Literature DB >> 28209743

Skeletal muscle bioenergetics during all-out exercise: mechanistic insight into the oxygen uptake slow component and neuromuscular fatigue.

Ryan M Broxterman1,2, Gwenael Layec2,3, Thomas J Hureau2, Markus Amann4,2,3,5,6, Russell S Richardson4,2,3,6.   

Abstract

Although all-out exercise protocols are commonly used, the physiological mechanisms underlying all-out exercise performance are still unclear, and an in-depth assessment of skeletal muscle bioenergetics is lacking. Therefore, phosphorus magnetic resonance spectroscopy (31P-MRS) was utilized to assess skeletal muscle bioenergetics during a 5-min all-out intermittent isometric knee-extensor protocol in eight healthy men. Metabolic perturbation, adenosine triphosphate (ATP) synthesis rates, ATP cost of contraction, and mitochondrial capacity were determined from intramuscular concentrations of phosphocreatine (PCr), inorganic phosphate (Pi), diprotonated phosphate ([Formula: see text]), and pH. Peripheral fatigue was determined by exercise-induced alterations in potentiated quadriceps twitch force (Qtw) evoked by supramaximal electrical femoral nerve stimulation. The oxidative ATP synthesis rate (ATPOX) attained and then maintained peak values throughout the protocol, despite an ~63% decrease in quadriceps maximal force production. ThusATPOX normalized to force production (ATPOX gain) significantly increased throughout the exercise (1st min: 0.02 ± 0.01, 5th min: 0.04 ± 0.01 mM·min-1·N-1), as did the ATP cost of contraction (1st min: 0.048 ± 0.019, 5th min: 0.052 ± 0.015 mM·min-1·N-1). Additionally, the pre- to postexercise change in Qtw (-52 ± 26%) was significantly correlated with the exercise-induced change in intramuscular pH (r = 0.75) and [Formula: see text] concentration (r = 0.77). In conclusion, the all-out exercise protocol utilized in the present study elicited a "slow component-like" increase in intramuscular ATPOX gain as well as a progressive increase in the phosphate cost of contraction. Furthermore, the development of peripheral fatigue was closely related to the perturbation of specific fatigue-inducing intramuscular factors (i.e., pH and [Formula: see text] concentration).NEW & NOTEWORTHY The physiological mechanisms and skeletal muscle bioenergetics underlying all-out exercise performance are unclear. This study revealed an increase in oxidative ATP synthesis rate gain and the ATP cost of contraction during all-out exercise. Furthermore, peripheral fatigue was related to the perturbation in pH and deprotonated phosphate ion. These findings support the concept that the oxygen uptake slow component arises from within active skeletal muscle and that skeletal muscle force generating capacity is linked to the intramuscular metabolic milieu.

Entities:  

Keywords:  ATP cost; ATP synthesis; magnetic resonance spectroscopy; muscle metabolism; neuromuscular fatigue

Mesh:

Substances:

Year:  2017        PMID: 28209743      PMCID: PMC5451539          DOI: 10.1152/japplphysiol.01093.2016

Source DB:  PubMed          Journal:  J Appl Physiol (1985)        ISSN: 0161-7567


  55 in total

1.  3-min all-out exercise test for running.

Authors:  R W Pettitt; N Jamnick; I E Clark
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2.  Similar metabolic perturbations during all-out and constant force exhaustive exercise in humans: a (31)P magnetic resonance spectroscopy study.

Authors:  Mark Burnley; Anni Vanhatalo; Jonathan Fulford; Andrew M Jones
Journal:  Exp Physiol       Date:  2010-04-01       Impact factor: 2.969

3.  A 3-min all-out test to determine peak oxygen uptake and the maximal steady state.

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4.  Determination of critical power using a 3-min all-out cycling test.

Authors:  Anni Vanhatalo; Jonathan H Doust; Mark Burnley
Journal:  Med Sci Sports Exerc       Date:  2007-03       Impact factor: 5.411

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Authors:  Andrew M Jones; Anni Vanhatalo; Mark Burnley; R Hugh Morton; David C Poole
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6.  Improved method for accurate and efficient quantification of MRS data with use of prior knowledge

Authors: 
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7.  Power output and fatigue of human muscle in maximal cycling exercise.

Authors:  N McCartney; G J Heigenhauser; N L Jones
Journal:  J Appl Physiol Respir Environ Exerc Physiol       Date:  1983-07

8.  The O2 cost of the tension-time integral in isolated single myocytes during fatigue.

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9.  Contribution of exercising legs to the slow component of oxygen uptake kinetics in humans.

Authors:  D C Poole; W Schaffartzik; D R Knight; T Derion; B Kennedy; H J Guy; R Prediletto; P D Wagner
Journal:  J Appl Physiol (1985)       Date:  1991-10

Review 10.  Critical Power: An Important Fatigue Threshold in Exercise Physiology.

Authors:  David C Poole; Mark Burnley; Anni Vanhatalo; Harry B Rossiter; Andrew M Jones
Journal:  Med Sci Sports Exerc       Date:  2016-11       Impact factor: 5.411

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4.  Bioenergetic Mechanisms Linking V˙O2 Kinetics and Exercise Tolerance.

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Journal:  Exerc Sport Sci Rev       Date:  2021-10-01       Impact factor: 6.642

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6.  On the role of skeletal muscle acidosis and inorganic phosphates as determinants of central and peripheral fatigue: A 31 P-MRS study.

Authors:  Thomas J Hureau; Ryan M Broxterman; Joshua C Weavil; Matthew T Lewis; Gwenael Layec; Markus Amann
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7.  Influence of group III/IV muscle afferents on small muscle mass exercise performance: a bioenergetics perspective.

Authors:  Ryan M Broxterman; Thomas J Hureau; Gwenael Layec; David E Morgan; Amber D Bledsoe; Jacob E Jessop; Markus Amann; Russell S Richardson
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8.  Bioenergetics and ATP Synthesis during Exercise: Role of Group III/IV Muscle Afferents.

Authors:  Ryan M Broxterman; Gwenael Layec; Thomas J Hureau; David E Morgan; Amber D Bledsoe; Jacob E Jessop; Markus Amann; Russell S Richardson
Journal:  Med Sci Sports Exerc       Date:  2017-12       Impact factor: 5.411

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Authors:  Andrew M Alexander; Kaylin D Didier; Shane M Hammer; Alex C Dzewaltowski; Karly N Kriss; Garrett M Lovoy; Joseph L Hammer; Joshua R Smith; Carl J Ade; Ryan M Broxterman; Thomas J Barstow
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