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Ral GTPases promote breast cancer metastasis by controlling biogenesis and organ targeting of exosomes

Cancer extracellular vesicles (EVs) shuttle at distance and fertilize pre-metastatic niches facilitating subsequent seeding by tumor cells. However, the link between EV secretion mechanisms and their capacity to form pre-metastatic niches remains obscure. Using mouse models, we show that GTPases of...

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Autores principales: Ghoroghi, Shima, Mary, Benjamin, Larnicol, Annabel, Asokan, Nandini, Klein, Annick, Osmani, Naël, Busnelli, Ignacio, Delalande, François, Paul, Nicodème, Halary, Sébastien, Gros, Frédéric, Fouillen, Laetitia, Haeberle, Anne-Marie, Royer, Cathy, Spiegelhalter, Coralie, André-Grégoire, Gwennan, Mittelheisser, Vincent, Detappe, Alexandre, Murphy, Kendelle, Timpson, Paul, Carapito, Raphaël, Blot-Chabaud, Marcel, Gavard, Julie, Carapito, Christine, Vitale, Nicolas, Lefebvre, Olivier, Goetz, Jacky G, Hyenne, Vincent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7822591/
https://www.ncbi.nlm.nih.gov/pubmed/33404012
http://dx.doi.org/10.7554/eLife.61539
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author Ghoroghi, Shima
Mary, Benjamin
Larnicol, Annabel
Asokan, Nandini
Klein, Annick
Osmani, Naël
Busnelli, Ignacio
Delalande, François
Paul, Nicodème
Halary, Sébastien
Gros, Frédéric
Fouillen, Laetitia
Haeberle, Anne-Marie
Royer, Cathy
Spiegelhalter, Coralie
André-Grégoire, Gwennan
Mittelheisser, Vincent
Detappe, Alexandre
Murphy, Kendelle
Timpson, Paul
Carapito, Raphaël
Blot-Chabaud, Marcel
Gavard, Julie
Carapito, Christine
Vitale, Nicolas
Lefebvre, Olivier
Goetz, Jacky G
Hyenne, Vincent
author_facet Ghoroghi, Shima
Mary, Benjamin
Larnicol, Annabel
Asokan, Nandini
Klein, Annick
Osmani, Naël
Busnelli, Ignacio
Delalande, François
Paul, Nicodème
Halary, Sébastien
Gros, Frédéric
Fouillen, Laetitia
Haeberle, Anne-Marie
Royer, Cathy
Spiegelhalter, Coralie
André-Grégoire, Gwennan
Mittelheisser, Vincent
Detappe, Alexandre
Murphy, Kendelle
Timpson, Paul
Carapito, Raphaël
Blot-Chabaud, Marcel
Gavard, Julie
Carapito, Christine
Vitale, Nicolas
Lefebvre, Olivier
Goetz, Jacky G
Hyenne, Vincent
author_sort Ghoroghi, Shima
collection PubMed
description Cancer extracellular vesicles (EVs) shuttle at distance and fertilize pre-metastatic niches facilitating subsequent seeding by tumor cells. However, the link between EV secretion mechanisms and their capacity to form pre-metastatic niches remains obscure. Using mouse models, we show that GTPases of the Ral family control, through the phospholipase D1, multi-vesicular bodies homeostasis and tune the biogenesis and secretion of pro-metastatic EVs. Importantly, EVs from RalA or RalB depleted cells have limited organotropic capacities in vivoand are less efficient in promoting metastasis. RalA and RalB reduce the EV levels of the adhesion molecule MCAM/CD146, which favors EV-mediated metastasis by allowing EVs targeting to the lungs. Finally, RalA, RalB, and MCAM/CD146, are factors of poor prognosis in breast cancer patients. Altogether, our study identifies RalGTPases as central molecules linking the mechanisms of EVs secretion and cargo loading to their capacity to disseminate and induce pre-metastatic niches in a CD146-dependent manner.
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spelling pubmed-78225912021-01-25 Ral GTPases promote breast cancer metastasis by controlling biogenesis and organ targeting of exosomes Ghoroghi, Shima Mary, Benjamin Larnicol, Annabel Asokan, Nandini Klein, Annick Osmani, Naël Busnelli, Ignacio Delalande, François Paul, Nicodème Halary, Sébastien Gros, Frédéric Fouillen, Laetitia Haeberle, Anne-Marie Royer, Cathy Spiegelhalter, Coralie André-Grégoire, Gwennan Mittelheisser, Vincent Detappe, Alexandre Murphy, Kendelle Timpson, Paul Carapito, Raphaël Blot-Chabaud, Marcel Gavard, Julie Carapito, Christine Vitale, Nicolas Lefebvre, Olivier Goetz, Jacky G Hyenne, Vincent eLife Cancer Biology Cancer extracellular vesicles (EVs) shuttle at distance and fertilize pre-metastatic niches facilitating subsequent seeding by tumor cells. However, the link between EV secretion mechanisms and their capacity to form pre-metastatic niches remains obscure. Using mouse models, we show that GTPases of the Ral family control, through the phospholipase D1, multi-vesicular bodies homeostasis and tune the biogenesis and secretion of pro-metastatic EVs. Importantly, EVs from RalA or RalB depleted cells have limited organotropic capacities in vivoand are less efficient in promoting metastasis. RalA and RalB reduce the EV levels of the adhesion molecule MCAM/CD146, which favors EV-mediated metastasis by allowing EVs targeting to the lungs. Finally, RalA, RalB, and MCAM/CD146, are factors of poor prognosis in breast cancer patients. Altogether, our study identifies RalGTPases as central molecules linking the mechanisms of EVs secretion and cargo loading to their capacity to disseminate and induce pre-metastatic niches in a CD146-dependent manner. eLife Sciences Publications, Ltd 2021-01-06 /pmc/articles/PMC7822591/ /pubmed/33404012 http://dx.doi.org/10.7554/eLife.61539 Text en © 2021, Ghoroghi et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cancer Biology
Ghoroghi, Shima
Mary, Benjamin
Larnicol, Annabel
Asokan, Nandini
Klein, Annick
Osmani, Naël
Busnelli, Ignacio
Delalande, François
Paul, Nicodème
Halary, Sébastien
Gros, Frédéric
Fouillen, Laetitia
Haeberle, Anne-Marie
Royer, Cathy
Spiegelhalter, Coralie
André-Grégoire, Gwennan
Mittelheisser, Vincent
Detappe, Alexandre
Murphy, Kendelle
Timpson, Paul
Carapito, Raphaël
Blot-Chabaud, Marcel
Gavard, Julie
Carapito, Christine
Vitale, Nicolas
Lefebvre, Olivier
Goetz, Jacky G
Hyenne, Vincent
Ral GTPases promote breast cancer metastasis by controlling biogenesis and organ targeting of exosomes
title Ral GTPases promote breast cancer metastasis by controlling biogenesis and organ targeting of exosomes
title_full Ral GTPases promote breast cancer metastasis by controlling biogenesis and organ targeting of exosomes
title_fullStr Ral GTPases promote breast cancer metastasis by controlling biogenesis and organ targeting of exosomes
title_full_unstemmed Ral GTPases promote breast cancer metastasis by controlling biogenesis and organ targeting of exosomes
title_short Ral GTPases promote breast cancer metastasis by controlling biogenesis and organ targeting of exosomes
title_sort ral gtpases promote breast cancer metastasis by controlling biogenesis and organ targeting of exosomes
topic Cancer Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7822591/
https://www.ncbi.nlm.nih.gov/pubmed/33404012
http://dx.doi.org/10.7554/eLife.61539
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