Nerve growth factor-induced glutamate release is via p75 receptor, ceramide, and Ca(2+) from ryanodine receptor in developing cerebellar neurons

J Biol Chem. 2003 Oct 17;278(42):41259-69. doi: 10.1074/jbc.M304409200. Epub 2003 Aug 5.

Abstract

Very little is known about the contribution of a low affinity neurotrophin receptor, p75, to neurotransmitter release. Here we show that nerve growth factor (NGF) induced a rapid release of glutamate and an increase of Ca2+ in cerebellar neurons through a p75-dependent pathway. The NGF-induced release occurred even in the presence of the Trk inhibitor K252a. The release caused by NGF but not brain-derived neurotrophic factor was enhanced in neurons overexpressing p75. Further, after transfection of p75-small interfering RNA, which down-regulated the endogenous p75 expression, the NGF-induced release was inhibited, suggesting that the NGF-induced glutamate release was through p75. We found that the NGF-increased Ca2+ was derived from the ryanodine-sensitive Ca2+ receptor and that the NGF-increased Ca2+ was essential for the NGF-induced glutamate release. Furthermore, scyphostatin, a sphingomyelinase inhibitor, blocked the NGF-dependent Ca2+ increase and glutamate release, suggesting that a ceramide produced by sphingomyelinase was required for the NGF-stimulated Ca2+ increase and glutamate release. This action of NGF only occurred in developing neurons whereas the brain-derived neurotrophic factor-mediated Ca2+ increase and glutamate release was observed at the mature neuronal stage. Thus, we demonstrate that NGF-mediated neurotransmitter release via the p75-dependent pathway has an important role in developing neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoviridae / genetics
  • Amides / pharmacology
  • Amino Acids / metabolism
  • Animals
  • Calcium / metabolism*
  • Calcium / pharmacology
  • Cells, Cultured
  • Ceramides / metabolism*
  • Cerebellum / metabolism*
  • Chelating Agents / pharmacology
  • Dose-Response Relationship, Drug
  • Down-Regulation
  • Egtazic Acid / analogs & derivatives*
  • Egtazic Acid / pharmacology
  • Enzyme Activation
  • Glutamic Acid / metabolism*
  • Immunoblotting
  • Immunohistochemistry
  • Magnesium / metabolism
  • Nerve Growth Factor / metabolism*
  • Neurons / metabolism*
  • Pyrones / pharmacology
  • Rats
  • Receptor, Nerve Growth Factor
  • Receptors, Nerve Growth Factor / metabolism*
  • Ryanodine Receptor Calcium Release Channel / metabolism*
  • Sphingomyelin Phosphodiesterase / metabolism
  • Time Factors
  • Transfection

Substances

  • Amides
  • Amino Acids
  • Ceramides
  • Chelating Agents
  • Pyrones
  • Receptor, Nerve Growth Factor
  • Receptors, Nerve Growth Factor
  • Ryanodine Receptor Calcium Release Channel
  • scyphostatin
  • 1,2-bis(2-aminophenoxy)ethane N,N,N',N'-tetraacetic acid acetoxymethyl ester
  • Glutamic Acid
  • Egtazic Acid
  • Nerve Growth Factor
  • Sphingomyelin Phosphodiesterase
  • Magnesium
  • Calcium