Mitochondrial functional specialization in glycolytic and oxidative muscle fibers: Tailoring the organelle for optimal function

American Journal of Physiology - Cell Physiology

Volumn 302, Issue 4, 2012, Pages

  Picard, Martin ^a   Hepple, Russell T ^a,b   Burelle, Yan ^c  

^a MCGILL UNIVERSITY   (Canada)

^b ROYAL VICTORIA HOSPITAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Calcium retention capacity; Mitochondria; Oxidative capacity; Reactive oxygen species

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; CALCIUM ION; CYTOCHROME C OXIDASE; HYDROGEN PEROXIDE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOCHONDRIAL PROTEIN; PROTON; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE);

ANTIOXIDANT ACTIVITY; BIOGENESIS; CALCIUM CELL LEVEL; CELL DEATH; CELL ENERGY; CELL ORGANELLE; CELL STRUCTURE; GLYCOLYSIS; GLYCOLYTIC MUSCLE FIBER; HUMAN; INTRACELLULAR SIGNALING; MEMBRANE PERMEABILITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MITOPHAGY; MUSCLE CELL; MUSCLE FIBER CONTRACTION; MUSCLE FUNCTION; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE COUPLING; OXIDATIVE MUSCLE FIBER; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVIEW; SKELETAL MUSCLE;

ANIMALS; CALCIUM; CELL DEATH; GLYCOLYSIS; HUMANS; MICE; MITOCHONDRIA, MUSCLE; MUSCLE CONTRACTION; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; RATS; REACTIVE OXYGEN SPECIES;

EID: 84856579589     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00368.2011     Document Type: Review

References (122)

