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

The transforming growth factor β (TGF‐β) superfamily includes bone morphogenetic proteins, activins and TGF‐β sensu 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 pr...

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Published in:FEBS Journal
Main Authors: Herpin, Amaury, Lelong, Christophe, Becker, Thomas, Rosa, Frederic, Favrel, Pascal, Cunningham, Charles
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2005
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Online Access:http://dx.doi.org/10.1111/j.1742-4658.2005.04761.x
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spelling crwiley:10.1111/j.1742-4658.2005.04761.x 2024-06-09T07:45:31+00:00 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, Frederic Favrel, Pascal Cunningham, Charles 2005 http://dx.doi.org/10.1111/j.1742-4658.2005.04761.x https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fj.1742-4658.2005.04761.x https://febs.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1742-4658.2005.04761.x en eng Wiley http://onlinelibrary.wiley.com/termsAndConditions#vor The FEBS Journal volume 272, issue 13, page 3424-3440 ISSN 1742-464X 1742-4658 journal-article 2005 crwiley https://doi.org/10.1111/j.1742-4658.2005.04761.x 2024-05-16T14:28:08Z The transforming growth factor β (TGF‐β) superfamily includes bone morphogenetic proteins, activins and TGF‐β sensu 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‐ TGFβsfR2 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‐ TGFβsfR2, 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‐ TGFβsfR2 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‐β 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‐ TGFβsfR2 would be the shared type II receptor interface for both BMP and activin ligands. Article in Journal/Newspaper Crassostrea gigas Wiley Online Library FEBS Journal 272 13 3424 3440
institution Open Polar
collection Wiley Online Library
op_collection_id crwiley
language English
description The transforming growth factor β (TGF‐β) superfamily includes bone morphogenetic proteins, activins and TGF‐β sensu 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‐ TGFβsfR2 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‐ TGFβsfR2, 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‐ TGFβsfR2 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‐β 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‐ TGFβsfR2 would be the shared type II receptor interface for both BMP and activin ligands.
format Article in Journal/Newspaper
author Herpin, Amaury
Lelong, Christophe
Becker, Thomas
Rosa, Frederic
Favrel, Pascal
Cunningham, Charles
spellingShingle Herpin, Amaury
Lelong, Christophe
Becker, Thomas
Rosa, Frederic
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
author_facet Herpin, Amaury
Lelong, Christophe
Becker, Thomas
Rosa, Frederic
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 Wiley
publishDate 2005
url http://dx.doi.org/10.1111/j.1742-4658.2005.04761.x
https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fj.1742-4658.2005.04761.x
https://febs.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1742-4658.2005.04761.x
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source The FEBS Journal
volume 272, issue 13, page 3424-3440
ISSN 1742-464X 1742-4658
op_rights http://onlinelibrary.wiley.com/termsAndConditions#vor
op_doi https://doi.org/10.1111/j.1742-4658.2005.04761.x
container_title FEBS Journal
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container_issue 13
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