On–off asymmetries in oxygen consumption kinetics of single Xenopus laevis skeletal muscle fibres suggest higher‐order control
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Key points Skeletal muscles increase oxygen consumption to produce energy during exercise; however, the processes controlling the rate of adaptation (its kinetics) at exercise onset and offset are not well understood. Here we measure kinetics 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 muscle kinetics are best described by a biphasic ‘activation’ and ‘exponential’ profile, whereas at cessation recovers 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 explain kinetics 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 response electrode to measure every second before, during and after stimulated isometric contractions. A first‐order model did not well characterise on‐transient kinetics. 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, and was 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 of at 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.
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- Wüst RCI, McDonald JR, Ferguson BS, Sun Y, Rogatzki MJ, Spires J, Kowalchuk JM, Gladden LB, Rossiter HB. Is there a time-delay in muscle oxygen uptake at the onset of contractions. Proc Physiol Soc. 2012;26 c16 and pc16. [Google Scholar]
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Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease
Smith, R. L., Soeters, M. R., Wüst, R. C. I., & Houtkooper, R. H. (2018) · Endocrine Reviews · doi:10.1210/er.2017-00211 · Cited by 787 · see citing works
Self-citation
- Authors
- Wüst, R. C. I., van der Laarse, W. J., & Rossiter, H. B.
- Affiliations
- University of Leeds (GB)
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2013-01-14
- Volume
- 591
- Issue
- 3
- Pages
- 731-744
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC3577546
- OpenAlex
- W1579448109
- Cited by
- 44
- References
- 57
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 4 · 2020: 4 · 2019: 2 · 2018: 7 · 2017: 6 · 2016: 4 · 2015: 3 · 2014: 4 · 2013: 1
- FWCI
- 6.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- VU Research Portal (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/F019521/1)
- Topics
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- exercise onset, exercise cessation, time delay, oxidative capacity, oxygen deficit, isometric contraction, stimulation intensity, exercise adaptation
- MeSH terms
- Animals, Female, Kinetics, Mitochondria, Muscle Contraction, Oxygen Consumption, Xenopus laevis, Muscle Fibers, Skeletal, In Vitro Techniques
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