Insulin stimulates fusion, but not tethering, of GLUT4 vesicles in skeletal muscle of HA-GLUT4-GFP transgenic mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 8, 2012, Pages

  Lizunov, Vladimir A ^a   Stenkula, Karin G ^b,c   Lisinski, Ivonne ^c   Gavrilova, Oksana ^d   Yver, Dena R ^c   Chadt, Alexandra ^e   Al Hasani, Hadi ^e,f   Zimmerberg, Joshua ^a   Cushman, Samuel W ^c  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b LUND UNIVERSITY   (Sweden)

^c Diabetes Endocrinology and Obesity Branch ^*  (United States)

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

^e GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^f HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Fusion; Glucose transporter 4; Green fluorescent protein; Hemagglutinin; Insulin

Indexed keywords

GLUCOSE TRANSPORTER 4; GREEN FLUORESCENT PROTEIN; HEMAGGLUTININ; INSULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELL STIMULATION; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EXOCYTOSIS; FEMALE; FLUORESCENCE ANALYSIS; HEART; INSULIN METABOLISM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SARCOLEMMA; SKELETAL MUSCLE; TOTAL INTERNAL REFLECTION FLUORESCENCE; TRANSVERSE TUBULAR SYSTEM;

ANIMALS; CYTOPLASMIC VESICLES; EXOCYTOSIS; FEMALE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; GREEN FLUORESCENT PROTEINS; HEMAGGLUTININS; INSULIN; MALE; MEMBRANE FUSION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MUSCLE, SKELETAL; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SARCOLEMMA;

EID: 84859476275     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00466.2011     Document Type: Article

References (37)

