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Tissue Capacity for Mitochondrial Oxidative Phosphorylation and its Adaptation to Stress

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Regulation of the Rate of Mitochondrial Oxidative Phosphorylation in Vivo
1.1 “Supply” and “Demand” in Determining the Mitochondrial Respiratory Rate
1.2 On the Mechanism of Regulation of Mitochondrial ATP Synthesis In Vivo
1.3 Oxygen Dependence of Mitochondrial Oxidative Phosphorylation In Vivo
2 Mitochondrial Enzyme Content in Cells with Different Rates of Respiration
3 Metabolic Adaptation of Heart Muscle to Alterations in Physiological Work Rate
4 Metabolic Adaptations of Skeletal Muscle in Response to Endurance Training and to Electrical Stimulation
4.1 General Observations
4.2 Effects of Increased Energy Demand on Enzyme Content and Metabolism of Skeletal Muscle
4.3 Enhancement of Protein Synthesis
4.4 Possible Second Messengers
4.5 Resistance to Fatigue During Exertion
5 Effects of Conditioning on the Capacity for Oxygen Delivery to Local Regions of the Muscle
5.1 Changes in Muscle Capillarity
5.2 Changes in Myoglobin Content
6 Evolutionary Design of Muscles for Different Work Loads
7 Effects of Deconditioning on the Activity of Oxidative Enzymes in Muscle
8 Effects of Chronic Diminished Substrate Delivery on Energy Metabolism in Muscle
8.1 Effect of Restricted Blood Flow in Muscle
8.2 High‐Altitude Induced Adaptation
9 Summary
References
 1. Acker, M., W. A. Anderson, R. L. Hammond, F. DiMeo Jr., J. McCullum, M. Staum, M. Velchik, W. E. Brown, D. Gale, S. Salmons, and L. W. Stephenson. Oxygen consumption of chronically stimulated skeletal muscle. J. Thorac. Cardiovasc. Surg. 94: 702–709, 1987.
 2. Acker, M., R. L. Hammond, J. D. Mannion. S. Salmons, and L. W. Stephenson. Skeletal muscle as the potential power source for a cardiovascular pump: Assessment in vivo. Science 236: 324–327, 1987.
 3. Astrand, I., P. O. Astrand, E. H. Christensen, and R. Hedman. Myoglobin as an oxygen‐store in man. Acta Physiol. Scand. 48: 454–460, 1960.
 4. Balaban, R. S. Regulation of oxidative phosphorylation in the mammalian cell. Am. J. Physiol. 258 (Cell Physiol. 27): C377–C389, 1990.
 5. Bass, A., E. Gutmann, and V. Hanzlikova. Biochemical and his‐tochemical changes in energy supply‐enzyme pattern of muscles of the rat during old age. Gerontologia (Basel). 21: 31–45, 1975.
 6. Bigard, A. X., A. Brunet, B. Serrurier, C. Y. Guezennec, and H. Monod. Effects of endurance training at high altitude on diaphragm muscle properties. Pflugers Arch. 422 (3): 239–244, 1992.
 7. Blomquvist, C. G., and B. Saltin. Cardiovascular adaptations to physical training. Annu. Rev. Physiol. 45: 169–189, 1983.
 8. Booth, F. W., and J. O. Holloszy. Cytochrome c turnover in rat skeletal muscles. J. Biol. Chem. 252 (2): 416–419, 1977.
 9. Booth, F. W., and D. B. Thomason. Molecular and cellular adaptation of muscle in response to exercise: Perspectives of various models. Physiol. Rev. 71 (2): 541–585, 1991.
 10. Braunlin, E. A., G. M. Wahler, C. R. Swayze, R. V. Lucas, and I. J. Fox. Myoglobin facilitated oxygen diffusion maintains mechanical function of mammalian cardiac muscle. Cardiovasc. Res. 20: 627–636, 1986.
