iScience (Apr 2023)

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,
  • Stefan Kaufmann,
  • Manfred Burghammer,
  • Ulrike Engel,
  • Frank Stein,
  • Suat Özbek,
  • Thomas W. Holstein,
  • Motomu Tanaka

Journal volume & issue
Vol. 26, no. 4
p. 106416

Abstract

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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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