Regulation of PDGF-stimulated SHIP2 tyrosine phosphorylation and association with Shc in 3T3-L1 preadipocytes

J Cell Physiol. 2007 Jun;211(3):598-607. doi: 10.1002/jcp.20965.

Abstract

In 3T3-L1 and human preadipocytes, insulin results in the isolated rise in phosphatidylinositol (PI)-3,4,5-P3, whereas PDGF produces PI(3,4)P2 in addition to PI(3,4,5)P3. SH2 domain-containing inositol 5-phosphatase 2 (SHIP2) converts PI(3,4,5)P3 into PI(3,4)P2. PDGF, but not insulin, stimulates SHIP2 tyrosine phosphorylation and its association with Shc in human and 3T3-L1 preadipocytes. We now demonstrate that SHIP2 tyrosine phosphorylation and association with Shc in PDGF-treated 3T3-L1 preadipocytes was reduced by bisindolylmaleimide I (BisI), an inhibitor of conventional/novel protein kinase C (PKC). However, the production of PI(3,4)P2 and PI(3,4,5)P3 by PDGF was unaffected by BisI. Activation of PKC by 12-O-tetradecanoylphorbol-13-acetate (TPA) was not sufficient to induce SHIP2 tyrosine phosphorylation. Furthermore, we identified threonine 958 (T958) as a novel PDGF-responsive SHIP2 phosphorylation site. Mutation of T958 to alanine reduced PDGF-stimulated SHIP2 tyrosine phosphorylation and association with Shc, but did not alter its anti-proliferative effect on preadipocytes. This study demonstrates that SHIP2 tyrosine phosphorylation and Shc association can be regulated by serine/threonine signaling pathways, either indirectly (via PKC), or directly (via T958). Interestingly, the anti-proliferative effect of SHIP2 T958A, as well as another SHIP2 mutant (Y986F, Y987F) that also displays defective tyrosine phosphorylation and Shc association, does not depend on these molecular events.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3-L1 Cells
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Adipocytes / cytology
  • Adipocytes / enzymology*
  • Amino Acid Substitution
  • Animals
  • Cell Division / physiology
  • Drug Interactions
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Indoles / pharmacology
  • Inositol Polyphosphate 5-Phosphatases
  • Maleimides / pharmacology
  • Mice
  • Mutagenesis, Site-Directed
  • Phosphatidylinositol Phosphates / metabolism
  • Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / metabolism*
  • Phosphorylation / drug effects
  • Platelet-Derived Growth Factor / pharmacology*
  • Protein Kinase C / metabolism
  • Shc Signaling Adaptor Proteins
  • Src Homology 2 Domain-Containing, Transforming Protein 1
  • Transfection
  • Tyrosine / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Enzyme Inhibitors
  • Indoles
  • Maleimides
  • Phosphatidylinositol Phosphates
  • Platelet-Derived Growth Factor
  • SHC1 protein, human
  • Shc Signaling Adaptor Proteins
  • Shc1 protein, mouse
  • Src Homology 2 Domain-Containing, Transforming Protein 1
  • phosphatidylinositol 3,4,5-triphosphate
  • phosphatidylinositol 3,4-diphosphate
  • Tyrosine
  • Protein Kinase C
  • Phosphoric Monoester Hydrolases
  • Inositol Polyphosphate 5-Phosphatases
  • INPPL1 protein, human
  • Inppl1 protein, mouse
  • Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases
  • bisindolylmaleimide I