Contraction regulates site-specific phosphorylation of TBC1D1 in skeletal muscle

Biochemical Journal

Volumn 431, Issue 2, 2010, Pages 311-320

  Vichaiwong, Kanokwan ^a,c   Purohit, Suneet ^a   An, Ding ^a   Toyoda, Taro ^a,d   Jessen, Niels ^a,e   Hirshman, Michael F ^a   Goodyear, Laurie J ^a,b  

^a JOSLIN DIABETES CENTER   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c MAHIDOL UNIVERSITY   (Thailand)

^d KYOTO UNIVERSITY   (Japan)

^e AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Akt; AMP activated protein kinase (AMPK); Contraction; Glucose transport; Skeletal muscle; TBC1D1

Indexed keywords

AKT; AMP-ACTIVATED PROTEIN KINASE; CONTRACTION; GLUCOSE TRANSPORT; SKELETAL MUSCLE; TBC1D1;

ENZYME ACTIVITY; GLUCOSE; INSULIN; MUSCLE; PROTEINS;

PHOSPHORYLATION;

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; PROTEIN KINASE B; PROTEIN TBC1D1; UNCLASSIFIED DRUG; 5 AMINO 4 IMIDAZOLECARBOXAMIDE; AICA RIBONUCLEOTIDE; DRUG DERIVATIVE; GLUCOSE; MUTANT PROTEIN; NUCLEAR PROTEIN; PHOSPHOSERINE; PHOSPHOSPECIFIC ANTIBODY; RIBONUCLEOTIDE; TBC1D1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; FEMALE; GLUCOSE TRANSPORT; LIPID DIET; MOUSE; MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; ANIMAL; CONSENSUS SEQUENCE; DRUG EFFECT; ENZYMOLOGY; FAT INTAKE; GENETICS; IN VITRO STUDY; METABOLISM; MUSCLE CONTRACTION; MUTATION; PHOSPHORYLATION; PHYSIOLOGY;

MUS; MUS MUSCULUS;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIBODIES, PHOSPHO-SPECIFIC; CONSENSUS SEQUENCE; DIETARY FATS; GLUCOSE; INSULIN; MICE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MUTANT PROTEINS; MUTATION; NUCLEAR PROTEINS; PHOSPHORYLATION; PHOSPHOSERINE; PROTO-ONCOGENE PROTEINS C-AKT; RIBONUCLEOTIDES;

EID: 77957893519     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101100     Document Type: Article

References (45)

