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

TL;DR

This study reveals that embryonic gut peristalsis is driven by inter-cellular calcium waves in smooth muscle, which are mechanosensitive and form the basis of early digestive movements.

Contribution

It demonstrates that calcium wave propagation in embryonic gut smooth muscle underlies primitive peristalsis and is triggered by mechanical stimuli, revealing a fundamental mechanism of gut motility development.

Findings

Calcium waves propagate via gap junctions in embryonic gut smooth muscle.

Mechanical stimuli induce contractile calcium waves, showing mechanosensitivity.

Inter-cellular tension does not influence calcium wave propagation.

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 transverse sections 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 an ubiquitous dynamic signaling mechanism in biology: here I show that they are the foundation of digestive movements in the developing embryo.