Hibernating squirrel muscle activates the endurance exercise pathway despite prolonged immobilization

Experimental Neurology

Volumn 247, Issue , 2013, Pages 392-401

  Xu, Ran ^a,b   Andres Mateos, Eva ^a   Mejias, Rebeca ^a   MacDonald, Elizabeth M ^a   Leinwand, Leslie A ^c   Merriman, Dana K ^d   Fink, Rainer H A ^b   Cohn, Ronald D ^a,e,f  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WISCONSIN OSHKOSH   (United States)

^e HOSPITAL FOR SICK CHILDREN   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

Endurance exercise; Hibernation; Muscle atrophy; Muscle fiber type; Oxidative balance; Peroxisome proliferator activated receptor (PPAR ) coactivator 1 (PGC 1 )

Indexed keywords

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SIRTUIN; MITOCHONDRIAL PROTEIN; MUSCLE PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PPARGC1A PROTEIN, RAT; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDURANCE TRAINING; FEMALE; HIBERNATION; IMMOBILIZATION; IN VIVO STUDY; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE EXERCISE; MUSCLE FIBER CONTRACTION; MUSCLE METABOLISM; MUSCLE MITOCHONDRION; MUSCLE TWITCH; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN FUNCTION; SKELETAL MUSCLE; ANIMAL; ENDURANCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; SCIURIDAE; SIGNAL TRANSDUCTION; SLOW MUSCLE FIBER;

ANIMALS; GENE EXPRESSION REGULATION; HIBERNATION; IMMOBILIZATION; MITOCHONDRIAL PROTEINS; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE PROTEINS; MUSCLE, SKELETAL; OXIDATIVE STRESS; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL ENDURANCE; PPAR GAMMA; SCIURIDAE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84881375602     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.01.005     Document Type: Article

References (85)

