GLUT4 exocytosis

Journal of Cell Science

Volumn 124, Issue 24, 2011, Pages 4147-4159

  Stöckli, Jacqueline ^a   Fazakerley, Daniel J ^a   James, David E ^a,b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Exocytosis; GLUT4 storage vesicles; GLUT4 trafficking; Insulin regulation

Indexed keywords

GLUCOSE TRANSPORTER 4; INSULIN; MYOSIN; RAB PROTEIN; SNARE PROTEIN; SYNTAXIN 16;

ADIPOSE TISSUE; CELL MEMBRANE; CELL VACUOLE; CYTOSKELETON; ENDOSOME; EXOCYTOSIS; FLUORESCENCE MICROSCOPY; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; GLYCEMIC CONTROL; HUMAN; IMMUNOELECTRON MICROSCOPY; MEMBRANE FUSION; MOLECULAR DOCKING; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NOTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EXOCYTOSIS; GLUCOSE TRANSPORTER TYPE 4; PROTEIN TRANSPORT; SECRETORY VESICLES; SIGNAL TRANSDUCTION;

EID: 84856900480     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.097063     Document Type: Note

References (183)

1. Abel, E. D., Peroni, O., Kim, J. K., Kim, Y. B., Boss, O., Hadro, E., Minnemann, T., Shulman, G. I. and Kahn, B. B.(2001). Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 409, 729-733.
2. Aledo, J. C., Darakhshan, F. and Hundal, H. S.(1995). Rab4, but not the transferrin receptor, is colocalized with GLUT4 in an insulin-sensitive intracellular compartment in rat skeletal muscle. Biochem. Biophys. Res. Commun. 215, 321-328.
3. Antonescu, C. N., Diaz, M., Femia, G., Planas, J. V. and Klip, A.(2008). Clathrindependent and independent endocytosis of glucose transporter 4 (GLUT4) in myoblasts: regulation by mitochondrial uncoupling. Traffic 9, 1173-1190.
4. Aran, V., Bryant, N. J. and Gould, G. W.(2011). Tyrosine phosphorylation of Munc18c on residue 521 abrogates binding to Syntaxin 4. BMC Biochem. 12, 19.
5. Babbey, C. M., Bacallao, R. L. and Dunn, K. W.(2010). Rab10 associates with primary cilia and the exocyst complex in renal epithelial cells. Am. J. Physiol. Renal Physiol. 299, F495-F506.
6. 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.
7. Bao, Y., Lopez, J. A., James, D. E. and Hunziker, W.(2008). Snapin interacts with the Exo70 subunit of the exocyst and modulates GLUT4 trafficking. J. Biol. Chem. 283, 324-331.
8. Berwick, D. C., Dell, G. C., Welsh, G. I., Heesom, K. J., Hers, I., Fletcher, L. M., Cooke, F. T. and Tavare, J. M.(2004). Protein kinase B phosphorylation of PIKfyve regulates the trafficking of GLUT4 vesicles. J. Cell Sci. 117, 5985-5993.
9. Birnbaum, M. J.(1989). Identification of a novel gene encoding an insulin-responsive glucose transporter protein. Cell 57, 305-315.
10. Blot, V. and McGraw, T. E.(2006). GLUT4 is internalized by a cholesterol-dependent nystatin-sensitive mechanism inhibited by insulin. EMBO J. 25, 5648-5658.
11. Blot, V. and McGraw, T. E.(2008). Molecular mechanisms controlling GLUT4 intracellular retention. Mol. Biol. Cell 19, 3477-3487.
12. Bogan, J. S., Hendon, N., McKee, A. E., Tsao, T. S. and Lodish, H. F.(2003). Functional cloning of TUG as a regulator of GLUT4 glucose transporter trafficking. Nature 425, 727-733.
13. Bose, A., Guilherme, A., Robida, S. I., Nicoloro, S. M., Zhou, Q. L., Jiang, Z. Y., Pomerleau, D. P. and Czech, M. P.(2002). Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature 420, 821-824.
14. Brewer, P. D., Romenskaia, I., Kanow, M. A. and Mastick, C. C.(2011). Loss of AS160 causes Glut4 to accumulate in compartments that are primed for fusion in basal adipocytes. J. Biol. Chem. 286, 26287-26297.
15. Brosius, F. C., 3rd, Briggs, J. P., Marcus, R. G., Barac-Nieto, M. and Charron, M. J.(1992). Insulin-responsive glucose transporter expression in renal microvessels and glomeruli. Kidney Int. 42, 1086-1092.
16. Brown, F. C. and Pfeffer, S. R.(2010). An update on transport vesicle tethering. Mol. Membr. Biol. 27, 457-461.
17. Bruton, J. D., Katz, A. and Westerblad, H.(1999). Insulin increases near-membrane but not global Ca2+ in isolated skeletal muscle. Proc. Natl. Acad. Sci. USA 96, 3281-3286.
18. Bryant, N. J. and Gould, G. W.(2011). SNARE proteins underpin insulin-regulated GLUT4 traffic. Traffic 12, 657-664.
19. Bryant, N. J., Govers, R. and James, D. E.(2002). Regulated transport of the glucose transporter GLUT4. Nat. Rev. Mol. Cell Biol. 3, 267-277.
