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Energy turnover for Ca2+ cycling in skeletal muscle

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Abstract

The majority of energy consumed by contracting muscle can be accounted for by two ATP-dependent processes, cross-bridge cycling and Ca2+ cycling. The energy for Ca2+ cycling is necessary for contraction but is an overhead cost, energy that cannot be converted into mechanical work. Measurement of the energy used for Ca2+ cycling also provides a means of determining the total Ca2+ released from the sarcoplasmic reticulum into the sarcoplasm during a contraction. To make such a measurement requires a method to selectively inhibit cross-bridge cycling without altering Ca2+ cycling. In this review, we provide a critical analysis of the methods used to partition skeletal muscle energy consumption between cross-bridge and non-cross-bridge processes and present a summary of data for a wide range of skeletal muscles. It is striking that the cost of Ca2+ cycling is almost the same, 30–40% of the total cost of isometric contraction, for most muscles studied despite differences in muscle contractile properties, experimental conditions, techniques used to measure energy cost and to partition energy use and in absolute rates of energy use. This fraction increases with temperature for amphibian or fish muscle. Fewer data are available for mammalian muscle but most values are similar to those for amphibian muscle. For mammalian muscles there are no obvious effects of animal size, muscle fibre type or temperature.

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References

  • Allen DG, Blinks JR (1978) Calcium transients in aequorin-injected frog cardiac muscle. Nature 273:509–513

    Article  PubMed  CAS  Google Scholar 

  • Altringham JD, Bottinelli R (1985) The descending limb of the sarcomere length-force relation in single muscle fibres of the frog. J Muscle Res Cell Motil 6:585–600

    Article  PubMed  CAS  Google Scholar 

  • Ananthaswamy J, Atkinson G (1985) Thermodynamics of concentrated electrolyte mixtures 5. A review of the thermodynamic properties of aqueous calcium chloride in the temperature range 273.15–373.15 K. J Chem Eng Data 30:120–128

    Article  CAS  Google Scholar 

  • Baker AJ, Brandes R, Schendel TM, Trocha SD, Miller RG, Weiner MW (1994) Energy use by contractile and noncontractile processes in skeletal muscle estimated by 31P-NMR. Am J Physiol 266:C825–C831

    PubMed  CAS  Google Scholar 

  • Balnave CD, Allen DG (1996) The effect of muscle length on intracellular calcium and force in single fibres from mouse skeletal muscle. J Physiol 492:705–713

    PubMed  CAS  Google Scholar 

  • Balog EM, Fitts RH (1996) Effects of fatiguing stimulation on intracellular Na+ and K+ in frog skeletal muscle. J Appl Physiol 81:679–685

    PubMed  CAS  Google Scholar 

  • Barclay CJ (1996) Mechanical efficiency and fatigue of fast and slow muscles of the mouse. J Physiol 497:781–794

    PubMed  CAS  Google Scholar 

  • Barclay CJ, Loiselle DS (2007) Can activation account for 80% of skeletal muscle energy use during isometric contraction? Am J Physiol 292:C612

    Article  CAS  Google Scholar 

  • Barclay CJ, Curtin NA, Woledge RC (1993) Changes in crossbridge and non-crossbridge energetics during moderate fatigue of frog muscle fibres. J Physiol 468:543–555

    PubMed  CAS  Google Scholar 

  • Barsotti RJ, Butler TM (1984) Chemical energy usage and myosin light chain phosphorylation in mammalian skeletal muscle. J Muscle Res Cell Motil 5:45–64

    Article  PubMed  CAS  Google Scholar 

  • Baylor SM, Hollingworth S (2000) Measurement and interpretation of cytoplasmic [Ca2+] signals from calcium-indicator dyes. News Physiol Sci 15:19–26

    PubMed  CAS  Google Scholar 

  • Baylor SM, Hollingworth S (2003) Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol 551:125–138

    Article  PubMed  CAS  Google Scholar 

  • Baylor SM, Chandler WK, Marshall MW (1983) Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients. J Physiol 344:625–666

    PubMed  CAS  Google Scholar 

  • Blinks JR, Rudel R, Taylor SR (1978) Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin. J Physiol 277:291–323

    PubMed  CAS  Google Scholar 

  • Burchfield DM, Rall JA (1985) Energetics of activation in frog skeletal muscle at sarcomere lengths beyond myofilament overlap. Biophys J 48:1049–1051

    PubMed  CAS  Google Scholar 

  • Buschman H, van der Laarse W, Stienen G, Elzinga G (1996) Force-dependent and force-independent heat production in single slow- and fast-twitch muscle fibres from Xenopus laevis. J Physiol 496:503–519

