From depolarization-dependent contractions in gastrointestinal smooth muscle to aortic pulse-synchronized contractions

Sarah B Marion, Allen W MangelRTI Health Solutions, Research Triangle Park, NC, USAAbstract: For decades, it was believed that the diameter of gastrointestinal smooth muscle cells is sufficiently narrow, and that the diffusion of calcium across the plasma membrane is sufficient, to support contract...

Full description

Bibliographic Details
Main Authors: Marion SB, Mangel AW
Format: Article
Language:English
Published: Dove Medical Press 2014-03-01
Series:Clinical and Experimental Gastroenterology
Online Access:http://www.dovepress.com/from-depolarization-dependent-contractions-in-gastrointestinal-smooth--a16269
id doaj-fa0be69d6c8842278f6b7349ce697afa
record_format Article
spelling doaj-fa0be69d6c8842278f6b7349ce697afa2020-11-24T23:22:37ZengDove Medical PressClinical and Experimental Gastroenterology1178-70232014-03-012014default616616269From depolarization-dependent contractions in gastrointestinal smooth muscle to aortic pulse-synchronized contractionsMarion SBMangel AW Sarah B Marion, Allen W MangelRTI Health Solutions, Research Triangle Park, NC, USAAbstract: For decades, it was believed that the diameter of gastrointestinal smooth muscle cells is sufficiently narrow, and that the diffusion of calcium across the plasma membrane is sufficient, to support contractile activity. Thus, depolarization-triggered release of intracellular calcium was not believed to be operative in gastrointestinal smooth muscle. However, after the incubation of muscle segments in solutions devoid of calcium and containing the calcium chelator ethylene glycol tetraacetic acid, an alternative electrical event occurred that was distinct from normal slow waves and spikes. Subsequently, it was demonstrated in gastrointestinal smooth muscle segments that membrane depolarization associated with this alternative electrical event triggered rhythmic contractions by release of intracellular calcium. Although this concept of depolarization-triggered calcium release was iconoclastic, it has now been demonstrated in multiple gastrointestinal smooth muscle preparations. On the basis of these observations, we investigated whether a rhythmic electrical and mechanical event would occur in aortic smooth muscle under the same calcium-free conditions. The incubation of aortic segments in a solution with no added calcium plus ethylene glycol tetraacetic acid induced a fast electrical event without corresponding tension changes. On the basis of the frequency of these fast electrical events, we pursued, contrary to what has been established dogma for more than three centuries, the question of whether the smooth muscle wall of the aorta undergoes rhythmic activation during the cardiac cycle. As with depolarization-triggered contractile activity in gastrointestinal smooth muscle, it was “well known” that rhythmic activation of the aorta does not occur in synchrony with the heartbeat. In a series of experiments, however, it was demonstrated that rhythmic contractions occur in the aortic wall in synchrony with the heartbeat and share a common pacemaker with the heart. We conclude that important observations in the vascular system became derivative from those in the gastrointestinal system. The challenging of scientific dogma potentially leads to the expansion of our fundamental knowledge base.Keywords: gastrointestinal smooth muscle, aortic smooth muscle, contractions, intracellular calcium pools, Windkessel hypothesis, pulse-synchronized contractionshttp://www.dovepress.com/from-depolarization-dependent-contractions-in-gastrointestinal-smooth--a16269
collection DOAJ
language English
format Article
sources DOAJ
author Marion SB
Mangel AW
spellingShingle Marion SB
Mangel AW
From depolarization-dependent contractions in gastrointestinal smooth muscle to aortic pulse-synchronized contractions
Clinical and Experimental Gastroenterology
author_facet Marion SB
Mangel AW
author_sort Marion SB
title From depolarization-dependent contractions in gastrointestinal smooth muscle to aortic pulse-synchronized contractions
title_short From depolarization-dependent contractions in gastrointestinal smooth muscle to aortic pulse-synchronized contractions
title_full From depolarization-dependent contractions in gastrointestinal smooth muscle to aortic pulse-synchronized contractions
title_fullStr From depolarization-dependent contractions in gastrointestinal smooth muscle to aortic pulse-synchronized contractions
title_full_unstemmed From depolarization-dependent contractions in gastrointestinal smooth muscle to aortic pulse-synchronized contractions
title_sort from depolarization-dependent contractions in gastrointestinal smooth muscle to aortic pulse-synchronized contractions
publisher Dove Medical Press
series Clinical and Experimental Gastroenterology
issn 1178-7023
publishDate 2014-03-01
description Sarah B Marion, Allen W MangelRTI Health Solutions, Research Triangle Park, NC, USAAbstract: For decades, it was believed that the diameter of gastrointestinal smooth muscle cells is sufficiently narrow, and that the diffusion of calcium across the plasma membrane is sufficient, to support contractile activity. Thus, depolarization-triggered release of intracellular calcium was not believed to be operative in gastrointestinal smooth muscle. However, after the incubation of muscle segments in solutions devoid of calcium and containing the calcium chelator ethylene glycol tetraacetic acid, an alternative electrical event occurred that was distinct from normal slow waves and spikes. Subsequently, it was demonstrated in gastrointestinal smooth muscle segments that membrane depolarization associated with this alternative electrical event triggered rhythmic contractions by release of intracellular calcium. Although this concept of depolarization-triggered calcium release was iconoclastic, it has now been demonstrated in multiple gastrointestinal smooth muscle preparations. On the basis of these observations, we investigated whether a rhythmic electrical and mechanical event would occur in aortic smooth muscle under the same calcium-free conditions. The incubation of aortic segments in a solution with no added calcium plus ethylene glycol tetraacetic acid induced a fast electrical event without corresponding tension changes. On the basis of the frequency of these fast electrical events, we pursued, contrary to what has been established dogma for more than three centuries, the question of whether the smooth muscle wall of the aorta undergoes rhythmic activation during the cardiac cycle. As with depolarization-triggered contractile activity in gastrointestinal smooth muscle, it was “well known” that rhythmic activation of the aorta does not occur in synchrony with the heartbeat. In a series of experiments, however, it was demonstrated that rhythmic contractions occur in the aortic wall in synchrony with the heartbeat and share a common pacemaker with the heart. We conclude that important observations in the vascular system became derivative from those in the gastrointestinal system. The challenging of scientific dogma potentially leads to the expansion of our fundamental knowledge base.Keywords: gastrointestinal smooth muscle, aortic smooth muscle, contractions, intracellular calcium pools, Windkessel hypothesis, pulse-synchronized contractions
url http://www.dovepress.com/from-depolarization-dependent-contractions-in-gastrointestinal-smooth--a16269
work_keys_str_mv AT marionsb fromdepolarizationdependentcontractionsingastrointestinalsmoothmuscletoaorticpulsesynchronizedcontractions
AT mangelaw fromdepolarizationdependentcontractionsingastrointestinalsmoothmuscletoaorticpulsesynchronizedcontractions
_version_ 1725567309817315328