Health  Vol.9 No.5 , May 2017
Changes in Myofibrillar and Mitochondrial Compartments during Increased Activity: Dependance from Oxidative Capacity of Muscle
Striated muscle tissue contains fibers with high oxidative capacity (heart muscle), higher oxidative capacity (type I and IIA fibers of skeletal muscle) and low oxidative capacity (type IIB/X fibers of skeletal muscle). Muscle fibers with higher oxidative capacity contain large mitochondria tightly packed with cristae as well as small forms of mitochondria containing relatively few cristae. The intensive development of the mitochondrial apparatus in the post-activity period reflects the adaptive processes, which is intended to supply the increased energy requirements of muscle fibers with higher oxidative capacity. Muscle fibers with low oxidative capacity contain significantly less mitochondria than fibers with higher capacity. It is typical to type IIB fibers that after intensive muscle activity there are damaged myofibrils in a relatively small area, some myofibrils are twisted and lose the connection with the neighboring structures. It is still not fully known how skeletal muscles with different oxidative capacity respond to an increased functional activity and what differences exist in these fibers between oxidative capacity and function of myofibrils. The aim of the present short review was to compare structural-functional changes in mitochondrial and myofibrillar compartments of heart and skeletal muscle fibers with different oxidative capacity and the effect of increased functional activity on the interaction of these compartments.
Cite this paper: Seene, T. , Kaasik, P. and Seppet, E. (2017) Changes in Myofibrillar and Mitochondrial Compartments during Increased Activity: Dependance from Oxidative Capacity of Muscle. Health, 9, 779-798. doi: 10.4236/health.2017.95056.

[1]   Seppet, E.K., Käämbre, T., Sikk, P., Tiivel, T., Vija, H., Tonkonogi, M., Sahlin, K., Kay, L., Appaix, F., Braun, U., Eimre, M. and Saks, V.A. (2001) Functional Complexes of Mitochondria with Ca, MgATPases of Myofibrils and Sarcoplasmic Reticulum in Muscle Cells. Biochimica et Biophysica Acta, 1504, 379-395.

[2]   Saks, V.A., Kuznetsov, A.V., Vendelin, M., Guerrero, K., Kay, L. and Seppet, E.K. (2004) Functional Coupling as a Basic Mechansim of Feedback Regulation of Cardiac Energy Metabolism. Molecular and Cellular Biochemistry, 256, 185-199.

[3]   Vendelin, M., Béraud, N., Guerrero, K., Andrienko, T., Kuznetsov, A.V., Olivares, J., Kay, L. and Saks, V.A. (2005) Mitochondrial Regular Arrangement in Muscle Cells: A “Crystal-Like” Pattern. American Journal of Physiology. Cell Physiology, 288, C757-C767.

[4]   Seppet, E.K., Eimre, M., Anmann, T., Seppet, E., Peet, N., Käämbre, T., Paju, K., Piirsoo, A., Kuznetsov, A.V., Vendelin, M., Gellerich, F.N., Zierz, S. and Saks, V.A. (2005) Intracellular Energetic Units in Healthy and Diseased Hearts. Experimental and Clinical Cardiology, 10, 173-183.

[5]   Dirks, A.J. and Leeuwenburgh, C. (2005) The Role of Apoptosis in Age-Related Skeletal Muscle Atrophy. Sports Medicine, 35, 473-483.

[6]   Saks, V., Kaambre, T., Sikk, P., Eimre, M., Orlova, E., Paju, K., Piirsoo, A., Appaix, F., Kay, L., Regitz-Zagrosek, V., Fleck, E. and Seppet, E. (2001) Intracellular Energetics Units in Red Muscle Cells. Biochemical Journal, 356, 643-657.

[7]   Aschenbach, W.G., Sakamoto, K. and Goodyear, L.J. (2004) 5’Adenosine Monophosphate-Activated Protein Kinase, Metabolism and Exercise. Sports Medicine, 34, 91-103.

[8]   Nader, G.A. (2006) Concurrent Strength and Endurance Training: From Molecules to Man. Medicine and Science in Sports and Exercise, 38, 1965-1970.

[9]   Abbiss, C.R. and Laursen, P.B. (2005) Models to Explain Fatigue during Prolonged Endurance Cycling. Sports Medicine, 35, 865-898.