1. DeFronzo, R. A., Jacot, E., Jequier, E., Maeder, E., Wahren, J. and Felber, J. P. (1981) The effect of insulin on the disposal of intravenous glucoseResults from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30, 1000-1007
2. Baron, A. D., Brechtel, G., Wallace, P. and Edelman, S. V. (1988) Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans. Am. J. Physiol. 255, E769-E774
3. DeFronzo, R. A., Simonson, D. and Ferrannini, E. (1982) Hepatic and peripheral insulin resistance: a common feature of type II (non-insulin- dependent) and type I (insulin dependent) diabetes mellitus. Diabetologia 23, 313-319 (Pubitemid 12020666)
4. Dohm, G. L., Tapscott, E. B., Pories, W. J., Dabbs, D. J., Flickinger, E. G., Meelheim, D., Fushiki, T., Atkinson, S. M., Elton, C. W. and Caro, J. F. (1988) An in vitro human muscle preparation suitable for metabolic studies. Decreased insulin stimulation of glucose transport in muscle from morbidly obese and diabetic subjects. J. Clin. Invest. 82, 486-494
5. Kennedy, J. W., Hirshman, M. F., Gervino, E. V., Ocel, J. V., Forse, R. A., Hoenig, S. J., Aronson, D., Goodyear, L. J. and Horton, E. S. (1999) Acute exercise induces GLUT4 translocation in skeletal muscle of normal human subjects and subjects with type 2 diabetes. Diabetes 48, 1192-1197
6. Martin, I. K., Katz, A. and Wahren, J. (1995) Splanchnic and muscle metabolism during exercise in NIDDM patients. Am. J. Physiol. 269, E583-E590
7. Minuk, H. L., Vranic, M., Marliss, E. B., Hanna, A. K., Albisser, A. M. and Zinman, B. (1981) Glucoregulatory and metabolic response to exercise in obese noninsulin-dependent diabetes. Am. J. Physiol. 240, E458-E464
8. Hirshman, M. F., Wallberg-Henriksson, H., Wardzala, L. J., Horton, E. D. and Horton, E. S. (1988) Acute exercise increases the number of plasma membrane glucose transporters in rat skeletal muscle. FEBS Lett. 238, 235-239
9. Douen, A. G., Ramlal, T., Klip, A., Young, D. A., Cartee, G. D. and Holloszy, J. O. (1989) Exercise-induced increase in glucose transporters in plasma membranes of rat skeletal muscle. Endocrinology 124, 449-454
10. Ploug, T., van Deurs, B., Ai, H., Cushman, S. W. and Ralston, E. (1998) 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
11. Roy, D. and Marette, A. (1996) Exercise induces the translocation of GLUT4 to transverse tubules from an intracellular pool in rat skeletal muscle. Biochem. Biophys. Res. Commun. 223, 147-152
12. Lauritzen, H. P., Galbo, H., Brandauer, J., Goodyear, L. J. and Ploug, T. (2008) Large GLUT4 vesicles are stationary while locally and reversibly depleted during transient insulin stimulation of the skeletal muscle of living mice. Imaging analysis of GLUT4-EGFP vesicle dynamics. Diabetes 57, 315-324
13. Lauritzen, H. P., Galbo, H., Toyoda, T. and Goodyear, L. J. (2010), Kinetics of contraction-induced GLUT4 translocation in skeletal muscle fibers from living mice. Diabetes 59, 2134-2144
14. Sakamoto, K. and Holman, G. D. (2008) Emerging role for AS160/TBC1D4 and TBC1D1 in the regulation of GLUT4 traffic. Am. J. Physiol. Endocrinol. Metab. 295, E29-E37
15. Kramer, H. F., Witczak, C. A., Fujii, N., Jessen, N., Taylor, E. B., Arnolds, D. E., Sakamoto, K., Hirshman, M. F. and Goodyear, L. J. (2006) Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes 55, 2067-2076
16. 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
17. Zaid, H., Antonescu, C. N., Randhawa, V. K. and Klip, A. (2008) Insulin action on glucose transporters through molecular switches, tracks and tethers. Biochem. J. 413, 201-215
18. Ishikura, S. and Klip, A. (2008) Muscle cells engage Rab8A and myosin Vb in insulin-dependent GLUT4 translocation. Am. J. Physiol. Cell Physiol. 295, C1016-C1025
19. Chen, S., Murphy, J., Toth, R., Campbell, D. G., Morrice, N. A. and MacKintosh, C. (2008) Complementary regulation of TBC1D1 and AS160 by growth factors, insulin and AMPK activators. Biochem. J. 409, 449-459
20. Roach, W. G., Chavez, J. A., Miinea, C. P. and Lienhard, G. E. (2007) Substrate specificity and effect on GLUT4 translocation of the Rab GTPase-activating protein Tbc1d1. Biochem. J. 403, 353-358
21. Taylor, E. B., An, D., Kramer, H. F., Yu, H., Fujii, N. L., Roeckl, K. S., Bowles, N., Hirshman, M. F., Xie, J., Feener, E. P. and Goodyear, L. J. (2008) Discovery of TBC1D1 as an insulin-, AICAR-, and contraction-stimulated signaling nexus in mouse skeletal muscle. J. Biol. Chem. 283, 9787-9796
22. Chavez, J. A., Roach, W. G., Keller, S. R., Lane, W. S. and Lienhard, G. E. (2008) Inhibition of GLUT4 translocation by Tbc1d1, a Rab GTPase-activating protein abundant in skeletal muscle, is partially relieved by AMP-activated protein kinase activation. J. Biol. Chem. 283, 9187-9195
23. Funai, K., Schweitzer, G. G., Castorena, C. M., Kanzaki, M. and Cartee, G. D. (2010) In vivo exercise followed by in vitro contraction additively elevates subsequent insulin-stimulated glucose transport by rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 298, E999-E1010
