Abstract
Muscular activity converts chemical energy into useful work and metabolism restores muscle to its original state. This essay explores the organization and interactions of the regulatory system(s) which allow this energy balance to occur. The term “energy balance” is used in a biochemical rather than a thermodynamic sense—concerned not with deductions from the physical principles of thermodynamics, but rather with those enzymatic processes which nature evolved and which operate at remarkably fixed stoichiometry. Energy balance is a statement of conservation of energy put into biochemical observables.31P NMR spectroscopy is one of the most useful techniques for investigating these questions quantitatively under physiological conditionsin vivo. The author (1) describes the rules or principles of biochemical energy balance; (2) discusses sample results from human muscle to demonstrate its use in studying this class of questions; (3) presents a simple model of integrated cellular respiration to demonstrate its sufficiency to account for the main observations.
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Barany, M. (1967).J. Gen. Physiol. 50, 197–218.
Blei, M. L., Conley, K. E., and Kushmerick, M. J. (1993a).J. Physiol. (London) 465, 203–222.
Blei, M. L., Conley, K. E., Odderson, I. R., Esselman, P. C., and Kushmerick, M. J. (1993b).Proc. Natl. Acad. Sci. USA 90, 7396–7400.
Boska, M. (1991).NMR Biomed. 4, 173–181.
Brand, M. D., Chien, L. F., and Diolez, P. (1994).Biochem J. 297, 27–29.
Brenner, B. (1990). InMolecular Mechanisms in Muscular Contraction (Squire, J. M., ed.), Macmillan London, pp. 77–149.
Burke, R. E., and Edgerton, V. R. (1975).Exercise Sport Sci. Rev. 3, 31–81.
Burke, R. E., Levine, D. N., Tsairis, P., and Zajac III, F. E. (1973).J. Physiol. (London) 234, 723–748.
Chance, B., and Williams, G. R. (1956).Adv. Enzymol. 17, 65–134.
Chance, B., Leigh, J. S., Kent, J., McCully, K., Nioka, S., Clark, B. J., and Maris, J. M. (1986).Proc. Natl. Acad. Sci. USA 83, 9458–9462.
Chase, P. B., Martyn, D. A., and Hannon, J. D. (1994).Biophys. J. 67, 1994–2001.
Conley, K. E. (1994).Adv. Vet. Sci Comp. Med. 38A, 1–39.
Connett, R. J. (1988).Am. J. Physiol. 254, R949-R959.
Cooke, R., (1986).CRC Crit. Rev. Biochem. 21, 53–118.
Crow, M. T., and Kushmerick, M. J. (1982).J. Gen. Physiol. 79, 147–166.
Dudley, G. A., Tullson, P. C., and Terjung, R. L. (1987).J. Biol. Chem. 262, 9109–9114.
Eddinger, T. J., and Moss, R. L. (1987).Am. J. Physiol. 253, C210-C218.
Edstrom, L., Hultman, E., Sahlin, K., and Sjoholm, H. (1982).J. Physiol. (London) 332, 47–58.
Fitts, R. H. (1994).Physiol. Rev. 74, 49–94.
Greenhaff, P. L., Söderlund, K., Ren, J. M., and Hultman, E. (1993).J. Physiol. (London) 460, 443–453.
Groen, A. L., Wanders, R. J. A., Westerhoff, H. V., van der Meer, R., and Tager, J. M. (1982).J. Biol. Chem. 257, 2754–2757.
Harris, R. C., Hultman, E., Kaijser, L., and Nordesjo, L.-O. (1975).Scand. J. Clin. Lab. 35, 87–95.
Heineman, F. W., and Balaban, R. S. (1990).Anna. Rev. Physiol. 52, 523–542.
Henneman, E., Somjen, G., and Carpenter, D. O. (1965a)J. Neurophysiol. 28, 560–580.
Henneman, E., Somjen, G., and Carpenter, D. O. (1965b)J. Neurophysiol. 28, 599–620.
Hoppeler, H. (1986).Int. J. Sports Med. 7, 187–204.
Howald, H., Hoppeler, H., Claassen, H., Mathieu, O., and Straub, R. (1985).Pflugers Arch. 403, 369–376.
Huang, A. H., and Feigl, E. O. (1988).Cire. Res. 62, 286–298.
Jeneson, J., Nelson, S. J., Vigneron, D. B., Taylor, J. S., Murphy, Boesch J., and Brown, T. R. (1992).Am. J. Physiol. 263, C357-C364.
Katz, L. A., Swain, J. A., Portman, M. A., and Balaban, R. S. (1989).Am. J. Physiol. 256, H265-H274.
Kingsley-Hickman, P. B., Sako, E. Y., Mohanakrishnan, P., Robitaille, P. M. L., From, A. H. L., Foker, J. E., and Ugurbil, K. (1987).26, 7501–7510.
Kushmerick, M. J. (1981). InMembrane Structure and Function (Bittar, E.E., ed.), Wiley, New York, 161–229.