[10]   Ratel, S., Duché, P. and Williams, C.A. (2006) Muscle Fatigue during High-Intensity Exercise in Children. Sports Medicine, 36, 1031-1065.

[11]   Russ, D.W. and Kent-Braun, J.A. (2004) Is Skeletal Muscle Oxidative Capacity Decreased in Old Age? Sports Medicine, 34, 221-229.

[12]   Harris, B.A. (2005) The Influence of Endurance and Resistance Exercise on Muscle Capillarization in the Elderly: A Review. Acta Physiologica Scandinavica, 185, 89-97.

[13]   Seene, T., Kaasik, P. and Umnova, M. (2009) Structural Rearrangements in Contractile Apparatus and Resulting Skeletal Muscle Remodelling: Effect of Exercise Training. Journal of Sports Medicine and Physical Fitness, 49, 410-423.

[14]   Seene, T., Alev, K., Kaasik, P. and Pehme, A. (2007) Changes in Fast-Twitch Muscle Oxidative Capacity and Myosin Isoforms Modulation during Endurance Training. Journal of Sports Medicine and Physical Fitness, 47, 124-132.

[15]   Magaudda, L., Di Mauro, D., Trimarchi, F. and Anastasi, G. (2004) Effects of Physical Exercise on Skeletal Muscle Fiber: Ultrastructural and Molecular Aspects. Basic Applied Myology, 14, 17-21.

[16]   Seene, T., Kaasik, P., Alev, K., Pehme, A. and Riso, E.M. (2004) Composition and Turnover of Contractile Proteins in Volume-Overtrained Skeletal Muscle. International Journal of Sports Medicine, 25, 438-445.

[17]   Seene, T., Alev, K., Kaasik, P., Pehme, A. and Parring, A.M. (2005) Endurance Training: Volume-Dependent Adaptational Changes in Myosin. International Journal of Sports Medicine, 26, 815-821.

[18]   Folland, J.P. and Williams, A.G. (2007) The Adaptations to Strength Training: Morphological and Neurological Contributions to Increased Strength. Sports Medicine, 37, 145-168.

[19]   Andersen, J.L. and Aagaard, P. (2000) Myosin Heavy Chain IIX Overshoot in Human Skeletal Muscle. Muscle & Nerve, 23, 1095-1104.<1095::AID-MUS13>3.0.CO;2-O

[20]   Kendall, B. and Eston, R. (2002) Exercise-Induced Muscle Damage and the Potential Protective Role of Estrogen. Sports Medicine, 32, 103-123.

[21]   Kibler, W.B. and Chandler, T.J. (1998) Musculoskeletal and Orthopedic Considerations. In: Kreider, R.B., Fry, A.C. and O’Toole, M.L., Eds., Overtraining in Sport, Human Kinetics, Champaign, IL, 169-190.

[22]   Fridén, J., Leiber, R.L. and Thornell, L.E. (1991) Subtle Indications of Muscle Damage Following Eccentric Contractions. Acta Physiologica Scandinavica, 142, 523-524.

[23]   Lehmann, M., Foster, C., Netzer, N., Lormes, W., Steinacker, J.M., Liu, Y., Opitz-Gress, A. and Gastmann, U. (1998) Physiological Responses to Short- and Long-Term Overtraining In Endurance Athletes. In: Kreider, R., Fry, A. and O’Toole, M., Eds., Overtraining in Sport, Human Kinetics, Champaign, IL, 19-46.

[24]   Sjöström, M., Johansson, C. and Lorentzon, R. (1988) Muscle Pathomorphology in m. Quadericeps of Marathon runners. Early Signs of Strain Disease or Functional Adaptation? Acta Physiologica Scandinavica, 132, 537-541.

[25]   Umnova, M. and Seene, T. (1991) The Effect of Increased Functional Load on the Activation of Satellite Cells in the Skeletal Muscle of Adult Rats. International Journal of Sports Medicine, 12, 501-504.

[26]   Seene, T. and Umnova, M. (1992) Relations between the Changes in the Turnover Rate of Contractile Proteins, Activation of Satellite Cells and Ultra-Structural Response of Neuromuscular Junctions in the Fast-Oxidative-Glucolytic Muscle Fibres in Endurance Trained Rats. Basic Applied Myology, 2, 39-46.