 11. Brodal, P., F. Ingjer, and L. Hermansen. Capillary supply of skeletal muscle fibers in untrained and endurance‐trained men. Am. J. Physiol. 232 (6) (Heart Circ. Physiol. 3): H705–H712, 1977.
 12. Brown, J. M. C., J. Henriksson, and S. Salmons. Restoration of fast muscle characteristics following cessation of chronic stimulation: physiological, histochemical and metabolic changes during slow‐to‐fast transformation. Proc. R. Soc. Lond. B. Biol. Sci. 235: 321–346, 1989.
 13. Burton, H. W., and J. K. Barclay. Metabolic factors from exercising muscle and the proliferation of endothelial cells. Med. Sci. Sports Exerc. 18 (4): 390–395, 1986.
 14. Bylund, A.‐C., J. Hammarsten, J. Holm, and T. Schersten. Enzyme activities in skeletal muscle from patients with peripheral arterial insufficiency. Eur. J. Clin. Invest. 6 (6): 425–429, 1976.
 15. Bylund‐Fellenius, A.‐C., P. M. Walker, A. Elander, S. Holm, J. Holm, and T. Schersten. Energy metabolism in relation to oxygen partial pressure in human skeletal muscle during exercise. Biochem. J. 200: 247–255, 1981.
 16. Chi, M. M.‐Y., C. S. Hintz, J. Henriksson, S. Salmons, R. P. Hellendahl, J. L. Park, P. M. Nemeth, and O. H. Lowry. Chronic stimulation of mammalian muscle: enzyme changes in individual fibers. Am. J. Physiol. 251 (Cell Physiol. 20): C633–C642, 1986.
 17. Clark, A. Jr., P. A. A. Clark, R. J. Connett, T. E. J. Gayeski, and C. R. Honig. How large is the drop in PO2 between cytosol and mitochondrion? Am. J. Physiol. 252 (Cell Physiol. 21): C583–C587, 1987.
 18. Clarke III, B. J., M. A. Acker, K. McCully, H. V. Subramanian, R. L. Hammond, S. Salmons, B. Chance, and L. W. Stephenson. In vivo 31P‐NMR spectroscopy of chronically stimulated canine skeletal muscle. Am. J. Physiol. 254 (Cell Physiol. 23): C258–C266, 1988.
 19. Cole, R. P. Myoglobin function in exercising skeletal muscle. Science 216: 523–525, 1982.
 20. Connett, R. J., C. R. Honig, T. E. J. Gayeski, and G. A. Brooks. Defining hypoxia: a systems view of VO2, glycolysis, energetics, and intracellular PO2. J. Appl. Physiol. 68 (3): 833–842, 1990.
 21. Davies, K. J. A., L. Packer, and G. Brooks. Exercise bioenergetics following sprint training. Arch. Biochem. Biophys. 209: 539–554, 1981.
 22. Degn, H., and H. Wohlrab. Measurements of steady‐state values of respiration rate and oxidation levels of respiratory pigments at low oxygen tensions. A new technique. Biochim. Biophys. Acta 245: 347–355, 1971.
 23. Denton, R. M., and J. G. McCormack. Calcium transport by mammalian mitochondria and its role in hormone action. Am. J. Physiol. 249 (Endocrinol. Metab. 12): E543–E554, 1985.
 24. Dione, K. E. Oxygen transport to respiring myocytes. J. Biol. Chem. 265: 15400–15402, 1990.
 25. Dudley, G. A., P. C. Tullson, and R. I. Terjung. Influence of mitochondrial content on the sensitivity of respiratory control. J. Biol. Chem. 262 (19): 9109–9114, 1987.
 26. Eisenberg, B. R., and S. Salmons. The reorganization of subcellular structure in muscle undergoing fast‐to‐slow type transformation. Cell. Tissue Res. 220: 449–471, 1981.
