binding Protein G / physiology
  • Seizures / metabolism*
  • Seizures / prevention & control*
  • Selenium / pharmacology
  • Selenoproteins / metabolism
  • Selenoproteins / physiology*
  • Vitamin E / pharmacology

Substances

  • Calb2 protein, mouse
  • Calbindin 2
  • Parvalbumins
  • RNA, Transfer, Amino Acyl
  • S100 Calcium Binding Protein G
  • Selenoproteins
  • selenocysteinyl-tRNA
  • Vitamin E
  • Phospholipid Hydroperoxide Glutathione Peroxidase
  • Glutathione Peroxidase
  • Selenium