[27]   Dauber, W., Voight, T. and Heini, A. (1999) Junctions between Subsynaptic Folds and Rough Sarcoplasmic Reticulum of Muscle Fibers. Journal of Muscle Research & Cell Motility, 20, 697-701.

[28]   Dauber, W. and Meister, A. (1986) Ultrastructure of Junctional Folds of Motor End Plates in Extensor Digitorum Longus Muscle of Mice. Journal of Ultrastructure and Molecular Structure Research, 97, 158-164.

[29]   Dauber, W., Voight, T., Härtel, X. and Mayer, J. (2000) The T-Tubular Network and Its Triads in the Sole Plate Sarcoplasm of the Motor End-Plate of Mammals. Journal of Muscle Research & Cell Motility, 21, 443-449.

[30]   van Wessel, T., de Haan, A., van der Laarse, W.J. and Jaspers, R.T. (2010) The Muscle Fiber Type-Fiber Size Paradox: Hypertrophy or Oxidative Metabolism? European Journal of Applied Physiology, 110, 665-694.

[31]   Bekedam, M.A., van Beek-Harmsen, B.J., Boonstra, A., van Mechelen, W., Visser, F.C. and van der Laarse, W.J. (2003) Maximum Rate of Oxygen Consumption Related to Succinate Dehydrogenase Activity in Skeletal Muscle Fibres of Chronic Heart Failure Patients and Controls. Clinical Physiology and Functional Imaging, 23, 337-343.

[32]   Blomstrand, E., Rådegran, G. and Saltin, B. (1997) Maximum Rate of Oxygen Uptake by Human Skeletal Muscle in Relation to Maximal Activities of Enzymes in the Krebs Cycle. The Journal of Physiology, 501, 455-460.

[33]   Hoppeler, H. and Billeter, R. (1991) Conditions for Oxygen and Substrate Transport in Muscles in Exercising Mammals. The Journal of Experimenthal Biology, 160, 263-283.

[34]   Reichmann, H., Wasl, R., Simoneau, J.A. and Pette, D. (1991) Enzyme Activities of Fatty Acid Oxidation and the Respiratory Chain in Chronically Stimulated Fast-Twitch Muscle of the Rabbit. Pflügers Archiv: European Journal of Physiology, 418, 572-574.

[35]   Kayar, S.R. and Banchero, N. (1987) Volume Density and Distribution of Mitochondria in Myocardial Growth and Hypertrophy. Respiation Physiology, 70, 275- 286.

[36]   Rivero, J.L., Talmadge, R.J. and Edgerton, V.R. (1999) Interrelationships of Myofibrillar ATPase Activity and Metabolic Properties of Myosin Heavy Chain-Based Fibre Types in Rat Skeletal Muscle. Histochemistry and Cell Biology, 111, 277-287.

[37]   Bodine, S.C., Stitt, T.N., Gonzalez, M., Kline, W.O., Stover, G.L., Bauerlein, R., Zlotchenko, E., Scrimgeour, A., Lawrence, J.C., Glass, D.J. and Yancopoulos, G.D. (2001) Akt/mTOR Pathway Is a Crucial Regulator of Skeletal Muscle Hypertrophy and Can Prevent Muscle Atrophy in Vivo. Nature Cell Biology, 3, 1014-1019.

[38]   Stitt, T.N., Drujan, D., Clarke, B.A., Panaro, F., Timofeyva, Y., Kline, W.O., Gonzalez, M., Yancopoulos, G.D. and Glass, D.J. (2004) The IGF-1/PI3K/Akt Pathway Prevents Expression of Muscle Atrophy-Induced Ubiquitin Ligases by Inhibiting FOXO Transcription Factors. Molecular Cell, 14, 395-403.

[39]   Lee, S.J. and McPherron, A.C. (2001) Regulation of Myostatin Activity and Muscle Growth. Proceedings of the National Academy of Sciences of the United States of America, 98, 9306-93011.

