Mechanisms of P<sub>i</sub> regulation of the  skeletal muscle SR Ca<sup>2+</sup> release channel

Balog, Edward M.; Fruen, Bradley R.; Kane, Patricia K.; Louis, Charles F.

doi:10.1152/ajpcell.2000.278.3.c601

Cited by 26 publications

(26 citation statements)

References 41 publications

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“…3C) (WT% initial ⌬F/F0 ϭ 5.0 Ϯ 3.0%, n ϭ 5; KO ϭ 3.3 Ϯ 1.1%, n ϭ 9; P ϭ 0.53). This initial facilitation of tetanic Ca 2ϩ transient amplitude is consistent with previous single fiber analyses of repetitive stimulation (5) and is generally attributed to elevated inorganic phosphate initially stimulating release (4,8). WT fibers then sustained maximal tetanic amplitude for a longer duration than KO fibers, after which both WT and KO fibers eventually showed a consistent decline in train amplitude (Fig.…”

Section: Ap-initiated Casupporting

confidence: 89%

S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle

Prosser

Hernández‐Ochoa²,

Lovering

et al. 2010

American Journal of Physiology-Cell Physiology

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MF. S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle. Am J Physiol Cell Physiol 299: C891-C902, 2010. First published August 4, 2010; doi:10.1152/ajpcell.00180.2010.-The role of S100A1 in skeletal muscle is just beginning to be elucidated. We have previously shown that skeletal muscle fibers from S100A1 knockout (KO) mice exhibit decreased action potential (AP)-evoked Ca 2ϩ transients, and that S100A1 binds competitively with calmodulin to a canonical S100 binding sequence within the calmodulinbinding domain of the skeletal muscle ryanodine receptor. Using voltage clamped fibers, we found that Ca 2ϩ release was suppressed at all test membrane potentials in S100A1 Ϫ/Ϫ fibers. Here we examine the role of S100A1 during physiological AP-induced muscle activity, using an integrative approach spanning AP propagation to muscle force production. With the voltage-sensitive indicator di-8-aminonaphthylethenylpyridinium, we first demonstrate that the AP waveform is not altered in flexor digitorum brevis muscle fibers isolated from S100A1 KO mice. We then use a model for myoplasmic Ca 2ϩ binding and transport processes to calculate sarcoplasmic reticulum Ca 2ϩ release flux initiated by APs and demonstrate decreased release flux and greater inactivation of flux in KO fibers. Using in vivo stimulation of tibialis anterior muscles in anesthetized mice, we show that the maximal isometric force response to twitch and tetanic stimulation is decreased in S100A1 Ϫ/Ϫ muscles. KO muscles also fatigue more rapidly upon repetitive stimulation than those of wild-type counterparts. We additionally show that fiber diameter, type, and expression of key excitation-contraction coupling proteins are unchanged in S100A1 KO muscle. We conclude that the absence of S100A1 suppresses physiological AP-induced Ca 2ϩ release flux, resulting in impaired contractile activation and force production in skeletal muscle. S100; excitation-contraction coupling; calcium signaling; muscle IN SKELETAL AND CARDIAC MUSCLE, action potential (AP) depolarization triggers Ca 2ϩ release from the sarcoplasmic reticulum (SR), which in turn enables actomyosin interaction and contractile force generation in a process termed excitationcontraction (EC) coupling. The small Ca 2ϩ -binding protein S100A1 positively modulates EC coupling in both skeletal and cardiac muscle (34,39,40,48). In skeletal muscle, S100A1 localizes to sarcolemmal invaginations known as transverse tubules (t-tubules) and the adjacent junctional faces of the SR (jSR) (7,14,40). This region is termed the triad junction and houses the Ca 2ϩ release machinery of the muscle fiber (11, 16). S100A1 binds to the Ca 2ϩ release channel of the jSR ryanodine receptor type-1 (RyR1) and enhances RyR1-mediated Ca 2ϩ release (17,39,40,48). We have recently demonstrated that S100A1 competes with calmodulin (CaM) for the previously well-characterized CaM binding domain (CaMBD) on RyR1 (40, 55), a site documented to sensitize RyR1 to activation (43,49). Furthermore, s...

