WNT/β-Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella

Lapébie, Pascal; Gazave, Eve; Ereskovsky, Alexander; Derelle, Romain; Bézac, Chantal; Renard, Emmanuelle; Houliston, Evelyn; Borchiellini, Carole

doi:10.1371/journal.pone.0005823

Title: WNT/β-Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella

Journal Article · 08 June 2009 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0005823 · OSTI ID:1627373

Lapébie, Pascal ^[1]; Gazave, Eve ^[2]; Ereskovsky, Alexander ^[3]; Derelle, Romain ^[4]; Bézac, Chantal ^[2]; Renard, Emmanuelle ^[2]; Houliston, Evelyn ^[4]; Borchiellini, Carole ^[2]

Aix-Marseille Univ., Marseille (France). Centre National de la Recherche Scientifique (CNRS). Centre d’Oceanologie de Marseille; DOE/OSTI
Aix-Marseille Univ., Marseille (France). Centre National de la Recherche Scientifique (CNRS). Centre d’Oceanologie de Marseille
Aix-Marseille Univ., Marseille (France). Centre National de la Recherche Scientifique (CNRS). Centre d’Oceanologie de Marseille; St. Petersburg State Univ. (Russian Federation). Faculty of Biology and Soils
Univ. Pierre et Marie Curie, Paris (France). Centre National de la Recherche Scientifique (CNRS). Biologie du Developpement. Observatoire Oceanologique

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, GSK3β). 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/β-catenin pathway using GSK3β 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.

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Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI ID:: 1627373

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 6 Vol. 4; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (44)

