GLUT4 is sorted to vesicles whose accumulation beneath and insertion into the plasma membrane are differentially regulated by insulin and selectively affected by insulin resistance

Molecular Biology of the Cell

Volumn 21, Issue 8, 2010, Pages 1375-1386

  Xiong, Wenyong ^a   Jordens, Ingrid ^a   Gonzalez, Eva ^a   McGraw, Timothy E ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL MEMBRANE TRANSPORT; CELL STRAIN 3T3; CELL VACUOLE; CONTROLLED STUDY; GLUCOSE TRANSPORT; INSULIN RESISTANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING;

3T3-L1 CELLS; ADIPOCYTES; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; ENDOCYTOSIS; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INSULIN; INSULIN RESISTANCE; MICE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; PROTEIN TRANSPORT; TRANSFERRIN; TRANSPORT VESICLES;

EID: 77950893000     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-08-0751     Document Type: Article

References (39)

1. Bai, L., Wang, Y., Fan, J., Chen, Y., Ji, W., Qu, A., Xu, P., James, D. E., and Xu, T. (2007). Dissecting multiple steps of GLUT4 trafficking and identifying the sites of insulin action. Cell Metab 5, 47-57. (Pubitemid 44939397)
2. Barnett, S. F., et al. (2005). Identification and characterization of pleckstrin-homology-domain-dependent and isoenzyme-specific Akt inhibitors. Biochem J. 385, 399-408. (Pubitemid 40165072)
3. Blot, V., and McGraw, T. E. (2008). Molecular mechanisms controlling GLUT4 intracellular retention. Mol. Biol. Cell 19, 3477-3487.
4. Brown, M. S., and Goldstein, J. L. (2008). Selective versus total insulin resistance: a pathogenic paradox. Cell Metab. 7, 95-96.
5. Brozinick, J. T., Jr., Berkemeier, B. A., and Elmendorf, J. S. (2007). "Actin"g on GLUT4, membrane and cytoskeletal components of insulin action. Curr. Diabet. Rev. 3, 111-122.
6. Chen, G., Liu, P., Pattar, G. R., Tackett, L., Bhonagiri, P., Strawbridge, A. B., and Elmendorf, J. S. (2006). Chromium activates glucose transporter 4 trafficking and enhances insulin-stimulated glucose transport in 3T3-L1 adipocytes via a cholesterol-dependent mechanism. Mol. Endocrinol. 20, 857-870.
7. Chen, G., Raman, P., Bhonagiri, P., Strawbridge, A. B., Pattar, G. R., and Elmendorf, J. S. (2004). Protective effect of phosphatidylinositol 4,5-bisphosphate against cortical filamentous actin loss and insulin resistance induced by sustained exposure of 3T3-L1 adipocytes to insulin. J. Biol. Chem. 279, 39705-39709.
8. Dugani, C. B., and Klip, A. (2005). Glucose transporter 4, cycling, compartments and controversies. EMBO Rep. 6, 1137-1142.
9. Eguez, L., Lee, A., Chavez, J. A., Miinea, C. P., Kane, S., Lienhard, G. E., and McGraw, T. E. (2005). Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein. Cell Metab. 2, 263-272.
10. Gonzalez, E., and McGraw, T. E. (2006). Insulin signaling diverges into Akt-dependent and -independent signals to regulate the recruitment/docking and the fusion of GLUT4 vesicles to the plasma membrane. Mol. Biol. Cell 17, 4484-4493.
11. Govers, R., Coster, A. C., and James, D. E. (2004). Insulin increases cell surface GLUT4 levels by dose dependently discharging GLUT4 into a cell surface recycling pathway. Mol. Cell. Biol. 24, 6456-6466.
