Differential regulation of secretory compartments containing the insulin-responsive glucose transporter 4 in 3T3-L1 adipocytes

Molecular Biology of the Cell

Volumn 10, Issue 11, 1999, Pages 3675-3688

  Millar, Caroline A ^a,c   Shewan, Annette ^b   Hickson, Gilles R X ^a   James, David E ^b   Gould, Gwyn W ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL SECRETION; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; INTERNALIZATION; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT;

EID: 0032719409     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.11.3675     Document Type: Article

References (47)

1. Aledo, J.C., Lavoie, L., Volchuck, A., Keller, S.R., Klip, A., and Hundal, H.S. (1997). Identification and characterization of two distinct intracellular GLUT4 pools in rat skeletal muscle: evidence for an endosomal and an insulin-sensitive GLUT4 compartment. Biochem. J., 325, 727-732.
2. Baldini, G., Hohman, R., Charron, M.J., and Lodish, H.F. (1991). Insulin and nonhydrolyzable GTP analogs induce translocation of GLUT4 to the plasma membrane in a-toxin-permeabilized rat adipose cells J. Biol. Chem., 266, 4037-4040.
3. Bottger, G., Nagelkerken, B., and van der Sluijs, P. (1996) Rab4 and Rab7 define distinct nonoverlapping endosomal compartments J. Biol. Chem., 271, 29191-29197.
4. Calderhead, D.M., Kitagawa, K., Tanner, L.I., Holman, G.D., and Lienhard, G.E. (1990). Insulin regulation of the two glucose transporters in 3T3-L1 adipocytes J. Biol. Chem., 265, 13800-13808.
5. Chen, D., Elmendorf, J.S., Olson, A.L., Li, X., Earp, H.S., and Pessin, J.E. (1997). Osmotic shock stimulates GLUT4 translocation in 3T3-L1 adipocytes by a novel tyrosine kinase pathway J. Biol. Chem. 272, 27401-27410.
6. Clarke, J.F., Young, P.W., Yonezawa, K., Kasuga, M., and Holman, G.D. (1994). Inhibition of translocation of GLUT1 and GLUT4 in 3T3-L1 cells by the phosphatidylinositol 3′-kinase inhibitor, wortmannin Biochem. J., 300, 631-635.
7. Coderre, L., Kandror, K.V., Vallega, G., and Pilch, P.F. (1995). Identification and characterization of an exercise-sensitive pool of glucose transporters in skeletal muscle. J. Biol. Chem. 270, 27584-27588.
8. Cormont, M., Van Obberghen, E., Zerial, M., and Le Marchand-Brustel, Y. (1996). Insulin induces a change in Rab5 subcellular localization in adipocytes independently of phosphatidylinositol 3-kinase activation Endocrinology 137, 3408-3415.
9. Daro, E., van der Sluijs, P., Galli, T., and Mellman, I. (1996). Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling. Proc. Natl. Acad. Sci. USA 93, 9559-9564.
10. El-Jack, A.K., Hamm, J.K., Pilch, P.F., and Farmer, S.R. (1999a). Reconstitution of insulin-sensitive glycose transport in fibroblasts requires expression of both PPAR gamma and C/EBP alpha. J. Biol. Chem. 274, 7946-7951.
11. El-Jack, A.K., Kandror, K., and Pilch, P.P. (1999b). The formation of an insulin-responsive vesicular cargo compartment is an early event in 3T3-L1 adipocyte differentiation. Mol. Biol. Cell 10, 1581-1594.
12. Elmendorf, J.S., Chen, D., and Pessin, J.E. (1998). Guanosine 5′-O-(3-triphosphate) (GTPγS) stimulation of GLUT4 translocation is tyrosine kinase dependent. J. Biol. Chem. 273, 13289-13296.
13. Frost, S.C., and Lane, M.D. (1988) Evidence for the involvement of vicinal sulfydryl groups in insulin-activated hexose transport in 3T3-L1 adipocytes. J. Biol. Chem. 260, 2646-2652.
14. Gibbs, E.M., Calderhead, D.M., Holman, G.D., and Gould, G.W. (1991). Phorbol esters only partially mimic the effect of insulin on glucose transport and transporter distribution in 3T3-L1 adipocytes. Biochem. J. 275, 145-150.
