Contraction-stimulated glucose transport in muscle is controlled by AMPK and mechanical stress but not sarcoplasmatic reticulum Ca2+ release

Molecular Metabolism

Volumn 3, Issue 7, 2014, Pages 742-753

  Jensen, Thomas E ^a   Sylow, Lykke ^a   Rose, Adam J ^a,b   Madsen, Agnete B ^a   Angin, Yeliz ^a   Maarbjerg, Stine J ^a,c   Richter, Erik A ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c NOVO NORDISK A S   (Denmark)

Author keywords

AMPK; Ca2+; Exercise; Skeletal muscle; Stretch

Indexed keywords

ADENYLATE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; TRANSCRIPTION FACTOR E2F1;

ANALYSIS OF VARIANCE; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CONTROLLED STUDY; EX VIVO STUDY; EXTENSOR DIGITORUM LONGUS MUSCLE; FEEDBACK SYSTEM; FEMALE; GLUCOSE TRANSPORT; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MECHANICAL STRESS; MOUSE; MUSCLE CONTRACTION; NONHUMAN; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SOLEUS MUSCLE;

EID: 84908218504     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2014.07.005     Document Type: Article

References (59)

1. James D.E., Kraegen E.W., Chisholm D.J. Muscle glucose metabolism in exercising rats: comparison with insulin stimulation. American Journal of Physiology 1985, 248:E575-E580.
2. Goodyear L.J., Kahn B.B. Exercise, glucose transport, and insulin sensitivity. Annual Review of Medicine 1998, 49:235-261.
3. Richter E.A., Hargreaves M. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiological Reviews 2013, 93:993-1017.
4. Mu J., Brozinick J.T., Valladares O., Bucan M., Birnbaum M.J. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Molecular Cell 2001, 7:1085-1094.
5. Ihlemann J., Ploug T., Hellsten Y., Galbo H. Effect of tension on contraction-induced glucose transport in rat skeletal muscle. American Journal of Physiology 1999, 277:E208-E214.
6. Youn J.H., Gulve E.A., Holloszy J.O. Calcium stimulates glucose transport in skeletal muscle by a pathway independent of contraction. American Journal of Physiology 1991, 260:C555-C561.
7. Wright D.C., Hucker K.A., Holloszy J.O., Han D.H. Ca2+ and AMPK both mediate stimulation of glucose transport by muscle contractions. Diabetes 2004, 53:330-335.
8. Wright D.C., Geiger P.C., Holloszy J.O., Han D.H. Contraction- and hypoxia-stimulated glucose transport is mediated by a Ca2+-dependent mechanism in slow-twitch rat soleus muscle. American Journal of Physiology. Endocrinology and Metabolism 2005, 288:E1062-E1066.
9. Raney M.A., Turcotte L.P. Evidence for the involvement of CaMKII and AMPK in Ca2+-dependent signaling pathways regulating FA uptake and oxidation in contracting rodent muscle. Journal of Applied Physiology 2008, 104:1366-1373.
10. Jensen T.E., Rose A.J., Hellsten Y., Wojtaszewski J.F., Richter E.A. Caffeine-induced Ca(2+) release increases AMPK-dependent glucose uptake in rodent soleus muscle. American Journal of Physiology. Endocrinology and Metabolism 2007, 293:E286-E292.
11. Egawa T., Hamada T., Ma X., Karaike K., Kameda N., Masuda S., et al. Caffeine activates preferentially alpha1-isoform of 5'AMP-activated protein kinase in rat skeletal muscle. Acta Physiologica (Oxford) 2011, 201:227-238.
12. Smith I.C., Bombardier E., Vigna C., Tupling A.R. ATP consumption by sarcoplasmic reticulum Ca(2)(+) pumps accounts for 40-50% of resting metabolic rate in mouse fast and slow twitch skeletal muscle. PLoS ONE 2013, 8:e68924.
13. Abbott M.J., Bogachus L.D., Turcotte L.P. AMPKalpha2 deficiency uncovers time dependency in the regulation of contraction-induced palmitate and glucose uptake in mouse muscle. Journal of Applied Physiology 2011, 111:125-134.