1. Adhihetty PJ, Ljubicic V, Menzies KJ, Hood DA. Differential susceptibility of subsarcolemmal and intermyofibrillar mitochondria to apoptotic stimuli. Am J Physiol Cell Physiol 289: C994-C1001, 2005.
2. Anderson EJ, Neufer PD. Type II skeletal myofibers possess unique properties that potentiate mitochondrial H2O2 generation. Am J Physiol Cell Physiol 290: C844-C851, 2006.
3. Andrews JL, Zhang X, McCarthy JJ, McDearmon EL, Hornberger TA, Russell B, Campbell KS, Arbogast S, Reid MB, Walker JR, Hogenesch JB, Takahashi JS, Esser KA. CLOCK and BMAL1 regulate MyoD and are necessary for maintenance of skeletal muscle phenotype and function. Proc Natl Acad Sci USA 107: 19090-19095, 2010.
4. Arany Z. PGC-1 coactivators and skeletal muscle adaptations in health and disease. Curr Opin Genet Dev 18: 426-434, 2008.
5. Armstrong RB, Phelps RO. Muscle fiber type composition of the rat hindlimb. Am J Anat 171: 259-272, 1984.
6. Bahi L, Garnier A, Fortin D, Serrurier B, Veksler V, Bigard AX, Ventura-Clapier R. Differential effects of thyroid hormones on energy metabolism of rat slow-and fast-twitch muscles. J Cell Physiol 203: 589-598, 2005.
7. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell 120: 483-495, 2005.
8. Balaban RS. Modeling mitochondrial function. Am J Physiol Cell Physiol 291: C1107-C1113, 2006.
9. Barrès R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, Krook A, Zierath JR. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 10: 189-198, 2009.
10. Baylor SM, Hollingworth S. Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol 551: 125-138, 2003.
11. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79: 1127-1155, 1999.
12. 2+-mediated cell death by the transcriptional coactivator PGC-1alpha. Cell Death Differ 13: 586-596, 2006.
13. Bock C, Tomazou EM, Brinkman AB, Müller F, Simmer F, Gu H, Jäger N, Gnirke A, Stunnenberg HG, Meissner A. Quantitative comparison of genome-wide DNA methylation mapping technologies. Nat Biotechnol 28: 1106-1114, 2010.
14. Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL, Parker N. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med 37: 755-767, 2004.
15. Brand MD, Chien LF, Ainscow EK, Rolfe DF, Porter RK. The causes and functions of mitochondrial proton leak. Biochim Biophys Acta 1187: 132-139, 1994.
16. Braun U, Paju K, Eimre M, Seppet E, Orlova E, Kadaja L, Trumbeckaite S, Gellerich FN, Zierz S, Jockusch H, Seppet EK. Lack of dystrophin is associated with altered integration of the mitochondria and ATPases in slow-twitch muscle cells of MDX mice. Biochim Biophys Acta 1505: 258-270, 2001.
17. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287: C817-C833, 2004.
18. Burelle Y, Hochachka PW. Endurance training induces muscle-specific changes in mitochondrial function in skinned muscle fibers. J Appl Physiol 92: 2429-2438, 2002.
19. Burelle Y, Khairallah M, Ascah A, Allen BG, Deschepper CF, Petrof BJ, Rosiers Des C. Alterations in mitochondrial function as a harbinger of cardiomyopathy: lessons from the dystrophic heart. J Mol Cell Cardiol 48: 310-321, 2010.
20. Carroll S, Nicotera P, Pette D. Calcium transients in single fibers of low-frequency stimulated fast-twitch muscle of rat. Am J Physiol Cell Physiol 277: C1122-C1129, 1999.
21. Carroll SL, Klein MG, Schneider MF. Decay of calcium transients after electrical stimulation in rat fast-and slow-twitch skeletal muscle fibres. J Physiol 501: 573-588, 1997.
22. Chabi B, Ljubicic V, Menzies KJ, Huang JH, Saleem A, Hood DA. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 7: 2-12, 2008.
23. Chan RK, Austen WG, Ibrahim S, Ding GY, Verna N, Hechtman HB, Moore FD. Reperfusion injury to skeletal muscle affects primarily type II muscle fibers. J Surg Res 122: 54-60, 2004.
24. Colombini M. Regulation of the mitochondrial outer membrane channel, VDAC. J Bioenerg Biomembr 19: 309-320, 1987.
25. Crompton M, Virji S, Doyle V, Johnson N, Ward JM. The mitochondrial permeability transition pore. Biochem Soc Symp 66: 167-179, 1999.
26. Deng N, Zhang J, Zong C, Wang Y, Lu H, Yang P, Wang W, Young GW, Wang Y, Korge P, Lotz C, Doran P, Liem DA, Apweiler R, Weiss JN, Duan H, Ping P. Phosphoproteome analysis reveals regulatory sites in major pathways of cardiac mitochondria. Mol Cell Proteomics 10: M110.000117, 2011.
