Immunocytochemical evidence that GLUT4 resides in a specialized translocation post-endosomal VAMP2-positive compartment in rat adipose cells in the absence of insulin

Journal of Histochemistry and Cytochemistry

Volumn 45, Issue 8, 1997, Pages 1083-1095

  Malide, Daniela ^a,b   Dwyer, Nancy K ^a   Blanchette Mackie, E Joan ^a   Cushman, Samuel W ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Adipose cells; GLUT4; Immunofluorescence; Insulin

Indexed keywords

CLATHRIN; GLUCOSE; GLUCOSE TRANSPORTER; INSULIN; MANNOSIDASE; MEMBRANE PROTEIN; SOMATOMEDIN B RECEPTOR; SYNAPTOBREVIN; TRANSFERRIN RECEPTOR;

ADIPOSE TISSUE CELL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOSOME; GLUCOSE TRANSPORT; GOLGI COMPLEX; IMMUNOCYTOCHEMISTRY; MALE; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT;

ANIMALIA;

EID: 0030786951     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1177/002215549704500806     Document Type: Article

References (70)

1. Anderson RGW, Kamen BA, Rothberg KG, Lacey SW (1992) Potocytosis: sequestration and transport of small molecules by caveolae. Science 255:410-413
2. Appell KC, Simpson IA, Cushman SW (1988) Characterization of the stimulatory action of insulin on insulin-like growth factor ll binding to rat adipose cells. Differences in the mechanism of insulin action on insulin-like growth factor ll receptors and glucose transporters. J Biol Chem 263:10824-10829
3. Birnbaum MJ (1992) The insulin-sensitive glucose transporter. Int Rev Cytol 137A:239-297
4. Burke B, Griffiths G, Reggio H, Louvard D, Warren G (1982) A monoclonal antibody against a 135 K Golgi membrane protein. EMBO J 1:1621-1628
5. Cain CC, Trimble WS, Lienhard GE (1992) Members ot the VAMP family of synaptic vesicle proteins are components of glucose transporter-containing vesicles from rat adipocytes. J Biol Chem 267:11681-11684
6. Chavez RA, Miller SG, Moore H-PH (1996) A biosynthetic regulated secretory pathway in constitutive secretory cells. J Cell Biol 133:1177-1191
7. Cushman SW, Wardzala LJ (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
8. Dahan S, Ahluwalia JP, Wong L, Posner BI, Bergeron JJM (1994) Concentration of intracellular hepatic apolipoprotem E in Golgi apparatus saccular distensions and endosomes. J Cell Biol 127:1859-1869
9. Davis RJ, Corvera S, Czech MP (1986) Insulin stimulates cellular iron uptake and causes the redistribution of intracellular transferrin receptors to the plasma membrane. J Biol Chem 261:8708-8711
10. Foley JE, Kashiwagi A, Verso MA, Reaven G, Andrews J (1983) Improvement in in vitro insulin action after one months insulin therapy in obese non-insulin dependent diabetes: measurements of glucose transport and metabolism, insulin binding and lipolysis in isolated adipocytes. J Clin Invest 72:1901-1909
11. Gaisano HY, Sheu L, Foksett JK, Trimble WS (1994) Tetanus toxin light chain cleaves a vesicle-associated membrane protein (VAMP) isoform 2 in rat pancreatic zymogen granules and inhibits enzyme secretion. J Biol Chem 269:17062-17066
12. Griffiths G (1993) Fine Structure Immunocytochemistry. Berlin, Heidelberg, Springer-Verlag
13. Grote E, Kelly RB (1996) Endocytosis of VAMP is facilitated by a synaptic vesicle targeting signal. J Cell Biol 132:537-547
14. Hanpeter H, James DE (1995) Characterization of the intracellular GLUT-4 compartment. Mol Membr Biol 12:263-269
15. Herman GA, Bonzelius F, Cieutat A-M, Kelly RB (1994) Evidence for a class of intracellular storage vesicles, identified by expression of glucose transporter GLUT4. Proc Natl Acad Sci USA 91:12750-12754
16. Holman GD, Cushman SW (1994) Subcellular localization and trafficking of the GLUT4 glucose transporter isoform in insulin-responsive cells. Bioessays 10:753-759
17. Holman GD, Kozka IJ, Clark AE, Flower CJ, Saltis J, Habberfield AD, Simpson IA, Cushman SW (1990) Cell surface labeling of glucose transporter isoform GLUT4 by bis-mannose photolabel. Correlation with stimulation of glucose transport in rat adipose cells by insulin and phorbol ester. J Biol Chem 265:18172-18179
18. Holman GD, Leggio LL, Cushman SW (1994) Insulin-stimulated GLUT4 glucose transporter recycling. A problem in membrane protein subcellular trafficking through multiple pools. J Biol Chem 269:17516-17524
19. Horn M, Banting G (1994) Okadaic acid treatment leads to a fragmentation of the trans-Golgi network and an increase in expression of TGN38 at the cell surface. Biochem J 301:69-73
20. Hudson AW, Fingar DC, Seidner GA, Griffith G, Burke B, Birnbaum MJ (1993) Targeting of the insulin-responsive glucose transporter (GLUT4) to the regulated secretory pathway in PC12 cells. J Cell Biol 122:579-588
