Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates
Abstract The mode of evolution of left-right asymmetries in the vertebrate habenulae remains largely unknown. Using a transcriptomic approach, we show that in a cartilaginous fish, the catshark Scyliorhinus canicula, habenulae exhibit marked asymmetries, in both their medial and lateral components....
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Nature Portfolio
2024-11-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-54042-2 |
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| author | Maxence Lanoizelet Léo Michel Ronan Lagadec Hélène Mayeur Lucile Guichard Valentin Logeux Dany Séverac Kyle Martin Christophe Klopp Sylvain Marcellini Héctor Castillo Nicolas Pollet Eva Candal Mélanie Debiais-Thibaud Catherine Boisvert Bernard Billoud Michael Schubert Patrick Blader Sylvie Mazan |
| author_facet | Maxence Lanoizelet Léo Michel Ronan Lagadec Hélène Mayeur Lucile Guichard Valentin Logeux Dany Séverac Kyle Martin Christophe Klopp Sylvain Marcellini Héctor Castillo Nicolas Pollet Eva Candal Mélanie Debiais-Thibaud Catherine Boisvert Bernard Billoud Michael Schubert Patrick Blader Sylvie Mazan |
| author_sort | Maxence Lanoizelet |
| collection | DOAJ |
| description | Abstract The mode of evolution of left-right asymmetries in the vertebrate habenulae remains largely unknown. Using a transcriptomic approach, we show that in a cartilaginous fish, the catshark Scyliorhinus canicula, habenulae exhibit marked asymmetries, in both their medial and lateral components. Comparisons across vertebrates suggest that those identified in lateral habenulae reflect an ancestral gnathostome trait, partially conserved in lampreys, and independently lost in tetrapods and neopterygians. Asymmetry formation involves distinct mechanisms in the catshark lateral and medial habenulae. Medial habenulae are submitted to a marked, asymmetric temporal regulation of neurogenesis, undetectable in their lateral counterparts. Conversely, asymmetry formation in lateral habenulae results from asymmetric choices of neuronal identity in post-mitotic progenitors, a regulation dependent on the repression of Wnt signaling by Nodal on the left. Based on comparisons with the mouse and the zebrafish, we propose that habenular asymmetry formation involves a recurrent developmental logic across vertebrates, which relies on conserved, temporally regulated genetic programs sequentially shaping choices of neuronal identity on both sides and asymmetrically modified by Wnt activity. |
| format | Article |
| id | doaj-art-b83e617c41ed45da84e231d605a16003 |
| institution | DOAJ |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-b83e617c41ed45da84e231d605a160032025-08-20T02:49:09ZengNature PortfolioNature Communications2041-17232024-11-0115111610.1038/s41467-024-54042-2Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebratesMaxence Lanoizelet0Léo Michel1Ronan Lagadec2Hélène Mayeur3Lucile Guichard4Valentin Logeux5Dany Séverac6Kyle Martin7Christophe Klopp8Sylvain Marcellini9Héctor Castillo10Nicolas Pollet11Eva Candal12Mélanie Debiais-Thibaud13Catherine Boisvert14Bernard Billoud15Michael Schubert16Patrick Blader17Sylvie Mazan18CNRS, Sorbonne Université, UMR7232-Biologie Intégrative des Organismes Marins, Observatoire OcéanologiqueCNRS, Sorbonne Université, UMR7232-Biologie Intégrative des Organismes Marins, Observatoire OcéanologiqueCNRS, Sorbonne Université, UMR7232-Biologie Intégrative des Organismes Marins, Observatoire OcéanologiqueCNRS, Sorbonne Université, UMR7232-Biologie Intégrative des Organismes Marins, Observatoire OcéanologiqueCNRS, Sorbonne Université, UMR7232-Biologie Intégrative des Organismes Marins, Observatoire OcéanologiqueCentre de Ressources Biologiques Marines, Sorbonne Université, Observatoire Océanologique, UMS 2348MGX, Université Montpellier, CNRS, INSERMUK Research and Innovation, Biotechnology and Biological Sciences Research CouncilPlateforme Bioinformatique, Genotoul, BioinfoMics, UR875 Biométrie et Intelligence Artificielle, INRAEDepartment of Cell Biology, School of Biological Sciences, University of ConcepcionDepartment of Cell Biology, School of Biological Sciences, University of ConcepcionUniversité Paris-Saclay, CNRS, IRD, Évolution, Génomes, Comportement et Écologie, Université Paris-SaclayDepartament of Functional Biology, CIBUS, Faculty of Biology, Universidade de Santiago de CompostelaISEM, Université de Montpellier, CNRS, IRD, EPHESchool of Molecular and Life Sciences, Curtin UniversityUMR8227, CNRS-Sorbonne Université, Station BiologiqueLaboratoire de Biologie du Développement de Villefranche-sur-Mer, Institut de la Mer de Villefranche, Sorbonne Université, CNRSCentre de Biologie Intégrative (CBI, FR 3743), Université de Toulouse, CNRS, UPSCNRS, Sorbonne Université, UMR7232-Biologie Intégrative des Organismes Marins, Observatoire OcéanologiqueAbstract The mode of evolution of left-right asymmetries in the vertebrate habenulae remains largely unknown. Using a transcriptomic approach, we show that in a cartilaginous fish, the catshark Scyliorhinus canicula, habenulae exhibit marked asymmetries, in both their medial and lateral components. Comparisons across vertebrates suggest that those identified in lateral habenulae reflect an ancestral gnathostome trait, partially conserved in lampreys, and independently lost in tetrapods and neopterygians. Asymmetry formation involves distinct mechanisms in the catshark lateral and medial habenulae. Medial habenulae are submitted to a marked, asymmetric temporal regulation of neurogenesis, undetectable in their lateral counterparts. Conversely, asymmetry formation in lateral habenulae results from asymmetric choices of neuronal identity in post-mitotic progenitors, a regulation dependent on the repression of Wnt signaling by Nodal on the left. Based on comparisons with the mouse and the zebrafish, we propose that habenular asymmetry formation involves a recurrent developmental logic across vertebrates, which relies on conserved, temporally regulated genetic programs sequentially shaping choices of neuronal identity on both sides and asymmetrically modified by Wnt activity.https://doi.org/10.1038/s41467-024-54042-2 |
| spellingShingle | Maxence Lanoizelet Léo Michel Ronan Lagadec Hélène Mayeur Lucile Guichard Valentin Logeux Dany Séverac Kyle Martin Christophe Klopp Sylvain Marcellini Héctor Castillo Nicolas Pollet Eva Candal Mélanie Debiais-Thibaud Catherine Boisvert Bernard Billoud Michael Schubert Patrick Blader Sylvie Mazan Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates Nature Communications |
| title | Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates |
| title_full | Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates |
| title_fullStr | Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates |
| title_full_unstemmed | Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates |
| title_short | Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates |
| title_sort | analysis of a shark reveals ancient wnt dependent habenular asymmetries in vertebrates |
| url | https://doi.org/10.1038/s41467-024-54042-2 |
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