Application of tissue-scale tension to avian epitheliain vivoto study multiscale mechanics and inter-germ layer coupling

Abstract

As cross-disciplinary approaches drawing from physics and mechanics have increasingly influenced our understanding of morphogenesis, the tools available to measure and perturb physical aspects of embryonic development have expanded as well. However, it remains a challenge to measure mechanical properties and apply exogenous tissue-scale forcesin vivo, particularly for epithelia. Exploiting the size and accessibility of the developing chick embryo, here we describe a simple technique to quantitatively apply exogenous forces on the order of ∼1-100µN to the endodermal epithelium. To demonstrate the utility of this approach, we performed a series of proof-of-concept experiments that reveal fundamental and unexpected mechanical behaviors in the early chick embryo, including mechanotype heterogeneity among cells of the midgut endoderm, complex non-cell autonomous effects of actin disruption, and a high degree of mechanical coupling between the endoderm and adjacent paraxial mesoderm. To illustrate the broader utility of this method, we determined that forces on the order of ∼ 10µN are sufficient to unzip the neural tube during primary neurulation. Together, these findings provide basic insights into the mechanics of embryonic epitheliain vivoin the early avian embryo, and provide a useful tool for future investigations of how morphogenesis is influenced by mechanical factors.Graphical AbstractSummary StatementA simple approach is devised for quantitatively applying tension to epitheliain vivo, and used to study the mechanics of embryonic epithelia in the chick embryo.