Literature DB >> 30249773

The first digestive movements in the embryo are mediated by mechanosensitive smooth muscle calcium waves.

Nicolas R Chevalier1.   

Abstract

Peristalsis enables transport of the food bolus in the gut. Here, I show by dynamic ex vivo intra-cellular calcium imaging on living embryonic gut explants that the most primitive form of peristalsis that occurs in the embryo is the result of inter-cellular, gap-junction-dependent calcium waves that propagate in the circular smooth muscle layer. I show that the embryonic gut is an intrinsically mechanosensitive organ, as the slightest externally applied mechanical stimulus triggers contractile waves. This dynamic response is an embryonic precursor of the 'law of the intestine' (peristaltic reflex). I show how characteristic features of early peristalsis such as counter-propagating wave annihilation, mechanosensitivity and nucleation after wounding all result from known properties of calcium waves. I finally demonstrate that inter-cellular mechanical tension does not play a role in the propagation mechanism of gut contractile waves, unlike what has been recently shown for the embryonic heartbeat. Calcium waves are a ubiquitous dynamic signalling mechanism in biology: here I show that they are the foundation of digestive movements in the developing embryo.This article is part of the Theo Murphy meeting issue on 'Mechanics of development'.
© 2018 The Author(s).

Entities:  

Keywords:  calcium imaging; embryonic gut; gap junctions; mechanosensitivity; motility; peristalsis

Mesh:

Substances:

Year:  2018        PMID: 30249773      PMCID: PMC6158196          DOI: 10.1098/rstb.2017.0322

Source DB:  PubMed          Journal:  Philos Trans R Soc Lond B Biol Sci        ISSN: 0962-8436            Impact factor:   6.237


  34 in total

1.  Reentrant waves in a ring of embryonic chick ventricular cells imaged with a Ca2+ sensitive dye.

Authors:  Hortensia González; Yoshihiko Nagai; G Bub; Leon Glass; Alvin Shrier
Journal:  Biosystems       Date:  2003-09       Impact factor: 1.973

2.  The first intestinal motility patterns in fetal mice are not mediated by neurons or interstitial cells of Cajal.

Authors:  Rachael R Roberts; Melina Ellis; Rachel M Gwynne; Annette J Bergner; Martin D Lewis; Elizabeth A Beckett; Joel C Bornstein; Heather M Young
Journal:  J Physiol       Date:  2010-02-08       Impact factor: 5.182

Review 3.  The emergence of neural activity and its role in the development of the enteric nervous system.

Authors:  Marlene M Hao; Joel C Bornstein; Pieter Vanden Berghe; Alan E Lomax; Heather M Young; Jaime P P Foong
Journal:  Dev Biol       Date:  2012-12-19       Impact factor: 3.582

4.  Microfluidic chest cavities reveal that transmural pressure controls the rate of lung development.

Authors:  Celeste M Nelson; Jason P Gleghorn; Mei-Fong Pang; Jacob M Jaslove; Katharine Goodwin; Victor D Varner; Erin Miller; Derek C Radisky; Howard A Stone
Journal:  Development       Date:  2017-10-30       Impact factor: 6.868

5.  A Gαq-Ca²⁺ signaling pathway promotes actin-mediated epidermal wound closure in C. elegans.

Authors:  Suhong Xu; Andrew D Chisholm
Journal:  Curr Biol       Date:  2011-11-17       Impact factor: 10.834

6.  How do injured cells communicate with the surviving cell monolayer?

Authors:  P J Sammak; L E Hinman; P O Tran; M D Sjaastad; T E Machen
Journal:  J Cell Sci       Date:  1997-02       Impact factor: 5.285

7.  Ca2+ responses in enteric glia are mediated by connexin-43 hemichannels and modulate colonic transit in mice.

Authors:  Jonathon McClain; Vladimir Grubišić; David Fried; Roberto A Gomez-Suarez; Gina M Leinninger; Jean Sévigny; Vladimir Parpura; Brian D Gulbransen
Journal:  Gastroenterology       Date:  2013-11-06       Impact factor: 22.682

Review 8.  The gut as a neurological organ.

Authors:  P Holzer; R Schicho; U Holzer-Petsche; I T Lippe
Journal:  Wien Klin Wochenschr       Date:  2001-09-17       Impact factor: 1.704

9.  Theoretical analysis of calcium wave propagation based on inositol (1,4,5)-trisphosphate (InsP3) receptor functional properties.

Authors:  I Bezprozvanny
Journal:  Cell Calcium       Date:  1994-09       Impact factor: 6.817

10.  Origin of the c-kit-positive interstitial cells in the avian bowel.

Authors:  L Lecoin; G Gabella; N Le Douarin
Journal:  Development       Date:  1996-03       Impact factor: 6.868

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  5 in total

1.  Embryogenesis of the peristaltic reflex.

Authors:  Nicolas R Chevalier; Nicolas Dacher; Cécile Jacques; Lucas Langlois; Chloé Guedj; Orestis Faklaris
Journal:  J Physiol       Date:  2019-04-21       Impact factor: 5.182

2.  Mechanics of development.

Authors:  Niamh C Nowlan; Philippa Francis-West; Celeste Nelson
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2018-09-24       Impact factor: 6.237

3.  Genetic and Mechanical Regulation of Intestinal Smooth Muscle Development.

Authors:  Tyler R Huycke; Bess M Miller; Hasreet K Gill; Nandan L Nerurkar; David Sprinzak; L Mahadevan; Clifford J Tabin
Journal:  Cell       Date:  2019-09-19       Impact factor: 41.582

4.  Smooth muscle contractility causes the gut to grow anisotropically.

Authors:  Diana Khalipina; Yusuke Kaga; Nicolas Dacher; Nicolas R Chevalier
Journal:  J R Soc Interface       Date:  2019-10-09       Impact factor: 4.118

5.  Distribution Map of Peristaltic Waves in the Chicken Embryonic Gut Reveals Importance of Enteric Nervous System and Inter-Region Cross Talks Along the Gut Axis.

Authors:  Yuuki Shikaya; Yuta Takase; Ryosuke Tadokoro; Ryo Nakamura; Masafumi Inaba; Yoshiko Takahashi
Journal:  Front Cell Dev Biol       Date:  2022-02-04
  5 in total

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