15. Gould, G.W., Merrall, N.W., Martin, S., Jess, T.J., Campbell, I.W., Calderhead, D.M., Gibbs, E.M., Holman, G.D., and Plevin, R.J. (1994). Growth factor induced stimulation of hexose transport in 3T3-L1 adipocytes: evidence that insulin-induced translocation of GLUT4 is independent of activation of MAP kinase. Cell. Signal. 6, 313-320.
16. Herbst, J.J., Andrews, G.C., Contillo, L.G., Singleton, D.H., Genereux, P.E., Gibbs, E.M., and Lienhard, G.E. (1995). Effects of the activation of phosphatidylinositol 3′-kinase by a thiophosphotyrosine peptide on glucose transport in 3T3-L1 adipocytes. J. Biol. Chem. 270, 26000-26005.
17. Herman, G.A., Bonzelius, F., Cieutat, A.-M., and Kelly, R.B. (1994). A distinct class of intracellular storage vesicles, identified by expression of the glucose transporter GLUT4. Proc. Natl. Acad. Sci. USA 91, 12750-12754.
18. 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 down-regulates cell-surface transferrin receptor numbers independently of any effect on fluid-phase endocytosis in fibroblasts. Cell. Signal. 8, 297-304.
19. Kandror, K.V., and Pilch, P.F. (1996). The insulin-like growth factor II/mannose 6-phosphate receptor utilizes the same membrane compartments as GLUT4 for insulin-dependent trafficking to and from the rat adipocyte cell surface. J. Biol. Chem. 271, 21703-21708.
20. Kandror, K.V., and Pilch, P.F. (1998). Multiple endosomal recycling pathways in rat adipose cells. Biochem. J. 331, 829-835.
21. Livingstone, C., James, D.E., Rice, J.E., Hanpeter, D., and Gould, G.W. (1996). Compartment ablation analysis of the insulin responsive glucose transporter, GLUT4, in 3T3-L1 adipocytes. Biochem. J. 315, 487-495.
22. Malide, D., Dwyer, N.K., Blanchette-Mackie, E.J., and Cushman, S.W. (1997). Immunocytochemical evidence that GLUT4 resides in a specialized translocation postendosomal VAMP2-positive compartment in rat adipose cells in the absence of insulin J. Histochem. Cytochem. 45, 1083-1095.
23. Martin, L., Shewan, A., Millar, C.A., Gould, G.W., and James, D.E. (1998). Vesicle associated membrane protein-2 (VAMP2) 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.
24. Martin, S., Reaves, B., Banting, G., and Gould, G.W. (1994). Analysis of the colocalization of the insulin-responsive glucose transporter (GLUT4) and the trans Golgi network marker TGN38 within 3T3-L1 adipocytes. Biochem. J. 300, 743-749.
25. Martin, S., Tellam, J., Livingstone, C., Slot, J.W., Gould, G.W., and James, D.E. (1996). The glucose transporter (GLUT4) and vesicle-associated membrane protein (VAMP2) are segregated from recycling endosomes in insulin-sensitive cells. J. Cell Biol. 134, 625-635.
26. McLauchlan, H., Newell, J., Morrice, N., Osborne, A., West, M., and Smythe, E. (1998). A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr. Biol. 8, 34-45.
27. Oka, Y., Mottola, C., Oppenheimer, C.L., and Czech, M.P. (1984). Insulin activates the appearance of insulin-like growth factor II receptors on the adipocyte cell surface. Proc. Natl. Acad. Sci. USA 81, 4028-4032.
28. Olson, A.L., Knight, J.B., and Pessin, J.E. (1997). Syntaxin 4, VAMP2, and/or VAMP3/Cellubrevin are functional target membrane and vesicle SNAP receptors for insulin-stimulated GLUT4 translocation in adipocytes. Mol. Cell. Biol. 17, 2425-2435.
29. Pessin, J.E., Thurmond, D.C., Elmendorf, J.S., Coker, K.J., and Okada, S. (1999). Molecular basis of insulin stimulated GLUT4 vesicle trafficking: location! location! location! J. Biol. Chem. 274, 2593-2596.