1. Adams G.R., Cheng D.C., Haddad F., Baldwin K.M. Skeletal muscle hypertrophy in response to isometric, lengthening, and shortening training bouts of equivalent duration. J. Appl. Physiol. 2004, 96:1613-1618.
2. Adhihetty P.J., O'Leary M.F., Chabi B., Wicks K.L., Hood D.A. Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J. Appl. Physiol. 2007, 102:1143-1151.
3. Adhihetty P.J., Uguccioni G., Leick L., Hidalgo J., Pilegaard H., Hood D.A. The role of PGC-1alpha on mitochondrial function and apoptotic susceptibility in muscle. American Journal of Physiology. Cell Physiol. 2009, 297:C217-C225.
4. Akimoto T., Pohnert S.C., Li P., Zhang M., Gumbs C., Rosenberg P.B., Williams R.S., Yan Z. Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J. Biol. Chem. 2005, 280:19587-19593.
5. Allan M.E., Storey K.B. Expression of NF-kappaB and downstream antioxidant genes in skeletal muscle of hibernating ground squirrels, Spermophilus tridecemlineatus. Cell Biochem. Funct. 2012, 30:166-174.
6. Andres-Mateos E., Brinkmeier H., Burks T.N., Mejias R., Files D.C., Steinberger M., Soleimani A., Marx R., Simmers J.L., Lin B., Finanger Hedderick E., Marr T.G., Lin B.M., Hourde C., Leinwand L.A., Kuhl D., Foller M., Vogelsang S., Hernandez-Diaz I., Vaughan D.K., Alvarez de la Rosa D., Lang F., Cohn R.D. Activation of serum/glucocorticoid-induced kinase 1 (SGK1) is important to maintain skeletal muscle homeostasis and prevent atrophy. EMBO Mol. Med. 2013, 5(1):80-91.
7. Atherton P.J., Babraj J., Smith K., Singh J., Rennie M.J., Wackerhage H. Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J. 2005, 19:786-788.
8. Baar K., Esser K. Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am. J. Physiol. 1999, 276:C120-C127.
9. Baar K., Wende A.R., Jones T.E., Marison M., Nolte L.A., Chen M., Kelly D.P., Holloszy J.O. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J. 2002, 16:1879-1886.
10. Baar K., Song Z., Semenkovich C.F., Jones T.E., Han D.H., Nolte L.A., Ojuka E.O., Chen M., Holloszy J.O. Skeletal muscle overexpression of nuclear respiratory factor 1 increases glucose transport capacity. FASEB J. 2003, 17:1666-1673.
11. Bassel-Duby R., Olson E.N. Signaling pathways in skeletal muscle remodeling. Annu. Rev. Biochem. 2006, 75:19-37.
12. Berman S.B., Pineda F.J., Hardwick J.M. Mitochondrial fission and fusion dynamics: the long and short of it. Cell Death Differ 2008, 15:1147-1152.
13. Booth F. Effects of endurance exercise on cytochrome C turnover in skeletal muscle. Ann. N. Y. Acad. Sci. 1977, 301:431-439.
14. Boyer B.B., Barnes B.M., Lowell B.B., Grujic D. Differential regulation of uncoupling protein gene homologues in multiple tissues of hibernating ground squirrels. Am. J. Physiol. 1998, 275:R1232-R1238.
15. Calvo J.A., Daniels T.G., Wang X., Paul A., Lin J., Spiegelman B.M., Stevenson S.C., Rangwala S.M. Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake. J. Appl. Physiol. 2008, 104:1304-1312.
16. Canto C., Jiang L.Q., Deshmukh A.S., Mataki C., Coste A., Lagouge M., Zierath J.R., Auwerx J. Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab. 2010, 11:213-219.
17. Carey H.V., Andrews M.T., Martin S.L. Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol. Rev. 2003, 83:1153-1181.
18. Cartoni R., Leger B., Hock M.B., Praz M., Crettenand A., Pich S., Ziltener J.L., Luthi F., Deriaz O., Zorzano A., Gobelet C., Kralli A., Russell A.P. Mitofusins 1/2 and ERRalpha expression are increased in human skeletal muscle after physical exercise. J. Physiol. 2005, 567:349-358.
19. Chen H., Chan D.C. Emerging functions of mammalian mitochondrial fusion and fission. Hum. Mol. Genet. 2005, 14:R283-R289. (Spec No. 2).
20. D'Antona G., Ragni M., Cardile A., Tedesco L., Dossena M., Bruttini F., Caliaro F., Corsetti G., Bottinelli R., Carruba M.O., Valerio A., Nisoli E. Branched-chain amino acid supplementation promotes survival and supports cardiac and skeletal muscle mitochondrial biogenesis in middle-aged mice. Cell metabolism 2010, 12:362-372.
