Enhanced fasting glucose turnover in mice with disrupted action of TUG protein in skeletal muscle

Journal of Biological Chemistry

Volumn 288, Issue 28, 2013, Pages 20135-20150

  Löffler, Michael G ^a   Birkenfeld, Andreas L ^a   Philbrick, Katerina M ^a   Belman, Jonathan P ^a   Habtemichael, Estifanos N ^a   Booth, Carmen J ^a   Castorena, Carlos M ^b   Choi, Cheol Soo ^a   Jornayvaz, Francois R ^a   Gassaway, Brandon M ^a   Lee, Hui Young ^a   Cartee, Gregory D ^b   Philbrick, William ^a   Shulman, Gerald I ^a   Samuel, Varman T ^a,c   Bogan, Jonathan S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPROTEOLYTIC CLEAVAGE; ENERGY EXPENDITURE; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORTER 4; GLUCOSE TRANSPORTERS; INSULIN CONCENTRATIONS; INSULIN RESISTANCE; TRANSGENIC EXPRESSION;

CARBON DIOXIDE; CELL MEMBRANES; GLUCOSE; INSULIN; MAMMALS; METABOLISM; NUTRITION; PROTEINS; PROTEOLYSIS;

MUSCLE;

CARBON DIOXIDE; DEOXYGLUCOSE; GLUCOSE; GLUCOSE TRANSPORTER 4; GLYCOGEN; INSULIN; OXYGEN; PIST PROTEIN; PROTEIN; TUG PROTEIN; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRAIN 3T3; CELL SURFACE; DIET RESTRICTION; ENERGY EXPENDITURE; ENERGY METABOLISM; FEMALE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE CLAMP TECHNIQUE; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOGEN MUSCLE LEVEL; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; MALE; METABOLIC RATE; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSGENE; TRANSGENIC MOUSE; TRANSVERSE TUBULAR SYSTEM;

DIABETES; ENERGY METABOLISM; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLUT4; INSULIN; INSULIN RESISTANCE; MEMBRANE TRAFFICKING; NUTRITION; TRANSGENIC MICE;

3T3-L1 CELLS; ANIMALS; BLOOD GLUCOSE; CARBON DIOXIDE; CARRIER PROTEINS; DEOXYGLUCOSE; FASTING; FEMALE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; GLYCOGEN; HYPOGLYCEMIC AGENTS; IMMUNOBLOTTING; INSULIN; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, TRANSGENIC; MUSCLE, SKELETAL; OXYGEN CONSUMPTION; PROTEIN TRANSPORT; PROTEOLYSIS;

EID: 84880058904     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.458075     Document Type: Article

References (72)