 27. Elander, A., J.‐P. Idstrom, S. Holm, T. Schersten, and A.‐C. Bylund‐Fellenius. Metabolic adaptation to reduced muscle blood flow. II. Mechanisms and beneficial effects. Am. J. Physiol. 249 (Endocrinol. Metab. 12): E70–E76, 1985.
 28. Elander, A., J.‐P. Idstrom, T. Schersten, and A.‐C. Bylund‐Fellenius. Metabolic adaptation to reduced muscle blood flow. I. Enzyme and metabolic alterations. Am. J. Physiol. 249 (Endocrinol. Metab. 12): E63–E69, 1985.
 29. Erecińska, M., and D. F. Wilson. Regulation of cellular energy metabolism. J. Membr. Biol. 70: 1–14, 1982.
 30. Erecińska, M., D. F. Wilson, and K. Nishiki. Homeostatic regulation of cellular energy metabolism: experimental characterization in vivo and fit to a model. Am. J. Physiol. 234 (3) (Cell Physiol. 3): C82–C89, 1978.
 31. Federspiel, W. J. A model study of intracellular oxygen gradients in a myoglobin‐containing skeletal muscle fiber. Biophys. J. 49: 857–868, 1986.
 32. Forman, N. G., and D. F. Wilson. Energetics and stoichiometry of oxidative phosphorylation from NADH to cytochrome c in isolated rat liver mitochondria. J. Biol. Chem. 257: 12908–12915, 1982.
 33. Gayeski, T. E. J., and C. R. Honig. O2 gradients from the sar‐colemma to cell interior in red muscle at maximal VO2. Am. J. Physiol. 251 (Heart Circ. Physiol. 20): H789–H799, 1986.
 34. Green, H. J., J. R. Sutton, E. E. Wolfe, J. T. Reeves, G. E. Butterfield, and G. A. Brooks. Altitude acclimatization and energy metabolic adaptations in skeletal muscle during exercise. J. Appl. Physiol. 73 (6): 2701–2708, 1992.
 35. Groebe, K., and G. Thews. Role of geometry and anisotropic diffusion for modelling PO2 profiles in working red muscle. Respir. Physiol. 79: 255–278, 1990.
 36. Gollnick, P. D., R. B. Armstrong, C. W. Saubert IV, K. Piehl, and B. Saltin. Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. J. Appl. Physiol. 33 (3): 312–319, 1972.
 37. Goodrick, C. L., D. K. Ingram, M. A. Reynolds, J. R. Freeman, and N. L. Cider. Differential effects of intermittent feeding and voluntary exercise on body weight and life span in adult rats. J. Gerontol. 38: 36–45, 1983.
 38. Hagler, L., R. I. Coppes, E. W. Askew, A. L. Hecker, and R. H. Herman. The influence of exercise and diet on myoglobin and metmyoglobin reductase in the rat. J. Lab. Clin. Med. 95: 222–230, 1980.
 39. Hansford, R. G. Control of mitochondrial substrate oxidation. Curr. Top. Bioenerg. 10: 217–283, 1980.
 40. Hansford, R. G., and F. Castro. Age‐linked changes in the activity of enzymes of the tricarboxylate cycle and lipid oxidation and of carnitine content in muscles in the rat. Mech. Ageing Dev. 19: 191–201, 1982.
 41. Henriksson, J., M. M.‐Y. Chi, C. S. Hintz, D. A. Young, K. K. Kaiser, S. Salmons, and O. H. Lowry. Chronic stimulation of mammalian muscle: changes in enzymes of six metabolic pathways. Am. J. Physiol. 251 (Cell Physiol. 20): C614–C632, 1986.
 42. Hermansen, L., and M. Wachtlova. Capillary density of skeletal muscle in well‐trained and untrained men. J. Appl. Physiol. 30: (6), 860–863, 1971.
 43. Hickson, R. C. Skeletal muscle cytochrome c and myoglobin, endurance and frequency of training. J. Appl. Physiol. 51: 746–749, 1981.