1. Abel ED, Peroni O, Kim JK, Kim YB, Boss O, Hadro E, Minnemann T, Shulman GI, Kahn BB. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 409: 729-733, 2001.
2. Bai L, Wang Y, Fan J, Chen Y, Ji W, Qu A, Xu P, James DE, Xu T. Dissecting multiple steps of GLUT4 trafficking and identifying the sites of insulin action. Cell Metab 5: 47-57, 2007.
3. Brozinick JT Jr, Yaspelkis BB 3rd, Wilson CM, Grant KE, Gibbs EM, Cushman SW, and Ivy JL. Glucose transport and GLUT4 protein distribution in skeletal muscle of GLUT4 transgenic mice. Biochem J 313: 133-140, 1996.
4. Bruning JC, Michael MD, Winnay JN, Hayashi T, Horsch D, Accili D, Goodyear LJ, Kahn CR. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 2: 559-569, 1998.
5. Bryant NJ, Govers R, James DE. Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol 3: 267-277, 2002.
6. Carvalho E, Schellhorn SE, Zabolotny JM, Martin S, Tozzo E, Peroni OD, Houseknecht KL, Mundt A, James DE, Kahn BB. GLUT4 overexpression or deficiency in adipocytes of transgenic mice alters the composition of GLUT4 vesicles and the subcellular localization of GLUT4 and insulin-responsive aminopeptidase. J Biol Chem 279: 21598-21605, 2004.
7. Chadt A, Leicht K, Deshmukh A, Jiang LQ, Scherneck S, Bernhardt U, Dreja T, Vogel H, Schmolz K, Kluge R, Zierath JR, Hultschig C, Hoeben RC, Schurmann A, Joost HG, Al-Hasani H. Tbc1d1 mutation in lean mouse strain confers leanness and protects from diet-induced obesity. Nat Genet 40: 1354-1359, 2008.
8. Chen Y, Deng Y, Zhang J, Yang L, Xie X, Xu T. GDI-1 preferably interacts with Rab10 in insulin-stimulated GLUT4 translocation. Biochem J 422: 229-235, 2009.
9. Dawson K, Aviles-Hernandez A, Cushman SW, Malide D. Insulin regulated trafficking of dual-labeled glucose transporter 4 in primary rat adipose cells. Biochem Biophys Res Commun 287: 445-454, 2001.
10. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30: 1000-1007, 1981.
11. Eguez L, Lee A, Chavez JA, Miinea CP, Kane S, Lienhard GE, McGraw TE. Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein. Cell Metab 2: 263-272, 2005.
12. Fazakerley DJ, Lawrence SP, Lizunov VA, Cushman SW, Holman GD. A common trafficking route for GLUT4 in cardiomyocytes in response to insulin, contraction and energy-status signalling. J Cell Sci 122: 727-734, 2009.
13. Goodyear LJ, King PA, Hirshman MF, Thompson CM, Horton ED, Horton ES. Contractile activity increases plasma membrane glucose transporters in absence of insulin. Am J Physiol Endocrinol Metab 258: E667-E672, 1990.
14. Heron-Milhavet L, Haluzik M, Yakar S, Gavrilova O, Pack S, Jou WC, Ibrahimi A, Kim H, Hunt D, Yau D, Asghar Z, Joseph J, Wheeler MB, Abumrad NA, LeRoith D. Muscle-specific overexpression of CD36 reverses the insulin resistance and diabetes of MKR mice. Endocrinology 145: 4667-4676, 2004.
15. Holman GD, Lo Leggio L, Cushman SW. Insulin-stimulated GLUT4 glucose transporter recycling. A problem in membrane protein subcellular trafficking through multiple pools. J Biol Chem 269: 17516-17524, 1994.
16. Lauritzen HP, Galbo H, Brandauer J, Goodyear LJ, Ploug T. Large GLUT4 vesicles are stationary while locally and reversibly depleted during transient insulin stimulation of skeletal muscle of living mice: imaging analysis of GLUT4-enhanced green fluorescent protein vesicle dynamics. Diabetes 57: 315-324, 2008.
17. Lauritzen HP, Galbo H, Toyoda T, Goodyear LJ. Kinetics of contraction-induced GLUT4 translocation in skeletal muscle fibers from living mice. Diabetes 59: 2134-2144, 2010.
18. Lauritzen HP, Ploug T, Prats C, Tavare JM, Galbo H. Imaging of insulin signaling in skeletal muscle of living mice shows major role of T-tubules. Diabetes 55: 1300-1306, 2006.
19. Lauritzen HP, Reynet C, Schjerling P, Ralston E, Thomas S, Galbo H, Ploug T. Gene gun bombardment-mediated expression and translocation of EGFP-tagged GLUT4 in skeletal muscle fibres in vivo. Pflügers Arch 444: 710-721, 2002.
20. Lauritzen HP, Schertzer JD. Measuring GLUT4 translocation in mature muscle fibers. Am J Physiol Endocrinol Metab 299: E169-E179, 2010.
21. Li CH, Bai L, Li DD, Xia S, Xu T. Dynamic tracking and mobility analysis of single GLUT4 storage vesicle in live 3T3-L1 cells. Cell Res 14: 480-486, 2004.
22. Lizunov VA, Lisinski I, Stenkula K, Zimmerberg J, Cushman SW. Insulin regulates fusion of GLUT4 vesicles independent of Exo70-mediated tethering. J Biol Chem 284: 7914-7919, 2009.
23. Lizunov VA, Matsumoto H, Zimmerberg J, Cushman SW, Frolov VA. Insulin stimulates the halting, tethering, and fusion of mobile GLUT4 vesicles in rat adipose cells. J Cell Biol 169: 481-489, 2005.
24. Marette A, Burdett E, Douen A, Vranic M, Klip A. Insulin induces the translocation of GLUT4 from a unique intracellular organelle to transverse tubules in rat skeletal muscle. Diabetes 41: 1562-1569, 1992.
25. Miinea CP, Sano H, Kane S, Sano E, Fukuda M, Peranen J, Lane WS, Lienhard GE. AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem J 391: 87-93, 2005.
26. Mitsumoto Y, Burdett E, Grant A, 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.
27. Niu W, Bilan PJ, Yu J, Gao J, Boguslavsky S, Schertzer JD, Chu G, Yao Z, Klip A. PKCepsilon regulates contraction-stimulated GLUT4 traffic in skeletal muscle cells. J Cell Physiol 226: 173-180, 2011.
28. Ploug T, van Deurs B, Ai H, Cushman SW, 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.
29. Randhawa VK, Ishikura S, Talior-Volodarsky I, Cheng AW, Patel N, Hartwig JH, Klip A. GLUT4 vesicle recruitment and fusion are differentially regulated by Rac, AS160, and Rab8A in muscle cells. J Biol Chem 283: 27208-27219, 2008.
30. Sano H, Eguez L, Teruel MN, Fukuda M, Chuang TD, Chavez JA, Lienhard GE, McGraw TE. Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab 5: 293-303, 2007.
31. Sbalzarini IF, Koumoutsakos P. Feature point tracking and trajectory analysis for video imaging in cell biology. J Struct Biol 151: 182-195, 2005.
32. Schertzer JD, Antonescu CN, Bilan PJ, Jain S, Huang X, Liu Z, Bonen A, Klip A. A transgenic mouse model to study glucose transporter 4myc regulation in skeletal muscle. Endocrinology 150: 1935-1940, 2009.
33. Stenkula KG, Lizunov VA, Cushman SW, Zimmerberg J. Insulin controls the spatial distribution of GLUT4 on the cell surface through regulation of its postfusion dispersal. Cell Metab 12: 250-259, 2010.
34. Sun Y, Bilan PJ, Liu Z, Klip A. Rab8A and Rab13 are activated by insulin and regulate GLUT4 translocation in muscle cells. Proc Natl Acad Sci USA 107: 19909-19914, 2010.
35. Wang Q, Khayat Z, Kishi K, Ebina Y, Klip A. GLUT4 translocation by insulin in intact muscle cells: detection by a fast and quantitative assay. FEBS Lett 427: 193-197, 1998.
36. Zeigerer A, McBrayer MK, McGraw TE. Insulin stimulation of GLUT4 exocytosis, but not its inhibition of endocytosis, is dependent on RabGAP AS160. Mol Biol Cell 15: 4406-4415, 2004.
37. Zisman A, Peroni OD, Abel ED, Michael MD, Mauvais-Jarvis F, Lowell BB, Wojtaszewski JF, Hirshman MF, Virkamaki A, Goodyear LJ, Kahn CR, Kahn BB. Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat Med 6: 924-928, 2000.