1. Cline, G. W., Petersen, K. F., Krssak, M., Shen, J., Hundal, R. S., Trajanoski, Z., Inzucchi, S., Dresner, A., Rothman, D. L., and Shulman, G. I. (1999) Impaired glucose transport as a cause of decreased insulin-stimulated muscle glycogen synthesis in type 2 diabetes. N. Engl. J. Med. 341, 240-246 (Pubitemid 29334522)
2. Minokoshi, Y., Kahn, C. R., and Kahn, B. B. (2003) Tissue-specific ablation of the GLUT4 glucose transporter or the insulin receptor challenges assumptions about insulin action and glucose homeostasis. J. Biol. Chem. 278, 33609-33612 (Pubitemid 37553190)
3. Bogan, J. S. (2012) Regulation of glucose transporter translocation in health and diabetes. Annu. Rev. Biochem. 81, 507-532
4. Samuel, V. T., and Shulman, G. I. (2012) Mechanisms for insulin resistance: common threads and missing links. Cell 148, 852-871
5. Garvey, W. T., Maianu, L., Zhu, J. H., Brechtel-Hook, G., Wallace, P., and Baron, A. D. (1998) Evidence for defects in the trafficking and translocation of GLUT4 glucose transporters in skeletal muscle as a cause of human insulin resistance. J. Clin. Investig. 101, 2377-2386 (Pubitemid 28270432)
6. Maianu, L., Keller, S. R., and Garvey, W. T. (2001) Adipocytes exhibit abnormal subcellular distribution and translocation of vesicles containing glucose transporter 4 and insulin-regulated aminopeptidase in type 2 diabetes mellitus: implications regarding defects in vesicle trafficking. J. Clin. Endocrinol. Metab. 86, 5450-5456 (Pubitemid 33070274)
7. Vassilopoulos, S., Esk, C., Hoshino, S., Funke, B. H., Chen, C. Y., Plocik, A. M., Wright, W. E., Kucherlapati, R., and Brodsky, F. M. (2009)Arole for the CHC22 clathrin heavy-chain isoform in human glucose metabolism. Science 324, 1192-1196
8. Petersen, K. F., Dufour, S., Savage, D. B., Bilz, S., Solomon, G., Yonemitsu, S., Cline, G. W., Befroy, D., Zemany, L., Kahn, B. B., Papademetris, X., Rothman, D. L., and Shulman, G. I. (2007) The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc. Natl. Acad. Sci. U.S.A. 104, 12587-12594 (Pubitemid 47255198)
9. Rubin, B. R., and Bogan, J. S. (2009) Intracellular retention and insulin-stimulated mobilization of GLUT4 glucose transporters. Vitam. Horm. 80, 155-192
10. Bogan, J. S., and Kandror, K. V. (2010) Biogenesis and regulation of insulin-responsive vesicles containing GLUT4. Curr. Opin. Cell Biol. 22, 506-512
11. 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 (Pubitemid 37314316)
12. Yu, C., Cresswell, J., Löffler, 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 (Pubitemid 47093657)
13. 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
14. Orme, C. M., and Bogan, J. S. (2012) The ubiquitin regulatory X (UBX) domain-containing protein TUG regulates the p97 ATPase and resides at the endoplasmic reticulum-Golgi intermediate compartment. J. Biol. Chem. 287, 6679-6692
15. Bogan, J. S., Rubin, B. R., Yu, C., Löffler, M. G., Orme, C. M., Belman, J. P., McNally, L. J., Hao, M., and Cresswell, J. A. (2012) Endoproteolytic cleavage of TUG protein regulates GLUT4 glucose transporter translocation. J. Biol. Chem. 287, 23932-23947
16. Cho, H., Mu, J., Kim, J. K., Thorvaldsen, J. L., Chu, Q., Crenshaw, E. B., 3rd, Kaestner, K. H., Bartolomei, M. S., Shulman, G. I., and Birnbaum, M. J. (2001) Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKBβ). Science 292, 1728-1731 (Pubitemid 32506248)
17. Cartee, G. D., and Wojtaszewski, J. F. (2007) Role of Akt substrate of 160 kDa in insulin-stimulated and contraction-stimulated glucose transport. Appl. Physiol. Nutr. Metab. 32, 557-566
18. Chen, Y., Wang, Y., Zhang, J., Deng, Y., Jiang, L., Song, E., Wu, X. S., Hammer, J. A., Xu, T., and Lippincott-Schwartz, J. (2012) Rab10 and my-osin- Va mediate insulin-stimulated GLUT4 storage vesicle translocation in adipocytes. J. Cell Biol. 198, 545-560
19. 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
20. Lansey, M. N., Walker, N. N., Hargett, S. R., Stevens, J. R., and Keller, S. R. (2012) Deletion of Rab GAP AS160 modifies glucose uptake and GLUT4 translocation in primary skeletal muscles and adipocytes and impairs glucose homeostasis. Am. J. Physiol. Endocrinol. Metab. 303, E1273-E1286
