Selective ceramide binding to protein kinase C-alpha and -delta isoenzymes in renal mesangial cells

Biochemistry. 1998 Oct 13;37(41):14556-62. doi: 10.1021/bi981401i.

Abstract

Ceramide is an important lipid second messenger produced by sphingolipid metabolism in cells exposed to a limited number of agonists and in turn triggers several cell responses in a protein kinase C (PKC)-dependent manner. Stimulation of mesangial cells with a radioiodinated photoaffinity labeling analogue of ceramide, (N-[3-[[[2-(125I)iodo-4-[3-(trifluoromethyl)-3H-diazirin-3-yl]benz yl] oxy]carbonyl]propanoyl]-D-erythro-sphingosine) ([125I]-TID-ceramide), defines PKC-alpha and PKC-delta as direct targets of ceramide. No binding of ceramide to PKC-epsilon and PKC-zeta could be detected. Moreover, TID-ceramide selectively binds to recombinant PKC-alpha and -delta but not to PKC-epsilon and -zeta isoenzymes. In vitro kinase activity assays reveal that only the binding of ceramide to PKC-alpha is accompanied by an increase in kinase activity. In contrast, there is no change in in vitro kinase activity of the other isoforms tested, i.e., PKC-delta, -epsilon, and -zeta, toward any of the conventional substrates tested. However, it is noteworthy that PKC-delta shows a decreased autophosphorylation upon ceramide binding. In vivo, activation of PKC-alpha by ceramide is monitored by a delayed translocation of the isoform from the cytosol to the membrane fraction, detectable after 1 h of stimulation. In contrast, neither PKC-delta, nor -epsilon nor -zeta is redistributed by ceramide. One functional cell response mediated by PKC-alpha in mesangial cells is a negative feedback regulation of ligand-stimulated phosphoinositide hydrolysis. When cells are pretreated with ceramide, ATP-induced inositol trisphosphate formation is time-dependently reduced. A maximal inhibition is observed after 2 h of ceramide exposure. In summary, these results suggest that ceramide selectively interacts with the alpha- and delta-isoforms of PKC in mesangial cells. Whereas PKC-alpha is activated with pronounced inhibition of hormone-stimulated phosphoinositide signaling, PKC-delta displays a decrease in its autophosphorylation, suggesting a negative role of ceramide binding on PKC-delta activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Azirines / metabolism*
  • Azirines / pharmacology
  • Binding Sites
  • Biological Transport / drug effects
  • Cell Membrane / enzymology
  • Cells, Cultured
  • Ceramides / metabolism*
  • Ceramides / pharmacology
  • Enzyme Activation / drug effects
  • Feedback / drug effects
  • Glomerular Mesangium / enzymology*
  • Glomerular Mesangium / metabolism
  • Isoenzymes / metabolism*
  • Membrane Proteins / metabolism
  • Molecular Sequence Data
  • Phosphatidylinositols / antagonists & inhibitors
  • Phosphatidylinositols / metabolism
  • Phosphorylation / drug effects
  • Photoaffinity Labels*
  • Protein Kinase C / metabolism*
  • Protein Kinase C-alpha
  • Protein Kinase C-delta
  • Rats

Substances

  • 3-trifluoromethyl-3-(3-iodophenyl)diazirineceramide
  • Azirines
  • Ceramides
  • Isoenzymes
  • Membrane Proteins
  • Phosphatidylinositols
  • Photoaffinity Labels
  • Prkcd protein, rat
  • Protein Kinase C
  • Protein Kinase C-alpha
  • Protein Kinase C-delta