Abstract

The Na+,K+-ATPase (NKA) plays a fundamental role in the regulation of skeletal muscle membrane Na+ and K+ gradients, excitability and fatigue during repeated intense contractions. Many studies have investigated the effects of acute concentric exercise on K+ regulation and skeletal muscle NKA, but almost nothing is known about the effects of repeated eccentric contractions. We therefore investigated the effects of unaccustomed maximal eccentric knee extensor contractions on K+ regulation during exercise, peak knee extensor muscle torque, and vastus lateralis muscle NKA content and 3-O-MFPase activity. Torque measurements, muscle biopsies, and venous blood samples were taken before, during and up to 7 days following the contractions in six healthy adults. Eccentric contractions reduced peak isometric muscle torque immediately post-exercise by 26±11% and serum creatine kinase concentration peaked 24 h post-exercise at 339±90 IU/L. During eccentric contractions, plasma [K+] rose during Set 1 and remained elevated at ∼4.9 mM during sets 4–10; this was despite a decline in work output by Set 4, which fell by 18.9% at set 10. The rise in plasma [K+].work−1 ratio was elevated over Set 2 from Set 4– Set 10. Eccentric contractions had no effect on muscle NKA content or maximal in-vitro 3-O-MFPase activity immediately post- or up to 7 d post-exercise. The sustained elevation in plasma [K+] despite a decrease in work performed by the knee extensor muscles suggests an impairment in K+ regulation during maximal eccentric contractions, possibly due to increased plasma membrane permeability or to excitation-contraction uncoupling.

Highlights

  • The Na+,K+-ATPase (NKA) plays a fundamental role in skeletal muscle contractility via the regulation of skeletal muscle membrane excitability

  • The calculated rise in plasma [K+]/work ratio (D[K+].work21) during eccentric exercise was elevated at Set 4 above Set 2 (P,0.05) and despite declining work output, remained elevated at this level during Sets 6, 8 and 10 (P,0.05) (Figure 3C)

  • There was no significant effect of eccentric exercise on [3H]ouabain binding site content (P = 0.314, Figure 4A) or maximal in vitro K+-stimulated 3-O-MFPase activity (P = 0.414, Figure 4B). This is the first study to investigate the effects of unaccustomed intense eccentric contractions on K+ regulation during exercise and on skeletal muscle NKA content and 3-O-MFPase

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Summary

Introduction

The Na+,K+-ATPase (NKA) plays a fundamental role in skeletal muscle contractility via the regulation of skeletal muscle membrane excitability (for review see [1,2]). The majority of studies that have investigated the effects of acute exercise on K+ regulation have utilized experimental models that involve predominantly concentric muscle contractions, such as sprint or endurance cycling, and isolated knee extension exercise [7,8,9,10,11]. These studies have consistently shown a net release of K+ from contracting skeletal muscle, indicating an inability of the NKA to fully counteract the excitation-induced loss of K+ from the muscle in-vivo [5]. During submaximal cycling exercise, venous and arterial plasma [K+] have been reported to be between 5.5–7.0 mM [12], and can exceed

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