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J Biol Chem, Vol. 274, Issue 36, 25210-25217, September 3, 1999
From the Boston University School of Medicine, Boston,
Massachusetts 02118
Rat adipocytes were biotinylated with
cell-impermeable reagents,
sulfo-N-hydroxysuccinimide-biotin and
sulfo-N-hydroxysuccinimide-S-S-biotin in the absence
and presence of insulin. Biotinylated and nonbiotinylated populations of the insulin-like growth factor-II/mannose 6-phosphate receptor, the transferrin receptor, and insulin-responsive
aminopeptidase were separated by adsorption to streptavidin-agarose to
determine the percentage of the biotinylated protein molecules
versus their total amount in different subcellular
compartments. Results indicate that adipose cells possess at least two
distinct cell surface recycling pathways for insulin-like growth
factor-II/mannose 6-phosphate receptor (MPR) and transferrin receptor
(TfR): one which is mediated by glucose transporter isoform
4(Glut4)-vesicles and another that bypasses this compartment. Under
basal conditions, the first pathway is not active, and cell surface
recycling of TfR and, to a lesser extent, MPR proceeds via
the second pathway. Insulin dramatically stimulates recycling through
the first pathway and has little effect on the second.
Within the Glut4-containing compartment, insulin has profoundly
different effects on intracellular trafficking of insulin-responsive aminopeptidase on one hand and MPR and TfR on the other. After insulin administration, insulin-responsive aminopeptidase is
redistributed from Glut4-containing vesicles to the plasma
membrane and stays there for at least 30 min with minimal detectable
internalization and recycling, whereas MPR and TfR rapidly shuttle
between Glut4 vesicles and the plasma membrane in such a way that after
30 min of insulin treatment, virtually every receptor molecule in this compartment completes at least one trafficking cycle to the cell surface. Thus, different recycling proteins, which compose
Glut4-containing vesicles, are internalized into this compartment at
their own distinctive rates.
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