Insulin but not PDGF relies on actin remodeling and on VAMP2 for GLUT4 translocation in myoblasts

Journal of Cell Science

Volumn 117, Issue 22, 2004, Pages 5447-5455

  Török, Dòra ^a   Patel, Nish ^a,b   JeBailey, Lellean ^a,b   Thong, Farah S L ^a   Randhawa, Varinder K ^a,b   Klip, Amira ^a,b   Rudich, Assaf ^a,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Actin; GLUT4; Insulin; PDGF; VAMP2

Indexed keywords

ACTIN; CYTOCHALASIN D; GLUCOSE TRANSPORTER 4; INSULIN; JASPAMIDE; LATRUNCULIN B; MYC PROTEIN; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE B; SNARE PROTEIN; SYNAPTOBREVIN 2; TETANUS TOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CELL STIMULATION; CELL STRAIN; CELL SURFACE; CONTROLLED STUDY; CYTOSKELETON; ENDOCYTOSIS; ENZYME PHOSPHORYLATION; EXOCYTOSIS; GENE TRANSLOCATION; GENETIC TRANSFECTION; MOLECULAR STABILITY; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RAT; SENSITIVITY ANALYSIS; STATISTICAL ANALYSIS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTINS; ANIMALS; CELL LINE; CYTOSKELETON; EXOCYTOSIS; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; IMMUNOBLOTTING; INSULIN; INSULIN RESISTANCE; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MONOSACCHARIDE TRANSPORT PROTEINS; MUSCLE PROTEINS; MUSCLES; PLATELET-DERIVED GROWTH FACTOR; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; R-SNARE PROTEINS; RATS; TETANUS TOXIN; TIME FACTORS; TRANSFECTION; VESICLE-ASSOCIATED MEMBRANE PROTEIN 3;

ANIMALIA;

EID: 9444259803     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01421     Document Type: Article

References (41)