21. Hudson AW, Ruiz M, Birnbaum MJ (1992) Isoform-specific subcellular targeting of glucose transporter in mouse fibroblast. J Cell Biol 116:785-797
22. Jhun BH, Rampal AL, Liu H, Lachaal M, Jung CY (1992) Effects of insulin on steady state kinetics of GLUT4 subcellular distribution in rat adipocytes. J Biol Chem 267:17710-17715
23. Kandror K, Pilch PF (1994) Identification and isolation of glycoproteins that translocate to the cell surface from GLUT4-enriched vesicles in an insulin-dependent fashion. J Biol Chem 269:138-142
24. Kandror KV, Pilch PF (1996) The IGFll/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
25. Kandror KV, Yu L, Pilch PF (1994) The major protein of GLUT4-containing vesicles, gp 160 has aminopeptidase activity. J Biol Chem 269:30777-30780
26. Karnieli E, Zarnowski MJ, Hissin PJ, Simpson IA, Salans LB, Cushman SW (1981) Insulin stimulated translocation of glucose transport systems in the isolated adipose cell: time course, reversal, insulin concentration dependency and relationship to glucose transport activity. J Biol Chem 256:4772-4777
27. Laurie SM, Cain CC, Lienhard GE, Castle JD (1993) The glucose transporter GLUT4 and the secretory carrier membrane proteins (SCAMPs) colocalize in rat adipocyte and partially segregate during insulin stimulation. J Biol Chem 268:19110-19117
28. Lewis V, Green SA, Marsh M, Vihko P, Helenius A, Mellman I (1985) Glycoproteins of the lysosomal membrane. J Cell Biol 100:1839-1847
29. Livingstone C, James DE, Rice JE, Hanpeter D, Gould GW (1996) Compartment ablation analysis of the insulin-responsive glucose transporter (GLUT4) in 3T3-L1 adipocytes. Biochem J 315:487-495
30. Luzio JP, Banting G (1993) Eukaryotic membrane traffic: retrieval and retention mechanisms to achieve organelle residence. Trends Biochem Sci 18:395-398
31. Luzio JP, Brake B, Banting G, Howell KE, Braghetta P, Stanley KK (1990) Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38). Biochem J 270:97-102
32. Malide D, Tosh D, Clark AE, Cushman SW, Holman GD (1996) Altered GLUT4 subcellular trafficking in primary adipose cell cultures: immunocytochemical evidence. Mol Biol Cell 7(suppl):A2636
33. Martin S, Reaves B, Banting G, Gould GW (1994). Analysis of the co-localization of the insulin-responsive glucose transporter (GLUT4) and the trans-Golgi network marker TGN38 within 3T3-L1 adipocytes. Biochem J 300:743-749
34. Martin S, Tellam J, Livingstone C, Slot JW, Gould GW, James DE (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
35. Mastick CC, Aebersold R, Lienhard GE (1994) Characterization of a major protein in GLUT4 vesicles. J Biol Chem 269:6089-6092
36. Matsumoto B, ed. (1993) Cell biological applications of confocal microscopy. Methods in Cell Biology. Vol 38. San Diego, Academic Press
37. McKeel DW, Jarett L (1970) Preparation and characterization of a plasma membrane fraction from isolated fat cells. J Cell Biol 44:417-432
38. McMahon HT, Ushkaryov YA, Edelman L, Link E, Binz T, Niemann H, Jahn R, Sudhof TC (1993) Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature 359:346-349
39. Nielsen S, Marples D, Birn H, Mohtashami M, Dalby NO, Trimble W, Knepper M (1995) Expression of VAMP2-like protein in kidney collecting duct intracellular vesicles. Colocalization with aquaporin-2 water channels. J Clin Invest 96:1834-1844
40. Omatsu-Kanbe M, Zarnowski MJ, Cushman SW (1996) Hormonal-regulation of glucose transport in a brown adipose cell preparation isolated from rats that show a large response to insulin. Biochem J 315:25-31
41. Page LJ, Robinson MS (1995) Targeting signals and subunit interactions in coated vesicle adaptor complexes. J Cell Biol 131:619-630
42. Pawley, J, ed. (1995) The Handbook of Biological Confocal Microscopy. Madison, WI, IMR Press
43. Pearse BM, Robinson MS (1990) Clathrin, adaptors, and sorting. Annu Rev Cell Biol 6:151-171
44. Ploug T, Wojtaszewski J, Kristiansen S, Hespel P, Galbo H, Richter EA (1993) Glucose transport and transporters in muscle giant vesicles: differential effects of insulin and contractions. Am J Physiol 264:E270-E278
45. Ralston ES, Beushausen S, Ploug T (1994) Expression of the synaptic vesicle proteins VAMPs/synaptobrevins 1 and 2 in non-neural tissues. J Biol Chem 269:15403-15406
46. Reaves BJ, Bright NA, Mullock BM, Luzio JP (1996) The effect of wortmannin on the localization of lysosomal type l integral membrane glycoproteins suggests a role for phophoinositide 3-kinase activity in regulating membrane traffic late in the endocytic pathway. J Cell Sci 109:749-762
