Mechanical oscillations orchestrate axial patterning through Wnt activation in
            <i>Hydra</i>

Ferenc, Jaroslav; Papasaikas, Panagiotis; Ferralli, Jacqueline; Nakamura, Yukio; Smallwood, Sébastien A.; Tsiairis, Charisios D.

doi:10.1126/sciadv.abj6897

Cited by 30 publications

(42 citation statements)

References 60 publications

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“…3J) (Lengfeld et al 2009; Hobmayer et al 2000; Gee et al 2010; Broun et al 2005), gata1-3 as a regulator of aboral tissue (Fig. 3K) (Ferenc et al 2021), and zic4 as a regulator of epithelial tentacle tissue (Supplemental Fig. S13J) (Vogg et al 2021).…”

Section: Resultsmentioning

confidence: 99%

New Hydra genomes reveal conserved principles of hydrozoan transcriptional regulation

Cazet¹,

Siebert

Little³

et al. 2022

Preprint

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The epithelial and interstitial stem cells of the freshwater polyp Hydra are the best characterized stem cell systems in any cnidarian, providing valuable insight into cell type evolution and the origin of stemness in animals. However, little is known about the transcriptional regulatory mechanisms that determine how these stem cells are maintained and how they give rise to their diverse differentiated progeny. To address such questions, a thorough understanding of transcriptional regulation in Hydra is needed. To this end, we generated extensive new resources for characterizing transcriptional regulation in Hydra, including new genome assemblies for Hydra oligactis and the AEP strain of Hydra vulgaris, an updated whole-animal single-cell RNA-seq atlas, and genome-wide maps of chromatin interactions, chromatin accessibility, sequence conservation, and histone modifications. These data revealed the existence of large chromatin interaction domains in the Hydra genome that likely influence transcriptional regulation in a manner distinct from topologically associating domains in bilaterians. We also uncovered the transcriptomic profiles of two previously molecularly uncharacterized cell types, isorhiza-containing nematocytes and somatic gonad ectoderm. We identified novel candidate regulators of cell-type-specific transcription, several of which have likely been conserved at least since the divergence of Hydra and the jellyfish Clytia hemisphaerica over 200 million years ago. The resources generated in this study, which collectively represent the most comprehensive characterization of transcriptional regulation in a cnidarian to date, are accessible through a newly created genome portal, available at research.nhgri.nih.gov/HydraAEP/.

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Section: Resultsmentioning

confidence: 99%

New Hydra genomes reveal conserved principles of hydrozoan transcriptional regulation

Cazet¹,

Siebert

Little³

et al. 2022

Preprint

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“…Traditionally, inflation is induced and studied in lumenized structures by using pharmaceutical agents targeting ion channels (39)(40)(41)(42) and osmotic flow (43). Here we evaluated the effect of the commonly used drug forskolin, which acts by elevating cyclic AMP (cAMP) levels to trigger downstream protein kinase A (PKA) and the apical chloride channel 'chloride channel cystic fibrosis transmembrane conductance regula-tor' (CFTR) (Supplementary Fig.…”

Section: Resultsmentioning

confidence: 99%

Pump it up: bioelectric stimulation controls tissue shape and size

Shim

Breinyn

Martínez-Calvo

et al. 2022

Preprint

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Epithelial tissues sheath many organs, separating 'outside' from 'inside' and exquisitely regulating ion and water transport via electromechanical pumping to maintain homeostatic balance and tissue hydrostatic pressure. While it is becoming increasingly clear that the ionic microenvironment and external electric stimuli can affect epithelial function and behavior, the coupling between electrical perturbation and tissue form remain unclear. We investigated this by combining electrical stimulation with three-dimensional epithelial tissues with hollow 'lumens'--both kidney cysts and complex intestinal stem cell organoids. Our core finding is that physiological strength electrical stimulation of order 1-3 V/cm (with both direct and alternating currents) can drive powerful and rapid inflation of hollow tissues through a process we call 'electro-inflation', inducing a nearly threefold increase in tissue volume and striking asymmetries in tissue form. Electro-inflation is primarily driven by activation of the CFTR ion channel pumping chloride into the tissue, causing water to osmotically flow. This influx generates hydrostatic pressure, and inflation results from a competition between this pressure and cell cytoskeletal tension. We validated these interpretations with computational models connecting ion dynamics in the Diffuse Double Layer around tissues to tissue mechanics. Electro-inflation is a unique biophysical process to study and control complex tissue function.

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“…The foot- and tentacle-specific markers were selected on the basis of the average expression profiles in the positional RNA-seq data ( 74 ). Genes with low expression were first filtered out of this dataset (average CPM ≤ 200 in the body part with the lowest expression), and the remaining values were normalized for each gene to the body position with its maximum expression.…”

Section: Methodsmentioning

confidence: 99%

The transcription factor Zic4 promotes tentacle formation and prevents epithelial transdifferentiation in Hydra

et al. 2022

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The molecular mechanisms that maintain cellular identities and prevent dedifferentiation or transdifferentiation remain mysterious. However, both processes are transiently used during animal regeneration. Therefore, organisms that regenerate their organs, appendages, or even their whole body offer a fruitful paradigm to investigate the regulation of cell fate stability. Here, we used Hydra as a model system and show that Zic4, whose expression is controlled by Wnt3/β-catenin signaling and the Sp5 transcription factor, plays a key role in tentacle formation and tentacle maintenance. Reducing Zic4 expression suffices to induce transdifferentiation of tentacle epithelial cells into foot epithelial cells. This switch requires the reentry of tentacle battery cells into the cell cycle without cell division and is accompanied by degeneration of nematocytes embedded in these cells. These results indicate that maintenance of cell fate by a Wnt-controlled mechanism is a key process both during homeostasis and during regeneration.

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Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra

Abstract: Mechanochemical feedback drives patterning in Hydra tissue during regeneration.

Cited by 30 publications

References 60 publications

New Hydra genomes reveal conserved principles of hydrozoan transcriptional regulation

New Hydra genomes reveal conserved principles of hydrozoan transcriptional regulation

Pump it up: bioelectric stimulation controls tissue shape and size

The transcription factor Zic4 promotes tentacle formation and prevents epithelial transdifferentiation in Hydra

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