20. Buse, J. B., Yasuda, K., Lay, T. P., Seo, T. S., Olson, A. L., Pessin, J. E., Karam, J. H., Seino, S. and Bell, G. I.(1992). Human GLUT4/muscle-fat glucose-transporter gene. Characterization and genetic variation. Diabetes 41, 1436-1445.
21. Cain, C. C., Trimble, W. S. and Lienhard, G. E.(1992). Members of the VAMP family of synaptic vesicle proteins are components of glucose transporter-containing vesicles from rat adipocytes. J. Biol. Chem. 267, 11681-11684.
22. Charron, M. J., Brosius, F. C., 3rd, Alper, S. L. and Lodish, H. F.(1989). A glucose transport protein expressed predominately in insulin-responsive tissues. Proc. Natl. Acad. Sci. USA 86, 2535-2539.
23. Cheatham, B., Volchuk, A., Kahn, C. R., Wang, L., Rhodes, C. J. and Klip, A.(1996). Insulin-stimulated translocation of GLUT4 glucose transporters requires SNAREcomplex proteins. Proc. Natl. Acad. Sci. USA 93, 15169-15173.
24. Chen, X. W., Leto, D., Chiang, S. H., Wang, Q. and Saltiel, A. R.(2007). Activation of RalA is required for insulin-stimulated Glut4 trafficking to the plasma membrane via the exocyst and the motor protein Myo1c. Dev. Cell 13, 391-404.
25. Chen, X. W., Leto, D., Xiao, J., Goss, J., Wang, Q., Shavit, J. A., Xiong, T., Yu, G., Ginsburg, D., Toomre, D. et al.(2011). Exocyst function is regulated by effector phosphorylation. Nat. Cell Biol. 13, 580-588.
26. Chiu, T. T., Jensen, T. E., Sylow, L., Richter, E. A. and Klip, A.(2011). Rac1 signalling towards GLUT4/glucose uptake in skeletal muscle. Cell. Signal. 23, 1546-1554.
27. Cong, L. N., Chen, H., Li, Y., Zhou, L., McGibbon, M. A., Taylor, S. I. and Quon, M. J.(1997). Physiological role of Akt in insulin-stimulated translocation of GLUT4 in transfected rat adipose cells. Mol. Endocrinol. 11, 1881-1890.
28. Coster, A. C., Govers, R. and James, D. E.(2004). Insulin stimulates the entry of GLUT4 into the endosomal recycling pathway by a quantal mechanism. Traffic 5, 763-771.
29. Cushman, S. W. and Wardzala, L. J.(1980). Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. Apparent translocation of intracellular transport systems to the plasma membrane. J. Biol. Chem. 255, 4758-4762.
30. Czech, M. P., Chawla, A., Woon, C. W., Buxton, J., Armoni, M., Tang, W., Joly, M. and Corvera, S.(1993). Exofacial epitope-tagged glucose transporter chimeras reveal COOH-terminal sequences governing cellular localization. J. Cell Biol. 123, 127-135.
31. Das, A. and Guo, W.(2011). Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol. 21, 383-386.
32. Dash, S., Sano, H., Rochford, J. J., Semple, R. K., Yeo, G., Hyden, C. S., Soos, M. A., Clark, J., Rodin, A., Langenberg, C. et al.(2009). A truncation mutation in TBC1D4 in a family with acanthosis nigricans and postprandial hyperinsulinemia. Proc. Natl. Acad. Sci. USA 106, 9350-9355.
33. Dawson, K., Aviles-Hernandez, A., Cushman, S. W. and Malide, D.(2001). Insulinregulated trafficking of dual-labeled glucose transporter 4 in primary rat adipose cells. Biochem. Biophys. Res. Commun. 287, 445-454.
34. Dugani, C. B. and Klip, A.(2005). Glucose transporter 4, cycling, compartments and controversies. EMBO Rep. 6, 1137-1142.
35. Ebstensen, R. D. and Plagemann, P. G.(1972). Cytochalasin B: inhibition of glucose and glucosamine transport. Proc. Natl. Acad. Sci. USA 69, 1430-1434.
36. 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.
37. Fazakerley, D. J., Holman, G. D., Marley, A., James, D. E., Stöckli, J. and Coster, A. C.(2010). Kinetic evidence for unique regulation of GLUT4 trafficking by insulin and AMP-activated protein kinase activators in L6 myotubes. J. Biol. Chem. 285, 1653-1660.
38. Foley, K., Boguslavsky, S. and Klip, A.(2011). Endocytosis, recycling, and regulated exocytosis of glucose transporter 4. Biochemistry 50, 3048-3061.
39. Fujita, H., Hatakeyama, H., Watanabe, T. M., Sato, M., Higuchi, H. and Kanzaki, M.(2010). Identification of three distinct functional sites of insulin-mediated GLUT4 trafficking in adipocytes using quantitative single molecule imaging. Mol. Biol. Cell 21, 2721-2731.
40. Fukuda, N., Emoto, M., Nakamori, Y., Taguchi, A., Miyamoto, S., Uraki, S., Oka, Y. and Tanizawa, Y.(2009). DOC2B: a novel syntaxin-4 binding protein mediating insulin-regulated GLUT4 vesicle fusion in adipocytes. Diabetes 58, 377-384.
