Distinct effects of subcellular glycogen localization on tetanic relaxation time and endurance in mechanically skinned rat skeletal muscle fibres

May 28, 2009The Journal of physiology

Different roles of glycogen location inside muscle cells on muscle relaxation speed and endurance in rat muscle fibers

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Abstract

Single skeletal muscle fibres contain 0.46% myofibrillar glycogen, with distinct roles for glycogen located in different cellular compartments.

Glycogen is found in two main compartments: intermyofibrillar (72%) and intramyofibrillar (28%).
Higher levels of intramyofibrillar glycogen are associated with increased fatigue resistance (r(2) = 0.32, P = 0.02).
Conversely, greater amounts of intermyofibrillar glycogen correlate with longer half-relaxation times during unfatigued contractions (r(2) = 0.25, P = 0.03).
These findings suggest that different glycogen locations may influence muscle fibre contractility and fatigue differently.

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In vitro experiments indicate a non-metabolic role of muscle glycogen in contracting skeletal muscles. Since the sequence of events in excitation\#8211;contraction (E\#8211;C) coupling is known to be located close to glycogen granules, at specific sites on the fibre, we hypothesized that the distinct compartments of glycogen have specific effects on muscle fibre contractility and fatigability. Single skeletal muscle fibres (n = 19) from fed and fasted rats were mechanically skinned and divided into two segments. In one segment glycogen localization and volume fraction were estimated by transmission electron microscopy. The other segment was mechanically skinned and, in the presence of high and constant myoplasmic ATP and PCr, electrically stimulated (10 Hz, 0.8 s every 3 s) eliciting repeated tetanic contractions until the force response was decreased by 50% (mean +/- S.E.M., 81 +/- 16, range 22-252 contractions). Initially the total myofibrillar glycogen volume percentage was 0.46 +/- 0.07%, with 72 +/- 3% in the intermyofibrillar space and 28 +/- 3% in the intramyofibrillar space. The intramyofibrillar glycogen content was positively correlated with the fatigue resistance capacity (r(2) = 0.32, P = 0.02). Intermyofibrillar glycogen was inversely correlated with the half-relaxation time in the unfatigued tetanus (r(2) = 0.25, P = 0.03). These results demonstrate for the first time that two distinct subcellular populations of glycogen have different roles in contracting single muscle fibres under conditions of high myoplasmic ATP.

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Distinct effects of subcellular glycogen localization on tetanic relaxation time and endurance in mechanically skinned rat skeletal muscle fibres

Abstract

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