 44. Hochacka, P. W. Muscle enzymatic composition and metabolic regulation in high altitude adapted natives. Int. J. Sports Med. 13 (1): S206–S209, 1992.
 45. Holian, A., C. S. Owen, and D. F. Wilson. Control of respiration in isolated mitochondria: quantitative evaluation of the dependence of respiratory rates on [ATP], [ADP], and [Pi]. Arch. Biochem. Biophys. 181: 164–171, 1977.
 46. Holm, J. P. Bjorntorp, and T. Schersten. Metabolic activity in human skeletal muscle. Effect of peripheral arterial insufficiency. Eur. J. Clin. Invest. 2 (5): 321–325, 1972.
 47. Holloszy, J. Biochemical adaptations in muscle. Effect of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J. Biol. Chem. 242 (9): 2278–2282, 1967.
 48. Holloszy, J. O., and F. W. Booth. Biochemical adaptation to endurance exercise in muscle. Annu. Rev. Physiol. 38: 273–291, 1976.
 49. Holloszy, J. O., and E. F. Coyle. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J. Appl. Physiol. 56 (4): 831–838, 1984.
 50. Holloszy, J. O., L. B. Oscai, I. J. Don, and P. A. Mole. Mitochondrial citric acid cycle and related enzymes: adaptive response to exercise. Biochem. Biophys. Res. Commun. 40: 1368–1373, 1970.
 51. Honig, C. R. Hypoxia in skeletal muscle at rest and during the transition to steady work. Microvasc. Res. 13: 377–398, 1977.
 52. Honig, C. R., R. J. Connett, and T. E. Gayeski. O2 transport and its interaction with metabolism; a systems view of aerobic capacity. Med. Sci. Sports Exerc. 24 (1): 47–53, 1992.
 53. Honig, C. R., J. L. Frierson, and T. E. J. Gayeski. Anatomical determinants of O2 flux density at coronary capillaries. Am. J. Physiol. 256 (Heart Circ. Physiol. 25): H375–H382, 1989.
 54. Hood, D. A., R. Zak, and D. Pette. Chronic stimulation of rat skeletal muscle induces coordinate increases in mitochondrial and nuclear mRNAs of cytochrome‐c‐oxidase subunits. Eur. J. Biochem. 179: 275–280, 1989.
 55. Hudlicka, O. Effect of training on macro‐ and microcirculatory changes in exercise. Exerc. Sport Sci. Rev. 5: 181–231, 1977.
 56. Hudlicka, O. Development of microcirculation: capillary growth and adaptation. In: Handbook of Physiology. Cardiovascular System. Editors: E. M. Renkin, C. C. Michel and S. R. Geiger. Bethesda, MD: Am. Physiol. Soc., 1984, sect. 2, chapt. 5, p. 165–216.
 57. Hudlicka, O., L. Dodd, E. M. Renkin, and S. D. Gray. Early changes in fiber profile and capillary density in long‐term stimulated muscles. Am. J. Physiol. 243 (Heart Circ. Physiol. 12): H528–H535, 1982.
 58. Hudlicka, O., D. Pette, and H. Staudte. The relation between blood flow and enzymatic activities in slow and fast muscles during development. Pflügers Arch. 343: 341–346, 1973.
 59. Hudlicka, O., and S. Price. The role of blood flow and/or muscle hypoxia in capillary growth in chronically stimulated fast muscles. Pflügers Arch. 417: 67–72, 1990.
 60. Hudlicka, O., and K. R. Tyler. The effect of long‐term high‐frequency stimulation on capillary density and fibre types in rabbit fast muscles. J. Physiol. 353: 435–445, 1984.
 61. Hudlicka, O., K. R. Tyler, A. J. A. Wright, and A. M. Ziada. The effect of long‐term vasodilation on capillary growth and performance in rabbit heart and skeletal muscle. J. Physiol. 334: 49P, 1983.