27. Di Lisa F, Bernardi P. Mitochondrial function as a determinant of recovery or death in cell response to injury. Mol Cell Biochem 184: 379-391, 1998.
28. Duchen MR, Verkhratsky A, Muallem S. Mitochondria and calcium in health and disease. Cell Calcium 44: 1-5, 2008.
29. Esterbauer H, Oberkofler H, Krempler F, Patsch W. Human peroxisome proliferator activated receptor gamma coactivator 1 (PPARGC1) gene: cDNA sequence, genomic organization, chromosomal localization, and tissue expression. Genomics 62: 98-102, 1999.
30. Ferreira R, Vitorino R, Alves RMP, Appell HJ, Powers SK, Duarte JA, Amado F. Subsarcolemmal and intermyofibrillar mitochondria proteome differences disclose functional specializations in skeletal muscle. Proteomics 10: 3142-3154, 2010.
31. Fryer MW, Stephenson DG. Total and sarcoplasmic reticulum calcium contents of skinned fibres from rat skeletal muscle. J Physiol 493: 357-370, 1996.
32. Gellerich FN, Khuchua ZA, Kuznetsov AV. Influence of the mitochondrial outer membrane and the binding of creatine kinase to the mitochondrial inner membrane on the compartmentation of adenine nucleotides in the intermembrane space of rat heart mitochondria. Biochim Biophys Acta 1140: 327-334, 1993.
33. Glancy B, Balaban RS. Protein composition and function of red and white skeletal muscle mitochondria. Am J Physiol Cell Physiol 300: C1280-C1290, 2011.
34. Glatz JFC, Schaap FG, Binas B, Bonen A, van der Vusse GJ, Luiken JJFP. Cytoplasmic fatty acid-binding protein facilitates fatty acid utilization by skeletal muscle. Acta Physiol Scand 178: 367-371, 2003.
35. Gnaiger E, Méndez G, Hand SC. High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proc Natl Acad Sci USA 97: 11080-11085, 2000.
36. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 305: 626-629, 2004.
37. Gustafsson R, Tata JR, Lindberg O, Ernster L. The relationship between the structure and activity of rat skeletal muscle mitochondria after thyroidectomy and thyroid hormone treatment. J Cell Biol 26: 555-578, 1965.
38. Handschin C, Spiegelman BM. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27: 728-735, 2006.
39. Hansford RG, Hogue BA, Mildaziene V. Dependence of H2O2 formation by rat heart mitochondria on substrate availability and donor age. J Bioenerg Biomembr 29: 89-95, 1997.
40. 2+trigger site. Arch Biochem Biophys 195: 460-467, 1979.
41. Hengartner MO. The biochemistry of apoptosis. Nature 407: 770-776, 2000.
42. Hochachka PW. Muscles as Molecular and Metabolic Machines. Boca Raton, FL: CRC, 1994.
43. Hood DA, Irrcher I, Ljubicic V, Joseph AM. Coordination of metabolic plasticity in skeletal muscle. J Exp Biol 209: 2265-2275, 2006.
44. Ichas F, Jouaville LS, Mazat JP. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89: 1145-1153, 1997.
45. Irwin W, Fontaine E, Agnolucci L, Penzo D, Betto R, Bortolotto S, Reggiani C, Salviati G, Bernardi P. Bupivacaine myotoxicity is mediated by mitochondria. J Biol Chem 277: 12221-12227, 2002.
46. Jackman MR, Willis WT. Characteristics of mitochondria isolated from type I and type IIb skeletal muscle. Am J Physiol Cell Physiol 270: C673-C678, 1996.
47. Jang YC, Lustgarten MS, Liu Y, Müller FL, Bhattacharya A, Liang H, Salmon AB, Brooks SV, Larkin L, Hayworth CR, Richardson A, Van Remmen H. Increased superoxide in vivo accelerates age-associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration. FASEB J 24: 1376-1390, 2010.
48. Jang YC, Remmen VH. The mitochondrial theory of aging: insight from transgenic and knockout mouse models. Exp Gerontol 44: 256-260, 2009.
49. Jouaville LS, Ichas F, Mazat JP. Modulation of cell calcium signals by mitochondria. Mol Cell Biochem 184: 371-376, 1998.
50. Kaasik A, Veksler V, Boehm E, Novotova M, Minajeva A, Ventura-Clapier R. Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ Res 89: 153-159, 2001.
51. Kaasik A, Veksler V, Boehm E, Novotova M, Ventura-Clapier R. From energy store to energy flux: a study in creatine kinase-deficient fast skeletal muscle. FASEB J 17: 708-710, 2003.
52. Kadenbach B. Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim Biophys Acta 1604: 77-94, 2003.
