On–off asymmetries in oxygen consumption kinetics of single Xenopus laevis skeletal muscle fibres suggest higher-order control

Authors

  • Rob C.I. Wüst,

    1. School of Biomedical Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, UK
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  • Willem J. van der Laarse,

    1. Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, the Netherlands
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  • Harry B. Rossiter

    1. School of Biomedical Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, UK
    2. Rehabilitation Clinical Trials Center, Division of Respiratory and Critical Care Physiology and Medicine, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA
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H. B. Rossiter: Rehabilitation Clinical Trials Center, Division of Respiratory and Critical Care Physiology and Medicine, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA. Email: hrossiter@ucla.edu

Key points

  • Skeletal muscles increase oxygen consumption inline image to produce energy during exercise; however, the processes controlling the rate of inline image adaptation (its kinetics) at exercise onset and offset are not well understood.

  • Here we measure inline image 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 inline image kinetics are best described by a biphasic ‘activation’ and ‘exponential’ profile, whereas at cessation inline image 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 (inline image) during exercise are not well understood. We determined whether first-order control could explain inline image kinetics at contractions onset (inline image) and cessation (inline image) in single skeletal muscle fibres differing in oxidative capacity, and across stimulation intensities up to inline image. Xenopus laevis fibres (n= 21) were suspended in a sealed chamber with a fast response inline image electrode to measure inline image every second before, during and after stimulated isometric contractions. A first-order model did not well characterise on-transient inline image 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 inline image (mean ± SD TD: 14 ± 3 s). On-transient kinetics (inline image) was weakly and linearly related to inline image (R2= 0.271, P= 0.015). Off-transient kinetics, however, were first-order, and inline image was greater in low-oxidative (inline image < 0.05 nmol mm−3 s−1) than high-oxidative fibres (inline image > 0.10 nmol mm−3 s−1; 170 ± 70 vs. 29 ± 6 s, P < 0.001). inline image was proportional to inline image (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 inline image. These data show a clear dissociation between the kinetic control of inline image 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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