The dynamic regulation of myocardial oxidative phosphorylation: Analysis of the response time of oxygen consumption

Beek, Hans van; Tian, Xuefei; Zuurbier, Coert J.; Groot, Bas de; Echteld, C.J.A. van; Eijgelshoven, M. H. J.; Hak, J. B.

doi:10.1007/978-1-4615-5653-4_21

Bioenergetics of the Cell: Quantitative Aspects 1998

DOI: 10.1007/978-1-4615-5653-4_21

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The dynamic regulation of myocardial oxidative phosphorylation: Analysis of the response time of oxygen consumption

Hans van Beek

Xuefei Tian²,

Coert J. Zuurbier

et al.

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Cited by 23 publications

(45 citation statements)

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“…Whereas anaerobic glycolysis may only produce as little as 3-7% of the total ATP under aerobic conditions in ex vivo preparations (8, 17), its contribution to cellular bioenergetics may increase significantly during ischemia and hypoxia (31). In addition, ATP from glycolysis may be used in the heart early during dynamic workload changes (7), as observed previously in skeletal muscle (24).We can measure the time course of oxygen consumption (V O 2 ) in response to pacing-induced workload steps, which reflects the transcytosolic energy signaling speeds between myofibrils and ion pumps and the mitochondria in isolated rabbit hearts to match ATP synthesis to hydrolysis (7,37,38). The mitochondrial delay time (t mito ) is sensitive to altered exogenous substrate (35) and ischemia (46).…”

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confidence: 94%

“…We can measure the time course of oxygen consumption (V O 2 ) in response to pacing-induced workload steps, which reflects the transcytosolic energy signaling speeds between myofibrils and ion pumps and the mitochondria in isolated rabbit hearts to match ATP synthesis to hydrolysis (7,37,38). The mitochondrial delay time (t mito ) is sensitive to altered exogenous substrate (35) and ischemia (46).…”

mentioning

confidence: 99%

“…Calculation of tmito. Detailed description of the techniques, including the oxygen transport model and the equations, assumptions, and correction values, is to be found elsewhere (37,38). Briefly, the venous mean response time (tv) is integrated from the time course of the venous PO2 (Pv O 2 ) during a step to and from a higher heart rate.…”

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confidence: 99%

“…ttransport is calculated from the venous O2 response times to a combination of three experimental interventions conducted in series following the heart rate steps (37). First, a small step in arterial concentration (ACS) is made by instantaneous exchange immediately above the heart of 10% of the normal oxygenated Tyrode with identical Tyrode gassed with 95% N2-5% CO2 (PO2 ϳ30 mmHg at coronary ostia) and the venous O2 response to this step is assessed.…”

mentioning

confidence: 99%

“…These steps are repeated after the treatment to assess the effects of IAA and IA on oxygen transport. The technique has been tested and compared with other techniques such as near-infrared spectroscopy, nuclear magnetic resonance (NMR) spectroscopy (7), and heat rate measurements as extensively discussed in a review (37).…”

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confidence: 99%

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Glycolytic buffering affects cardiac bioenergetic signaling and contractile reserve similar to creatine kinase

