Local overexpression of the myostatin propeptide increases glucose transporter expression and enhances skeletal muscle glucose disposal

American Journal of Physiology - Endocrinology and Metabolism

Volumn 306, Issue 7, 2014, Pages

  Cleasby, M E ^a   Jarmin, S ^b   Eilers, W ^c   Elashry, M ^c   Andersen, D K ^a   Dickson, G ^b   Foster, K ^c  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF READING   (United Kingdom)

Author keywords

AMP activated protein kinase; Glucose transporters; Hypertrophy; Insulin sensitivity; Insulin like growth factor I

Indexed keywords

DEOXYGLUCOSE; GLUCOSE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 4; GLYCOGEN; INSULIN; LATENCY ASSOCIATED PEPTIDE; MYOSTATIN; PHOSPHATIDYLINOSITOL 3 KINASE; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EXTENSOR DIGITORUM LONGUS MUSCLE; GENE OVEREXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT; GLYCOGEN ANALYSIS; GLYCOGEN SYNTHESIS; INSULIN BLOOD LEVEL; INSULIN RELEASE; MALE; MUSCLE MASS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE;

AMP-ACTIVATED PROTEIN KINASE; GLUCOSE TRANSPORTERS; HYPERTROPHY; INSULIN SENSITIVITY; INSULIN-LIKE GROWTH FACTOR-I;

ANIMALS; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; HEK293 CELLS; HUMANS; HYPERTROPHY; INSULIN RESISTANCE; MALE; MUSCLE, SKELETAL; MYOSTATIN; PROTEIN PRECURSORS; RATS; RATS, TRANSGENIC; RATS, WISTAR; TISSUE DISTRIBUTION; UP-REGULATION;

EID: 84900562545     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00586.2013     Document Type: Article

References (60)