12. Hoehn, K. L., Hohnen-Behrens, C., Cederberg, A., Wu, L. E., Turner, N., Yuasa, T., Ebina, Y., and James, D. E. (2008). IRS1-independent defects define major nodes of insulin resistance. Cell Metab. 7, 421-433. (Pubitemid 351598028)
13. Huang, P., Altshuller, Y. M., Hou, J. C., Pessin, J. E., and Frohman, M. A. (2005). Insulin-stimulated plasma membrane fusion of Glut4 glucose transporter-containing vesicles is regulated by phospholipase D1. Mol. Biol. Cell 16, 2614-2623.
14. Huang, S., and Czech, M. P. (2007). The GLUT4 glucose transporter. Cell Metab. 5, 237-252.
15. Huang, S., Lifshitz, L. M., Jones, C., Bellve, K. D., Standley, C., Fonseca, S., Corvera, S., Fogarty, K. E., and Czech, M. P. (2007). Insulin stimulates membrane fusion and GLUT4 accumulation in clathrin coats on adipocyte plasma membranes. Mol. Cell. Biol. 27, 3456-3469.
16. Jess, T. J., Belham, C. M., Thomson, F. J., Scott, P. H., Plevin, R. J., and Gould, G. W. (1996). Phosphatidylinositol 3′-kinase, but not p70 ribosomal S6 kinase, is involved in membrane protein recycling: wortmannin inhibits glucose transport and downregulates cell-surface transferrin receptor numbers independently of any effect on fluid-phase endocytosis in fibroblasts. Cell Signal. 8, 297-304.
17. Jiang, L., Fan, J., Bai, L., Wang, Y., Chen, Y., Yang, L., Chen, L., and Xu, T. (2008). Direct quantification of fusion rate reveals a distal role for AS160 in insulin-stimulated fusion of GLUT4 storage vesicles. J. Biol. Chem. 283, 8508-8516.
18. Kandror, K. V., and Pilch, P. F. (1994). gp160, a tissue-specific marker for insulin-activated glucose transport. Proc. Natl. Acad. Sci. USA 91, 8017-8021.
19. Karylowski, O., Zeigerer, A., Cohen, A., and McGraw, T. E. (2004). GLUT4 is retained by an intracellular cycle of vesicle formation and fusion with endosomes. Mol. Biol. Cell 15, 870-882.
20. Keller, S. R., Scott, H. M., Mastick, C. C., Aebersold, R., and Lienhard, G. E. (1995). Cloning and characterization of a novel insulin-regulated membrane aminopeptidase from Glut4 vesicles [published erratum appears in J. Biol. Chem. 1995 Dec 15; 270(50):30236]. J. Biol. Chem. 270, 23612-23618.
21. Klip, A. (2009). The many ways to regulate glucose transporter 4. Appl. Physiol. Nutr. Metab. 34, 481-487.
22. Lampson, M. A., Racz, A., Cushman, S. W., and McGraw, T. E. (2000). Demonstration of insulin-responsive trafficking of GLUT4 and vpTR in fibroblasts. J. Cell Sci. 113(Pt 22), 4065-4076. (Pubitemid 32194531)
23. Lampson, M. A., Schmoranzer, J., Zeigerer, A., Simon, S. M., and McGraw, T. E. (2001). Insulin-regulated release from the endosomal recycling compartment is regulated by budding of specialized vesicles. Mol. Biol. Cell 12, 3489-3501.
24. Larance, M., et al. (2005). Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J. Biol. Chem. 280, 37803-37813.
25. Lizunov, V. A., Matsumoto, H., Zimmerberg, J., Cushman, S. W., and Frolov, V. A. (2005). Insulin stimulates the halting, tethering, and fusion of mobile GLUT4 vesicles in rat adipose cells. J. Cell Biol. 169, 481-489. (Pubitemid 40686698)
26. Lopez, J. A., Burchfield, J. G., Blair, D. H., Mele, K., Ng, Y., Vallotton, P., James, D. E., and Hughes, W. E. (2009). Identification of a distal GLUT4 trafficking event controlled by actin polymerization. Mol. Biol. Cell 17, 3918-3929.
