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Comparison of myoplasmic calcium movements during excitation–contraction coupling in frog twitch and mouse fast-twitch muscle fibers

Single twitch fibers from frog leg muscles were isolated by dissection and micro-injected with furaptra, a rapidly responding fluorescent Ca(2+) indicator. Indicator resting fluorescence (F(R)) and the change evoked by an action potential (ΔF) were measured at long sarcomere length (16°C); ΔF/F(R) w...

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Autores principales: Hollingworth, Stephen, Baylor, Stephen M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3639574/
https://www.ncbi.nlm.nih.gov/pubmed/23630340
http://dx.doi.org/10.1085/jgp.201310961
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author Hollingworth, Stephen
Baylor, Stephen M.
author_facet Hollingworth, Stephen
Baylor, Stephen M.
author_sort Hollingworth, Stephen
collection PubMed
description Single twitch fibers from frog leg muscles were isolated by dissection and micro-injected with furaptra, a rapidly responding fluorescent Ca(2+) indicator. Indicator resting fluorescence (F(R)) and the change evoked by an action potential (ΔF) were measured at long sarcomere length (16°C); ΔF/F(R) was scaled to units of Δf(CaD), the change in fraction of the indicator in the Ca(2+)-bound form. Δf(CaD) was simulated with a multicompartment model of the underlying myoplasmic Ca(2+) movements, and the results were compared with previous measurements and analyses in mouse fast-twitch fibers. In frog fibers, sarcoplasmic reticulum (SR) Ca(2+) release evoked by an action potential appears to be the sum of two components. The time course of the first component is similar to that of the entire Ca(2+) release waveform in mouse fibers, whereas that of the second component is severalfold slower; the fractional release amounts are ∼0.8 (first component) and ∼0.2 (second component). Similar results were obtained in frog simulations with a modified model that permitted competition between Mg(2+) and Ca(2+) for occupancy of the regulatory sites on troponin. An anatomical basis for two release components in frog fibers is the presence of both junctional and parajunctional SR Ca(2+) release channels (ryanodine receptors [RyRs]), whereas mouse fibers (usually) have only junctional RyRs. Also, frog fibers have two RyR isoforms, RyRα and RyRβ, whereas the mouse fibers (usually) have only one, RyR1. Our simulations suggest that the second release component in frog fibers functions to supply extra Ca(2+) to activate troponin, which, in mouse fibers, is not needed because of the more favorable location of their triadic junctions (near the middle of the thin filament). We speculate that, in general, parajunctional RyRs permit increased myofilament activation in fibers whose triadic junctions are located at the z-line.
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spelling pubmed-36395742013-11-01 Comparison of myoplasmic calcium movements during excitation–contraction coupling in frog twitch and mouse fast-twitch muscle fibers Hollingworth, Stephen Baylor, Stephen M. J Gen Physiol Research Article Single twitch fibers from frog leg muscles were isolated by dissection and micro-injected with furaptra, a rapidly responding fluorescent Ca(2+) indicator. Indicator resting fluorescence (F(R)) and the change evoked by an action potential (ΔF) were measured at long sarcomere length (16°C); ΔF/F(R) was scaled to units of Δf(CaD), the change in fraction of the indicator in the Ca(2+)-bound form. Δf(CaD) was simulated with a multicompartment model of the underlying myoplasmic Ca(2+) movements, and the results were compared with previous measurements and analyses in mouse fast-twitch fibers. In frog fibers, sarcoplasmic reticulum (SR) Ca(2+) release evoked by an action potential appears to be the sum of two components. The time course of the first component is similar to that of the entire Ca(2+) release waveform in mouse fibers, whereas that of the second component is severalfold slower; the fractional release amounts are ∼0.8 (first component) and ∼0.2 (second component). Similar results were obtained in frog simulations with a modified model that permitted competition between Mg(2+) and Ca(2+) for occupancy of the regulatory sites on troponin. An anatomical basis for two release components in frog fibers is the presence of both junctional and parajunctional SR Ca(2+) release channels (ryanodine receptors [RyRs]), whereas mouse fibers (usually) have only junctional RyRs. Also, frog fibers have two RyR isoforms, RyRα and RyRβ, whereas the mouse fibers (usually) have only one, RyR1. Our simulations suggest that the second release component in frog fibers functions to supply extra Ca(2+) to activate troponin, which, in mouse fibers, is not needed because of the more favorable location of their triadic junctions (near the middle of the thin filament). We speculate that, in general, parajunctional RyRs permit increased myofilament activation in fibers whose triadic junctions are located at the z-line. The Rockefeller University Press 2013-05 /pmc/articles/PMC3639574/ /pubmed/23630340 http://dx.doi.org/10.1085/jgp.201310961 Text en © 2013 Hollingworth and Baylor This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Research Article
Hollingworth, Stephen
Baylor, Stephen M.
Comparison of myoplasmic calcium movements during excitation–contraction coupling in frog twitch and mouse fast-twitch muscle fibers
title Comparison of myoplasmic calcium movements during excitation–contraction coupling in frog twitch and mouse fast-twitch muscle fibers
title_full Comparison of myoplasmic calcium movements during excitation–contraction coupling in frog twitch and mouse fast-twitch muscle fibers
title_fullStr Comparison of myoplasmic calcium movements during excitation–contraction coupling in frog twitch and mouse fast-twitch muscle fibers
title_full_unstemmed Comparison of myoplasmic calcium movements during excitation–contraction coupling in frog twitch and mouse fast-twitch muscle fibers
title_short Comparison of myoplasmic calcium movements during excitation–contraction coupling in frog twitch and mouse fast-twitch muscle fibers
title_sort comparison of myoplasmic calcium movements during excitation–contraction coupling in frog twitch and mouse fast-twitch muscle fibers
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3639574/
https://www.ncbi.nlm.nih.gov/pubmed/23630340
http://dx.doi.org/10.1085/jgp.201310961
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