C2C12 myocytes lack an insulin-responsive vesicular compartment despite dexamethasone-induced GLUT4 expression

American Journal of Physiology - Endocrinology and Metabolism

Volumn 283, Issue 3 46-3, 2002, Pages

  Tortorella, Lori L ^a   Pilch, Paul F ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

C2C12 cells; Glucocorticoid; Glucose transporter; Insulin; Protein trafficking; Skeletal muscle

Indexed keywords

AMINOPEPTIDASE; DEXAMETHASONE; GLUCOSE TRANSPORTER 4; INSULIN RECEPTOR; N ETHYLMALEIMIDE; PROTEIN KINASE B; SNARE PROTEIN; SYNAPTOBREVIN; SYNTAXIN; TRANSFERRIN RECEPTOR; DEOXYGLUCOSE; GLUCOCORTICOID; GLUCOSE TRANSPORTER; INSULIN; MUSCLE PROTEIN;

ADIPOCYTE; ADIPOSE TISSUE CELL; ANIMAL CELL; ARTICLE; CELL SURFACE; CELL VACUOLE; CONTROLLED STUDY; ENDOSOME; GLUCOSE TRANSPORT; INSULIN RESPONSE; MUSCLE CELL; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SKELETAL MUSCLE; ANIMAL; CYTOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; DEOXYGLUCOSE; DEXAMETHASONE; GLUCOCORTICOIDS; GLUCOSE TRANSPORTER TYPE 4; INSULIN; MONOSACCHARIDE TRANSPORT PROTEINS; MUSCLE PROTEINS; MUSCLE, SKELETAL;

EID: 0036710325     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00092.2002     Document Type: Article

References (60)

