A century of exercise physiology: effects of muscle contraction and exercise on skeletal muscle Na+,K+-ATPase, Na+ and K+ ions, and on plasma K+ concentration—historical developments

Michael J. McKenna; Jean Marc Renaud; Niels Ørtenblad; Kristian Overgaard

doi:10.1007/s00421-023-05335-9

A century of exercise physiology: effects of muscle contraction and exercise on skeletal muscle Na⁺,K⁺-ATPase, Na⁺ and K⁺ ions, and on plasma K⁺ concentration—historical developments

Michael J. McKenna^*, Jean Marc Renaud, Niels Ørtenblad, Kristian Overgaard

^*Corresponding author af dette arbejde

Institut for Folkesundhed - Idræt

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Review › Forskning › peer review

Abstract

This historical review traces key discoveries regarding K⁺ and Na⁺ ions in skeletal muscle at rest and with exercise, including contents and concentrations, Na⁺,K⁺-ATPase (NKA) and exercise effects on plasma [K⁺] in humans. Following initial measures in 1896 of muscle contents in various species, including humans, electrical stimulation of animal muscle showed K⁺ loss and gains in Na⁺, Cl⁻ and H₂0, then subsequently bidirectional muscle K⁺ and Na⁺ fluxes. After NKA discovery in 1957, methods were developed to quantify muscle NKA activity via rates of ATP hydrolysis, Na⁺/K⁺ radioisotope fluxes, [³H]-ouabain binding and phosphatase activity. Since then, it became clear that NKA plays a central role in Na⁺/K⁺ homeostasis and that NKA content and activity are regulated by muscle contractions and numerous hormones. During intense exercise in humans, muscle intracellular [K⁺] falls by 21 mM (range − 13 to − 39 mM), interstitial [K⁺] increases to 12–13 mM, and plasma [K⁺] rises to 6–8 mM, whilst post-exercise plasma [K⁺] falls rapidly, reflecting increased muscle NKA activity. Contractions were shown to increase NKA activity in proportion to activation frequency in animal intact muscle preparations. In human muscle, [³H]-ouabain-binding content fully quantifies NKA content, whilst the method mainly detects α₂ isoforms in rats. Acute or chronic exercise affects human muscle K⁺, NKA content, activity, isoforms and phospholemman (FXYD1). Numerous hormones, pharmacological and dietary interventions, altered acid–base or redox states, exercise training and physical inactivity modulate plasma [K⁺] during exercise. Finally, historical research approaches largely excluded female participants and typically used very small sample sizes.

Originalsprog	Engelsk
Tidsskrift	European Journal of Applied Physiology
Vol/bind	124
Nummer	3
Sider (fra-til)	681-751
Antal sider	71
ISSN	1439-6319
DOI	https://doi.org/10.1007/s00421-023-05335-9
Status	Udgivet - mar. 2024

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10.1007/s00421-023-05335-9Licens: CC BY

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@article{d193de2305864139b40e652931d909da,

title = "A century of exercise physiology: effects of muscle contraction and exercise on skeletal muscle Na+,K+-ATPase, Na+ and K+ ions, and on plasma K+ concentration—historical developments",

abstract = "This historical review traces key discoveries regarding K+ and Na+ ions in skeletal muscle at rest and with exercise, including contents and concentrations, Na+,K+-ATPase (NKA) and exercise effects on plasma [K+] in humans. Following initial measures in 1896 of muscle contents in various species, including humans, electrical stimulation of animal muscle showed K+ loss and gains in Na+, Cl− and H20, then subsequently bidirectional muscle K+ and Na+ fluxes. After NKA discovery in 1957, methods were developed to quantify muscle NKA activity via rates of ATP hydrolysis, Na+/K+ radioisotope fluxes, [3H]-ouabain binding and phosphatase activity. Since then, it became clear that NKA plays a central role in Na+/K+ homeostasis and that NKA content and activity are regulated by muscle contractions and numerous hormones. During intense exercise in humans, muscle intracellular [K+] falls by 21 mM (range − 13 to − 39 mM), interstitial [K+] increases to 12–13 mM, and plasma [K+] rises to 6–8 mM, whilst post-exercise plasma [K+] falls rapidly, reflecting increased muscle NKA activity. Contractions were shown to increase NKA activity in proportion to activation frequency in animal intact muscle preparations. In human muscle, [3H]-ouabain-binding content fully quantifies NKA content, whilst the method mainly detects α2 isoforms in rats. Acute or chronic exercise affects human muscle K+, NKA content, activity, isoforms and phospholemman (FXYD1). Numerous hormones, pharmacological and dietary interventions, altered acid–base or redox states, exercise training and physical inactivity modulate plasma [K+] during exercise. Finally, historical research approaches largely excluded female participants and typically used very small sample sizes.",

