Regulation of oxygen consumption in fast- and slow-twitch muscle

Kushmerick, Martin J.; Meyer, Ronald A.; Brown, Truman R.

doi:10.1152/ajpcell.1992.263.3.c598

Cited by 222 publications

(187 citation statements)

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“…In contrast, in slow-twitch oxidative fibers (which dominate the soleus muscle), neither ADP nor Pi seems to be of any particular regulatory significance -a situation rather reminiscent of the heart of large mammals (5) including humans (23) and in agreement with those few animal studies that have examined this issue in slow-twitch muscle noninvasively (24). In earlier studies (19,21,22), the coupling patterns between ATP-demand and ATP-supply pathways in cardiac and slow-twitch muscles were described as tighter than in fast-twitch muscles because large changes in ATP turnover rates could be sustained with modest (or immeasurable) changes in these key high energy phosphate metabolites.…”

Section: Regulation Of Human Muscle Metabolism During Worksupporting

confidence: 60%

Two research paths for probing the roles of oxygen in metabolic regulation

Hochachka

1999

Braz J Med Biol Res

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Tissues such as skeletal and cardiac muscles must sustain very largescale changes in ATP turnover rate during equally large changes in work. In many skeletal muscles these changes can exceed 100-fold. Examination of a number of cell and whole-organism level systems identifies ATP concentration as a key parameter of the interior milieu that is nearly universally homeostatic ; it is common to observe no change in ATP concentration even while change in its turnover rate can increase or decrease by two orders of magnitude or more. A large number of other intermediates of cellular metabolism are also regulated within narrow concentration ranges, but none seemingly as precisely as is [ATP]. In fact, the only other metabolite in aerobic energy metabolism that is seemingly as homeostatic is oxygen -at least in working muscles where myoglobin serves to buffer oxygen concentrations at stable and constant values at work rates up to the aerobic maximum. In contrast to intracellular oxygen concentration, a 1:1 relationship between oxygen delivery and metabolic rate is observed over biologically realistic and large-magnitude changes in work. The central regulatory question is how the oxygen delivery signal is transmitted to the intracellular metabolic machinery. Traditional explanations assume diffusion as the dominant mechanism, while proponents of an ultrastructurally dominated view of the cell assume an intracellular perfusion system to account for the data which have been most perplexing to metabolic biochemistry so far: the striking lack of correlation between changes in pathway reaction rates and changes in concentrations of pathway substrates, including oxygen and pathway intermediates.

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Section: Regulation Of Human Muscle Metabolism During Worksupporting

confidence: 60%

Two research paths for probing the roles of oxygen in metabolic regulation

Hochachka

1999

Braz J Med Biol Res

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“…However, similar work carried out on isolated hearts showed that a large increase in the rate of oxygen consumption could be seen even at decreasing cytoplasmic ADP levels [l-51. Kushmerick et al have shown very different metabolic responses of fast-twitch and low-twitch skeletal muscles to increased frequency of stimulation and recovery after exercise [6]. Only in fast-twitch, glycolytic muscles, where mitochondria are activated only at the step of metabolic recovery after exercise and participate mostly in the recovery of high levels of phosphocreatine, could the results be explained by feedback control of respiration by ADP concentration according to a Michaelis-Menten relationship, and the authors concluded that the mechanisms of control of cellular respiration are quantitatively and qualitatively different in fast-twitch and slow-twitch skeletal muscle 161.…”

Section: Discussionmentioning

confidence: 99%

Striking Differences Between the Kinetics of Regulation of Respiration by ADP in Slow‐Twitch and Fast‐Twitch Muscles In Vivo

Кузнецов

Tiivel

Sikk

et al. 1996

European Journal of Biochemistry

178

209

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The kinetics of in vivo regulation of mitochondrial respiration by ADP was studied in rat heart, slowtwitch skeletal muscle (soleus) and fast-twitch skeletal muscle (gastrocnemius, plantaris, quadriceps and tibialis anterior) by means of saponin-skinned fibres. Mitochondria1 respiratory parameters were determined in the absence and presence of creatine (20 mM), and the effect of proteolytic enzymes (trypsin, chymotrypsin or elastase) on these parameters was investigated in detail. Chem. 270, 19921 -199291, who studied muscle fibres from normal and transgenic mice, that the kinetics of respiration regulation in muscle cells is tissue specific. We found that in rat cardiac and soleus muscle fibres the apparent K,,, for respiration regulation was 300-400 pM and decreased to 50-80 pM in the presence of creatine. In contrast, in skinned fibres from gastrocnemius, plantaris, tibialis anterior and quadriceps muscles, this value was initially very low, 10-20 pM, i.e. the same as that is in isolated muscle mitochondria, and the effect of creatine was not observable under these experimental conditions. Treatment of the fibres with trypsin, chymotrypsin or elastase (0.125 pg/ml) for 15 min decreased the apparent K,,, for ADP in cardiac and soleus muscle fibres to 40-98 pM without significant alteration of V,,,, or the intactness of outer mitochondrial membrane, as assessed by the cytochrome c test. In fibres from gastrocnemius, trypsin increased the apparent K,,, for ADP transiently. The effects of trypsin and chymotrypsin were studied in detail and found to be concentration dependent and time dependent. The effects were characterised by saturation phenomenon with respect to the proteolytic enzyme concentration, saturation being observed above 1 pM enzyme. These results are taken to show that in cardiac and slow-twitch skeletal muscle, the permeability of the outer mitochondrial membrane to adenine nucleotides is low and controlled by a cytoplasmic protein that is sensitive to trypsin and chymotrypsin. This protein may participate in feedback signal transduction by a mechanism of vectorial-ligand conduction. This protein factor is not expressed in fasttwitch skeletal muscle, in which cellular mechanism of regulation of respiration is probably very different from that of slow-twitch muscles.Keywords: heart; skeletal muscle; respiration ; regulation; adenine nucleotide.The cellular mechanism of regulation of respiration in vivo is still unknown. The conventional explanation that the rate of respiration of mitochondria in intact cells is governed by the cytoplasmic ADP concentration according to a simple Michaelis-Menten type relationship is in disagreement with many experimental data [l-51. First, it has been shown in numerous experiments on isolated hearts that the increases in workload and oxygen consumption are usually observed at stable, low and sometimes even decreasing steady-state ADP levels [I -51. Second, Kushmerick et al. have found that in slow-twitch skeletal muscle, an increase of frequency of stimulation does...

