Characterization of two distinct intracellular GLUT4 membrane populations in muscle fiber. Differential protein composition and sensitivity to insulin

Endocrinology

Volumn 138, Issue 7, 1997, Pages 3006-3015

  Sevillat, Libia ^a   Tomas, Eva ^a   Muñoz, Purificaciön ^b   Gumà, Anna ^a   Fischer, Yvan ^c   Thomas, Julia ^d   Ruiz Montasell, Bonaventura ^a   Testar, Xavier ^a   Palacin, Manuel ^a   Blasi, Joan ^b   Zorzano, Antonio ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c Ministerio do Educatión y Ciencia ^*  (Spain)

^d Institut Universitari de Salut Pública de Catalunya   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELLUBREVIN; GLUCOSE TRANSPORTER; INSULIN; SCAMP PROTEIN; SYNTAXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; FEMALE; GLUCOSE METABOLISM; INSULIN SENSITIVITY; INTRACELLULAR TRANSPORT; MALE; MEMBRANE VESICLE; MUSCLE FIBER MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; TRANSPORT KINETICS;

ANIMALS; BIOLOGICAL TRANSPORT; GLUCOSE TRANSPORTER TYPE 4; INSULIN; MALE; MEMBRANE PROTEINS; MONOSACCHARIDE TRANSPORT PROTEINS; MUSCLE FIBERS; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOCARDIUM; NERVE TISSUE PROTEINS; R-SNARE PROTEINS; RATS; RATS, WISTAR; SNARE PROTEINS; SYNTAXIN 1; TISSUE DISTRIBUTION; VESICLE-ASSOCIATED MEMBRANE PROTEIN 3; VESICULAR TRANSPORT PROTEINS;

EID: 8244241098     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.138.7.3006     Document Type: Article

References (64)

