Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway
International audience The transforming growth factor beta (TGF-beta) superfamily includes bone morphogenetic proteins, activins and TGF-betasensu stricto (s.s). These ligands, which transduce their signal through a heteromeric complex of type I and type II receptors, have been shown to play a key r...
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ftccsdartic:oai:HAL:hal-02682824v1 2023-05-15T15:58:27+02:00 Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway Herpin, Amaury Lelong, Christophe Becker, Thomas Rosa, Frédéric Favrel, Pascal Cunningham, Charles SARS International Centre for Marine Molecular Biology Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Institut National de la Santé et de la Recherche Médicale (INSERM) Norwegian Research Council, Basse-Normandie Regional Council, France, and the French-Norwegian Foundation for Scientific, Technical and Industrial Research 2005 https://hal.inrae.fr/hal-02682824 https://doi.org/10.1111/j.1742-4658.2005.04761.x en eng HAL CCSD Wiley info:eu-repo/semantics/altIdentifier/doi/10.1111/j.1742-4658.2005.04761.x info:eu-repo/semantics/altIdentifier/pmid/15978047 hal-02682824 https://hal.inrae.fr/hal-02682824 doi:10.1111/j.1742-4658.2005.04761.x PRODINRA: 273945 PUBMED: 15978047 WOS: 000230054600018 ISSN: 1742-464X EISSN: 1742-4658 FEBS Journal https://hal.inrae.fr/hal-02682824 FEBS Journal, Wiley, 2005, 272 (13), pp.3424-3440. ⟨10.1111/j.1742-4658.2005.04761.x⟩ zebrafish BMP TGF-beta early embyogenesis [SDV.BA]Life Sciences [q-bio]/Animal biology [SDV.BDD]Life Sciences [q-bio]/Development Biology info:eu-repo/semantics/article Journal articles 2005 ftccsdartic https://doi.org/10.1111/j.1742-4658.2005.04761.x 2021-04-03T22:35:19Z International audience The transforming growth factor beta (TGF-beta) superfamily includes bone morphogenetic proteins, activins and TGF-betasensu stricto (s.s). These ligands, which transduce their signal through a heteromeric complex of type I and type II receptors, have been shown to play a key role in numerous biological processes including early embryonic development in both deuterostomes and ecdyzozoans. Lophochotrozoans, the third major group of bilaterian animals, have remained in the background of the molecular survey of metazoan development. We report the cloning and functional study of the central part of the BMP pathway machinery in the bivalve mollusc Crassostrea gigas (Cg-BMPR1 type I receptor and Cg-TGFbetasfR2 type II receptor), showing an unusual functional mode of signal transduction for this superfamily. The use of the zebrafish embryo as a reporter organism revealed that Cg-BMPR1, Cg-TGFbetasfR2, Cg-ALR I, an activin Type I receptor or their dominant negative acting truncated forms, when overexpressed during gastrulation, resulted in a range of phenotypes displaying severe disturbance of anterioposterior patterning, due to strong modulations of ventrolateral mesoderm patterning. The results suggest that Cg-BMPR1, and to a certain degree Cg-TGFbetasfR2 proteins, function in C. gigas in a similar way to their zebrafish orthologues. Finally, based on phylogenetic analyses, we propose an evolutionary model within the complete TGF-beta superfamily. Thus, evidence provided by this study argues for a possible conserved endomesoderm/ectomesoderm inductive mechanism in spiralians through an ancestral BMP/activin pathway in which the singular, promiscuous and probably unique Cg-TGFbetasfR2 would be the shared type II receptor interface for both BMP and activin ligands. Article in Journal/Newspaper Crassostrea gigas Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) FEBS Journal 272 13 3424 3440 |
institution |
Open Polar |
collection |
Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) |
op_collection_id |
ftccsdartic |
language |
English |
topic |
zebrafish BMP TGF-beta early embyogenesis [SDV.BA]Life Sciences [q-bio]/Animal biology [SDV.BDD]Life Sciences [q-bio]/Development Biology |
spellingShingle |
zebrafish BMP TGF-beta early embyogenesis [SDV.BA]Life Sciences [q-bio]/Animal biology [SDV.BDD]Life Sciences [q-bio]/Development Biology Herpin, Amaury Lelong, Christophe Becker, Thomas Rosa, Frédéric Favrel, Pascal Cunningham, Charles Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway |
