Moving GLUT4: The biogenesis and trafficking of GLUT4 storage vesicles

Diabetes

Volumn 46, Issue 11, 1997, Pages 1667-1677

  Rea, Shane ^a   James, David E ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER; INSULIN;

ADIPOCYTE; CELL VACUOLE; ENDOSOME; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; HUMAN; INTRACELLULAR TRANSPORT; MUSCLE CELL; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVIEW;

EID: 0030669618     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diab.46.11.1667     Document Type: Review

References (90)

1. Suzuki K, Kono T: Evidence that insulin causes the translocation of glucose transport activity to the plasma membrane from an intracellular storage site. Proc Natl Acad Sci 77:2542-2545, 1980
2. Cushman SW, Wardzala LJ: 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, 1980
3. Rothman JE, Warren G: Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Current Biology 4:220-233,1994
4. Bennett MK, Scheller RH: The molecular machinery for secretion is conserved from yeast to neurons. Proc Natl Acad Sci USA 90:2559-2563, 1993
5. Sudhof TC: The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375:645-653, 1995
6. Birnbaum MJ: The insulin-sensitive glucose transporter. Int Rev Cytol 137A:239-297, 1992
7. James DE, Piper RC: Insulin resistance, diabetes, and the insulin-regulated trafficking of GLUT-4. J Cell Biol 126:1123-1126, 1994
8. Bell GI, Burant CF, Takeda J, Gould GW: Structure and function of mammalian facilitative sugar transporters. J Biol Chem 268:19161-19164,1993
9. Gould GW, Merrall NW, Martin S, Jess TJ, Campbell IW, Calderhead DM, Gibbs EM, Holman GD, Plevin RJ: 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 Signalling 6:313-320, 1994
10. Merrall NW, Plevin R, Gould GW: Growth factors, mitogens, oncogenes and the regulation of glucose transport. Cell Signalling 5:667-675, 1993
11. Sviderskaya EV, Jazrawi E, Baldwin SA, Widnell CC, Pasternak CA: Cellular stress causes accumulation of the glucose transporter at the surface of cells independently of their insulin sensitivity. J Membrane Biol 149:133-140, 1996
12. Kobayashi M, Nikami H, Morimatsu M, Saito M: Expression and localization of insulin-regulatable glucose transporter (GLUT4) in rat brain. Neurosci Lets 213:103-106,1996
13. McCall AL, van Bueren AM, Huang L, Stenbit A, Celnik E, Charron MJ: Forebrain endothelium expresses GLUT4, the insulin-responsive glucose transporter. Brain Res 744:318-326, 1997
14. Anderson T, Martin S, Berka J, James D, Slot J, Stow J: Distinct localization of renin and GLUT4 in juxtaglomerular cells of mouse kidney. Am J Physiol: Renal. In press
15. Toyoda N, Robinson FW, Smith MM, Flanagan JE, Kono T: Apparent translocation of glucose transport activity in rat epididymal adipocytes by insulin-like of high pH or hyperosmolarity. J Biol Chem 261:2117-2122, 1986
16. Katz EB, Stenbit AE, Hatton K, DePinho R, Charron MJ: Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature 377:151-155, 1995
17. James DE, Jenkins AB, Kraegen EW: Heterogeneity of insulin action in individual muscles in vivo: euglycemic clamp studies in rats. Am J Physiol 248:E567-E574, 1985
18. DeFronzo RA, Ferrannini E: Insulin resistance: a multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabet Care 14:173-194, 1991
19. Studelska DR, Campbell C, Pang S, Rodnick KJ, James DE: Developmental expression of insulin-regulatable glucose transporter GLUT-4. Am J Physiol 263:E102-E106, 1992
20. Slot JW, Geuze HJ, Gigengack S, Lienhard GE, James DE: Immunolocalization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J Cell Biol 113:123-135,1991
21. Slot JW, Geuze HJ, Gigengack S, James DE, Lienhard GE: Translocation of the glucose transporter GLUT4 in cardiac myocytes of the rat. Proc Natl Acad Sei USA 88:7815-7819, 1991
22. Piper RC, Hess LJ, James DE: Differential sorting of two glucose transporters expressed in insulin-sensitive cells. Am J Physiol 260:C570-C580, 1991