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Section: Ap-initiated Casupporting

confidence: 89%

S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle

Prosser

Hernández‐Ochoa²,

Lovering

et al. 2010

American Journal of Physiology-Cell Physiology

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“…ST fibers already have a reduced rate of Ca 2ϩ release, force production, and relaxation rate (3,5). As mentioned above, Fig.…”

Section: Physiological Relevancementioning

confidence: 59%

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

Posterino

Dunn²

2008

American Journal of Physiology-Cell Physiology

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We compared the effects of 50 mM P(i) on caffeine-induced Ca(2+) release in mechanically skinned fast-twitch (FT) and slow-twitch (ST) skeletal muscle fibers of the rat. The time integral (area) of the caffeine response was reduced by approximately 57% (FT) and approximately 27% (ST) after 30 s of exposure to 50 mM P(i) in either the presence or absence of creatine phosphate (to buffer ADP). Differences in the sarcoplasmic reticulum (SR) Ca(2+) content between FT and ST fibers [ approximately 40% vs. 100% SR Ca(2+) content (pCa 6.7), respectively] did not contribute to the different effects of P(i) observed; underloading the SR of ST fibers so that the SR Ca(2+) content approximated that of FT fibers resulted in an even smaller ( approximately 21%), but not significant, reduction in caffeine-induced Ca(2+) release by P(i). These observed differences between FT and ST fibers could arise from fiber-type differences in the ability of the SR to accumulate Ca(2+)-P(i) precipitate. To test this, fibers were Ca(2+) loaded in the presence of 50 mM P(i). In FT fibers, the maximum SR Ca(2+) content (pCa 6.7) was subsequently increased by up to 13 times of that achieved when loading for 2 min in the absence of P(i). In ST fibers, the SR Ca(2+) content was only doubled. These data show that Ca(2+) release in ST fibers was less affected by P(i) than FT fibers, and this may be due to a reduced capacity of ST SR to accumulate Ca(2+)-P(i) precipitate. This may account, in part, for the fatigue-resistant nature of ST fibers.

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“…Second, P i might act on the RyR and increase SR Ca 2ϩ release. Accordingly, elevated P i has been shown to increase the open probability of isolated RyR incorporated into lipid bilayers as well as the rate of Ca 2ϩ -induced Ca 2ϩ release in SR vesicles and skinned fibers (27,174). However, it has since been shown that P i decreases caffeine-and depolarization-induced SR Ca 2ϩ release in mechanically skinned rat skeletal muscle fibers in a Mg 2ϩ -dependent manner (135).…”

Section: P I and The Increase Of Tetanic [Ca 2ϩ ] I In Early Fatiguementioning

confidence: 99%

Skeletal Muscle Fatigue: Cellular Mechanisms

Allen¹,

Lamb²,

Westerblad³

2008

Physiological Reviews

1,896

1,876

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Repeated, intense use of muscles leads to a decline in performance known as muscle fatigue. Many muscle properties change during fatigue including the action potential, extracellular and intracellular ions, and many intracellular metabolites. A range of mechanisms have been identified that contribute to the decline of performance. The traditional explanation, accumulation of intracellular lactate and hydrogen ions causing impaired function of the contractile proteins, is probably of limited importance in mammals. Alternative explanations that will be considered are the effects of ionic changes on the action potential, failure of SR Ca2+ release by various mechanisms, and the effects of reactive oxygen species. Many different activities lead to fatigue, and an important challenge is to identify the various mechanisms that contribute under different circumstances. Most of the mechanistic studies of fatigue are on isolated animal tissues, and another major challenge is to use the knowledge generated in these studies to identify the mechanisms of fatigue in intact animals and particularly in human diseases.

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Mechanisms of P_i regulation of the skeletal muscle SR Ca²⁺ release channel

Cited by 26 publications

References 41 publications

S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle

S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle

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

Skeletal Muscle Fatigue: Cellular Mechanisms

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Mechanisms of Pi regulation of the skeletal muscle SR Ca2+ release channel

Cited by 26 publications

References 41 publications

S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle

S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle

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

Skeletal Muscle Fatigue: Cellular Mechanisms

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Mechanisms of P_i regulation of the skeletal muscle SR Ca²⁺ release channel

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