The effect of myoglobin-facilitated oxygen transport on the basal metabolism of papillary muscle

Loiselle, Denis S.

doi:10.1016/s0006-3495(87)83418-5

Cited by 16 publications

(21 citation statements)

References 22 publications

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“…Our papillary muscles are about 0.4 to 1.0 mm 2 in cross-sectional areas and are not hypoxic (for a recent calculation, see [56]), so the depression of metabolism is certainly not brought about by the presence of an anoxic core (see also Loiselle [54,55]). To us, the most probable answer is that in isolated papillary muscles, where there is no flow through the microcirculation, we are dealing with the effect of an inhibitory endothelial factor [227]-an idea currently being tested.…”

Section: Modifiers Of Basal Metabolismmentioning

confidence: 92%

“…Many mathematical simulations have been developed to allow the calculation of critical diameters (for a review see [53], but explicit calculations are provided in [54][55][56]). In general, even papillary preparations obtained from mice, which have a very high basal metabolism (ϳ50 mW g Ϫ1 , see section III), will not be diffusion limited if the CSA is kept below 0.50 mm 2 .…”

Section: (I) Whole Heartsmentioning

confidence: 99%

“…A tempting interpretation is that larger papillary muscles are oxygen-starved in vitro and develop an anoxic core. Mathematical models of oxygen diffusion into cylindrical cardiac preparations, whether including [55] or ignoring [54] the improvement of oxygen-carrying capacity conferred by the presence of myoglobin, rule out this possibility. The change of radius and consequent diminution of a previous anoxic core, conferred by stretches of even improbable extent, is just too small to explain the increases of metabolic rate observed experimentally.…”

Section: Modifiers Of Basal Metabolismmentioning

confidence: 99%

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Cardiac Basal Metabolism.

Gibbs

Loiselle²

2001

JJP

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The cardiac basal metabolism is the rate of energy expenditure of the quiescent myocardium. It is also called the resting metabolism or the arrested heart metabolism. It has been measured in numerous ways, and in vivo there is good evidence that it accounts for about 1/5 to 1/3 of the total energy flux. The difficulty arises, however, when the heart is stopped because the magnitude of the basal metabolism depends, as blood viscosity, on how and under what physiological condition it is measured. It is possible for the in vivo basal value to fall to less than 1/5 of its original value without cellular damage or to increase to values 5 times greater than its probable in vivo magnitude (i.e., to rise to values in excess of the energy flux of the normally beating heart) by altering the composition of the perfusion medium. We have written on this subject several times [1][2][3], but believe that developments in knowledge now make it possible for us to speculate in a more informed manner. Since several million openheart operations are performed on arrested hearts worldwide each year, it would seem imperative that we understand the cellular mechanisms that can change the magnitude of basal metabolism.A. V. Hill [4] has pointed out that in examining physiological activities, it is necessary to assume a baseline from which some quantity or rate can be measured. If the energy flux produced by the beating heart were very large compared with the energy flux of the arrested heart, baseline ambiguity would be relatively unimportant. But this is not so in regard to the heart; its basal metabolism is high. Within a species, the basal metabolism of cardiac tissue is several-fold higher than the resting metabolism of skeletal muscle and is an order of magnitude greater than the resting metabolism of amphibian skeletal muscle.Species differences are clearly evident in the magnitude of cardiac basal metabolism, and we believe that the major reason for these differences relates to the leakiness of cell membranes, such as those of the sarcolemma and sarcoplasmic reticulum and those of Japanese Journal of Physiology, 51, 399-426, 2001 Key words: whole hearts, isolated preparations, biochemical contributors, modifiers, species difference, temperature, substrate, hypoxia. Abstract:We endeavor to show that the metabolism of the nonbeating heart can vary over an extreme range: from values approximating those measured in the beating heart to values of only a small fraction of normal-perhaps mimicking the situation of nonflow arrest during cardiac bypass surgery. We discuss some of the technical issues that make it difficult to establish the magnitude of basal metabolism in vivo. We consider some of the likely contributors to its magnitude and point out that the biochemical reasons for a sizable fraction of the heart's basal ATP usage remain unresolved. We consider many of the physiological factors that can alter the basal metabolic rate, stressing the importance of substrate supply. We point out that the protective effect of hypothermia ...

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Section: Modifiers Of Basal Metabolismmentioning

confidence: 92%

Section: (I) Whole Heartsmentioning

confidence: 99%

Section: Modifiers Of Basal Metabolismmentioning

confidence: 99%

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Cardiac Basal Metabolism.

Gibbs

Loiselle²

2001

JJP

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“…32 Oxygen diffusing from a superfusate into excised tissue will continuously decrease in concentration because ongoing consumption acts as a sink. 33 This makes it difficult in superfused tissue to estimate a critical O 2 level at which uncoupling develops. Thus, uncoupling was observed in ventricular tissue superfused with solutions containing up to 40 mm Hg of oxygen by Woijtzak 14 who qualitatively demonstrated for the first time cell-to-cell uncoupling in hypoxic myocardium.…”

Section: Changes In Intracellular Longitudinal Resistancementioning

confidence: 99%

Effect of oxygen withdrawal on active and passive electrical properties of arterially perfused rabbit ventricular muscle.