24. Pehmøller, C., Treebak, J. T., Birk, J. B., Chen, S., MacKintosh, C., Hardie, D. G., Richter, E. A. and Wojtaszewski, J. F. (2009) Genetic disruption of AMPK signaling abolishes both contraction- and insulin-stimulated TBC1D1 phosphorylation and 14-3-3 binding in mouse skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 297, E665-E675
25. Dale, S., Wilson, W. A., Edelman, A. M. and Hardie, D. G. (1995) Similar substrate recognition motifs for mammalian AMP-activated protein kinase, higher plant HMG-CoA reductase kinase-A, yeast SNF1, and mammalian calmodulin-dependent protein kinase I. FEBS Lett. 361, 191-195
26. Peck, G. R., Chavez, J. A., Roach, W. G., Budnik, B. A., Lane, W. S., Karlsson, H. K., Zierath, J. R. and Lienhard, G. E. (2009) Insulin-stimulated phosphorylation of the Rab GTPase-activating protein TBC1D1 regulates GLUT4 translocation. J. Biol. Chem. 284, 30016-30023
27. An, D., Toyoda, T., Taylor, E. B., Yu, H., Fujii, N., Hirshman, M. F. and Goodyear, L. J. (2010) TBC1D1 regulates insulin- and contraction-induced glucose transport in mouse skeletal muscle. Diabetes 59, 1358-1365
28. Fujii, N., Hirshman, M. F., Kane, E. M., Ho, R. C., Peter, L. E., Seifert, M. M. and Goodyear, L. J. (2005) AMP-activated protein kinase α2 activity is not essential for contraction- and hyperosmolarity-induced glucose transport in skeletal muscle. J. Biol. Chem. 280, 39033-39041
29. Cho, H., Mu, J., Kim, J. K., Thorvaldsen, J. L., Chu, Q., Crenshaw, III, E. B., 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
30. Fujii, N., Boppart, M. D., Dufresne, S. D., Crowley, P. F., Jozsi, A. C., Sakamoto, K., Yu, H., Aschenbach, W. G., Kim, S., Miyazaki, H. et al. (2004) Overexpression or ablation of JNK in skeletal muscle has no effect on glycogen synthase activity. Am. J. Physiol. Cell Physiol. 287, C200-C208
31. Aihara, H. and Miyazaki, J. (1998) Gene transfer into muscle by electroporation in vivo. Nat. Biotechnol. 16, 867-870
32. Kramer, H. F., Witczak, C. A., Taylor, E. B., Fujii, N., Hirshman, M. F. and Goodyear, L. J. (2006) AS160 regulates insulin- and contraction-stimulated glucose uptake in mouse skeletal muscle. J. Biol. Chem. 281, 31478-31485
33. Sakamoto, K., Hirshman, M. F., Aschenbach, W. G. and Goodyear, L. J. (2002) Contraction regulation of Akt in rat skeletal muscle. J. Biol. Chem. 277, 11910-11917
34. Beausoleil, S. A., Villen, J., Gerber, S. A., Rush, J. and Gygi, S. P. (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24, 1285-1292
35. Bruss, M. D., Arias, E. B., Lienhard, G. E. and Cartee, G. D. (2005) Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity. Diabetes 54, 41-50
36. Deshmukh, A., Coffey, V. G., Zhong, Z., Chibalin, A. V., Hawley, J. A. and Zierath, J. R. (2006) Exercise-induced phosphorylation of the novel Akt substrates AS160 and filamin A in human skeletal muscle. Diabetes 55, 1776-1782
37. Kramer, H. F., Taylor, E. B., Witczak, C. A., Fujii, N., Hirshman, M. F. and Goodyear, L. J. (2007) The calmodulin-binding domain of AS160 regulates contraction- but not insulin-stimulated glucose uptake in skeletal muscle. Diabetes 56, 2854-2862
38. Hayashi, T., Hirshman, M. F., Kurth, E. J., Winder, W. W. and Goodyear, L. J. (1998) Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47, 1369-1373
39. Jessen, N. and Goodyear, L. J. (2005) Contraction signaling to glucose transport in skeletal muscle. J. Appl. Physiol. 99, 330-337
40. Koh, H. J., Toyoda, T., Fujii, N., Jung, M. M., Rathod, A., Middelbeek, R. J. W., Lessard, S. J., Treebak, J. T., Tsudhihara, K., Esumi, H. et al. (2010), Sucrose nonfermenting AMPK-related kinase (SNARK) mediates contraction-stimulated glucose transport in mouse skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 107, 15541-15546
41. Mu, J., Brozinick, Jr, J. T., Valladares, O., Bucan, M. and Birnbaum, M. J. (2001) A role for AMP-activated protein kinase in contraction-and hypoxia-regulated glucose transport in skeletal muscle. Mol. Cell 7, 1085-1094
42. Jørgensen, S. B., Viollet, B., Andreelli, F., Frøsig, C., Birk, J. B., Schjerling, P., Vaulont, S., Richter, E. A. and Wojtaszewski, J. F. (2004) Knockout of the α2 but not α1 5′-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4-carboxamide-1-β-4- ribofuranoside but not contraction-induced glucose uptake in skeletal muscle. J. Biol. Chem. 279, 1070-1079
43. Funai, K. and Cartee, G. D. (2009) Inhibition of contraction-stimulated AMPK inhibits contraction-stimulated increases in PAS-TBC1D1 and glucose transport without altering PAS-AS160 in rat skeletal muscle. Diabetes 58, 1096-1104
44. Oakes, N. D., Bell, K. S., Furler, S. M., Camilleri, S., Saha, A. K., Ruderman, N. B., Chisholm, D. J. and Kraegen, E. W. (1997) Diet-induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise: parallel relationship between insulin stimulation of glucose uptake and suppression of long-chain fatty acyl-CoA. Diabetes 46, 2022-2028
45. Liu, S., Baracos, V. E., Quinney, H. A. and Clandinin, M. T. (1996) Dietary fat modifies exercise-dependent glucose transport in skeletal muscle. J. Appl. Physiol. 80, 1219-1224