Catenin Signalling and Epithelial Patterning in the Homoscleromorph
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WNT/β-Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella Pascal Lapébie, Eve Gazave, Alexander Ereskovsky, Romain Derelle, Chantal Bézac, Emmanuelle Renard, Evelyn Houliston, Carole Borchiellini To cite this version: Pascal Lapébie, Eve Gazave, Alexander Ereskovsky, Romain Derelle, Chantal Bézac, et al.. WNT/β- Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella. PLoS ONE, Public Library of Science, 2009, 4 (6), 10.1371/journal.pone.0005823. hal-01793109 HAL Id: hal-01793109 https://hal.archives-ouvertes.fr/hal-01793109 Submitted on 25 Sep 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. 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Distributed under a Creative Commons Attribution| 4.0 International License WNT/b-Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella Pascal Lape´ bie1*, Eve Gazave1, Alexander Ereskovsky1,2, Romain Derelle3, Chantal Be´zac4, Emmanuelle Renard1, Evelyn Houliston3, Carole Borchiellini1 1 Centre d’Oce´anologie de Marseille, Aix-Marseille Universite´, CNRS - UMR 6540, Station marine d’Endoume, Marseille, France, 2 Faculty of Biology and Soils, Saint- Petersburg State University, St. Petersburg, Russia, 3 Universite´ Pierre et Marie Curie-Paris 6, CNRS UMR 7009 Biologie du De´veloppement, Observatoire Oce´anologique, Villefranche-sur-Mer, France, 4 Centre d’Oce´anologie de Marseille, Aix-Marseille Universite´, CNRS–UMS 2196, Station marine d’Endoume, Marseille, France Abstract Sponges branch basally in the metazoan phylogenetic tree and are thus well positioned to provide insights into the evolution of mechanisms controlling animal development, likely to remain active in adult sponges. Of the four sponge clades, the Homoscleromorpha are of particular interest as they alone show the ‘‘true’’ epithelial organization seen in other metazoan phyla (the Eumetazoa). We have examined the deployment in sponges of Wnt signalling pathway components, since this pathway is an important regulator of many developmental patterning processes. We identified a reduced repertoire of three divergent Wnt ligand genes in the recently-sequenced Amphimedon queenslandica (demosponge) genome and two Wnts from our EST collection from the homoscleromorph Oscarella lobularis, along with well-conserved genes for intracellular pathway components (b-catenin, GSK3b). Remarkably, the two O. lobularis Wnt genes showed complementary expression patterns in relation to the evenly spaced ostia (canal openings) of the exopinacoderm (ectoderm), highly reminiscent of Wnt expression during skin appendage formation in vertebrates. Furthermore, experimental activation of the Wnt/b-catenin pathway using GSK3b inhibitors provoked formation of ectopic ostia, as has been shown for epithelial appendages in Eumetazoa. We thus suggest that deployment of Wnt signalling is a common and perhaps ancient feature of metazoan epithelial patterning and morphogenesis. Citation: Lape´bie P, Gazave E, Ereskovsky A, Derelle R, Be´zac C, et al. (2009) WNT/b-Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella. PLoS ONE 4(6): e5823. doi:10.1371/journal.pone.0005823 Editor: Vincent Laudet, Ecole Normale Supe´rieure de Lyon, France Received December 27, 2008; Accepted May 4, 2009; Published June 8, 2009 Copyright: ß 2009 Lape´bie et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: CNRS-Universite´ de la Me´diterrane´e. This work was partly supported by program RFBR No 09-04-00337 and European Marie Curie Mobility program (fellowship of A. Ereskovsky, MIF1-CT-2006-040065). The funders had no role in study design, data collection¯ and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction they show epithelial-type morphogenesis during development [14,15]. In this context, it is interesting to note that the The earliest steps in animal evolution remain obscure, but can Homoscleromorpha and the Eumetazoa share quasi equivalent be illuminated by comparative studies between the most basally molecular toolkits for two key aspects of epithelial function, cell branching animal groups, notably sponges, cnidarians and adhesion and signalling [16]. A subset of molecules involved in ctenophores. The sponges are widely accepted as one of the both these functions has been identified in Choanoflagellates, and oldest metazoan lineages, with