41. Fukumoto, H., Kayano, T., Buse, J. B., Edwards, Y., Pilch, P. F., Bell, G. I. and Seino, S.(1989). Cloning and characterization of the major insulin-responsive glucose transporter expressed in human skeletal muscle and other insulin-responsive tissues. J. Biol. Chem. 264, 7776-7779.
42. Garvey, W. T., Maianu, L., Huecksteadt, T. P., Birnbaum, M. J., Molina, J. M. and Ciaraldi, T. P.(1991). Pretranslational suppression of a glucose transporter protein causes insulin resistance in adipocytes from patients with non-insulin-dependent diabetes mellitus and obesity. J. Clin. Invest. 87, 1072-1081.
43. Garvey, W. T., Maianu, L., Hancock, J. A., Golichowski, A. M. and Baron, A.(1992). Gene expression of GLUT4 in skeletal muscle from insulin-resistant patients with obesity, IGT, GDM, and NIDDM. Diabetes 41, 465-475.
44. Gerber, S. H., Rah, J. C., Min, S. W., Liu, X., de Wit, H., Dulubova, I., Meyer, A. C., Rizo, J., Arancillo, M., Hammer, R. E. et al.(2008). Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science 321, 1507-1510.
45. 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.
46. Gridley, S., Chavez, J. A., Lane, W. S. and Lienhard, G. E.(2006). Adipocytes contain a novel complex similar to the tuberous sclerosis complex. Cell. Signal. 18, 1626-1632.
47. Habtemichael, E. N., Brewer, P. D., Romenskaia, I. and Mastick, C. C.(2011). Kinetic evidence that Glut4 follows different endocytic pathways than the receptors for transferrin and alpha2-macroglobulin. J. Biol. Chem. 286, 10115-10125.
48. Hashiramoto, M. and James, D. E.(2000). Characterization of insulin-responsive GLUT4 storage vesicles isolated from 3T3-L1 adipocytes. Mol. Cell. Biol. 20, 416-427.
49. Hayashi, T., Hirshman, M. F., Kurth, E. J., Winder, W. W. and Goodyear, L. J.(1998). Evidence for 5' AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47, 1369-1373.
50. Hertzog, M. and Chavrier, P.(2011). Cell polarity during motile processes: keeping on track with the exocyst complex. Biochem. J. 433, 403-409.
51. Ho, P. C., Lin, Y. W., Tsui, Y. C., Gupta, P. and Wei, L. N.(2009). A negative regulatory pathway of GLUT4 trafficking in adipocyte: new function of RIP140 in the cytoplasm via AS160. Cell Metab. 10, 516-523.
52. Hoffman, N. J. and Elmendorf, J. S.(2011). Signaling, cytoskeletal and membrane mechanisms regulating GLUT4 exocytosis. Trends Endocrinol. Metab. 22, 110-116.
53. Hsu, S. C., Hazuka, C. D., Roth, R., Foletti, D. L., Heuser, J. and Scheller, R. H.(1998). Subunit composition, protein interactions, and structures of the mammalian brain sec6/8 complex and septin filaments. Neuron 20, 1111-1122.
54. Hu, S. H., Latham, C. F., Gee, C. L., James, D. E. and Martin, J. L.(2007). Structure of the Munc18c/Syntaxin4 N-peptide complex defines universal features of the Npeptide binding mode of Sec1/Munc18 proteins. Proc. Natl. Acad. Sci. USA 104, 8773-8778.
55. Huang, J., Imamura, T. and Olefsky, J. M.(2001). Insulin can regulate GLUT4 internalization by signaling to Rab5 and the motor protein dynein. Proc. Natl. Acad. Sci. USA 98, 13084-13089.
56. 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.
57. Imamura, T., Huang, J., Usui, I., Satoh, H., Bever, J. and Olefsky, J. M.(2003). Insulin-induced GLUT4 translocation involves protein kinase C-lambda-mediated functional coupling between Rab4 and the motor protein kinesin. Mol. Cell. Biol. 23, 4892-4900.
58. Inoue, M., Chang, L., Hwang, J., Chiang, S. H. and Saltiel, A. R.(2003). The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature 422, 629-633.
59. Ishikura, S., Bilan, P. J. and Klip, A.(2007). Rabs 8A and 14 are targets of the insulinregulated Rab-GAP AS160 regulating GLUT4 traffic in muscle cells. Biochem. Biophys. Res. Commun. 353, 1074-1079.
60. James, D. E., Brown, R., Navarro, J. and Pilch, P. F.(1988). Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein. Nature 333, 183-185.
61. James, D. E., Strube, M. and Mueckler, M.(1989). Molecular cloning and characterization of an insulin-regulatable glucose transporter. Nature 338, 83-87.
62. Jedrychowski, M. P., Gartner, C. A., Gygi, S. P., Zhou, L., Herz, J., Kandror, K. V. and Pilch, P. F.(2010). Proteomic analysis of GLUT4 storage vesicles reveals LRP1 to be an important vesicle component and target of insulin signaling. J. Biol. Chem. 285, 104-114.