[40]   Zimmers, T.A., Davies, M.V., Koniaris, L.G., Haynes, P., Esquela, A.F., Tomkinson, K.N., et al. (2002) Induction of Cachexia in Mice by Systemically Administered Myostatin. Science, 296, 1486-1488.

[41]   Hickson, R.C. and Rosenkoetter, M.A. (1981) Separate Turnover of Cytochrome c and Myoglobin in the Red Types of Skeletal Muscle. The American Journal of Physiology, 241, C140-C144.

[42]   Hood, D.A. (2009) Mechanisms of Exercise-Induced Mitochondrial Biogenesis in Skeletal Muscle. Applied Physiology, Nutrition, and Metabolism, 34, 465-472.

[43]   Ljubicic, V., Joseph, A.M., Saleem, A., Uquccioni, G., Collu-Marchese, M., Lai, R.Y., Nquyen, L.M. and Hood, D.A. (2010) Transcriptional and Post-Transcriptional Regulation of Mitochondrial Biogenesis in Skeletal Muscle: Effects of Exercise and Aging. Biochimica et Biophysica Acta, 1800, 223-234.

[44]   Stepto, N.K., Martin, D.T., Fallon, K.E. and Hawley, J.A. (2001) Metabolic Demands of Intense Aerobic Interval Training in Competitive Cyclists. Medicine and Science in Sports and Exercise, 33, 303-310.

[45]   Yeo, W.K., Paton, C.D., Garnham, A.P., Burke, L.M., Carey, A.L. and Hawley, J.A. (2008) Skeletal Muscle Adaptation and Performance Responses to Once a Day versus Twice Every Second Day Endurance Training Regimens. Journal of Applied Physiology, 105, 1462-1470.

[46]   Laursen, P.B. and Jenkins, D.G. (2002) The Scientific Basis for High-Intensity Interval Training: Optimising Training Programmes and Maximising Performance in Highly Trained Endurance Athletes. Sports Medicine, 32, 53-73.

[47]   Iaia, F.M., Thomassen, M., Kolding, H., Gunnarsson, T., Wendell, J., Rostgaard, T., Nordsborg, N., Krustrup, P., Nybo, L., Hellsten, Y. and Bangsbo, J. (2008) Reduced Volume but Increased Training Intensity Elevates Muscle Na+-K+ Pump α1-Subunit and NHE1 Expression as Well as Short-Term Work Capacity in Humans. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 294, R966-R974.

[48]   Iaia, F.M., Hellsten, Y., Nielsen, J.J., Fernström, M., Sahlin, K. and Bangsbo, J. (2009) Four Weeks of Speed Endurance Training Reduces Energy Expenditure during Exercise and Maintains Muscle Oxidative Capacity Despite a Reduction in Training Volume. Journal of Applied Physiology, 106, 73-80.

[49]   Winder, W.W. and Hardie, D.G. (1996) Inactivation of Acetyl-CoA Carboxylase and Activation of AMP-Activated Protein Kinase in Muscle during Exercise. The American Journal of Physiology, 270, E299-E304.

[50]   Hardie, D.G. and Sakamoto, K. (2006) AMPK: A Key Sensor of Fuel and Energy Status in Skeletal Muscle. Physiology, 21, 48-60.

[51]   McGee, S.L., Kristy, J., Mustard, D., Hardie, D.G. and Baar, K. (2008) Normal Hypertrophy Accompanied by Phosphoryation and Activation of AMP-Activated Protein Kinase α1 following Overload in LKB1 Knockout Mice. The Journals of Physiology, 586, 1731-1741.

[52]   Luquet, S., Lopez-Soriano, J., Holst, D., Fredenrich, A., Melki, J., Rassoulzadegan, M. and Grimaldi, P. (2003) Peroxisome Proliferator-Activated Receptor Delta Controls Muscle Development and Oxidative Capability. FASEB Journal, 17, 2299-2301.

[53]   Wang, Y.X., Zhang, C.L., Yu, R.T., Cho, H.K., Nelson, M.C., Bayuga-Ocampo, C.R., Ham, J., Kang, H. and Evans, R.M. (2004) Regulation of Muscle Fibre Type and Running Endurance by PPARδ. PLoS Biology, 2, e294.

