Relationships Between Distention-, Butyrate- and Pellet-Induced Stimulation of Peristalsis in the Mouse Colon

Background/AimsLuminal factors such as short-chain fatty acids are increasingly recognized for playing a regulatory role in peristaltic activity. Our objective was to understand the roles of butyrate and propionate in regulating peristaltic activity in relation to distention-induced activities.Metho...

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Main Authors: Wei Tan, Grace Lee, Ji-Hong Chen, Jan D. Huizinga
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-02-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fphys.2020.00109/full
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spelling doaj-1b68783272dd41209d83f8272f5648b42020-11-25T02:11:45ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-02-011110.3389/fphys.2020.00109509617Relationships Between Distention-, Butyrate- and Pellet-Induced Stimulation of Peristalsis in the Mouse ColonWei Tan0Wei Tan1Grace Lee2Ji-Hong Chen3Jan D. Huizinga4Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, ChinaDepartment of Medicine, Division of Gastroenterology, Farncombe Family Digestive Health Research Institute, McMaster University, Hamilton, ON, CanadaDepartment of Medicine, Division of Gastroenterology, Farncombe Family Digestive Health Research Institute, McMaster University, Hamilton, ON, CanadaDepartment of Medicine, Division of Gastroenterology, Farncombe Family Digestive Health Research Institute, McMaster University, Hamilton, ON, CanadaDepartment of Medicine, Division of Gastroenterology, Farncombe Family Digestive Health Research Institute, McMaster University, Hamilton, ON, CanadaBackground/AimsLuminal factors such as short-chain fatty acids are increasingly recognized for playing a regulatory role in peristaltic activity. Our objective was to understand the roles of butyrate and propionate in regulating peristaltic activity in relation to distention-induced activities.MethodsButyrate and propionate were perfused intraluminally under varying intraluminal pressures in murine colons bathed in Krebs solution. We used video recording and spatiotemporal maps to examine peristalsis induced by the intrinsic rhythmic colonic motor complex (CMC) as well as pellet-induced peristaltic reflex movements.ResultsThe CMC showed several configurations at different levels of excitation, culminating in long distance contractions (LDCs) which possess a triangular shape in murine colon spatiotemporal maps. Butyrate increased the frequency of CMCs but was a much weaker stimulus than distention and only contributed to significant changes under low distention. Propionate inhibited CMCs by decreasing either their amplitudes or frequencies, but only in low distention conditions. Butyrate did not consistently counteract propionate-induced inhibition likely due to the multiple and distinct mechanisms of action for these signaling molecules in the lumen. Pellet movement occurred through ongoing CMCs as well as pellet induced peristaltic reflex movements and butyrate augmented both types of peristaltic motor patterns to decrease the amount of time required to expel each pellet.ConclusionsButyrate is effective in promoting peristalsis, but only when the level of colonic activity is low such as under conditions of low intraluminal pressure. This suggests that it may play a significant role in patients with poor fiber intake, where there is low mechanical stimulation in the lumen.https://www.frontiersin.org/article/10.3389/fphys.2020.00109/fullbutyratepropionateperistalsisperistaltic reflexcolonic motility
collection DOAJ
language English
format Article
sources DOAJ
author Wei Tan
Wei Tan
Grace Lee
Ji-Hong Chen
Jan D. Huizinga
spellingShingle Wei Tan
Wei Tan
Grace Lee
Ji-Hong Chen
Jan D. Huizinga
Relationships Between Distention-, Butyrate- and Pellet-Induced Stimulation of Peristalsis in the Mouse Colon
Frontiers in Physiology
butyrate
propionate
peristalsis
peristaltic reflex
colonic motility
author_facet Wei Tan
Wei Tan
Grace Lee
Ji-Hong Chen
Jan D. Huizinga
author_sort Wei Tan
title Relationships Between Distention-, Butyrate- and Pellet-Induced Stimulation of Peristalsis in the Mouse Colon
title_short Relationships Between Distention-, Butyrate- and Pellet-Induced Stimulation of Peristalsis in the Mouse Colon
title_full Relationships Between Distention-, Butyrate- and Pellet-Induced Stimulation of Peristalsis in the Mouse Colon
title_fullStr Relationships Between Distention-, Butyrate- and Pellet-Induced Stimulation of Peristalsis in the Mouse Colon
title_full_unstemmed Relationships Between Distention-, Butyrate- and Pellet-Induced Stimulation of Peristalsis in the Mouse Colon
title_sort relationships between distention-, butyrate- and pellet-induced stimulation of peristalsis in the mouse colon
publisher Frontiers Media S.A.
series Frontiers in Physiology
issn 1664-042X
publishDate 2020-02-01
description Background/AimsLuminal factors such as short-chain fatty acids are increasingly recognized for playing a regulatory role in peristaltic activity. Our objective was to understand the roles of butyrate and propionate in regulating peristaltic activity in relation to distention-induced activities.MethodsButyrate and propionate were perfused intraluminally under varying intraluminal pressures in murine colons bathed in Krebs solution. We used video recording and spatiotemporal maps to examine peristalsis induced by the intrinsic rhythmic colonic motor complex (CMC) as well as pellet-induced peristaltic reflex movements.ResultsThe CMC showed several configurations at different levels of excitation, culminating in long distance contractions (LDCs) which possess a triangular shape in murine colon spatiotemporal maps. Butyrate increased the frequency of CMCs but was a much weaker stimulus than distention and only contributed to significant changes under low distention. Propionate inhibited CMCs by decreasing either their amplitudes or frequencies, but only in low distention conditions. Butyrate did not consistently counteract propionate-induced inhibition likely due to the multiple and distinct mechanisms of action for these signaling molecules in the lumen. Pellet movement occurred through ongoing CMCs as well as pellet induced peristaltic reflex movements and butyrate augmented both types of peristaltic motor patterns to decrease the amount of time required to expel each pellet.ConclusionsButyrate is effective in promoting peristalsis, but only when the level of colonic activity is low such as under conditions of low intraluminal pressure. This suggests that it may play a significant role in patients with poor fiber intake, where there is low mechanical stimulation in the lumen.
topic butyrate
propionate
peristalsis
peristaltic reflex
colonic motility
url https://www.frontiersin.org/article/10.3389/fphys.2020.00109/full
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