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. 2003 Nov 1;375(Pt 3):799–804. doi: 10.1042/BJ20030882

Regulation of oxidative phosphorylation in different muscles and various experimental conditions.

Bernard Korzeniewski 1
PMCID: PMC1223721  PMID: 12901719

Abstract

It has been shown previously that direct stimulation of oxidative-phosphorylation complexes in parallel with the stimulation of ATP usage is able to explain the stability of intermediate metabolite (ATP/ADP, phosphocreatine/creatine, NADH/NAD+, protonmotive force) concentrations accompanied by a large increase in oxygen consumption and ATP turnover during transition from rest to intensive exercise in skeletal muscle. It has been also postulated that intensification of parallel activation in the ATP supply-demand system is one of the mechanisms of training-induced adaptation of oxidative phosphorylation in skeletal muscle. In the present paper, it is demonstrated, using the computer model of oxidative phosphorylation in intact skeletal muscle developed previously, that the direct activation of oxidative phosphorylation during muscle contraction can account for the following kinetic properties of oxidative phosphorylation in skeletal muscle encountered in different experimental studies: (i) increase in the respiration rate per mg of mitochondrial protein at a given ADP concentration as a result of muscle training and decrease in this parameter in hypothyroidism; (ii) asymmetry (different half-transition time, t(1/2)) in phosphocreatine concentration time course between on-transient (rest-->work transition) and off-transient (recovery after exercise); (iii) overshoot in phosphocreatine concentration during recovery after exercise; (iv) variability in the kinetic properties of oxidative phosphorylation in different kinds of muscle under different experimental conditions. No other postulated mechanism is able to explain all these phenomena at the same time and therefore the present paper strongly supports the idea of the parallel activation of ATP usage and different oxidative-phosphorylation complexes during muscle contraction.