topic_facet |
zebrafish BMP TGF-beta early embyogenesis [SDV.BA]Life Sciences [q-bio]/Animal biology [SDV.BDD]Life Sciences [q-bio]/Development Biology |
description |
International audience The transforming growth factor beta (TGF-beta) superfamily includes bone morphogenetic proteins, activins and TGF-betasensu stricto (s.s). These ligands, which transduce their signal through a heteromeric complex of type I and type II receptors, have been shown to play a key role in numerous biological processes including early embryonic development in both deuterostomes and ecdyzozoans. Lophochotrozoans, the third major group of bilaterian animals, have remained in the background of the molecular survey of metazoan development. We report the cloning and functional study of the central part of the BMP pathway machinery in the bivalve mollusc Crassostrea gigas (Cg-BMPR1 type I receptor and Cg-TGFbetasfR2 type II receptor), showing an unusual functional mode of signal transduction for this superfamily. The use of the zebrafish embryo as a reporter organism revealed that Cg-BMPR1, Cg-TGFbetasfR2, Cg-ALR I, an activin Type I receptor or their dominant negative acting truncated forms, when overexpressed during gastrulation, resulted in a range of phenotypes displaying severe disturbance of anterioposterior patterning, due to strong modulations of ventrolateral mesoderm patterning. The results suggest that Cg-BMPR1, and to a certain degree Cg-TGFbetasfR2 proteins, function in C. gigas in a similar way to their zebrafish orthologues. Finally, based on phylogenetic analyses, we propose an evolutionary model within the complete TGF-beta superfamily. Thus, evidence provided by this study argues for a possible conserved endomesoderm/ectomesoderm inductive mechanism in spiralians through an ancestral BMP/activin pathway in which the singular, promiscuous and probably unique Cg-TGFbetasfR2 would be the shared type II receptor interface for both BMP and activin ligands. |
author2 |
SARS International Centre for Marine Molecular Biology Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Institut National de la Santé et de la Recherche Médicale (INSERM) Norwegian Research Council, Basse-Normandie Regional Council, France, and the French-Norwegian Foundation for Scientific, Technical and Industrial Research |
format |
Article in Journal/Newspaper |
author |
Herpin, Amaury Lelong, Christophe Becker, Thomas Rosa, Frédéric Favrel, Pascal Cunningham, Charles |
author_facet |
Herpin, Amaury Lelong, Christophe Becker, Thomas Rosa, Frédéric Favrel, Pascal Cunningham, Charles |
author_sort |
Herpin, Amaury |
title |
Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway |
title_short |
Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway |
title_full |
Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway |
title_fullStr |
Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway |
title_full_unstemmed |
Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway |
title_sort |
structural and functional evidence for a singular repertoire of bmp receptor signal transducing proteins in the lophotrochozoan crassostrea gigas suggests a shared ancestral bmp/activin pathway |
publisher |
HAL CCSD |
publishDate |
2005 |
url |
https://hal.inrae.fr/hal-02682824 https://doi.org/10.1111/j.1742-4658.2005.04761.x |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
ISSN: 1742-464X EISSN: 1742-4658 FEBS Journal https://hal.inrae.fr/hal-02682824 FEBS Journal, Wiley, 2005, 272 (13), pp.3424-3440. ⟨10.1111/j.1742-4658.2005.04761.x⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1111/j.1742-4658.2005.04761.x info:eu-repo/semantics/altIdentifier/pmid/15978047 hal-02682824 https://hal.inrae.fr/hal-02682824 doi:10.1111/j.1742-4658.2005.04761.x PRODINRA: 273945 PUBMED: 15978047 WOS: 000230054600018 |
op_doi |
https://doi.org/10.1111/j.1742-4658.2005.04761.x |
container_title |
FEBS Journal |
container_volume |
272 |
container_issue |
13 |
container_start_page |
3424 |
op_container_end_page |
3440 |
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1766394194852577280 |