47. Robinson LJ, Pang S, Harris DS, Heuser J, James DE (1992) Translocation of the glucose transporter (GLUT4) to the cell surface in permeabilized 3T3-L1 adipocytes: effects of ATP, insulin, and GTPγS and localization of GLUT4 to clathrin lattices. J Cell Biol 117:1181-1196
48. Satoh S, Nishimura H, Clark AE, Kozka IJ, Vannucci SJ, Simpson IA, Quon MJ, Cushman SW, Holman GD (1993) Use of bismannose photolabel to elucidate the 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
49. Simpson F, Bright NA, West MA, Newman LS, Darnell RB, Robinson MS (1996) A novel adaptor-related protein complex. J Cell Biol 133:749-760
50. Simpson IA, Yver DR, Hissin PJ, Wardzala LJ, Karnielli E, Salans LB, Cushman SW (1983) Insulin-stimulated translocation of glucose transporters in the isolated rat adipose cells: characterization of subcellular fractions. Biochim Biophys Acta 763:393-407
51. Slot IW, Geuze HJ, Gigengack S, Lienhard GE, James DE (1991) Immunolocalization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J Cell Biol 113:123-135
52. Smith RM, Charron MJ, Shah N, Lodish HF, Jarett L (1991) Immunoelectron microscopic demonstration of insulin-stimulated translocation of glucose transporters to the plasma membrane of isolated rat adipocytes and masking of the carboxyl-terminal epitope of intracellular GLUT4. Proc Natl Acad Sci USA 88:6893-6897
53. Stephens JM, Pilch PF (1995) The metabolic regulation and vesicular transport of GLUT4, the major insulin-responsive glucose transporter. Endocrine Rev 16:529-546
54. Sudhof TC, Baumert M, Perin MS, Jahn R (1989) A synaptic vesicle membrane protein is conserved from mammals to Drosophila. Neuron 2:1475-1481
55. Suzuki K, 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
56. Tanner LI, Lienhard GE (1989) Localization of transferrin receptors and insulin-like growth factor ll receptors in vesicles from 3T3-L1 adipocytes that contain intracellular glucose transporters. J Cell Biol 108:1537-1545
57. Tanner LI, Lienhard GE (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
58. Thoidis GN, Kotliar N, Pilch PF (1993) Immunological analysis of GLUT4-enriched vesicles. J Biol Chem 268:11691-11696
59. Thorens B, Roth J (1996) Intracellular targeting of GLUT4 in transfected insulinoma cells: evidence for association with constitutively recycling vesicles distinct from synaptophysin and insulin vesicles. J Cell Sci 109:1311-1323
60. Timmers KI, Clark AE, Omatsu-Kanbe M, Whiteheart SW, Bennett MK, Holman GD, Cushman SW (1996) Identification of SNAP receptors in rat adipose cell membrane fractions and in SNARE complexes co-immunoprecipitated with epitope-tagged NSF. Biochem J 320:429-436
61. Trimble WS (1993) Analysis of structure and expression of the VAMP family synaptic proteins. J Physiol (Paris) 87:107-114
62. Vannucci SJ, Nishimura H, Satoh S, Cushman SW, Holman GD, Simpson IA (1992) Cell surface accessibility of GLUT4 glucose transporters in insulin-stimulated rat adipose cells. Modulation by isoprenaline and adenosine. Biochem J 288:325-330
63. Verhey KJ, Yeh JI, Birnbaum MJ (1995) Distinct signals in the GLUT4 glucose transporter for internalization and for targeting to insulin-responsive compartment. J Cell Biol 130:1071-1079
64. Vinten J, Gliemann J, Osterlind J (1976) Exchange of 3-O-methyl-glucose in isolated fat cells. Concentration dependence and effect of insulin. J Biol Chem 251:794-800
65. Volchuk A, Mitsumoto Y, He L, Lui Z, Habermann E, Trimble WS, Klip A (1994) Expression of vesicle-associated membrane protein 2 (VAMP2)/synaptobrevin ll and cellubrevin in rat skeletal muscle and in a muscle cell line. Biochem J 304:139-145
66. Volchuk A, Sargeant R, Sumitani S, Lui Z, He L, 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
67. +-ATPase and glucose transporter isoform in rat adipocyte plasma membrane by immunogold labeling. J Membr Biol 136:63-73
68. Weber TM, Joost HG, Simpson IA, Cushman SW (1988) Methods for assessment of glucose transport activity and the number of glucose transporters in isolated rat adipose cells and membrane fractions. In Kahn CR, Harrison LC, eds. The Insulin Receptor. Part B. New York, Alan R. Liss, 171-187
69. Yang J, Holman GD (1993) Comparison of GLUT4 and GLUT1 subcellular trafficking in basal and insulin-stimulated 3T3-L1 cells. J Biol Chem 268:4600-4603
70. Zorzano A, Wilkinson W, Kotliar N, Thoidis G, Wadzinkski BE, Ruoho AE, Pilch PF (1989) 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