21. Wang, H. Y., Ducommun, S., Quan, C., Xie, B., Li, M., Wasserman, D. H., Sakamoto, K., Mackintosh, C., and Chen, S. (2013) AS160 deficiency causes whole-body insulin resistance via composite effects in multiple tissues. Biochem. J. 449, 479-489
22. Hatakeyama, H., and Kanzaki, M. (2013) Regulatory mode shift of Tbc1d1 is required for acquisition of insulin-responsive GLUT4-trafficking activity. Mol. Biol. Cell 24, 809-817
23. 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 (Pubitemid 38891144)
24. Thurmond, D. C., and Pessin, J. E. (2000) Discrimination of GLUT4 vesicle trafficking from fusion using a temperature-sensitive Munc18c mutant. EMBO J. 19, 3565-3575 (Pubitemid 30462115)
25. Hatakeyama, H., and Kanzaki, M. (2011) Molecular basis of insulin-responsive GLUT4 trafficking systems revealed by single molecule imaging. Traffic 12, 1805-1820
26. Schertzer, J. D., Antonescu, C. N., Bilan, P. J., Jain, S., Huang, X., Liu, Z., Bonen, A., and Klip, A. (2009) A transgenic mouse model to study glucose transporter 4myc regulation in skeletal muscle. Endocrinology 150, 1935-1940
27. Castorena, C. M., Mackrell, J. G., Bogan, J. S., Kanzaki, M., and Cartee, G. D. (2011) Clustering of GLUT4, TUG, and RUVBL2 protein levels correlate with myosin heavy chain isoform pattern in skeletal muscles, but AS160 and TBC1D1 levels do not. J. Appl. Physiol. 111, 1106-1117
28. Jaynes, J. B., Johnson, J. E., Buskin, J. N., Gartside, C. L., and Hauschka, S. D. (1988) The muscle creatine kinase gene is regulated by multiple upstream elements, including a muscle-specific enhancer. Mol. Cell. Biol. 8, 62-70
29. Donoviel, D. B., Shield, M. A., Buskin, J. N., Haugen, H. S., Clegg, C. H., and Hauschka, S. D. (1996) Analysis of muscle creatine kinase gene regulatory elements in skeletal and cardiac muscles of transgenic mice. Mol. Cell. Biol. 16, 1649-1658 (Pubitemid 26095637)
30. Nguyen, Q. G., Buskin, J. N., Himeda, C. L., Shield, M. A., and Hauschka, S. D. (2003) Differences in the function of three conserved E-boxes of the muscle creatine kinase gene in cultured myocytes and in transgenic mouse skeletal and cardiac muscle. J. Biol. Chem. 278, 46494-46505 (Pubitemid 37452222)
31. Hong, E. G., Ko, H. J., Cho, Y. R., Kim, H. J., Ma, Z., Yu, T. Y., Friedline, R. H., Kurt-Jones, E., Finberg, R., Fischer, M. A., Granger, E. L., Norbury, C. C., Hauschka, S. D., Philbrick, W. M., Lee, C. G., Elias, J. A., and Kim, J. K. (2009) Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 58, 2525-2535
32. Jurczak, M. J., Lee, A. H., Jornayvaz, F. R., Lee, H. Y., Birkenfeld, A. L., Guigni, B. A., Kahn, M., Samuel, V. T., Glimcher, L. H., and Shulman, G. I. (2012) Dissociation of inositol-requiring enzyme (IRE1α)-mediated c-Jun N-terminal kinase activation from hepatic insulin resistance in conditional X-box-binding protein-1 (XBP1) knock-out mice. J. Biol. Chem. 287, 2558-2567
33. Ayala, J. E., Samuel, V. T., Morton, G. J., Obici, S., Croniger, C. M., Shulman, G. I., Wasserman, D. H., and McGuinness, O. P. (2010) Standard operating procedures for describing and performing metabolic tests of glucose homeostasis in mice. Dis. Model. Mech. 3, 525-534
34. Youn, J. H., and Buchanan, T. A. (1993) Fasting does not impair insulin-stimulated glucose uptake but alters intracellular glucose metabolism in conscious rats. Diabetes 42, 757-763 (Pubitemid 23127167)
35. Choi, C. S., Savage, D. B., Abu-Elheiga, L., Liu, Z. X., Kim, S., Kulkarni, A., Distefano, A., Hwang, Y. J., Reznick, R. M., Codella, R., Zhang, D., Cline, G. W., Wakil, S. J., and Shulman, G. I. (2007) Continuous fat oxidation in acetyl-CoA carboxylase 2 knockout mice increases total energy expenditure, reduces fat mass, and improves insulin sensitivity. Proc. Natl. Acad. Sci. U.S.A. 104, 16480-16485 (Pubitemid 350211044)
36. Zhang, B., Arun, G., Mao, Y. S., Lazar, Z., Hung, G., Bhattacharjee, G., Xiao, X., Booth, C. J., Wu, J., Zhang, C., and Spector, D. L. (2012) The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep. 2, 111-123
