Nerve growth factor-induced protein kinase C stimulation contributes to TrkA-dependent inhibition of p75 neurotrophin receptor sphingolipid signaling

J Neurosci Res. 2004 Aug 15;77(4):465-74. doi: 10.1002/jnr.20189.

Abstract

Previous studies have established that reciprocal interactions between the low-affinity p75 nerve growth factor (NGF) receptor (p75(NTR)) and the high-affinity TrkA NGF receptor can dictate the cellular response to NGF. As the most important interaction, TrkA signaling was found to inhibit p75(NTR)-mediated sphingomyelinase (SMase) stimulation, ceramide production, and apoptosis. However, the mechanism by which TrkA counteracts p75(NTR)-coupled sphingolipid signaling is still unclear. Considering the stimulatory effect of NGF on protein kinase C (PKC) activity, we investigated the role of PKC in TrkA/p75(NTR) signaling interaction. In this study, we found that, in SK-N-BE cells, which selectively express p75(NTR), phorbol ester-induced PKC stimulation resulted in the abrogation of SMase stimulation and ceramide production induced by NGF. Moreover, in SK-N-BE neuroblastoma cells, which selectively express TrkA, NGF stimulated global PKC activity through two independent pathways involving phospholipase Cgamma (PLCgamma) and phosphoinositide-3 kinase (PI3K). In SH-SY5Y, another neuroblastoma cell line, which coexpresses TrkA and p75(NTR), NGF induced PKC stimulation through a TrkA/PI3K signaling pathway, whereas there was no ceramide production. However, in these cells, the inhibition of TrkA, PI3K, and PKC resulted in the restoration of NGF-induced ceramide production. Thus, our study demonstrates for the first time that TrkA interferes with p75(NTR) signaling through a PI3K/PKC-dependent mechanism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line, Tumor
  • Ceramides / metabolism
  • Feedback, Physiological / physiology
  • Humans
  • Nerve Growth Factor / pharmacology*
  • Neurons / drug effects
  • Neurons / enzymology*
  • Phorbol Esters / pharmacology
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phospholipase C gamma
  • Protein Kinase C / drug effects
  • Protein Kinase C / metabolism*
  • Receptor, Nerve Growth Factor
  • Receptor, trkA / genetics
  • Receptor, trkA / metabolism*
  • Receptors, Nerve Growth Factor / genetics
  • Receptors, Nerve Growth Factor / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Sphingolipids / metabolism*
  • Type C Phospholipases / metabolism

Substances

  • Ceramides
  • Phorbol Esters
  • Receptor, Nerve Growth Factor
  • Receptors, Nerve Growth Factor
  • Sphingolipids
  • Nerve Growth Factor
  • Phosphatidylinositol 3-Kinases
  • Receptor, trkA
  • Protein Kinase C
  • Type C Phospholipases
  • Phospholipase C gamma