Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria.

International audience The transforming growth factor beta (TGFbeta) superfamily includes bone morphogenetic proteins, activins and TGF-betasensu stricto (s.s.). These ligands have been shown to play a key role in numerous biological processes including early embryonic development and immune regulat...

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Published in:Mechanisms of Development
Main Authors: Herpin, Amaury, Lelong, C., Becker, T., Rosa, F.M., Favrel, P., Cunningham, C.
Other Authors: 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
Language:English
Published: HAL CCSD 2005
Subjects:
Online Access:https://hal.inrae.fr/hal-02678886
https://doi.org/10.1016/j.mod.2004.12.004
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spelling ftccsdartic:oai:HAL:hal-02678886v1 2023-05-15T15:58:20+02:00 Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria. Herpin, Amaury Lelong, C. Becker, T. Rosa, F.M. Favrel, P. Cunningham, C. 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-02678886 https://doi.org/10.1016/j.mod.2004.12.004 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.mod.2004.12.004 info:eu-repo/semantics/altIdentifier/pmid/15817226 hal-02678886 https://hal.inrae.fr/hal-02678886 doi:10.1016/j.mod.2004.12.004 PRODINRA: 273941 PUBMED: 15817226 WOS: 000228795200007 ISSN: 0925-4773 Mechanisms of Development https://hal.inrae.fr/hal-02678886 Mechanisms of Development, Elsevier, 2005, 122 (5), pp.695-705. ⟨10.1016/j.mod.2004.12.004⟩ http://www.sciencedirect.com/science/article/pii/S0925477304002849 gastrulation lophotrochozoans [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/10.1016/j.mod.2004.12.004 2021-04-03T22:35:24Z International audience The transforming growth factor beta (TGFbeta) superfamily includes bone morphogenetic proteins, activins and TGF-betasensu stricto (s.s.). These ligands have been shown to play a key role in numerous biological processes including early embryonic development and immune regulation. They transduce their signal through a hetromeric complex of type I and type II receptors. Such receptors have been identified in ecdysozoans but none have been found as yet in the other major protostomal clade, the lophotrochozoans. Here, we report the identification of the first lophotrochozoan TGFbetas.s. type I receptor (Cg-TGFbetaRI) from the mollusk Crassostrea gigas. The phylogenetic and structural analyses as well as the expression pattern during early development suggest Cg-TGFbetaRI to belong to the TGFbetas.s./activin type I receptor clade and functional studies corroborate these deductions. The use of the zebrafish embryo as a reporter organism reveals that either Cg-TGFbetaRI or its dominant negative acting truncated form, when overexpressed during gastrulation, resulted in a range of phenotypes displaying severe disturbance of anterioposterior patterning due to a strong modulation of ventrolateral mesoderm patterning. Finally, a Cg-TGFbetaRI cytokine activity during immune regulation in C. gigas has been investigated by real-time PCR in haemocytes and mantle edge during an in vivo bacterial LPS challenge. One piece of evidence from this study suggests that the molecular mechanisms controlling mesodermal patterning and some immune regulations across all bilateria could be conserved through a functional TGF-beta s.s. pathway in lophotrochozoans. Article in Journal/Newspaper Crassostrea gigas Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Mechanisms of Development 122 5 695 705
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 gastrulation
lophotrochozoans
[SDV.BA]Life Sciences [q-bio]/Animal biology
[SDV.BDD]Life Sciences [q-bio]/Development Biology
spellingShingle gastrulation
lophotrochozoans
[SDV.BA]Life Sciences [q-bio]/Animal biology
[SDV.BDD]Life Sciences [q-bio]/Development Biology
Herpin, Amaury
Lelong, C.
Becker, T.
Rosa, F.M.
Favrel, P.
Cunningham, C.
Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria.
topic_facet gastrulation
lophotrochozoans
[SDV.BA]Life Sciences [q-bio]/Animal biology
[SDV.BDD]Life Sciences [q-bio]/Development Biology
description International audience The transforming growth factor beta (TGFbeta) superfamily includes bone morphogenetic proteins, activins and TGF-betasensu stricto (s.s.). These ligands have been shown to play a key role in numerous biological processes including early embryonic development and immune regulation. They transduce their signal through a hetromeric complex of type I and type II receptors. Such receptors have been identified in ecdysozoans but none have been found as yet in the other major protostomal clade, the lophotrochozoans. Here, we report the identification of the first lophotrochozoan TGFbetas.s. type I receptor (Cg-TGFbetaRI) from the mollusk Crassostrea gigas. The phylogenetic and structural analyses as well as the expression pattern during early development suggest Cg-TGFbetaRI to belong to the TGFbetas.s./activin type I receptor clade and functional studies corroborate these deductions. The use of the zebrafish embryo as a reporter organism reveals that either Cg-TGFbetaRI or its dominant negative acting truncated form, when overexpressed during gastrulation, resulted in a range of phenotypes displaying severe disturbance of anterioposterior patterning due to a strong modulation of ventrolateral mesoderm patterning. Finally, a Cg-TGFbetaRI cytokine activity during immune regulation in C. gigas has been investigated by real-time PCR in haemocytes and mantle edge during an in vivo bacterial LPS challenge. One piece of evidence from this study suggests that the molecular mechanisms controlling mesodermal patterning and some immune regulations across all bilateria could be conserved through a functional TGF-beta s.s. pathway in lophotrochozoans.
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, C.
Becker, T.
Rosa, F.M.
Favrel, P.
Cunningham, C.
author_facet Herpin, Amaury
Lelong, C.
Becker, T.
Rosa, F.M.
Favrel, P.
Cunningham, C.
author_sort Herpin, Amaury
title Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria.
title_short Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria.
title_full Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria.
title_fullStr Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria.
title_full_unstemmed Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria.
title_sort structural and functional evidences for a type 1 tgf-beta sensu stricto receptor in the lophotrochozoan crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria.
publisher HAL CCSD
publishDate 2005
url https://hal.inrae.fr/hal-02678886
https://doi.org/10.1016/j.mod.2004.12.004
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source ISSN: 0925-4773
Mechanisms of Development
https://hal.inrae.fr/hal-02678886
Mechanisms of Development, Elsevier, 2005, 122 (5), pp.695-705. ⟨10.1016/j.mod.2004.12.004⟩
http://www.sciencedirect.com/science/article/pii/S0925477304002849
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1016/j.mod.2004.12.004
info:eu-repo/semantics/altIdentifier/pmid/15817226
hal-02678886
https://hal.inrae.fr/hal-02678886
doi:10.1016/j.mod.2004.12.004
PRODINRA: 273941
PUBMED: 15817226
WOS: 000228795200007
op_doi https://doi.org/10.1016/j.mod.2004.12.004
container_title Mechanisms of Development
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container_issue 5
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