Myostatin is a key mediator between energy metabolism and endurance capacity of skeletal muscle

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 307, Issue 4, 2014, Pages

  Mouisel, Etienne ^a,b   Relizani, Karima ^c,d   Mille Hamard, Laurence ^e   Denis, Raphaël ^f   Hourdé, Christophe ^b,g   Agbulut, Onnik ^a   Patel, Ketan ^h   Arandel, Ludovic ^b   Morales Gonzalez, Susanne ^c   Vignaud, Alban ⁱ   Garcia, Luis ^d,j   Ferry, Arnaud ^b,f   Luquet, Serge ^a,f   Billat, Véronique ^e   Ventura Clapier, Renée ^k   Schuelke, Markus ^c   Amthor, Helge ^b,d,j  

^a CNRS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^e UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g UNIVERSITÉ DE SAVOIE   (France)

^h UNIVERSITY OF READING   (United Kingdom)

ⁱ GÉNÉTHON   (France)

^j CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

^k Universite Paris Sud   (France)

more..

Author keywords

Exercise capacity; Mitochondria; Muscle fatigue; Myostatin; Oxidative phosphorylation; Peroxisome proliferatior activated receptor

Indexed keywords

ADENOVIRUS VECTOR; ENOLASE; MYOSTATIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

ADULT; ANAEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDURANCE; ENERGY COST; ENERGY METABOLISM; ENZYME ACTIVITY; FEMALE; GENE OVEREXPRESSION; LACTIC ACIDOSIS; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE CELL; MUSCLE FATIGUE; MUSCLE FUNCTION; MUSCLE MASS; MUSCLE STRENGTH; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PHENOTYPE; PHYSICAL CAPACITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RUNNING; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WILD TYPE;

EXERCISE CAPACITY; MITOCHONDRIA; MUSCLE FATIGUE; MYOSTATIN; OXIDATIVE PHOSPHORYLATION; PEROXISOME PROLIFERATIOR-ACTIVATED RECEPTOR;

ANIMALS; ENERGY METABOLISM; GENOTYPE; GLYCOLYSIS; LACTIC ACID; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, MUSCLE; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL; MYOSTATIN; OXYGEN CONSUMPTION; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; PHENOTYPE; PHOSPHOPYRUVATE HYDRATASE; PHYSICAL ENDURANCE; RUNNING; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84907678063     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00377.2013     Document Type: Article

References (49)

