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Skeletal muscle: A paradigm for testing principles of bioenergetics

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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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References

  • Barany, M. (1967).J. Gen. Physiol. 50, 197–218.

    PubMed  Google Scholar 

  • Blei, M. L., Conley, K. E., and Kushmerick, M. J. (1993a).J. Physiol. (London) 465, 203–222.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Boska, M. (1991).NMR Biomed. 4, 173–181.

    PubMed  Google Scholar 

  • Brand, M. D., Chien, L. F., and Diolez, P. (1994).Biochem J. 297, 27–29.

    PubMed  Google Scholar 

  • Brenner, B. (1990). InMolecular Mechanisms in Muscular Contraction (Squire, J. M., ed.), Macmillan London, pp. 77–149.

    Google Scholar 

  • Burke, R. E., and Edgerton, V. R. (1975).Exercise Sport Sci. Rev. 3, 31–81.

    Google Scholar 

  • Burke, R. E., Levine, D. N., Tsairis, P., and Zajac III, F. E. (1973).J. Physiol. (London) 234, 723–748.

    Google Scholar 

  • Chance, B., and Williams, G. R. (1956).Adv. Enzymol. 17, 65–134.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Chase, P. B., Martyn, D. A., and Hannon, J. D. (1994).Biophys. J. 67, 1994–2001.

    PubMed  Google Scholar 

  • Conley, K. E. (1994).Adv. Vet. Sci Comp. Med. 38A, 1–39.

    PubMed  Google Scholar 

  • Connett, R. J. (1988).Am. J. Physiol. 254, R949-R959.

    PubMed  Google Scholar 

  • Cooke, R., (1986).CRC Crit. Rev. Biochem. 21, 53–118.

    PubMed  Google Scholar 

  • Crow, M. T., and Kushmerick, M. J. (1982).J. Gen. Physiol. 79, 147–166.

    PubMed  Google Scholar 

  • Dudley, G. A., Tullson, P. C., and Terjung, R. L. (1987).J. Biol. Chem. 262, 9109–9114.

    PubMed  Google Scholar 

  • Eddinger, T. J., and Moss, R. L. (1987).Am. J. Physiol. 253, C210-C218.

    PubMed  Google Scholar 

  • Edstrom, L., Hultman, E., Sahlin, K., and Sjoholm, H. (1982).J. Physiol. (London) 332, 47–58.

    Google Scholar 

  • Fitts, R. H. (1994).Physiol. Rev. 74, 49–94.

    PubMed  Google Scholar 

  • Greenhaff, P. L., Söderlund, K., Ren, J. M., and Hultman, E. (1993).J. Physiol. (London) 460, 443–453.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Harris, R. C., Hultman, E., Kaijser, L., and Nordesjo, L.-O. (1975).Scand. J. Clin. Lab. 35, 87–95.

    Google Scholar 

  • Heineman, F. W., and Balaban, R. S. (1990).Anna. Rev. Physiol. 52, 523–542.

    Google Scholar 

  • Henneman, E., Somjen, G., and Carpenter, D. O. (1965a)J. Neurophysiol. 28, 560–580.

    PubMed  Google Scholar 

  • Henneman, E., Somjen, G., and Carpenter, D. O. (1965b)J. Neurophysiol. 28, 599–620.

    PubMed  Google Scholar 

  • Hoppeler, H. (1986).Int. J. Sports Med. 7, 187–204.

    PubMed  Google Scholar 

  • Howald, H., Hoppeler, H., Claassen, H., Mathieu, O., and Straub, R. (1985).Pflugers Arch. 403, 369–376.

    PubMed  Google Scholar 

  • Huang, A. H., and Feigl, E. O. (1988).Cire. Res. 62, 286–298.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Katz, L. A., Swain, J. A., Portman, M. A., and Balaban, R. S. (1989).Am. J. Physiol. 256, H265-H274.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Kushmerick, M. J., Meyer, R. A., and Brown, T. R. (1992a).Am. J. Physiol. 263, C598-C606.

    PubMed  Google Scholar 

  • Kushmerick, M. J., Moerland, T. S., and Wiseman, R. W. (1992b).Proc. Natl. Acad. Sci. USA 89, 7521–7525.

    PubMed  Google Scholar 

  • Kushmerick, M. J., Moerland, T. S., and Wiseman, R. W. (1993).Adv. Exp. Med. Biol. 332, 749–761.

    PubMed  Google Scholar 

  • Larsson, L., and Moss, R. L. (1993).J. Physiol. (London) 472, 595–614.

