Differential Role of Insulin/IGF-1 Receptor Signaling in Muscle Growth and Glucose Homeostasis

Cell Reports

Volumn 11, Issue 8, 2015, Pages 1220-1235

  O'Neill, Brian T ^a   Lauritzen, Hans P M M ^a   Hirshman, Michael F ^a   Smyth, Graham ^a   Goodyear, Laurie J ^a   Kahn, C Ronald ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 4; INSULIN RECEPTOR; SOMATOMEDIN C RECEPTOR; GLUCOSE; MUSCLE PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE PREDISPOSITION; ENERGY EXPENDITURE; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; HYPOGLYCEMIA; INSULIN TOLERANCE TEST; MALE; METABOLIC REGULATION; MOUSE; MUSCLE GROWTH; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SUBCUTANEOUS FAT; ANIMAL; FEMALE; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; SKELETAL MUSCLE;

ANIMALIA; MUS;

ANIMALS; FEMALE; GLUCOSE; HOMEOSTASIS; MALE; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHOSPHORYLATION; RECEPTOR, IGF TYPE 1; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 84929966244     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.04.037     Document Type: Article

References (43)

1. An D., Toyoda T., Taylor E.B., Yu H., Fujii N., Hirshman M.F., Goodyear L.J. TBC1D1 regulates insulin- and contraction-induced glucose transport in mouse skeletal muscle. Diabetes 2010, 59:1358-1365.
2. Boström P., Wu J., Jedrychowski M.P., Korde A., Ye L., Lo J.C., Rasbach K.A., Boström E.A., Choi J.H., Long J.Z., et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 2012, 481:463-468.
3. Boucher J., Macotela Y., Bezy O., Mori M.A., Kriauciunas K., Kahn C.R. A kinase-independent role for unoccupied insulin and IGF-1 receptors in the control of apoptosis. Sci. Signal. 2010, 3:ra87.
4. Boucher J., Mori M.A., Lee K.Y., Smyth G., Liew C.W., Macotela Y., Rourk M., Bluher M., Russell S.J., Kahn C.R. Impaired thermogenesis and adipose tissue development in mice with fat-specific disruption of insulin and IGF-1 signalling. Nat. Commun. 2012, 3:902.
5. Brüning J.C., Michael M.D., Winnay J.N., Hayashi T., Hörsch D., Accili D., Goodyear L.J., Kahn C.R. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol. Cell 1998, 2:559-569.
6. Dokas J., Chadt A., Nolden T., Himmelbauer H., Zierath J.R., Joost H.G., Al-Hasani H. Conventional knockout of Tbc1d1 in mice impairs insulin- and AICAR-stimulated glucose uptake in skeletal muscle. Endocrinology 2013, 154:3502-3514.
7. Fafalios A., Ma J., Tan X., Stoops J., Luo J., Defrances M.C., Zarnegar R. A hepatocyte growth factor receptor (Met)-insulin receptor hybrid governs hepatic glucose metabolism. Nat. Med. 2011, 17:1577-1584.
8. Fernández A.M., Kim J.K., Yakar S., Dupont J., Hernandez-Sanchez C., Castle A.L., Filmore J., Shulman G.I., Le Roith D. Functional inactivation of the IGF-I and insulin receptors in skeletal muscle causes type 2 diabetes. Genes Dev. 2001, 15:1926-1934.
9. Fernández A.M., Dupont J., Farrar R.P., Lee S., Stannard B., Le Roith D. Muscle-specific inactivation of the IGF-I receptor induces compensatory hyperplasia in skeletal muscle. J.Clin. Invest. 2002, 109:347-355.
10. Fujii N., Jessen N., Goodyear L.J. AMP-activated protein kinase and the regulation of glucose transport. Am. J. Physiol. Endocrinol. Metab. 2006, 291:E867-E877.
11. Fulks R.M., Li J.B., Goldberg A.L. Effects of insulin, glucose, and amino acids on protein turnover in rat diaphragm. J.Biol. Chem. 1975, 250:290-298.
12. Hayashi T., Hirshman M.F., Kurth E.J., Winder W.W., Goodyear L.J. Evidence for 5' AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 1998, 47:1369-1373.
13. Ishikura S., Klip A. Muscle cells engage Rab8A and myosin Vb in insulin-dependent GLUT4 translocation. Am. J. Physiol. Cell Physiol. 2008, 295:C1016-C1025.
14. Kim H., Haluzik M., Asghar Z., Yau D., Joseph J.W., Fernandez A.M., Reitman M.L., Yakar S., Stannard B., Heron-Milhavet L., et al. Peroxisome proliferator-activated receptor-alpha agonist treatment in a transgenic model of type 2 diabetes reverses the lipotoxic state and improves glucose homeostasis. Diabetes 2003, 52:1770-1778.
15. Kim K.H., Jeong Y.T., Oh H., Kim S.H., Cho J.M., Kim Y.N., Kim S.S., Kim H., Hur K.Y., Kim H.K., et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat. Med. 2013, 19:83-92.
16. Klip A. The many ways to regulate glucose transporter 4. Appl. Physiol. Nutr. Metab. 2009, 34:481-487.
17. Koh H.J., Brandauer J., Goodyear L.J. LKB1 and AMPK and the regulation of skeletal muscle metabolism. Curr. Opin. Clin. Nutr. Metab. Care 2008, 11:227-232.
18. Lauritzen H.P. Imaging of protein translocation insitu in skeletal muscle of living mice. Methods Mol. Biol. 2010, 637:231-244.