1. Abel ED, Peroni O, Kim JK, Kim YB, Boss O, Hadro E, Minnemann T, Shulman GI, and Kahn BB. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 409: 729-733, 2001.
2. Asano T, Takata K, Katagiri H, Ishihara H, Inukai K, Anai M, Hirano H, Yazaki Y, and Oka Y. The role of N-glycosylation in the targeting and stability of GLUT1 glucose transporter. FEBS Lett 324: 258-261, 1993.
3. Cadepond F, Ulmann A, and Baulieu EE. RU486 (mifepristone): Mechanisms of action and clinical uses. Annu Rev Med 48: 129-156, 1997.
4. Cheatham B. GLUT4 and company: SNAREing roles in insulin-regulated glucose uptake. Trends Endocrinol Metab 11: 356-361, 2000.
5. Cho H, Mu J, Kim JK, Thorvaldsen JL, Chu Q, Crenshaw EB III, Kaestner KH, Bartolomei MS, Shulman GI, and Birnbaum MJ. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292: 1728-1731, 2001.
6. Chomczynski P and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
7. Coderre L, Kandror KV, Vallega G, and Pilch PF. Identification and characterization of an exercise-sensitive pool of glucose transporters in skeletal muscle. J Biol Chem 270: 27584-27588, 1995.
8. Coderre L, Vallega GA, Pilch PF, and Chipkin SR. In vivo effects of dexamethasone and sucrose on glucose transport (GLUT-4) protein tissue distribution. Am J Physiol Endocrinol Metab 271: E643-E648, 1996.
9. Cushman SW, Goodyear LJ, Pilch PF, Ralston E, Galbo H, Ploug T, Kristiansen S, and Klip A. Molecular mechanisms involved in GLUT4 translocation in muscle during insulin and contraction stimulation. Adv Exp Med Biol 441: 63-71, 1998.
10. Dimitriadis G, Leighton B, Parry-Billings M, Sasson S, Young M, Krause U, Bevan S, Piva T, Wegener G, and Newsholme EA. Effects of glucocorticoid excess on the sensitivity of glucose transport and metabolism to insulin in rat skeletal muscle. Biochem J 321: 707-712, 1997.
11. Douen AG, Burdett E, Ramlal T, Rastogi S, Vranic M, and Klip A. Characterization of glucose transporter-enriched membranes from rat skeletal muscle: Assessment of endothelial cell contamination and presence of sarcoplasmic reticulum and transverse tubules. Endocrinology 128: 611-616, 1991.
12. Ewart HS, Somwar R, and Klip A. Dexamethasone stimulates the expression of GLUT1 and GLUT4 proteins via different signalling pathways in L6 skeletal muscle cells. FEBS Lett 421: 120-124, 1998.
13. Feinberg AP and Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6-13, 1983.
14. Fiedler K and Simons K. The role of N-glycans in the secretory pathway. Cell 81: 309-312, 1995.
15. Foster LJ and Klip A. Mechanism and regulation of GLUT-4 vesicle fusion in muscle and fat cells. Am J Physiol Cell Physiol 279: C877-C890, 2000.
16. Goodyear LJ and Kahn BB. Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 49: 235-261, 1998.
17. Green H and Meuth M. An established pre-adipose cell line and its differentiation in culture. Cell 3: 127-133, 1974.
18. Guillet-Deniau I, Leturque A, and Girard J. Expression and cellular localization of glucose transporters (GLUT1, GLUT3, GLUT4) during differentiation of myogenic cells isolated from rat foetuses. J Cell Sci 107: 487-496, 1994.
19. Hashiramoto M and James DE. Snareing GLUT4 at the plasma membrane in muscle and fat. Adv Exp Med Biol 441: 47-61, 1998.
20. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, and Goodyear LJ. Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47: 1369-1373, 1998.
21. Hudson AW, Ruiz M, and Birnbaum MJ. Isoform-specific subcellular targeting of glucose transporters in mouse fibroblasts. J Cell Biol 116: 785-797, 1992.
22. Ing BL, Chen H, Robinson KA, Buse MG, and Quon MJ. Characterization of a mutant GLUT4 lacking the N-glycosylation site: Studies in transfected rat adipose cells. Biochem Biophys Res Commun 218: 76-82, 1996.
23. James DE, Brown R, Navarro J, and Pilch PF. Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein. Nature 333: 183-185, 1988.
24. Kandror KV, Coderre L, Pushkin AV, and Pilch PF. Comparison of glucose-transporter-containing vesicles from rat fat and muscle tissues: Evidence for a unique endosomal compartment. Biochem J 307: 383-390, 1995.
25. Kandror KV and Pilch PF. Compartmentalization of protein traffic in insulin-sensitive cells. Am J Physiol Endocrinol Metab 271: E1-E14, 1996.
26. Kandror KV, Yu L, and Pilch PF. The major protein of GLUT4-containing vesicles, gp160, has aminopeptidase activity. J Biol Chem 269: 30777-30780, 1994.
27. Klip A and Marette A. Acute and chronic signals controlling glucose transport in skeletal muscle. J Cell Biochem 48: 51-60, 1992.
28. Kotliar N and Pilch PF. Expression of the glucose transporter isoform GLUT 4 is insufficient to confer insulin-regulatable hexose uptake to cultured muscle cells. Mol Endocrinol 6: 337-345, 1992.
29. Kurth-Kraczek EJ, Hirshman MF, Goodyear LJ, and Winder WW. 5′ AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48: 1667-1671, 1999.
30. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