    PubMed  CAS  Google Scholar 

  • Cain SM, Davies RE (1964) Rapid arrest of metabolism with melting freon. In: Chance B, Eisenhardt RH, Gibson QH, Lonberg-Holm KK (eds) Rapid mixing and sampling techniques in biochemistry. Academic Press, New York, pp 229–237

    Google Scholar 

  • Chance B, Im J, Nioka S, Kushmerick M (2006) Skeletal muscle energetics with PNMR: personal views and historic perspectives. NMR Biomed 19:904–926

    Article  PubMed  Google Scholar 

  • Cheung A, Dantzig JA, Hollingworth S, Baylor SM, Goldman YE, Mitchison TJ, Straight AF (2002) A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4:83–88

    Article  PubMed  CAS  Google Scholar 

  • Curtin NA, Woledge RC (1975) Chemical change, production of tension and energy following stretch of active muscle of frog. J Physiol 297:539–550

    Google Scholar 

  • Curtin NA, Woledge RC (1981) Effect of muscle length on energy balance in frog skeletal muscle. J Physiol 316:453–468

    PubMed  CAS  Google Scholar 

  • Ebashi S, Endo M (1968) Calcium ion and muscle contraction. Progres Biophys Mol Biol 18:123–183

    Article  CAS  Google Scholar 

  • Edman KA, Reggiani C (1984) Redistribution of sarcomere length during isometric contraction of frog muscle fibres and its relation to tension creep. J Physiol 351:169–198

    PubMed  CAS  Google Scholar 

  • Epstein M, Kuriki Y, Biltonen R, Racker E (1980) Calorimetric studies of ligand-induced modulation of calcium adenosine 5(-triphosphatase from sarcoplasmic reticulum. Biochemistry 19:5564–5568

    Article  PubMed  CAS  Google Scholar 

  • Fryer MW, Gage PW, Neering IR, Dulhunty AF, Lamb GD (1988a) Paralysis of skeletal muscle by butanedione monoxime, a chemical phosphatase. Pflugers Archiv 411:76–79

    Article  PubMed  CAS  Google Scholar 

  • Fryer MW, Neering IR, Stephenson DG (1988b) Effects of 2,3-butanedione monoxime on the contractile activation properties of fast- and slow-twitch rat muscle fibres. J Physiol 407:53–75

    PubMed  CAS  Google Scholar 

  • Gibbs CL, Gibson WR (1972) Energy production of rat soleus muscle. Am J Physiol 223:864–871

    PubMed  CAS  Google Scholar 

  • Gibbs CL, Ricchiuti NV, Mommaerts WFHM (1966) Activation heat in frog sartorius muscle. J Gen Physiol 49:517–535

    Article  PubMed  CAS  Google Scholar 

  • Gilbert C, Kretzschmar KM, Wilkie DR, Woledge RC (1971) Chemical change and energy output during muscular contraction. J Physiol 218:163–193

    PubMed  CAS  Google Scholar 

  • Gillis JM (1985) Relaxation of vertebrate skeletal muscle. A synthesis of the biochemical and physiological approaches. Biochim Biophys Acta 811:97–145

    PubMed  CAS  Google Scholar 

  • Gordon AM, Huxley AF, Julian FJ (1966a) Tension development in highly stretched vertebrate muscle fibres. J Physiol 184:143–169

    PubMed  CAS  Google Scholar 

  • Gordon AM, Huxley AF, Julian FJ (1966b) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184:170–192

    PubMed  CAS  Google Scholar 

  • Guillain F, Gingold MP, Champeil P (1982) Direct fluorescence measurements of Mg2+ binding to sarcoplasmic reticulum ATPase. J Biol Chem 257:7366–7371

    PubMed  CAS  Google Scholar 

  • Heizmann CW, Berchtold MW, Rowlerson AM (1982) Correlation of parvalbumin concentration with relaxation speed in mammalian muscles. Proc Natl Acadamy Sci USA 79:7243–7247

    Article  CAS  Google Scholar 

  • Hicks A, McComas AJ (1989) Increased sodium pump activity following repetitive stimulation of rat soleus muscles. J Physiol 414:337–349

    PubMed  CAS  Google Scholar 

  • Hill AV (1949) The heat of activation and the heat of shortening in a muscle twitch. Proc R Soc Lond. Ser B: Biol Sci 136:195–211

    CAS  Google Scholar 

  • Hodgkin AL, Horowicz P (1959) Movements of Na and K in single muscle fibres. J Physiol 145:405–432

    PubMed  CAS  Google Scholar 

  • Homsher E, Mommaerts WF, Ricchiuti NV, Wallner A (1972) Activation heat, activation metabolism and tension-related heat in frog semitendinosus muscles. J Physiol 220:601–625

