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Extracellular vesicles direct migration by synthesizing and releasing chemotactic signals

Chemotactic signals are relayed to neighboring cells through the secretion of additional chemoattractants. We previously showed in Dictyostelium discoideum that the adenylyl cyclase A, which synthesizes the chemoattractant cyclic adenosine monophosphate (cAMP), is present in the intraluminal vesicle...

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Autores principales: Kriebel, Paul W., Majumdar, Ritankar, Jenkins, Lisa M., Senoo, Hiroshi, Wang, Weiye, Ammu, Sonia, Chen, Song, Narayan, Kedar, Iijima, Miho, Parent, Carole A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6080930/
https://www.ncbi.nlm.nih.gov/pubmed/29884750
http://dx.doi.org/10.1083/jcb.201710170
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author Kriebel, Paul W.
Majumdar, Ritankar
Jenkins, Lisa M.
Senoo, Hiroshi
Wang, Weiye
Ammu, Sonia
Chen, Song
Narayan, Kedar
Iijima, Miho
Parent, Carole A.
author_facet Kriebel, Paul W.
Majumdar, Ritankar
Jenkins, Lisa M.
Senoo, Hiroshi
Wang, Weiye
Ammu, Sonia
Chen, Song
Narayan, Kedar
Iijima, Miho
Parent, Carole A.
author_sort Kriebel, Paul W.
collection PubMed
description Chemotactic signals are relayed to neighboring cells through the secretion of additional chemoattractants. We previously showed in Dictyostelium discoideum that the adenylyl cyclase A, which synthesizes the chemoattractant cyclic adenosine monophosphate (cAMP), is present in the intraluminal vesicles of multivesicular bodies (MVBs) that coalesce at the back of cells. Using ultrastructural reconstructions, we now show that ACA-containing MVBs release their contents to attract neighboring cells. We show that the released vesicles are capable of directing migration and streaming and are central to chemotactic signal relay. We demonstrate that the released vesicles not only contain cAMP but also can actively synthesize and release cAMP to promote chemotaxis. Through proteomic, pharmacological, and genetic approaches, we determined that the vesicular cAMP is released via the ABCC8 transporter. Together, our findings show that extracellular vesicles released by D. discoideum cells are functional entities that mediate signal relay during chemotaxis and streaming.
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spelling pubmed-60809302019-02-06 Extracellular vesicles direct migration by synthesizing and releasing chemotactic signals Kriebel, Paul W. Majumdar, Ritankar Jenkins, Lisa M. Senoo, Hiroshi Wang, Weiye Ammu, Sonia Chen, Song Narayan, Kedar Iijima, Miho Parent, Carole A. J Cell Biol Research Articles Chemotactic signals are relayed to neighboring cells through the secretion of additional chemoattractants. We previously showed in Dictyostelium discoideum that the adenylyl cyclase A, which synthesizes the chemoattractant cyclic adenosine monophosphate (cAMP), is present in the intraluminal vesicles of multivesicular bodies (MVBs) that coalesce at the back of cells. Using ultrastructural reconstructions, we now show that ACA-containing MVBs release their contents to attract neighboring cells. We show that the released vesicles are capable of directing migration and streaming and are central to chemotactic signal relay. We demonstrate that the released vesicles not only contain cAMP but also can actively synthesize and release cAMP to promote chemotaxis. Through proteomic, pharmacological, and genetic approaches, we determined that the vesicular cAMP is released via the ABCC8 transporter. Together, our findings show that extracellular vesicles released by D. discoideum cells are functional entities that mediate signal relay during chemotaxis and streaming. Rockefeller University Press 2018-08-06 /pmc/articles/PMC6080930/ /pubmed/29884750 http://dx.doi.org/10.1083/jcb.201710170 Text en © 2018 Kriebel et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Research Articles
Kriebel, Paul W.
Majumdar, Ritankar
Jenkins, Lisa M.
Senoo, Hiroshi
Wang, Weiye
Ammu, Sonia
Chen, Song
Narayan, Kedar
Iijima, Miho
Parent, Carole A.
Extracellular vesicles direct migration by synthesizing and releasing chemotactic signals
title Extracellular vesicles direct migration by synthesizing and releasing chemotactic signals
title_full Extracellular vesicles direct migration by synthesizing and releasing chemotactic signals
title_fullStr Extracellular vesicles direct migration by synthesizing and releasing chemotactic signals
title_full_unstemmed Extracellular vesicles direct migration by synthesizing and releasing chemotactic signals
title_short Extracellular vesicles direct migration by synthesizing and releasing chemotactic signals
title_sort extracellular vesicles direct migration by synthesizing and releasing chemotactic signals
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6080930/
https://www.ncbi.nlm.nih.gov/pubmed/29884750
http://dx.doi.org/10.1083/jcb.201710170
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