Energetics of muscle contraction: further trials

Abstract

Knowledge accumulated in the field of energetics of muscle contraction has been reviewed in this article. Active muscle converts chemical energy into heat and work. Therefore, measurements of heat production and mechanical work provide the framework for understanding the process of energy conversion in contraction. In the 1970s, precise comparison between energy output and the associated chemical reactions was performed. It has been found that the two do not match in several situations, resulting in an energy balance discrepancy. More recently, efforts in resolving these discrepancies in the energy balance have been made involving chemical analysis, phosphorus nuclear magnetic resonance spectroscopy, and microcalorimetry. Through reviewing the evidence from these studies, the energy balance discrepancy developed early during isometric contraction has become well understood on a quantitative basis. In this situation energy balance is established when we take into account the binding of Ca to sarcoplasmic proteins such as troponin and parvalbumin, and also the shift of cross-bridge states. On the other hand, the energy balance discrepancy observed during rapid shortening still remains to be clarified. The problem may be related to the essential mechanism of cross-bridge action.

Keywords: 31P NMR; Actomyosin; Calcium binding proteins; Calorimetry; Energy balance; MRS; Muscle heat production.

Fig. 1

Results of analysis of galvanometer deflections obtained by stimulating frog sartorius muscles for 1.2 s (90 Hz) at 0 °C. The results show the rate of heat production in blocks of 0.2 s. These represent the first three phases, viz the heat production associated respectively with a the development, b the maintenance, and c the disappearance of the mechanical response. The recovery heat is not seen because it is very slow at low temperature. Heat production given in cal/g muscle. Hill and Hartree [57]. Although the analysis involved large corrections, the results are remarkably similar to those in later studies [59, 60]

Fig. 2

Variations of work and heat (ordinate) in units of 100 ergs (10⁻⁵ J) in isotonic contractions of sartorius muscle of the frog against variations in load (abscissa). The heat represents only the heat in excess of the isometric. Fenn [84]

Fig. 3

Heat and work produced, and break-down of PCr during and following a 15-s tetanus at 0 °C. The uppermost graph represents the tension during a typical 15-s isometric tetanus. The physical (h + w) and chemical (PCr) changes are shown in a dimensionless ratio, mol/mol creatine (M/MCr, Cr = total creatine in muscle). The heat plus work (h + w) is plotted in equivalent chemical units (M/MCr) using a conversion factor of 11 kcal/mol (46 kJ/mol) (see text). Muscles (light lines) used for studying changes during contractions were placed in O₂, while muscles (heavy lines with ± 1 S.E. bars) used for studying changes during the recovery period had been treated with IAA and were placed in N₂ in order to avoid complications arising from the recovery process. Gilbert et al. [2]. Printing errors are corrected and labels added

Fig. 4

Enthalpy production (mJ/g) during rapid shortening. Unshaded, observed enthalpy (h + w); diagonal shading, explained enthalpy; dots, unexplained enthalpy (observed − explained). Columns from left to right show results for the rapid shortening period (S), post-shortening period (PS), the sum of these two (S + PS) and the period (I) of an isometric tetanus (of duration equal to that of S plus PS). Mean ± S.E. of mean. Homsher, Irving and Wallner [132]

Fig. 5

Design of experimental chambers for muscles. a Experimental chamber (7.5 mm diameter) for ³¹P NMR studies of contracting frog muscles. A single pair of frog sartorius muscles can be held in a vertical position parallel to the central glass tube by the support system constructed of Teflon, glass and epoxy resin. By these arrangements muscles can be stimulated, force produced can be recorded and the muscles can be superfused with oxygenated Ringer solution. Dawson et al. [22]. b Chamber of 25 mm diameter for ³¹P NMR studies, in which 8 pairs of semitendinosus muscles of bullfrogs can be held. The use of many muscles (average 4.4 g) greatly improved the signal intensity as is seen from the results shown in Fig. 6. Yamada and Tanokura [115]

Fig. 6

Time course of changes of metabolites after tetanic contractions of frog muscles studied by ³¹P NMR. a Recovery of frog muscles from contractions studied by using the chamber apparatus for ³¹P NMR shown in Fig. 5a. Four frog sartorius muscles were repeatedly stimulated for 25 s every 56 min and spectra accumulated into eight bins of 7 min each. The graph shows how PCr (+), P_i (×) and sugar P (Δ) varied. The ordinates show the resonance peak areas as multiples of the mean area for the β ATP peak. The right-hand scale applies to PCr. The exponential curve drawn through the PCr points has a T _1/2 of 9.1 min. Dawson, Gadian and Wilkie [22]. b The changes of PCr concentrations associated with 10-s isometric tetanus using chamber apparatus shown in Fig. 5b with sixteen dorsal heads of bullfrog semitendinosus muscles at 4 °C. Note that the time resolution is greatly improved compared to the results in a. The curve is the same exponential for P_i in c. Kawano, Tanokura and Yamada [26]. c Changes in P_i concentrations in the same experiments and muscle preparations as in b. The curve shows a single exponential fitted to the time course of the recovery of P_i (τ 37.5 min; T _1/2 26 min). Kawano, Tanokura and Yamada [26]

Fig. 7

Inorganic phosphate released (ΔP_i), and the difference between ΔP_i and −ΔPCr, plotted against the duration of contraction. Vertical bars represent ±1 S.D. The inset shows the difference between ΔP_i and −ΔPCr (ΔPi + ΔPCr) in an enlarged scale. Kawano et al. [26]

Fig. 8

Microcalorimetric titrations of TnC with Ca. Total heat produced per mol TnC against the concentration ratio of Ca (or Mg) added to TnC at pH7 and 10 °C. a Titration of Mg-free TnC with Ca; b in the presence of 0.2 mM Mg; c 1 mM Mg; d the titration with Mg. Yamada and Kometani [153]

Fig. 9

Dependence of enthalpy changes associated with Ca binding on temperature. a Rabbit TnC. a Mg-free TnC and b TnC in the presence of 1 mM Mg. Numbers attached indicate the particular site involved; 1 one of the Ca–Mg sites for which Ca binds first; 2 another Ca–Mg site for which Ca binds next; 3 and 4 Ca-specific sites. Yamada and Kometani [153]. b Bullfrog TnC. Symbols are the same as in a, except that the Mg concentration is 5 mM. Imaizumi and Tanokura [164]