1. Santalucía T, Camps M, Castellô, A, Muñoz F, Nuel A, Testai X, Palacín M, Zorzano A 1992 Developmental regulation of GLUT-1 (Etytroid/HepG2) and GLUT-4 (muscle/fat) glucose transporter expression in rat-heart, skeletalmuscle, and brown adipose-tissue. Endocrinology 130:837-846
2. Castelló, A, Cadefau J, Cussô, R, Testar X, Hesketh JE, Palacin M, Zorzano A 1993 Glut-4 and Glut-1 glucose transporter expression is regulated by contractile activity in skeletal-muscle. J Biol Chem 268:14998-15003
3. Castello, A, Rodriguez-Manzaneque JC, Camps M, Pérez-Castillo A, Testar X, Palacîn M, Santos A, Zorzano A1994 Perinatal hypothyroidism impairs the normal transition of GLUT4 and GLUT1 glucose transporters from fetal to neonatal levés in heart and brown adipose tissue. Evidence for tissue-specific regulation of GLUT4 expression by thyroid hormone. J Biol Chem 269:5905-5912 -
4. Marette A, Richardson JM, Ramlal T, Balon TW, Vranic M, Pessin JE, Klip A 1992 Abundance, localization, and insulin-induced translocation of glucose transporters in red and white muscle. Am J Physiol 263:C443-C452
5. Munoz P, Rosemblatt MR, Testar X, Palacin M Zorzano A1995 Isolation and characterization of distinct domains of sarcolema and T-tubules from rat skeletal muscle. Biochem J 307:273-280
6. Friedman JE, Dudek RW, Whitehead DS, Downes DL, Frisell WR, Caro JF, Dohm GL 1991 Immunolocalization of glucose transporter GLUT4 within human skeletal-muscle. Diabetes 40:150-154
7. Bornemann A, Floug T, Schmalbruch H 1992 Subcellular localization of GLUT4 in nonstimulated and insulin-stimulated soleus muscle of rat. Diabetes 41:215-221
8. Rodnick KJ, Slot JW, Studelska DR, Hanpeter DE, Robinson LJ, Geuze HJ, James DE 1992 Immunocytochemical and biochemical sudies of GLUT4 in rat skeletal muscle. J Biol Chem 267:6278-6285
9. Takata K, Ezaki O, Hirano H 1992 Immunocytochemical localization of fat muscle-type glucose transporter (GLUT4) in the rat skeletal-muscle-effect of insulin-treatment. Acta Histochem Cytochem 25:689-696
10. Zorzano A, Munoz P, Camps M, Mora C, Testar X Falacîn M 1996 Insulininduced redistribution of GLUT4 glucose carriers in the muscle fiber: in search of GLUT4 trafficking pathways. Diabetes 45:S70-S81
11. Douen AG, Ramlal T, Cariée GD, Klip A1990 Exercise modulates the insulininduced translocation of glucose transporters in rat skeletal-muscle. FEES Lett 261:256-260
12. Douen AG, Ramlal T, Rastogi S, Bilan PJ, Cartee GD, Vranic M, Holloszy JO, Klip A1990 Exercise induces recruitment of the insulin-responsive glucose transporter - evidence for distinct intracellular insulin-recruitable and exerciserecruitable transporter pools in skeletal-muscle. J Biol Chem 265:3427-3430
13. Hirshman MF, Goodyear LJ, Wardzala LJ, Horion ED, Horion ES 1990 Identification of an intracellular pool of glucose transporters from basal and insulinstimulated rat skeletal-muscle. J Biol Chem 265:987-991
14. Brozinick JT, Etgen GJ, Yaspelkis BB, Ivy JL 1994 The effects of muscle contraction and insulin on glucose-transporter translocation in rat skeletal muscle. Biochem J 297:539-545
15. Munoz P, Rosemblatt M, Testar X, Falacin M, Thoidis G, Pilch PF, Zorzano A 1995 The T-tubuIe is a cell-surface target for insulin-regulated recycling of membrane proteins in skeletal muscle. Biochem J 312:393-400
16. Goodyear LJ, Hirshman MF, Horion ES 1991 Exercise-Induced Translocation of Skeletal-Muscle Glucose Transporters. Am J Physiol 261:E795-E799
17. Lund S, Holman GD, Schmilz O, Pedersen O 1993 Glut-4 content in the plasma membrane of rat skeletal muscle - comparative studies of subcellular fraction method and the exofacial photolabelling technique using ATB-BMPA. FEES Lett 330:312-318
18. Wilson CM, Cushman SW 1994 Insulin stimulation of glucose transport activity in rat skeletal muscle: increase in cell surface GLUT4 as assessed by photolabelling. Biochem J 299:755-759
19. Marelle A, Burdelt E, Douen A, Vranic M Klip A 1992 Insulin induces the Iranslocation of GLUT4 from a unique intracellular organelle to transverse tubules in rat skeletal muscle. Diabetes 41:1562-1569
20. Dudek RW, Dohm GL, Holman GD, Cushman SW, Wilson CM 1994 Glucose transporter localization in rat skeletal muscle. Autoradiographic study using ATB-(2-3h)BMPA photolabel. FEES Lett 339:205-208
