Increased muscle glycogen content is associated with increased capacity to respond to T-system depolarisation in mechanically skinned skeletal muscle fibres from the rat

Abstract

The ability of mechanically skinned muscle fibres from the rat to respond to T-system depolarisation was studied in relation to muscle glycogen content. Muscle glycogen was altered by incubating extensor digitorum longus (EDL) muscles in Krebs solution without glucose or in Krebs solution with glucose (10 mM) and insulin (20 U.l-1). The glycogen content of muscles stored without glucose was rather stable between 30 and 480 min (11.27 +/- 0.39 mumol.g-1), while the muscles stored with glucose and insulin maintained an elevated and stable level of glycogen (23.48 +/- 1.67 mumol.g-1) between 100 and 360 min. Single mechanically skinned fibres from paired muscles, incubated in either glucose-free Krebs or in Krebs with glucose and insulin, were subjected to cycles of T-system depolarisation-repolarisation in a controlled environment (8 mM ATP, 10 mM creatine phosphate, 1 mM Mg2+, pH 7.10) and the force response was monitored until the force had declined to 50% of the maximum response (50% rundown). Fibres from muscles with a higher glycogen content reached 50% rundown after a larger number of depolarisations and displayed consistently larger average response capacity values, calculated as the sum of the force responses to 50% rundown divided by the maximum Ca(2+)-activated force response in that fibre. Thus skinned fibres originating from muscles with a higher glycogen content have an increased ability to respond to T-system depolarisation when the effect of metabolite accumulation is minimised and the function of glycogen acting as an energy source is by-passed. This provides direct support to the hypothesis that glycogen has a protective role in maintaining fibre excitability.

Skeletal Muscle Fatigue: Cellular Mechanisms

“…In these skinned fiber experiments, ATP and PCr were present in the bathing solutions, suggesting that glycogen had a structural rather than a metabolic role. Similar studies were subsequently performed on skinned rat EDL fibers, and these mammalian fibers showed only a small (34) or no (191) ATP-and PCr-independent effect of glycogen on the capacity to respond to depolarizations. Data from fatigue studies on intact muscle cells may be used in support of both a metabolic and structural role of glycogen.…”

Skeletal muscle lipid flux: running water carries no poison

“…TG content alone cannot predict muscle physiology, since elevated muscle TG content in endurance-trained athletes is an adaptive response to increased demand for fuel utilization (45,93), whereas elevated muscle TG content in obese individuals is a maladaptive response to energy excess (30,65). In trained muscles, exercise enhances intramuscular TG breakdown, which promotes ATP resynthesis to spare glycogen (the depletion of which probably leads to muscle exhaustion) (8,32). Exercise training also induces an increase in protein abundance for enzymes that are associated with synthesis, breakdown, and utilization of intramuscular TG (1,42,52,60,87,98).…”

Impaired calcium release during fatigue

“…Also, the accelerated fatigue development in glycogen-depleted intact toad fibers was not associated with the normal decrease in the rapidly releasable SR Ca 2ϩ store (73). However, skinned rat EDL fibers showed only a small (11) or no (59) ATP-and PCr-independent effect of glycogen on the capacity to respond to depolarizations. Moreover, the faster fatigue development in glycogen depleted mouse muscle preparations was accompanied by normal changes in other fatigue-induced parameters (i.e., decreased myofibrillar Ca 2ϩ sensitivity and maximum force, slowed relaxation, and increased resting [Ca 2ϩ ] myo ), which are generally attributed to metabolic changes (30,62).…”