Metamorphosis of cinctoblastula larvae (Homoscleromorpha, porifera) Ereskovsky, Alexander V.; Tokina, Daria B.; Bézac, Chantal Journal of Morphology, Vol. 268, Issue 6 https://doi.org/10.1002/jmor.10506	journal	January 2007
Activation of the Wnt Signaling Pathway: A Molecular Mechanism for Lithium Action Hedgepeth, Chester M.; Conrad, Leslee J.; Zhang, Jie Developmental Biology, Vol. 185, Issue 1 https://doi.org/10.1006/dbio.1997.8552	journal	May 1997
NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges Gazave, Eve; Lapébie, Pascal; Renard, Emmanuelle Development Genes and Evolution, Vol. 218, Issue 9 https://doi.org/10.1007/s00427-008-0242-z	journal	August 2008
The Mammary Bud as a Skin Appendage: Unique and Shared Aspects of Development Mikkola, Marja L.; Millar, Sarah E. Journal of Mammary Gland Biology and Neoplasia, Vol. 11, Issue 3-4 https://doi.org/10.1007/s10911-006-9029-x	journal	November 2006
Isolation and characterization of Wnt pathway-related genes from Porifera☆ Adell, Teresa; Thakur, Archana N.; Müller, Werner E. G. Cell Biology International, Vol. 31, Issue 9 https://doi.org/10.1016/j.cellbi.2007.03.003	journal	September 2007
GSK-3-Selective Inhibitors Derived from Tyrian Purple Indirubins Meijer, Laurent; Skaltsounis, Alexios-Leandros; Magiatis, Prokopios Chemistry & Biology, Vol. 10, Issue 12 https://doi.org/10.1016/j.chembiol.2003.11.010	journal	December 2003
Phylogenomics Revives Traditional Views on Deep Animal Relationships Philippe, Hervé; Derelle, Romain; Lopez, Philippe Current Biology, Vol. 19, Issue 8 https://doi.org/10.1016/j.cub.2009.02.052	journal	April 2009
Distinct Wnt members regulate the hierarchical morphogenesis of skin regions (spinal tract) and individual feathers Chang, Chung-Hsing; Jiang, Ting-Xin; Lin, Chih-Min Mechanisms of Development, Vol. 121, Issue 2 https://doi.org/10.1016/j.mod.2003.12.004	journal	February 2004
Wnt/β-catenin signaling directs multiple stages of tooth morphogenesis Liu, Fei; Chu, Emily Y.; Watt, Brenda Developmental Biology, Vol. 313, Issue 1 https://doi.org/10.1016/j.ydbio.2007.10.016	journal	January 2008
Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution Borchiellini, Carole; Chombard, Catherine; Manuel, Michaël Molecular Phylogenetics and Evolution, Vol. 32, Issue 3 https://doi.org/10.1016/j.ympev.2004.02.021	journal	September 2004
Mechanisms of ectodermal organogenesis Pispa, Johanna; Thesleff, Irma Developmental Biology, Vol. 262, Issue 2 https://doi.org/10.1016/s0012-1606(03)00325-7	journal	October 2003
β-Catenin Controls Hair Follicle Morphogenesis and Stem Cell Differentiation in the Skin Huelsken, Joerg; Vogel, Regina; Erdmann, Bettina Cell, Vol. 105, Issue 4 https://doi.org/10.1016/s0092-8674(01)00336-1	journal	May 2001
Type IV collagen in sponges, the missing link in basement membrane ubiquity* Boute, Nicolas; Exposito, Jean-Yves; Boury-Esnault, Nicole Biology of the Cell, Vol. 88, Issue 1-2 https://doi.org/10.1016/s0248-4900(97)86829-3	journal	January 1996
Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis Reddy, Seshamma; Andl, Thomas; Bagasra, Alexander Mechanisms of Development, Vol. 107, Issue 1-2 https://doi.org/10.1016/s0925-4773(01)00452-x	journal	September 2001
Phylogenetic Analysis of the Wnt Gene Family Prud'homme, Benjamin; Lartillot, Nicolas; Balavoine, Guillaume Current Biology, Vol. 12, Issue 16 https://doi.org/10.1016/s0960-9822(02)01068-0	journal	August 2002
WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra Hobmayer, Bert; Rentzsch, Fabian; Kuhn, Kerstin Nature, Vol. 407, Issue 6801 https://doi.org/10.1038/35025063	journal	September 2000
Wnt signaling and stem cell control Nusse, Roel Cell Research, Vol. 18, Issue 5 https://doi.org/10.1038/cr.2008.47	journal	April 2008
Unexpected complexity of the Wnt gene family in a sea anemone Kusserow, Arne; Pang, Kevin; Sturm, Carsten Nature, Vol. 433, Issue 7022 https://doi.org/10.1038/nature03158	journal	January 2005
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans King, Nicole; Westbrook, M. Jody; Young, Susan L. Nature, Vol. 451, Issue 7180 https://doi.org/10.1038/nature06617	journal	February 2008
Tasteless Without Wingless? Nakagawa, Hiroshi Gastroenterology, Vol. 132, Issue 5 https://doi.org/10.1053/j.gastro.2007.03.100	journal	May 2007
Early evolution of animal cell signaling and adhesion genes Nichols, S. A.; Dirks, W.; Pearse, J. S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 33 https://doi.org/10.1073/pnas.0604065103	journal	August 2006
Continuous tooth generation in mouse is induced by activated epithelial Wnt/β-catenin signaling Järvinen, Elina; Salazar-Ciudad, Isaac; Birchmeier, Walter Proceedings of the National Academy of Sciences, Vol. 103, Issue 49 https://doi.org/10.1073/pnas.0607289103	journal	December 2006
Wnt/β-Catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra Philipp, Isabelle; Aufschnaiter, Roland; Özbek, Suat Proceedings of the National Academy of Sciences, Vol. 106, Issue 11 https://doi.org/10.1073/pnas.0812847106	journal	March 2009
