Abstract
The increase in force development in the heart with increase in end-diastolic pressure (Frank-Starling mechanism) has been ascribed to an increase in contractile responsiveness of the myofibrils to calcium. We now show that this calcium sensitization is also associated with an increase in calcium responsiveness of the myofibrillar ATPase. Thus, at submaximal Ca activation (pCa 6.0), the ATPase activity of skinned fibres from pig right ventricles is increased from 57.9±4.4% to 70.6±4.4% of the maximal Ca2+ activation of ATPase by stretching (by 15%l o). At maximal Ca2+ activation, ATPase was barely altered by stretching. The relationship between ATPase activity of skinned trabecula of pig right ventricle and ATPase-Ca2+ concentrations is shifted (by 0.1 pCa unit) to higher pCa values after a stretch-induced increase of the sarcomere length from 2.1 μm to 2.4 μm. The relationship between force and pCa was affected in a similar way by extension. This increased calcium sensitivity is, however, not associated with an alteration in the relationship between ATPase activity and force development (tension cost). In accordance with Brenner's hypothesis, we propose therefore that stretch activation of ATPase is associated with an increase in the apparent rate constant of crossbridge attachment rather than with a decrease in the apparent rate constant of crossbridge detachment.
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References
Allen DG, Kentish JC (1985) The cellular basis of the length-tension relation in cardiac muscle. J Mol Cell Cardiol 17:821–840
Allen DG, Kentish JC (1988) Calcium concentration in the myoplasm of skinned ferret ventricular muscle following changes in muscle length. J Physiol (Lond) 407:489–503B
Allen DG, Kurihara S (1982) The effect of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol (Lond) 327:79–94
Babu A, Sonnenblick E, Gulati J (1988) Molecular basis for the influence of muscle length on myocardial performance. Science 240:74–76
Barsotti RJ, Ferenczi MA (1988) Kinetics of ATP hydrolysis and tension production in skinned cardiac muscle of the guinea pig. J. -Biol Chem 263:16750–16756
Brenner B (1988) Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers. Proc Natl Acad Sci USA 85:3265–3269
Fabiato A, Fabiato F (1979) Calculator programs for computing the composition of the solutions containing multiple metal and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 75:463–505
Gordon AM, Huxley AF, Julian FJ (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol (Lond) 184:170–192
Griffiths PJ, Güth K, Kuhn HJ, Rüegg JC (1980) ATPase activity in rapidly activated skinned muscle fibres. Pflügers Arch 387:167–173
Güth K, Potter JD (1987) Effect of rigor and cycling crossbridges on the structure of troponin-C and on the calcium affinity of the calcium specific regulatory sites in skinned rabbit psoas fibers. J Biol Chem 262:13627–13635
Güth K, Wojciechowski R (1986) Perfusion cuvette for the simultaneous measurement of mechanical, optical and energetic parameters of skinned muscle fibres. Pflügers Arch 407:552–557
Hibberd MG, Jewell B (1982) Calcium- and length-dependent force production in rat ventricular muscle. J Physiol (Lond) 329: 527–540
Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Chem 7:255–318
Itoh Y, Kimura S, Suzuki T, Ohashi K, Maruyama K (1986) Native connectin from porcine cardiac muscle. J Biochem (Tokyo) 100:439–447
Kuhn HJ, Güth K, Bletz C, Rüegg JC (1985) Stretch-induced increase in calcium sensitivity of cardiac myofibrillar ATPase. Pflügers Arch 405 [suppl 2]:R14
Kushmerick MJ, Krasner B (1982) Force and ATP-ase rate in skinned skeletal muscle fibres. Fed Proc 41:2232–2237
Morano I, Arndt H, Gärtner C, Rüegg JC (1988) Skinned fibers of human atrium and ventricle: myosin isoenzymes and contractility. Circ Res 62:632–639
Rüegg JC (1988) Calcium in muscle activation. Springer, Berlin Heidelberg New York, corrected, second printing
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Kuhn, H.J., Bletz, C. & Rüegg, J.C. Stretch-induced increase in the Ca2+ sensitivity of myofibrillar ATPase activity in skinned fibres from pig ventricles. Pflugers Arch. 415, 741–746 (1990). https://doi.org/10.1007/BF02584014
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DOI: https://doi.org/10.1007/BF02584014