63. Jewell, J. L., Oh, E., Ramalingam, L., Kalwat, M. A., Tagliabracci, V. S., Tackett, L., Elmendorf, J. S. and Thurmond, D. C.(2011). Munc18c phosphorylation by the insulin receptor links cell signaling directly to SNARE exocytosis. J. Cell Biol. 193, 185-199.
64. 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.
65. Kaddai, V., Gonzalez, T., Keslair, F., Gremeaux, T., Bonnafous, S., Gugenheim, J., Tran, A., Gual, P., Le Marchand-Brustel, Y. and Cormont, M.(2009). Rab4b is a small GTPase involved in the control of the glucose transporter GLUT4 localization in adipocyte. PLoS ONE 4, e5257.
66. Kaestner, K. H., Christy, R. J., McLenithan, J. C., Braiterman, L. T., Cornelius, P., Pekala, P. H. and Lane, M. D.(1989). Sequence, tissue distribution, and differential expression of mRNA for a putative insulin-responsive glucose transporter in mouse 3T3-L1 adipocytes. Proc. Natl. Acad. Sci. USA 86, 3150-3154.
67. 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.
68. Kanda, H., Tamori, Y., Shinoda, H., Yoshikawa, M., Sakaue, M., Udagawa, J., Otani, H., Tashiro, F., Miyazaki, J. and Kasuga, M.(2005). Adipocytes from Munc18c-null mice show increased sensitivity to insulin-stimulated GLUT4 externalization. J. Clin. Invest. 115, 291-301.
69. Kandror, K. V. and Pilch, P. F.(1994). gp160, a tissue-specific marker for insulinactivated glucose transport. Proc. Natl. Acad. Sci. USA 91, 8017-8021.
70. Kandror, K. V. and Pilch, P. F.(2011). The sugar is sIRVed: sorting Glut4 and its fellow travelers. Traffic 12, 665-671.
71. Kandror, K. V., Yu, L. and Pilch, P. F.(1994). The major protein of GLUT4-containing vesicles, gp160, has aminopeptidase activity. J. Biol. Chem. 269, 30777-30780.
72. Kane, S., Sano, H., Liu, S. C., Asara, J. M., Lane, W. S., Garner, C. C. and Lienhard, G. E.(2002). A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J. Biol. Chem. 277, 22115-22118.
73. Karcher, R. L., Roland, J. T., Zappacosta, F., Huddleston, M. J., Annan, R. S., Carr, S. A. and Gelfand, V. I.(2001). Cell cycle regulation of myosin-V by calcium/calmodulin-dependent protein kinase II. Science 293, 1317-1320.
74. Karnieli, E., Zarnowski, M. J., Hissin, P. J., Simpson, I. A., Salans, L. B. and Cushman, S. W.(1981). Insulin-stimulated translocation of glucose transport systems in the isolated rat adipose cell. Time course, reversal, insulin concentration dependency, and relationship to glucose transport activity. J. Biol. Chem. 256, 4772-4777.
75. 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.
76. Katz, E. B., Stenbit, A. E., Hatton, K., DePinho, R. and Charron, M. J.(1995). Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature 377, 151-155.
77. 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. J. Biol. Chem. 270, 23612-23618.
78. Kessler, A., Tomas, E., Immler, D., Meyer, H. E., Zorzano, A. and Eckel, J.(2000). Rab11 is associated with GLUT4-containing vesicles and redistributes in response to insulin. Diabetologia 43, 1518-1527.
79. Kohn, A. D., Barthel, A., Kovacina, K. S., Boge, A., Wallach, B., Summers, S. A., Birnbaum, M. J., Scott, P. H., Lawrence, J. C., Jr and Roth, R. A.(1998). Construction and characterization of a conditionally active version of the serine/threonine kinase Akt. J. Biol. Chem. 273, 11937-11943.
80. 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.
81. Kotani, K., Peroni, O. D., Minokoshi, Y., Boss, O. and Kahn, B. B.(2004). GLUT4 glucose transporter deficiency increases hepatic lipid production and peripheral lipid utilization. J. Clin. Invest. 114, 1666-1675.
82. Kupriyanova, T. A. and Kandror, K. V.(2000). Cellugyrin is a marker for a distinct population of intracellular Glut4-containing vesicles. J. Biol. Chem. 275, 36263-36268.
83. Kupriyanova, T. A., Kandror, V. and Kandror, K. V.(2002). Isolation and characterization of the two major intracellular Glut4 storage compartments. J. Biol. Chem. 277, 9133-9138.
84. Kurth-Kraczek, E. J., Hirshman, M. F., Goodyear, L. J. and Winder, W. W.(1999). 5' AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48, 1667-1671.
85. Lalioti, V., Muruais, G., Dinarina, A., van Damme, J., Vandekerckhove, J. and Sandoval, I. V.(2009). The atypical kinase Cdk5 is activated by insulin, regulates the association between GLUT4 and E-Syt1, and modulates glucose transport in 3T3-L1 adipocytes. Proc. Natl. Acad. Sci. USA 106, 4249-4253.
86. 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.
87. Larance, M., Ramm, G., Stöckli, J., van Dam, E. M., Winata, S., Wasinger, V., Simpson, F., Graham, M., Junutula, J. R., Guilhaus, 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.