14. Rose A.J., Alsted T.J., Jensen T.E., Kobbero J.B., Maarbjerg S.J., Jensen J., et al. A Ca(2+)-calmodulin-eEF2K-eEF2 signalling cascade, but not AMPK, contributes to the suppression of skeletal muscle protein synthesis during contractions. The Journal of Physiology 2009, 587:1547-1563.
15. Baylor S.M., Hollingworth S. Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. The Journal of Physiology 2003, 551:125-138.
16. Cheung A., Dantzig J.A., Hollingworth S., Baylor S.M., Goldman Y.E., Mitchison T.J., et al. A small-molecule inhibitor of skeletal muscle myosin II. Nature Cell Biology 2002, 4:83-88.
17. Straight A.F., Cheung A., Limouze J., Chen I., Westwood N.J., Sellers J.R., et al. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 2003, 299:1743-1747.
18. Dou Y., Arlock P., Arner A. Blebbistatin specifically inhibits actin-myosin interaction in mouse cardiac muscle. American Journal of Physiology. Cell Physiology 2007, 293:C1148-C1153.
19. Steimle P.A., Fulcher F.K., Patel Y.M. A novel role for myosin II in insulin-stimulated glucose uptake in 3T3-L1 adipocytes. Biochemical and Biophysical Research Communications 2005, 331:1560-1565.
20. Chambers M.A., Moylan J.S., Smith J.D., Goodyear L.J., Reid M.B. Stretch-stimulated glucose uptake in skeletal muscle is mediated by reactive oxygen species and p38 MAP-kinase. The Journal of Physiology 2009, 587:3363-3373.
21. Blair D.R., Funai K., Schweitzer G.G., Cartee G.D. A myosin II ATPase inhibitor reduces force production, glucose transport, and phosphorylation of AMPK and TBC1D1 in electrically stimulated rat skeletal muscle. American Journal of Physiology. Endocrinology and Metabolism 2009, 296:E993-E1002.
22. Sandstrom M.E., Zhang S.J., Westerblad H., Katz A. Mechanical load plays little role in contraction-mediated glucose transport in mouse skeletal muscle. The Journal of Physiology 2007, 579:527-534.
23. Birk J.B., Wojtaszewski J.F. Predominant alpha2/beta2/gamma3 AMPK activation during exercise in human skeletal muscle. The Journal of Physiology 2006, 577:1021-1032.
24. Frosig C., Pehmoller C., Birk J.B., Richter E.A., Wojtaszewski J.F. Exercise-induced TBC1D1 Ser237 phosphorylation and 14-3-3 protein binding capacity in human skeletal muscle. The Journal of Physiology 2010, 588:4539-4548.
25. Sylow L., Jensen T.E., Kleinert M., Mouatt J.R., Maarbjerg S.J., Jeppesen J., et al. Rac1 is a novel regulator of contraction-stimulated glucose uptake in skeletal muscle. Diabetes 2013, 62:1139-1151.
26. Sandstrom M.E., Zhang S.J., Bruton J., Silva J.P., Reid M.B., Westerblad H., et al. Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. The Journal of Physiology 2006, 575:251-262.
27. Koh H.J., Toyoda T., Fujii N., Jung M.M., Rathod A., Middelbeek R.J., et al. Sucrose nonfermenting AMPK-related kinase (SNARK) mediates contraction-stimulated glucose transport in mouse skeletal muscle. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:15541-15546.
28. Jensen T.E., Maarbjerg S.J., Rose A.J., Leitges M., Richter E.A. Knockout of the predominant conventional PKC isoform, PKCalpha, in mouse skeletal muscle does not affect contraction-stimulated glucose uptake. American Journal of Physiology. Endocrinology and Metabolism 2009, 297:E340-E348.
29. Wojtaszewski J.F., Laustsen J.L., Derave W., Richter E.A. Hypoxia and contractions do not utilize the same signaling mechanism in stimulating skeletal muscle glucose transport. Biochimica et Biophysica Acta 1998, 1380:396-404.
