Frog ventricular cardiac muscle has structural features which set it apart from frog and mammalian skeletal muscle and mammalian cardiac muscle. In describing these differences, our attention focused chiefly on the distribution of cellular membranes. Abundant inter cellular clefts, the absence of tranverse tubules, and the paucity of sarcotubules, together with exceedingly small cell diameters (less than 5 p), support the suggestion that the mechanism of excitation-contraction coupling differs in these muscle cells from that now thought to be characteristic of striated muscle such as skeletal muscle and mammalian cardiac muscle. These structural dissimilarities also imply that the mechanism of relaxation in frog ventricular muscle differs from that considered typical of other striated muscles. Additional ultrastructural features of frog ventricular heart muscle include spherical electron-opaque bodies on thin filaments, inconstantly present, forming a rank across the I band about 150 mgt from the Z line, and membrane-bounded dense granules resembling neurosecretory granules. The functional significance of these features is not yet clear.In frog skeletal muscle, tubular membranebounded spaces, continuous with the interstitial space, penetrate the muscle cell transversely at the level of the Z lines of the myofibrils lying in register with one another. The continuity of the membranes of this transverse tubular system with the cell membrane and of its lumen with the interstitial space of muscle has been clearly demonstrated by Huxley (1) using ferritin.Mammalian heart muscle appears also to possess a transverse tubular system penetrating the muscle cells and having continuities with the cell membrane and interstitial space (2, 3). Rayns et al. (4), using a freeze-etching technique, observed the portals of these transverse tubules on the surface of the cell membrane. The probable role of this internal membrane system in the inward spread of the excitatory signal to the contractile sites in the myofibrils has been elegantly demonstrated by Huxley and Taylor (5) who used microelectrodes to achieve local depolarization of the cell membrane.From these observations and the ones on the role of calcium in the activation of the contractile mechanism (6, 7), a concept of excitation-contraction coupling has emerged which states that the effects of excitation are borne inward across the muscle fiber by the transverse tubular system releasing calcium ion from the sarcoplasmic reticulum surrounding the myofibrils and thereby activating the contractile elements (8).In frog heart muscle, however, Niedergerke 99 on May 12, 2018 jcb.rupress.org Downloaded from
An electron microscopic study of rabbit and human myocardium provides further evidence of the existence of two distinct components of the sarcoplasmic reticulum. A thin-walled tubular system (termed longitudinal system) is arranged in anastomosing channels sursurrounding each sarcomere and has transverse and possibly also longitudinal connections with the tubules of adjacent sarcomeres. A thick-walled tubular system traverses the myofiber transversely at the level of the Z lines of the myofibrils. The structure of these tubules very closely resembles that of deep sarcolemmal invaginations. Indeed, the membranes of the tubules appear to be continuous with the sarcolemma in favorable sections so that there seems to be an extension of the cell membrane and extracellular fluid to all depths of the myocardial fiber. Certain physiologic data which support this concept are discussed. The calculations of A. V. Hill comparing the kinetics of diffusion and the time-distance relationships between excitation and activation in frog sartorius muscle are reconsidered for cardiac muscle.After Bennett and Porter's first electron microscopic observations of the sarcoplasmic reticulum in the breast muscle of the domestic fowl (I), Porter and Palade presented detailed descriptions of this subcellular structure in different types of striated muscle (2). These findings provided a structural basis for consideration of the mechanisms of excitation-contraction coupling in muscle.Using a micropipette electrode to achieve local depolarization of the cell membrane, Huxley and Taylor (3) demonstrated transverse, two-dimensional conduction of excitation toward the central axis of an isolated intact fiber of frog striated muscle. The geometry of excitation and spread indicated very strongly that conduction inward took place along some structure in the plane of the Z lines of the myofibrils lying in register with one another. This conclusion conformed with an earlier prediction by A. V. Hill (4), based on consideration of the kinetics of diffusion and the time-distance relationships between excitation and activation in frog sartorius muscle. Hill proposed that, while excitation undoubtedly occurred at the cell surface, diffusion was far too slow a means of bearing the impulse into the interior of the fiber. He concluded that a process, not a substance, must carry the excitation inward.The electron microscopic observations of Porter and Palade (2) suggested the possible role of transversely oriented elements of the sarcoplasmic reticulum in excitation-contraction coupling.
In isolated perfused dog hearts, myocardial concentrations of creatine phosphate (CrP) and adenosine triphosphate (ATP) decreased following a 45-min period of anoxia. After partial resuscitation by perfusion of oxygenated blood for 30 min, CrP had risen again to approximately control values but ATP concentration had fallen lower. Increased concentrations of deaminated derivatives of ATP, chiefly inosine, were found in the myocardium and in the perfusion effluent after anoxia. The myocardial inosine was still elevated after resuscitation. We conclude that the dynamic equilibrium involving breakdown and resynthesis of ATP through deamination and reamination is disturbed by periods of anoxia as carried out in these experiments and, in addition, inosine is lost by diffusion into extracellular compartments.
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