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Cellular Processes Integrating the Metabolic Response to Exercise

Ronald A. Meyer, Jeanne M. Foley

10.1002/cphy.cp120118

Source: Supplement 29: Handbook of Physiology, Exercise: Regulation and Integration of Multiple Systems

Originally published: 1996

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 The Central Role of Adenine Nucleotides
1.1 Components of the High‐Energy Phosphate System
1.2 Phosphate Metabolites are a Linked Network
2 Approaches to Understanding Metabolic Control
2.1 Classic Enzyme Kinetics
2.2 Nonequilibrium Thermodynamics
2.3 Regulated Enzymes and the Role of Calcium
3 Determinants of Muscle Cell ATPase Rate
3.1 The Basal ATPase
3.2 The Contractile ATPase
4 Metabolite Changes During Muscle Stimulation
4.1 Methodology
4.2 The Low‐Rate, Nonfatiguing Domain
4.3 The High‐Rate, Fatiguing Domain
4.4 The Transitional Domain
5 Control of Oxidative Phosphorylation in Muscle
5.1 Kinetic Control by [ADP]
5.2 Thermodynamic Control by Cytoplasmic Phosphates
5.3 Experimental Tests of Control Models
5.4 The Importance of Muscle Aerobic Capacity
6 Control of Glycogenolysis/Glycolysis in Muscle
6.1 The Conventional View
6.2 Problems with the Conventional View
6.3 Reaction Disequilibria and Metabolite Diffusion
6.4 Enzyme Organization
7 Control of Force Generation
8 Summary and Future Directions
Figure 1. Figure 1.

Schematic illustrating the key roles of calcium and phosphate metabolites in regulating force and ATP production in skeletal muscle.
Figure 2. Figure 2.

A, Calculated changes in normalized metabolite levels as a function of high‐energy phosphate depletion assuming constant pH = 7. PCr is normalized as a fraction of the total creatine pool (TCr), adenine nucleotides as fractions of the total adenine nucleotide pool (TAN), and high‐energy phosphate (PCr + 2ATP + ADP) as a fraction of (TCr + 2TAN). [Recalculated from Connett 26.] B, Changes in ΔGATP as a function of high‐energy phosphate depletion, assuming constant pH = 7, TCr = 40 mM, TAN = 10 mM, and Pi = 0 at PCr/TCr = 1.
Figure 3. Figure 3.

A, Dependence of the net reaction rate of an enzyme‐catalyzed reaction on substrate concentration, [S], assuming classic Michaelis‐Menton kinetics with Kms = 0.5 mM, and [P] = 0. B, Dependence of net reaction rate on substrate concentration assuming Keq = 1, Kms = 0.5 mM, Kmp = 1 mM, and [P] = 1 mM. C, Dependence of net reaction rate on reaction affinity, assuming Keq = 100, Kms = 0.5 mM, Kmp = 1 mM, [S] + [P] = 10 mM.
Figure 4. Figure 4.

Schematic illustrating some important features of excitation‐contraction coupling and calcium cy cling in skeletal muscle. DHP‐R, dihy dropyridine‐sensitive voltage‐gated calcium channel; RY‐R, ryanodine‐sensitive SR calcium release channel; SERCA, sarcoplasmic/endoplasmic reticulum calcium ATPase.
Figure 5. Figure 5.

High‐energy phosphate utilization (∼P) as a function of tetanus tension–time integral in mouse soleus and EDL muscle at 20°C.

From Crow and Kushmerick 31
Figure 6. Figure 6.

A, Time course of PCr changes in rat gastrocnemius muscle during and after nonfatiguing twitch stimulation. [From Meyer 117.] B, Relationship between steady‐state PCr and oxygen consumption in rat gastrocnemius muscle during nonfatiguing stimulation. [From Meyer 117.] C, Relationship between time constant for PCr changes (τ) and muscle total creatine content. Total creatine content of rat gastrocnemius muscle was depleted by 2 or 4 weeks feeding the creatine analog, β‐guanidinopropionate. [From Meyer 118.] D, Relationship between rate constant for PCr recovery (1/τ) and muscle mitochondrial content. Mitochondrial content of rat gastrocnemius muscle was increased by endurance training (10 weeks' duration, 1 h/day on a running wheel, final mean speed 38 m/min). Mitochondrial content was decreased by chemical thyroidectomy (0.025% methiamizole in drinking water for 8 weeks).

From Paganini, Foley, and Meyer, unpublished observations
Figure 7. Figure 7.

Time course of changes in peak twitch force (A), PCr (B), ATP (C), and intracellular pH (D) during fatiguing (5 Hz) stimulation. PCr, ATP, and pH measured by 31P‐NMR as described in Meyer et al. 120.

