Wnt/β-Catenin Signaling Controls Spatio-Temporal Elasticity Patterns in Extracellular Matrix during Hydra Morphogenesis

Abstract

Albeit ample evidence has suggested the remodeling of extracellular matrix (ECM) in animals plays crucial roles in development and diseases, little is understood how ECM mechanics correlates with tissue morphogenesis. In this study, we quantitatively determined how spatio-temporal elasticity patterns in ECM change during the asexual reproduction of freshwater polyp Hydra. We first determined the mesoscopic protein arrangement in Hydra ECM (mesoglea) by grazing-incidence small-angle X-ray scattering with nano-beam (nano-GISAXS). Our data unraveled fibrillar type I collagen in Hydra mesoglea (Hcol-I) takes an anisotropic, more strongly distorted hexagonal lattice compared to those in vertebrates that could be attributed to the lower proline content and lack of lysin-crosslinks in Hcol-1 fibers. Then, we "mapped" the spatio-temporal changes in ECM stiffness ex vivo with aid of nano-indentation. We identified three representative elasticity patterns during tissue growth along the oral-aboral body axis of the animals. Our complementary proteome analysis demonstrated that the elasticity patterns of the ECM correlate with a gradient like distribution of proteases. Perturbations of the oral Wnt/{beta}-catenin signaling center further indicated that ECM elasticity patterns are governed by Wnt/{beta}-catenin signaling. The ex vivo biomechanical phenotyping of Hydra mesoglea established in this study will help us gain comprehensive insights into the spatio-temporal coordination of biochemical and biomechanical cues in tissue morphogenesis in vivo.