30. Li Q., Zhu X., Ishikura S., Zhang D., Gao J., Sun Y., et al. Ca2+ signals promote GLUT4 exocytosis and reduce its endocytosis in muscle cells. American Journal of Physiology. Endocrinology and Metabolism 2014, 307:E209-E224.
31. Witczak C.A., Jessen N., Warro D.M., Toyoda T., Fujii N., Anderson M.E., et al. CaMKII regulates contraction- but not insulin-induced glucose uptake in mouse skeletal muscle. American Journal of Physiology. Endocrinology and Metabolism 2010, 298:E1150-E1160.
32. Ikemoto T., Hosoya T., Takata K., Aoyama H., Hiramatsu T., Onoe H., et al. Functional role of neuroendocrine-specific protein-like 1 in membrane translocation of GLUT4. Diabetes 2009, 58:2802-2812.
33. Jensen T.E., Rose A.J., Jorgensen S.B., Brandt N., Schjerling P., Wojtaszewski J.F., et al. Possible CaMKK-dependent regulation of AMPK phosphorylation and glucose uptake at the onset of mild tetanic skeletal muscle contraction. American Journal of Physiology. Endocrinology and Metabolism 2007, 292:E1308-E1317.
34. Abbott M.J., Edelman A.M., Turcotte L.P. CaMKK is an upstream signal of AMP-activated protein kinase in regulation of substrate metabolism in contracting skeletal muscle. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2009, 297:R1724-R1732.
35. Lanner J.T., Bruton J.D., Assefaw-Redda Y., Andronache Z., Zhang S.J., Severa D., et al. Knockdown of TRPC3 with siRNA coupled to carbon nanotubes results in decreased insulin-mediated glucose uptake in adult skeletal muscle cells. FASEB Journal 2009, 23:1728-1738.
36. Kitajima N., Watanabe K., Morimoto S., Sato Y., Kiyonaka S., Hoshijima M., et al. TRPC3-mediated Ca2+ influx contributes to Rac1-mediated production of reactive oxygen species in MLP-deficient mouse hearts. Biochemical and Biophysical Research Communications 2011, 409:108-113.
37. Witczak C.A., Jessen N., Warro D.M., Toyoda T., Fujii N., Anderson M.E., et al. CaMKII regulates contraction-induced, but not insulin-induced, glucose uptake in mouse skeletal muscle. American Journal of Physiology. Endocrinology and Metabolism 2010, 298:E1150-E1160.
38. Merry T.L., Steinberg G.R., Lynch G.S., McConell G.K. Skeletal muscle glucose uptake during contraction is regulated by nitric oxide and ROS independently of AMPK. American Journal of Physiology. Endocrinology and Metabolism 2010, 298:E577-E585.
39. Lanner J.T., Katz A., Tavi P., Sandstrom M.E., Zhang S.J., Wretman C., et al. The role of Ca2+ influx for insulin-mediated glucose uptake in skeletal muscle. Diabetes 2006, 55:2077-2083.
40. Cartee G.D., Briggs-Tung C., Holloszy J.O. Diverse effects of calcium channel blockers on skeletal muscle glucose transport. American Journal of Physiology 1992, 263:R70-R75.
41. Limouze J., Straight A.F., Mitchison T., Sellers J.R. Specificity of blebbistatin, an inhibitor of myosin II. Journal of Muscle Research and Cell Motility 2004, 25:337-341.
42. Choi Y.O., Ryu H.J., Kim H.R., Song Y.S., Kim C., Lee W., et al. Implication of phosphorylation of the myosin II regulatory light chain in insulin-stimulated GLUT4 translocation in 3T3-F442A adipocytes. Experimental & Molecular Medicine 2006, 38:180-189.
43. Fulcher F.K., Smith B.T., Russ M., Patel Y.M. Dual role for myosin II in GLUT4-mediated glucose uptake in 3T3-L1 adipocytes. Experimental Cell Research 2008, 314:3264-3274.
44. Chung le T.K., Hosaka T., Harada N., Jambaldorj B., Fukunaga K., Nishiwaki Y., et al. Myosin IIA participates in docking of Glut4 storage vesicles with the plasma membrane in 3T3-L1 adipocytes. Biochemical and Biophysical Research Communications 2010, 391:995-999.
