Neuron‐derived extracellular vesicles contain synaptic proteins, promote spine formation, activate TrkB‐mediated signalling and preserve neuronal complexity

Abstract Extracellular vesicles (EVs) play an important role in intercellular communication as carriers of signalling molecules such as bioactive miRNAs, proteins and lipids. EVs are key players in the functioning of the central nervous system (CNS) by influencing synaptic events and modulating reci...

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Main Authors: Julia Solana‐Balaguer, Genís Campoy‐Campos, Núria Martín‐Flores, Leticia Pérez‐Sisqués, Laia Sitjà‐Roqueta, Melike Kucukerden, Ana Gámez‐Valero, Albert Coll‐Manzano, Eulàlia Martí, Esther Pérez‐Navarro, Jordi Alberch, Jordi Soriano, Mercè Masana, Cristina Malagelada
Format: Article
Language:English
Published: Wiley 2023-09-01
Series:Journal of Extracellular Vesicles
Subjects:
Online Access:https://doi.org/10.1002/jev2.12355
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author Julia Solana‐Balaguer
Genís Campoy‐Campos
Núria Martín‐Flores
Leticia Pérez‐Sisqués
Laia Sitjà‐Roqueta
Melike Kucukerden
Ana Gámez‐Valero
Albert Coll‐Manzano
Eulàlia Martí
Esther Pérez‐Navarro
Jordi Alberch
Jordi Soriano
Mercè Masana
Cristina Malagelada
author_facet Julia Solana‐Balaguer
Genís Campoy‐Campos
Núria Martín‐Flores
Leticia Pérez‐Sisqués
Laia Sitjà‐Roqueta
Melike Kucukerden
Ana Gámez‐Valero
Albert Coll‐Manzano
Eulàlia Martí
Esther Pérez‐Navarro
Jordi Alberch
Jordi Soriano
Mercè Masana
Cristina Malagelada
author_sort Julia Solana‐Balaguer
collection DOAJ
description Abstract Extracellular vesicles (EVs) play an important role in intercellular communication as carriers of signalling molecules such as bioactive miRNAs, proteins and lipids. EVs are key players in the functioning of the central nervous system (CNS) by influencing synaptic events and modulating recipient neurons. However, the specific role of neuron‐to‐neuron communication via EVs is still not well understood. Here, we provide evidence that primary neurons uptake neuron‐derived EVs in the soma, dendrites, and even in the dendritic spines, and carry synaptic proteins. Neuron‐derived EVs increased spine density and promoted the phosphorylation of Akt and ribosomal protein S6 (RPS6), via TrkB‐signalling, without impairing the neuronal network activity. Strikingly, EVs exerted a trophic effect on challenged nutrient‐deprived neurons. Altogether, our results place EVs in the spotlight for synaptic plasticity modulation as well as a possible therapeutic tool to fight neurodegeneration.
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spelling doaj.art-0be180b1fe9d4b65a4e9bd499c78dd972023-09-26T03:14:31ZengWileyJournal of Extracellular Vesicles2001-30782023-09-01129n/an/a10.1002/jev2.12355Neuron‐derived extracellular vesicles contain synaptic proteins, promote spine formation, activate TrkB‐mediated signalling and preserve neuronal complexityJulia Solana‐Balaguer0Genís Campoy‐Campos1Núria Martín‐Flores2Leticia Pérez‐Sisqués3Laia Sitjà‐Roqueta4Melike Kucukerden5Ana Gámez‐Valero6Albert Coll‐Manzano7Eulàlia Martí8Esther Pérez‐Navarro9Jordi Alberch10Jordi Soriano11Mercè Masana12Cristina Malagelada13Departament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Física de la Matèria Condensada Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainDepartament de Biomedicina, Institut de Neurociències (UBneuro) Universitat de Barcelona BarcelonaSpainAbstract Extracellular vesicles (EVs) play an important role in intercellular communication as carriers of signalling molecules such as bioactive miRNAs, proteins and lipids. EVs are key players in the functioning of the central nervous system (CNS) by influencing synaptic events and modulating recipient neurons. However, the specific role of neuron‐to‐neuron communication via EVs is still not well understood. Here, we provide evidence that primary neurons uptake neuron‐derived EVs in the soma, dendrites, and even in the dendritic spines, and carry synaptic proteins. Neuron‐derived EVs increased spine density and promoted the phosphorylation of Akt and ribosomal protein S6 (RPS6), via TrkB‐signalling, without impairing the neuronal network activity. Strikingly, EVs exerted a trophic effect on challenged nutrient‐deprived neurons. Altogether, our results place EVs in the spotlight for synaptic plasticity modulation as well as a possible therapeutic tool to fight neurodegeneration.https://doi.org/10.1002/jev2.12355extracellular vesicleneuronsynapsesynaptic plasticityTrkB
spellingShingle Julia Solana‐Balaguer
Genís Campoy‐Campos
Núria Martín‐Flores
Leticia Pérez‐Sisqués
Laia Sitjà‐Roqueta
Melike Kucukerden
Ana Gámez‐Valero
Albert Coll‐Manzano
Eulàlia Martí
Esther Pérez‐Navarro
Jordi Alberch
Jordi Soriano
Mercè Masana
Cristina Malagelada
Neuron‐derived extracellular vesicles contain synaptic proteins, promote spine formation, activate TrkB‐mediated signalling and preserve neuronal complexity
Journal of Extracellular Vesicles
extracellular vesicle
neuron
synapse
synaptic plasticity
TrkB
title Neuron‐derived extracellular vesicles contain synaptic proteins, promote spine formation, activate TrkB‐mediated signalling and preserve neuronal complexity
title_full Neuron‐derived extracellular vesicles contain synaptic proteins, promote spine formation, activate TrkB‐mediated signalling and preserve neuronal complexity
title_fullStr Neuron‐derived extracellular vesicles contain synaptic proteins, promote spine formation, activate TrkB‐mediated signalling and preserve neuronal complexity
title_full_unstemmed Neuron‐derived extracellular vesicles contain synaptic proteins, promote spine formation, activate TrkB‐mediated signalling and preserve neuronal complexity
title_short Neuron‐derived extracellular vesicles contain synaptic proteins, promote spine formation, activate TrkB‐mediated signalling and preserve neuronal complexity
title_sort neuron derived extracellular vesicles contain synaptic proteins promote spine formation activate trkb mediated signalling and preserve neuronal complexity
topic extracellular vesicle
neuron
synapse
synaptic plasticity
TrkB
url https://doi.org/10.1002/jev2.12355
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