From Paganini and Meyer, unpublished observations
Figure 8. Figure 8.

Schematic illustrating main features of mitochondrial oxidative phosphorylation.
Figure 9. Figure 9.

A, Steady‐state as a function of stimulation rate in cat soleus muscles perfused at 37°C with red cell suspension in Krebs‐Hensleit solution equilibrated with 5% CO2 (perfusate pH 7.4) and 70% CO2 (perfusate pH 6.7). Intracellular pH was 7.1 and 6.5, respectively. B, Relationship between steady‐state PCr and in cat soleus muscles during normocapnic and hypercapnic perfusion. C, Relationship between steady‐state calculated [ADP] and .

From Harkema and Meyer 65
Figure 10. Figure 10.

Parallel dose‐dependent effects of perfusion with my‐xothiazol on peak and NADH–cytochrome reductase activity in rat hindlimb muscle.

From McAllister and Terjung 112
Figure 11. Figure 11.

Schematic illustrating important control points in muscle glycogenolysis and glycolysis.
Figure 12. Figure 12.

Top, Kinetic model for the creatine kinase reaction 130. The assumed equilibrium constants for the depicted substrate binding reactions are given in mM. The rate constants kt and kr were selected so that model yielded equilibrium unidirectional fluxes of 10 mM/s for [ATP] = 10 mM, [PCr] = 36 mM, and [Cr] = 10 mM. pH was held constant at 7. ADP changes during tetani and twitches were computed by Euler's method (dt = 10 μs) assuming step changes in ATPase rate, Q. Bottom, Calculated [ADP] during tetanic and twitch contractions using the above model with high and low initial [PCr]/[Cr] ratio. Total phosphagen use was assumed to be 1.5 mM and 0.3 mM for single tetani and twitches, respectively 49,75. Solid lines are [ADP] calculated from the kinetic model, and dashed lines are [ADP] calculated from the same PCr levels assuming instantaneous equilibrium of the net creatine kinase re action.
Figure 13. Figure 13.

Calculated drop in ΔGATP at the center of a cylinder in which ATP is consumed at a constant, steady‐state rate (Q = 1 mM/s), as a function of cylinder radius, and in the presence or absence of the creatine kinase reaction at equilibrium (Keq = 1.66 × 109 M−1, pH 7). Metabolites outside the cylinder were assumed to be constant at the indicated levels. Diffusion coefficients of Pi, adenine nucleotides, and PCr and creatine were assumed to be 3 × 10−6, 1 × 10−6, and 2 × 10−6 cm2/s, respectively 125. Even over the dimensions of a large cyclindrical cell (radius 30 μm) the creatine kinase reaction virtually abolishes any radial gradient in ΔGATP.
Figure 14. Figure 14.

Relationship between intracellular pH and peak tetanic force during repetitive tetanic stimulation (open circles) and during perfusion with hypercapnic media (closed), in cat biceps brachii (top) and soleus (bottom) muscles.

From Adams et al. (1


Figure 1.

Schematic illustrating the key roles of calcium and phosphate metabolites in regulating force and ATP production in skeletal muscle.



Figure 2.

A, Calculated changes in normalized metabolite levels as a function of high‐energy phosphate depletion assuming constant pH = 7. PCr is normalized as a fraction of the total creatine pool (TCr), adenine nucleotides as fractions of the total adenine nucleotide pool (TAN), and high‐energy phosphate (PCr + 2ATP + ADP) as a fraction of (TCr + 2TAN). [Recalculated from Connett 26.] B, Changes in ΔGATP as a function of high‐energy phosphate depletion, assuming constant pH = 7, TCr = 40 mM, TAN = 10 mM, and Pi = 0 at PCr/TCr = 1.



Figure 3.

A, Dependence of the net reaction rate of an enzyme‐catalyzed reaction on substrate concentration, [S], assuming classic Michaelis‐Menton kinetics with Kms = 0.5 mM, and [P] = 0. B, Dependence of net reaction rate on substrate concentration assuming Keq = 1, Kms = 0.5 mM, Kmp = 1 mM, and [P] = 1 mM. C, Dependence of net reaction rate on reaction affinity, assuming Keq = 100, Kms = 0.5 mM, Kmp = 1 mM, [S] + [P] = 10 mM.



Figure 4.

Schematic illustrating some important features of excitation‐contraction coupling and calcium cy cling in skeletal muscle. DHP‐R, dihy dropyridine‐sensitive voltage‐gated calcium channel; RY‐R, ryanodine‐sensitive SR calcium release channel; SERCA, sarcoplasmic/endoplasmic reticulum calcium ATPase.



