Neuronal activity triggers uptake of hematopoietic extracellular vesicles in vivo.
Communication with the hematopoietic system is a vital component of regulating brain function in health and disease. Traditionally, the major routes considered for this neuroimmune communication are by individual molecules such as cytokines carried by blood, by neural transmission, or, in more sever...
Main Authors: | , , , , , , , , , , |
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Format: | Article |
Language: | English |
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Public Library of Science (PLoS)
2020-03-01
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Series: | PLoS Biology |
Online Access: | https://doi.org/10.1371/journal.pbio.3000643 |
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author | Ivan-Maximiliano Kur Pierre-Hugues Prouvot Ting Fu Wei Fan Felicia Müller-Braun Avash Das Saumya Das Thomas Deller Jochen Roeper Albrecht Stroh Stefan Momma |
author_facet | Ivan-Maximiliano Kur Pierre-Hugues Prouvot Ting Fu Wei Fan Felicia Müller-Braun Avash Das Saumya Das Thomas Deller Jochen Roeper Albrecht Stroh Stefan Momma |
author_sort | Ivan-Maximiliano Kur |
collection | DOAJ |
description | Communication with the hematopoietic system is a vital component of regulating brain function in health and disease. Traditionally, the major routes considered for this neuroimmune communication are by individual molecules such as cytokines carried by blood, by neural transmission, or, in more severe pathologies, by the entry of peripheral immune cells into the brain. In addition, functional mRNA from peripheral blood can be directly transferred to neurons via extracellular vesicles (EVs), but the parameters that determine their uptake are unknown. Using varied animal models that stimulate neuronal activity by peripheral inflammation, optogenetics, and selective proteasome inhibition of dopaminergic (DA) neurons, we show that the transfer of EVs from blood is triggered by neuronal activity in vivo. Importantly, this transfer occurs not only in pathological stimulation but also by neuronal activation caused by the physiological stimulus of novel object placement. This discovery suggests a continuous role of EVs under pathological conditions as well as during routine cognitive tasks in the healthy brain. |
first_indexed | 2024-12-23T19:13:13Z |
format | Article |
id | doaj.art-445dbee201c447f9a0b3af1243c3375c |
institution | Directory Open Access Journal |
issn | 1544-9173 1545-7885 |
language | English |
last_indexed | 2024-12-23T19:13:13Z |
publishDate | 2020-03-01 |
publisher | Public Library of Science (PLoS) |
record_format | Article |
series | PLoS Biology |
spelling | doaj.art-445dbee201c447f9a0b3af1243c3375c2022-12-21T17:34:24ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852020-03-01183e300064310.1371/journal.pbio.3000643Neuronal activity triggers uptake of hematopoietic extracellular vesicles in vivo.Ivan-Maximiliano KurPierre-Hugues ProuvotTing FuWei FanFelicia Müller-BraunAvash DasSaumya DasThomas DellerJochen RoeperAlbrecht StrohStefan MommaCommunication with the hematopoietic system is a vital component of regulating brain function in health and disease. Traditionally, the major routes considered for this neuroimmune communication are by individual molecules such as cytokines carried by blood, by neural transmission, or, in more severe pathologies, by the entry of peripheral immune cells into the brain. In addition, functional mRNA from peripheral blood can be directly transferred to neurons via extracellular vesicles (EVs), but the parameters that determine their uptake are unknown. Using varied animal models that stimulate neuronal activity by peripheral inflammation, optogenetics, and selective proteasome inhibition of dopaminergic (DA) neurons, we show that the transfer of EVs from blood is triggered by neuronal activity in vivo. Importantly, this transfer occurs not only in pathological stimulation but also by neuronal activation caused by the physiological stimulus of novel object placement. This discovery suggests a continuous role of EVs under pathological conditions as well as during routine cognitive tasks in the healthy brain.https://doi.org/10.1371/journal.pbio.3000643 |
spellingShingle | Ivan-Maximiliano Kur Pierre-Hugues Prouvot Ting Fu Wei Fan Felicia Müller-Braun Avash Das Saumya Das Thomas Deller Jochen Roeper Albrecht Stroh Stefan Momma Neuronal activity triggers uptake of hematopoietic extracellular vesicles in vivo. PLoS Biology |
title | Neuronal activity triggers uptake of hematopoietic extracellular vesicles in vivo. |
title_full | Neuronal activity triggers uptake of hematopoietic extracellular vesicles in vivo. |
title_fullStr | Neuronal activity triggers uptake of hematopoietic extracellular vesicles in vivo. |
title_full_unstemmed | Neuronal activity triggers uptake of hematopoietic extracellular vesicles in vivo. |
title_short | Neuronal activity triggers uptake of hematopoietic extracellular vesicles in vivo. |
title_sort | neuronal activity triggers uptake of hematopoietic extracellular vesicles in vivo |
url | https://doi.org/10.1371/journal.pbio.3000643 |
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