1. Agbulut O, Noirez P, Beaumont F, Butler-Browne G. Myosin heavy chain isoforms in postnatal muscle development of mice. Biol Cell 95: 399-406, 2003.
2. Agbulut O, Vignaud A, Hourde C, Mouisel E, Fougerousse F, Butler-Browne GS, Ferry A. Slow myosin heavy chain expression in the absence of muscle activity. Am J Physiol Cell Physiol 296: C205-C214, 2009.
3. 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 33: 1265-1273, 2009.
4. Amthor H, Macharia R, Navarrete R, Schuelke M, Brown SC, Otto A, Voit T, Muntoni F, Vrbova G, Partridge T, Zammit P, Bunger L, Patel K. Lack of myostatin results in excessive muscle growth but impaired force generation. Proc Natl Acad Sci USA 104: 1835-1840, 2007.
5. Athea Y, Viollet B, Mateo P, Rousseau D, Novotova M, Garnier A, Vaulont S, Wilding JR, Grynberg A, Veksler V, Hoerter J, Ventura-Clapier R. AMP-activated protein kinase 2 deficiency affects cardiac cardiolipin homeostasis and mitochondrial function. Diabetes 56: 786-794, 2007.
6. Baligand C, Gilson H, Menard JC, Schakman O, Wary C, Thissen JP, Carlier PG. Functional assessment of skeletal muscle in intact mice lacking myostatin by concurrent NMR imaging and spectroscopy. Gene Ther 17: 328-337, 2010.
7. Bernardo BL, Wachtmann TS, Cosgrove PG, Kuhn M, Opsahl AC, Judkins KM, Freeman TB, Hadcock JR, LeBrasseur NK. Postnatal PPARδ activation and myostatin inhibition exert distinct yet complimentary effects on the metabolic profile of obese insulin-resistant mice. PLoS One 5: e11307, 2010.
8. Billat VL, Mouisel E, Roblot N, Melki J. Inter-and intrastrain variation in mouse critical running speed. J Appl Physiol 98: 1258-1263, 2005.
9. Brown ML, Bonomi L, Ungerleider N, Zina J, Kimura F, Mukherjee A, Sidis Y, Schneyer A. Follistatin and follistatin like-3 differentially regulate adiposity and glucose homeostasis. Obesity (Silver Spring) 19: 1940-1949, 2011.
10. Butler-Browne GS, Whalen RG. Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. Dev Biol 102: 324-334, 1984.
11. Cadena SM, Tomkinson KN, Monnell TE, Spaits MS, Kumar R, Underwood KW, Pearsall RS, Lachey JL. Administration of a soluble activin type IIB receptor promotes skeletal muscle growth independent of fiber type. J Appl Physiol 109: 635-642, 2010.
12. Cleasby ME, Jarmin S, Eilers W, Elashry M, Andersen DK, Dickson G, Foster K. Local overexpression of the myostatin propeptide increases glucose transporter expression and enhances skeletal muscle glucose disposal. Am J Physiol Endocrinol Metab 306: E814-E823, 2014.
13. Fournier B, Murray B, Gutzwiller S, Marcaletti S, Marcellin D, Bergling S, Brachat S, Persohn E, Pierrel E, Bombard F, Hatakeyama S, Trendelenburg AU, Morvan F, Richardson B, Glass DJ, Lach-Trifilieff E, Feige JN. Blockade of the activin receptor IIb activates functional brown adipogenesis and thermogenesis by inducing mitochondrial oxidative metabolism. Mol Cell Biol 32: 2871-2879, 2012.
14. Gan Z, Rumsey J, Hazen BC, Lai L, Leone TC, Vega RB, Xie H, Conley KE, Auwerx J, Smith SR, Olson EN, Kralli A, Kelly DP. Nuclear receptor/microRNA circuitry links muscle fiber type to energy metabolism. J Clin Invest 123: 2564-2575, 2013.
15. Giannesini B, Vilmen C, Amthor H, Bernard M, Bendahan D. Lack of myostatin impairs mechanical performance and ATP cost of contraction in exercising mouse gastrocnemius muscle in vivo. Am J Physiol Endocrinol Metab 305: E33-E40, 2013.
16. Gonin P, Arandel A, Van Wittenberghe L, Marais T, Perez N, Danos O. Femoralintra-arterial injection: a tool to deliver and assess recombinant AAV constructs in rodents whole hind limb. J Gene Med 7: 782-791, 2005.
17. Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Menissier F, Massabanda J, Fries R, Hanset R, Georges M. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 17: 71-74, 1997.
18. Hennebry A, Berry C, Siriett V, O'Callaghan P, Chau L, Watson T, Sharma M, Kambadur R. Myostatin regulates fiber-type composition of skeletal muscle by regulating MEF2 and MyoD gene expression. Am J Physiol Cell Physiol 296: C525-C534, 2009.
19. Heineke J, Auger-Messier M, Xu J, Sargent M, York A, Welle S, Molkentin JD. Genetic deletion of myostatin from the heart prevents skeletal muscle atrophy in heart failure. Circulation 121: 419-425, 2010.
20. Holmes JH, Ashmore CR, Robinson DW. Effects of stress on cattle with hereditary muscular hypertrophy. J Anim Sci 36: 684-694, 1973.
21. Holmes JH, Robinson DW, Ashmore CR. Blood lactic acid and behaviour in cattle with hereditary muscular hypertrophy. J Anim Sci 35: 1011-1013, 1972.
22. Hourde C, Vignaud A, Beurdy I, Martelly I, Keller A, Ferry A. Sustained peripheral arterial insufficiency durably impairs normal and regenerating skeletal muscle function. J Physiol Sci 56: 361-367, 2006.
23. Hulmi JJ, Oliveira BM, Silvennoinen M, Hoogaars WM, Ma H, Pierre P, Pasternack A, Kainulainen H, Ritvos O. Muscle protein synthesis, mTORC1/MAPK/Hippo signaling, and capillary density are altered by blocking of myostatin and activins. Am J Physiol Endocrinol Metab 304: E41-E50, 2013.