88. Latham, C. F., Lopez, J. A., Hu, S. H., Gee, C. L., Westbury, E., Blair, D. H., Armishaw, C. J., Alewood, P. F., Bryant, N. J., James, D. E. et al.(2006). Molecular dissection of the Munc18c/syntaxin4 interaction: implications for regulation of membrane trafficking. Traffic 7, 1408-1419.
89. Li, F., Pincet, F., Perez, E., Eng, W. S., Melia, T. J., Rothman, J. E. and Tareste, D.(2007). Energetics and dynamics of SNAREpin folding across lipid bilayers. Nat. Struct. Mol. Biol. 14, 890-896.
90. Lin, B. Z., Pilch, P. F. and Kandror, K. V.(1997). Sortilin is a major protein component of Glut4-containing vesicles. J. Biol. Chem. 272, 24145-24147.
91. 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.
92. 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.
93. Lodhi, I. J., Chiang, S. H., Chang, L., Vollenweider, D., Watson, R. T., Inoue, M., Pessin, J. E. and Saltiel, A. R.(2007). Gapex-5, a Rab31 guanine nucleotide exchange factor that regulates Glut4 trafficking in adipocytes. Cell Metab. 5, 59-72.
94. 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 20, 3918-3929.
95. Lundsgaard, E.(1939). On the mode of action of insulin. Uppsala Läkareförenings Förhandlinger 45, 143-152.
96. Malide, D., Ramm, G., Cushman, S. W. and Slot, J. W.(2000). Immunoelectron microscopic evidence that GLUT4 translocation explains the stimulation of glucose transport in isolated rat white adipose cells. J. Cell Sci. 113, 4203-4210.
97. Martin, D. B. and Carter, J. R., Jr. (1970). Insulin-stimulated glucose uptake by subcellular particles from adipose tissue cells. Science 167, 873-874.
98. 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.
99. Martin, O. J., Lee, A. and McGraw, T. E.(2006). GLUT4 distribution between the plasma membrane and the intracellular compartments is maintained by an insulinmodulated bipartite dynamic mechanism. J. Biol. Chem. 281, 484-490.
100. Martin, S., Rice, J. E., Gould, G. W., Keller, S. R., Slot, J. W. and James, D. E.(1997). The glucose transporter GLUT4 and the aminopeptidase vp165 colocalise in tubulovesicular elements in adipocytes and cardiomyocytes. J. Cell Sci. 110, 2281-2291.
101. Martin, S., Millar, C. A., Lyttle, C. T., Meerloo, T., Marsh, B. J., Gould, G. W. and James, D. E.(2000). Effects of insulin on intracellular GLUT4 vesicles in adipocytes: evidence for a secretory mode of regulation. J. Cell Sci. 113, 3427-3438.
102. Martin, S. S., Haruta, T., Morris, A. J., Klippel, A., Williams, L. T. and Olefsky, J. M.(1996). Activated phosphatidylinositol 3-kinase is sufficient to mediate actin rearrangement and GLUT4 translocation in 3T3-L1 adipocytes. J. Biol. Chem. 271, 17605-17608.
103. Mastick, C. C., Aebersold, R. and Lienhard, G. E.(1994). Characterization of a major protein in GLUT4 vesicles. Concentration in the vesicles and insulin-stimulated translocation to the plasma membrane. J. Biol. Chem. 269, 6089-6092.
104. McMahon, H. T., Kozlov, M. M. and Martens, S.(2010). Membrane curvature in synaptic vesicle fusion and beyond. Cell 140, 601-605.
105. Melia, T. J., Weber, T., McNew, J. A., Fisher, L. E., Johnston, R. J., Parlati, F., Mahal, L. K., Sollner, T. H. and Rothman, J. E.(2002). Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins. J. Cell Biol. 158, 929-940.
106. Merrill, G. F., Kurth, E. J., Hardie, D. G. and Winder, W. W.(1997). AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am. J. Physiol. 273, E1107-E1112.
107. Miesenbock, G., De Angelis, D. A. and Rothman, J. E.(1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195.
108. Miinea, C. P., Sano, H., Kane, S., Sano, E., Fukuda, M., Peranen, J., Lane, W. S. and Lienhard, G. E.(2005). AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem. J. 391, 87-93.
109. Misura, K. M., Scheller, R. H. and Weis, W. I.(2000). Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature 404, 355-362.
110. Moskalenko, S., Henry, D. O., Rosse, C., Mirey, G., Camonis, J. H. and White, M. A.(2002). The exocyst is a Ral effector complex. Nat. Cell Biol. 4, 66-72.
111. Mueckler, M., Caruso, C., Baldwin, S. A., Panico, M., Blench, I., Morris, H. R., Allard, W. J., Lienhard, G. E. and Lodish, H. F.(1985). Sequence and structure of a human glucose transporter. Science 229, 941-945.
112. Munson, M. and Novick, P.(2006). The exocyst defrocked, a framework of rods revealed. Nat. Struct. Mol. Biol. 13, 577-581.
113. Muretta, J. M., Romenskaia, I. and Mastick, C. C.(2008). Insulin releases Glut4 from static storage compartments into cycling endosomes and increases the rate constant for Glut4 exocytosis. J. Biol. Chem. 283, 311-323.
