PACAP and C2-ceramide generate different AP-1 complexes through a MAP-kinase-dependent pathway: involvement of c-Fos in PACAP-induced Bcl-2 expression

J Neurochem. 2006 Nov;99(4):1237-50. doi: 10.1111/j.1471-4159.2006.04148.x. Epub 2006 Oct 5.

Abstract

The neuropeptide pituitary adenylate cyclase-activating polypeptide (PACAP) inhibits C2-ceramide-induced cell death through blockade of the mitochondrial apoptotic pathway in rat cerebellar granule neurones. However, the gene induction processes and transcription factors involved in the anti-apoptotic effect of PACAP remain unknown. Here, we show that PACAP and C2-ceramide activate activator protein-1 (AP-1) DNA binding in a dose- and time-dependent manner, but generate different AP-1 dimers. Thus, PACAP increased the proportion of c-Fos and Jun D while C2-ceramide increased c-Jun and reduced c-Fos in AP-1 complexes. In addition, PACAP strongly activated c-Fos gene expression while C2-ceramide markedly increased c-Jun phosphorylation. The effect of PACAP on c-Fos expression was blocked by the mitogen-activated protein kinase/extracellular signal-regulated kinase (MEK) inhibitor, U0126, while phosphorylation of c-Jun induced by C2-ceramide was abrogated by the protein phosphatase 2A (PP2A) inhibitor, okadaic acid. Transfection of immature granule cells with c-Fos siRNA, which strongly reduced basal and PACAP-stimulated levels of the protein, totally prevented the stimulatory effect of PACAP on Bcl-2 expression. The present study demonstrates that AP-1 complexes containing c-Fos mediate the effect of PACAP on Bcl-2 gene expression in cerebellar granule neurones. Our data also indicate that different AP-1 dimers are associated with the pro-apoptotic effect of C2-ceramide and the anti-apoptotic effect of PACAP.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Apoptosis / drug effects
  • Apoptosis / physiology
  • Cell Survival / drug effects
  • Cell Survival / physiology
  • Cells, Cultured
  • Cerebellar Cortex / drug effects
  • Cerebellar Cortex / metabolism
  • DNA-Binding Proteins / drug effects
  • DNA-Binding Proteins / metabolism
  • Dose-Response Relationship, Drug
  • Down-Regulation / genetics
  • Enzyme Inhibitors / pharmacology
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • MAP Kinase Signaling System / drug effects
  • MAP Kinase Signaling System / physiology*
  • Neurons / drug effects
  • Neurons / metabolism
  • Phosphoprotein Phosphatases / antagonists & inhibitors
  • Phosphoprotein Phosphatases / metabolism
  • Phosphorylation / drug effects
  • Pituitary Adenylate Cyclase-Activating Polypeptide / metabolism*
  • Pituitary Adenylate Cyclase-Activating Polypeptide / pharmacology
  • Protein Phosphatase 2
  • Proto-Oncogene Proteins c-bcl-2 / drug effects
  • Proto-Oncogene Proteins c-bcl-2 / metabolism*
  • Proto-Oncogene Proteins c-fos / drug effects
  • Proto-Oncogene Proteins c-fos / genetics
  • Proto-Oncogene Proteins c-fos / metabolism*
  • Proto-Oncogene Proteins c-jun / drug effects
  • Proto-Oncogene Proteins c-jun / metabolism
  • Rats
  • Rats, Wistar
  • Sphingosine / analogs & derivatives*
  • Sphingosine / metabolism
  • Sphingosine / pharmacology
  • Transcription Factor AP-1 / metabolism*
  • Transcriptional Activation / drug effects
  • Transcriptional Activation / physiology

Substances

  • DNA-Binding Proteins
  • Enzyme Inhibitors
  • N-acetylsphingosine
  • Pituitary Adenylate Cyclase-Activating Polypeptide
  • Proto-Oncogene Proteins c-bcl-2
  • Proto-Oncogene Proteins c-fos
  • Proto-Oncogene Proteins c-jun
  • Transcription Factor AP-1
  • Phosphoprotein Phosphatases
  • Protein Phosphatase 2
  • Sphingosine