Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis

J Neurosci. 2004 Jul 21;24(29):6590-9. doi: 10.1523/JNEUROSCI.5747-03.2004.

Abstract

Manic-depressive illness has been conceptualized as a neurochemical illness. However, brain imaging and postmortem studies reveal gray-matter reductions, as well as neuronal and glial atrophy and loss in discrete brain regions of manic-depressive patients. The roles of such cerebral morphological deficits in the neuropathophysiology and therapeutic mechanisms of manic-depressive illness are unknown. Valproate (2-propylpentanoate) is a commonly used mood stabilizer. The ERK (extracellular signal-regulated kinase) pathway is used by neurotrophic factors to regulate neurogenesis, neurite outgrowth, and neuronal survival. We found that chronic treatment of rats with valproate increased levels of activated phospho-ERK44/42 in neurons of the anterior cingulate, a region in which we found valproate-induced increases in expression of an ERK pathway-regulated gene, bcl-2. Valproate time and concentration dependently increased activated phospho-ERK44/42 and phospho-RSK1 (ribosomal S6 kinase 1) levels in cultured cortical cells. These increases were attenuated by Raf and MEK (mitogen-activated protein kinase/ERK kinase) inhibitors. Although valproate affects the functions of GSK-3 (glycogen synthase kinase-3) and histone deacetylase (HDAC), its effects on the ERK pathway were not fully mimicked by selective inhibitors of GSK-3 or HDAC. Similar to neurotrophic factors, valproate enhanced ERK pathway-dependent cortical neuronal growth. Valproate also promoted neural stem cell proliferation-maturation (neurogenesis), demonstrated by bromodeoxyuridine (BrdU) incorporation and double staining of BrdU with nestin, Tuj1, or the neuronal nuclei marker NeuN (neuronal-specific nuclear protein). Chronic treatment with valproate enhanced neurogenesis in the dentate gyrus of the hippocampus. Together, these data demonstrate that valproate activates the ERK pathway and induces ERK pathway-mediated neurotrophic actions. This cascade of events provides a potential mechanism whereby mood stabilizers alleviate cerebral morphometric deficits associated with manic-depressive illness.

Publication types

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

MeSH terms

  • Animals
  • Antimanic Agents / pharmacology*
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Cerebral Cortex / cytology
  • Cerebral Cortex / drug effects*
  • Cerebral Cortex / embryology
  • Cerebral Cortex / enzymology*
  • Extracellular Signal-Regulated MAP Kinases / analysis
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Glycogen Synthase Kinase 3 / physiology
  • Gyrus Cinguli / enzymology
  • Hippocampus / cytology
  • Hippocampus / drug effects
  • Hippocampus / growth & development
  • Histone Deacetylases / physiology
  • MAP Kinase Signaling System / drug effects*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / enzymology*
  • Rats
  • Rats, Wistar
  • Ribosomal Protein S6 Kinases, 90-kDa / metabolism
  • Valproic Acid / pharmacology*
  • p38 Mitogen-Activated Protein Kinases / physiology

Substances

  • Antimanic Agents
  • Valproic Acid
  • Ribosomal Protein S6 Kinases, 90-kDa
  • Rps6ka1 protein, mouse
  • Rps6ka1 protein, rat
  • Extracellular Signal-Regulated MAP Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Glycogen Synthase Kinase 3
  • Histone Deacetylases