21. Daugaard J.R., Nielsen J.N., Kristiansen S., Andersen J.L., Hargreaves M., Richter E.A. Fiber type-specific expression of GLUT4 in human skeletal muscle: influence of exercise training. Diabetes 2000, 49:1092-1095.
22. Degens H., Alway S.E. Control of muscle size during disuse, disease, and aging. Int. J. Sports Med. 2006, 27:94-99.
23. Depre C., Shipley G.L., Chen W., Han Q., Doenst T., Moore M.L., Stepkowski S., Davies P.J., Taegtmeyer H. Unloaded heart in vivo replicates fetal gene expression of cardiac hypertrophy. Nat. Med. 1998, 4:1269-1275.
24. di Prampero P.E., Narici M.V. Muscles in microgravity: from fibres to human motion. J. Biomech. 2003, 36:403-412.
25. Ding H., Jiang N., Liu H., Liu X., Liu D., Zhao F., Wen L., Liu S., Ji L.L., Zhang Y. Response of mitochondrial fusion and fission protein gene expression to exercise in rat skeletal muscle. Biochim. Biophys. Acta 2010, 1800:250-256.
26. Eddy S.F., Morin P., Storey K.B. Cloning and expression of PPAR-gamma and PGC-1alpha from the hibernating ground squirrel, Spermophilus tridecemlineatus. Mol. Cell. Biochem. 2005, 269:175-182.
27. Fitts R.H., Riley D.R., Widrick J.J. Functional and structural adaptations of skeletal muscle to microgravity. J. Exp. Biol. 2001, 204:3201-3208.
28. Fluck M., Hoppeler H. Molecular basis of skeletal muscle plasticity-from gene to form and function. Rev. Physiol. Biochem. Pharmacol. 2003, 146:159-216.
29. Frezza C., Cipolat S., Scorrano L. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat. Protoc. 2007, 2:287-295.
30. Gerhart-Hines Z., Rodgers J.T., Bare O., Lerin C., Kim S.H., Mostoslavsky R., Alt F.W., Wu Z., Puigserver P. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J. 2007, 26:1913-1923.
31. Glass D.J. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat. Cell Biol. 2003, 5:87-90.
32. Greer E.L., Oskoui P.R., Banko M.R., Maniar J.M., Gygi M.P., Gygi S.P., Brunet A. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J. Biol. Chem. 2007, 282:30107-30119.
33. Gurd B.J., Perry C.G., Heigenhauser G.J., Spriet L.L., Bonen A. High-intensity interval training increases SIRT1 activity in human skeletal muscle. Appl. Physiol. Nutr. Metabol. 2010, 35:350-357.
34. Haddad F., Adams G.R. Selected contribution: acute cellular and molecular responses to resistance exercise. J. Appl. Physiol. 2002, 93:394-403.
35. Haigis M.C., Sinclair D.A. Mammalian sirtuins: biological insights and disease relevance. Annu. Rev.Pathol. 2010, 5:253-295.
36. Handschin C., Chin S., Li P., Liu F., Maratos-Flier E., Lebrasseur N.K., Yan Z., Spiegelman B.M. Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knock-out animals. J. Biol. Chem. 2007, 282:30014-30021.
37. Hockenbery D.M., Oltvai Z.N., Yin X.M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 1993, 75:241-251.
38. Holloszy J.O. Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J. Biol. Chem. 1967, 242:2278-2282.
39. Hornberger T.A., Hunter R.B., Kandarian S.C., Esser K.A. Regulation of translation factors during hindlimb unloading and denervation of skeletal muscle in rats. Am. J. Physiol. Cell Physiol. 2001, 281:C179-C187.
40. Hortobagyi T., Dempsey L., Fraser D., Zheng D., Hamilton G., Lambert J., Dohm L. Changes in muscle strength, muscle fibre size and myofibrillar gene expression after immobilization and retraining in humans. J. Physiol. 2000, 524(Pt 1):293-304.
41. Jackman R.W., Kandarian S.C. The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 2004, 287:C834-C843.
42. Jager S., Handschin C., St-Pierre J., Spiegelman B.M. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12017-12022.
43. Jiang N., Zhang G., Bo H., Qu J., Ma G., Cao D., Wen L., Liu S., Ji L.L., Zhang Y. Upregulation of uncoupling protein-3 in skeletal muscle during exercise: a potential antioxidant function. Free Radic. Biol. Med. 2009, 46:138-145.
44. Jorgensen S.B., Wojtaszewski J.F., Viollet B., Andreelli F., Birk J.B., Hellsten Y., Schjerling P., Vaulont S., Neufer P.D., Richter E.A., Pilegaard H. Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle. FASEB J. 2005, 19:1146-1148.
