Insulin-independent and wortmannin-resistant targeting of IRS-3 to the plasma membrane via its pleckstrin homology domain mediates a different interaction with the insulin receptor from that of IRS-1

Diabetologia. 2001 Aug;44(8):992-1004. doi: 10.1007/s001250100587.

Abstract

Aims/hypothesis: In primary adipocytes, although IRS-1 and IRS-3 are expressed in comparable amounts, these proteins manifest distinct distribution and significance in insulin signalling. We investigated the molecular basis of the difference between these two proteins.

Methods: In Cos-1 cells transiently expressing rat IRS-1, IRS-3, or chimeric proteins of these two proteins we examined the tyrosine phosphorylation via the wild-type or mutant insulin receptors and evaluated their targeting to the plasma membrane by immunostaining the membrane ghost.

Results: In contrast to IRS-1, IRS-3 was tyrosine-phosphorylated by the insulin receptor altering Tyr960 to Phe (Y960F), which disrupts the binding site of the PTB domain of IRSs, to an extent comparable to the wild-type receptor. The tyrosine phosphorylation of IRS-3 with the PH domain replacement via the Y960F insulin receptor markedly decreased, whereas that of IRS-3 with the PTB domain alteration was mildly impaired. Insulin-stimulated translocation of IRS-1 to the plasma membrane, as well as that of IRS-3 with the PH domain replacement, was wortmannin-sensitive, although that of IRS-3 was insulin-independent and wortmannin-resistant.

Conclusions/interpretation: The affinity of the PH domain for the phospholipids in the plasma membrane seems to influence the receptor-substrate interaction required for IRS tyrosine phosphorylation, indicating that the PH domain and the PTB domain of IRSs cooperatively function in insulin-stimulated tyrosine phosphorylation of these proteins.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Androstadienes / pharmacology*
  • Animals
  • Binding Sites
  • Blood Proteins / chemistry
  • Blood Proteins / genetics*
  • COS Cells / metabolism
  • Drug Resistance
  • Electrophoresis, Polyacrylamide Gel
  • Enzyme Inhibitors / pharmacology
  • Gene Expression
  • Humans
  • Insulin / pharmacology*
  • Insulin Receptor Substrate Proteins
  • Mice
  • Mutagenesis, Site-Directed
  • Phosphoproteins / chemistry
  • Phosphoproteins / genetics*
  • Phosphoproteins / metabolism*
  • Phosphorylation
  • Phosphotyrosine / metabolism
  • Protein Kinase Inhibitors
  • Rabbits
  • Receptor, Insulin / genetics
  • Receptor, Insulin / metabolism*
  • Sequence Homology
  • Structure-Activity Relationship
  • Transfection
  • Wortmannin

Substances

  • Androstadienes
  • Blood Proteins
  • Enzyme Inhibitors
  • IRS1 protein, human
  • IRS3P protein, human
  • Insulin
  • Insulin Receptor Substrate Proteins
  • Irs1 protein, mouse
  • Irs1 protein, rat
  • Irs3 protein, mouse
  • Irs3 protein, rat
  • Phosphoproteins
  • Protein Kinase Inhibitors
  • platelet protein P47
  • Phosphotyrosine
  • Receptor, Insulin
  • Wortmannin