114. Ng, Y., Ramm, G., Lopez, J. A. and James, D. E.(2008). Rapid activation of Akt2 is sufficient to stimulate GLUT4 translocation in 3T3-L1 adipocytes. Cell Metab. 7, 348-356.
115. Ng, Y., Ramm, G., Burchfield, J. G., Coster, A. C., Stockli, J. and James, D. E.(2010). Cluster analysis of insulin action in adipocytes reveals a key role for Akt at the plasma membrane. J. Biol. Chem. 285, 2245-2257.
116. Okada, S., Yamada, E., Saito, T., Ohshima, K., Hashimoto, K., Yamada, M., Uehara, Y., Tsuchiya, T., Shimizu, H., Tatei, K. et al.(2008). CDK5-dependent phosphorylation of the Rho family GTPase TC10(alpha) regulates insulin-stimulated GLUT4 translocation. J. Biol. Chem. 283, 35455-35463.
117. 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.
118. Omata, W., Shibata, H., Li, L., Takata, K. and Kojima, I.(2000). Actin filaments play a critical role in insulin-induced exocytotic recruitment but not in endocytosis of GLUT4 in isolated rat adipocytes. Biochem. J. 346, 321-328.
119. Oztan, A., Silvis, M., Weisz, O. A., Bradbury, N. A., Hsu, S. C., Goldenring, J. R., Yeaman, C. and Apodaca, G.(2007). Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells. Mol. Biol. Cell 18, 3978-3992.
120. Pang, Z. P. and Sudhof, T. C.(2010). Cell biology of Ca2+-triggered exocytosis. Curr. Opin. Cell Biol. 22, 496-505.
121. Peck, G. R., Ye, S., Pham, V., Fernando, R. N., Macaulay, S. L., Chai, S. Y. and Albiston, A. L.(2006). Interaction of the Akt substrate, AS160, with the glucose transporter 4 vesicle marker protein, insulin-regulated aminopeptidase. Mol. Endocrinol. 20, 2576-2583.
122. Pedersen, O., Bak, J. F., Andersen, P. H., Lund, S., Moller, D. E., Flier, J. S. and Kahn, B. B.(1990). Evidence against altered expression of GLUT1 or GLUT4 in skeletal muscle of patients with obesity or NIDDM. Diabetes 39, 865-870.
123. Piper, R. C., Hess, L. J. and James, D. E.(1991). Differential sorting of two glucose transporters expressed in insulin-sensitive cells. Am. J. Physiol. 260, C570-C580.
124. 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.
125. Quon, M. J., Guerre-Millo, M., Zarnowski, M. J., Butte, A. J., Em, M., Cushman, S. W. and Taylor, S. I.(1994). Tyrosine kinase-deficient mutant human insulin receptors (Met1153->Ile) overexpressed in transfected rat adipose cells fail to mediate translocation of epitope-tagged GLUT4. Proc. Natl. Acad. Sci. USA 91, 5587-5591.
126. 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.
127. Ramm, G., Larance, M., Guilhaus, M. and James, D. E.(2006). A role for 14-3-3 in insulin-stimulated GLUT4 translocation through its interaction with the RabGAP AS160. J. Biol. Chem. 281, 29174-29180.
128. Rayner, D. V., Thomas, M. E. and Trayhurn, P.(1994). Glucose transporters (GLUTs 1-4) and their mRNAs in regions of the rat brain: insulin-sensitive transporter expression in the cerebellum. Can. J. Physiol. Pharmacol. 72, 476-479.
129. Rea, S., Martin, L. B., McIntosh, S., Macaulay, S. L., Ramsdale, T., Baldini, G. and James, D. E.(1998). Syndet, an adipocyte target SNARE involved in the insulininduced translocation of GLUT4 to the cell surface. J. Biol. Chem. 273, 18784-18792.
130. Rink, J., Ghigo, E., Kalaidzidis, Y. and Zerial, M.(2005). Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749.
131. Rivera-Molina, F. E. and Novick, P. J.(2009). A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc. Natl. Acad. Sci. USA 106, 14408-14413.
132. Rodbell, M.(1964). Metabolism of isolated fat cells. I. Effects of hormones on glucose metabolism and lipolysis. J. Biol. Chem. 239, 375-380.
133. Rodnick, K. J., Slot, J. W., Studelska, D. R., Hanpeter, D. E., Robinson, L. J., Geuze, H. J. and James, D. E.(1992). Immunocytochemical and biochemical studies of GLUT4 in rat skeletal muscle. J. Biol. Chem. 267, 6278-6285.
134. Roland, J. T., Bryant, D. M., Datta, A., Itzen, A., Mostov, K. E. and Goldenring, J. R.(2011). Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc. Natl. Acad. Sci. USA 108, 2789-2794.
135. Ross, S. A., Scott, H. M., Morris, N. J., Leung, W. Y., Mao, F., Lienhard, G. E. and Keller, S. R.(1996). Characterization of the insulin-regulated membrane aminopeptidase in 3T3-L1 adipocytes. J. Biol. Chem. 271, 3328-3332.
136. Rothman, D. L., Shulman, R. G. and Shulman, G. I.(1992). 31P nuclear magnetic resonance measurements of muscle glucose-6-phosphate. Evidence for reduced insulindependent muscle glucose transport or phosphorylation activity in non-insulin-dependent diabetes mellitus. J. Clin. Invest. 89, 1069-1075.
