Mechanical strain focusing at topological defect sites in regenerating Hydra

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Yonit Maroudas-Sacks - , Technion-Israel Institute of Technology (Author)
  • S. Suganthan - , Max-Planck-Institute for the Physics of Complex Systems (Author)
  • Liora Garion - , Technion-Israel Institute of Technology (Author)
  • Yael Ascoli-Abbina - , Technion-Israel Institute of Technology (Author)
  • Ariel Westfried - , Technion-Israel Institute of Technology (Author)
  • Noam Dori - , Technion-Israel Institute of Technology (Author)
  • Iris Pasvinter - , Technion-Israel Institute of Technology (Author)
  • Marko Popović - , Max-Planck-Institute for the Physics of Complex Systems, TUD Dresden University of Technology, Center for Systems Biology Dresden (CSBD), Clusters of Excellence PoL: Physics of Life (Author)
  • Kinneret Keren - , Technion-Israel Institute of Technology (Author)

Abstract

The formation of a new head during Hydra regeneration involves the establishment of a head organizer that functions as a signaling center and contains an aster-shaped topological defect in the organization of the supracellular actomyosin fibers. Here, we show that the future head region in regenerating tissue fragments undergoes multiple instances of extensive stretching and rupture events from the onset of regeneration. These recurring localized tissue deformations arise due to transient contractions of the supracellular ectodermal actomyosin fibers that focus mechanical strain at defect sites. We further show that stabilization of aster-shaped defects is disrupted by perturbations of the Wnt signaling pathway. We propose a closed-loop feedback mechanism promoting head organizer formation, and develop a biophysical model of regenerating Hydra tissues that incorporates a morphogen source activated by mechanical strain and an alignment interaction directing fibers along morphogen gradients. We suggest that this positive-feedback loop leads to mechanical strain focusing at defect sites, enhancing local morphogen production and promoting robust organizer formation.

Details

Original languageEnglish
Article numberdev204514
JournalDevelopment (Cambridge)
Volume152
Issue number4
Publication statusPublished - Feb 2025
Peer-reviewedYes

Keywords

Keywords

  • Actomyosin fibers, Hydra regeneration, Mechanochemical feedback, Morphogenesis, Topological defects