31. Lehto M, Xiang K, Stoffel M, Espinosa R III, Groop LC, Le Beau MM, and Bell GI. Human hexokinase II: Localization of the polymorphic gene to chromosome 2. Diabetologia 36: 1299-1302, 1993.
32. Luz JM and Lennarz WJ. Protein disulfide isomerase: a Multifunctional protein of the endoplasmic reticulum. Exper Suppl 77: 97-117, 1996.
33. Lyons GE, Ontell M, Cox R, Sassoon D, and Buckingham M. The expression of myosin genes in developing skeletal muscle in the mouse embryo. J Cell Biol 111: 1465-1476, 1990.
34. Martin JF, Schwarz JJ, and Olson EN. Myocyte enhancer factor (MEF) 2C: A tissue-restricted member of the MEF-2 family of transcription factors. Proc Natl Acad Sci USA 90: 5282-5286, 1993.
35. McMahon RJ and Frost SC. Nutrient control of GLUT1 processing and turnover in 3T3-L1 adipocytes. J Biol Chem 270: 12094-12099, 1995.
36. McMahon RJ, Hwang JB, and Frost SC. Glucose deprivation does not affect GLUT1 targeting in 3T3-L1 adipocytes. Biochem Biophys Res Commun 273: 859-864, 2000.
37. Merrill GF, Kurth EJ, Hardie DG, and Winder WW. AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol Endocrinol Metab 273: E1107-E1112, 1997.
38. Michael LF, Wu Z, Cheatham RB, Puigserver P, Adelmant G, Lehman JJ, Kelly DP, and Spiegelman BM. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc Natl Acad Sci USA 98: 3820-3825, 2001.
39. Mitsumoto Y, Burdett E, Grant A, and Klip A. Differential expression of the GLUT1 and GLUT4 glucose transporters during differentiation of L6 muscle cells. Biochem Biophys Res Commun 175: 652-659, 1991.
40. Mu J, Brozinick JT Jr, Valladares O, Bucan M, and Birnbaum MJ. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7: 1085-1094, 2001.
41. Musaro A, McCullagh KJ, Naya FJ, Olson EN, and Rosenthal N. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 400: 581-585, 1999.
42. Pessin JE, Thurmond DC, Elmendorf JS, Coker KJ, and Okada S. Molecular basis of insulin-stimulated GLUT4 vesicle trafficking. Location! Location! Location! J Biol Chem 274: 2593-2596, 1999.
43. Ploug T, van Deurs B, Ai H, Cushman SW, and Ralston E. 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, 1998.
44. Ramsay TG. Fat cells. Endocrinol Metab Clin North Am 25: 847-870, 1996.
45. Rapoport TA, Matlack KE, Plath K, Misselwitz B, and Staeck O. Posttranslational protein translocation across the membrane of the endoplasmic reticulum. Biol Chem 380: 1143-1150, 1999.
46. Robinson R, Robinson LJ, James DE, and Lawrence JC Jr. Glucose transport in L6 myoblasts overexpressing GLUT1 and GLUT4. J Biol Chem 268: 22119-22126, 1993.
47. Ryder JW, Chibalin AV, and Zierath JR. Intracellular mechanisms underlying increases in glucose uptake in response to insulin or exercise in skeletal muscle. Acta Physiol Scand 171: 249-257, 2001.
48. Santalucia T, Camps M, Castello A, Munoz P, Nuel A, Testar X, Palacin M, and Zorzano A. Developmental regulation of GLUT-1 (erythroid/Hep G2) and GLUT-4 (muscle/fat) glucose transporter expression in rat heart, skeletal muscle, and brown adipose tissue. Endocrinology 130: 837-846, 1992.
49. Semsarian C, Wu MJ, Ju YK, Marciniec T, Yeoh T, Allen DG, Harvey RP, and Graham RM. Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signalling pathway. Nature 400: 576-581, 1999.
50. Shibasaki Y, Asano T, Lin JL, Tsukuda K, Katagiri H, Ishihara H, Yazaki Y, and Oka Y. Two glucose transporter isoforms are sorted differentially and are expressed in distinct cellular compartments. Biochem J 281: 829-834, 1992.
51. Simpson IA, Yver DR, Hissin PJ, Wardzala LJ, Karnieli E, Salans LB, and Cushman SW. Insulin-stimulated translocation of glucose transporters in the isolated rat adipose cells: Characterization of subcellular fractions. Biochim Biophys Acta 763: 393-407, 1983.
52. Ueyama A, Yaworsky KL, Wang Q, Ebina Y, and Klip A. GLUT-4myc ectopic expression in L6 myoblasts generates a GLUT-4-specific pool conferring insulin sensitivity. Am J Physiol Endocrinol Metab 277: E572-E578, 1999.
53. Wilson CM, Mitsumoto Y, Maher F, and Klip A. Regulation of cell surface GLUT1, GLUT3, and GLUT4 by insulin and IGF-I in L6 myotubes. FEBS Lett 368: 19-22, 1995.
54. Wright WE, Sassoon DA, and Lin VK. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56: 607-617, 1989.
55. Yaffe D. Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci USA 61: 477-483, 1968.
56. Yaffe D and Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270: 725-727, 1977.
57. Yeh JI, Gulve EA, Rameh L, and Birnbaum MJ. 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, 1995.
58. Yoshiko Y, Hirao K, and Maeda N. Dexamethasone regulates the actions of endogenous insulin-like growth factor-II during myogenic differentiation. Life Sci 63: 77-85, 1998.
59. Zhou M, Sevilla L, Vallega G, Chen P, Palacin M, Zorzano A, Pilch PF, and Kandror KV. Insulin-dependent protein trafficking in skeletal muscle cells. Am J Physiol Endocrinol Metab 275: E187-E196, 1998.
60. Zhou M, Vallega G, Kandror KV, and Pilch PF. Insulin-mediated translocation of GLUT-4-containing vesicles is preserved in denervated muscles. Am J Physiol Endocrinol Metab 278: E1019-E1026, 2000.