Harrison

Wijhe²,

Groot³

et al. 2003

American Journal of Physiology-Heart and Circulatory Physiology

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buffering affects cardiac bioenergetic signaling and contractile reserve similar to creatine kinase. Am J Physiol Heart Circ Physiol 285: H883-H890, 2003. First published April 24, 2003 10.1152/ajpheart.00725.2002 and glycolysis represent important energy-buffering processes in the cardiac myocyte. Although the role of compartmentalized CK in energy transfer has been investigated intensely, similar duties for intracellular glycolysis have not been demonstrated. By measuring the response time of mitochondrial oxygen consumption to dynamic workload jumps (t mito) in isolated rabbit hearts, we studied the effect of inhibiting energetic systems (CK and/or glycolysis) on transcytosolic signal transduction that couples cytosolic ATP hydrolysis to activation of oxidative phosphorylation. Tyrode-perfused hearts were exposed to 15 min of the following: 1) 0.4 mM iodoacetamide (IA; n ϭ 6) to block CK (CK activity Ͻ3% vs. control), 2) 0.3 mM iodoacetic acid (IAA; n ϭ 5) to inhibit glycolysis (GAPDH activity Ͻ3% vs. control), or 3) vehicle (control, n ϭ 7) at 37°C. Pretreatment t mito was similar across groups at 4.3 Ϯ 0.3 s (means Ϯ SE). No change in tmito was observed in control hearts; however, in IAA-and IA-treated hearts, t mito decreased by 15 Ϯ 3% and 40 Ϯ 5%, respectively (P Ͻ 0.05 vs. control), indicating quicker energy supply-demand signaling in the absence of ADP/ATP buffering by CK or glycolysis. The faster response times in IAA and IA groups were independent of the size of the workload jump, and the increase in myocardial oxygen consumption during workload steps was unaffected by CK or glycolysis blockade. Contractile function was compromised by IAA and IA treatment versus control, with contractile reserve (defined as increase in rate-pressure product during a standard heart rate jump) reduced to 80 Ϯ 8% and 80 Ϯ 10% of baseline, respectively (P Ͻ 0.05 vs. control), and significant elevations in end-diastolic pressure, suggesting raised ADP concentration. These results demonstrate that buffering of phosphate metabolites by glycolysis in the cytosol contributes appreciably to slower mitochondrial activation and may enhance contractile efficiency during increased cardiac workloads. Glycolysis may therefore play a role similar to CK in heart muscle. glycolysis; energy transduction; mitochondria; regulation of oxidative phosphorylation THE RELATIONSHIP BETWEEN CONTRACTILE function of the myocardium and myocyte bioenergetics is centered on the generation of ATP by oxidative phosphorylation, anaerobic glycolysis, and the conversion of phosphocreatine by creatine kinase (CK). The role of CK as an energy reserve and transfer system in the heart has been intensively studied (1,27,28,30,40), focusing on the functional significance of the compartmentation of CK isozymes to the mitochondria and myofibrils (39,44) and the regulators of CK flux during conditions of altered ATP synthesis or hydrolysis (22). Moreover, changes have been observed in CK activity and levels of its substrates and products in human patients sufferi...

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confidence: 94%

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confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Glycolytic buffering affects cardiac bioenergetic signaling and contractile reserve similar to creatine kinase

Harrison

Wijhe²,

Groot³

et al. 2003

American Journal of Physiology-Heart and Circulatory Physiology

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Phenomenological Definition of Response Times with Application to Metabolic Reactions

Torralba

Rodrı́guez

Montero

2003

Journal of Theoretical Biology

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Slow $$ \dot{V}{\text{O}}_{2} $$ kinetics during moderate-intensity exercise as markers of lower metabolic stability and lower exercise tolerance

et al. 2010

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An analysis of previously published data obtained by our group on patients characterized by markedly slower pulmonary VO₂ kinetics (heart transplant recipients, patients with mitochondrial myopathies, patients with McArdle disease) was carried out in order to suggest that slow VO₂ kinetics should not be considered the direct cause, but rather a marker, of impaired exercise tolerance. For a given ATP turnover rate, faster (or slower) VO₂ kinetics are associated with smaller (or greater) muscle [PCr] decreases. The latter, however, should not be taken per se responsible for the higher (or lower) exercise tolerance, but should be considered within the general concept of "metabolic stability". Good muscle metabolic stability at a given ATP turnover rate (~power output) is associated with relatively smaller decreases, compared to rest, in [PCr] and in the Gibbs free energy of ATP hydrolysis, as well as with relatively smaller increases in [Pi], [ADP(free)], [AMP(free)], and [IMP(free)], metabolites directly related to fatigue. Disturbances in muscle metabolic stability can affect muscle function in various ways, whereas good metabolic stability is associated with less fatigue and higher exercise tolerance. Smaller [PCr] decreases, however, are strictly associated with a faster VO₂ kinetics. Thus, faster VO₂ kinetics may simply be an "epiphenomenon" of a relatively higher metabolic stability, which would then represent the relevant variable in terms of fatigue and exercise tolerance.

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The dynamic regulation of myocardial oxidative phosphorylation: Analysis of the response time of oxygen consumption

Cited by 23 publications

References 77 publications

Glycolytic buffering affects cardiac bioenergetic signaling and contractile reserve similar to creatine kinase

Glycolytic buffering affects cardiac bioenergetic signaling and contractile reserve similar to creatine kinase

Phenomenological Definition of Response Times with Application to Metabolic Reactions

Slow $$ \dot{V}{\text{O}}_{2} $$ kinetics during moderate-intensity exercise as markers of lower metabolic stability and lower exercise tolerance

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