On the Mechanisms Whereby Temperature Affects Excitation-Contraction Coupling in Smooth Muscle

Moderate cooling of smooth muscle can modulate force production and may contribute to pathophysiological conditions, but the mechanisms underlying its effects are poorly understood. Interestingly, cooling increases force in rat ureter, but decreases it in guinea pigs. Therefore, this study used uret...

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Main Authors: Burdyga, Theodor V., Wray, Susan
Format: Online
Language:English
Published: The Rockefeller University Press 2002
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2233859/
id pubmed-2233859
recordtype oai_dc
spelling pubmed-22338592008-04-21 On the Mechanisms Whereby Temperature Affects Excitation-Contraction Coupling in Smooth Muscle Burdyga, Theodor V. Wray, Susan Original Article Moderate cooling of smooth muscle can modulate force production and may contribute to pathophysiological conditions, but the mechanisms underlying its effects are poorly understood. Interestingly, cooling increases force in rat ureter, but decreases it in guinea pigs. Therefore, this study used ureteric smooth muscle as a model system to elucidate the mechanisms of the effects of cooling on excitation-contraction coupling. Simultaneous recordings of force, intracellular [Ca2+], and electrical activity were made in intact ureter and ionic currents measured in isolated cells. The increase in force amplitude in rat ureter with cooling was found to be due to a significant increase in the duration of the Ca2+ transient. This in turn was due to a marked prolongation of the action potential. In guinea pigs, both these parameters were much less affected by cooling. Examination of membrane currents revealed that differences in ion channel contribution to the action potential underlie these differences. In particular, cooling potentiated Ca2+-activated Cl− currents, which are present in rat but not guinea pig ureteric smooth muscle, and prolonged the plateau of the action potential and Ca2+ entry. The force-Ca2+ relationship revealed that the increased duration of the Ca2+ transient was sufficient in the rat, but not in the guinea pig, to overcome kinetic lags produced in both species by cooling and potentiate force. Ca2+ entry and release processes were largely temperature-insensitive, but the rate of relaxation was very temperature-sensitive. Effects of cooling on myosin light chain phosphatase, confirmed in experiments using calyculin A, appear to be the predominant mechanisms affecting relaxation. Thus, smooth muscle is diverse in its response to temperature, even when experimental variables, such as the mode of stimulation, are removed. Although the biochemical and mechanical events accompanying contraction are likely to be affected in similar ways by temperature, differences in electrical events lead to subsequent differences in these processes between smooth muscles. The Rockefeller University Press 2002-01-01 /pmc/articles/PMC2233859/ /pubmed/11773241 Text en © 2002 The Rockefeller University Press 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 4.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/4.0/).
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Burdyga, Theodor V.
Wray, Susan
spellingShingle Burdyga, Theodor V.
Wray, Susan
On the Mechanisms Whereby Temperature Affects Excitation-Contraction Coupling in Smooth Muscle
author_facet Burdyga, Theodor V.
Wray, Susan
author_sort Burdyga, Theodor V.
title On the Mechanisms Whereby Temperature Affects Excitation-Contraction Coupling in Smooth Muscle
title_short On the Mechanisms Whereby Temperature Affects Excitation-Contraction Coupling in Smooth Muscle
title_full On the Mechanisms Whereby Temperature Affects Excitation-Contraction Coupling in Smooth Muscle
title_fullStr On the Mechanisms Whereby Temperature Affects Excitation-Contraction Coupling in Smooth Muscle
title_full_unstemmed On the Mechanisms Whereby Temperature Affects Excitation-Contraction Coupling in Smooth Muscle
title_sort on the mechanisms whereby temperature affects excitation-contraction coupling in smooth muscle
description Moderate cooling of smooth muscle can modulate force production and may contribute to pathophysiological conditions, but the mechanisms underlying its effects are poorly understood. Interestingly, cooling increases force in rat ureter, but decreases it in guinea pigs. Therefore, this study used ureteric smooth muscle as a model system to elucidate the mechanisms of the effects of cooling on excitation-contraction coupling. Simultaneous recordings of force, intracellular [Ca2+], and electrical activity were made in intact ureter and ionic currents measured in isolated cells. The increase in force amplitude in rat ureter with cooling was found to be due to a significant increase in the duration of the Ca2+ transient. This in turn was due to a marked prolongation of the action potential. In guinea pigs, both these parameters were much less affected by cooling. Examination of membrane currents revealed that differences in ion channel contribution to the action potential underlie these differences. In particular, cooling potentiated Ca2+-activated Cl− currents, which are present in rat but not guinea pig ureteric smooth muscle, and prolonged the plateau of the action potential and Ca2+ entry. The force-Ca2+ relationship revealed that the increased duration of the Ca2+ transient was sufficient in the rat, but not in the guinea pig, to overcome kinetic lags produced in both species by cooling and potentiate force. Ca2+ entry and release processes were largely temperature-insensitive, but the rate of relaxation was very temperature-sensitive. Effects of cooling on myosin light chain phosphatase, confirmed in experiments using calyculin A, appear to be the predominant mechanisms affecting relaxation. Thus, smooth muscle is diverse in its response to temperature, even when experimental variables, such as the mode of stimulation, are removed. Although the biochemical and mechanical events accompanying contraction are likely to be affected in similar ways by temperature, differences in electrical events lead to subsequent differences in these processes between smooth muscles.
publisher The Rockefeller University Press
publishDate 2002
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2233859/
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