 62. Hudlicka, O., A. J. A. Wright, and A. M. A. R. Ziada. Angiogenesis in the heart and skeletal muscle. Can. J. Cardiol. 2 (2): 120–123, 1986.
 63. Ji, L. L., D. L. F. Lennon, R. G. Kochan, F. J. Nagle, and H. A. Lardy. Enzymatic adaptation to physical training under β‐blockade in the rat. Evidence of a β2‐adrenergic mechanism in skeletal muscle. J. Clin. Invest. 78: 771–778, 1986.
 64. Jones, D. P. Intracellular diffusion gradients of O2 and ATP. Am. J. Physiol. 250 (Cell Physiol. 19): C663–C675, 1986.
 65. Jones, D. P., T. Y. Aw, C. Bai, and A. H. Sillau. Regulation of mitochondrial distribution: an adaptive response to changes in oxygen supply. In: Response and Adaptation to Hypoxia: Organ to Organelle, edited by S. Lahiri, N. S. Cherniack, and R. S. Fitzgerald. Oxford: Oxford Univer. Press, 1991, p. 25–35.
 66. Katz, L. A., J. A. Swain, M. A. Portman, and R. S. Balaban. Relation between phosphate metabolites and oxygen consumption in heart in vivo. Am. J. Physiol. 256 (Heart Circ. Physiol. 25): H265–H274, 1989.
 67. Kaufmann, M., J.‐A. Simoneau, J. H. Veerkamp, and D. Pette. Electrostimulation‐induced increases in fatty acid‐binding protein and myoglobin in rat fast‐twitch muscle and comparison with tissue levels in heart. FEBS Lett. 245: 181–184, 1989.
 68. Kiviluoma, K. T., K. J. Peuhkurinen, and I. E. Hassinen. Role of cellular energy state and adenosine in the regulation of coronary flow during variation in contraction frequency in an isolated perfused heart. J. Mol. Cell. Cardiol. 18: 1133–1142, 1986.
 69. Knabb, R. M., S. W. Ely, A. N. Bacchus, R. Rubio, and R. M. Berne. Consistent parallel relationships among myocardial oxygen consumption, coronary blood flow, and pericardial infusate adenosine concentration with various interventions and β‐blockade in the dog. Circ. Res. 53: 33–41, 1983.
 70. Kraus, W. E., T. S. Bernard, and R. S. Williams. Interactions between sustained contractile activity and β‐adrenergic receptors in regulation of gene expression in skeletal muscles. Am. J. Physiol. 256 (Cell Physiol. 25): C506–C514, 1989.
 71. Lawrence Jr. J. C., and W. J. Salsgiver. Evidence that levels of malate dehydrogenase and fumarase are increased by cAMP in rat myotubes. Am. J. Physiol. 247 (Cell Physiol. 16): C33–C38, 1984.
 72. Lawrie, R. A. The activity of the cytochrome system in muscle and its relation to myoglobin. Biochem. J. 55: 298–305, 1953.
 73. Lee, Y. P., and H. Lardy. Influence of thyroid hormone on L‐α‐glycerophosphate dehydrogenase and other dehydrogenases in various organs of the rat. J. Biol. Chem. 240: 1427–1436, 1965.
 74. Longmuir, I. S. Respiration rate of rat‐liver cells at low oxygen concentrations. Biochem. J. 65: 378–382, 1957.
 75. Lundgren, F., A.‐G. Dahllof, T. Schersten, and A.‐C. Bylund‐Fellenius. Muscle enzyme adaptations with peripheral arterial insufficiency: spontaneous adaptation, effect of different treatments and consequences on walking performance. Clin. Sci. (Colch) 77: 485–493, 1989.
 76. Mathieu‐Costello, O. Comparative aspects of muscle capillary supply. Annu. Rev. Physiol. 55: 503–525, 1993.
 77. Mathieu‐Costello, O., J. M. Szewczak, R. B. Logemann, and P. J. Agey, Geometry of blood tissue exchange in bat flight muscle compared to bat hindlimb and rat soleus muscle. Am. J. Physiol. 262 (Regulatory Integrative Comp. Physiol. 31): R955–R965, 1992.
