On–off asymmetries in oxygen consumption kinetics of singleXenopus laevisskeletal muscle fibres suggest higher‐order control
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| Title: | On–off asymmetries in oxygen consumption kinetics of singleXenopus laevisskeletal muscle fibres suggest higher‐order control |
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| Authors: | Harry B. Rossiter, Rob C. I. Wüst, Willem J. van der Laarse |
| Source: | Wust, R C I, van der Laarse, W J & Rossiter, H B 2013, 'On-off asymmetries in oxygen consumption kinetics of single Xenopus laevis skeletal muscle fibres suggest higher-order control', Journal of Physiology-London, vol. 591, no. 3, pp. 731-744. https://doi.org/10.1113/jphysiol.2012.241992 |
| Publisher Information: | Wiley, 2013. |
| Publication Year: | 2013 |
| Subject Terms: | 0301 basic medicine, 0303 health sciences, Muscle Fibers, Skeletal, In Vitro Techniques, Muscle Fibers, Oxygen Consumption/physiology, Mitochondria, Kinetics, Xenopus laevis, 03 medical and health sciences, Oxygen Consumption, Skeletal/physiology, Mitochondria/physiology, Animals, Female, Muscle Contraction/physiology, Muscle Contraction |
| Description: | Key pointsSkeletal muscles increase oxygen consumptionto produce energy during exercise; however, the processes controlling the rate ofadaptation (its kinetics) at exercise onset and offset are not well understood.Here we measurekinetics in single frog skeletal muscle fibres using a unique experimental system that allows features of intracellular control mechanisms to be elucidated.We show for the first time that at contractions onset skeletal musclekinetics are best described by a biphasic ‘activation’ and ‘exponential’ profile, whereas at cessationrecovers with a single smooth exponential.Additionally these features were dependent on oxidative capacity and the intensity of stimulated contractions.These data show that the intracellular processes that activate oxidative energy provision at the onset of contractions are far more complex than previously suggested.Abstract The mechanisms controlling skeletal muscle oxygen consumption () during exercise are not well understood. We determined whether first‐order control could explainkinetics at contractions onset () and cessation () in single skeletal muscle fibres differing in oxidative capacity, and across stimulation intensities up to.Xenopus laevisfibres (n= 21) were suspended in a sealed chamber with a fast responseelectrode to measureevery second before, during and after stimulated isometric contractions. A first‐order model did not well characterise on‐transientkinetics. Including a time delay (TD) in the model provided a significantly improved characterisation than a first‐order fit without TD (F‐ratio;P <0.05), and revealed separate ‘activation’ and ‘exponential’ phases in 15/21 fibres contracting at(mean ± SD TD: 14 ± 3 s). On‐transient kinetics () was weakly and linearly related to(R2= 0.271,P= 0.015). Off‐transient kinetics, however, were first‐order, andwas greater in low‐oxidative (< 0.05 nmol mm−3s−1) than high‐oxidative fibres (> 0.10 nmol mm−3s−1; 170 ± 70vs. 29 ± 6 s,P< 0.001).was proportional to(R2= 0.727,P< 0.001), unlike in the on‐transient. The calculated oxygen deficit was larger (P< 0.05) than the post‐contraction volume of consumed oxygen at all intensities except. These data show a clear dissociation between the kinetic control ofat the onset and cessation of contractions and across stimulation intensities. More complex models are therefore required to understand the activation of mitochondrial respiration in skeletal muscle at the start of exercise. |
| Document Type: | Article |
| Language: | English |
| ISSN: | 1469-7793 0022-3751 |
| DOI: | 10.1113/jphysiol.2012.241992 |
| Access URL: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3577546 https://pubmed.ncbi.nlm.nih.gov/23165768 https://research.vumc.nl/en/publications/on-off-asymmetries-in-oxygen-consumption-kinetics-of-single-xenop https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3577546/ https://physoc.onlinelibrary.wiley.com/doi/full/10.1113/jphysiol.2012.241992 http://onlinelibrary.wiley.com/doi/10.1113/jphysiol.2012.241992/references http://onlinelibrary.wiley.com/doi/10.1113/jphysiol.2012.241992/full https://research.vu.nl/en/publications/on-off-asymmetries-in-oxygen-consumption-kinetics-of-single-xenop-2 https://research.vumc.nl/en/publications/a53243e9-88d2-4c9e-acfb-9f7a375d8909 |
| Rights: | Wiley Online Library User Agreement |
| Accession Number: | edsair.doi.dedup.....f741c44dbd5eff9e7d93daba53740814 |
| Database: | OpenAIRE |
| Abstract: | Key pointsSkeletal muscles increase oxygen consumptionto produce energy during exercise; however, the processes controlling the rate ofadaptation (its kinetics) at exercise onset and offset are not well understood.Here we measurekinetics in single frog skeletal muscle fibres using a unique experimental system that allows features of intracellular control mechanisms to be elucidated.We show for the first time that at contractions onset skeletal musclekinetics are best described by a biphasic ‘activation’ and ‘exponential’ profile, whereas at cessationrecovers with a single smooth exponential.Additionally these features were dependent on oxidative capacity and the intensity of stimulated contractions.These data show that the intracellular processes that activate oxidative energy provision at the onset of contractions are far more complex than previously suggested.Abstract The mechanisms controlling skeletal muscle oxygen consumption () during exercise are not well understood. We determined whether first‐order control could explainkinetics at contractions onset () and cessation () in single skeletal muscle fibres differing in oxidative capacity, and across stimulation intensities up to.Xenopus laevisfibres (n= 21) were suspended in a sealed chamber with a fast responseelectrode to measureevery second before, during and after stimulated isometric contractions. A first‐order model did not well characterise on‐transientkinetics. Including a time delay (TD) in the model provided a significantly improved characterisation than a first‐order fit without TD (F‐ratio;P <0.05), and revealed separate ‘activation’ and ‘exponential’ phases in 15/21 fibres contracting at(mean ± SD TD: 14 ± 3 s). On‐transient kinetics () was weakly and linearly related to(R2= 0.271,P= 0.015). Off‐transient kinetics, however, were first‐order, andwas greater in low‐oxidative (< 0.05 nmol mm−3s−1) than high‐oxidative fibres (> 0.10 nmol mm−3s−1; 170 ± 70vs. 29 ± 6 s,P< 0.001).was proportional to(R2= 0.727,P< 0.001), unlike in the on‐transient. The calculated oxygen deficit was larger (P< 0.05) than the post‐contraction volume of consumed oxygen at all intensities except. These data show a clear dissociation between the kinetic control ofat the onset and cessation of contractions and across stimulation intensities. More complex models are therefore required to understand the activation of mitochondrial respiration in skeletal muscle at the start of exercise. |
|---|---|
| ISSN: | 14697793 00223751 |
| DOI: | 10.1113/jphysiol.2012.241992 |
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