AUTHOR=Lombardi Marta , Scaroni Federica , Gabrielli Martina , Raffaele Stefano , Bonfanti Elisabetta , Filipello Fabia , Giussani Paola , Picciolini Silvia , de Rosbo Nicole Kerlero , Uccelli Antonio , Golia Maria Teresa , D’Arrigo Giulia , Rubino Tiziana , Hooshmand Kourosh , Legido-Quigley Cristina , Fenoglio Chiara , Gualerzi Alice , Fumagalli Marta , Verderio Claudia TITLE=Extracellular vesicles released by microglia and macrophages carry endocannabinoids which foster oligodendrocyte differentiation JOURNAL=Frontiers in Immunology VOLUME=15 YEAR=2024 URL=https://www.frontiersin.org/journals/immunology/articles/10.3389/fimmu.2024.1331210 DOI=10.3389/fimmu.2024.1331210 ISSN=1664-3224 ABSTRACT=Introduction

Microglia and macrophages can influence the evolution of myelin lesions through the production of extracellular vesicles (EVs). While microglial EVs promote in vitro differentiation of oligodendrocyte precursor cells (OPCs), whether EVs derived from macrophages aid or limit OPC maturation is unknown.

Methods

Immunofluorescence analysis for the myelin protein MBP was employed to evaluate the impact of EVs from primary rat macrophages on cultured OPC differentiation. Raman spectroscopy and liquid chromatography-mass spectrometry was used to define the promyelinating lipid components of myelin EVs obtained in vitro and isolated from human plasma.

Results and discussion

Here we show that macrophage-derived EVs do not promote OPC differentiation, and those released from macrophages polarized towards an inflammatory state inhibit OPC maturation. However, their lipid cargo promotes OPC maturation in a similar manner to microglial EVs. We identify the promyelinating endocannabinoids anandamide and 2-arachidonoylglycerol in EVs released by both macrophages and microglia in vitro and circulating in human plasma. Analysis of OPC differentiation in the presence of the endocannabinoid receptor antagonists SR141716A and AM630 reveals a key role of vesicular endocannabinoids in OPC maturation. From this study, EV-associated endocannabinoids emerge as important mediators in microglia/macrophage-oligodendrocyte crosstalk, which may be exploited to enhance myelin repair.