53. Kay L, Li Z, Mericskay M, Olivares J, Tranqui L, Fontaine E, Tiivel T, Sikk P, Kaambre T, Samuel JL, Rappaport L, Usson Y, Leverve X, Paulin D, Saks VA. Study of regulation of mitochondrial respiration in vivo. An analysis of influence of ADP diffusion and possible role of cytoskeleton. Biochim Biophys Acta 1322: 41-59, 1997.
54. Kim JS, He L, Lemasters JJ. Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 304: 463-470, 2003.
55. Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416: 15-18, 1997.
56. Kowaltowski AJ, Castilho RF, Vercesi AE. Mitochondrial permeability transition and oxidative stress. FEBS Lett 495: 12-15, 2001.
57. Kuznetsov AV, Tiivel T, Sikk P, Kaambre T, Kay L, Daneshrad Z, Rossi A, Kadaja L, Peet N, Seppet E, Saks VA. Striking differences between the kinetics of regulation of respiration by ADP in slow-twitch and fast-twitch muscles in vivo. Eur J Biochem 241: 909-915, 1996.
58. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 3: 965-976, 2008.
59. Kwong LK, Sohal RS. Substrate and site specificity of hydrogen peroxide generation in mouse mitochondria. Arch Biochem Biophys 350: 118-126, 1998.
60. Laterveer FD, Nicolay K, Gellerich FN. Experimental evidence for dynamic compartmentation of ADP at the mitochondrial periphery: coupling of mitochondrial adenylate kinase and mitochondrial hexokinase with oxidative phosphorylation under conditions mimicking the intracellular colloid osmotic pressure. Mol Cell Biochem 174: 43-51, 1997.
61. Leary SC, Lyons CN, Rosenberger AG, Ballantyne JS, Stillman J, Moyes CD. Fiber-type differences in muscle mitochondrial profiles. Am J Physiol Regul Integr Comp Physiol 285: R817-R826, 2003.
62. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418: 797-801, 2002.
63. Ling C, Poulsen P, Simonsson S, Rönn T, Holmkvist J, Almgren P, Hagert P, Nilsson E, Mabey AG, Nilsson P, Vaag A, Groop L. Genetic and epigenetic factors are associated with expression of respiratory chain component NDUFB6 in human skeletal muscle. J Clin Invest 117: 3427-3435, 2007.
64. 2+signaling. Int J Biochem Cell Biol 41: 1957-1971, 2009.
65. Lustgarten MS, Jang YC, Liu Y, Müller FL, Qi W, Steinhelper M, Brooks SV, Larkin L, Shimizu T, Shirasawa T, McManus LM, Bhattacharya A, Richardson A, Van Remmen H. Conditional knockout of Mn-SOD targeted to type IIB skeletal muscle fibers increases oxidative stress and is sufficient to alter aerobic exercise capacity. Am J Physiol Cell Physiol 297: C1520-C1532, 2009.
66. Mansouri A, Müller FL, Liu Y, Ng R, Faulkner J, Hamilton M, Richardson A, Huang TT, Epstein CJ, Van Remmen H. Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mech Ageing Dev 127: 298-306, 2006.
67. McMillan EM, Quadrilatero J. Differential apoptosis-related protein expression, mitochondrial properties, proteolytic enzyme activity, and DNA fragmentation between skeletal muscles. Am J Physiol Regul Integr Comp Physiol 300: R531-R543, 2011.
68. Meaney MJ, Ferguson-Smith AC. Epigenetic regulation of the neural transcriptome: the meaning of the marks. Nat Neurosci 13: 1313-1318, 2010.
69. Millay DP, Sargent MA, Osinska H, Baines CP, Barton ER, Vuagniaux G, Sweeney HL, Robbins J, Molkentin JD. Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat Med 14: 442-447, 2008.
70. Mogensen M, Sahlin K. Mitochondrial efficiency in rat skeletal muscle: influence of respiration rate, substrate and muscle type. Acta Physiol Scand 185: 229-236, 2005.
71. O'Connor RS, Steeds CM, Wiseman RW, Pavlath GK. Phosphocreatine as an energy source for actin cytoskeletal rearrangements during myoblast fusion. J Physiol 586: 2841-2853, 2008.
72. Ogata T, Yamasaki Y. Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers. Anat Rec 248: 214-223, 1997.
73. Palmer JW, Tandler B, Hoppel CL. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 252: 8731-8739, 1977.
74. Pande SV. On rate-controlling factors of long chain fatty acid oxidation. J Biol Chem 246: 5384-5390, 1971.
75. Pandorf CE, Haddad F, Wright C, Bodell PW, Baldwin KM. Differential epigenetic modifications of histones at the myosin heavy chain genes in fast and slow skeletal muscle fibers and in response to muscle unloading. Am J Physiol Cell Physiol 297: C6-C16, 2009.
76. Perry CGR, Kane DA, Lin CT, Kozy R, Cathey BL, Lark DS, Kane CL, Brophy PM, Gavin TP, Anderson EJ, Neufer PD. Inhibiting myosin-ATPase reveals a dynamic range of mitochondrial respiratory control in skeletal muscle. Biochem J 437: 215-222, 2011.