24. Janssen AJ, Schuelke M, Smeitink JA, Trijbels FJ, Sengers RC, Lucke B, Wintjes LT, Morava E, van Engelen BG, Smits BW, Hol FA, Siers MH, Ter Laak H, van der Knaap MS, Van Spronsen FJ, Rodenburg RJ, van den Heuvel LP. Muscle 3243A¡G mutation load and capacity of the mitochondrial energy-generating system. Ann Neurol 63: 473-481, 2008.
25. Kemi OJ, Loennechen JP, Wisloff U, Ellingsen O. Intensity-controlled treadmill running in mice: cardiac and skeletal muscle hypertrophy. J Appl Physiol 93: 1301-1309, 2002.
26. Lipina C, Kendall H, McPherron AC, Taylor PM, Hundal HS. Mechanisms involved in the enhancement of mammalian target of rapamycin signalling and hypertrophy in skeletal muscle of myostatin-deficient mice. FEBS Lett 584: 2403-2408, 2010.
27. Macdonald EM, Andres-Mateos E, Mejias R, Simmers JL, Mi R, Park JS, Ying S, Hoke A, Lee SJ, Cohn RD. Denervation atrophy is independent from Akt and mTOR activation and is not rescued by myostatin inhibition. Dis Model Mech 7: 471-481, 2014.
28. Matsakas A, Macharia R, Otto A, Elashry MI, Mouisel E, Romanello V, Sartori R, Amthor H, Sandri M, Narkar V, Patel K. Exercise training attenuates the hypermuscular phenotype and restores skeletal muscle function in the myostatin null mouse. Exp Physiol 97: 125-140, 2012.
29. Matsakas A, Mouisel E, Amthor H, Patel K. Myostatin knockout mice increase oxidative muscle phenotype as an adaptive response to exercise. J Muscle Res Cell Motil 31: 111-125, 2010.
30. McPherron AC, Lee SJ. Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94: 12457-12461, 1997.
31. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-β superfamily member. Nature 387: 83-90, 1997.
32. McPherron AC. Metabolic functions of myostatin and GDF11. Immunol Endocr Metab Agents Med Chem 10: 217-231, 2010.
33. McPherron AC, Guo T, Wang Q, Portas J. Soluble activin receptor type IIB treatment does not cause fat loss in mice with diet-induced obesity. Diabetes Obes Metab 14: 279-282, 2012.
34. Mendias CL, Marcin JE, Calerdon DR, Faulkner JA. Contractile properties of EDL and soleus muscles of myostatin-deficient mice. J Appl Physiol 101: 898-905, 2006.
35. Merkulova T, Dehaupas M, Nevers MC, Creminon C, Alameddine H, Keller A. Differential modulation of alpha, beta and gamma enolase isoforms in regenerating mouse skeletal muscle. Eur J Biochem 267: 3735-3743, 2000.
36. Morine KJ, Bish LT, Selsby JT, Gazzara JA, Pendrak K, Sleeper MM, Barton ER, Lee SJ, Sweeney HL. Activin IIB receptor blockade attenuates dystrophic pathology in a mouse model of Duchenne muscular dystrophy. Muscle Nerve 42: 722-730, 2010.
37. Mosher DS, Quignon P, Bustamante CD, Sutter NB, Mellersh CS, Parker HG, Ostrander EA. A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs. PLoS Genet 3: e79, 2007.
38. Murphy KT, Koopman R, Naim T, Léger B, Trieu J, Ibebunjo C, Lynch GS. Antibody-directed myostatin inhibition in 21-mo-old mice reveals novel roles for myostatin signaling in skeletal muscle structure and function. FASEB J 24: 4433-4442, 2010.
39. Ploquin C, Chabi B, Fouret G, Vernus B, Feillet-Coudray C, Coudray C, Bonnieu A, Ramonatxo C. Lack of myostatin alters intermyofibrillar mitochondria activity, unbalances redox status, and impairs tolerance to chronic repetitive contractions in muscle. Am J Physiol Endocrinol Metab 302: E1000-E1008, 2012.
40. Qaisar R, Renaud G, Morine K, Barton ER, Sweeney HL, Larsson L. Is functional hypertrophy and specific force coupled with the addition of myonuclei at the single muscle fiber level? FASEB J 26: 1077-1085, 2012.
41. Rahimov F, King OD, Warsing LC, Powell RE, Emerson CP Jr, Kunkel LM, Wagner KR. Gene expression profiling of skeletal muscles treated with a soluble activin type IIB receptor. Physiol Genomics 43: 398-407, 2011.
42. Savage KJ, McPherron AC. Endurance exercise training in myostatin null mice. Muscle Nerve 42: 355-362, 2010.
43. Schuler M, Ali F, Chambon C, Duteil D, Bornert JM, Tardivel A, Desvergne B, Wahli W, Chambon P, Metzger D. PGC1 expression is controlled in skeletal muscles by PPARα, whose ablation results in fiber-type switching, obesity, and type 2 diabetes. Cell Metab 4: 407-414, 2006.
44. Shan T, Liang X, Bi P, Kuang S. Myostatin knockout drives browning of white adipose tissue through activating the AMPK-PGC1-Fndc5 pathway in muscle. FASEB J 27: 1981-1989, 2013.
45. Wagner KD, Wagner N. Peroxisome proliferator-activated receptor beta/ delta (PPARβ/δ) acts as regulator of metabolism linked to multiple cellular functions. Pharmacol Ther 125: 423-435, 2010.
46. Weber JM. Metabolic fuels: regulating fluxes to select mix. J Exp Biol 214: 286-294, 2011.
47. Yadav H, Quijano C, Kamaraju AK, Gavrilova O, Malek R, Chen W, Zerfas P, Zhigang D, Wright EC, Stuelten C, Sun P, Lonning S, Skarulis M, Sumner AE, Finkel T, Rane SG. Protection from obesity and diabetes by blockade of TGF-β/Smad3 signaling. Cell Metab 14: 67-79, 2011.
48. 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.
49. Zhou X, Wang JL, Lu J, Song Y, Kwak KS, Jiao Q, Rosenfeld R, Chen Q, Boone T, Simonet WS, Lacey DL, Goldberg AL, Han HQ. Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 142: 531-543, 2010.