the unicellular choanoflagellates therefore predates multicellularity [17,18]. forming a sister group to the metazoa as a whole [1,2,3,4]. Since Among major signalling molecules, the WNTs are metazoan sponge choanocytes and choanoflagellates show many similarities, protein ligands that control diverse processes such as cell the first step of animal evolution has been proposed to have been proliferation, cell-fate determination, cell migration and differen- the acquisition of multicellularity from a choanoflagellate-like tiation during multiple steps of embryonic development [19], as ancestor, with early metazoans comprising epithelial-type cell layer well as in tissue homeostasis in adults, regulating stem cell containing feeding choanocytes and non-feeding cells [1,5,6]. Such populations [20] in regenerating tissues including Hydra polyps multicellular epithelia are considered as a fundamental metazoan and [21] vertebrate intestine [22]. The WNT family appears to innovation, enabling a range of morphogenetic processes and have made an early apparition and diversification during animal leading to body plan diversification [7]. evolution, since twelve of the thirteen known Wnt subfamilies have Among the four sponge lineages -Hexactinellida, Calcispongiae, been identified in cnidarians [23] but none in the genome of the Demospongiae and Homoscleromorpha- [8,9] the homosclero- choanoflagellate Monosiga brevicollis [18]. morphs are a key group for understanding the origin and evolution WNT ligands can influence cell behaviour by activating a of epithelia [1,10]. The homoscleromorphs are the only sponge number of distinguishable downstream intracellular pathways group to possess eumetazoan-like true epithelia, characterized by [24]. The most intensively studied is the ‘‘canonical’’ or Wnt/b- the presence of basement membrane with type IV collagen and catenin pathway, in which WNT binding to Frizzled family regularly distributed zonula adhaerens cell junctions both in larval receptors provokes stabilization and nuclear translocation of the and in adult forms [11,12,13]. In addition, unlike other sponges, transcriptional co-regulator b-catenin via inhibition of the PLoS ONE | www.plosone.org 1 June 2009 | Volume 4 | Issue 6 | e5823 WNTs in Homoscleromorpha cytoplasmic kinase GSK-3b [19]. Components of this pathway WNT proteins showed typical structural characteristics, including a have been identified in Demospongiae [25], with polarized highly conserved cysteine pattern (alignment available upon request) expression of a Wnt gene in Amphimedon queenslandica larva and peptide secretion signals, but their sequences were highly suggesting a role in embryo patterning [26]. divergent compared to a reference dataset comprising the complete Among the Homoscleromorpha, the existence of Wnt signalling WNT repertoire retrieved from selected deuterostome, protostome components was noted previously in Oscarella carmela [16]. We now and cnidarian genomes. They could thus not be assigned orthology to report complementary expressions of two Wnts in adult tissue of any of the previously defined eumetazoan WNT sub-families Oscarella lobularis [10]. By comparison with known epithelial Wnt (Figure1),ashasbeenthecaseforWNTsfromfast-evolving expression patterns in Eumetazoa, the observed expression patterns bilaterian [28] and hydrozoan [23,29] species. Another indicator of indicate that canonical Wnt signalling is involved in epithelial the considerable evolutionary divergence of WNT sequences was the patterning in these animals. This conclusion was supported by our sensitivity of the relationships between WNT subfamilies to the pharmacological inhibition experiments, the first functional test of the method of analysis and to gene sampling. Given this marked role of Wnt signalling in a sponge. In the light of these findings we divergence of Wnt sequences, more genomic data from different propose that Wnt signalling have a common and perhaps ancestral sponge clades and from other basally diverging metazoan phyla will function in metazoans to regulate epithelial morphogenesis, be required to discriminate between the evolutionary scenarios of Wnt gene loss in one or more sponge groups from a larger set present in Results and Discussion the last common ancestor of Metazoa, versus significant diversification of the family in the eumetazoan lineage post-dating the