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
Affiliations
Mariam Veschgini
Physical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, D69120 Heidelberg, Germany
Ryo Suzuki
Physical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, D69120 Heidelberg, Germany; Center for Integrated Medicine and Physics, Institute for Advanced Study, Kyoto University, Kyoto 606-8501, Japan
Svenja Kling
Molecular Evolution and Genomics, Centre for Organismal Studies, Heidelberg University, D69120 Heidelberg, Germany
Hendrik O. Petersen
Molecular Evolution and Genomics, Centre for Organismal Studies, Heidelberg University, D69120 Heidelberg, Germany
Bruno Gideon Bergheim
Molecular Evolution and Genomics, Centre for Organismal Studies, Heidelberg University, D69120 Heidelberg, Germany
Wasim Abuillan
Physical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, D69120 Heidelberg, Germany
Philipp Linke
Physical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, D69120 Heidelberg, Germany
Stefan Kaufmann
Physical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, D69120 Heidelberg, Germany
Manfred Burghammer
European Synchrotron Radiation Facility, F38000 Grenoble, France
Ulrike Engel
Molecular Evolution and Genomics, Centre for Organismal Studies, Heidelberg University, D69120 Heidelberg, Germany; Nikon Imaging Center, Heidelberg University, D69120 Heidelberg, Germany
Frank Stein
European Molecular Biology Laboratory, Meyerhofstrasse 1, D69117 Heidelberg, Germany
Suat Özbek
Molecular Evolution and Genomics, Centre for Organismal Studies, Heidelberg University, D69120 Heidelberg, Germany
Thomas W. Holstein
Center for Integrated Medicine and Physics, Institute for Advanced Study, Kyoto University, Kyoto 606-8501, Japan; Molecular Evolution and Genomics, Centre for Organismal Studies, Heidelberg University, D69120 Heidelberg, Germany; Corresponding author
Motomu Tanaka
Physical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, D69120 Heidelberg, Germany; Center for Integrated Medicine and Physics, Institute for Advanced Study, Kyoto University, Kyoto 606-8501, Japan; Corresponding author
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.
