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Effect of sarcoplasmic reticulum Ca 2+ content on action potential‐induced Ca 2+ release in rat skeletal muscle fibres
Author(s) -
Posterino G. S.,
Lamb G. D.
Publication year - 2003
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1111/j.1469-7793.2003.00219.x
Subject(s) - endoplasmic reticulum , skeletal muscle , chemistry , calcium , sarcoplasm , biophysics , medicine , endocrinology , biology , biochemistry
This study examined the relationship between the level of Ca 2+ loading in the sarcoplasmic reticulum (SR) and the amount of Ca 2+ released by an action potential (AP) in fast‐twitch skeletal muscle fibres of the rat. Single muscle fibres were mechanically skinned and electric field stimulation was used to induce an AP in the transverse‐tubular system and a resulting twitch response. Responses were elicited in the presence of known amounts (0–0.38 mM) of BAPTA, a fast Ca 2+ buffer, with the SR Ca 2+ pump either functional or blocked by 50 μM 2,5‐di‐tert‐butyl‐1,4‐hydroquinone (TBQ). When Ca 2+ reuptake was blocked, an estimate of the amount of Ca 2+ released by an AP could be derived from the size of the force response. In a fibre with the SR loaded with Ca 2+ at the endogenous level (≈1.2 mM, expressed as total Ca 2+ per litre fibre volume; approximately one‐third of maximal loading), a single AP triggered the release of ≈230 μM Ca 2+ . If a second AP was elicited 10 ms after the first, only a further ≈60 μM Ca 2+ was released, the reduction probably being due to Ca 2+ inactivation of Ca 2+ release. When Ca 2+ reuptake was blocked, APs applied 15 s apart elicited similar amounts of Ca 2+ release (≈230 μM) on the first two or three occasions and then progressively less Ca 2+ was released until the SR was fully depleted after a total of approximately eight APs. When the SR was loaded to near‐maximal capacity (≈3–4 mM), each AP (or pair of APs 10 ms apart) still only released approximately the same amount of Ca 2+ as that released when the fibre was endogenously loaded. Consistent with this, successive APs (15 s apart) elicited similar amounts of Ca 2+ release ≈10–16 times before the amount released declined, and the SR was fully depleted of Ca 2+ after a total release calculated to be ≈3–4 mM. When the SR was loaded maximally, increasing the [BAPTA] above 280 μM resulted in an increase in the amount of Ca 2+ released per AP, probably because the greater level of cytoplasmic Ca 2+ buffering prevented Ca 2+ inactivation from adequately limiting Ca 2+ release. These results show that the amount of Ca 2+ released by AP stimulation in rat fast‐twitch fibres normally stays virtually constant over a wide range of SR Ca 2+ content, in spite of the likely large change in the electrochemical gradient for Ca 2+ . This was also found to be the case in toad twitch fibres. This constancy in Ca 2+ release should help ensure precise regulation of force production in fast‐twitch muscle in a range of circumstances.