1. Akpan I, Goncalves MD, Dhir R, Yin X, Pistilli EE, Bogdanovich S, Khurana TS, Ucran J, Lachey J, Ahima RS. The effects of a soluble activin type IIB receptor on obesity and insulin sensitivity. Int J Obes (Lond) 33: 1265-1273, 2009.
2. Allen DL, Cleary AS, Speaker KJ, Lindsay SF, Uyenishi J, Reed JM, Madden MC, Mehan RS. Myostatin, activin receptor IIb, and follistatinlike-3 gene expression are altered in adipose tissue and skeletal muscle of obese mice. Am J Physiol Endocrinol Metab 294: E918-E927, 2008.
3. Amirouche A, Durieux AC, Banzet S, Koulmann N, Bonnefoy R, Mouret C, Bigard X, Peinnequin A, Freyssenet D. Down-regulation of Akt/mammalian target of rapamycin signaling pathway in response to myostatin overexpression in skeletal muscle. Endocrinology 150: 286-294, 2009.
4. Anderson SB, Goldberg AL, Whitman M. Identification of a novel pool of extracellular pro-myostatin in skeletal muscle. J Biol Chem 283: 7027-7035, 2008.
5. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
6. Brandt C, Nielsen AR, Fischer CP, Hansen J, Pedersen BK, Plomgaard P. Plasma and muscle myostatin in relation to type 2 diabetes. PLoS One 7: e37236, 2012.
7. Bruss MD, Arias EB, Lienhard GE, Cartee GD. Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity. Diabetes 54: 41-50, 2005.
8. Chen BL, Ma YD, Meng RS, Xiong ZJ, Wang HN, Zeng JY, Liu C, Dong YG. Activation of AMPK inhibits cardiomyocyte hypertrophy by modulating of the FOXO1/MuRF1 signaling pathway in vitro. Acta Pharmacol Sinica 31: 798-804, 2010.
9. Cho H, Mu J, Kim JK, Thorvaldsen JL, Chu Q, Crenshaw EB, III, Kaestner KH, Bartolomei MS, Shulman GI, Birnbaum MJ. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292: 1728-1731, 2001.
10. Cleasby ME, Dzamko N, Hegarty BD, Cooney GJ, Kraegen EW, Ye JM. Metformin prevents the development of acute lipid-induced insulin resistance in the rat through altered hepatic signaling mechanisms. Diabetes 53: 3258-3266, 2004.
11. Cleasby ME, Reinten TA, Cooney GJ, James DE, Kraegen EW. Functional studies of Akt isoform specificity in skeletal muscle in vivo; maintained insulin sensitivity despite reduced insulin receptor substrate-1 expression. Mol Endocrinol 21: 215-228, 2007.
12. Foster K, Graham IR, Otto A, Foster H, Trollet C, Yaworsky PJ, Walsh FS, Bickham D, Curtin NA, Kawar SL, Patel K, Dickson G. Adeno-associated virus-8-mediated intravenous transfer of myostatin propeptide leads to systemic functional improvements of slow but not fast muscle. Rejuvenation Res 12: 85-94, 2009.
13. Gilson H, Schakman O, Combaret L, Lause P, Grobet L, Attaix D, Ketelslegers JM, Thissen JP. Myostatin gene deletion prevents glucocorticoid-induced muscle atrophy. Endocrinology 148: 452-460, 2007.
14. Goncalves MD, Pistilli EE, Balduzzi A, Birnbaum MJ, Lachey J, Khurana TS, Ahima RS. Akt deficiency attenuates muscle size and function but not the response to ActRIIB inhibition. PLoS One 5: e12707, 2010.
15. Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP, Brunet A. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282: 30107-30119, 2007.
16. Guo T, Bond ND, Jou W, Gavrilova O, Portas J, McPherron AC. Myostatin inhibition prevents diabetes and hyperphagia in a mouse model of lipodystrophy. Diabetes 61: 2414-2423, 2012.
17. Guo T, Jou W, Chanturiya T, Portas J, Gavrilova O, McPherron AC. Myostatin inhibition in muscle, but not adipose tissue, decreases fat mass and improves insulin sensitivity. PLoS One 4: e4937, 2009.
18. Haidet AM, Rizo L, Handy C, Umapathi P, Eagle A, Shilling C, Boue D, Martin PT, Sahenk Z, Mendell JR, Kaspar BK. Long-term enhancement of skeletal muscle mass and strength by single gene administration of myostatin inhibitors. Proc Natl Acad Sci USA 105: 4318-4322, 2008.
19. Hittel DS, Axelson M, Sarna N, Shearer J, Huffman KM, Kraus WE. Myostatin decreases with aerobic exercise and associates with insulin resistance. Med Sci Sports Exerc 42: 2023-2029, 2010.