45. Kelly G. A review of the sirtuin system, its clinical implications, and the potential role of dietary activators like resveratrol: part 1. Altern. Med. Rev. 2010, 15:245-263.
46. Khassaf M., Child R.B., McArdle A., Brodie D.A., Esanu C., Jackson M.J. Time course of responses of human skeletal muscle to oxidative stress induced by nondamaging exercise. J. Appl. Physiol. 2001, 90:1031-1035.
47. Kong X., Wang R., Xue Y., Liu X., Zhang H., Chen Y., Fang F., Chang Y. Sirtuin 3, a new target of PGC-1alpha, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLoS One 2010, 5:e11707.
48. Koves T.R., Li P., An J., Akimoto T., Slentz D., Ilkayeva O., Dohm G.L., Yan Z., Newgard C.B., Muoio D.M. Peroxisome proliferator-activated receptor-gamma co-activator 1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J. Biol. Chem. 2005, 280:33588-33598.
49. Kowaltowski A.J., Fenton R.G., Fiskum G. Bcl-2 family proteins regulate mitochondrial reactive oxygen production and protect against oxidative stress. Free Radic. Biol. Med. 2004, 37:1845-1853.
50. Kubica N., Bolster D.R., Farrell P.A., Kimball S.R., Jefferson L.S. Resistance exercise increases muscle protein synthesis and translation of eukaryotic initiation factor 2Bepsilon mRNA in a mammalian target of rapamycin-dependent manner. J. Biol. Chem. 2005, 280:7570-7580.
51. Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., Messadeq N., Milne J., Lambert P., Elliott P., Geny B., Laakso M., Puigserver P., Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006, 127:1109-1122.
52. Lee K., Park J.Y., Yoo W., Gwag T., Lee J.W., Byun M.W., Choi I. Overcoming muscle atrophy in a hibernating mammal despite prolonged disuse in dormancy: proteomic and molecular assessment. J. Cell. Biochem. 2008, 104:642-656.
53. Leick L., Lyngby S.S., Wojtaszewski J.F., Pilegaard H. PGC-1alpha is required for training-induced prevention of age-associated decline in mitochondrial enzymes in mouse skeletal muscle. Exp. Gerontol. 2010, 45:336-342.
54. Lin J., Wu H., Tarr P.T., Zhang C.Y., Wu Z., Boss O., Michael L.F., Puigserver P., Isotani E., Olson E.N., Lowell B.B., Bassel-Duby R., Spiegelman B.M. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002, 418:797-801.
55. Lin J., Handschin C., Spiegelman B.M. Metabolic control through the PGC-1 family of transcription coactivators. Cell metabolism 2005, 1:361-370.
56. Minnaard R., Drost M.R., Wagenmakers A.J., van Kranenburg G.P., Kuipers H., Hesselink M.K. Skeletal Muscle wasting and contractile performance in septic rats. Muscle Nerve 2005, 31:339-348.
57. Momken I., Stevens L., Bergouignan A., Desplanches D., Rudwill F., Chery I., Zahariev A., Zahn S., Stein T.P., Sebedio J.L., Pujos-Guillot E., Falempin M., Simon C., Coxam V., Andrianjafiniony T., Gauquelin-Koch G., Picquet F., Blanc S. Resveratrol prevents the wasting disorders of mechanical unloading by acting as a physical exercise mimetic in the rat. FASEB J. 2011, 25:3646-3660.
58. Morin P., Storey K.B. Antioxidant defense in hibernation: cloning and expression of peroxiredoxins from hibernating ground squirrels, Spermophilus tridecemlineatus. Arch. Biochem. Biophys. 2007, 461:59-65.
59. Morin P., Ni Z., McMullen D.C., Storey K.B. Expression of Nrf2 and its downstream gene targets in hibernating 13-lined ground squirrels, Spermophilus tridecemlineatus. Mol. Cell. Biochem. 2008, 312:121-129.
60. Nader G.A. Concurrent strength and endurance training: from molecules to man. Med. Sci. Sports Exerc. 2006, 38:1965-1970.
61. Narici M.V., de Boer M.D. Disuse of the musculo-skeletal system in space and on earth. Eur. J. Appl. Physiol. 2011, 111:403-420.
62. Nicks D.K., Beneke W.M., Key R.M., Timson B.F. Muscle fibre size and number following immobilisation atrophy. J. Anat. 1989, 163:1-5.
63. Powers S.K., Jackson M.J. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol. Rev. 2008, 88:1243-1276.