137. Rowland, A. F., Fazakerley, D. J. and James, D. E.(2011). Mapping Insulin/GLUT4 Circuitry. Traffic 12, 672-681.
138. 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 GTPaseactivating protein regulates GLUT4 translocation. J. Biol. Chem. 278, 14599-14602.
139. Sano, H., Eguez, L., Teruel, M. N., Fukuda, M., Chuang, T. D., Chavez, J. A., Lienhard, G. E. and McGraw, T. E.(2007). Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab. 5, 293-303.
140. Sano, H., Roach, W. G., Peck, G. R., Fukuda, M. and Lienhard, G. E.(2008). Rab10 in insulin-stimulated GLUT4 translocation. Biochem. J. 411, 89-95.
141. Satoh, S., Nishimura, H., Clark, A. E., Kozka, I. J., Vannucci, S. J., Simpson, I. A., Quon, M. J., Cushman, S. W. and Holman, G. D.(1993). Use of bismannose photolabel to elucidate insulin-regulated GLUT4 subcellular trafficking kinetics in rat adipose cells. Evidence that exocytosis is a critical site of hormone action. J. Biol. Chem. 268, 17820-17829.
142. Semiz, S., Park, J. G., Nicoloro, S. M., Furcinitti, P., Zhang, C., Chawla, A., Leszyk, J. and Czech, M. P.(2003). Conventional kinesin KIF5B mediates insulin-stimulated GLUT4 movements on microtubules. EMBO J. 22, 2387-2399.
143. 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.
144. Shepherd, P. R., Gnudi, L., Tozzo, E., Yang, H., Leach, F. and Kahn, B. B.(1993). Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J. Biol. Chem. 268, 22243-22246.
145. Shewan, A. M., van Dam, E. M., Martin, S., Luen, T. B., Hong, W., Bryant, N. J. and James, D. E.(2003). GLUT4 recycles via a trans-Golgi network (TGN) subdomain enriched in Syntaxins 6 and 16 but not TGN38: involvement of an acidic targeting motif. Mol. Biol. Cell 14, 973-986.
146. Shimizu, Y. and Shimazu, T.(1994). Effects of wortmannin on increased glucose transport by insulin and norepinephrine in primary culture of brown adipocytes. Biochem. Biophys. Res. Commun. 202, 660-665.
147. Sinha, M. K., Raineri-Maldonado, C., Buchanan, C., Pories, W. J., Carter-Su, C., Pilch, P. F. and Caro, J. F.(1991). Adipose tissue glucose transporters in NIDDM. Decreased levels of muscle/fat isoform. Diabetes 40, 472-477.
148. Slot, J. W., Geuze, H. J., Gigengack, S., James, D. E. and Lienhard, G. E.(1991a). Translocation of the glucose transporter GLUT4 in cardiac myocytes of the rat. Proc. Natl. Acad. Sci. USA 88, 7815-7819.
149. Slot, J. W., Geuze, H. J., Gigengack, S., Lienhard, G. E. and James, D. E.(1991b). Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J. Cell Biol. 113, 123-135.
150. Stenbit, A. E., Tsao, T. S., Li, J., Burcelin, R., Geenen, D. L., Factor, S. M., Houseknecht, K., Katz, E. B. and Charron, M. J.(1997). GLUT4 heterozygous knockout mice develop muscle insulin resistance and diabetes. Nat. Med. 3, 1096-1101.
151. Stenkula, K. G., Lizunov, V. A., Cushman, S. W. and Zimmerberg, J.(2010). Insulin controls the spatial distribution of GLUT4 on the cell surface through regulation of its postfusion dispersal. Cell Metab. 12, 250-259.
152. Stöckli, J. and James, D. E.(2009). GLUT4. UCSD-Nature Molecule Pages doi:10.1038/mp.a001046.01.
153. Stöckli, J., Davey, J. R., Hohnen-Behrens, C., Xu, A., James, D. E. and Ramm, G.(2008). Regulation of glucose transporter 4 translocation by the Rab guanosine triphosphatase-activating protein AS160/TBC1D4: role of phosphorylation and membrane association. Mol. Endocrinol. 22, 2703-2715.
154. 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.
155. Sudhof, T. C. and Rothman, J. E.(2009). Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477.
156. Sun, Y., Bilan, P. J., Liu, Z. and Klip, A.(2010). Rab8A and Rab13 are activated by insulin and regulate GLUT4 translocation in muscle cells. Proc. Natl. Acad. Sci. USA 107, 19909-19914.
157. Suzuki, K. and Kono, T.(1980). Evidence that insulin causes translocation of glucose transport activity to the plasma membrane from an intracellular storage site. Proc. Natl. Acad. Sci. USA 77, 2542-2545.
158. 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.
159. 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 in 3T3-L1 adipocytes. Putative role in insulin-dependent movement of GLUT-4. J. Biol. Chem. 272, 6179-6186.
160. TerBush, D. R., Maurice, T., Roth, D. and Novick, P.(1996). The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15, 6483-6494.
