The lamprey habenula provides an extreme example for the temporal regulation of asymmetric development
By their phylogenetic position and their marked epithalamic asymmetries, lampreys are relevant models for understanding the formation and evolution of this trait across vertebrates. In this study, we use a transcriptomic approach to identify novel signature markers to characterize the highly asymmet...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2025-02-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2025.1528797/full |
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| author | Lucile Guichard Ronan Lagadec Léo Michel Hélène Mayeur Michaël Fuentès Jordan Pain Noah Heier Quentin Rougemont Maria Celina Rodicio Antón Barreiro-Iglesias Antón Barreiro-Iglesias Patrick Blader Michael Schubert Sylvie Mazan |
| author_facet | Lucile Guichard Ronan Lagadec Léo Michel Hélène Mayeur Michaël Fuentès Jordan Pain Noah Heier Quentin Rougemont Maria Celina Rodicio Antón Barreiro-Iglesias Antón Barreiro-Iglesias Patrick Blader Michael Schubert Sylvie Mazan |
| author_sort | Lucile Guichard |
| collection | DOAJ |
| description | By their phylogenetic position and their marked epithalamic asymmetries, lampreys are relevant models for understanding the formation and evolution of this trait across vertebrates. In this study, we use a transcriptomic approach to identify novel signature markers to characterize the highly asymmetric, bipartite organization of habenulae in lampreys. Lamprey habenulae are subdivided into two complementary subdomains related, respectively, to the lateral/ventral and the medial/dorsal habenulae of jawed vertebrates: a dorsal, right-restricted subdomain and a bilateral subdomain that includes the left habenula as well as its ventral right counterpart. Analysis of the formation of the lamprey habenula at prolarval and larval stages using a combination of morphological, immunohistochemical, and in situ hybridization approaches highlights a marked asymmetric temporal regulation. The dorsal right subdomain forms and already expresses all identified signature markers in prolarval stages. In contrast, the left and ventral right subdomain appears significantly later, with the first indication of neuronal identity elaboration in these territories being observed in larval stages. As in gnathostomes, Wnt signaling may be involved in the regulation of this unique, asymmetric mode of development, since β-catenin shows asymmetric and highly dynamic nuclear distributions both in neural progenitors and differentiated neuronal precursors of the two habenular subdomains. These data confirm the importance of lampreys to unravel the developmental logic underlying the recurrence and variation of habenular asymmetries in vertebrates and pave the way for future functional analyses. |
| format | Article |
| id | doaj-art-4f6a4709ef06425e9d49c9863d4f5c84 |
| institution | Kabale University |
| issn | 2296-634X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj-art-4f6a4709ef06425e9d49c9863d4f5c842025-02-06T07:09:42ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2025-02-011310.3389/fcell.2025.15287971528797The lamprey habenula provides an extreme example for the temporal regulation of asymmetric developmentLucile Guichard0Ronan Lagadec1Léo Michel2Hélène Mayeur3Michaël Fuentès4Jordan Pain5Noah Heier6Quentin Rougemont7Maria Celina Rodicio8Antón Barreiro-Iglesias9Antón Barreiro-Iglesias10Patrick Blader11Michael Schubert12Sylvie Mazan13CNRS, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, FranceCNRS, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, FranceCNRS, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, FranceCNRS, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, FranceCNRS, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, FranceCNRS, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, FranceCNRS, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, FranceCNRS, AgroParisTech, Laboratoire Ecologie Systématique et Evolution, Université Paris-Saclay, Gif-sur-Yvette, FranceDepartamento de Bioloxía Funcional, Facultade de Bioloxía, Universidade de Santiago de Compostela, Santiago de Compostela, SpainDepartamento de Bioloxía Funcional, Facultade de Bioloxía, Universidade de Santiago de Compostela, Santiago de Compostela, SpainAquatic One Health Research Center (ARCUS), Universidade de Santiago de Compostela, Santiago de Compostela, SpainMolecular, Cellular and Developmental Biology (MCD, UMR5077), Centre de Biologie Intégrative (CBI, FR3743), Université de Toulouse, CNRS, UPS, Toulouse, FranceLaboratoire de Biologie du Développement de Villefranche-sur-Mer, Institut de la Mer de Villefranche, Sorbonne Université, CNRS, Villefranche-sur-Mer, FranceCNRS, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, FranceBy their phylogenetic position and their marked epithalamic asymmetries, lampreys are relevant models for understanding the formation and evolution of this trait across vertebrates. In this study, we use a transcriptomic approach to identify novel signature markers to characterize the highly asymmetric, bipartite organization of habenulae in lampreys. Lamprey habenulae are subdivided into two complementary subdomains related, respectively, to the lateral/ventral and the medial/dorsal habenulae of jawed vertebrates: a dorsal, right-restricted subdomain and a bilateral subdomain that includes the left habenula as well as its ventral right counterpart. Analysis of the formation of the lamprey habenula at prolarval and larval stages using a combination of morphological, immunohistochemical, and in situ hybridization approaches highlights a marked asymmetric temporal regulation. The dorsal right subdomain forms and already expresses all identified signature markers in prolarval stages. In contrast, the left and ventral right subdomain appears significantly later, with the first indication of neuronal identity elaboration in these territories being observed in larval stages. As in gnathostomes, Wnt signaling may be involved in the regulation of this unique, asymmetric mode of development, since β-catenin shows asymmetric and highly dynamic nuclear distributions both in neural progenitors and differentiated neuronal precursors of the two habenular subdomains. These data confirm the importance of lampreys to unravel the developmental logic underlying the recurrence and variation of habenular asymmetries in vertebrates and pave the way for future functional analyses.https://www.frontiersin.org/articles/10.3389/fcell.2025.1528797/fullhabenulaasymmetrylampreytemporal regulationWnt signaling |
| spellingShingle | Lucile Guichard Ronan Lagadec Léo Michel Hélène Mayeur Michaël Fuentès Jordan Pain Noah Heier Quentin Rougemont Maria Celina Rodicio Antón Barreiro-Iglesias Antón Barreiro-Iglesias Patrick Blader Michael Schubert Sylvie Mazan The lamprey habenula provides an extreme example for the temporal regulation of asymmetric development Frontiers in Cell and Developmental Biology habenula asymmetry lamprey temporal regulation Wnt signaling |
| title | The lamprey habenula provides an extreme example for the temporal regulation of asymmetric development |
| title_full | The lamprey habenula provides an extreme example for the temporal regulation of asymmetric development |
| title_fullStr | The lamprey habenula provides an extreme example for the temporal regulation of asymmetric development |
| title_full_unstemmed | The lamprey habenula provides an extreme example for the temporal regulation of asymmetric development |
| title_short | The lamprey habenula provides an extreme example for the temporal regulation of asymmetric development |
| title_sort | lamprey habenula provides an extreme example for the temporal regulation of asymmetric development |
| topic | habenula asymmetry lamprey temporal regulation Wnt signaling |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2025.1528797/full |
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