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Npr3 regulates neural crest and cranial placode progenitors formation through its dual function as clearance and signaling receptor

Natriuretic peptide signaling has been implicated in a broad range of physiological processes, regulating blood volume and pressure, ventricular hypertrophy, fat metabolism, and long bone growth. Here, we describe a completely novel role for natriuretic peptide signaling in the control of neural cre...

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Autores principales: Devotta, Arun, Juraver-Geslin, Hugo, Griffin, Casey, Saint-Jeannet, Jean-Pierre
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212560/
https://www.ncbi.nlm.nih.gov/pubmed/37162198
http://dx.doi.org/10.7554/eLife.84036
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author Devotta, Arun
Juraver-Geslin, Hugo
Griffin, Casey
Saint-Jeannet, Jean-Pierre
author_facet Devotta, Arun
Juraver-Geslin, Hugo
Griffin, Casey
Saint-Jeannet, Jean-Pierre
author_sort Devotta, Arun
collection PubMed
description Natriuretic peptide signaling has been implicated in a broad range of physiological processes, regulating blood volume and pressure, ventricular hypertrophy, fat metabolism, and long bone growth. Here, we describe a completely novel role for natriuretic peptide signaling in the control of neural crest (NC) and cranial placode (CP) progenitors formation. Among the components of this signaling pathway, we show that natriuretic peptide receptor 3 (Npr3) plays a pivotal role by differentially regulating two developmental programs through its dual function as clearance and signaling receptor. Using a combination of MO-based knockdowns, pharmacological inhibitors and rescue assays we demonstrate that Npr3 cooperate with guanylate cyclase natriuretic peptide receptor 1 (Npr1) and natriuretic peptides (Nppa/Nppc) to regulate NC and CP formation, pointing at a broad requirement of this signaling pathway in early embryogenesis. We propose that Npr3 acts as a clearance receptor to regulate local concentrations of natriuretic peptides for optimal cGMP production through Npr1 activation, and as a signaling receptor to control cAMP levels through inhibition of adenylyl cyclase. The intracellular modulation of these second messengers therefore participates in the segregation of NC and CP cell populations.
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spelling pubmed-102125602023-05-26 Npr3 regulates neural crest and cranial placode progenitors formation through its dual function as clearance and signaling receptor Devotta, Arun Juraver-Geslin, Hugo Griffin, Casey Saint-Jeannet, Jean-Pierre eLife Developmental Biology Natriuretic peptide signaling has been implicated in a broad range of physiological processes, regulating blood volume and pressure, ventricular hypertrophy, fat metabolism, and long bone growth. Here, we describe a completely novel role for natriuretic peptide signaling in the control of neural crest (NC) and cranial placode (CP) progenitors formation. Among the components of this signaling pathway, we show that natriuretic peptide receptor 3 (Npr3) plays a pivotal role by differentially regulating two developmental programs through its dual function as clearance and signaling receptor. Using a combination of MO-based knockdowns, pharmacological inhibitors and rescue assays we demonstrate that Npr3 cooperate with guanylate cyclase natriuretic peptide receptor 1 (Npr1) and natriuretic peptides (Nppa/Nppc) to regulate NC and CP formation, pointing at a broad requirement of this signaling pathway in early embryogenesis. We propose that Npr3 acts as a clearance receptor to regulate local concentrations of natriuretic peptides for optimal cGMP production through Npr1 activation, and as a signaling receptor to control cAMP levels through inhibition of adenylyl cyclase. The intracellular modulation of these second messengers therefore participates in the segregation of NC and CP cell populations. eLife Sciences Publications, Ltd 2023-05-10 /pmc/articles/PMC10212560/ /pubmed/37162198 http://dx.doi.org/10.7554/eLife.84036 Text en © 2023, Devotta, Juraver-Geslin et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Devotta, Arun
Juraver-Geslin, Hugo
Griffin, Casey
Saint-Jeannet, Jean-Pierre
Npr3 regulates neural crest and cranial placode progenitors formation through its dual function as clearance and signaling receptor
title Npr3 regulates neural crest and cranial placode progenitors formation through its dual function as clearance and signaling receptor
title_full Npr3 regulates neural crest and cranial placode progenitors formation through its dual function as clearance and signaling receptor
title_fullStr Npr3 regulates neural crest and cranial placode progenitors formation through its dual function as clearance and signaling receptor
title_full_unstemmed Npr3 regulates neural crest and cranial placode progenitors formation through its dual function as clearance and signaling receptor
title_short Npr3 regulates neural crest and cranial placode progenitors formation through its dual function as clearance and signaling receptor
title_sort npr3 regulates neural crest and cranial placode progenitors formation through its dual function as clearance and signaling receptor
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212560/
https://www.ncbi.nlm.nih.gov/pubmed/37162198
http://dx.doi.org/10.7554/eLife.84036
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