21. Del Vecchio RL, Pilch FF 1991 Phosphatidylinositol 4-kinase is a component of glucose transporter (GLUT4)-containing vesicles. J Biol Chem 266:3278 -3283
22. Thoidis G, Kotliar N, Pilch PF 1993 Immunological analysis of GLUT4-enriched vesicles - identification of novel proteins regulated by insulin and diabetes. J Biol Chem 268:11691-11696
23. Laurie SM, Cain CC, Lienhard GE, Castle JD 1993 The glucose transporter GLUT4 and secretory carrier membrane proteins (SCAMPs) colocalize in rat adipocytes and partially segregate during insulin stimulation. J Biol Chem 268:19110-19117
24. Kandror K, Pilch PF 1994 Identification and isolation of glycoproteins that translocate to the cell surface from GLUT4-enriched vesicles in an insulindependent fashion. J Biol Chem 269:138-142
25. Kandror K, Pilch PF 1994 gpl60, a tissue-specific marker for insulin-actived glucose transport. Proc Natl Acad Sei USA 91:8017-8021
26. Mastick CC, Aebersold R, Lienhard GE 1994 Charactherization of a major protein GLUT4 vesicles. Concentration in the vesicles and insulin-stimulated translocation to the plasma membrane. J Biol Chem 269:6089-6092
27. Cormont M, Tanti JF, Gremeaux T, Van Obberghen E, Le Marchand-Brustel Y 1991 Subcellular-distribution of low-molecular-weight guanosine triphosphate-binding proteins in adipocytes-colocalization with the glucose transporter GLUT4. Endocrinology 129:3343-3350
28. Cormont M, Tanti JF, Zahraoui A, Van Obberghen E, Tavitian A, Le Marchand-Brustel Y 1993 Insulin and okadaic acid induce rab4 redistri bution in adipocytes. J Biol Chem 268:19491-19496
29. Cain CC, Trimble WS, Lienhard GE 1992 Members of the VAMP family of synaptic vesicle proteins are components of glucose transporter-containing vesicles from rat adipocytes. J Biol Chem 267:1681-1684
30. Volchuk A, Sargeant R, Sumitani S, Liu Z, He L Klip A 1995 Cellubrevine is a resident protein of insulin-sensitive GLUT4 glucose transporter vesicles in 3T3-L1 adipocytes. J Biol Chem 270:8233-8240
31. 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 insulin-regulated GLUT4 subcellular trafficking kinetics in rat adipose cells. J Biol Chem 268:17820-17829
32. Clark AE, Holman GD, Kozka IJ 1991 Determination of the rates of appearance and loss of glucose transporters at the cell-surface of rat adipose-cells. Biochem J 278:235-241
33. Holman GD, Lo-Leggio L, Cushman SW 1994 Evidence for the involvement of rab3A in Ca2-dependent exocytosis from adrenal chromaffin cells. J Biol Chem 269:17516-17524
34. Verhey KJ, Yeh JI, Birnbaum MJ 1995 Distinct signals in the GLUT4 glucose transporter for internalization and for targeting to an insulin-responsive compartment. J Cell Biol 130:1071-1079
35. Yeh JI, Verhey KJ, Birnbaum MJ 1995 Kinetic analysis of glucose transporter trafficking in fibroblasts and adipocytes. Biochemistry 34:15523-15531
36. Livingstone C, James DE, Hanpeter D, Gould GW 1996 Compartment ablation analysis of the insulin-responsive glucose transporter (GLUT4) in 3T3-L1 adipocytes. Biochem J 315:487-495
37. SöIIner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE 1993 SNPA receptors implicated in vesicle targeting and fusion. Nature 362:318-324
38. Ikonen, E, Tagaya, M, Ullrich, O, Montecucco, C, Simons K 1995 Different requirements for NSF, SNAP, and RAB proteins in apical and basolateral transport in MDCK cells. Cell 81:571-580
39. Jacobsson G, Bean AJ, Scheller RH, Juntti-Berggren L, Deeney JT, Berggren PO, Meister B 1994 Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc Natl Acad Sei USA 91:12487-12491
40. Sadoul K, Lang J, Monlecucco C, Weller U, Regazzi R, Catsicas S, Wollheim CB, Halban PA 1995 SNAP-25 is expressed in islets of Langerhans and is involved in insulin release. J Cell Biol 128:1019-1028
41. Galli T, Chilcote T, Mundigl O, Binz T, Niemann H, De Camilli P 1994 Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells. J Cell Biol 125:1015-1024
42. Bennett, MK, Garcîa-Arrarâs, JE, Elferink, LA, Peterson, K, Fleming AM, Hazuka C, Scheller RH 1993 The syntaxin family of vesicular transport receptors. Cell 74:863-873