77. Philippi M, Sillau AH. Oxidative capacity distribution in skeletal muscle fibers of the rat. J Exp Biol 189: 1-11, 1994.
78. Phillips D, Aponte AM, Covian R, Balaban RS. Intrinsic protein kinase activity in mitochondrial oxidative phosphorylation complexes. Biochemistry 50: 2515-2529, 2011.
79. Picard M, Csukly K, Robillard ME, Godin R, Ascah A, Bourcier-Lucas C, Burelle Y. Resistance to Ca2_-induced opening of the permeability transition pore differs in mitochondria from glycolytic and oxidative muscles. Am J Physiol Regul Integr Comp Physiol 295: R659-R668, 2008.
80. Picard M, Godin R, Sinnreich M, Baril J, Bourbeau J, Perrault H, Taivassalo T, Burelle Y. The mitochondrial phenotype of peripheral muscle in chronic obstructive pulmonary disease: disuse or dysfunction? Am J Respir Crit Care Med 178: 1040-1047, 2008.
81. Picard M, Ritchie D, Wright KJ, Romestaing C, Thomas MM, Rowan SL, Taivassalo T, Hepple RT. Mitochondrial functional impairment with aging is exaggerated in isolated mitochondria compared with permeabilized myofibers. Aging Cell 9: 1032-1046, 2010.
82. Picard M, Ritchie D, Wright KJ, Thomas MM, Hepple RT. Alterations in intrinsic mitochondrial function with aging are fiber type-specific and do not explain differential atrophy between muscles. Aging Cell 6: e18317, 2011.
83. Picard M, Taivassalo T, Gouspillou G, Hepple RT. Mitochondria: isolation, structure and function. J Physiol 589: 4413-4421, 2011.
84. Piquereau J, Novotova M, Fortin D, Garnier A, Ventura-Clapier R, Veksler V, Joubert F. Postnatal development of mouse heart: formation of energetic microdomains. J Physiol 588: 2443-2454, 2010.
85. Ponsot E, Zoll J, N'guessan B, Ribera F, Lampert E, Richard R, Veksler V, Ventura-Clapier R, Mettauer B. Mitochondrial tissue specificity of substrates utilization in rat cardiac and skeletal muscles. J Cell Physiol 203: 479-486, 2005.
86. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol 28: 1057-1068, 2010.
87. Qin W, Khuchua Z, Boero J, Payne RM, Strauss AW. Oxidative myocytes of heart and skeletal muscle express abundant sarcomeric mitochondrial creatine kinase. Histochem J 31: 357-365, 1999.
88. Rangwala SM, Wang X, Calvo JA, Lindsley L, Zhang Y, Deyneko G, Beaulieu V, Gao J, Turner G, Markovits J. Estrogen-related receptor gamma is a key regulator of muscle mitochondrial activity and oxidative capacity. J Biol Chem 285: 22619-22629, 2010.
89. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447: 425-432, 2007.
90. Ristow M, Zarse K, Oberbach A, Klöting N, Birringer M, Kiehntopf M, Stumvoll M, Kahn CR, Bluher M. Antioxidants prevent healthpromoting effects of physical exercise in humans. Proc Natl Acad Sci USA 106: 8665-8670, 2009.
91. Rizzuto R, Marchi S, Bonora M, Aguiari P, Bononi A, De Stefani D, Giorgi C, Leo S, Rimessi A, Siviero R, Zecchini E, Pinton P. Ca(2+) transfer from the ER to mitochondria: when, how and why. Biochim Biophys Acta 1787: 1342-1351, 2009.
92. 2+: molecular determinants and functional consequences. Physiol Rev 86: 369-408, 2006.
93. Saks V, Guzun R, Timohhina N, Tepp K, Varikmaa M, Monge C, Beraud N, Kaambre T, Kuznetsov A, Kadaja L, Eimre M, Seppet E. Structure-function relationships in feedback regulation of energy fluxes in vivo in health and disease: mitochondrial interactosome. Biochim Biophys Acta 1797: 678-697, 2010.
94. Saks V. The phosphocreatine-creatine kinase system helps to shape muscle cells and keep them healthy and alive. J Physiol 586: 2817-2818, 2008.
95. Saks VA, Kaambre T, Sikk P, Eimre M, Orlova E, Paju K, Piirsoo A, Appaix F, Kay L, Regitz-Zagrosek V, Fleck E, Seppet E. Intracellular energetic units in red muscle cells. Biochem J 356: 643-657, 2001.
96. Saks VA, Khuchua ZA, Vasilyeva EV, Belikova O, Yu Kuznetsov AV. Metabolic compartmentation and substrate channelling in muscle cells. Role of coupled creatine kinases in in vivo regulation of cellular respiration-a synthesis. Mol Cell Biochem 133-134: 155-192, 1994.
97. Saks VA, Kuznetsov AV, Khuchua ZA, Vasilyeva EV, Belikova JO, Kesvatera T, Tiivel T. Control of cellular respiration in vivo by mitochondrial outer membrane and by creatine kinase. A new speculative hypothesis: possible involvement of mitochondrial-cytoskeleton interactions. J Mol Cell Cardiol 27: 625-645, 1995.