45. Ihlemann J., Ploug T., Hellsten Y., Galbo H. Effect of stimulation frequency on contraction-induced glucose transport in rat skeletal muscle. American Journal of Physiology. Endocrinology and Metabolism 2000, 279:E862-E867.
46. Stephenson D.G., Williams D.A. Calcium-activated force responses in fast- and slow-twitch skinned muscle fibres of the rat at different temperatures. The Journal of Physiology 1981, 317:281-302.
47. Derave W., Straumann N., Olek R.A., Hespel P. Electrolysis stimulates creatine transport and transporter cell surface expression in incubated mouse skeletal muscle: potential role of ROS. American Journal of Physiology. Endocrinology and Metabolism 2006, 291:E1250-E1257.
48. Jensen T.E., Richter E.A. Regulation of glucose and glycogen metabolism during and after exercise. The Journal of Physiology 2012, 590:1069-1076.
49. Lai Y.C., Kviklyte S., Vertommen D., Lantier L., Foretz M., Viollet B., et al. A small-molecule benzimidazole derivative that potently activates AMPK to increase glucose transport in skeletal muscle: comparison with effects of contraction and other AMPK activators. Biochemical Journal 2014, 460:363-375.
50. Jørgensen S.B., Viollet B., Andreelli F., Frosig C., Birk J.B., Schjerling P., et al. Knockout of the alpha2 but not alpha1 5'-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4-carboxamide-1-beta-4-ribofuranosidebut not contraction-induced glucose uptake in skeletal muscle. The Journal of Biological Chemistry 2004, 279:1070-1079.
51. An D., Toyoda T., Taylor E.B., Yu H., Fujii N., Hirshman M.F., et al. TBC1D1 regulates insulin- and contraction-induced glucose transport in mouse skeletal muscle. Diabetes 2010, 59:1358-1365.
52. Lee-Young R.S., Griffee S.R., Lynes S.E., Bracy D.P., Ayala J.E., McGuinness O.P., et al. Skeletal muscle AMP-activated protein kinase is essential for the metabolic response to exercise in vivo. The Journal of Biological Chemistry 2009, 284:23925-23934.
53. Thomas M.M., Wang D.C., D'Souza D.M., Krause M.P., Layne A.S., Criswell D.S., et al. Muscle-specific AMPK beta1beta2-null mice display a myopathy due to loss of capillary density in nonpostural muscles. FASEB Journal 2014, 28:2098-2107.
54. Liu Y., Lai Y.C., Hill E.V., Tyteca D., Carpentier S., Ingvaldsen A., et al. Phosphatidylinositol 3-phosphate 5-kinase (PIKfyve) is an AMPK target participating in contraction-stimulated glucose uptake in skeletal muscle. Biochemical Journal 2013, 455:196-206.
55. Ikemoto T., Suzuki M., Onoe H. Involvement of a phosphorylation-mediated pathway to regulate the function of NSPL1 in exercise. Journal of Veterinary Medical Science 2011, 73:733-738.
56. Chen Q., Quan C., Xie B., Chen L., Zhou S., Toth R., et al. GARNL1, a major RalGAP alpha subunit in skeletal muscle, regulates insulin-stimulated RalA activation and GLUT4 trafficking via interaction with 14-3-3 proteins. Cell Signal 2014, 26:1636-1648.
57. Nozaki S., Ueda S., Takenaka N., Kataoka T., Satoh T. Role of RalA downstream of Rac1 in insulin-dependent glucose uptake in muscle cells. Cell Signal 2012, 24:2111-2117.
58. O'Neill H.M., Maarbjerg S.J., Crane J.D., Jeppesen J., Jorgensen S.B., Schertzer J.D., et al. AMP-activated protein kinase (AMPK) beta1beta2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:16092-16097.
59. Lantier L., Fentz J., Mounier R., Leclerc J., Treebak J.T., Pehmoller C., et al. AMPK controls exercise endurance, mitochondrial oxidative capacity, and skeletal muscle integrity. FASEB Journal 2014, 28:3211-3224.