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“…On the other hand all fibres may be recruited at the start of exercise, however there may be a progressive increase over time in the neural stimulation of the type II fibres. As type II muscle fibres are less efficient than type I muscle fibres and posses an 18% lower phosphate produced to oxygen consumed ratio (P:O 2 ratio), 33,34 recruitment of these fibres would result in more oxygen consumption when required to maintain a given work rate. No correlation existed between the magnitude of the relative SC and the percentage of type IIx muscle fibres for the either the Tr or the RA groups, or when both groups were combined.…”

Section: Slow Component Of V á O 2 Kineticsmentioning

confidence: 99%

Slow component of V̇O2 kinetics: the effect of training status, fibre type, UCP3 mRNA and citrate synthase activity

et al. 2002

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OBJECTIVE:In healthy individuals performing constant-load exercise at intensities above the lactate threshold a secondary rise in pulmonary oxygen uptake (V O 2 ) occurs. V O 2 reaches a maximum and exhaustion rapidly prevails for a range of work rates lower than the maximal work rate achieved during a conventional rapid-incremental test. This phenomenon is called the slow component (SC) of V O 2 kinetics and represents an increase in V O 2 without an increase in work rate. Although still under debate, the magnitude of the SC is believed to be associated with the percentage of type II muscle fibres and their recruitment. In this study we investigated the relationship between the magnitude of the relative SC, citrate synthase activity, UCP2 and UCP3 mRNA levels and muscle fibre composition in both endurance-trained and recreationally active subjects. METHOD: The magnitude of the relative SC was measured in 12 endurance-trained (Tr) and 15 recreationally active (RA) male subjects. The magnitude of the relative SC was determined as the difference between the end-exercise V O 2 and 3 min V O 2 divided by the difference between end-exercise V O 2 and baseline V O 2 . UCP2 and UCP3 mRNA expression in the vastus lateralis was measured by RT-PCR with b-actin mRNA used as an internal control. These values were also normalized against cytochromeb mRNA to control for training induced changes in mitochondria when comparing the Tr and RA groups. Type I, IIa and IIx skeletal muscle fibre composition was determined using a routine myosin ATPase histochemical staining technique. Citrate synthase (CS) activity was measured using spectrophotometric detection. RESULTS:The magnitude of the relative SC of the Tr group had the highest correlation with citrate synthase activity (r ¼ 7 0.90, P < 0.001) and that of the RA group with V O 2 peak (r ¼ 7 0.68, P < 0.01). For the Tr group other correlations with the magnitude of the relative SC included UCP3 mRNA levels (r ¼ 0.69, P < 0.05) and the percentage of type I fibres (r ¼ 7 0.58, P < 0.05), while for the RA group they included UCP3 mRNA (r ¼ 0.58, P < 0.05) and the percentage of type IIa muscle fibres (r ¼ 0.59, P < 0.05). The Tr subjects had a lower relative SC (P ¼ 0.04) and a lower expression of UCP2 (P ¼ 0.04), and UCP3 mRNA (P ¼ 0.01) than the RA subjects. When the groups were combined the magnitude of the relative SC correlated with UCP3 mRNA (r ¼ 0.70, P < 0.01), percentage of type IIa muscle fibres (r ¼ 0.60, P < 0.01) and V O 2 peak (r ¼ 7 0.73, P < 0.01). Additionally UCP3 mRNA correlated with the percentage of type IIa muscle fibres (r ¼ 0.63, P < 0.001). CONCLUSION: Citrate synthase activity and V O 2 peak are indicators of aerobic fitness. The high negative correlations between the magnitude of the relative SC and citrate synthase activity and V O 2 peak, of the Tr and RA subjects, respectively, suggests that the magnitude of the relative SC is inversely correlated with aerobic fitness. Additionally the correlations between UCP3 mRNA and the magnitude of the relative SC...

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Regulation of oxygen consumption in fast- and slow-twitch muscle

Cited by 222 publications

References 4 publications

Two research paths for probing the roles of oxygen in metabolic regulation

Two research paths for probing the roles of oxygen in metabolic regulation

Striking Differences Between the Kinetics of Regulation of Respiration by ADP in Slow‐Twitch and Fast‐Twitch Muscles In Vivo

Slow component of V̇O2 kinetics: the effect of training status, fibre type, UCP3 mRNA and citrate synthase activity

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