1. Cheatham, B., Vlahos, C. J., Cheatham, L., Wang, L., Blenis, J. and Kahn, C. R. (1994). Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase, DNA synthesis, and glucose transporter translocation. Mol. Cell. Biol. 14, 4902-4911.
2. Clark, S. F., Martin, S., Carozzi, A. J., Hill, M. M. and James, D. E. (1998). Intracellular localization of phosphatidylinositide 3-kinase and insulin receptor substrate-1 in adipocytes, potential involvement of a membrane skeleton. J. Cell Biol. 140, 1211-1225.
3. Evans, J. L., Honer, C. M., Womelsdorf, B. E., Kaplan, E. L. and Bell, P. A. (1995). The effects of wortmannin, a potent inhibitor of phosphatidylinositol 3-kinase, on insulin-stimulated glucose transport, GLUT4 translocation, antilipolysis, and DNA synthesis. Cell. Signal. 7, 365-376.
4. Fiaschi, T., Chiarugi, P., Buricchi, F., Giannoni, E., Taddei, M. L., Magnelli, L., Cozzi, G., Raugei, G. and Ramponi, G. (2003). Down-regulation of platelet-derived growth factor receptor signaling during myogenesis. Cell. Mol. Life Sci. 60, 2721-2735.
5. Foster, L. J., Li, D., Randhawa, V. K. and Klip, A. (2001). Insulin accelerates inter-endosomal GLUT4 traffic via phosphatidylinositol 3-kinase and protein kinase B. J. Biol. Chem. 276, 44212-44221.
6. Garvey, W. T., Maianu, L., Zhu, J. H., Brechtel-Hook, G., Wallace, P. and Baron, A. D. (1998). Evidence for defects in the trafficking and translocation of GLUT4 glucose transporters in skeletal muscle as a cause of human insulin resistance. J. Clin. Invest. 101, 2377-2386.
7. Guilherme, A. and Czech, M. P. (1998). Stimulation of IRS-1-associated phosphatidylinositol 3-kinase and Akt/protein kinase B but not glucose transport by beta1-integrin signaling in rat adipocytes. J. Biol. Chem. 273, 33119-33122.
8. Heldin, C. H. and Westermark, B. (1999). Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 79, 1283-1316.
9. Hooshmand-Rad, R., Hajkova, L., Klint, P., Karlsson, R., Vanhaesebroeck, B., Claesson-Welsh, L. and Heldin, C. H. (2000). The PI 3-kinase isoforms p110(alpha) and p110(beta) have differential roles in PDGF- and insulin-mediated signaling. J. Cell Sci. 113, 207-214.
10. Isakoff, S. J., Taha, C., Rose, E., Marcusohn, J., Klip, A. and Skolnik, E. Y. (1995). The inability of phosphatidylinositol 3-kinase activation to stimulate GLUT4 translocation indicates additional signaling pathways are required for insulin-stimulated glucose uptake. Proc. Natl. Acad. Sci. USA 92, 10247-10251.
11. Kahn, B. B., Rossetti, L., Lodish, H. F. and Charron, M. J. (1991). Decreased in vivo glucose uptake but normal expression of GLUT1 and GLUT4 in skeletal muscle of diabetic rats. J. Clin. Invest. 87, 2197-2206.
12. Kanai, F., Nishioka, Y., Hayashi, H., Kamohara, S., Todaka, M. and Ebina, Y. (1993). Direct demonstration of insulin-induced GLUT4 translocation to the surface of intact cells by insertion of a c-Myc epitope into an exofacial GLUT4 domain. J. Biol. Chem. 268, 14523-14526.
13. Kennedy, J. W., Hirshman, M. F., Gervino, E. V., Ocel, J. V., Forse, R. A., Hoenig, S. J., Aronson, D., Goodyear, L. J. and Horton, E. S. (1999). Acute exercise induces GLUT4 translocation in skeletal muscle of normal human subjects and subjects with type 2 diabetes. Diabetes 48, 1192-1197.
14. Khayat, Z. A., Tong, P., Yaworsky, K., Bloch, R. J. and Klip, A. (2000). Insulin-induced actin filament remodeling colocalizes actin with phosphatidylinositol 3-kinase and GLUT4 in L6 myotubes. J. Cell Sci. 113, 279-290.
15. Kotani, K., Carozzi, A. J., Sakaue, H., Hara, K., Robinson, L. J., Clark, S. F., Yonezawa, K., James, D. E. and Kasuga, M. (1995). Requirement for phosphoinositide 3-kinase in insulin-stimulated GLUT4 translocation in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 209, 343-348.
16. Li, D., Randhawa, V. K., Patel, N., Hayashi, M. and Klip, A. (2001). Hyperosmolarity reduces GLUT4 endocytosis and increases its exocytosis from a VAMP2-independent pool in 16 muscle cells. J. Biol. Chem. 276, 22883-22891.
17. Maffucci, T., Brancaccio, A., Piccolo, E., Stein, R. C. and Falasca, M. (2003). Insulin induces phosphatidylinositol-3-phosphate formation through TC10 activation. EMBO J. 22, 4178-4189.
18. Malide, D., Dwyer, N. K., Blanchette-Mackie, E. J. and Cushman, S. W. (1997). Immunocytochemical evidence that GLUT4 resides in a specialized translocation post-endosomal VAMP2-positive compartment in rat adipose cells in the absence of insulin. J. Histochem. Cytochem. 45, 1083-1096.
19. Martin, L. B., Shewan, A., Millar, C. A., Gould, G. W. and James, D. E. (1998). Vesicle-associated membrane protein 2 plays a specific role in the insulin-dependent trafficking of the facilitative glucose transporter GLUT4 in 3T3-L1 adipocytes. J. Biol. Chem. 273, 1444-1452.
20. Niu, W., Huang, C., Nawaz, Z., Levy, M., Somwar, R., Li, D., Bilan, P. J. and Klip, A. (2003). Maturation of the regulation of GLUT4 activity by p38 MAPK during L6 cell myogenesis. J. Biol. Chem. 278, 17953-17962.
