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Vol. 11, Issue 12, 4079-4091, December 2000
and
*Department of Cell Biology, Faculty of Medicine and Institute of
Biomembranes, Utrecht University, 3584 CX Utrecht, The Netherlands; and
Insulin treatment of fat cells results in the translocation of the
insulin-responsive glucose transporter type 4, GLUT4, from intracellular compartments to the plasma membrane. However, the precise
nature of these intracellular GLUT4-carrying compartments is debated.
To resolve the nature of these compartments, we have performed an
extensive morphological analysis of GLUT4-containing compartments,
using a novel immunocytochemical technique enabling high labeling
efficiency and 3-D resolution of cytoplasmic rims isolated
from rat epididymal adipocytes. In basal cells, GLUT4 was localized to
three morphologically distinct intracellular structures: small
vesicles, tubules, and vacuoles. In response to insulin the increase of
GLUT4 at the cell surface was compensated by a decrease in small
vesicles, whereas the amount in tubules and vacuoles was unchanged.
Under basal conditions, many small GLUT4 positive vesicles also
contained IRAP (88%) and the v-SNARE, VAMP2 (57%) but not markers of
sorting endosomes (EEA1), late endosomes, or lysosomes (lgp120). A
largely distinct population of GLUT4 vesicles (56%) contained the
cation-dependent mannose 6-phosphate receptor (CD-MPR), a marker
protein that shuttles between endosomes and the trans-Golgi network
(TGN). In response to insulin, GLUT4 was recruited both from VAMP2 and
CD-MPR positive vesicles. However, while the concentration of GLUT4 in
the remaining VAMP2-positive vesicles was unchanged, the concentration
of GLUT4 in CD-MPR-positive vesicles decreased. Taken together, we
provide morphological evidence indicating that, in response to insulin, GLUT4 is recruited to the plasma membrane by fusion of preexisting VAMP2-carrying vesicles as well as by sorting from the dynamic endosomal-TGN system.
Centre for Molecular and Cellular Biology, University of
Queensland, St. Lucia, Brisbane, QLD 4072, Australia
Corresponding author. E-mail address:
w.stoorvogel{at}lab.azu.nl
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