Ectodermal Wnt signaling, cell fate determination, and polarity of the skate gill arch skeleton

Jenaid M. Rees; Victoria A. Sleight; Stephen J. Clark; Tetsuya Nakamura; J. Andrew Gillis

doi:10.7554/elife.79964

Ectodermal Wnt signaling, cell fate determination, and polarity of the skate gill arch skeleton

Jenaid M. Rees, Victoria A. Sleight, Stephen J. Clark, Tetsuya Nakamura, J. Andrew Gillis^*

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

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Abstract

The gill skeleton of cartilaginous fishes (sharks, skates, rays, and holocephalans) exhibits a striking anterior–posterior polarity, with a series of fine appendages called branchial rays projecting from the posterior margin of the gill arch cartilages. We previously demonstrated in the skate (Leucoraja erinacea) that branchial rays derive from a posterior domain of pharyngeal arch mesenchyme that is responsive to Sonic hedgehog (Shh) signaling from a distal gill arch epithelial ridge (GAER) signaling centre. However, how branchial ray progenitors are specified exclusively within posterior gill arch mesenchyme is not known. Here, we show that genes encoding several Wnt ligands are expressed in the ectoderm immediately adjacent to the skate GAER, and that these Wnt signals are transduced largely in the anterior arch environment. Using pharmacological manipulation, we show that inhibition of Wnt signalling results in an anterior expansion of Shh signal transduction in developing skate gill arches, and in the formation of ectopic anterior branchial ray cartilages. Our findings demonstrate that ectodermal Wnt signalling contributes to gill arch skeletal polarity in skate by restricting Shh signal transduction and chondrogenesis to the posterior arch environment and highlights the importance of signalling interactions at embryonic tissue boundaries for cell fate determination in vertebrate pharyngeal arches.

Original language	English
Article number	e79964
Journal	eLife
Volume	12
Early online date	20 Mar 2023
DOIs	https://doi.org/10.7554/elife.79964
Publication status	E-pub ahead of print - 20 Mar 2023

Bibliographical note

Funding Information:
With thanks to Dr Kate Criswell and Dr Christine Hirschberger for advice, and to the University of Cambridge Wellcome PhD. Programme in Developmental Mechanisms. The authors were funded by a Wellcome PhD studentship (214953/Z/18/Z) to JMR, and by a Royal Society University Research Fellowship (UF130182 and URF\R\191007) and Royal Society Research Grant (RG140377) to JAG.
For the purpose of Open Access, the authors have applied a CC BY public copyright license to any Author Accepted Manuscript version arising from this submission.

Data Availability Statement

All data and R scripts for analysis have been deposited on Figshare: 10.6084/m9.figshare.19615779. RNA sequencing data are available at NCBI-SRA under BioProject ID: PRJNA825354. Biosample accessions: SAMN27512544, SAMN27512545, SAMN27512546, SAMN27512547, SAMN27512548, SAMN27512549, SAMN27512550, SAMN27512551, SAMN27512552, SAMN27512553, SAMN27512554, SAMN27512555, SAMN27512556, SAMN27512557, SAMN27512558, SAMN27512559, SAMN27512560, SAMN27512561, SAMN27512562, SAMN27512563. Probes were purchased from Molecular Instruments (Los Angeles, California, USA). This included the following: for skate Shh (Lot PRA753), Ptc2 (Lot PRA754), Wnt2b (Lot PRE300), Wnt3 (Lot PRG814), Wnt4 (Lot PRE301), Wnt7b (Lot PRE302), Wnt9b (Lot PRE303), Notum (Lot PRG817), Kremen1 (Lot PRG816), Axin2 (Lot PRG818), Apcdd1 (Lot PRG815), Col2a1 (Lot PRB574) and Sox9 (Lot PRB571).

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abstract = "The gill skeleton of cartilaginous fishes (sharks, skates, rays, and holocephalans) exhibits a striking anterior–posterior polarity, with a series of fine appendages called branchial rays projecting from the posterior margin of the gill arch cartilages. We previously demonstrated in the skate (Leucoraja erinacea) that branchial rays derive from a posterior domain of pharyngeal arch mesenchyme that is responsive to Sonic hedgehog (Shh) signaling from a distal gill arch epithelial ridge (GAER) signaling centre. However, how branchial ray progenitors are specified exclusively within posterior gill arch mesenchyme is not known. Here, we show that genes encoding several Wnt ligands are expressed in the ectoderm immediately adjacent to the skate GAER, and that these Wnt signals are transduced largely in the anterior arch environment. Using pharmacological manipulation, we show that inhibition of Wnt signalling results in an anterior expansion of Shh signal transduction in developing skate gill arches, and in the formation of ectopic anterior branchial ray cartilages. Our findings demonstrate that ectodermal Wnt signalling contributes to gill arch skeletal polarity in skate by restricting Shh signal transduction and chondrogenesis to the posterior arch environment and highlights the importance of signalling interactions at embryonic tissue boundaries for cell fate determination in vertebrate pharyngeal arches.",

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Ectodermal Wnt signaling, cell fate determination, and polarity of the skate gill arch skeleton

Abstract

Bibliographical note

Data Availability Statement

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