Emergence and development of gut motility in the chicken embryo

PLoS One. 2017 Feb 21;12(2):e0172511. doi: 10.1371/journal.pone.0172511. eCollection 2017.

Abstract

The gastrointestinal tract transports the food bolus by peristalsis. Gut motility starts at an early age in the developing embryo, well before it is required for nutrition of the organism. We present a comprehensive kinematic study of the emergence and physiological development of gut motility in all regions of the lower digestive tract of the chicken embryo from embryonic days E5 through E9. We characterized motility emergence time, propagation patterns, speed, frequency and amplitude of peristalsis waves. We found that the emergence of an uninterrupted circular ring of smooth muscle correlated with the appearance of propagative contractile waves, at E6 in the hindgut and midgut, and at E9 in the caecal appendix. We show that peristalsis at these stages is critically dependent on calcium and is not mediated by neurons as gut motility is insensitive to tetrodotoxin and takes place in the hindgut in the absence of neurons. We further demonstrate that motility also matures in ex-vivo organ culture. We compare our results to existing literature on zebrafish, mouse and human motility development, and discuss their chronological relationship with other major developmental events occurring in the chicken embryonic gut at these stages. Our work sets a baseline for further investigations of motility development in this important animal model.

Publication types

  • Video-Audio Media

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium / pharmacology
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels / physiology
  • Cell Movement
  • Chick Embryo / physiology*
  • Cobalt / pharmacology
  • Disease Models, Animal
  • Hirschsprung Disease
  • Intestines / embryology
  • Intestines / innervation
  • Intestines / physiology
  • Muscle, Smooth / embryology
  • Muscle, Smooth / physiology
  • Myenteric Plexus / embryology
  • Neural Crest / cytology
  • Organ Culture Techniques
  • Peristalsis* / drug effects
  • Tetrodotoxin / pharmacology
  • Time-Lapse Imaging

Substances

  • Calcium Channel Blockers
  • Calcium Channels
  • Cobalt
  • Tetrodotoxin
  • cobaltous chloride
  • Calcium

Grants and funding

This research was funded by Agence Nationale de la Recherche (ANR) through "Initiatives d’Excellence" Idex (ANR-11-IDEX-0005-02), and "Labex Who Am I?" (ANR-11-LABX-0071) Collaborative Project (VPG, AA, NRC) and Postdoctoral Fellowship Grants (NRC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.