Kushmerick, M. J. (1983). InHandbook of Physiology: Skeletal Muscle (Peachey, L., Adrian, R., and Geiger, S. R., eds.), American Physiological Society, Bethesda, Maryland, pp. 189–236.
Kushmerick, M. J., Meyer, R. A., and Brown, T. R. (1992a).Am. J. Physiol. 263, C598-C606.
Kushmerick, M. J., Moerland, T. S., and Wiseman, R. W. (1992b).Proc. Natl. Acad. Sci. USA 89, 7521–7525.
Kushmerick, M. J., Moerland, T. S., and Wiseman, R. W. (1993).Adv. Exp. Med. Biol. 332, 749–761.
Larsson, L., and Moss, R. L. (1993).J. Physiol. (London) 472, 595–614.
Lipmann, F. (1941). InAdvances in Enzymology (Nord, F. F. and Werkman, C. H., eds.), Interscience, New York, pp. 99–162.
McCormack, J. G., and Denton, R. M. (1990).Ann. Rev. Physiol. 52, 451–466.
McCormack, J. G., and Denton, R. M. (1993).Biochem. Soc. Trans. 21, 793–799.
McFarland, E. W., Kushmerick, M. J., and Moerland, T. S. (1994).Biophys. J. 67, 1912–1924.
Meyer, R. A. (1988).Am. J. Physiol. 254, C548-C553.
Meyer, R. A. (1989).Am. J. Physiol. 257, C1149-C1157.
Meyer, R. A., Sweeney, H. L., and Kushmerick, M. J. (1984).Am. J. Physiol. 246, C365-C377.
Meyer, R. A., Brown, T. R., and Kushmerick, M. J. (1985).Am. J. Physiol. 248, C279-C287.
Miller, K., Halow, J., and Koretsky, A. P. (1993).Am. J. Physiol. 265, C1544-C1551.
Mizuno, M., Secher, N. H., and Quistorff, B. (1994)J. Appl. Physiol. 76, 531–538.
Moss, R. L. (1992).Circ. Res. 70, 865–884.
Nemeth, P., Hofer, H. W., and Pette, D. (1979).Histochemistry 63, 191–201.
Pette, D., and Staron, R. S. (1990).Rev. Physiol. Biochem. Pharmacol. 116, 1–76.
Pette, D., and Staron, R. S. (1993).NIPS 8, 153–157.
Saltin, B. and Gollnick, P. D. (1983). InHandbook of Physiology: Skeletal Muscle (Peachey, L., Adrian, R. and Geiger, S. R., eds.), American Physiological Society, Bethesda, Maryland, pp. 555–631.
Schimerlik, M. L., and Cleland, W. W. (1973).J. Biol. Chem. 248, 8418–8423.
Söderlund, K., and Hultman, E. (1991).Am. J. Physiol. 261, E737-E741.
Ugurbil, K., Kingsley-Hickman, P. B., Sako, E. Y., Zimmer, S., Mohanakrishnan, P., Robitaille, P. M. L., Thoma, W. J., Johnson, A., Foker, J. E., and From, A. H. L. (1987).Ann. N. Y. Acad. Sci. 508, 265–286.
Van Deursen, J., Heerschap, A., Oerlemans, F., Ruitenbeek, W., Jap, P., ter Laak, H., and Wieringa, B. (1993).Cell 74, 621–631.
Van Deursen, J., Ruitenbeek W., Heerschap A., Jap, P., and ter Laak, H. (1994).Proc. Natl. Acad. Sci. USA 91, 9091–9095.
Vandenborne, K., Walter G., Goelman G., Ploutz, L., Dudley, G., and Leigh, J. S. (1993).Proc. Soc. Magn. Resn. Med. 3, 1140a.
Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K., and Eppenberger, H. M. (1992).Biochem. J. 281, 21–40.
Westerhoff, H. V., and van Dam, K. (1992). InMolecular Mechanisms in Bioenergetics (Ernster, L., ed.), Elsevier, Amsterdam, pp. 1–35.
Woledge, R. C., Curtin, N. A., and Homsher, E. (1986).Energetic Aspects of Muscle Contraction, Academic Press, New York.
Wyss, M., Smeitink, J., Wevers, R. A., and Wallimann, T. (1992).Biochim. Biophys. Acta Bio Energ. 1102, 119–166.
Yoshizaki, K., Seo, Y., Nishikawa, H., and Morimoto, T. (1982).Biophys. J. 38, 209–211.
Yoskizaki, K., Nishikawa, H., and Watari, H. (1987).Jpn. J. Physiol. 37, 923–928.
Yoshizaki, K., Watari, H., and Radda, G. K. (1990).Biochim. Biophys. Acta 1051, 144–150.
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Kushmerick, M.J. Skeletal muscle: A paradigm for testing principles of bioenergetics. J Bioenerg Biomembr 27, 555–569 (1995). https://doi.org/10.1007/BF02111654
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DOI: https://doi.org/10.1007/BF02111654