keywords = "Exercise, Fatigue, FXYD, Na, K-pump, Plasma, Potassium, Skeletal muscle, Sodium",

author = "McKenna, {Michael J.} and Renaud, {Jean Marc} and Niels {\O}rtenblad and Kristian Overgaard",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = mar,

doi = "10.1007/s00421-023-05335-9",

language = "English",

volume = "124",

pages = "681--751",

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A century of exercise physiology: effects of muscle contraction and exercise on skeletal muscle Na⁺,K⁺-ATPase, Na⁺ and K⁺ ions, and on plasma K⁺ concentration—historical developments. / McKenna, Michael J.; Renaud, Jean Marc; Ørtenblad, Niels et al.
I: European Journal of Applied Physiology, Bind 124, Nr. 3, 03.2024, s. 681-751.

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Review › Forskning › peer review

TY - JOUR

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T2 - effects of muscle contraction and exercise on skeletal muscle Na+,K+-ATPase, Na+ and K+ ions, and on plasma K+ concentration—historical developments

AU - McKenna, Michael J.

AU - Renaud, Jean Marc

AU - Ørtenblad, Niels

AU - Overgaard, Kristian

N1 - Publisher Copyright: © The Author(s) 2024.

PY - 2024/3

Y1 - 2024/3

N2 - This historical review traces key discoveries regarding K+ and Na+ ions in skeletal muscle at rest and with exercise, including contents and concentrations, Na+,K+-ATPase (NKA) and exercise effects on plasma [K+] in humans. Following initial measures in 1896 of muscle contents in various species, including humans, electrical stimulation of animal muscle showed K+ loss and gains in Na+, Cl− and H20, then subsequently bidirectional muscle K+ and Na+ fluxes. After NKA discovery in 1957, methods were developed to quantify muscle NKA activity via rates of ATP hydrolysis, Na+/K+ radioisotope fluxes, [3H]-ouabain binding and phosphatase activity. Since then, it became clear that NKA plays a central role in Na+/K+ homeostasis and that NKA content and activity are regulated by muscle contractions and numerous hormones. During intense exercise in humans, muscle intracellular [K+] falls by 21 mM (range − 13 to − 39 mM), interstitial [K+] increases to 12–13 mM, and plasma [K+] rises to 6–8 mM, whilst post-exercise plasma [K+] falls rapidly, reflecting increased muscle NKA activity. Contractions were shown to increase NKA activity in proportion to activation frequency in animal intact muscle preparations. In human muscle, [3H]-ouabain-binding content fully quantifies NKA content, whilst the method mainly detects α2 isoforms in rats. Acute or chronic exercise affects human muscle K+, NKA content, activity, isoforms and phospholemman (FXYD1). Numerous hormones, pharmacological and dietary interventions, altered acid–base or redox states, exercise training and physical inactivity modulate plasma [K+] during exercise. Finally, historical research approaches largely excluded female participants and typically used very small sample sizes.

AB - This historical review traces key discoveries regarding K+ and Na+ ions in skeletal muscle at rest and with exercise, including contents and concentrations, Na+,K+-ATPase (NKA) and exercise effects on plasma [K+] in humans. Following initial measures in 1896 of muscle contents in various species, including humans, electrical stimulation of animal muscle showed K+ loss and gains in Na+, Cl− and H20, then subsequently bidirectional muscle K+ and Na+ fluxes. After NKA discovery in 1957, methods were developed to quantify muscle NKA activity via rates of ATP hydrolysis, Na+/K+ radioisotope fluxes, [3H]-ouabain binding and phosphatase activity. Since then, it became clear that NKA plays a central role in Na+/K+ homeostasis and that NKA content and activity are regulated by muscle contractions and numerous hormones. During intense exercise in humans, muscle intracellular [K+] falls by 21 mM (range − 13 to − 39 mM), interstitial [K+] increases to 12–13 mM, and plasma [K+] rises to 6–8 mM, whilst post-exercise plasma [K+] falls rapidly, reflecting increased muscle NKA activity. Contractions were shown to increase NKA activity in proportion to activation frequency in animal intact muscle preparations. In human muscle, [3H]-ouabain-binding content fully quantifies NKA content, whilst the method mainly detects α2 isoforms in rats. Acute or chronic exercise affects human muscle K+, NKA content, activity, isoforms and phospholemman (FXYD1). Numerous hormones, pharmacological and dietary interventions, altered acid–base or redox states, exercise training and physical inactivity modulate plasma [K+] during exercise. Finally, historical research approaches largely excluded female participants and typically used very small sample sizes.

KW - Exercise

KW - Fatigue

KW - FXYD

KW - Na, K-pump

KW - Plasma

KW - Potassium

KW - Skeletal muscle

KW - Sodium

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