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Environmental cues from neural crest derivatives act as metastatic triggers in an embryonic neuroblastoma model

Embryonic malignant transformation is concomitant to organogenesis, often affecting multipotent and migratory progenitors. While lineage relationships between malignant cells and their physiological counterparts are extensively investigated, the contribution of exogenous embryonic signals is not ful...

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Autores principales: Ben Amar, Dounia, Thoinet, Karine, Villalard, Benjamin, Imbaud, Olivier, Costechareyre, Clélia, Jarrosson, Loraine, Reynaud, Florie, Novion Ducassou, Julia, Couté, Yohann, Brunet, Jean-François, Combaret, Valérie, Corradini, Nadège, Delloye-Bourgeois, Céline, Castellani, Valérie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9091272/
https://www.ncbi.nlm.nih.gov/pubmed/35538114
http://dx.doi.org/10.1038/s41467-022-30237-3
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author Ben Amar, Dounia
Thoinet, Karine
Villalard, Benjamin
Imbaud, Olivier
Costechareyre, Clélia
Jarrosson, Loraine
Reynaud, Florie
Novion Ducassou, Julia
Couté, Yohann
Brunet, Jean-François
Combaret, Valérie
Corradini, Nadège
Delloye-Bourgeois, Céline
Castellani, Valérie
author_facet Ben Amar, Dounia
Thoinet, Karine
Villalard, Benjamin
Imbaud, Olivier
Costechareyre, Clélia
Jarrosson, Loraine
Reynaud, Florie
Novion Ducassou, Julia
Couté, Yohann
Brunet, Jean-François
Combaret, Valérie
Corradini, Nadège
Delloye-Bourgeois, Céline
Castellani, Valérie
author_sort Ben Amar, Dounia
collection PubMed
description Embryonic malignant transformation is concomitant to organogenesis, often affecting multipotent and migratory progenitors. While lineage relationships between malignant cells and their physiological counterparts are extensively investigated, the contribution of exogenous embryonic signals is not fully known. Neuroblastoma (NB) is a childhood malignancy of the peripheral nervous system arising from the embryonic trunk neural crest (NC) and characterized by heterogeneous and interconvertible tumor cell identities. Here, using experimental models mimicking the embryonic context coupled to proteomic and transcriptomic analyses, we show that signals released by embryonic sympathetic ganglia, including Olfactomedin-1, induce NB cells to shift from a noradrenergic to mesenchymal identity, and to activate a gene program promoting NB metastatic onset and dissemination. From this gene program, we extract a core signature specifically shared by metastatic cancers with NC origin. This reveals non-cell autonomous embryonic contributions regulating the plasticity of NB identities and setting pro-dissemination gene programs common to NC-derived cancers.
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spelling pubmed-90912722022-05-12 Environmental cues from neural crest derivatives act as metastatic triggers in an embryonic neuroblastoma model Ben Amar, Dounia Thoinet, Karine Villalard, Benjamin Imbaud, Olivier Costechareyre, Clélia Jarrosson, Loraine Reynaud, Florie Novion Ducassou, Julia Couté, Yohann Brunet, Jean-François Combaret, Valérie Corradini, Nadège Delloye-Bourgeois, Céline Castellani, Valérie Nat Commun Article Embryonic malignant transformation is concomitant to organogenesis, often affecting multipotent and migratory progenitors. While lineage relationships between malignant cells and their physiological counterparts are extensively investigated, the contribution of exogenous embryonic signals is not fully known. Neuroblastoma (NB) is a childhood malignancy of the peripheral nervous system arising from the embryonic trunk neural crest (NC) and characterized by heterogeneous and interconvertible tumor cell identities. Here, using experimental models mimicking the embryonic context coupled to proteomic and transcriptomic analyses, we show that signals released by embryonic sympathetic ganglia, including Olfactomedin-1, induce NB cells to shift from a noradrenergic to mesenchymal identity, and to activate a gene program promoting NB metastatic onset and dissemination. From this gene program, we extract a core signature specifically shared by metastatic cancers with NC origin. This reveals non-cell autonomous embryonic contributions regulating the plasticity of NB identities and setting pro-dissemination gene programs common to NC-derived cancers. Nature Publishing Group UK 2022-05-10 /pmc/articles/PMC9091272/ /pubmed/35538114 http://dx.doi.org/10.1038/s41467-022-30237-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Ben Amar, Dounia
Thoinet, Karine
Villalard, Benjamin
Imbaud, Olivier
Costechareyre, Clélia
Jarrosson, Loraine
Reynaud, Florie
Novion Ducassou, Julia
Couté, Yohann
Brunet, Jean-François
Combaret, Valérie
Corradini, Nadège
Delloye-Bourgeois, Céline
Castellani, Valérie
Environmental cues from neural crest derivatives act as metastatic triggers in an embryonic neuroblastoma model
title Environmental cues from neural crest derivatives act as metastatic triggers in an embryonic neuroblastoma model
title_full Environmental cues from neural crest derivatives act as metastatic triggers in an embryonic neuroblastoma model
title_fullStr Environmental cues from neural crest derivatives act as metastatic triggers in an embryonic neuroblastoma model
title_full_unstemmed Environmental cues from neural crest derivatives act as metastatic triggers in an embryonic neuroblastoma model
title_short Environmental cues from neural crest derivatives act as metastatic triggers in an embryonic neuroblastoma model
title_sort environmental cues from neural crest derivatives act as metastatic triggers in an embryonic neuroblastoma model
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9091272/
https://www.ncbi.nlm.nih.gov/pubmed/35538114
http://dx.doi.org/10.1038/s41467-022-30237-3
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