    Google Scholar 

  • Lipmann, F. (1941). InAdvances in Enzymology (Nord, F. F. and Werkman, C. H., eds.), Interscience, New York, pp. 99–162.

    Google Scholar 

  • McCormack, J. G., and Denton, R. M. (1990).Ann. Rev. Physiol. 52, 451–466.

    Google Scholar 

  • McCormack, J. G., and Denton, R. M. (1993).Biochem. Soc. Trans. 21, 793–799.

    PubMed  Google Scholar 

  • McFarland, E. W., Kushmerick, M. J., and Moerland, T. S. (1994).Biophys. J. 67, 1912–1924.

    PubMed  Google Scholar 

  • Meyer, R. A. (1988).Am. J. Physiol. 254, C548-C553.

    PubMed  Google Scholar 

  • Meyer, R. A. (1989).Am. J. Physiol. 257, C1149-C1157.

    PubMed  Google Scholar 

  • Meyer, R. A., Sweeney, H. L., and Kushmerick, M. J. (1984).Am. J. Physiol. 246, C365-C377.

    PubMed  Google Scholar 

  • Meyer, R. A., Brown, T. R., and Kushmerick, M. J. (1985).Am. J. Physiol. 248, C279-C287.

    PubMed  Google Scholar 

  • Miller, K., Halow, J., and Koretsky, A. P. (1993).Am. J. Physiol. 265, C1544-C1551.

    PubMed  Google Scholar 

  • Mizuno, M., Secher, N. H., and Quistorff, B. (1994)J. Appl. Physiol. 76, 531–538.

    PubMed  Google Scholar 

  • Moss, R. L. (1992).Circ. Res. 70, 865–884.

    PubMed  Google Scholar 

  • Nemeth, P., Hofer, H. W., and Pette, D. (1979).Histochemistry 63, 191–201.

    PubMed  Google Scholar 

  • Pette, D., and Staron, R. S. (1990).Rev. Physiol. Biochem. Pharmacol. 116, 1–76.

    PubMed  Google Scholar 

  • Pette, D., and Staron, R. S. (1993).NIPS 8, 153–157.

    Google Scholar 

  • 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.

    Google Scholar 

  • Schimerlik, M. L., and Cleland, W. W. (1973).J. Biol. Chem. 248, 8418–8423.

    PubMed  Google Scholar 

  • Söderlund, K., and Hultman, E. (1991).Am. J. Physiol. 261, E737-E741.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Van Deursen, J., Heerschap, A., Oerlemans, F., Ruitenbeek, W., Jap, P., ter Laak, H., and Wieringa, B. (1993).Cell 74, 621–631.

    PubMed  Google Scholar 

  • Van Deursen, J., Ruitenbeek W., Heerschap A., Jap, P., and ter Laak, H. (1994).Proc. Natl. Acad. Sci. USA 91, 9091–9095.

    PubMed  Google Scholar 

  • Vandenborne, K., Walter G., Goelman G., Ploutz, L., Dudley, G., and Leigh, J. S. (1993).Proc. Soc. Magn. Resn. Med. 3, 1140a.

    Google Scholar 

  • Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K., and Eppenberger, H. M. (1992).Biochem. J. 281, 21–40.

    PubMed  Google Scholar 

  • Westerhoff, H. V., and van Dam, K. (1992). InMolecular Mechanisms in Bioenergetics (Ernster, L., ed.), Elsevier, Amsterdam, pp. 1–35.

    Google Scholar 

  • Woledge, R. C., Curtin, N. A., and Homsher, E. (1986).Energetic Aspects of Muscle Contraction, Academic Press, New York.

    Google Scholar 

  • Wyss, M., Smeitink, J., Wevers, R. A., and Wallimann, T. (1992).Biochim. Biophys. Acta Bio Energ. 1102, 119–166.

    Google Scholar 

  • Yoshizaki, K., Seo, Y., Nishikawa, H., and Morimoto, T. (1982).Biophys. J. 38, 209–211.

    PubMed  Google Scholar 

  • Yoskizaki, K., Nishikawa, H., and Watari, H. (1987).Jpn. J. Physiol. 37, 923–928.

    PubMed  Google Scholar 

  • Yoshizaki, K., Watari, H., and Radda, G. K. (1990).Biochim. Biophys. Acta 1051, 144–150.

    PubMed  Google Scholar 

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  1. Departments of Radiology, Bioengineering, and Physiology and Biophysics, University of Washington, 98195, Seattle, Washington

    M. J. Kushmerick

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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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