43. James DE, Brown R, Navarro J Filch PF 1988 Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein. Nature 333:183-185
44. Gumà A, Mora C, Santalucîa T, Vinals F, Testar X, Palacm M, Zorzano A1992 System A transport activity is stimulated in skeletal muscle in response to diabetes. FEBS Lett 310:51-54
45. Pujades C, Forsberg E, Enrich C, Johansson S 1992 Dystrophin colocalizes with beta-spectrin in distinct subsarcolemmal domains in mammmalian skeletal muscle. J Cell Sei 102:815-820
46. Schmid A, Barhanin J, Coppola T, Borsotto M Lazdunski M 1986 Immunochemical analysis of subunit structure of 1,4-dihydropyridine receptors asso-dated with voltage-dependent Ca2+ channels in skeletal, cardiac, and smooth muscle. Biochemistry 25:3492-3495
47. Rosemblatt MS, Scales DJ1989 Morphological, immunological and biochemical characterization of purified transverse tubule membranes isolated from rabbit skeletal muscle. Mol Cell Biochem 87:57-69
48. Jose M, Biosca JA, Trujillo R, Harte E 1992 Characterization of the hepatic insulin receptor undergoing internalization through clathrin-coated vesicles and endosomes. FEES Lett 334:286-288
49. Barnstable CJ, Hofstein R, Akagawa K 1985 A marker of early amacrine cell development in rat retina. Dev Brain Res 20:286-290
50. Aguado F, Majo G, Ruiz-Montasell B, Canals JM, Casanova A, Marsal J, Blasi J 1996 Expression of synaptosomal-associated protein SNAP-25 in endocrine anterior pituitary cells. Eur J Cell Biol 69:351-359
51. Munoz P, Mora S, Sevilla L, Kaliman P, Tomas E, Gumà A, Testar X, Palacin M, Zorzano A 1996 Expression and insulin-regulated distribution of caveolin in skeletal muscle. Caveolin does not colocalize with GLUT4 in intracellular membranes. J Biol Chem 271:8133-8139
52. Hidalgo C, Gonzalez ME Lagos R 1983 Characterization of the Ca2+ or Mg2+-ATPse of transverse tubule membranes isolated from rabbit skeletal muscle. J Biol Chem 258:3937-13945
53. Bradford MM 1976 A rapid and sensitive method for the quantification of microgram quantities utilizing the principle protein-dye binding. Anal Biochem 72:248-254
54. Fischer Y, Rose H, Kammermeier H 1991 Highly insulin-responsive isolated rat heart muscle cells yielded by a modified isolation method. Life Sei 49:1679-1688
55. Fischer Y, Thomas J, Rosen P, Kammermeier H 1995 Action of metformin on glucose transport and glucose transporter GLUT1 and GLUT4 in heart muscle cells from healthy and diabetic rats. Endocrinology 136:412-420
56. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
57. Schlenstedt G, Gudmundsson GH, Boman HG, Zimmermann R1990 A large presecretory protein translocates both cotranslationally, using signal recognition particle and ribosome, and post-translationally, without these ribonucleoparticles, when synthesized in the presence of mammalian microsomes. J Biol Chcm 265:13960-13968
58. Camps M, Castellô, A, Mufioz P, Monfar M, Testar X, Palacîn M, Zorzano A 1992 Effect of diabetes and fasting on GLUT4 (muscle/fat) glucose-transporter expression in insulin-sensitive tissue heterogeneous responses in heart, red and white muscle. Biochem J 282:765-772
59. Brozinick JT, Etgen GJ, Yaspelkis BB, Ivy JL 1994 The effects of muscle contraction and insulin on glucose-transporter translocation in rat skeletal muscle. Biochem J 297:539-545
60. Goodyear LJ, Hirshman MF, Horton ES 1991 Glucose transporter number, activity, and isoform content in plasma-membranes of red and white skeletalmuscle. Am J Physiol 261:E795-E799
61. Fushiki T, Wells JA, Tapscott EB Dohm GL 1989 Changes in glucose transporters in muscle in response to exercise. Am J Physiol 256:E580-E587
62. Coderre L, Kandror KV, Vallega G Pilch PF 1995 Identification and characterization of an exercise-sensitive pool of glucose transporters in skeletal muscle. J Biol Chem 270:27584-27588
63. Tamori Y, Hashiramoto M, Araki S, Kamata Y, Takahashi M, Kozaki S, Kasuga M 1996 Cleavage of vesicle-associated membrane protein (VAMP)-2 and cellubrevin on GLUT4-containing vesicles inhibits the translocation of GLUT4 in 3T3-L1 adipocytes. Biochem Biophys Res Commun 220:740-745
64. Sumitani S, Ramlal T, Liu Z Klip A 1995 Expression of syntaxin 4 in rat skeletal muscle cells in culture. Biochem Biophys Res Commun 213:462-468