98. Saks VA, Veksler VI, Kuznetsov AV, Kay L, Sikk P, Tiivel T, Tranqui L, Olivares J, Winkler K, Wiedemann F, Kunz WS. Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem 184: 81-100, 1998.
99. Santos dos RA, Giannocco G, Nunes MT. Thyroid hormone stimulates myoglobin expression in soleus and extensorum digitalis longus muscles of rats: concomitant alterations in the activities of Krebs cycle oxidative enzymes. Thyroid 11: 545-550, 2001.
100. Scarpulla RC. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta 1813: 1269-1278, 2010.
101. Schwerzmann K, Hoppeler H, Kayar SR, Weibel ER. Oxidative capacity of muscle and mitochondria: correlation of physiological, biochemical, and morphometric characteristics. Proc Natl Acad Sci USA 86: 1583-1587, 1989.
102. Seppet EK, Kaambre T, Sikk P, Tiivel T, Vija H, Tonkonogi M, Sahlin K, Kay L, Appaix F, Braun U, Eimre M, Saks VA. Functional complexes of mitochondria with Ca,MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells. Biochim Biophys Acta 1504: 379-395, 2001.
103. Servais S, Couturier K, Koubi H, Rouanet JL, Desplanches D, Sornay-Mayet MH, Sempore B, Lavoie JM, Favier R. Effect of voluntary exercise on H2O2 release by subsarcolemmal and intermyofibrillar mitochondria. Free Radic Biol Med 35: 24-32, 2003.
104. Shock LS, Thakkar PV, Peterson EJ, Moran RG, Taylor SM. DNA methyltransferase 1, cytosine methylation, and cytosine hydroxymethylation in mammalian mitochondria. Proc Natl Acad Sci USA 108: 3630-3635, 2011.
105. Sousa-Victor P, Muñoz-Cánoves P, Perdiguero E. Regulation of skeletal muscle stem cells through epigenetic mechanisms. Toxicol Mech Methods 21: 334-342, 2011.
106. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jäger S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127: 397-408, 2006.
107. Starkov AA, Fiskum G. Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state. J Neurochem 86: 1101-1107, 2003.
108. Strobel NA, Peake JM, Matsumoto A, Marsh SA, Coombes JS, Wadley GD. Antioxidant supplementation reduces skeletal muscle mitochondrial biogenesis. Med Sci Sports Exerc 43: 1017-1024, 2011.
109. Treberg JR, Quinlan CL, Brand MD. Hydrogen peroxide efflux from muscle mitochondria underestimates matrix superoxide production-a correction using glutathione depletion. FEBS J 277: 2766-2778, 2010.
110. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 552: 335-344, 2003.
111. Vercesi AE, Kowaltowski AJ, Grijalba MT, Meinicke AR, Castilho RF. The role of reactive oxygen species in mitochondrial permeability transition. Biosci Rep 17: 43-52, 1997.
112. Votyakova TV, Reynolds IJ. DeltaPsi (m)-dependent and-independent production of reactive oxygen species by rat brain mitochondria. J Neurochem 79: 266-277, 2001.
113. Wagner BK, Kitami T, Gilbert TJ, Peck D, Ramanathan A, Schreiber SL, Golub TR, Mootha VK. Large-scale chemical dissection of mitochondrial function. Nat Biotechnol 26: 343-351, 2008.
114. Wallace DC, Fan W. Energetics, epigenetics, mitochondrial genetics. Mitochondrion 10: 12-31, 2010.
115. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the "phosphocreatine circuit" for cellular energy homeostasis. Biochem J 281: 21-40, 1992.
116. Webster C, Silberstein L, Hays AP, Blau HM. Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52: 503-513, 1988.
117. 2+signal transmission between the ER and mitochondria. Biochem Biophys Res Commun 348: 393-399, 2006.
118. Woitaske MD, McCarter RJ. Effects of fiber type on ischemia-reperfusion injury in mouse skeletal muscle. Plast Reconstr Surg 102: 2052-2063, 1998.
119. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124, 1999.
120. Yajid F, Mercier JG, Mercier BM, Dubouchaud H, Prefaut C. Effects of 4 wk of hindlimb suspension on skeletal muscle mitochondrial respiration in rats. J Appl Physiol 84: 479-485, 1998.
121. Zhang TY, Meaney MJ. Epigenetics and the environmental regulation of the genome and its function. Annu Rev Psychol 61: 439-466, C1-3, 2010.
122. Zoratti M, Szabò I, De Marchi U. Mitochondrial permeability transitions: how many doors to the house? Biochim Biophys Acta 1706: 40-52, 2005.