Wnt/β-Catenin Signaling Controls Spatio-Temporal Elasticity Patterns in Extracellular Matrix during<i>Hydra</i>Morphogenesis

Veschgini, Mariam; Petersen, Hendrik O.; Kaufmann, Stefan; Abuillan, Wasim; Suzuki, Ryo; Burghammer, Manfred; Özbek, Suat; Tanaka, Motomu

doi:10.1101/214718

Cited by 3 publications

(6 citation statements)

References 61 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…5d,e) and in intact animals the number of buds was increased (53). This suggests a softening of bud tissue, which otherwise has a high intercellular tension (61). Our data are related to other patterning events, e.g.…”

Section: Hippo-yap Signaling In Symmetrysupporting

confidence: 57%

“…This is also consistent with siYAP knockdowns showing an increase in the number of buds in the budding region. This tissue has a higher intercellular tension than the upper gastric region (61), so that a loss of Yap could contribute to the softening of the tissue (see Discussion). Moreover, the highly fluctuating 𝑀 ̂2 of the siYAP tissue (Fig.…”

Section: Hippo-yap Signaling Acts During Symmetry Breaking Inmentioning

confidence: 97%

See 1 more Smart Citation

Spatio-temporal Coordination of Active Deformation Forces and Wnt / Hippo-Yap Signaling inHydraRegeneration

Suzuki,

Hiraiwa,

Tursch

et al. 2023

Preprint

View full text Add to dashboard Cite

Ample evidence suggests that Wnt signaling and tissue deformation are key determinants for pattern formation in animals. The coordination of these biochemical and biomechanical spatio temporal asymmetries is often unknown or controversial. We investigated this relationship by studying regeneration in the freshwater polyp Hydra. In both reaggregates of dissociated cells and tissue regenerates we found significant tissue contraction waves and upregulation of Wnt signaling. Applying a simple mechanical model to the mode analysis of the active deformations, we quantitatively defined the phase reversal of size change and axial deformation in those oscillations as the time point of biomechanical symmetry breaking. Moreover, overexpression and inhibition of canonical Wnt signaling modulated the timing of this biomechanical symmetry breaking. A direct comparison with the RNAseq data indicates that the biomechanical symmetry breaking occurs only after the upregulation of canonical Wnt signaling. Further data suggest that biochemical signaling and biomechanical active deformation synergistically stabilize the body axis and hence the following head structure formation by Hippo-Yap signaling. The symmetry breaking mechanism identified here in Hydra most likely represents a patterning module that is evolutionary conserved from early metazoan to bilaterian animals.

show abstract

Section: Hippo-yap Signaling In Symmetrysupporting

confidence: 57%

Section: Hippo-yap Signaling Acts During Symmetry Breaking Inmentioning

confidence: 97%

Spatio-temporal Coordination of Active Deformation Forces and Wnt / Hippo-Yap Signaling inHydraRegeneration

Suzuki,

Hiraiwa,

Tursch

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…Additionally to its role as an important transcriptional co-factor in cell nuclei, the membrane-associated distribution of β -Catenin in other body regions indicates its function in Hydra tissue mechanics [21,40,41,44], such as in cell-cell adhesions [71]. Furthermore, β -Catenin expression levels have been recently linked to ECM elasticity [100], which in turn plays an important chemical and mechanical role during pattern formation and regeneration. It has been also recently shown that even external biotic or abiotic environmental cues affect β -Catenin mediated signaling and pattern formation [12, 90].…”

Section: Resultsmentioning

confidence: 99%

“…Thus, it seems to be unlikely that the head organizer formation solely depends on β -catenin/Tcf activity considering the variety of extrinsic and intrinsic factors modulating β -catenin/Tcf levels in Hydra , e.g. [12, 36, 44, 77, 90, 100].…”

Section: Resultsmentioning

confidence: 99%

Two separate but interconnected pattern formation systems are required to control body-axis and head-organiser formation inHydra

Mercker

Lengfeld

Höger

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Formation of the body axes and the subsequent formation of the apical termini are two fundamental steps during animal development. In Hydra, nuclear β-Catenin and canonical HyWnt3 were identified as major players active in both processes. Based on molecular knowledge of canonical Wnt signaling directly linking nuclear Beta-Catenin and HyWnt3 activity, it was frequently assumed that de novo axis formation and the head formation were part of the same pattern formation system. In this work, combining new model simulations with available experimental results, we demonstrate that nuclear Beta-Catenin and HyWnt3 most likely contribute to two separate de novo pattern formation systems in Hydra, organizing development and differentiation on two different spatial scales. In particular, our results suggest that the nuclear Beta-Catenin acts on the scale of the whole body, controlling axis formation, whereas canonical HyWnt3 signaling is involved in a downstream pathway responsible for small-scale patterning of the head. Consequently, also in other animals where axis formation was ascribed to canonical Wnt signaling, the underlying mechanisms may be more complex than previously assumed.

show abstract

“…It is clearly possible that the deformations and stresses induced by the osmotic oscillations are differently transmitted and have different effects on these different layers, a refinement which will need to be addressed in the future. In particular, it was recently suggested that the mechanical properties of the ECM, which were not specifically measured here, could be linked to morphogenesis in Hydra (54).…”

Section: Discussionmentioning

confidence: 96%

Mechanical characterization of regeneratingHydratissue spheres

Perros,

Biquet-Bisquert,

Ben Meriem

et al. 2023

Preprint

View full text Add to dashboard Cite

Hydra vulgaris has long been known for its remarkable regenerative capabilities. As such, they are an historical inspiration for reaction-diffusion systems trying to explain their spontaneous patterning. Recently, it became clear that their patterning is an integrated mechano-chemical process where morphogen dynamics is influenced by tissue mechanics. One roadblock to understand their self-organization is our lack of knowledge about the mechanical properties of these organisms. In this paper, we combined microfluidic developments to perform parallelized microaspiration rheological experiments and numerical simulations to fully characterize these mechanical properties. We found three different behaviors depending on the amount of applied stresses: an elastic response, a visco-elastic one and tissue rupture. Using rheological models of deformable shells, we quantify their elastic modulus, effective viscosity as well as the critical stresses required to switch between behaviors. Based on these experimental results, we propose a full description of the internal tissue mechanics during normal regeneration. Our results provide the first step towards the development of original mechano-chemical models of patterning grounded in quantitative, experimental data.

show abstract

Wnt/β-Catenin Signaling Controls Spatio-Temporal Elasticity Patterns in Extracellular Matrix duringHydraMorphogenesis

Cited by 3 publications

References 61 publications

Spatio-temporal Coordination of Active Deformation Forces and Wnt / Hippo-Yap Signaling inHydraRegeneration

Spatio-temporal Coordination of Active Deformation Forces and Wnt / Hippo-Yap Signaling inHydraRegeneration

Two separate but interconnected pattern formation systems are required to control body-axis and head-organiser formation inHydra

Mechanical characterization of regeneratingHydratissue spheres

Contact Info

Product

Resources

About