Figure 5.

High‐energy phosphate utilization (∼P) as a function of tetanus tension–time integral in mouse soleus and EDL muscle at 20°C.

From Crow and Kushmerick 31


Figure 6.

A, Time course of PCr changes in rat gastrocnemius muscle during and after nonfatiguing twitch stimulation. [From Meyer 117.] B, Relationship between steady‐state PCr and oxygen consumption in rat gastrocnemius muscle during nonfatiguing stimulation. [From Meyer 117.] C, Relationship between time constant for PCr changes (τ) and muscle total creatine content. Total creatine content of rat gastrocnemius muscle was depleted by 2 or 4 weeks feeding the creatine analog, β‐guanidinopropionate. [From Meyer 118.] D, Relationship between rate constant for PCr recovery (1/τ) and muscle mitochondrial content. Mitochondrial content of rat gastrocnemius muscle was increased by endurance training (10 weeks' duration, 1 h/day on a running wheel, final mean speed 38 m/min). Mitochondrial content was decreased by chemical thyroidectomy (0.025% methiamizole in drinking water for 8 weeks).

From Paganini, Foley, and Meyer, unpublished observations


Figure 7.

Time course of changes in peak twitch force (A), PCr (B), ATP (C), and intracellular pH (D) during fatiguing (5 Hz) stimulation. PCr, ATP, and pH measured by 31P‐NMR as described in Meyer et al. 120.

From Paganini and Meyer, unpublished observations


Figure 8.

Schematic illustrating main features of mitochondrial oxidative phosphorylation.



Figure 9.

A, Steady‐state as a function of stimulation rate in cat soleus muscles perfused at 37°C with red cell suspension in Krebs‐Hensleit solution equilibrated with 5% CO2 (perfusate pH 7.4) and 70% CO2 (perfusate pH 6.7). Intracellular pH was 7.1 and 6.5, respectively. B, Relationship between steady‐state PCr and in cat soleus muscles during normocapnic and hypercapnic perfusion. C, Relationship between steady‐state calculated [ADP] and .

From Harkema and Meyer 65


Figure 10.

Parallel dose‐dependent effects of perfusion with my‐xothiazol on peak and NADH–cytochrome reductase activity in rat hindlimb muscle.

From McAllister and Terjung 112


Figure 11.

Schematic illustrating important control points in muscle glycogenolysis and glycolysis.



Figure 12.

Top, Kinetic model for the creatine kinase reaction 130. The assumed equilibrium constants for the depicted substrate binding reactions are given in mM. The rate constants kt and kr were selected so that model yielded equilibrium unidirectional fluxes of 10 mM/s for [ATP] = 10 mM, [PCr] = 36 mM, and [Cr] = 10 mM. pH was held constant at 7. ADP changes during tetani and twitches were computed by Euler's method (dt = 10 μs) assuming step changes in ATPase rate, Q. Bottom, Calculated [ADP] during tetanic and twitch contractions using the above model with high and low initial [PCr]/[Cr] ratio. Total phosphagen use was assumed to be 1.5 mM and 0.3 mM for single tetani and twitches, respectively 49,75. Solid lines are [ADP] calculated from the kinetic model, and dashed lines are [ADP] calculated from the same PCr levels assuming instantaneous equilibrium of the net creatine kinase re action.



Figure 13.

Calculated drop in ΔGATP at the center of a cylinder in which ATP is consumed at a constant, steady‐state rate (Q = 1 mM/s), as a function of cylinder radius, and in the presence or absence of the creatine kinase reaction at equilibrium (Keq = 1.66 × 109 M−1, pH 7). Metabolites outside the cylinder were assumed to be constant at the indicated levels. Diffusion coefficients of Pi, adenine nucleotides, and PCr and creatine were assumed to be 3 × 10−6, 1 × 10−6, and 2 × 10−6 cm2/s, respectively 125. Even over the dimensions of a large cyclindrical cell (radius 30 μm) the creatine kinase reaction virtually abolishes any radial gradient in ΔGATP.



Figure 14.

Relationship between intracellular pH and peak tetanic force during repetitive tetanic stimulation (open circles) and during perfusion with hypercapnic media (closed), in cat biceps brachii (top) and soleus (bottom) muscles.

From Adams et al. (1
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Article Title: Cellular Processes Integrating the Metabolic Response to Exercise
 

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Ronald A. Meyer, Jeanne M. Foley. Cellular Processes Integrating the Metabolic Response to Exercise. Compr Physiol 2011, Supplement 29: Handbook of Physiology, Exercise: Regulation and Integration of Multiple Systems: 841-869. First published in print 1996. doi: 10.1002/cphy.cp120118