Riegger

Alperovich

Kléber

1989

Circulation Research

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Oxygen withdrawal from myocardial cells leads to changes of the transmembrane action potential (mainly action potential shortening), to cellular uncoupling, and to changes of vascular permeability. This study was aimed at the simultaneous measurement of electrical activity and passive electrical properties (extracellular and intracellular longitudinal resistance) in arterially perfused rabbit papillary muscles under different conditions of changed oxygen supply. These included 1) complete anoxia (erythrocyte-free perfusate), 2) hypoxia (Po 2 between 23-28 mm Hg, erythrocytes present) in the presence and absence of glucose, and 3) normoxia with erythrocyte-free perfusate. Similarly to myocardial ischemia, rapid cellular uncoupling occurred only after an initial stable period of approximately 17 minutes, and it required complete anoxia. The marked shortening of the action potential developed before cellular uncoupling. In six out of eight experiments, the fibers were inexcitable when uncoupling started. In severe hypoxia, no significant change of internal longitudinal resistance was observed over 35-40 minutes. The time course of the extracellular longitudinal resistance was different from the change in intracellular resistance: A marked decrease occurred almost immediately after the onset of oxygen withdrawal. This decrease was followed by a small increase in conduction velocity, which was most likely due to a change in the interstitial compartment (edema). It was observed during anoxic as well as during hypoxic perfusion. We conclude that 1) cellular uncoupling in arterially perfused tissue requires almost complete oxygen lack and occurs with a delay of more than 10 minutes, 2) marked action potential shortening precedes uncoupling, and therefore can not simply be attributed to an increase in free, intracellular calcium, and 3) vascular endothelial function is more sensitive to oxygen withdrawal than the myocyte. (Circulation Research 1989;64:532-541) R emoval of the oxygen supply from ventricular myocardium leads to rapid changes of electrical activity 1 and to the early development of malignant ventricular arrhythmias.2 Two experimental models are widely used for investigation of metabolic and electrical changes associated with inadequate myocardial oxygen supply. These include the production of 1) myocardial anoxia or hypoxia by decreasing the oxygen content of the coronary perfusate, or 2) myocardial ischemia by the arrest of coronary flow. The essential difference between these two conditions is the complete absence of extracellular washout in the case of myocardial ischemia. This causes products of ischFrom the Department of Physiology, University of Berne, Beme, Switzerland.Supported by the Swiss National Science Foundation (Grant 3.903.0-85 to A.G.K.) and the Swiss Foundation of Cardiology.Address for correspondence: Andrt G. Kteber, MD, Department of Physiology, University of Beme, Bflhlplatz 5, CH-3012, Berne, Switzerland.Received March 31, 1988; accepted August 18, 1988. emic metabolism (e.g., lact...

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“…Here less agreement is found in the literature as to what extent the flux of oxymyoglobin contributes to the overall oxygen transport within the cell. Experimental (3,4) and theoretical (5,6) studies yielded contradictory results. Quantitative statements so far were derived only from model calculations.…”

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confidence: 99%

Diffusivity of myoglobin in intact skeletal muscle cells.

Jürgens

Peters

Gros

1994

Proc. Natl. Acad. Sci. U.S.A.

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We report a method that allows us to determine the diffusion coefficient of native myoglobin in intact and mechanically unaffected red muscle fibers. The method is based on an optical recording of intracellular diffusion of metmyoglobin, which is produced inside the cells by photooxidation of oxymyoglobin with a UV light pulse. We find a myoglobin diffusivity of 1.2 x 10-7 cm2/s (22C), which is only 1/10th of the value measured in very dilute myoglobin solutions and 1/5th of the value obtained from measurements in solutions of myoglobin at 18 g/dl. The latter value often has been used in model calculations of oxygen transport to tissue incorporating myoglobin-facilitated oxygen diffusion. Recalculating facilitated diffusion with the value obtained by us implies that its contribution to total intracellular oxygen transport is of minor importance. Furthermore, it shows that sterical hindrance to myoglobin diffusion is dominated by the muscle-cell architecture rather than by the overall protein concentration of the muscle fiber.It is widely accepted that myoglobin serves as an oxygen buffer during temporary deficits in oxygen supply-for instance, as a long-term reservoir during dives of aquatic mammals, in which it occurs in concentrations up to 5 mmol/kg of muscle (1), or as a short-term oxygen store in times of restricted blood perfusion in the beating heart or exercising skeletal muscle of land mammals (2), in which it is found in concentrations up to 0.5 mmol/kg of muscle (1). Another potential role of myoglobin is that it enhances intracellular oxygen diffusion in red skeletal muscle cells by loading oxygen at sites where the Po2 is high enough to saturate the hemoprotein and releasing the oxygen according to its oxygen-binding properties at sites with low Po2. Here less agreement is found in the literature as to what extent the flux of oxymyoglobin contributes to the overall oxygen transport within the cell. Experimental (3, 4) and theoretical (5, 6) studies yielded contradictory results. Quantitative statements so far were derived only from model calculations. Such results strongly depend on the value that is used for the mobility of myoglobin inside the muscle cell. Since the actual value of the intracellular diffusion coefficient of native myoglobin (DMb) has not been determined so far in mammalian skeletal muscle cells, a value obtained from measurements in concentrated (18 g/dl) myoglobin solutions has been used instead.In general, only little is known about the cytoplasmic mobilities ofproteins. Furthermore, the few data available so far for the intracellular diffusion coefficients of proteins were all obtained in artificially altered cells-e.g., in skinned muscle fibers, from injection of labeled molecules into cells, or from fused cells.We have now developed a method that allows us to measure diffusivities of intracellular hemoproteins without mechanically affecting the cells at all. The method is described, and a result is presented for the intracellular DMb in intact cells of rat diaphragm m...

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The effect of myoglobin-facilitated oxygen transport on the basal metabolism of papillary muscle

Cited by 16 publications

References 22 publications

Cardiac Basal Metabolism.

Cardiac Basal Metabolism.

Effect of oxygen withdrawal on active and passive electrical properties of arterially perfused rabbit ventricular muscle.

Diffusivity of myoglobin in intact skeletal muscle cells.

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