 78. Matheson, G. O., P. S. Allen, D. C. Ellinger, C. C. Hanstock, D. Gheorghiu, D. C. McKenzie, C. Stanley, W. S. Parkhouse, and P. W. Hochacka. Skeletal muscle metabolism and work capacity: a 31P‐NMR study of Andean natives and lowlanders. J. Appl. Physiol. 70 (5): 1963–1976, 1991.
 79. McCarter, R. J. M., E. J. Masoro, and B. P. Yu. Rat muscle structure and metabolism in relation to age and food intake. Am. J. Physiol. 242 (Regulatory Integrative Comp. Physiol. 13): R89–R93, 1982.
 80. Meininger, C., and H. J. Granger. Mechanisms leading to adenosine‐stimulated proliferation of microvascular endothelial cells. Am. J. Physiol. 258 (Heart Circ. Physiol. 27): H198–H206, 1990.
 81. Mole, P. A., L. B. Oscai, and J. O. Holloszy. Adaptation of muscle to exercise. Increase in levels of palmitoyl CoA synthetase, carnitine palmityltransferase, and palmityl CoA dehydrogenase, and in the capacity to oxidize fatty acids. J. Clin. Invest. 50: 2323–2330, 1971.
 82. Morrison, P. R., R. B. Biggs, and F. W. Booth. Daily running for 2 wk and mRNAs for cytochrome c and α‐actin in rat skeletal muscle. Am. J. Physiol. 257 (Cell Physiol. 26): C936–C939, 1989.
 83. Nishiki, K., M. Erecińska, D. F. Wilson, and S. Cooper. Evaluation of oxidative phosphorylation in hearts from euthyroid, hypothyroid, and hyperthyroid rats. Am. J. Physiol. 235 (Cell. Physiol. 4): C212–C219, 1978.
 84. Oscai, L. B., P. A. Mole, and J. O. Holloszy. Biochemical adaptations in muscle. II. Response of mitochondrial adenosine triphosphatase, creatine phosphokinase, and adenylate kinase activities in skeletal muscle to exercise. J. Biol. Chem. 246 (22): 6968–6972, 1971.
 85. Oscai, L. B., P. A. Mole, and J. O. Holloszy. Effects of exercise on cardiac weight and mitochondria in male and female rats. Am. J. Physiol. 220 (6): 1944–1948, 1971.
 86. Owen, C. S., and D. F. Wilson Control of respiration by the mitochondrial phosphorylation potential. Arch. Biochem. Biophys. 161: 581–591, 1974.
 87. Pattengale, P., and J. O. Holloszy. Augmentation of skeletal muscle myoglobin by a program of treadmill running. Am. J. Physiol. 213 (3): 783–785, 1967.
 88. Pette, D. Activity‐induced fast to slow transitions in mammalian muscle. Med. Sci. Sports Exerc. 16 (6): 517–528, 1984.
 89. Pette, D., W. Muller, E. Leisner, and G. Vrbova. Time dependent effects on contractile properties, fibre population, myosin light chains and enzymes of energy metabolism in intermittently and continuously stimulated fast twitch muscles of the rabbit. Pflügers Arch. 364: 103–112, 1976.
 90. Pette, D., M. E. Smith, H. W. Staudte, and G. Vrbova. Effects of long‐term electrical stimulation on some contractile and metabolic characteristics of fast rabbit muscles. Pflügers Arch. 338: 257–272, 1973.
 91. Portman, M. A., F. W. Heineman, and R. S. Balaban. Developmental changes in the relation between phosphate metabolites and oxygen consumption in the sheep heart in vivo. J. Clin. Invest. 83: 456–464, 1989.
 92. Reaven, E. P., and G. M. Reaven. Structure and function changes in the endocrine pancreas of aging rats with reference to the modulating effects of exercise and caloric restriction. J. Clin. Invest. 68: 75–84, 1981.