37. Bogan, J. S., McKee, A. E., and Lodish, H. F. (2001) Insulin-responsive compartments containing GLUT4 in 3T3-L1 and CHO cells: regulation by amino acid concentrations. Mol. Cell. Biol. 21, 4785-4806 (Pubitemid 32588258)
38. Zorzano, A., and Camps, M. (2006) Isolation of T-tubules from skeletal muscle. Curr. Protoc. Cell Biol. Chapter 3, Unit 3.24
39. Pietrini, G., Matteoli, M., Banker, G., and Caplan, M. J. (1992) Isoforms of the Na,K-ATPase are present in both axons and dendrites of hippocampal neurons in culture. Proc. Natl. Acad. Sci. U.S.A. 89, 8414-8418
40. Rechsteiner, M., and Rogers, S. W. (1996) PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21, 267-271 (Pubitemid 26228278)
41. Hicks, S. W., and Machamer, C. E. (2005) Isoform-specific interaction of golgin-160 with the Golgi-associated protein PIST. J. Biol. Chem. 280, 28944-28951 (Pubitemid 41161340)
42. Sbodio, J. I., Hicks, S. W., Simon, D., and Machamer, C. E. (2006) GCP60 preferentially interacts with a caspase-generated golgin-160 fragment. J. Biol. Chem. 281, 27924-27931 (Pubitemid 44414504)
43. Sbodio, J. I., and Machamer, C. E. (2007) Identification of a redox-sensitive cysteine in GCP60 that regulates its interaction with golgin-160. J. Biol. Chem. 282, 29874-29881 (Pubitemid 350035278)
44. Andrikopoulos, S., Blair, A. R., Deluca, N., Fam, B. C., and Proietto, J. (2008) Evaluating the glucose tolerance test in mice. Am. J. Physiol. Endocrinol. Metab. 295, E1323-E1332
45. Park, S. Y., Kim, H. J., Wang, S., Higashimori, T., Dong, J., Kim, Y. J., Cline, G., Li, H., Prentki, M., Shulman, G. I., Mitchell, G. A., and Kim, J. K. (2005) Hormone-sensitive lipase knockout mice have increased hepatic insulin sensitivity and are protected from short-term diet-induced insulin resistance in skeletal muscle and heart. Am. J. Physiol. Endocrinol. Metab. 289, E30-E39 (Pubitemid 40874931)
46. Zhang, D., Christianson, J., Liu, Z. X., Tian, L., Choi, C. S., Neschen, S., Dong, J., Wood, P. A., and Shulman, G. I. (2010) Resistance to high-fat diet-induced obesity and insulin resistance in mice with very long-chain acyl-CoA dehydrogenase deficiency. Cell Metab. 11, 402-411
47. Yue, Z., Horton, A., Bravin, M., DeJager, P. L., Selimi, F., and Heintz, N. (2002) A novel protein complex linking the δ2 glutamate receptor and autophagy: implications for neurodegeneration in lurcher mice. Neuron 35, 921-933
48. Williams, D., Hicks, S. W., Machamer, C. E., and Pessin, J. E. (2006) Golgin-160 is required for the Golgi membrane sorting of the insulin-responsive glucose transporter GLUT4 in adipocytes. Mol. Biol. Cell 17, 5346-5355 (Pubitemid 44907374)
49. Chiang, S. H., Baumann, C. A., Kanzaki, M., Thurmond, D. C., Watson, R. T., Neudauer, C. L., Macara, I. G., Pessin, J. E., and Saltiel, A. R. (2001) Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 410, 944-948 (Pubitemid 32335841)
50. JeBailey, L., Rudich, A., Huang, X., Di Ciano-Oliveira, C., Kapus, A., and Klip, A. (2004) Skeletal muscle cells and adipocytes differ in their reliance on TC10 and Rac for insulin-induced actin remodeling. Mol. Endocrinol. 18, 359-372
51. Chiang, S. H., Chang, L., and Saltiel, A. R. (2006) TC10 and insulin-stimulated glucose transport. Methods Enzymol. 406, 701-714 (Pubitemid 43207480)
52. Chang, L., Chiang, S. H., and Saltiel, A. R. (2007) TC10α is required for insulin-stimulated glucose uptake in adipocytes. Endocrinology 148, 27-33 (Pubitemid 46021435)
53. Neudauer, C. L., Joberty, G., Tatsis, N., and Macara, I. G. (1998) Distinct cellular effects and interactions of the Rho-family GTPase TC10. Curr. Biol. 8, 1151-1160 (Pubitemid 28494713)
54. Gupte, A., and Mora, S. (2006) Activation of the Cbl insulin signaling pathway in cardiac muscle; dysregulation in obesity and diabetes. Biochem. Biophys. Res. Commun. 342, 751-757 (Pubitemid 43320462)
55. Liu, J., Kimura, A., Baumann, C. A., and Saltiel, A. R. (2002) APS facilitates c-Cbl tyrosine phosphorylation and GLUT4 translocation in response to insulin in 3T3-L1 adipocytes. Mol. Cell. Biol. 22, 3599-3609 (Pubitemid 34525204)
