Heat produced by rabbit papillary muscle during anoxia and reoxygenation.

Abstract

Resting heat rate was measured in superfused rabbit papillary muscles at 20°C during 40 minutes of anoxia and subsequent reoxygenation. To reveal the nature of the reactions underlying energy output under such conditions, the data obtained were compared with values predicted from data on chemical change. Before and after the anoxic period, muscles were stimulated at 0.2 Hz, during which time the contraction-related heat rate was measured. During anoxia, muscles were kept at rest or stimulated at 1 Hz. Stimulation was switched off intermittently to determine resting heat rate. Before anoxia, resting heat rate was 8.7+±1.1 (mean+SEM) mW g dry wt-'. During anoxia, it decreased to 38% and 50%1 of the preanoxic level in resting and stimulated muscles, respectively (P<.05). In resting muscles, heat rate increased with reoxygenation in approximately 10 to 15 minutes to 1.3 times the preanoxic level, whereas this was 3.7 times in stimulated muscles. Resting heat rate returned within 65 (resting muscles) or 150 (stimulated muscles) minutes to the baseline. The ratio of force-and contraction-related heat rate, ie, the economy of contraction, was not different before and after anoxia. We estimated that the heat produced by muscles during anoxia was not different from the heat to be expected from the hydrolysis of creatine phosphate, the breakdown of nucleotides, and the formation of lactate. The overshoot in resting heat during reoxygenation of resting muscles could be accounted for by the resynthesis of the energy store. The much larger overshoot in resting heat of stimulated muscles was due to the contracture. The finding that the economy of contraction was not altered by anoxia and reoxygenation suggests that both sarcoplasmic reticulum Ca2'-ATPase and myofibrillar ATPase are depressed by anoxia and that the enhancement of cytosolic calcium transients with reoxygenation, reported in other studies on papillary muscle, results from reduced binding of calcium rather than from enhanced release. (Circ Res. 1993;73:1177-1187 KEY WORDs * heat rate * stunning * anoxia * reoxygenation * heart T he leading event in the cascade of cellular responses in heart muscles after anoxia or reoxygenation is energetic in nature. However, rather few direct measurements have been reported on changes in energy output of the myocardium with anoxia and reoxygenation. In the present study, we measured the effects of anoxia and reoxygenation on heat production of isolated isometric cardiac muscle. We used a flow-through chamber, similar to the one described by Daut and Elzinga1 for trabeculas, built to accommodate papillary muscles. The latter preparation was preferred to be continuous with earlier work2-4 reporting data from that preparation on isometric force production, nucleotide composition, phosphocreatine (PCr), and lactate during anoxia and reoxygenation.This information was needed for the present work to explain the changes in heat output found with anoxia and reoxygenation.The following specific questions were pursued: (1) What is the ti...

Uncoupled ATPase Activity and Heat Production by the Sarcoplasmic Reticulum Ca2+-ATPase

“…ATP is needed for several cellular functions, and during anoxia the cell has to adapt to a lower consumption of ATP in order to survive. A decrease in the heat production rate is one of the earliest events noted in anoxia (51)(52)(53). Not only will this decrease the consumption of ATP, but a drop in cell temperature promotes a simultaneous decrease in the metabolic activity and ATP demand of the cell.…”

Mechanical Determinants of Myocardial Oxygen Consumption

“…It has become apparent that contractile strength can be enhanced by ejection and that this is accompanied by prolongation of the ejection phase and concomitant acceleration of relaxation, an effect noted many years ago in isolated cardiac strips by Elzinga and Westerhof (1981). There are therefore some questions being raised about the validity of the model at the present time, even though it continues to be widely used in both experimental and clinical studies to quantify contractility.…”

“…There is considerable complexity in cardiac basal metabolism and experimentally it is possible to move its magnitude through a 20-fold range (Gibbs & Kotsanas 1986). There are certainly species differences in magnitude (Loiselle & Gibbs 1979;Daut & Elzinga 1989) and in perfused hearts the exact magnitude of this component depends upon perfusion pressure and flow rate (Lochner et al 1968), the activity of the heart prior to rest (Lochner et al 1968;Dietrich & Elzinga 1993), substrate availability (Chapman & Gibbs 1974), type of cardioplegic agents (Lochner et al 1968) and hyperosmolality .…”

“…It would be fair comment to say that over the years since the model was first proposed it has been necessary to admit that under a number of physiological conditions the ESPVR is not always linear and does demonstrate some sensitivity to both afterload magnitude and to contractility (Burkhoff et al 1987b;Spratt et al 1987;Kass et al 1989;Burkhoff et al 1993;Noda et al 1993). It has become apparent that contractile strength can be enhanced by ejection and that this is accompanied by prolongation of the ejection phase and concomitant acceleration of relaxation, an effect noted many years ago in isolated cardiac strips by Elzinga and Westerhof (1981). There are therefore some questions being raised about the validity of the model at the present time, even though it continues to be widely used in both experimental and clinical studies to quantify contractility.…”

Resting metabolism of mouse papillary muscle

“…Papillary muscles are composed of ventricular myocytes aligned along the long axis of the muscle, making them ideal for measurement of ventricular muscle force generation, work output and energy expenditure [3,4,9,13,18]. The only source of O 2 for an isolated muscle preparation is diffusive supply from the muscle surface.…”