[54]   Carraro, F., Stuart, C.A., Hartl, W.H., Rosenblatt, J. and Wolfe, R.R. (1990) Effect of Exercise and Recovery on Muscle Protein Synthesis in Human Subjects. The American Journal of Physiology, 259, E470-E476.

[55]   Alev, K., Kaasik, P., Pehme, A., Aru, M., Parring, A.-M., Elart, A. and Seene, T. (2009) Physiological Role of Myosin Light and Heavy Chain Isoforms in Fast- and Slow-Twitch Muscles: Effect of Exercise. Biology of Sport, 26, 215-234.

[56]   Seene, T., Kaasik, P. and Alev, K. (2011) Muscle Protein Turnover in Endurance Training: A Review. International Journal of Sports Medicine, 32, 905-911.

[57]   Baldwin, K.M. and Haddad, F. (2001) Invited Review: Effect of Different Activity and Inactivity Paradigms on Myosin Heavy Chain Gene Expression in Studied Muscle. Journal of Applied Physiology, 90, 345-357.

[58]   Hayashibara, T. and Miyanishi, T. (1994) Binding of the Amino-Terminal Region of Myosin Alkali 1 Light Chain to Actin and Its Effect on Actin-Myosin Interaction. Biochemistry, 33, 12821-12827.

[59]   Green, H.J., Reichmann, H. and Pette, D. (1983) Fibre Type Specific Transformations in the Enzyme Activity Pattern of Rat Vastus Lateralis Muscle by Prolonged Endurance Training. Pflügers Archiv: European Journal of Physiology, 399, 216-222.

[60]   van der Vusse, G.J., Glatz, J.F., Stam, H.C. and Reneman, R.S. (1992) Fatty Acid Homeostasis in the Normoxic and Ischemic Heart. Physiological Reviews, 72, 881-940.

[61]   Matsakas, A., Macharia, R., Otto, A., Elashry, M.I., Mouisel, E., Romanello, V., Sartori, R., Amthor, H., Sandri, M., Narkar, V. and Patel, K. (2012) Exercise Training Attenuates the Hypermuscular Phenotype and Restores Skeletalmuscle function in the myostatin null mouse. Experimental Physiology, 97, 125-140.

[62]   Pierce, G.N., Sekhon, P.S., Meng, H.P. and Maddaford, T.G. (1989) Effects of Chronic Swimming Training on Cardiac Sarcolemmal Function and Composition. Journal of Applied Physiology, 66, 1715-1721.

[63]   Jin, H., Yang, R., Li, W., Lu, H., Ryan, A.M., Ogasawara, A.K., Van Peborgh, J. and Paoni, N.F. (2000) Effects of Exercise on Cardiac Function, Gene Expression and Apoptosis in Rats. American Journal of Physiology. Heart and Circulatory Physiology, 279, 2994-3002.

[64]   Wisloff, U., Loennechen, J.P., Falck, G., Beisvag, V., Currie, S., Smith, G. and Ellingsen, O. (2001) Increased Conractility and Calcium Sensitivity in Cardiac Myocytes Isolated from Endurance Trained Rats. Cardiovascular Research, 50, 495-508.

[65]   Diffee, G.M., Seversen, E.A., Stein, T.D. and Johnson, J.A. (2003) Microarray Expression Analysis of Effects of Exercise Training: Increase in Atrial MLC-1 in Rat Ventricles. American Journal of Physiology. Heart and Circulatory Physiology, 284, H830-H837.

[66]   Tate, C.A., Helgason, T., Hyek, M.F., McBride, R.P., Chen, M., Richardson, M.A. and Taffet, G.E. (1996) SERCA2a and Mitochondrial Cytochrome Oxidase Are Increased in Hearts of Exercise-Trained Old Rats. American Journal of Physiology, 271, 68-72.

[67]   Nuhr, M., Crevenna, R., Gohlsch, B., Bittner, C., Pleiner, J., Wiesinger, G., Fialka- Moser, V., Quittan, M. and Pette, D. (2003) Functional and Biochemical Properties of Chronically Stimulated Human Skeletal Muscle. European Journal of Applied Physiology, 89, 202-208.

[68]   Holloszy, J.O. (1967) Biochemical Adaptations in Muscle. Effects of Exercise on Mitochondrial Oxygen Uptake and Respiratory Enzyme Activity in Skeletal Muscle. The Journal of Biological Chemistry, 242, 2278-2282.

