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The adipocyte plasma membrane caveolin functional/structural organization is necessary for the efficient endocytosis of GLUT4.
J Biol Chem. 2003 Mar 21; 278(12):10683-90.JB

Abstract

It is well established that insulin stimulation of glucose uptake requires the translocation of intracellular localized GLUT4 protein to the cell surface membrane. This plasma membrane-redistributed GLUT4 protein was partially co-localized with caveolin as determined by confocal fluorescent microscopy but was fully excluded from lipid rafts based upon Triton X-100 extractability. Cholesterol depletion with methyl-beta-cyclodextrin, filipin, or cholesterol oxidase resulted in an insulin-independent increase in the amount of plasma membrane-localized GLUT4 that was fully reversible by cholesterol replenishment. This basal accumulation of cell surface GLUT4 occurred due to an inhibition of GLUT4 endocytosis. However, this effect was not specific since cholesterol extraction also resulted in a dramatic inhibition of clathrin-mediated endocytosis as assessed by transferrin receptor internalization. To functionally distinguish between caveolin- and clathrin-dependent endocytic processes, we took advantage of a dominant-interfering caveolin 1 mutant (Cav1/S80E) that specifically disrupts caveolae organization. Expression of Cav1/S80E, but not the wild type (Cav1/WT) or Cav1/S80A mutant, inhibited cholera toxin B internalization without any significant effect on transferrin receptor endocytosis. In parallel, Cav1/S80E expression increased the amount of plasma membrane-localized GLUT4 protein in an insulin-independent manner. Although Cav1/S80E also decreased GLUT4 endocytosis, the extent of GLUT4 internalization was only partially reduced (approximately 40%). In addition, expression of Cav1/WT and Cav1/S80A enhanced GLUT4 endocytosis by approximately 20%. Together, these data indicate that the endocytosis of GLUT4 requires clathrin-mediated endocytosis but that the higher order structural organization of plasma membrane caveolin has a significant influence on this process.

Authors+Show Affiliations

Department of Physiology and Biophysics, The University of Iowa, Iowa City 52242, USA.No affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, P.H.S.

Language

eng

PubMed ID

12496259

Citation

Shigematsu, Satoshi, et al. "The Adipocyte Plasma Membrane Caveolin Functional/structural Organization Is Necessary for the Efficient Endocytosis of GLUT4." The Journal of Biological Chemistry, vol. 278, no. 12, 2003, pp. 10683-90.
Shigematsu S, Watson RT, Khan AH, et al. The adipocyte plasma membrane caveolin functional/structural organization is necessary for the efficient endocytosis of GLUT4. J Biol Chem. 2003;278(12):10683-90.
Shigematsu, S., Watson, R. T., Khan, A. H., & Pessin, J. E. (2003). The adipocyte plasma membrane caveolin functional/structural organization is necessary for the efficient endocytosis of GLUT4. The Journal of Biological Chemistry, 278(12), 10683-90.
Shigematsu S, et al. The Adipocyte Plasma Membrane Caveolin Functional/structural Organization Is Necessary for the Efficient Endocytosis of GLUT4. J Biol Chem. 2003 Mar 21;278(12):10683-90. PubMed PMID: 12496259.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The adipocyte plasma membrane caveolin functional/structural organization is necessary for the efficient endocytosis of GLUT4. AU - Shigematsu,Satoshi, AU - Watson,Robert T, AU - Khan,Ahmir H, AU - Pessin,Jeffrey E, Y1 - 2002/12/20/ PY - 2002/12/24/pubmed PY - 2003/5/6/medline PY - 2002/12/24/entrez SP - 10683 EP - 90 JF - The Journal of biological chemistry JO - J. Biol. Chem. VL - 278 IS - 12 N2 - It is well established that insulin stimulation of glucose uptake requires the translocation of intracellular localized GLUT4 protein to the cell surface membrane. This plasma membrane-redistributed GLUT4 protein was partially co-localized with caveolin as determined by confocal fluorescent microscopy but was fully excluded from lipid rafts based upon Triton X-100 extractability. Cholesterol depletion with methyl-beta-cyclodextrin, filipin, or cholesterol oxidase resulted in an insulin-independent increase in the amount of plasma membrane-localized GLUT4 that was fully reversible by cholesterol replenishment. This basal accumulation of cell surface GLUT4 occurred due to an inhibition of GLUT4 endocytosis. However, this effect was not specific since cholesterol extraction also resulted in a dramatic inhibition of clathrin-mediated endocytosis as assessed by transferrin receptor internalization. To functionally distinguish between caveolin- and clathrin-dependent endocytic processes, we took advantage of a dominant-interfering caveolin 1 mutant (Cav1/S80E) that specifically disrupts caveolae organization. Expression of Cav1/S80E, but not the wild type (Cav1/WT) or Cav1/S80A mutant, inhibited cholera toxin B internalization without any significant effect on transferrin receptor endocytosis. In parallel, Cav1/S80E expression increased the amount of plasma membrane-localized GLUT4 protein in an insulin-independent manner. Although Cav1/S80E also decreased GLUT4 endocytosis, the extent of GLUT4 internalization was only partially reduced (approximately 40%). In addition, expression of Cav1/WT and Cav1/S80A enhanced GLUT4 endocytosis by approximately 20%. Together, these data indicate that the endocytosis of GLUT4 requires clathrin-mediated endocytosis but that the higher order structural organization of plasma membrane caveolin has a significant influence on this process. SN - 0021-9258 UR - https://www.unboundmedicine.com/medline/citation/12496259/The_adipocyte_plasma_membrane_caveolin_functional/structural_organization_is_necessary_for_the_efficient_endocytosis_of_GLUT4_ L2 - http://www.jbc.org/cgi/pmidlookup?view=long&pmid=12496259 DB - PRIME DP - Unbound Medicine ER -