23. Martin S, Tellam J, Livingstone C, Slot JW, Gould GW, James DE: 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, 1996
24. Zorzano A, Wilkinson W, Kotliar N, Thoidis G, Wadzinkski BE, Ruoho AE, Pilch PF: Insulin-regulated glucose uptake in rat adipocytes is mediated by two transporter isoforms present in at least two vesicle populations. J Biol Chem 264:12358-12363,1989
25. Robinson LJ, Pang S, Harris DS, HeuserJ, James DE: Translocation of the glucose transporter (GLUT4) to the cell surface in permeabilized 3T3-L1 adipocytes: effects of ATP, insulin and GTPgS and localization of GLUT4 to clathrin lattices. J Cell Biol 117:1181-1196,1992
26. Livingstone C, James DE, Rice JE, Hanpeter D, Gould GW: Compartment ablation analysis of the insulin-responsive glucose transporter (GLUT4) in 3T3-L1 adipocytes. Biochem J 315:487-495, 1996
27. Herman GA, Bonzelius F, Cieutat A-M, Kelly RB: A distinct class of intracellular storage vesicles, identified by expression of the glucose transporter GLUT4. Proc Natl Acad Sci USA 91:12750-12754, 1994
28. Martin S, Rice JE, Gould GW, Keller SR, Slot JW, James DE: The glucose transporter GLUT4 and the aminopeptidase vp165 colocalise in tubulovesicular elements in adipocytes and cardiomyocytes. J Cell Sci. In press
29. Kandror KV, Pilch PF: gp160, a tissue-specific marker for insulin-activated glucose transport. Proc Natl Acad Sci USA 91:8017-8021, 1994
30. Ross SA, Scott HM, Morris NJ, Leung WY, Mao F, Lienhard GE, Keller SR: Characterization of the insulin-regulated membrane aminopeptidase in 3T3-L1 adipocytes. J Biol Chem 271:3328-3332, 1996
31. Hudson AW, Fingar DC, Seidner GA, Griffiths G, Burke B, Birnbaum MJ: Targeting of the "insulin-responsive" glucose transporter (GLUT4) to the regulated secretory pathway in PC12 cells. J Cell Biol 122:579-588, 1993
32. Slot JW, Garruti G, Martin S, Oorschot V, Posthuma G, Kraegen EW, Laybutt R, Thibault G, James DE: Glucose transporter (GLUT-4) is targeted to secretory granules in rat atrial cardiomyocytes. J Cell Biol 137:1-12, 1997
33. James DE, Piper RC, Slot JW: Insulin stimulation of GLUT-4 translocation: a model for regulated recycling. Trends Cell Biol 4:120-126, 1994
34. Shepherd PR, Nave BT, Orahilly S: The role of phosphoinositide 3-kinase in insulin signalling. J Mol Endocrinol 17:175-184, 1996
35. White MF, Kahn CR: The insulin signaling system. J Biol Chem 269:1-4,1994
36. Kanai F, Nishioka Y, Hayashi H, Kamohara S, Todaka M, Ebina Y: 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, 1993
37. Cormont M, Bortoluzzi M-N, Gautier N, Mari M, Van Obberghen E, Le Marchand-Brustel Y: Potential role of Rab4 in the regulation of subcellular localization of GLUT4 in adipocytes. Molecular and Cellular Biology 16:6879-6886, 1996
38. Shibata H, Omata W, Suzuki Y, Tanaka S, Kojima I: A synthetic peptide corresponding to the Rab4 hypervariable carboxyl-terminal domain inhibits insulin action on glucose transport in rat adipocytes. J Bio Chem 271:9704-9709, 1996
39. Shepherd PR, Reaves BJ, Davidson HW: Phosphoinositide 3-kinases and membrane traffic. Trends Cell Biol 6:92-97, 1996
40. Stoorvogel W, Oorschot V, Geuze HJ: A novel class of clathrin-coated vesicles budding from endosomes. J Cell Biol 132:21-33, 1996
41. Schmidt A, Hannah MJ, Huttner WB: Synaptic-like microvesicles of neuroendocrine cells originate from a novel compartment that is continuous with the plasma membrane and devoid of transferrin receptor. J Cell Biol 137: 445-158, 1997
42. Robinson LJ, James DE: Insulin-regulated sorting of glucose transporters in 3T3-L1 adipocytes. Am J Physiol 263:E383-E393, 1992
43. Rodnick KJ, Slot JW, Studelska DR, Hanpeter DE, Robinson LJ, Geuze HJ, James DE: Immunocytochemical and biochemical studies of GLUT4 in rat skeletal muscle. J Biol Chem 267:6278-6285, 1992