[69]   Silva, L.A., Pinho, C.A., Scarabelot, K.S., Fraga, D.B., Volpato, A.M., Boeck, C.R., De Souza, C.T., Streck, E.L. and Pinho, R.A. (2009) Physical Exercise Increases Mitochondrial Function and Reduces Oxidative Damage in Skeletal Muscle. European Journal of Applied Physiology, 105, 861-867.

[70]   Spina, R.J., Chi, M.M., Hopkins, M.G., Nemeth, P.M., Lowry, O.H. and Holloszy, J.O. (1996) Mitochondrial Enzymes Increase in Muscle in Response to 7 - 10 Days of Cycle Exercise. Journal of Applied Physiology, 80, 2250-2254.

[71]   Terblanche, S.E., Gohil, K., Packer, L., Henderson, S. and Brooks, G.A. (2001) The Effects of Endurance Training and Exhaustive Exercise on Mitochondrial Enzymes in Tissues of the Rat (Rattus norvegicus). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 128, 889-896.

[72]   Bozner, A. and Meessen, H. (1969) The Ultrastructure of the Myocardium of the Rat after Single and Repeated Swim Exercises. Virchows Archiv. B: Cell Pathology, 3, 248-269.

[73]   Anversa, P., Beghi, C., Levicky, V., McDonald, S.L. and Kikkawa, Y. (1982) Morphometry of Right Ventricular Hypertrophy Induced by Strenuous Exercise in Rat. The American Journal of Physiology, 243, 856-861.

[74]   Kayar, S.R., Conley, K.E., Claassen, H. and Hoppeler, H. (1986) Capillarity and Mitochondrial Distribution in Rat Myocardium Following Exercise Training. The Journal of Experimental Biology, 120, 189-199.

[75]   Paniagua, R., Vázques, J.J. and López-Moratalla, N. (1977) Effects of Physical Training on Rat Myocardium. An Enzymatic and Ultrastructural Morphometric Study. Revista Española de Fisiologia, 33, 273-281.

[76]   Noble, E.G., Moraska, A., Mazzeo, R.S., Roth, D.A., Olsson, M.C., Moore, R.L. and Fleshner, M. (1999) Differential Expression of Stress Proteins in Rat Myocardium after Free Wheel or Treadmill Run Training. Journal of Applied Physiology, 86, 1696-1701.

[77]   Gleyzer, N., Vercauteren, K. and Scarpulla, R.C. (2005) Control of Mitochondrial Transcription Specificity Factors (TFB1M and TFB2M) by Nuclear Respiratory Factors (NRF-1 and NFR-2) and PGC-1 Family Coactivators. Molecular and Cell Biology, 25, 1354-1366.

[78]   Scheller, K. and Sekeris, C.E. (2003) The Effects of Steroid Hormones on the Transcription of Genes Encoding Enzymes of Oxidative Phosphorylation. Experimental Physiology, 88, 129-140.

[79]   Akimoto, T., Pohnert, S.C., Li, P., Zhang, M., Gumbs, C., Rosenberg, P.B., Williams, R.S. and Yan, Z. (2005) Exercise Stimulates PGC-1α Transcription in Skeletal Muscle through Activation of the p38 MAPK Pathway.The Journal of Biological Chemistry, 280, 19587-19593.

[80]   Fan, M., Rhee, J., St-Pierre, J., Handschin, C., Puigserver, P., Lin, J., Jäeger, S., Erdjument-Bromage, H., Tempst, P. and Spiegelman, B.M. (2004) Suppression of Mitochondrial Respiration through Recruitment of p160 myb Binding Protein to PGC-1α: Modulation by p38 MAPK. Genes & Development, 18, 278-289.

[81]   Puigserver, P., Rhee, J., Lin, J.Wu, Z., Yoon, J.C., Zhang, C.Y., Krauss, S., Mootha, V.K., Lowell, B.B. and Spiegelman, B.M. (2001) Cytokine Stimulation of Enenrgy Expenditure through p38 MAP kInase Activation of PPARγ Coactivator-1. Molecular Cell, 8, 971-982.