56. Ahn, M. Y., Katsanakis, K. D., Bheda, F., and Pillay, T. S. (2004) Primary and essential role of the adaptor protein APS for recruitment of both c-Cbl and its associated protein CAP in insulin signaling. J. Biol. Chem. 279, 21526-21532 (Pubitemid 38656563)
57. Mitra, P., Zheng, X., and Czech, M. P. (2004) RNAi-based analysis of CAP, Cbl, and CrkII function in the regulation of GLUT4 by insulin. J. Biol. Chem. 279, 37431-37435 (Pubitemid 39195452)
58. Minami, A., Iseki, M., Kishi, K., Wang, M., Ogura, M., Furukawa, N., Hayashi, S., Yamada, M., Obata, T., Takeshita, Y., Nakaya, Y., Bando, Y., Izumi, K., Moodie, S. A., Kajiura, F., Matsumoto, M., Takatsu, K., Takaki, S., and Ebina, Y. (2003) Increased insulin sensitivity and hypoinsulinemia in APS knockout mice. Diabetes 52, 2657-2665 (Pubitemid 37339694)
59. Molero, J. C., Jensen, T. E., Withers, P. C., Couzens, M., Herzog, H., Thien, C. B., Langdon, W. Y., Walder, K., Murphy, M. A., Bowtell, D. D., James, D. E., and Cooney, G. J. (2004) c-Cbl-deficient mice have reduced adiposity, higher energy expenditure, and improved peripheral insulin action. J. Clin. Investig. 114, 1326-1333 (Pubitemid 40385304)
60. Liu, J., DeYoung, S. M., Hwang, J. B., O'Leary, E. E., and Saltiel, A. R. (2003) The roles of Cbl-b and c-Cbl in insulin-stimulated glucose transport. J. Biol. Chem. 278, 36754-36762 (Pubitemid 37140009)
61. Hart, Y., and Alon, U. (2013) The utility of paradoxical components in biological circuits. Mol. Cell 49, 213-221
62. Szekeres, F., Chadt, A., Tom, R. Z., Deshmukh, A. S., Chibalin, A. V., Björnholm, M., Al-Hasani, H., and Zierath, J. R. (2012) The Rab-GTPase-activating protein TBC1D1 regulates skeletal muscle glucose metabolism. Am. J. Physiol. Endocrinol Metab. 303, E524-E533
63. Langer, O. (2000) Fetal macrosomia: etiologic factors. Clin. Obstet. Gynecol. 43, 283-297
64. Gulve, E. A., Ren, J. M., Marshall, B. A., Gao, J., Hansen, P. A., Holloszy, J. O., and Mueckler, M. (1994) Glucose transport activity in skeletal muscles from transgenic mice overexpressing GLUT1. Increased basal transport is associated with a defective response to diverse stimuli that activate GLUT4. J. Biol. Chem. 269, 18366-18370 (Pubitemid 24224064)
65. Liu, M. L., Gibbs, E. M., McCoid, S. C., Milici, A. J., Stukenbrok, H. A., McPherson, R. K., Treadway, J. L., and Pessin, J. E. (1993) Transgenic mice expressing the human GLUT4/muscle-fat facilitative glucose transporter protein exhibit efficient glycemic control. Proc. Natl. Acad. Sci. U.S.A. 90, 11346-11350 (Pubitemid 23354426)
66. Bao, S., and Garvey, W. T. (1997) Exercise in transgenic mice overexpressing GLUT4 glucose transporters: effects on substrate metabolism and glycogen regulation. Metabolism 46, 1349-1357 (Pubitemid 27473523)
67. Brozinick, J. T., Jr., McCoid, S. C., Reynolds, T. H., Wilson, C. M., Stevenson, R. W., Cushman, S. W., and Gibbs, E. M. (1997) Regulation of cell surface GLUT4 in skeletal muscle of transgenic mice. Biochem. J. 321, 75-81 (Pubitemid 27032571)
68. Treadway, J. L., Hargrove, D. M., Nardone, N. A., McPherson, R. K., Russo, J. F., Milici, A. J., Stukenbrok, H. A., Gibbs, E. M., Stevenson, R. W., and Pessin, J. E. (1994) Enhanced peripheral glucose utilization in transgenic mice expressing the human GLUT4 gene. J. Biol. Chem. 269, 29956-29961 (Pubitemid 24365165)
69. Hansen, P. A., Gulve, E. A., Marshall, B. A., Gao, J., Pessin, J. E., Holloszy, J. O., and Mueckler, M. (1995) Skeletal muscle glucose transport and metabolism are enhanced in transgenic mice overexpressing the Glut4 glucose transporter. J. Biol. Chem. 270, 1679-1684
70. Deems, R. O., Evans, J. L., Deacon, R. W., Honer, C. M., Chu, D. T., Bürki, K., Fillers, W. S., Cohen, D. K., and Young, D. A. (1994) Expression of human GLUT4 in mice results in increased insulin action. Diabetologia 37, 1097-1104 (Pubitemid 24325553)
71. 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 (Pubitemid 26010419)
72. Ren, J. M., Marshall, B. A., Mueckler, M. M., McCaleb, M., Amatruda, J. M., and Shulman, G. I. (1995) Overexpression of Glut4 protein in muscle increases basal and insulin-stimulated whole-body glucose disposal in conscious mice. J. Clin. Investig. 95, 429-432