Imaging of Cellular Epiblastic and Sub‐Epiblastic ECM Movements in Avian Primitive Streak Stage Embryos Elucidate Morphogenetic Mechanisms

Abstract

A century of scientific articles has advanced the concept that embryonic cells move ("migrate") in an autonomous fashion. In contrast, the (convective) motion of the extracellular matrix (ECM) has been largely ignored. We developed imaging methods that can measure the extent embryonic cells move ("crawl") relative to the ECM. We have applied these techniques to studying the movements of dorsal/ventral (epiblast/mesoderm) tissues in early‐stage quail embryos. Our time‐lapse data show that epiblastic cells largely move in concert with a sub‐epiblastic extracellular matrix in Stage 2‐3 primitive streak quail embryos. In other words, there is little cellular motion relative to the extracellular matrix scaffold ‐ both components move together as a tissue. The extracellular matrix displacements exhibit bilateral vortical motion, convergence to the midline and extension along the presumptive vertebral axis ‐ all patterns previously attributed solely to cellular "migration". Our time‐resolved data pose new challenges for understanding how extracellular chemical (morphogen) gradients, widely hypothesized to guide cellular trajectories at early gastrulation stages, are maintained in this dynamic extracellular environment. In general, we hope that our new techniques and findings will encourage others in the field to be more rigorous in defining and quantifying cell migration in the embryo.