64. Powers S.K., Wiggs M.P., Duarte J.A., Zergeroglu A.M., Demirel H.A. Mitochondrial signaling contributes to disuse muscle atrophy. American journal of physiology. Endocrinol. Metab. 2012, 303:E31-E39.
65. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92:829-839.
66. Ramachandran B., Yu G., Gulick T. Nuclear respiratory factor 1 controls myocyte enhancer factor 2A transcription to provide a mechanism for coordinate expression of respiratory chain subunits. J. Biol. Chem. 2008, 283:11935-11946.
67. Razeghi P., Myers T.J., Frazier O.H., Taegtmeyer H. Reverse remodeling of the failing human heart with mechanical unloading. Emerging concepts and unanswered questions. Cardiology 2002, 98:167-174.
68. Romanello V., Guadagnin E., Gomes L., Roder I., Sandri C., Petersen Y., Milan G., Masiero E., Del Piccolo P., Foretz M., Scorrano L., Rudolf R., Sandri M. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J. 2010, 29:1774-1785.
69. Rube D.A., van der Bliek A.M. Mitochondrial morphology is dynamic and varied. Mol. Cell. Biochem. 2004, 256-257:331-339.
70. Scarpulla R.C. Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 2002, 286:81-89.
71. Stevenson E.J., Giresi P.G., Koncarevic A., Kandarian S.C. Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J. Physiol. 2003, 551:33-48.
72. St-Pierre J., Lin J., Krauss S., Tarr P.T., Yang R., Newgard C.B., Spiegelman B.M. Bioenergetic analysis of peroxisome proliferator-activated receptor gamma coactivators 1alpha and 1beta (PGC-1alpha and PGC-1beta) in muscle cells. J. Biol. Chem. 2003, 278:26597-26603.
73. St-Pierre J., Drori S., Uldry M., Silvaggi J.M., Rhee J., Jager S., Handschin C., Zheng K., Lin J., Yang W., Simon D.K., Bachoo R., Spiegelman B.M. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006, 127:397-408.
74. Suwa M., Nakano H., Radak Z., Kumagai S. Endurance exercise increases the SIRT1 and peroxisome proliferator-activated receptor gamma coactivator-1alpha protein expressions in rat skeletal muscle. Metab. Clin. Exp. 2008, 57:986-998.
75. Thorlund J.B., Jakobsen O., Madsen T., Christensen P.A., Nedergaard A., Andersen J.L., Suetta C., Aagaard P. Changes in muscle strength and morphology after muscle unloading in Special Forces missions. Scand. J. Med. Sci. Sports 2011, 21:e56-e63.
76. Van Breukelen F., Martin S.L. Invited review: molecular adaptations in mammalian hibernators: unique adaptations or generalized responses?. J. Appl. Physiol. 2002, 92:2640-2647.
77. Vaughan D.K., Gruber A.R., Michalski M.L., Seidling J., Schlink S. Capture, care, and captive breeding of 13-lined ground squirrels, Spermophilus tridecemlineatus. Lab. Anim. (NY) 2006, 35:33-40.
78. Wagner K.R. Approaching a new age in Duchenne muscular dystrophy treatment. Neurotherapeutics 2008, 5:583-591.
79. Wang Y.X., Lee C.H., Tiep S., Yu R.T., Ham J., Kang H., Evans R.M. Peroxisome-proliferator-activated receptor delta activates fat metabolism to prevent obesity. Cell 2003, 113:159-170.
80. Wende A.R., Schaeffer P.J., Parker G.J., Zechner C., Han D.H., Chen M.M., Hancock C.R., Lehman J.J., Huss J.M., McClain D.A., Holloszy J.O., Kelly D.P. A role for the transcriptional coactivator PGC-1alpha in muscle refueling. J. Biol. Chem. 2007, 282:36642-36651.
81. Wenz T., Diaz F., Hernandez D., Moraes C.T. Endurance exercise is protective for mice with mitochondrial myopathy. J. Appl. Physiol. 2009, 106:1712-1719.
82. Wong T.S., Booth F.W. Skeletal muscle enlargement with weight-lifting exercise by rats. J. Appl. Physiol. 1988, 65:950-954.
83. Wright D.C., Han D.H., Garcia-Roves P.M., Geiger P.C., Jones T.E., Holloszy J.O. Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression. J. Biol. Chem. 2007, 282:194-199.
84. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
85. Yu M., Stepto N.K., Chibalin A.V., Fryer L.G., Carling D., Krook A., Hawley J.A., Zierath J.R. Metabolic and mitogenic signal transduction in human skeletal muscle after intense cycling exercise. J. Physiol. 2003, 546:327-335.