Comparison of crossbridge dynamics between intact and skinned myocardium from ferret right ventricles.

This study compares the crossbridge kinetics of intact and skinned preparations from ferret cardiac muscles at 20 degrees C to determine whether skinning causes any alteration in the crossbridge response to an imposed length change. A papillary or trabecular muscle was isolated from the right ventricle, the muscle length adjusted to give the maximum twitch tension (Lmax), and the preparation was subjected to Ba2+ contracture. When steady tension developed, the length of the preparation was perturbed sinusoidally in 19 discrete frequencies, ranging from 0.13 to 135 Hz, and at a small peak-to-peak amplitude (0.25% Lmax). We identified three exponential processes in the sinusodial force-response to the imposed length oscillation, and these were labeled processes B, C, and D in order of increasing speed. A slow process, A, normally present in fast-twitch skeletal muscles, is very small or absent in cardiac muscles. Process B is an exponential delay, and the muscle produces oscillatory work on the forcing apparatus; processes C and D are exponential advances in which the muscle absorbs work. The preparation was chemically skinned and activated in the presence of (mM) CaEGTA 6 (pCa 4.55), MgATP 5, magnesium propionate 1, and phosphate 1, pH 7.0, with ionic strength adjusted to 200 mM with potassium propionate. We found that the crossbridge kinetics were not altered by the skinning procedure. The apparent rate constants extracted from the sinusoidal analysis were nearly identical in Ba2+ contracture (intact preparation) and in Ca2+ activation (skinned preparation), and the Nyquist plots were similar. Because the rate constants changed sensitively with the substrate (MgATP) concentrations, we concluded that the substrate is adequately supplied during Ba2+ contracture in the intact preparation. Our study demonstrates the compatibility of results obtained from an intact and from a skinned preparation.

[1]  H. Suga,et al.  Transient tension responses of heart muscle in Ba2+ contracture to step length changes. , 1980, The American journal of physiology.

[2]  M. Kawai,et al.  Differences in the transient response of fast and slow skeletal muscle fibers. Correlations between complex modulus and myosin light chains. , 1984, Biophysical journal.

[3]  E. Marbán,et al.  Relationship between force and intracellular [Ca2+] in tetanized mammalian heart muscle , 1986, The Journal of general physiology.

[4]  H. Halvorson,et al.  Role of MgATP and MgADP in the cross-bridge kinetics in chemically skinned rabbit psoas fibers. Study of a fast exponential process (C) , 1989, Biophysical journal.

[5]  R. H. Abbott,et al.  Temperature and amplitude dependence of tension transients in glycerinated skeletal and insect fibrillar muscle. , 1977, The Journal of physiology.

[6]  G. M. Briggs,et al.  Modulation by the Thyroid State of Intracellular Calcium and Contractility in Ferret Ventricular Muscle , 1988, Circulation research.

[7]  E. Page,et al.  Brief Reviews: Magnesium in Heart Muscle , 1973 .

[8]  E. Taylor,et al.  Mechanism of adenosine triphosphate hydrolysis by actomyosin. , 1971, Biochemistry.

[9]  F. Julian,et al.  Sarcomere Length‐Tension Relations in Living Rat Papillary Muscle , 1975, Circulation research.

[10]  Measurement of rate constants for the contractile cycle of intact mammalian muscle fibers. , 1987, Biophysical journal.

[11]  E. Gorter,et al.  Muscular Contraction , 1926, Nature.

[12]  W. Hunter,et al.  Effect of isoproterenol on force transient time course and on stiffness spectra in rabbit papillary muscle in barium contracture. , 1988, Journal of molecular and cellular cardiology.

[13]  H. Shimizu,et al.  Symmetric and asymmetric processes in the mechano-chemical conversion in the cross-bridge mechanism studied by isometric tension transients. , 1984, Advances in experimental medicine and biology.

[14]  M. Kawai Head rotation or dissociation? A study of exponential rate processes in chemically skinned rabbit muscle fibers when MgATP concentration is changed. , 1978, Biophysical journal.

[15]  J. Gergely,et al.  Light chains of myosins from white, red, and cardiac muscles. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[16]  P. Poole‐Wilson Measurement of myocardial intracellular pH in pathological states. , 1978, Journal of molecular and cellular cardiology.

[17]  A. Fabiato,et al.  Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricle , 1981, The Journal of general physiology.

[18]  Machin Ke Feedback theory and its application to biological systems. , 1964 .

[19]  E. Eisenberg,et al.  The relation of muscle biochemistry to muscle physiology. , 1980, Annual review of physiology.