[82]   Narkar, V.A., Downes, M., Yu, R.T., Embler, E., Wang, Y.X., Banayo, E., Mihaylova, M.M., Nelson, M.C., Zou, Y., Juguilon, H., Kang, H., Shaw, R.J. and Evans, R.M. (2008) AMPK and PPARδ Agonists Are Exercise Mimetics. Cell, 134, 405-415.

[83]   Menzies, K.J. and Hood, D.A. (2012) The Role of SirT1 in Muscle Mitochondrial Turnover. Mitochondrion, 12, 5-13.

[84]   Amat, R., Planavila, A., Chen, S.L., Iglesias, R., Giralt, M. and Villarroya, F. (2009) SIRT1 Controls the Transcription of the Peroxisome Proliferator-Activated Receptor-γ Coactivator-1α (PGC-1α) Gene in Skeletal Muscle through the PGC-1α Autoregulatory Loop and Interaction with MyoD. The Journal of Biological Chemistry, 284, 21872-21880.

[85]   Dumke, C.L., Davis, J.M., Murphy, E.A., Nieman, D.C., Carmichael, M.D., Quindry, J.C., Travis Triplett, N., Utter, A.C., Gross Gowin, S.J., Henson, D.A., McAnulty, S.R. and McAnulty, L.S. (2009) Successive Bouts of Cycling Stimulates Genes Associated with Mitocondrial Biogenesis. European Journal of Applied Physiology, 107, 419-427.

[86]   Pillai, V.B., Sundaresan, N.R., Jeevanandam, V. and Gupta, M.P. (2010) Mitochondrial SIRT3 and Heart Disease. Cardiovascular Research, 88, 250-256.

[87]   Gurd, B.J., Holloway, G.P., Yoshida, Y. and Bonen, A. (2011) In Mammalian Muscle, SIRT3 Is Present in Mitochondria and Not in the Nucleus; and SIRT3 Is Upregulated by Chronic Muscle Contraction in an Adenosine Monophosphate-Activated Protein Kinase-Independent Manner. Metabolism: Clinical and Experimental, 61, 733-741.

[88]   Wu, Z., Huang, X., Feng, Y., Handschin, C., Feng, Y., Gullicksen, P.S., Bare, O., Labow, M., Spiegelman, B. and Stevenson, S.C. (2006) Transducer of Regulated CREB-Binding Proteins (TORCs) Induce PGC-1α Transcription and Mitochondrial Biogenesis in Muscle Cells. Proceedings of National Academy of Sciences of the United States of America, 103, 14379-14384.

[89]   Matoba, S., Kang, J.G., Patino, W.D., Wragg, A., Boehm, M., Gavrilova, O., Hurley, P.J., Bunz, F. and Hwang, P.M. (2006) p53 Regulates Mitochondrial Respiration. Scince, 312, 1650-1653.

[90]   Achanta, G., Sasaki, R., Feng, L., Carew, J.S., Lu, W., Pelicano, H., Keating, M.J. and Huang, P. (2005) Novel Role of p53 in Maintaining Mitochondrial Genetic Stability through Interaction with DNA Pol Gamma. The EMBO Journal, 24, 3482-3492.

[91]   Park, J.-Y., Wang, P.-Y., Matsumoto, T., Sung, H.J., Ma, W., Choi, J.W., Anderson, S.A., Leary, S.C., Balaban, R.S., Kang, J.G. and Hwang, P.M. (2009) p53 Improves Aerobic Exercise Capacity and Augments Skeletal Muscle Mitochondrial DNA Content. Circulation Research, 105, 705-712.

[92]   Saleem, A., Adhietty, P.J. and Hood, D.A. (2009) Role of p53 in Mitochondrial Biogenesis and Apoptosis in Skeletal Muscles. Physiological Genomics, 37, 58-66.

[93]   Rodriguez.-Bies, E., Santa-Cruz, S., Fontan-Lozano, A., Amaro, J.P., Berral de la Rosa, F.J., Carrion, A.M., Navas, P. and Lopez-Lluch, G. (2010) Muscle Physiology Changes Induced by Every Other Day Feeding and Endurance in Mice: Effects on Physical Performance. PLoS ONE, 5, e13900.