161. Thurmond, D. C., Ceresa, B. P., Okada, S., Elmendorf, J. S., Coker, K. and Pessin, J. E.(1998). Regulation of insulin-stimulated GLUT4 translocation by Munc18c in 3T3L1 adipocytes. J. Biol. Chem. 273, 33876-33883.
162. Tong, P., Khayat, Z. A., Huang, C., Patel, N., Ueyama, A. and Klip, A.(2001). Insulininduced cortical actin remodeling promotes GLUT4 insertion at muscle cell membrane ruffles. J. Clin. Invest. 108, 371-381.
163. 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.
164. Tsao, T. S., Burcelin, R., Katz, E. B., Huang, L. and Charron, M. J.(1996). Enhanced insulin action due to targeted GLUT4 overexpression exclusively in muscle. Diabetes 45, 28-36.
165. 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.
166. Volchuk, A., Wang, Q., Ewart, H. S., Liu, Z., He, L., Bennett, M. K. and Klip, A.(1996). Syntaxin 4 in 3T3-L1 adipocytes: regulation by insulin and participation in insulin-dependent glucose transport. Mol. Biol. Cell 7, 1075-1082.
167. Vollenweider, P., Martin, S. S., Haruta, T., Morris, A. J., Nelson, J. G., Cormont, M., Le Marchand-Brustel, Y., Rose, D. W. and Olefsky, J. M.(1997). The small guanosine triphosphate-binding protein Rab4 is involved in insulin-induced GLUT4 translocation and actin filament rearrangement in 3T3-L1 cells. Endocrinology 138, 4941-4949.
168. Wang, C. C., Ng, C. P., Shi, H., Liew, H. C., Guo, K., Zeng, Q. and Hong, W.(2010). A role for VAMP8/endobrevin in surface deployment of the water channel aquaporin 2. Mol. Cell. Biol. 30, 333-343.
169. Wardzala, L. J. and Jeanrenaud, B.(1983). Identification of the D-glucose-inhibitable cytochalasin B binding site as the glucose transporter in rat diaphragm plasma and microsomal membranes. Biochim. Biophys. Acta 730, 49-56.
170. Wardzala, L. J., Simpson, I. A., Rechler, M. M. and Cushman, S. W.(1984). Potential mechanism of the stimulatory action of insulin on insulin-like growth factor II binding to the isolated rat adipose cell. Apparent redistribution of receptors cycling between a large intracellular pool and the plasma membrane. J. Biol. Chem. 259, 8378-8383.
171. Whitehead, J. P., Molero, J. C., Clark, S., Martin, S., Meneilly, G. and James, D. E.(2001). The role of Ca2+ in insulin-stimulated glucose transport in 3T3-L1 cells. J. Biol. Chem. 276, 27816-27824.
172. Widberg, C. H., Bryant, N. J., Girotti, M., Rea, S. and James, D. E.(2003). Tomosyn interacts with the t-SNAREs syntaxin4 and SNAP23 and plays a role in insulinstimulated GLUT4 translocation. J. Biol. Chem. 278, 35093-35101.
173. Xiong, W., Jordens, I., Gonzalez, E. and McGraw, T. E.(2010). 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. Mol. Biol. Cell 21, 1375-1386.
174. Xu, Y., Rubin, B. R., Orme, C. M., Karpikov, A., Yu, C., Bogan, J. S. and Toomre, D. K.(2011). Dual-mode of insulin action controls GLUT4 vesicle exocytosis. J. Cell Biol. 193, 643-653.
175. Yang, J., Clark, A. E., Kozka, I. J., Cushman, S. W. and Holman, G. D.(1992). Development of an intracellular pool of glucose transporters in 3T3-L1 cells. J. Biol. Chem. 267, 10393-10399.
176. Yang, Q., Graham, T. E., Mody, N., Preitner, F., Peroni, O. D., Zabolotny, J. M., Kotani, K., Quadro, L. and Kahn, B. B.(2005). Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436, 356-362.
177. Yip, M. F., Ramm, G., Larance, M., Hoehn, K. L., Wagner, M. C., Guilhaus, M. and James, D. E.(2008). CaMKII-mediated phosphorylation of the myosin motor Myo1c is required for insulin-stimulated GLUT4 translocation in adipocytes. Cell Metab. 8, 384-398.
178. Yoshizaki, T., Imamura, T., Babendure, J. L., Lu, J. C., Sonoda, N. and Olefsky, J. M.(2007). Myosin 5a is an insulin-stimulated Akt2 (protein kinase Bbeta) substrate modulating GLUT4 vesicle translocation. Mol. Cell. Biol. 27, 5172-5183.
179. Yu, C., Cresswell, J., Loffler, M. G. and Bogan, J. S.(2007). The glucose transporter 4-regulating protein TUG is essential for highly insulin-responsive glucose uptake in 3T3-L1 adipocytes. J. Biol. Chem. 282, 7710-7722.
180. 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.
181. Zerial, M. and McBride, H.(2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2, 107-117.
182. 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.
183. Zisman, A., Peroni, O. D., Abel, E. D., Michael, M. D., Mauvais-Jarvis, F., Lowell, B. B., Wojtaszewski, J. F., Hirshman, M. F., Virkamaki, A., Goodyear, L. J. et al.(2000). Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat. Med. 6, 924-928.