    PubMed  CAS  Google Scholar 

  • Horiuti K, Higuchi H, Umazume Y, Konishi M, Okazaki O, Kurihara S (1988) Mechanism of action of 2, 3-butanedione 2-monoxime on contraction of frog skeletal muscle fibres. J Muscle Res Cell Motil 9:156–164

    Article  PubMed  CAS  Google Scholar 

  • Hou TT, Johnson JD, Rall JA (1991) Parvalbumin content and Ca2+ and Mg2+ dissociation rates correlated with changes in relaxation rate of frog muscle fibres. J Physiol 441:285–304

    PubMed  CAS  Google Scholar 

  • Hui CS, Maylie J (1991) Multiple actions of 2,3-butanedione monoxime on contractile activation in frog twitch fibres. J Physiol 442:527–549

    PubMed  CAS  Google Scholar 

  • Huxley AF, Peachey LD (1961) The maximum length for contraction in vertebrate striated muscle. J Physiol 156:150–165

    PubMed  CAS  Google Scholar 

  • Imaizumi M, Tanokura M (1990) Heat capacity and entropy changes of troponin C from bullfrog skeletal muscle induced by calcium binding. Eur J Biochem 192:275–281

    Article  PubMed  CAS  Google Scholar 

  • Julian FJ, Morgan DL (1979) Intersarcomere dynamics during fixed-end tetanic contractions of frog muscle fibres. J Physiol 293:365–378

    PubMed  CAS  Google Scholar 

  • Konishi M, Hollingworth S, Harkins AB, Baylor SM (1991) Myoplasmic calcium transients in intact frog skeletal muscle fibers monitored with the fluorescent indicator furaptra. J Gen Physiol 97:271–301

    Article  PubMed  CAS  Google Scholar 

  • Konishi M, Watanabe M (1995) Resting cytoplasmic free Ca2+ concentration in frog skeletal muscle measured with fura-2 conjugated to high molecular weight dextran. J Gen Physiol 106:1123–1150

    Article  PubMed  CAS  Google Scholar 

  • Krause KH, Milos M, Luan-Rilliet Y, Lew DP, Cox JA (1991) Thermodynamics of cation binding to rabbit skeletal muscle calsequestrin. Evidence for distinct Ca2+- and Mg2+-binding sites. J Biol Chem 266:9453–9459

    PubMed  CAS  Google Scholar 

  • Lou F, Curtin NA, Woledge RC (1997) The energetic cost of activation of white muscle fibres from the dogfish Scyliorhinus canicula. J Exp Biol 200:495–501

    PubMed  Google Scholar 

  • Lyster DJ, Stephenson DG (1995) Contractile activation and measurements of intracellular Ca2+ concentration in cane toad twitch fibres in the presence of 2,3-butanedione monoxime. Exp Physiol 80:543–560

    PubMed  CAS  Google Scholar 

  • Maylie J, Hui CS (1991) Action of 2,3-butanedione monoxime on calcium signals in frog cut twitch fibres containing antipyrylazo III. J Physiol 442:551–567

    PubMed  CAS  Google Scholar 

  • Nielsen OB, Clausen T (1997) Regulation of Na+–K+ pump activity in contracting rat muscle. J Physiol 503:571–581

    Article  PubMed  CAS  Google Scholar 

  • Nielsen OB, Harrison AP (1998) The regulation of the Na+, K+ pump in contracting skeletal muscle. Acta Physiol Scand 162:191–200

    Article  PubMed  CAS  Google Scholar 

  • Pinniger GJ, Bruton JD, Westerblad H, Ranatunga KW (2005) Effects of a myosin-II inhibitor (N-benzyl-p-toluene sulphonamide, BTS) on contractile characteristics of intact fast-twitch mammalian muscle fibres. J Muscle Res Cell Motil 26:135–141

    Article  PubMed  CAS  Google Scholar 

  • Potter JD, Gergely J (1975) The calcium and magnesium binding sites on troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J Biol Chem 250:4628–4633

    PubMed  CAS  Google Scholar 

  • Potter JD, Hsu FJ, Pownall HJ (1977) Thermodynamics of Ca2+ binding to troponin-C. J Biol Chem 252:2452–2454

    PubMed  CAS  Google Scholar 

  • Rall JA (1979) Effects of temperature on tension, tension-dependent heat, and activation heat in twitches of frog skeletal muscle. J Physiol 291:265–275

    PubMed  CAS  Google Scholar 

  • Rall JA, Schottelius BA (1973) Energetics of contraction in phasic and tonic skeletal muscles of the chicken. J Gen Physiol 62:303–323

    Article  PubMed  CAS  Google Scholar 

  • Robertson SP, Johnson JD, Potter JD (1981) The time-course of Ca2+ exchange with calmodulin, troponin, parvalbumin, and myosin in response to transient increases in Ca2+. Biophys J 34:559–569