44. Marks MS, Ohno H, Kirchausen T, Bonifacino JS: Protein sorting by tyrosinebased signals: adapting to the Ys and wherefores. J Cell Biol 7:124-128, 1997
45. 2 terminus contains a phenylalanine-based targeting motif that regulates intracellular sequestration. J Cell Biol 121:1221-1232, 1993
46. Garippa RJ, Judge TW, James DE, McGraw TE: The amino terminus of GLUT4 functions as an internalisation motif but not an intracellular retention signal when substituted for the transferrin receptor cytoplasmic domain. J Cell Biol 124:705-716, 1994
47. Verhey KJ, Birnbaum MJ: A Leu-Leu sequence is essential for COOH-terminal targeting signal of GLUT4 glucose transporter in fibroblasts. J Biol Chem 269:2353-2356, 1994
48. Marsh BJ, Aim RA, McIntosh SR, James DE: Molecular regulation of GLUT-4 targeting in 3T3-L1 adipocytes. J Cell Biol 130:1081-1091, 1995
49. Verhey KJ, Yeh J-I, Birnbaum MJ: Distinct signals in the GLUT4 glucose transporter for internalization and for targeting to an insulin-responsive compartment. J Cell Biol 130:1071-1079, 1995
50. Garippa RJ, Johnson A, Park J, Petrush RL, McGraw TE: The carboxyl terminus of GLUT4 contains a serine-leucine-leucine sequence that functions as a potent internalization motif in Chinese hamster ovary cells. J Biol Chem 271:20660-20668, 1996
51. James DE, Hiken J, Lawrence JC: Isoproterenol stimulates phosphorylation of the insulin-regulatable glucose transporter in rat adipocytes. Proc Natl Acad Sci 86:8368-8372, 1989
52. Bennett MK, Calakos N, Kreiner T, Serieller RH: Synaptic vesicle membrane proteins interact to form a multimeric complex. J Cell Biol 116:761-775, 1992
53. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE: SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318-324, 1993
54. Beckers CJM, Block MR, Glick BS, Rothman JE, Balch WE: Vesicular transport between the endoplasmic reticulum and the Golgi stack requires the NEM-sensitive fusion protein. Nature 339:397-398, 1989
55. Diaz R, Mayorga LS, Weidman PJ, Rothman JE, Stahl PD: Vesicle fusion following receptor-mediated endocytosis requires a protein active in Golgi transport. Nature 339:398-400, 1989
56. Wilson DW, Wilcox CA, Flynn GC, Chen E, Kuang W-J, Henzel WJ, Block MR, Ullrich A, Rothman JE: A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast. Nature 339:355-359, 1989
57. Bock JB, Scheller RH: A fusion of new ideas. Nature 387:133-134, 1997
58. Aalto MK, Ronne H, Keranen S: Yeast syntaxins SSO1p and SSO2p belong to a family of related membrane proteins that function in vesicular transport. EMBO J 12:4095-4104, 1993
59. Niemann H, Blasi J, Jahn R: Clostridial neurotoxins: new tools for dissecting exocytosis. Trends Cell Biol 4:179-185, 1994
60. Cain CC, Trimble WS, Lienhard GE: 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, 1992
61. Volchuk A, Sargeant R, Sumitani S, Liu Z, He L, Klip A: Cellubrevin is a resident protein of insulin-sensitive GLUT4 glucose transporter vesicles in 3T3-L1 adipocytes. J Biol Chem 270:8233-8240,1995
62. McMahon HT, Ushkaryov YA, Edelman L, Link E, Binz T, Niemann H, Jahn R, Sudhof TC: Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature 364:346-349, 1993
63. Calakos N, Bennett MK, Peterson KE, Scheller RH: Protein-protein interactions contributing to the specificity of intracellular vesicular trafficking. Science 263:1146-1149, 1994
64. Tellam JT, Macaulay SL, McIntosh S, Hewish DR, Ward CW, James DE: Characterization of Munc-18c and Syntaxin 4 in 3T3-L1 adipocytes. J Biol Chem 272:6179-6186, 1997
65. Volchuk A, Wang Q, Ewart S, Liu Z, He L, Bennett MK, Klip A: Syntaxin 4 in 3T3-L1 adipocytes: regulation by insulin and participation in insulin-dependent glucose transport. Mol Biol Cell 7:1075-1082, 1996
66. Popov SV, Poo M-M: Synaptotagmin: a calcium-sensitive inhibitor of exocytosis. Cell 73:1247-1249, 1993
67. Ploug T, Galbo H, Vinten J, Jogensen M, Richter EA: Kinetics of glucose transport in rat muscle: effects of insulin and contractions. Am J Physiol 253:E12-E20, 1987