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood Guindon, Stéphane; Gascuel, Olivier Systematic Biology, Vol. 52, Issue 5 https://doi.org/10.1080/10635150390235520	journal	October 2003
MRBAYES: Bayesian inference of phylogenetic trees Huelsenbeck, J. P.; Ronquist, F. Bioinformatics, Vol. 17, Issue 8 https://doi.org/10.1093/bioinformatics/17.8.754	journal	August 2001
Epithelium--The Primary Building Block for Metazoan Complexity Tyler, S. Integrative and Comparative Biology, Vol. 43, Issue 1 https://doi.org/10.1093/icb/43.1.55	journal	February 2003
The Protistan Origins of Animals and Fungi Steenkamp, Emma T.; Wright, Jane; Baldauf, Sandra L. Molecular Biology and Evolution, Vol. 23, Issue 1 https://doi.org/10.1093/molbev/msj011	journal	September 2005
A Phylogenomic Investigation into the Origin of Metazoa Ruiz-Trillo, Iñaki; Roger, Andrew J.; Burger, Gertraud Molecular Biology and Evolution, Vol. 25, Issue 4 https://doi.org/10.1093/molbev/msn006	journal	January 2008
A General Empirical Model of Protein Evolution Derived from Multiple Protein Families Using a Maximum-Likelihood Approach Whelan, Simon; Goldman, Nick Molecular Biology and Evolution, Vol. 18, Issue 5 https://doi.org/10.1093/oxfordjournals.molbev.a003851	journal	May 2001
Expression of Frizzled Genes in Developing and Postnatal Hair Follicles Reddy, Seshamma T.; Andl, Thomas; Lu, Min-Min Journal of Investigative Dermatology, Vol. 123, Issue 2 https://doi.org/10.1111/j.0022-202x.2004.23215.x	journal	August 2004
Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity Larroux, Claire; Fahey, Bryony; Liubicich, Danielle Evolution Development, Vol. 8, Issue 2 https://doi.org/10.1111/j.1525-142x.2006.00086.x	journal	March 2006
The Premetazoan Ancestry of Cadherins Abedin, Monika; King, Nicole Science, Vol. 319, Issue 5865 https://doi.org/10.1126/science.1151084	journal	February 2008
Alternative Wnt Signaling Is Initiated by Distinct Receptors van Amerongen, Renée; Mikels, Amanda; Nusse, Roel Science Signaling, Vol. 1, Issue 35 https://doi.org/10.1126/scisignal.135re9	journal	September 2008
The wnt Signaling Pathway in Development and Disease Logan, Catriona Y.; Nusse, Roel Annual Review of Cell and Developmental Biology, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.cellbio.20.010403.113126	journal	November 2004
Wnt signaling induces epithelial differentiation during cutaneous wound healing Fathke, Carrie; Wilson, Lynne; Shah, Kavita BMC Cell Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2121-7-4	journal	January 2006
Cellular and Molecular Regulation of Hematopoietic and Intestinal Stem Cell Behavior He, Xi C.; Zhang, Jiwang; Li, Linheng Annals of the New York Academy of Sciences, Vol. 1049, Issue 1 https://doi.org/10.1196/annals.1334.005	journal	May 2005
Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis Chu, E. Y. Development, Vol. 131, Issue 19 https://doi.org/10.1242/dev.01347	journal	October 2004
Sustained epithelial -catenin activity induces precocious hair development but disrupts hair follicle down-growth and hair shaft formation Narhi, K.; Jarvinen, E.; Birchmeier, W. Development, Vol. 135, Issue 6 https://doi.org/10.1242/dev.016550	journal	February 2008
Formation of the head organizer in hydra involves the canonical Wnt pathway Broun, M. Development, Vol. 132, Issue 12 https://doi.org/10.1242/dev.01848	journal	June 2005
A maternally localised Wnt ligand required for axial patterning in the cnidarianClytia hemisphaerica Momose, Tsuyoshi; Derelle, Romain; Houliston, Evelyn Development, Vol. 135, Issue 12 https://doi.org/10.1242/dev.021543	journal	June 2008
Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing Neumann, Carl J.; Cohen, Stephen M. Development, Vol. 124, Issue 4 https://doi.org/10.1242/dev.124.4.871	journal	February 1997
β-catenin signaling can initiate feather bud development Noramly, Selina; Freeman, Allison; Morgan, Bruce A. Development, Vol. 126, Issue 16 https://doi.org/10.1242/dev.126.16.3509	journal	August 1999
Wnt and TGF-β Expression in the Sponge Amphimedon queenslandica and the Origin of Metazoan Embryonic Patterning Adamska, Maja; Degnan, Sandie M.; Green, Kathryn M. PLoS ONE, Vol. 2, Issue 10 https://doi.org/10.1371/journal.pone.0001031	journal	October 2007
Cell-Cell Adhesion in the Cnidaria: Insights Into the Evolution of Tissue Morphogenesis Magie, Craig R.; Martindale, Mark Q. The Biological Bulletin, Vol. 214, Issue 3 https://doi.org/10.2307/25470665	journal	June 2008

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Typization of Sponge Development and Its Significance for Phylogeny Ereskovsky, Alexander V. The Comparative Embryology of Sponges https://doi.org/10.1007/978-90-481-8575-7_5	book	January 2010
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The many faces and functions of β-catenin: β-Catenin: a life by, beyond, and against the Wnt canon Valenta, Tomas; Hausmann, George; Basler, Konrad The EMBO Journal, Vol. 31, Issue 12 https://doi.org/10.1038/emboj.2012.150	journal	May 2012
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