Role of the Jun kinase pathway in the regulation of c-Jun expression and apoptosis in sympathetic neurons

J Neurosci. 1998 Mar 1;18(5):1713-24. doi: 10.1523/JNEUROSCI.18-05-01713.1998.

Abstract

When deprived of nerve growth factor (NGF), developing sympathetic neurons die by apoptosis. This death is associated with an increase in the level of c-Jun protein and is blocked by expression of a c-Jun dominant negative mutant. Here we have investigated whether NGF withdrawal activates Jun kinases, a family of stress-activated protein kinases that can stimulate the transcriptional activity of c-Jun by phosphorylating serines 63 and 73 in the transactivation domain and which can activate c-jun gene expression. We found that sympathetic neurons contained high basal levels of Jun kinase activity that increased further after NGF deprivation. In contrast, p38 kinase, another stress-activated protein kinase that can also stimulate c-jun gene expression, was not activated after NGF withdrawal. Consistent with Jun kinase activation, we found using a phospho-c-Jun-specific antibody that c-Jun was phosphorylated on serine 63 after NGF withdrawal. Furthermore, expression of a constitutively active form of MEK kinase 1 (MEKK1), which strongly activates the Jun kinase pathway, increased c-Jun protein levels and c-Jun phosphorylation and induced apoptosis in the presence of NGF. This death could be prevented by co-expression of SEKAL, a dominant negative mutant of SAPK/ERK kinase 1 (SEK1), an activator of Jun kinase that is a target of MEKK1. In contrast, expression of SEKAL alone did not prevent c-Jun expression, increases in c-Jun phosphorylation, or cell death after NGF withdrawal. Thus, activation of Jun kinase and increases in c-Jun phosphorylation and c-Jun protein levels occur at the same time after NGF withdrawal, but c-Jun levels and phosphorylation are regulated by an SEK1-independent pathway.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Apoptosis / physiology*
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism*
  • Enzyme Activation
  • Gene Expression Regulation, Enzymologic*
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinase Kinases*
  • Mitogen-Activated Protein Kinases*
  • Nerve Growth Factors / deficiency
  • Neurons / enzymology
  • Neurons / metabolism*
  • PC12 Cells
  • Phosphorylation
  • Protein Kinases / biosynthesis
  • Protein Kinases / genetics
  • Protein Serine-Threonine Kinases / biosynthesis
  • Protein-Tyrosine Kinases / biosynthesis
  • Proto-Oncogene Proteins c-jun / biosynthesis*
  • Proto-Oncogene Proteins c-jun / genetics
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / physiology
  • Superior Cervical Ganglion / cytology
  • Superior Cervical Ganglion / enzymology
  • Superior Cervical Ganglion / metabolism*
  • Transcription Factors / genetics
  • p38 Mitogen-Activated Protein Kinases

Substances

  • Nerve Growth Factors
  • Proto-Oncogene Proteins c-jun
  • Transcription Factors
  • Protein Kinases
  • Protein-Tyrosine Kinases
  • Protein Serine-Threonine Kinases
  • Calcium-Calmodulin-Dependent Protein Kinases
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinase Kinases