Anisotropic stretch biases the self-organization of actin fibers in multicellular Hydra aggregates

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Anaïs Bailles - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Giulia Serafini - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Heino Andreas - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Christoph Zechner - , Max Planck Institute of Molecular Cell Biology and Genetics, Center for Systems Biology Dresden (CSBD), Clusters of Excellence PoL: Physics of Life (Author)
  • Carl D. Modes - , Max Planck Institute of Molecular Cell Biology and Genetics, Center for Systems Biology Dresden (CSBD), Clusters of Excellence PoL: Physics of Life (Author)
  • Pavel Tomancak - , Max Planck Institute of Molecular Cell Biology and Genetics, Center for Systems Biology Dresden (CSBD), Clusters of Excellence PoL: Physics of Life (Author)

Abstract

During development, groups of cells generate shape by coordinating their mechanical properties through an interplay of self-organization and prepatterning. Hydra displays a striking planar pattern of actin fibers at the organism scale, and mechanics influence the morphogenesis of biological structures during its prepatterned regeneration. However, how mechanics participate in the formation of an ordered pattern from a totally disordered state remains unknown. To study this, we used cellular aggregates formed from dissociated Hydra cells, which initially lose all actin polarity yet regenerate a long-range actin pattern. We showed quantitatively that the actin meshwork evolves from a disordered symmetric state to an ordered state in which rotational symmetry is broken, and translation symmetry is partially broken, with the nematic and smectic order parameters increasing over days. During the first hours, the actin meshwork displayed spatial heterogeneity in the nematic order parameter, and ordered domains separated by line defects progressively grew and fused. This suggests that local cell-cell interactions drive the transition from disorder to order. To understand the mechanism of ordering, we perturbed the tissue's physical constraints. We showed that while topology and geometry do not have a direct effect, anisotropic stretch biases the emerging orientation of the actin meshwork within hours. Surprisingly, although a Wnt head organizer is expected to play a role in the actin ordering, the stretch-associated alignment happened without the prior formation of a head organizer. This demonstrates the role of tissue mechanics in the alignment of the actin fibers during the disorder-to-order transition.

Details

Original languageEnglish
Article numbere2423437122
JournalProceedings of the National Academy of Sciences of the United States of America
Volume122
Issue number32
Publication statusPublished - 12 Aug 2025
Peer-reviewedYes

External IDs

PubMed 40758890

Keywords

ASJC Scopus subject areas

Keywords

  • actin, Hydra, nematic order, self-organization, tissue mechanics