PKC-mediated phosphorylation regulates c-FLIP ubiquitylation and stability

Cell Death Differ. 2009 Sep;16(9):1215-26. doi: 10.1038/cdd.2009.35. Epub 2009 Apr 3.

Abstract

Cellular FLICE-inhibitory protein (c-FLIP) proteins are crucial regulators of the death-inducing signaling complex (DISC) and caspase-8 activation. To date, three c-FLIP isoforms with distinct functions and regulation have been identified. Our previous studies have shown that the stability of c-FLIP proteins is subject to isoform-specific regulation, but the underlying molecular mechanisms have not been known. Here, we identify serine 193 as a novel in vivo phosphorylation site of all c-FLIP proteins and demonstrate that S193 phosphorylation selectively influences the stability of the short c-FLIP isoforms, as S193D mutation inhibits the ubiquitylation and selectively prolongs the half-lives of c-FLIP short (c-FLIP(S)) and c-FLIP Raji (c-FLIP(R)). S193 phosphorylation also decreases the ubiquitylation of c-FLIP long (c-FLIP(L)) but, surprisingly, does not affect its stability, indicating that S193 phosphorylation has a different function in c-FLIP(L). The phosphorylation of this residue is operated by the protein kinase C (PKC), as S193 phosphorylation is markedly increased by treatment with 12-O-tetradecanoylphorbol-13-acetate and decreased by inhibition of PKCalpha and PKCbeta. S193 mutations do not affect the ability of c-FLIP to bind to the DISC, although S193 phosphorylation is increased by death receptor stimulation. Instead, S193 phosphorylation affects the intracellular level of c-FLIP(S), which then determines the sensitivity to death-receptor-mediated apoptosis. These results reveal that the differential stability of c-FLIP proteins is regulated in an isoform-specific manner by PKC-mediated phosphorylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis
  • CASP8 and FADD-Like Apoptosis Regulating Protein / metabolism*
  • Caspase 8 / metabolism
  • Cell Line, Tumor
  • Humans
  • K562 Cells
  • Mutation
  • Phosphorylation
  • Protein Isoforms / metabolism
  • Protein Kinase C / metabolism*
  • TNF-Related Apoptosis-Inducing Ligand / pharmacology
  • Tetradecanoylphorbol Acetate / pharmacology
  • Ubiquitination

Substances

  • CASP8 and FADD-Like Apoptosis Regulating Protein
  • Protein Isoforms
  • TNF-Related Apoptosis-Inducing Ligand
  • Protein Kinase C
  • Caspase 8
  • Tetradecanoylphorbol Acetate