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J Biol Chem, Vol. 273, Issue 19, 11548-11555, May 8, 1998
From the Research Division, Joslin Diabetes Center and Department
of Medicine, Harvard Medical School, Boston, Massachusetts 02215
The ability of the insulin receptor to
phosphorylate multiple substrates and their subcellular localization
are two of the determinants that contribute to diversity of signaling.
We find that insulin receptor substrate (IRS)-1 is 2-fold more
concentrated in the intracellular membrane (IM) compartment than in
cytosol, whereas IRS-2 is 2-fold more concentrated in cytosol than in
IM. Insulin stimulation induces rapid tyrosine phosphorylation of both
IRS-1 and IRS-2. This occurs mainly in the IM compartment, even though
IRS-2 is located predominantly in cytosol. Furthermore, after insulin
stimulation, both IRS-1 and IRS-2 translocate from IM to cytosol with a
t1/2 of 3.5 min. Using an in
vitro reconstitution assay, we have demonstrated an association
between IRS-1 and internal membranes and have shown that the
dissociation of IRS-1 from IM is dependent on serine/threonine
phosphorylation of IM. By comparison, within 1 min after insulin
stimulation, 40% of the total pool of the 85-kDa subunit of
phosphatidylinositol 3-kinase (p85) is recruited from cytosol to IM,
the greater part of which can be accounted for by binding to IRS-1
present in the IM. The p85 binding and phosphatidylinositol 3-kinase
activity associated with IRS-2 rapidly decrease in both IM and cytosol,
whereas those associated with IRS-1 stay at a relatively high level in
IM and increase with time in cytosol despite a return of p85 to the
cytosol and decreasing tyrosine phosphorylation of cytosolic IRS-1.
These data indicate that IRS-1 and IRS-2 are differentially distributed in the cell and move from IM to cytosol following insulin stimulation. Insulin-stimulated IRS-1 and IRS-2 signaling occurs mainly in the IM
and shows different kinetics; IRS-1-mediated signaling is more stable,
whereas IRS-2-mediated signaling is more transient. These differences
in substrate utilization and compartmentalization may contribute to the
complexity and diversity of the insulin signaling network.
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