27. Maianu, L., Keller, S. R., and Garvey, W. T. (2001). Adipocytes exhibit abnormal subcellular distribution and translocation of vesicles containing glucose transporter 4 and insulin-regulated aminopeptidase in type 2 diabetes mellitus: implications regarding defects in vesicle trafficking. J. Clin. Endocrinol. Metab. 86, 5450-5456.
28. Marsh, B. J., Martin, S., Melvin, D. R., Martin, L. B., Alm, R. A., Gould, G. W., and James, D. E. (1998). Mutational analysis of the carboxy-terminal phosphorylation site of GLUT-4 in 3T3-L1 adipocytes. Am. J. Physiol. 275, E412-E422.
29. Martin, O. J., Lee, A., and McGraw, T. E. (2006). GLUT4 distribution between the plasma membrane and the intracellular compartments is maintained by an insulin-modulated bipartite dynamic mechanism. J. Biol. Chem. 281, 484-490.
30. Martin, S., Tellam, J., Livingstone, C., Slot, J. W., Gould, G. W., and James, D. E. (1996). The glucose transporter (GLUT-4) and vesicle-associated membrane protein-2 (VAMP-2) are segregated from recycling endosomes in insulin-sensitive cells. J. Cell Biol. 134, 625-635. (Pubitemid 26269136)
31. McCarthy, A. M., Spisak, K. O., Brozinick, J. T., and Elmendorf, J. S. (2006). Loss of cortical actin filaments in insulin-resistant skeletal muscle cells impairs GLUT4 vesicle trafficking and glucose transport. Am. J. Physiol. Cell Physiol. 291, C860-C868.
32. Randhawa, V. K., Ishikura, S., Talior-Volodarsky, I., Cheng, A. W., Patel, N., Hartwig, J. H., and Klip, A. (2008). GLUT4 vesicle recruitment and fusion are differentially regulated by Rac, AS160, and Rab8A in muscle cells. J. Biol. Chem. 283, 27208-27219.
33. Sano, H., Eguez, L., Teruel, M., Fukuda, M., Chuang, T., Chavez, J., Lienhard, G., and McGraw, T. (2007). Rab10 is a target of the insulin regulated AS160 rabGAP protein required for insulin-stimulated translocation of GLUT4 to the plasma membrane of adipocytes. Cell Metab. 5, 293-303. (Pubitemid 46477855)
34. Sano, H., Kane, S., Sano, E., Miinea, C. P., Asara, J. M., Lane, W. S., Garner, C. W., and Lienhard, G. E. (2003). Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J. Biol. Chem. 278, 14599-14602.
35. Shi, J., and Kandror, K. V. (2005). Sortilin is essential and sufficient for the formation of Glut4 storage vesicles in 3T3-L1 adipocytes. Dev. Cell 9, 99-108. (Pubitemid 40903663)
36. Watson, R. T., and Pessin, J. E. (2007). GLUT4 translocation: the last 200 nanometers. Cell Signal. 19, 2209-2217.
37. Zeigerer, A., Lampson, M., Karylowski, O., Sabatini, D., Adesnik, M., Ren, M., and McGraw, T. (2002). GLUT4 retention in adipocytes requires two intracellular insulin-regulated transport steps. Mol. Biol. Cell 13, p2421-p2435.
38. Zeigerer, A., McBrayer, M. K., and McGraw, T. E. (2004). Insulin stimulation of GLUT4 exocytosis, but not its inhibition of endocytosis, is dependent on RabGAP AS160. Mol. Biol. Cell 15, 4406-4415.
39. Zhao, P., Yang, L., Lopez, J. A., Fan, J., Burchfield, J. G., Bai, L., Hong, W., Xu, T., and James, D. E. (2009). Variations in the requirement for v-SNAREs in GLUT4 trafficking in adipocytes. J. Cell Sci. 122, 3472-3480.