68. Holloszy JO, Narahara HT: Enhanced permeability to sugar associated with muscle contraction. Studies on the role of Ca++. J Gen Physiol 50:551-562, 1967
69. Mayer A, Wickner W, Haas A: Sec 18p (NSF)-driven release of Sec 17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles. Cell 85:83-94,1996
70. Pevsner J, Hsu S-C, Braun JEA, Calakos N, Ting AE, Bennett MK, Scheller RH: Specificity and regulation of a synaptic vesicle docking complex Neuron 13:353-361, 1994
71. Veit M, Sollner TH, Rothman JE: Multiple palmitoylation of synaptotagmin and the t-SNARE SNAP-25. FEBS Letters 385:119-123, 1996
72. Hayashi T, McMahon H, Yamasaki S, Binz T, Hata Y, Sudhof TC, Niemann H: Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J 13:5051-5061, 1994
73. Fujita Y, Sasaki T, Fukui K, Kotani H, Kimura T, Hata Y, Sudhof TC, Scheller RH, Takai Y: Phosphorylation of Munc-18/n-Sec1/rbSec1 by protein kinase C. J Biol Chem 271:7265-7268, 1996
74. Wang G, Witkin JW, Hao G, Bankaitis VA, Scherer PE, Baldini G: Syndet is a novel SNAP-25 related protein expressed in many tissues. J Cell Sci 110:505-513, 1997
75. Wong PP, Daneman N, Volchuk A, Lassam N, Wilson MC, Klip A, Trimble WS: Tissue distribution of SNAP-23 and its subcellular localization in 3T3-L1 cells. Biochem Biophys Res Commun 230:64-68, 1997
76. Verkman AS, Lencer WI, Brown D, Ausiello DA: Endosomes from kidney collecting tubule cells contain the vasopressin-sensitive water channel. Nature 333:268-269, 1988
77. Roush DL, Gottardi CJ, Caplan MJ: Sorting of the gastric H,K-ATPase in endocrine and epithelial cells. Ann NY Acad Sci 733:212-222,1994
78. Edelmann L, Hanson PI, Chapman ER, Jahn R: Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J 14:224-231, 1995
79. Skehel PA, Martin KC, Kandel ER, Bartsch D: A VAMP-binding protein from aplysia required for neurotransmitter release. Science 269:1580-1583, 1995
80. Pfeffer SR: Rab GTPases: master regulators of membrane trafficking. Current Opinion in Cell Biology 6:522-526, 1994
81. Mayer A, Whickner W: Docking of yeast vacuoles is catalyzed by the Ras-like GTPase Ypt7 after symmetric priming by Sec18 (NSF). J Cell Bio 136:307-317, 1997
82. Xu Z, Mayer A, Muller E, Whickner W: A heterodimer of Thioredoxin and IB2 cooperates with Sec 18p (NSF) to promote yeast vacuole inheritance. J Cell Bio 136:229-306,1997
83. Lupashin W, Waters MG: t-SNARE activation through transient interaction with a Rab-like guanosine triphosphatase. Science 276:1255-1258, 1997
84. Cormont M, Tanti JF, Gremeaux T, Van OE, Le M, Brustel Y: Subcellular distribution of low molecular weight guanosine triphosphate-binding proteins in adipocytes: colocalization with the glucose transporter Glut 4. Endocrinology 129:3343-3350, 1991
85. Mora S, Monden I, Zorzano A, Keller K: Heterologous expression of Rab4 reduces glucose transport and GLUT4 abundance at the cell surface in oocytes. Biochem J 324:445-459, 1997
86. van der Sluijs P, Hull M, Webster P, Male P, Goud B, Mellman L The small GTP binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70:729-740, 1992
87. Shibata H, Omata W, Kojima I: Insulin stimulates guanine nucleotide exchange on Rab4 via a Wortmannin-sensitive signalling pathway in rat adipocytes. J Bio Chem 272:14542-14546, 1997
88. Klarlund JK, Guilherme A, Holik JJ, Virbasius JV, Chawla A, Czech MP: Signalling by phosphoinosiude-3,4,5-trisphosphate through proteins containing pleckstrin and Sec7 homology domains. Science 275:1927-1930,1997
89. Pascoe W, Inukai K, Oka Y, Slot J, James D: Differential targeting of facilitative glucose transporters in polarized epithelial cells. Am J Physiol 271:C547-C554, 1996
90. Tsakiridis T, Vranic M, Klip A: Disassembly of the actin network inhibits insulin-dependent stimulation of glucose transport and prevents recruitment of glucose transporters to the plasma membrane. J Bio Chem 269:29934-29942, 1994