20. Jamieson PM, Cleasby ME, Kuperman Y, Morton NM, Kelly PA, Brownstein DG, Mustard KJ, Vaughan JM, Carter RN, Hahn CN, Hardie DG, Seckl JR, Chen A, Vale WW. Urocortin 3 transgenic mice exhibit a metabolically favourable phenotype resisting obesity and hyperglycaemia on a high-fat diet. Diabetologia 54: 2392-2403, 2011.
21. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, Mochida K, Hata T, Matsuda J, Aburatani H, Nishino I, Ezaki O. Skeletal muscle FOXO1 (FKHR)-transgenic mice have less skeletal muscle mass, down-regulated type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279: 41114-41123, 2004.
22. Kang JK, Malerba A, Popplewell L, Foster K, Dickson G. Antisenseinduced myostatin exon skipping leads to muscle hypertrophy in mice following octa-guanidine morpholino oligomer treatment. Mol Ther 19: 159-164, 2011.
23. Kinali M, Arechavala-Gomeza V, Feng L, Cirak S, Hunt D, Adkin C, Guglieri M, Ashton E, Abbs S, Nihoyannopoulos P, Garralda ME, Rutherford M, McCulley C, Popplewell L, Graham IR, Dickson G, Wood MJ, Wells DJ, Wilton SD, Kole R, Straub V, Bushby K, Sewry C, Morgan JE, Muntoni F. Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol 8: 918-928, 2009.
24. Kollias HD, McDermott JC. Transforming growth factor-beta and myostatin signaling in skeletal muscle. J Appl Physiol 104: 579-587, 2008.
25. Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277: 49831-49840, 2002.
26. Lantier L, Mounier R, Leclerc J, Pende M, Foretz M, Viollet B. Coordinated maintenance of muscle cell size control by AMP-activated protein kinase. FASEB J 24: 3555-3561, 2010.
27. Lee SJ. Extracellular regulation of myostatin: a molecular rheostat for muscle mass. Immunol Endocr Metab Agents Med Chem 10: 183-194, 2010.
28. Lee SJ, McPherron AC. Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci USA 98: 9306-9311, 2001.
29. Long YC, Zierath JR. AMP-activated protein kinase signaling in metabolic regulation. J Clin Invest 116: 1776-1783, 2006.
30. Magee TR, Artaza JN, Ferrini MG, Vernet D, Zuniga FI, Cantini L, Reisz-Porszasz S, Rajfer J, Gonzalez-Cadavid NF. Myostatin short interfering hairpin RNA gene transfer increases skeletal muscle mass. J Gene Med 8: 1171-1181, 2006.
31. Marshall A, Salerno MS, Thomas M, Davies T, Berry C, Dyer K, Bracegirdle J, Watson T, Dziadek M, Kambadur R, Bower R, Sharma M. Mighty is a novel promyogenic factor in skeletal myogenesis. Exp Cell Res 314: 1013-1029, 2008.
32. Matsakas A, Foster K, Otto A, Macharia R, Elashry MI, Feist S, Graham I, Foster H, Yaworsky P, Walsh F, Dickson G, Patel K. Molecular, cellular and physiological investigation of myostatin propeptide-mediated muscle growth in adult mice. Neuromuscul Disord 19: 489-499, 2009.
33. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387: 83-90, 1997.
34. McPherron AC, Lee SJ. Suppression of body fat accumulation in myostatin-deficient mice. J Clin Invest 109: 595-601, 2002.
35. Milan G, Dalla Nora E, Pilon C, Pagano C, Granzotto M, Manco M, Mingrone G, Vettor R. Changes in muscle myostatin expression in obese subjects after weight loss. J Clin Endocrinol Metab 89: 2724-2727, 2004.
36. Morrison BM, Lachey JL, Warsing LC, Ting BL, Pullen AE, Underwood KW, Kumar R, Sako D, Grinberg A, Wong V, Colantuoni E, Seehra JS, Wagner KR. A soluble activin type IIB receptor improves function in a mouse model of amyotrophic lateral sclerosis. Exp Neurol 217: 258-268, 2009.
37. Narici MV, Maffulli N. Sarcopenia: characteristics, mechanisms and functional significance. Br Med Bull 95: 139-159, 2010.
38. Ning J, Xi G, Clemmons DR. Suppression of AMPK activation via S485 phosphorylation by IGF-I during hyperglycemia is mediated by AKT activation in vascular smooth muscle cells. Endocrinology 152: 3143-3154, 2011.
39. Palsgaard J, Brons C, Friedrichsen M, Dominguez H, Jensen M, Storgaard H, Spohr C, Torp-Pedersen C, Borup R, De Meyts P, Vaag A. Gene expression in skeletal muscle biopsies from people with type 2 diabetes and relatives: differential regulation of insulin signaling pathways. PLoS One 4: e6575, 2009.
40. Park JJ, Berggren JR, Hulver MW, Houmard JA, Hoffman EP. GRB14, GPD1, and GDF8 as potential network collaborators in weight loss-induced improvements in insulin action in human skeletal muscle. Physiol Genomics 27: 114-121, 2006.
