Abundance, localization, and insulin-induced translocation of glucose transporters in red and white muscle

A. Marette, J. M. Richardson, T. Ramlal, T. W. Balon, M. Vranic, Jeffrey E. Pessin, A. Klip

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Abstract

D-Glucose protectable cytochalasin B (CB) binding to subcellular membrane fractions was used to determine glucose transporter number in red (quadriceps-gastrocnemius-soleus) and white (quadriceps-gastrocnemius) rat muscle. CB binding was twofold higher in isolated plasma membranes of red than of white muscle. In contrast, the number of transporters in an isolated insulin-sensitive intracellular membrane organelle was similar in the two muscle groups. Immunoblotting and immunofluorescence microscopy with anti- GLUT4 and anti-GLUT1 antibodies indicated that both GLUT1 and GLUT4 transporter isoforms account for the higher abundance of CB binding sites in plasma membranes of red than of white muscle. Immunofluorescence localized GLUT4 to both the surface and the interior of the muscle cell and demonstrated that type I (slow twitch oxidative) and type IIa (fast twitch oxidative-glycolytic) fibers are enriched in GLUT4 protein compared with type IIb (fast twitch glycolytic) fibers. In contrast, GLUT1 reactivity was restricted to the surface of the muscle cell and was also highly enriched in the perineurial sheaths of peripheral nerves and the capsules of muscle spindles present in both red and white muscles. Insulin caused a twofold increase in CB binding in isolated plasma membranes of red or white muscles with a corresponding 40-50% decrease in CB binding in isolated intracellular membranes. These changes in CB binding were paralleled by similar changes in the membrane distribution of the GLUT4 glucose transporter isoform and in glucose transport activity measured after insulin perfusion of hindquarter muscles. In contrast, insulin did not change the distribution of either GLUT1 glucose transporters or Na+-K+-ATPase α1-subunits. The molar ratio of GLUT4 to GLUT1 in red and white muscle plasma membranes was found to be 4:1 in the basal state and 7:1 in the insulin-stimulated state. These results indicate that red muscle contains a higher amount of GLUT1 and GLUT4 transporters at the plasma membrane than white muscle in the basal and insulin-stimulated states but that GLUT4 translocation does not differ between muscle types. In addition, GLUT4 expression correlates with the metabolic nature (oxidative vs. glycolytic) of skeletal muscle fibers, rather than with their contractile properties (slow twitch vs. fast twitch).

Original languageEnglish (US)
JournalAmerican Journal of Physiology - Cell Physiology
Volume263
Issue number2 32-2
StatePublished - 1992
Externally publishedYes

Fingerprint

Facilitative Glucose Transport Proteins
Muscle
Cytochalasin B
Insulin
Muscles
Cell Membrane
Cell membranes
Intracellular Membranes
Muscle Cells
Membranes
Protein Isoforms
Glucose Transporter Type 4
Muscle Spindles
Glucose
Subcellular Fractions
Fibers
Skeletal Muscle Fibers
Peripheral Nerves
Fluorescence Microscopy
Cells

Keywords

  • glucose transport
  • GLUT1
  • GLUT4
  • immunofluorescence microscopy
  • insulin action
  • muscle fibers
  • skeletal muscle

ASJC Scopus subject areas

  • Cell Biology
  • Clinical Biochemistry
  • Physiology

Cite this

Abundance, localization, and insulin-induced translocation of glucose transporters in red and white muscle. / Marette, A.; Richardson, J. M.; Ramlal, T.; Balon, T. W.; Vranic, M.; Pessin, Jeffrey E.; Klip, A.

In: American Journal of Physiology - Cell Physiology, Vol. 263, No. 2 32-2, 1992.

Research output: Contribution to journalArticle

Marette, A. ; Richardson, J. M. ; Ramlal, T. ; Balon, T. W. ; Vranic, M. ; Pessin, Jeffrey E. ; Klip, A. / Abundance, localization, and insulin-induced translocation of glucose transporters in red and white muscle. In: American Journal of Physiology - Cell Physiology. 1992 ; Vol. 263, No. 2 32-2.
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AU - Richardson, J. M.

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AU - Vranic, M.

AU - Pessin, Jeffrey E.

AU - Klip, A.

PY - 1992

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N2 - D-Glucose protectable cytochalasin B (CB) binding to subcellular membrane fractions was used to determine glucose transporter number in red (quadriceps-gastrocnemius-soleus) and white (quadriceps-gastrocnemius) rat muscle. CB binding was twofold higher in isolated plasma membranes of red than of white muscle. In contrast, the number of transporters in an isolated insulin-sensitive intracellular membrane organelle was similar in the two muscle groups. Immunoblotting and immunofluorescence microscopy with anti- GLUT4 and anti-GLUT1 antibodies indicated that both GLUT1 and GLUT4 transporter isoforms account for the higher abundance of CB binding sites in plasma membranes of red than of white muscle. Immunofluorescence localized GLUT4 to both the surface and the interior of the muscle cell and demonstrated that type I (slow twitch oxidative) and type IIa (fast twitch oxidative-glycolytic) fibers are enriched in GLUT4 protein compared with type IIb (fast twitch glycolytic) fibers. In contrast, GLUT1 reactivity was restricted to the surface of the muscle cell and was also highly enriched in the perineurial sheaths of peripheral nerves and the capsules of muscle spindles present in both red and white muscles. Insulin caused a twofold increase in CB binding in isolated plasma membranes of red or white muscles with a corresponding 40-50% decrease in CB binding in isolated intracellular membranes. These changes in CB binding were paralleled by similar changes in the membrane distribution of the GLUT4 glucose transporter isoform and in glucose transport activity measured after insulin perfusion of hindquarter muscles. In contrast, insulin did not change the distribution of either GLUT1 glucose transporters or Na+-K+-ATPase α1-subunits. The molar ratio of GLUT4 to GLUT1 in red and white muscle plasma membranes was found to be 4:1 in the basal state and 7:1 in the insulin-stimulated state. These results indicate that red muscle contains a higher amount of GLUT1 and GLUT4 transporters at the plasma membrane than white muscle in the basal and insulin-stimulated states but that GLUT4 translocation does not differ between muscle types. In addition, GLUT4 expression correlates with the metabolic nature (oxidative vs. glycolytic) of skeletal muscle fibers, rather than with their contractile properties (slow twitch vs. fast twitch).

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KW - glucose transport

KW - GLUT1

KW - GLUT4

KW - immunofluorescence microscopy

KW - insulin action

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KW - skeletal muscle

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