[20]  E. Morkin,et al.  Thyroid hormone stimulates synthesis of a cardiac myosin isozyme. Comparison of the two-two-dimensional electrophoretic patterns of the cyanogen bromide peptides of cardiac myosin heavy chains from euthyroid and thyrotoxic rabbits. , 1979, The Journal of biological chemistry.

[21]  A. J. Brady,et al.  Intrinsic Regulatory Properties of Contractility in the Myocardium , 1978, Circulation research.

[22]  J. Kentish The inhibitory effects of monovalent ions on force development in detergent‐skinned ventricular muscle from guinea‐pig. , 1984, The Journal of physiology.

[23]  T. L. Hill,et al.  Muscle contraction and free energy transduction in biological systems. , 1985, Science.

[24]  Poole-Wilson Pa Measurement of myocardial intracellular pH in pathological states. , 1978 .

[25]  D. Maughan,et al.  On the composition of the cytosol of relaxed skeletal muscle of the frog. , 1988, The American journal of physiology.

[26]  M. Kawai,et al.  Covalent cross-linking of single fibers from rabbit psoas increases oscillatory power. , 1990, Biophysical journal.

[27]  S. Ebashi,et al.  Calcium ion and muscle contraction. , 1968, Progress in biophysics and molecular biology.

[28]  A. Huxley,et al.  Proposed Mechanism of Force Generation in Striated Muscle , 1971, Nature.

[29]  E. Page,et al.  Cat heart muscle in vitro. III. The extracellular space. , 1962 .

[30]  The time-course of energy balance in an isometric tetanus , 1979, The Journal of general physiology.

[31]  P. Brandt,et al.  Two rigor states in skinned crayfish single muscle fibers , 1976, The Journal of general physiology.

[32]  G. Pollack,et al.  Sarcomere dynamics in intact cardiac muscle. , 1976, European journal of cardiology.

[33]  J W Krueger,et al.  Myocardial sarcomere dynamics during isometric contraction. , 1975, The Journal of physiology.

[34]  N. Yagi,et al.  Lateral filamentary spacing in chemically skinned murine muscles during contraction. , 1985, The Journal of physiology.

[35]  J. Rüegg,et al.  Myocardial Cross-Bridge Activity and Its Regulation by Ca++, Phosphate and Stretch , 1977 .

[36]  J. Telleria [Mechanism of muscular contraction]. , 1951, Medicina.

[37]  H. Halvorson,et al.  Two step mechanism of phosphate release and the mechanism of force generation in chemically skinned fibers of rabbit psoas muscle. , 1991, Biophysical journal.

[38]  Y. Goldman,et al.  Kinetics of the actomyosin ATPase in muscle fibers. , 1987, Annual review of physiology.

[39]  P. Heinl,et al.  Tension responses to quick length changes of glycerinated skeletal muscle fibres from the frog and tortoise , 1974, The Journal of physiology.

[40]  H. Suga,et al.  Dynamic Stiffness of Cat Heart Muscle in Ba2+‐Induced Contracting , 1978, Circulation research.

[41]  A. Huxley,et al.  Tension responses to sudden length change in stimulated frog muscle fibres near slack length , 1977, The Journal of physiology.

[42]  F. Alvarez-Leefmans,et al.  Intracellular free magnesium in frog skeletal muscle fibres measured with ion‐selective micro‐electrodes. , 1986, The Journal of physiology.

[43]  D. Maughan,et al.  Stretch and radial compression studies on relaxed skinned muscle fibers of the frog. , 1979, Biophysical journal.

[44]  D. Allen,et al.  Calcium concentration in the myoplasm of skinned ferret ventricular muscle following changes in muscle length. , 1988, The Journal of physiology.

[45]  A. Huxley Muscle structure and theories of contraction. , 1957, Progress in biophysics and biophysical chemistry.

[46]  B. Nadal-Ginard,et al.  Expression of the cardiac ventricular alpha- and beta-myosin heavy chain genes is developmentally and hormonally regulated. , 1984, The Journal of biological chemistry.

[47]  E. Haber,et al.  The heart and cardiovascular system , 1986 .

[48]  K Sagawa,et al.  Dynamic Stiffness Measured in Central Segment of Excised Rabbit Papillary Muscles During Barium Contracture , 1987, Circulation research.

[49]  D. Allen,et al.  The cellular basis of the length-tension relation in cardiac muscle. , 1985, Journal of molecular and cellular cardiology.

[50]  M. Kawai Correlation between exponential processes and cross-bridge kinetics. , 1982, Society of General Physiologists series.

[51]  N. Yagi,et al.  Cross‐bridge movement in rat cardiac muscle as a function of calcium concentration. , 1989, The Journal of physiology.