    Article  PubMed  CAS  Google Scholar 

  • Rome LC (2006) Design and function of superfast muscles: new insights into the physiology of skeletal muscle. Ann Rev Physiol 68:193–221

    Article  CAS  Google Scholar 

  • Rome LC, Klimov AA (2000) Superfast contractions without superfast energetics: ATP usage by SR-Ca2+ pumps and crossbridges in toadfish swimbladder muscle. J Physiol 526:279–286

    Article  PubMed  CAS  Google Scholar 

  • Sandberg JA, Carlson FD (1966) The dependence of phosphorylcreatine hydrolysis during an isometric tetanus. Biochem Z 345:212–231

    CAS  Google Scholar 

  • Siegman MJ, Mooers SU, Warren TB, Warshaw DM, Ikebe M, Butler TM (1994) Comparison of the effects of 2,3-butanedione monoxime on force production, myosin light chain phosphorylation and chemical energy usage in intact and permeabilized smooth and skeletal muscles. J Muscle Res Cell Motil 15:457–472

    Article  PubMed  CAS  Google Scholar 

  • Smith ICH (1972) Energetics of activation in frog and toad muscle. J Physiol 220:583–599

    PubMed  CAS  Google Scholar 

  • Smith SJ, Woledge RC (1985) Thermodynamic analysis of calcium binding to frog parvalbumin. J Muscle Res Cell Motil 6:757–768

    Article  PubMed  CAS  Google Scholar 

  • Stienen G, Zaremba R, Elzinga G (1995) ATP utilization for calcium uptake and force production in skinned muscle fibres of Xenopus laevis. J Physiol 482:109–122

    PubMed  CAS  Google Scholar 

  • Szentesi P, Zaremba R, van Mechelen W, Stienen GJM (2001) ATP utilization for calcium uptake and force production in different types of human skeletal muscle fibres. J Physiol 531:393–403

    Article  PubMed  CAS  Google Scholar 

  • Tanokura M, Yamada K (1985) A calorimetric study of Ca2+ binding to two major isotypes of bullfrog parvalbumin. FEBS Lett 185:165–169

    Article  PubMed  CAS  Google Scholar 

  • Venosa RA (1974) Inward movement of sodium ions in resting and stimulated frog’s sartorius muscle. J Physiol 241:155–173

    PubMed  CAS  Google Scholar 

  • Verjovski-Almeida S, Silva JL (1981) Different degrees of cooperativity of the Ca2+-induced changes in fluorescence intensity of solubilized sarcoplasmic reticulum ATPase. J Biol Chem 256:2940–2944

    PubMed  CAS  Google Scholar 

  • Walsh B, Howlett RA, Stary CM, Kindig CA, Hogan MC (2006) Measurement of activation energy and oxidative phosphorylation onset kinetics in isolated muscle fibers in the absence of cross-bridge cycling. Am J Physiol 290:R1707–1713

    CAS  Google Scholar 

  • Weber A, Herz R, Reiss I (1966) Study of the kinetics of calcium transport by isolated fragmented sarcoplasmic reticulum. Biochem Z 345:329–369

    CAS  Google Scholar 

  • Wendt IR, Barclay JK (1980) Effects of dantrolene on the energetics of fast- and slow- twitch muscles of the mouse. Am J Physiol 238:C56–C61

    PubMed  CAS  Google Scholar 

  • Wendt IR, Gibbs CL (1973) Energy production of rat extensor digitorum longus muscle. Am J Physiol 224:1081–1086

    PubMed  CAS  Google Scholar 

  • Young IS, Harwood CL, Rome LC (2003) Cross-bridge blocker BTS permits direct measurement of SR Ca2+ pump ATP utilization in toadfish swimbladder muscle fibers. Am J Physiol 285:C781–C787

    CAS  Google Scholar 

  • Zhang SJ, Andersson DC, Sandstrom ME, Westerblad H, Katz A (2006) Cross bridges account for only 20% of total ATP consumption during submaximal isometric contraction in mouse fast-twitch skeletal muscle. Am J Physiol 291:C147–C154

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. School of Physiotherapy and Exercise Science, Griffith University, PMB50 Gold Coast Mail Centre, Gold Coast, QLD, 9726, Australia

    C. J. Barclay

  2. National Heart and Lung Institute, Imperial College London, London, UK

    R. C. Woledge & N. A. Curtin

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  1. C. J. Barclay
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  2. R. C. Woledge
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  3. N. A. Curtin
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Correspondence to C. J. Barclay.

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Barclay, C.J., Woledge, R.C. & Curtin, N.A. Energy turnover for Ca2+ cycling in skeletal muscle. J Muscle Res Cell Motil 28, 259–274 (2007). https://doi.org/10.1007/s10974-007-9116-7

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  • DOI: https://doi.org/10.1007/s10974-007-9116-7

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