 93. Robiolio, M., W. L. Rumsey, and D. F. Wilson. Oxygen diffusion and mitochondrial respiration in neuroblastoma cells. Am. J. Physiol. 256 (Cell Physiol. 25): C1207–C1213, 1989.
 94. Rumsey, W. L., Z. V. Kendrick, and J W. Starnes. Bioenergetics in the aging Fischer 344 rat: Effects of exercise and food restriction. Exp. Gerontol. 22: 271–287, 1987.
 95. Rumsey, W. L., C. Schlosser, E. M. Nuutinen, M. Robiolio, and D. F. Wilson. Cellular energetics and the oxygen dependence of respiration in myocytes isolated from adult rat heart. J. Biol. Chem. 265: 15392–15402, 1990.
 96. Salmons, S., and J. Henriksson. The adaptive response of skeletal muscle to increased use. Muscle Nerve 4: 94–105, 1981.
 97. Saltin, B., and P. ‐O. Astrand. Maximal oxygen uptake in athletes. J. Appl. Physiol. 23: 353–358, 1967.
 98. Saltin, B., and P. D. Gollnick. Skeletal muscle adaptability: significance for metabolism and performance. In: Handbook of Physiology. Skeletal Muscle. Bethesda, MD: Am. Physiol. Soc, 1983, sect. 10, chapt. 19, p. 555–631.
 99. Saunders, D. K., and M. R. Fedde. Physical conditioning: Effect on the myoglobin concentration in skeletal and cardiac muscle of bar‐headed geese. Comp. Biochem. Physiol. 100A (2): 349–352, 1991.
 100. Scheel, K. W., E. Seavey, J. F. Gaugl, and S. E. Williams. Coronary and myocardial adaptations to high altitude in dogs. Am. J. Physiol. 259 (Heart Circ. Physiol. 28): H1667–H1673, 1990.
 101. Scholander, P. F. Oxygen transport through hemoglobin solutions. Science 131: 585–590, 1960.
 102. Seedorf, U., E. Leberer, B. J. Kirschbaum, and D. Pette. Neural control of gene expression in skeletal muscle. Effects of chronic stimulation on lactate dehydrogenase isoenzymes and citrate synthase. Biochem. J. 239: 115–120, 1986.
 103. Starnes, J. W., and W. L. Rumsey. Cardiac energetics and performance of exercised and food restricted rats during aging. Am. J. Physiol. 254 (Heart Circ. Physiol. 23): H599–H608, 1988.
 104. Suarez, R. K., J. R. B. Lighton, G. S. Brown, and O. Mathieu‐Costello. Mitochondrial respiration in hummingbird flight muscles. Proc. Natl. Acad. Sci. USA 88: 4870–4873, 1991.
 105. Sullivan, S. M., and R. N. Pittman. Relationship between mitochondrial volume density and capillarity in hamster muscles. Am. J. Physiol. 252 (Heart Circ. Physiol. 21): H149–H155, 1987.
 106. Sutton, J. R., J. T. Reeves, B. M. Groves, P. D. Wagner, J. K. Alexander, H. N. Huffgren, A. Cymerman, and C. S. Houston. Oxygen transport and cardiovascular function at extreme altitude: lessons from Operation Everest II. Int. J. Sports Med. 13 (1): S13–S18, 1992.
 107. Terrados, N. Altitude training and muscular metabolism. Int. J. Sports Med. 13 (1): S206–S209, 1992.
 108. Terrados, N., E. Jansson, C. Sylven, and L. Kaijser. Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin. J. Appl. Physiol. 68 (6): 2369–2372, 1990.
 109. Underwood, L. E., and R. S. Williams. Pretranslational regulation of myoglobin gene expression. Am. J. Physiol. 252 (Cell Physiol. 21): C450–C453, 1987.
