Subcellular distribution of glycogen and decreased tetanic Ca²⁺ in fatigued single intact mouse muscle fibres

Mar 5, 2014The Journal of physiology

Location of glycogen inside cells and reduced calcium during muscle fatigue in single mouse muscle fibers

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Abstract

At fatigue, tetanic cytoplasmic calcium levels decreased to 54 ± 4% of the initial value in low-intensity fatigued fibres.

Fatigue during muscle contractions resulted in a significant reduction of inter- and intramyofibrillar glycogen content by 60-75% compared to rested controls.
Subsarcolemmal glycogen levels remained unchanged compared to control fibres despite fatigue.
A strong correlation was observed between decreased calcium levels and reduced intramyofibrillar glycogen, suggesting a critical relationship between the two.
The findings indicate that energy supply from intramyofibrillar glycogen may be essential for calcium release from the sarcoplasmic reticulum during muscle fatigue.

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In skeletal muscle fibres, glycogen has been shown to be stored at different subcellular locations: (i) between the myofibrils (intermyofibrillar); (ii) within the myofibrils (intramyofibrillar); and (iii) subsarcolemmal. Of these, intramyofibrillar glycogen has been implied as a critical regulator of sarcoplasmic reticulum Ca(2+) release. The aim of the present study was to test directly how the decrease in cytoplasmic free Ca(2+) ([Ca(2+)]i) during repeated tetanic contractions relates to the subcellular glycogen distribution. Single fibres of mouse flexor digitorum brevis muscles were fatigued with 70 Hz, 350 ms tetani given at 2 s (high-intensity fatigue, HIF) or 10 s (low-intensity fatigue, LIF) intervals, while force and [Ca(2+)]i were measured. Stimulation continued until force decreased to 30% of its initial value. Fibres were then prepared for analyses of subcellular glycogen distribution by transmission electron microscopy. At fatigue, tetanic [Ca(2+)]i was reduced to 70 ± 4% and 54 ± 4% of the initial in HIF (P < 0.01, n = 9) and LIF (P < 0.01, n = 5) fibres, respectively. At fatigue, the mean inter- and intramyofibrillar glycogen content was 60-75% lower than in rested control fibres (P < 0.05), whereas subsarcolemmal glycogen was similar to control. Individual fibres showed a good correlation between the fatigue-induced decrease in tetanic [Ca(2+)]i and the reduction in intermyofibrillar (P = 0.051) and intramyofibrillar (P = 0.0008) glycogen. In conclusion, the fatigue-induced decrease in tetanic [Ca(2+)]i, and hence force, is accompanied by major reductions in inter- and intramyofibrillar glycogen. The stronger correlation between decreased tetanic [Ca(2+)]i and reduced intramyofibrillar glycogen implies that sarcoplasmic reticulum Ca(2+) release critically depends on energy supply from the intramyofibrillar glycogen pool.

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Subcellular distribution of glycogen and decreased tetanic Ca²⁺ in fatigued single intact mouse muscle fibres

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