Large fibre size in skeletal muscle is metabolically advantageous - PubMed (original) (raw)

Large fibre size in skeletal muscle is metabolically advantageous

Ana Gabriela Jimenez et al. Nat Commun. 2013.

Abstract

Skeletal muscle fibre size is highly variable, and while diffusion appears to limit maximal fibre size, there is no paradigm for the control of minimal size. The optimal fibre size hypothesis posits that the reduced surface area to volume in larger fibres reduces the metabolic cost of maintaining the membrane potential, and so fibres attain an optimal size that minimizes metabolic cost while avoiding diffusion limitation. Here we examine changes during hypertrophic fibre growth in metabolic cost and activity of the Na⁺-K⁺-ATPase in white skeletal muscle from crustaceans and fishes. We provide evidence for a major tenet of the optimal fibre size hypothesis by demonstrating that larger fibres are metabolically cheaper to maintain, and the cost of maintaining the membrane potential is proportional to fibre surface area to volume. The influence of surface area to volume on metabolic cost is apparent during growth in 16 species spanning a 20-fold range in fibre size, suggesting that this principle may apply widely.

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Figures

Figure 1

Figure 1

Example of 31P-NMR measurement of AP depletion rates. Representative experiment showing changes over time in (a) NMR spectra and (b) AP concentration during treatment with CN and IA or CN, IA and OU. The AP depletion rate was higher when energy metabolism alone was blocked with CN and IA than when energy metabolism and the Na+-K+-ATPase were inhibited with CN, IA and OU. The CN and IA treatment yields the total ATP demand, and the difference between slopes is the ATP cost of the Na+-K+-ATPase in isolated resting muscle.

Figure 2

Figure 2

Na+-K+ ATPase cost and enzymatic activity during hypertrophic fiber growth. (a) Absolute Na+-K+ ATPase cost and (b) maximal enzymatic activity, normalized to fit all species on a single plot. The straight colored lines connect the mean values for the small and large size classes (for visualization purposes only) and show that the changes in cost and activity during hypertrophic growth follow the pattern predicted for SA:V (red line) over a wide fiber size range. The data were normalized by dividing the absolute cost of the Na+-K+ ATPase (Table 2) by the adjustable coefficient, α, the value of which was determined for each species from an iterative curve fit as described in Supplemental Figure S1, allowing all data to be plotted in a single graph. The line color represents species group (pink = marine shrimp, green = marine lobster, gray = freshwater crayfish, black = marine crab, blue = marine teleost fish, cyan = freshwater teleost fish, and orange = marine elasmobranch). The insets are the same data plotted as a linear function of SA:V (linear regression equations: normalized cost = 0.942(SA:V) + 0.002, r2=0.72, p<.0001 (t-test, n=32); normalized activity = 0.812(SA:V) + 0.003, r2=0.86, p<0001 (t-test, n=32)).

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