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Selected References

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  1. Balaban R. S., Kantor H. L., Katz L. A., Briggs R. W. Relation between work and phosphate metabolite in the in vivo paced mammalian heart. Science. 1986 May 30;232(4754):1121–1123. doi: 10.1126/science.3704638. [DOI] [PubMed] [Google Scholar]
  2. CHANCE B., WILLIAMS G. R. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J Biol Chem. 1955 Nov;217(1):383–393. [PubMed] [Google Scholar]
  3. CHANCE B., WILLIAMS G. R. The respiratory chain and oxidative phosphorylation. Adv Enzymol Relat Subj Biochem. 1956;17:65–134. doi: 10.1002/9780470122624.ch2. [DOI] [PubMed] [Google Scholar]
  4. Constable S. H., Favier R. J., McLane J. A., Fell R. D., Chen M., Holloszy J. O. Energy metabolism in contracting rat skeletal muscle: adaptation to exercise training. Am J Physiol. 1987 Aug;253(2 Pt 1):C316–C322. doi: 10.1152/ajpcell.1987.253.2.C316. [DOI] [PubMed] [Google Scholar]
  5. Dudley G. A., Tullson P. C., Terjung R. L. Influence of mitochondrial content on the sensitivity of respiratory control. J Biol Chem. 1987 Jul 5;262(19):9109–9114. [PubMed] [Google Scholar]
  6. From A. H., Zimmer S. D., Michurski S. P., Mohanakrishnan P., Ulstad V. K., Thoma W. J., Uğurbil K. Regulation of the oxidative phosphorylation rate in the intact cell. Biochemistry. 1990 Apr 17;29(15):3731–3743. doi: 10.1021/bi00467a020. [DOI] [PubMed] [Google Scholar]
  7. Hickson R. C., Bomze H. A., Hollozy J. O. Faster adjustment of O2 uptake to the energy requirement of exercise in the trained state. J Appl Physiol Respir Environ Exerc Physiol. 1978 Jun;44(6):877–881. doi: 10.1152/jappl.1978.44.6.877. [DOI] [PubMed] [Google Scholar]
  8. Jeneson J. A., Wiseman R. W., Westerhoff H. V., Kushmerick M. J. The signal transduction function for oxidative phosphorylation is at least second order in ADP. J Biol Chem. 1996 Nov 8;271(45):27995–27998. doi: 10.1074/jbc.271.45.27995. [DOI] [PubMed] [Google Scholar]
  9. Katz L. A., Swain J. A., Portman M. A., Balaban R. S. Relation between phosphate metabolites and oxygen consumption of heart in vivo. Am J Physiol. 1989 Jan;256(1 Pt 2):H265–H274. doi: 10.1152/ajpheart.1989.256.1.H265. [DOI] [PubMed] [Google Scholar]
  10. Kavanagh N. I., Ainscow E. K., Brand M. D. Calcium regulation of oxidative phosphorylation in rat skeletal muscle mitochondria. Biochim Biophys Acta. 2000 Feb 24;1457(1-2):57–70. doi: 10.1016/s0005-2728(00)00054-2. [DOI] [PubMed] [Google Scholar]
  11. Korzeniewski B., Harper M. E., Brand M. D. Proportional activation coefficients during stimulation of oxidative phosphorylation by lactate and pyruvate or by vasopressin. Biochim Biophys Acta. 1995 May 10;1229(3):315–322. doi: 10.1016/0005-2728(95)00008-7. [DOI] [PubMed] [Google Scholar]
  12. Korzeniewski B., Mazat J. P. Theoretical studies on the control of oxidative phosphorylation in muscle mitochondria: application to mitochondrial deficiencies. Biochem J. 1996 Oct 1;319(Pt 1):143–148. doi: 10.1042/bj3190143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Korzeniewski B. Regulation of ATP supply during muscle contraction: theoretical studies. Biochem J. 1998 Mar 15;330(Pt 3):1189–1195. doi: 10.1042/bj3301189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Korzeniewski B. Regulation of ATP supply in mammalian skeletal muscle during resting state-->intensive work transition. Biophys Chem. 2000 Jan 10;83(1):19–34. doi: 10.1016/s0301-4622(99)00120-9. [DOI] [PubMed] [Google Scholar]
  15. Korzeniewski B. Theoretical studies on the regulation of oxidative phosphorylation in intact tissues. Biochim Biophys Acta. 2001 Mar 1;1504(1):31–45. doi: 10.1016/s0005-2728(00)00237-1. [DOI] [PubMed] [Google Scholar]
  16. Korzeniewski B., Zoladz J. A. A model of oxidative phosphorylation in mammalian skeletal muscle. Biophys Chem. 2001 Aug 30;92(1-2):17–34. doi: 10.1016/s0301-4622(01)00184-3. [DOI] [PubMed] [Google Scholar]
  17. Korzeniewski Bernard, Zoladz Jerzy A. Influence of rapid changes in cytosolic pH on oxidative phosphorylation in skeletal muscle: theoretical studies. Biochem J. 2002 Jul 1;365(Pt 1):249–258. doi: 10.1042/bj20020031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Korzeniewski Bernard, Zoladz Jerzy A. Training-induced adaptation of oxidative phosphorylation in skeletal muscles. Biochem J. 2003 Aug 15;374(Pt 1):37–40. doi: 10.1042/BJ20030526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kushmerick M. J., Meyer R. A., Brown T. R. Regulation of oxygen consumption in fast- and slow-twitch muscle. Am J Physiol. 1992 Sep;263(3 Pt 1):C598–C606. doi: 10.1152/ajpcell.1992.263.3.C598. [DOI] [PubMed] [Google Scholar]
  20. Kushmerick M. J., Meyer R. A. Chemical changes in rat leg muscle by phosphorus nuclear magnetic resonance. Am J Physiol. 1985 May;248(5 Pt 1):C542–C549. doi: 10.1152/ajpcell.1985.248.5.C542. [DOI] [PubMed] [Google Scholar]
  21. McCormack J. G., Halestrap A. P., Denton R. M. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev. 1990 Apr;70(2):391–425. doi: 10.1152/physrev.1990.70.2.391. [DOI] [PubMed] [Google Scholar]
  22. Meyer R. A. A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am J Physiol. 1988 Apr;254(4 Pt 1):C548–C553. doi: 10.1152/ajpcell.1988.254.4.C548. [DOI] [PubMed] [Google Scholar]
  23. Meyer R. A., Foley J. M. Testing models of respiratory control in skeletal muscle. Med Sci Sports Exerc. 1994 Jan;26(1):52–57. [PubMed] [Google Scholar]
  24. Mildaziene V., Baniene R., Nauciene Z., Marcinkeviciute A., Morkuniene R., Borutaite V., Kholodenko B., Brown G. C. Ca2+ stimulates both the respiratory and phosphorylation subsystems in rat heart mitochondria. Biochem J. 1996 Nov 15;320(Pt 1):329–334. doi: 10.1042/bj3200329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rolfe D. F., Newman J. M., Buckingham J. A., Clark M. G., Brand M. D. Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol. 1999 Mar;276(3 Pt 1):C692–C699. doi: 10.1152/ajpcell.1999.276.3.C692. [DOI] [PubMed] [Google Scholar]
  26. Rossiter H. B., Ward S. A., Kowalchuk J. M., Howe F. A., Griffiths J. R., Whipp B. J. Dynamic asymmetry of phosphocreatine concentration and O(2) uptake between the on- and off-transients of moderate- and high-intensity exercise in humans. J Physiol. 2002 Jun 15;541(Pt 3):991–1002. doi: 10.1113/jphysiol.2001.012910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sahlin K., Söderlund K., Tonkonogi M., Hirakoba K. Phosphocreatine content in single fibers of human muscle after sustained submaximal exercise. Am J Physiol. 1997 Jul;273(1 Pt 1):C172–C178. doi: 10.1152/ajpcell.1997.273.1.C172. [DOI] [PubMed] [Google Scholar]
  28. Tonkonogi M., Sahlin K. Rate of oxidative phosphorylation in isolated mitochondria from human skeletal muscle: effect of training status. Acta Physiol Scand. 1997 Nov;161(3):345–353. doi: 10.1046/j.1365-201X.1997.00222.x. [DOI] [PubMed] [Google Scholar]
  29. Yoshida T., Watari H. 31P-nuclear magnetic resonance spectroscopy study of the time course of energy metabolism during exercise and recovery. Eur J Appl Physiol Occup Physiol. 1993;66(6):494–499. doi: 10.1007/BF00634298. [DOI] [PubMed] [Google Scholar]

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