Bud detachment in hydra requires activation of fibroblast growth factor receptor and a Rho–ROCK–myosin II signaling pathway to ensure formation of a basal constriction

Abstract

Background: Hydra propagates asexually by exporting tissue into a bud, which detaches 4 days later as a fully differentiated young polyp. Prerequisite for detachment is activation of fibroblast growth factor receptor (FGFR) signaling. The mechanism which enables constriction and tissue separation within the monolayered ecto‐ and endodermal epithelia is unknown. Results: Histological sections and staining of F‐actin by phalloidin revealed conspicuous cell shape changes at the bud detachment site indicating a localized generation of mechanical forces and the potential enhancement of secretory functions in ectodermal cells. By gene expression analysis and pharmacological inhibition, we identified a candidate signaling pathway through Rho, ROCK, and myosin II, which controls bud base constriction and rearrangement of the actin cytoskeleton. Specific regional myosin phosphorylation suggests a crucial role of ectodermal cells at the detachment site. Inhibition of FGFR, Rho, ROCK, or myosin II kinase activity is permissive for budding, but represses myosin phosphorylation, rearrangement of F‐actin and constriction. The young polyp remains permanently connected to the parent by a broad tissue bridge. Conclusions: Our data suggest an essential role of FGFR and a Rho‐ROCK‐myosin II pathway in the control of cell shape changes required for bud detachment. Developmental Dynamics 246:502–516, 2017. © 2017 The Authors Developmental Dynamics published by Wiley Periodicals, Inc. on behalf of American Association of Anatomists

Model systems for regeneration: Hydra

“…As such, questions revolving around the properties of individual Hydra cells and their interactions with neighbours are surfacing. Budding and bud detachment in Hydra are associated with distinct changes in cell shape, and recently the FGFR and Rho-ROCK-Myosin pathways have been implicated in these events (Holz et al, 2017). The generation of Lifeact-GFP transgenic Hydra has allowed researchers to trace changes in cytoskeletal organization during bud formation (Aufschnaiter et al, 2017).…”

Cadherin switch marks germ layer formation in the diploblastic sea anemone Nematostella vectensis

“…These basal connections could be associated with the contractile actin bundles and used for the increased synchronized contractile activity within large epithelia sheets. Basal cellular contractions also have a major contribution in the process of bud formation in Hydra (Holz et al, 2017). Such basal contacts are absent from bilaterian embryos, which are mainly connected by apical junction belts.…”

Rho Family of Ras-Like GTPases in Early-Branching Animals

“…In vivo assays using ROCK inhibitors applied during early development of freshwater sponges provide solid evidence that ROCK is important for inducing the processes of morphogenesis and setting up the body plan [ 102 ]. Recently published data [ 103 ] suggest an essential role of FGFR (fibroblast growth factor receptor) and Rho-ROCK-myosin II pathways in the control of cell shape changes required for bud detachment in hydra. Using gene expression analysis and pharmacological inhibition, authors recognized a candidate signaling pathway through Rho, ROCK, and myosin II, which controls rearrangement of the actin cytoskeleton and bud base constriction.…”