41. Patel SA, Hoehn KL, Lawrence RT, Sawbridge L, Talbot NA, Tomsig JL, Turner N, Cooney GJ, Whitehead JP, Kraegen EW, Cleasby ME. Overexpression of the adiponectin receptor AdipoR1 in rat skeletal muscle amplifies local insulin sensitivity. Endocrinology 153: 5231-5246, 2012.
42. Philippou A, Halapas A, Maridaki M, Koutsilieris M. Type I insulinlike growth factor receptor signaling in skeletal muscle regeneration and hypertrophy. J Musculoskelet Neuronal Interact 7: 208-218, 2007.
43. Polkinghorne E, Lau Q, Cooney GJ, Kraegen EW, Cleasby ME. Local activation of the IκK-NFκB pathway in muscle does not cause insulin resistance. Am J Physiol Endocrinol Metab 294: E316-E325, 2008.
44. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3: 1009-1013, 2001.
45. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103: 16260-16265, 2006.
46. Sonntag F, Kother K, Schmidt K, Weghofer M, Raupp C, Nieto K, Kuck A, Gerlach B, Bottcher B, Muller OJ, Lux K, Horer M, Kleinschmidt JA. The assembly-activating protein promotes capsid assembly of different adeno-associated virus serotypes. J Virol 85: 12686-12697, 2011.
47. Stenholm S, Harris TB, Rantanen T, Visser M, Kritchevsky SB, Ferrucci L. Sarcopenic obesity: definition, cause and consequences. Curr Opin Clin Nutr Metab Care 11: 693-700, 2008.
48. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14: 395-403, 2004.
49. Sun XJ, Wang LM, Zhang Y, Yenush L, Myers MG Jr, Glasheen E, Lane WS, Pierce JH, White MF. Role of IRS-2 in insulin and cytokine signalling. Nature 377: 173-177, 1995.
50. Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ. Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 296: C1258-C1270, 2009.
51. Tsao TS, Burcelin R, Katz EB, Huang L, Charron MJ. Enhanced insulin action due to targeted GLUT4 overexpression exclusively in muscle. Diabetes 45: 28-36, 1996.
52. Wagner KR, Fleckenstein JL, Amato AA, Barohn RJ, Bushby K, Escolar DM, Flanigan KM, Pestronk A, Tawil R, Wolfe GI, Eagle M, Florence JM, King WM, Pandya S, Straub V, Juneau P, Meyers K, Csimma C, Araujo T, Allen R, Parsons SA, Wozney JM, Lavallie ER, Mendell JR. A phase I/IItrial of MYO-029 in adult subjects with muscular dystrophy. Ann Neurol 63: 561-571, 2008.
53. Whiteman EL, Cho H, Birnbaum MJ. Role of Akt/protein kinase B in metabolism. Trends Endocrinol Metab 13: 444-451, 2002.
54. Wilkes JJ, Lloyd DJ, Gekakis N. Loss-of-function mutation in myostatin reduces tumor necrosis factor alpha production and protects liver against obesity-induced insulin resistance. Diabetes 58: 1133-1143, 2009.
55. Williams NG, Interlichia JP, Jackson MF, Hwang D, Cohen P, Rodgers BD. Endocrine actions of myostatin: systemic regulation of the IGF and IGF binding protein axis. Endocrinology 152: 172-180, 2011.
56. Yang W, Zhang Y, Li Y, Wu Z, Zhu D. Myostatin induces cyclin D1 degradation to cause cell cycle arrest through a phosphatidylinositol 3-kinase/AKT/GSK-3 beta pathway and is antagonized by insulin-like growth factor 1. J Biol Chem 282: 3799-3808, 2007.
57. Yang Z, Zhang J, Cong H, Huang Z, Sun L, Liu C, Tien P. A retrovirus-based system to stably silence GDF-8 expression and enhance myogenic differentiation in human rhabdomyosarcoma cells. J Gene Med 10: 825-833, 2008.
58. Zhang C, McFarlane C, Lokireddy S, Bonala S, Ge X, Masuda S, Gluckman PD, Sharma M, Kambadur R. Myostatin-deficient mice exhibit reduced insulin resistance through activating the AMP-activated protein kinase signalling pathway. Diabetologia 54: 1491-1501, 2011.
59. Zhang C, McFarlane C, Lokireddy S, Masuda S, Ge X, Gluckman PD, Sharma M, Kambadur R. Inhibition of myostatin protects against diet-induced obesity by enhancing fatty acid oxidation and promoting a brown adipose phenotype in mice. Diabetologia 55: 183-193, 2012.
60. Zhao B, Wall RJ, Yang J. Transgenic expression of myostatin propeptide prevents diet-induced obesity and insulin resistance. Biochem Biophys Res Commun 337: 248-255, 2005.