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Wnt/β-catenin signaling induces axial elasticity patterns of Hydra extracellular matrix

Mariam Veschgini,Ryo Suzuki,Svenja Kling,Hendrik O. Petersen,Bruno Gideon Bergheim,Wasim Abuillan,Philipp Linke,S. Kaufmann,M. Burghammer,U. Engel,F. Stein,S. Özbek,T. Holstein,Motomu Tanaka

Published 2023 in iScience

ABSTRACT

Summary The extracellular matrix (ECM) plays crucial roles in animal development and diseases. Here, we report that Wnt/β-catenin signaling induces the ECM remodeling during Hydra axis formation. We determined the micro- and nanoscopic arrangement of fibrillar type I collagen along Hydra’s body axis using high-resolution microscopy and X-ray scattering. Elasticity mapping of the ECM ex vivo revealed distinctive elasticity patterns along the body axis. A proteomic analysis of the ECM showed that these elasticity patterns correlate with a gradient-like distribution of metalloproteases along the body axis. Activation of the Wnt/β-catenin pathway in wild-type and transgenic animals alters these patterns toward low ECM elasticity patterns. This suggests a mechanism whereby high protease activity under control of Wnt/β-catenin signaling causes remodeling and softening of the ECM. This Wnt-dependent spatiotemporal coordination of biochemical and biomechanical cues in ECM formation was likely a central evolutionary innovation for animal tissue morphogenesis.

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