30. Ploug, T., van Deurs, B., Ai, H., Cushman, S.W., and Ralston, E. (1998). Analysis of GLUT4 distribution in whole skeletal muscle fibers: Identification of distinct storage compartments that are recruited by insulin and muscle contractions J. Cell Biol. 142, 1429-1446.
31. Rea, S., and James, D.E. (1997). Moving GLUT4: the biogenesis and trafficking of GLUT4 storage vesicles. Diabetes 46, 1667-1677.
32. Robinson, L.J., Pang, S., Harris, D.S., Heuser, J., and James, D.E. (1992). Translocation of the glucose transporter (GLUT4) to the cell surface in permeablized 3T3-L1 adipocytes: effects of ATP, insulin and GTPγS and localization of GLUT 4 to clathrin lattices. J. Cell Biol. 117, 1181-1196.
33. Rybin, V., Illrich, O., Rubino, M., Alexandrov, K., Simon, I., Seabrea, M.C., Goody, R., and Zerial, M. (1996). GTPase activity of Rab5 acts as a timer for endocytic membrane fusion. Nature 383, 266-269.
34. Sheff, D.R., Daro, E.A., Hull, M., and Mellman, I. (1999). The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell Biol. 145, 123-139.
35. Slot, J.W., Garruti, G., Martin, S., Oorschot, V., Posthuma, G., Kraegen, E.W., Laybutt, R., Thibault, G., and James, D.E. (1997). Glucose transporter (GLUT-4) is targeted to secretory granules in rat atrial cardiomyocytes. J. Cell Biol. 137, 1243-1254.
36. Slot, J.W., Geuze, H.J., Gigengack, S., Lienhard, G.E., and James, D.E. (1991). Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J. Cell Biol. 113, 123-135.
37. Stenmark, H., Vitale, G., Ullrich, O., and Zerial, M. (1995). Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion. Cell 83, 423-432.
38. Stoorvogel, W., Geuze, H.J., Griffith, J.M., and Strous, G.J. (1988). The pathways of endocytosed transferrin and secretory protein are connected in the trans-Golgi reticulum. J. Cell Biol. 106, 1821-1829.
39. Stoorvogel, W., Geuze, H.J., and Strous, G.J. (1987). Sorting of endocytosed transferrin and asialoglycoprotein occurs immediately after internalization in HepG2 cells. J. Cell Biol. 104, 1261-1268.
40. Tanner, L.I., and Lienhard, G.E. (1987). Insulin elicits a redistribution of transferrin receptors in 3T3-L1 adipocytes through an increase in the rate constant for receptor externalization. J. Biol. Chem. 262, 8975-8980.
41. Tanner, L.I., and Lienhard, G.E. (1989). Localization of transferrin receptors and insulin-like growth factor II receptors in vesicles from 3T3-L1 adipocytes that contain intracellular glucose transporters J. Cell. Biol. 108, 1537-1545.
42. Tellam, J.T., Macaulay, S.L., McIntosh, S., Hewish, D.R., Ward, C.W., and James, D.E. (1997). Characterization of Munc-18c and Syntaxin-4 3T3-L1 adipocytes. J. Biol. Chem. 272, 6179-6186.
43. Ullrich, O., Reinsche, S., Urbe, S., Zerial, M., and Parton, R.G. (1996). Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 235, 913-924.
44. van der Sluijs, P., Hull, M., Zahraouri, A., Tavitian, A., Goud, B., and Mellman, I. (1992). The small GTP-binding protein rab4 controls and early sorting event on the endocytic pathway. Cell 70, 729-740.
45. Vitale, G., Rybin, V., Christofordis, S., Thornqvist, P.-O., McCaffrey, N., Stenmark, H., and Zerial, M. (1998). Distinct Rab-binding domains mediate the interaction of Rabaptin-5 with GTP-bound rab4 and rab5 EMBO J. 17, 1941-1951.
46. Volchuk, A., Sargeant, R., Sumitani, S., Liu, Z., He, L., and Klip, A. (1995). Cellubrevin is a resident protein of insulin-sensitive GLUT4 glucose transporter vesicles in 3T3-L1 adipocytes. J. Biol. Chem. 270, 8233-8240.
47. Yeh, J.I., Gulve, E.A., Rameh, L., and Birnbaum, M.J. (1995). The effects of wortmannin on rat skeletal muscle. Dissociation of signaling pathways for insulin- and contraction-activated hexose transport. J. Biol. Chem. 270, 2107-2111.