19. Lauritzen H.P., Schertzer J.D. Measuring GLUT4 translocation in mature muscle fibers. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E169-E179.
20. Lauritzen H.P., 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 invivo. Pflugers Arch. 2002, 444:710-721.
21. Lauritzen H.P., Ploug T., Prats C., Tavaré J.M., Galbo H. Imaging of insulin signaling in skeletal muscle of living mice shows major role of T-tubules. Diabetes 2006, 55:1300-1306.
22. Lauritzen H.P., Galbo H., Brandauer J., Goodyear L.J., 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 2008, 57:315-324.
23. Lauritzen H.P., Galbo H., Toyoda T., Goodyear L.J. Kinetics of contraction-induced GLUT4 translocation in skeletal muscle fibers from living mice. Diabetes 2010, 59:2134-2144.
24. Laustsen P.G., Russell S.J., Cui L., Entingh-Pearsall A., Holzenberger M., Liao R., Kahn C.R. Essential role of insulin and insulin-like growth factor 1 receptor signaling in cardiac development and function. Mol. Cell. Biol. 2007, 27:1649-1664.
25. Mammucari C., Milan G., Romanello V., Masiero E., Rudolf R., Del Piccolo P., Burden S.J., Di Lisi R., Sandri C., Zhao J., et al. FoxO3 controls autophagy in skeletal muscle invivo. Cell Metab. 2007, 6:458-471.
26. Marette A., Richardson J.M., Ramlal T., Balon T.W., Vranic M., Pessin J.E., Klip A. Abundance, localization, and insulin-induced translocation of glucose transporters in red and white muscle. Am. J. Physiol. 1992, 263:C443-C452.
27. Martin B.C., Warram J.H., Krolewski A.S., Bergman R.N., Soeldner J.S., Kahn C.R. Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study. Lancet 1992, 340:925-929.
28. Mavalli M.D., DiGirolamo D.J., Fan Y., Riddle R.C., Campbell K.S., van Groen T., Frank S.J., Sperling M.A., Esser K.A., Bamman M.M., Clemens T.L. Distinct growth hormone receptor signaling modes regulate skeletal muscle development and insulin sensitivity in mice. J.Clin. Invest. 2010, 120:4007-4020.
29. Meek S.E., Persson M., Ford G.C., Nair K.S. Differential regulation of amino acid exchange and protein dynamics across splanchnic and skeletal muscle beds by insulin in healthy human subjects. Diabetes 1998, 47:1824-1835.
30. Miniou P., Tiziano D., Frugier T., Roblot N., Le Meur M., Melki J. Gene targeting restricted to mouse striated muscle lineage. Nucleic Acids Res. 1999, 27:e27.
31. Moller D.E., Chang P.Y., Yaspelkis B.B., Flier J.S., Wallberg-Henriksson H., Ivy J.L. Transgenic mice with muscle-specific insulin resistance develop increased adiposity, impaired glucose tolerance, and dyslipidemia. Endocrinology 1996, 137:2397-2405.
32. Rommel C., Bodine S.C., Clarke B.A., Rossman R., Nunez L., Stitt T.N., Yancopoulos G.D., Glass D.J. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 2001, 3:1009-1013.
33. Sandri M., Sandri C., Gilbert A., Skurk C., Calabria E., Picard A., Walsh K., Schiaffino S., Lecker S.H., Goldberg A.L. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004, 117:399-412.
34. Scheepers A., Joost H.G., Schürmann A. The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function. JPEN J. Parenter. Enteral Nutr. 2004, 28:364-371.
35. Schiaffino S., Mammucari C. Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 2011, 1:4.
36. Storlien L., Oakes N.D., Kelley D.E. Metabolic flexibility. Proc. Nutr. Soc. 2004, 63:363-368.
37. Szekeres F., Chadt A., Tom R.Z., Deshmukh A.S., Chibalin A.V., Björnholm M., Al-Hasani H., Zierath J.R. The Rab-GTPase-activating protein TBC1D1 regulates skeletal muscle glucose metabolism. Am. J. Physiol. Endocrinol. Metab. 2012, 303:E524-E533.
38. Taniguchi C.M., Emanuelli B., Kahn C.R. Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 2006, 7:85-96.
39. 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., Goodyear L.J. Discovery of TBC1D1 as an insulin-, AICAR-, and contraction-stimulated signaling nexus in mouse skeletal muscle. J.Biol. Chem. 2008, 283:9787-9796.
40. Vaitheesvaran B., LeRoith D., Kurland I.J. MKR mice have increased dynamic glucose disposal despite metabolic inflexibility, and hepatic and peripheral insulin insensitivity. Diabetologia 2010, 53:2224-2232.
41. Wang W., Hansen P.A., Marshall B.A., Holloszy J.O., Mueckler M. Insulin unmasks a COOH-terminal Glut4 epitope and increases glucose transport across T-tubules in skeletal muscle. J.Cell Biol. 1996, 135:415-430.
42. Zhou Q.L., Jiang Z.Y., Holik J., Chawla A., Hagan G.N., Leszyk J., Czech M.P. Akt substrate TBC1D1 regulates GLUT1 expression through the mTOR pathway in 3T3-L1 adipocytes. Biochem. J. 2008, 411:647-655.
43. Zisman A., Peroni O.D., Abel E.D., Michael M.D., Mauvais-Jarvis F., Lowell B.B., Wojtaszewski J.F., Hirshman M.F., Virkamaki A., Goodyear L.J., et al. Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat. Med. 2000, 6:924-928.