 110. Wagner, P. D. Adaptation of O2 transport and utilization at altitude in man. Adv. Exp. Med. Biol. 317: 75–94, 1992.
 111. Whipple, G. H. The hemoglobin of striated muscle. I. Variations due to age and exercise. Am. J. Physiol. 76: 693–707, 1926.
 112. Williams, R. S. Mitochondrial gene expression in mammalian striated muscle. Evidence that variation in gene dosage is the major regulatory event. J. Biol. Chem. 261 (26): 12390–12394, 1986.
 113. Williams, R. S., M. G. Caron, and K. Daniel. Skeletal muscle β‐adrenergic receptors: variations due to fiber type and training. Am. J. Physiol. 246 (Endocrinol. Metab. 9): E160–E167, 1984.
 114. Williams, R. S., M. Garcia‐Moll, J. Mellor, S. Salmons, and W. Harlan. Adaptation of skeletal muscle to increased contractile activity. Expression of nuclear genes encoding mitochondrial proteins. J. Biol. Chem. 262 (6): 2764–2767, 1987.
 115. Williams, R. S., and W. Harlan. Effects of inhibition of mitochondrial protein synthesis in skeletal muscle. Am. J. Physiol. 253 (Cell Physiol. 22): C866–C871, 1987.
 116. Williams, R. S., S. Salmons, E. A. Newsholme, R. E. Kaufman, and J. Mellor. Regulation of nuclear and mitochondrial gene expression by contractile activity in skeletal muscle. J. Biol. Chem. 261 (1): 376–380, 1986.
 117. Wilson, D. F., and M. Erecińska. Effect of oxygen pressure on cellular metabolism. Chest 88S: 229S–232S, 1985.
 118. Wilson, D. F., M. Erecińska, C. Drown, and I. A. Silver. The oxygen dependence of cellular energy metabolism. Arch. Biochem. Biophys. 195: 485–493, 1979.
 119. Wilson, D. F., C. S. Owen, and M. Erecińska. Quantitative dependence of mitochondrial oxidative phosphorylation on oxygen concentration: a mathematical model. Arch. Biochem. Biophys. 195: 494–504, 1979.
 120. Wilson, D. F., C. S. Owen, and A. Holian. Control of mitochondrial respiration: a quantitative evaluation of the roles of cytochrome c and oxygen. Arch. Biochem. Biophys. 182: 749–762, 1977.
 121. Wilson, D. F., M. Stubbs, N. Oshino, and M. Erecińska. Thermodynamic relationships between the mitochondrial oxidation‐reduction reactions and cellular ATP levels in ascites tumor cells and perfused rat liver. Biochemistry 13: 5305–5311, 1974.
 122. Wilson, D. F., M. Stubbs, R. L. Veech, M. Erecińska, and H. A. Krebs. Equilibrium relations between the oxidation‐reduction reactions and the adenosine triphosphate synthesis in suspensions of isolated liver cells. Biochem. J. 140: 57–64, 1974.
 123. Wittenberg, J. B. Myoglobin‐faciliated oxygen diffusion: role of myoglobin in oxygen entry into muscle. Physiol. Rev. 50 (4): 559–636, 1970.
 124. Wittenberg, B. A., and J. B. Wittenberg. Oxygen pressure gradients in isolated cardiac myocytes. J. Biol. Chem. 260: 6548–6554, 1985.
 125. Wittenberg, B. A., and J. B. Wittenberg. Transport of oxygen in muscle. Annu. Rev. Physiol. 51: 857–878, 1989.
 126. Wittenberg, J. B., and B. A. Wittenberg. Mechanisms of cytoplasmic hemoglobin and myoglobin function. Annu. Rev. Biophys. Biophys. Chem. 19: 217–241, 1990.

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William L. Rumsey, David F. Wilson. Tissue Capacity for Mitochondrial Oxidative Phosphorylation and its Adaptation to Stress. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 1095-1113. First published in print 1996. doi: 10.1002/cphy.cp040247