Matching of Sarcoplasmic Reticulum and Contractile Properties in Rat Fast‐ and Slow‐twitch Muscle Fibres

Abstract

1. The twitch characteristics (fast-twitch or slow-twitch) of skeletal muscle fibres are determined not only by the contractile apparatus properties of the fibre, but also by the time-course of Ca2+ release and re-uptake by the sarcoplasmic reticulum (SR). The present study examined, in individual fibres from non-transforming muscle of the rat, whether particular SR properties are matched to the contractile apparatus properties of the fibre, in particular in the case of fibres with fast-twitch contractile apparatus located in a slow-twitch muscle, namely the soleus. 2. Force was recorded in single, mechanically skinned fibres from extensor digitorum longus (EDL), gastrocnemius, peroneus longus and soleus muscles. Using repeated cycles in which the SR was emptied of all releasable Ca2+ and then reloaded, it was possible to determine the relative amount of Ca2+ present in the SR endogenously, the maximum SR capacity and the rate of Ca2+ loading. The sensitivity of the contractile apparatus to Ca2+ and Sr2+ was used to classify the fibres as fast-twitch (FT), slow-twitch (ST) or mixed (< 3% of the fibres examined) and thereby identify the likely troponin C and myosin heavy chain types present. 3. There was no significant difference in SR properties between the groups of FT fibres obtained from the four different muscles, including soleus. Despite some overlap in the SR properties of individual fibres between the FT and ST groups, the properties of the FT fibres in all four muscles studied were significantly different from those of the ST and mixed fibres. 4. In general, in FT fibres the SR had a larger capacity and the endogenous Ca2+ content was a relatively lower percentage of maximum compared with ST fibres. Importantly, in terms of their SR properties, FT fibres from soleus muscle more closely resembled FT fibres from other muscles than they did ST fibres from soleus muscle.

Skeletal Muscle Fatigue: Cellular Mechanisms

“…Fast-twitch rat muscle stimulated in vitro at 40 Hz continuously or intermittently for a total of 30 s shows net uptake of 50 -100 mol Ca 2ϩ /kg wet wt (183,313), equivalent to ϳ5-10% of the Ca 2ϩ already present in the SR endogenously and representing Ͻ5% of the available SR Ca 2ϩ capacity. With continuous stimulation at 1 Hz for 2-4 h, fast-twitch rat muscles increase their Ca 2ϩ content to ϳ2.5 times the endogenous level, whereas slow-twitch muscle shows little increase (183), consistent with the endogenous Ca 2ϩ and maximum SR capacity observed in such muscle types (176,440). Frog muscle fibers stimulated in vitro to fatigue increased SR Ca 2ϩ content by ϳ10% (190).…”

“…Compared with fast-twitch fibers, slowtwitch fibers have fewer Ca 2ϩ binding sites on troponin C and the SR pumps, and a lower rate and amount of Ca 2ϩ release suffices for contraction, particularly given the much slower contraction rate of the predominant MHC isoform (type I) present (59,61). Thus SR and contractile properties in a given fiber are generally well matched (440).…”

“…3-1 mM (175, 274, 275, 382). The SR is normally loaded at only ϳ25% of maximum capacity in fast-twitch fibers, but at ϳ70% or greater in slow-twitch fibers (176,183,440). The relatively low fractional SR load level in fast-twitch fibers (and consequent low free [Ca 2ϩ ]) likely aids Ca 2ϩ uptake in adverse metabolic conditions.…”

Comparison of the effects of inorganic phosphate on caffeine-induced Ca2+ release in fast- and slow-twitch mammalian skeletal muscle

“…A qualitative assessment of the amount of releasable Ca 2ϩ from the SR of skinned fibers was determined by examining changes in the time integral (area) of the caffeine-induced force response elicited by exposure to the caffeine solution (see Table 1). The area of the caffeine-induced force transient has been previously shown to be directly proportional to the SR Ca 2ϩ content over a range of SR Ca 2ϩ concentration ([Ca 2ϩ ]) (33,37). Figure 1 shows the relationship between the area of the caffeineinduced force response versus the length of time fibers were loaded with Ca 2ϩ , in both FT and ST fibers.…”

Remodeling of calcium handling in skeletal muscle through PGC-1α: impact on force, fatigability, and fiber type

“…The latter concept is inextricably linked to calcium handling. The speed of calcium release, clearance, and its peak amplitude determine the characteristic of the twitch (5,50).…”