21. Oatey, P. B., Venkateswarlu, K., Williams, A. G., Fletcher, L. M., Foulstone, E. J., Cullen, P. J. and Tavare, J. M. (1999). Confocal imaging of the subcellular distribution of phosphatidylinositol 3,4,5-trisphosphate in insulin- and PDGF-stimulated 3T3-L1 adipocytes. Biochem. J. 344, 511-518.
22. Okada, T., Kawano, Y., Sakakibara, T., Hazeki, O. and Ui, M. (1994). Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin. J. Biol. Chem. 269, 3568-3573.
23. Patel, N., Rudich, A., Khayat, Z. A., Garg, R. and Klip, A. (2003). Intracellular segregation of phosphatidylinositol-3,4,5-trisphosphate by insulin-dependent actin remodeling in L6 skeletal muscle cells. Mol. Cell. Biol. 23, 4611-4626.
24. Quon, M. J., Chen, H., Lin, C. H., Zhou, L., Ing, B. L., Zarnowski, M. J., Klinghoffer, R., Kazlauskas, A., Cushman, S. W. and Taylor, S. I. (1996). Effects of overexpressing wild-type and mutant PDGF receptors on translocation of GLUT4 in transfected rat adipose cells. Biochem. Biophys. Res. Commun. 226, 587-594.
25. Ramm, G., Slot, J. W., James, D. E. and Stoorvogel, W. (2000). Insulin recruits GLUT4 from specialized VAMP2-carrying vesicles as well as from the dynamic endosomal/trans-Golgi network in rat adipocytes. Mol. Biol. Cell 11, 4079-4091.
26. Randhawa, V. K., Bilan, P. J., Khayat, Z. A., Daneman, N., Liu, Z., Ramlal, T., Volchuk, A., Peng, X. R., Coppola, T., Regazzi, R. et al. (2000). VAMP2, but not VAMP3/cellubrevin, mediates insulin-dependent incorporation of GLUT4 into the plasma membrane of L6 myoblasts. Mol. Biol. Cell 11, 2403-2417.
27. Ricort, J. M., Tanti, J. F., van Obberghen, E. and le Marchand-Brustel, Y. (1996). Different effects of insulin and platelet-derived growth factor on phosphatidylinositol 3-kinase at the subcellular level in 3T3-L1 adipocytes. A possible explanation for their specific effects on glucose transport. Eur. J. Biochem. 239, 17-22.
28. Rudich, A., Konrad, D., Torok, D., Ben-Romano, R., Huang, C., Niu, W., Garg, R. R., Wijesekara, N., Germinario, R. J., Bilan, P. J. et al. (2003). Indinavir uncovers different contributions of GLUT4 and GLUT1 towards glucose uptake in muscle and fat cells and tissues. Diabetologia 46, 649-658.
29. Shigematsu, S., Miller, S. L. and Pessin, J. E. (2001). Differentiated 3T3L1 adipocytes are composed of heterogenous cell populations with distinct receptor tyrosine kinase signaling properties. J. Biol. Chem. 276, 15292-15297.
30. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goecke, N. M., Olson, B. J. and Klenk, D. C. (1985). Measurement of protein using bicinchonic acid. Anal. Biochem. 150, 76-85.
31. Summers, S. A., Whiteman, E. L., Cho, H., Lipfert, L. and Birnbaum, M. J. (1999). Differentiation-dependent suppression of platelet-derived growth factor signaling in cultured adipocytes. J. Biol. Chem. 274, 23858-23867.
32. Tengholm, A. and Meyer, T. (2002). A PI3-kinase signaling code for insulin-triggered insertion of glucose transporters into the plasma membrane. Curr. Biol. 12, 1871-1876.
33. Tong, P., Khayat, Z. A., Huang, C., Patel, N., Ueyama, A. and Klip, A. (2001). Insulin-induced cortical actin remodeling promotes GLUT4 insertion at muscle cell membrane ruffles. J. Clin. Invest. 108, 371-381.
34. Tsakiridis, T., Vranic, M. and Klip, A. (1994). Disassembly of the actin network inhibits insulin-dependent stimulation of glucose transport and prevents recruitment of glucose transporters to the plasma membrane. J. Biol. Chem. 269, 29934-29942.
35. Ueyama, A., Yaworsky, K. L., Wang, Q., Ebina, Y. and Klip, A. (1999). GLUT-4Myc ectopic expression in L6 myoblasts generates a GLUT-4-specific pool conferring insulin sensitivity. Am. J. Physiol. 277, E572-E578.
36. Vaziri, C. and Faller, D. V. (1996). Down-regulation of platelet-derived growth factor receptor expression during terminal differentiation of 3T3-L1 pre-adipocyte fibroblasts. J. Biol. Chem. 271, 13642-13648.
37. Wang, L., Hayashi, H. and Ebina, Y. (1999). Transient effect of platelet-derived growth factor on GLUT4 translocation in 3T3-L1 adipocytes. J. Biol. Chem. 274, 19246-19253.
38. Wang, Q., Khayat, Z., Kishi, K., Ebina, Y. and Klip, A. (1998). GLUT4 translocation by insulin in intact muscle cells, detection by a fast and quantitative assay. FEBS Lett. 427, 193-197.
39. Whiteman, E. L., Chen, J. J. and Birnbaum, M. J. (2003). Platelet-derived growth factor (PDGF) stimulates glucose transport in 3T3-L1 adipocytes overexpressing PDGF receptor by a pathway independent of insulin receptor substrates. Endocrinology 144 3811-3820.
40. Wiese, R. J., Mastick, C. C., Lazar, D. F. and Saltiel, A. R. (1995). Activation of mitogen-activated protein kinase and phosphatidylinositol 3′-kinase is not sufficient for the hormonal stimulation of glucose uptake, lipogenesis, or glycogen synthesis in 3T3-L1 adipocytes. J. Biol. Chem. 270, 3442-3446.
41. Zierath, J. R., Krook, A. and Wallberg-Henriksson, H. (1998). Insulin action in skeletal muscle from patients with NIDDM. Mol. Cell. Biochem. 182, 153-160.