Phorbol esters induce intracellular accumulation of the anti-apoptotic protein PED/PEA-15 by preventing ubiquitinylation and proteasomal degradation

J Biol Chem. 2007 Mar 23;282(12):8648-57. doi: 10.1074/jbc.M608359200. Epub 2007 Jan 16.

Abstract

Phosphoprotein enriched in diabetes/phosphoprotein enriched in astrocytes (PED/PEA)-15 is an anti-apoptotic protein whose expression is increased in several cancer cells and following experimental skin carcinogenesis. Exposure of untransfected C5N keratinocytes and transfected HEK293 cells to phorbol esters (12-O-tetradecanoylphorbol-13-acetate (TPA)) increased PED/PEA-15 cellular content and enhanced its phosphorylation at serine 116 in a time-dependent fashion. Ser-116 --> Gly (PED(S116G)) but not Ser-104 --> Gly (PED(S104G)) substitution almost completely abolished TPA regulation of PED/PEA-15 expression. TPA effect was also prevented by antisense inhibition of protein kinase C (PKC)-zeta and by the expression of a dominant-negative PKC-zeta mutant cDNA in HEK293 cells. Similar to long term TPA treatment, overexpression of wild-type PKC-zeta increased cellular content and phosphorylation of WT-PED/PEA-15 and PED(S104G) but not of PED(S116G). These events were accompanied by the activation of Ca2+-calmodulin kinase (CaMK) II and prevented by the CaMK blocker, KN-93. At variance, the proteasome inhibitor lactacystin mimicked TPA action on PED/PEA-15 intracellular accumulation and reverted the effects of PKC-zeta and CaMK inhibition. Moreover, we show that PED/PEA-15 bound ubiquitin in intact cells. PED/PEA-15 ubiquitinylation was reduced by TPA and PKC-zeta overexpression and increased by KN-93 and PKC-zeta block. Furthermore, in HEK293 cells expressing PED(S116G), TPA failed to prevent ubiquitin-dependent degradation of the protein. Accordingly, in the same cells, TPA-mediated protection from apoptosis was blunted. Taken together, our results indicate that TPA increases PED/PEA-15 expression at the post-translational level by inducing phosphorylation at serine 116 and preventing ubiquitinylation and proteosomal degradation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis Regulatory Proteins
  • Benzylamines / pharmacology
  • Calcium / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism
  • Gene Expression Regulation
  • Humans
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Phorbol Esters / chemistry*
  • Phorbol Esters / pharmacology
  • Phosphoproteins / metabolism*
  • Phosphorylation
  • Proteasome Endopeptidase Complex / metabolism*
  • Protein Binding
  • Protein Kinase C / chemistry
  • Protein Kinase Inhibitors / pharmacology
  • Protein Processing, Post-Translational
  • Sulfonamides / pharmacology
  • Tetradecanoylphorbol Acetate / chemistry
  • Ubiquitin / chemistry*
  • Ubiquitin / metabolism

Substances

  • Apoptosis Regulatory Proteins
  • Benzylamines
  • Intracellular Signaling Peptides and Proteins
  • PEA15 protein, human
  • Phorbol Esters
  • Phosphoproteins
  • Protein Kinase Inhibitors
  • Sulfonamides
  • Ubiquitin
  • KN 93
  • protein kinase C zeta
  • Protein Kinase C
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Proteasome Endopeptidase Complex
  • Tetradecanoylphorbol Acetate
  • Calcium