Protection from rapamycin-induced apoptosis by insulin-like growth factor-I is partially dependent on protein kinase C signaling

Cancer Res. 2010 Mar 1;70(5):2000-9. doi: 10.1158/0008-5472.CAN-09-3693. Epub 2010 Feb 23.

Abstract

Rapamycin-induced apoptosis in sarcoma cells is inhibited by insulin-like growth factor-I (IGF-I) through a signaling pathway independent of Ras-extracellular signal-regulated kinase 1/2 and Akt. IGF-I induces Bad phosphorylation (Ser112, Ser136, and Ser155) in a pathway involving phosphoinositide 3' kinase (PI3K) and protein kinase C (PKC; mu, epsilon, or theta) resulting in sequestering Bad from mitochondria and subsequently interacting with 14-3-3gamma in the cytosol. Gene knockdown of Bad, Bid, Akt1, Akt2, PKC-mu, PKC-epsilon, or PKC-theta was achieved by transient transfection using small interfering RNAs. Results indicate that IGF-I signaling to Bad requires activation of PI3K and PKC (mu, theta, epsilon) but not mTOR, Ras-extracellular signal-regulated kinase 1/2, protein kinase A, or p90(RSK). Wortmannin blocked the phosphorylation of PKC-mu (Ser744/Ser748), suggesting that PI3K is required for the activation of PKCs. PKCs phosphorylate Bad under in vitro conditions, and the association of phosphorylated Bad with PKC-mu or PKC-epsilon, as shown by immunoprecipitation, indicated direct involvement of PKCs in Bad phosphorylation. To confirm these results, cells overexpressing pEGFP-N1, wt-Bad, or Bad with a single site mutated (Ser112Ala; Ser136Ala; Ser155Ala), two sites mutated (Ser(112/136)Ala; Ser(112/155)Ala; Ser(136/155)Ala), or the triple mutant were tested. IGF-I protected completely against rapamycin-induced apoptosis in cells overexpressing wt-Bad and mutants having either one or two sites of phosphorylation mutated. Knockdown of Bid using small interfering RNA showed that Bid is not required for rapamycin-induced cell death. Collectively, these data suggest that IGF-I-induced phosphorylation of Bad at multiple sites via a pathway involving PI3K and PKCs is important for protecting sarcoma cells from rapamycin-induced apoptosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / metabolism
  • Apoptosis / drug effects*
  • Apoptosis / physiology
  • Cell Line, Tumor
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Epidermal Growth Factor / pharmacology
  • Humans
  • Insulin / pharmacology
  • Insulin-Like Growth Factor I / pharmacology*
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphorylation / drug effects
  • Platelet-Derived Growth Factor / pharmacology
  • Protein Kinase C / metabolism*
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / biosynthesis
  • Rhabdomyosarcoma / enzymology
  • Rhabdomyosarcoma / pathology
  • Sirolimus / pharmacology*
  • TOR Serine-Threonine Kinases
  • bcl-Associated Death Protein / metabolism

Substances

  • 14-3-3 Proteins
  • BAD protein, human
  • Insulin
  • Intracellular Signaling Peptides and Proteins
  • Platelet-Derived Growth Factor
  • Proto-Oncogene Proteins c-bcl-2
  • bcl-Associated Death Protein
  • Epidermal Growth Factor
  • Insulin-Like Growth Factor I
  • MTOR protein, human
  • Protein Serine-Threonine Kinases
  • TOR Serine-Threonine Kinases
  • Cyclic AMP-Dependent Protein Kinases
  • Protein Kinase C
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Sirolimus