Genetically modified macrophages accelerate myelin repair

Abstract Preventing neurodegeneration‐associated disability progression in patients with multiple sclerosis (MS) remains an unmet therapeutic need. As remyelination prevents axonal degeneration, promoting this process in patients might enhance neuroprotection. In demyelinating mouse lesions, local o...

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Main Authors: Marie‐Stéphane Aigrot, Clara Barthelemy, Sarah Moyon, Gaelle Dufayet‐Chaffaud, Leire Izagirre‐Urizar, Beatrix Gillet‐Legrand, Satoru Tada, Laura Bayón‐Cordero, Juan‐Carlos Chara, Carlos Matute, Nathalie Cartier, Catherine Lubetzki, Vanja Tepavčević
Format: Article
Language:English
Published: Springer Nature 2022-07-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202114759
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author Marie‐Stéphane Aigrot
Clara Barthelemy
Sarah Moyon
Gaelle Dufayet‐Chaffaud
Leire Izagirre‐Urizar
Beatrix Gillet‐Legrand
Satoru Tada
Laura Bayón‐Cordero
Juan‐Carlos Chara
Carlos Matute
Nathalie Cartier
Catherine Lubetzki
Vanja Tepavčević
author_facet Marie‐Stéphane Aigrot
Clara Barthelemy
Sarah Moyon
Gaelle Dufayet‐Chaffaud
Leire Izagirre‐Urizar
Beatrix Gillet‐Legrand
Satoru Tada
Laura Bayón‐Cordero
Juan‐Carlos Chara
Carlos Matute
Nathalie Cartier
Catherine Lubetzki
Vanja Tepavčević
author_sort Marie‐Stéphane Aigrot
collection DOAJ
description Abstract Preventing neurodegeneration‐associated disability progression in patients with multiple sclerosis (MS) remains an unmet therapeutic need. As remyelination prevents axonal degeneration, promoting this process in patients might enhance neuroprotection. In demyelinating mouse lesions, local overexpression of semaphorin 3F (Sema3F), an oligodendrocyte progenitor cell (OPC) attractant, increases remyelination. However, molecular targeting to MS lesions is a challenge. A clinically relevant paradigm for delivering Sema3F to demyelinating lesions could be to use blood‐derived macrophages as vehicles. Thus, we chose transplantation of genetically modified hematopoietic stem cells (HSCs) as means of obtaining chimeric mice with circulating Sema3F‐overexpressing monocytes. We demonstrated that Sema3F‐transduced HSCs stimulate OPC migration in a neuropilin 2 (Nrp2, Sema3F receptor)‐dependent fashion, which was conserved in middle‐aged OPCs. While demyelinating lesions induced in mice with Sema3F‐expressing blood cells showed no changes in inflammation and OPC survival, OPC recruitment was enhanced which accelerated the onset of remyelination. Our results provide a proof of concept that blood cells, particularly monocytes/macrophages, can be used to deliver pro‐remyelinating agents “at the right time and place,” suggesting novel means for remyelination‐promoting strategies in MS.
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spelling doaj-art-c1839741b7e847299f847e6b2eb4852c2025-08-20T04:03:02ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842022-07-0114811710.15252/emmm.202114759Genetically modified macrophages accelerate myelin repairMarie‐Stéphane Aigrot0Clara Barthelemy1Sarah Moyon2Gaelle Dufayet‐Chaffaud3Leire Izagirre‐Urizar4Beatrix Gillet‐Legrand5Satoru Tada6Laura Bayón‐Cordero7Juan‐Carlos Chara8Carlos Matute9Nathalie Cartier10Catherine Lubetzki11Vanja Tepavčević12INSERM UMR1127 Sorbonne Université, Paris Brain Institute (ICM)INSERM UMR1127 Sorbonne Université, Paris Brain Institute (ICM)NYU Langone Health, Neuroscience InstituteINSERM UMR1127 Sorbonne Université, Paris Brain Institute (ICM)Achucarro Basque Center for Neuroscience/Department of Neuroscience, School of Medicine University of the Basque CountryINSERM UMR1127 Sorbonne Université, Paris Brain Institute (ICM)INSERM UMR1127 Sorbonne Université, Paris Brain Institute (ICM)Achucarro Basque Center for Neuroscience/Department of Neuroscience, School of Medicine University of the Basque CountryAchucarro Basque Center for Neuroscience/Department of Neuroscience, School of Medicine University of the Basque CountryAchucarro Basque Center for Neuroscience/Department of Neuroscience, School of Medicine University of the Basque CountryAsklepios Biopharmaceutical, Inc., Institut du Cerveau (ICM)INSERM UMR1127 Sorbonne Université, Paris Brain Institute (ICM)Achucarro Basque Center for Neuroscience/Department of Neuroscience, School of Medicine University of the Basque CountryAbstract Preventing neurodegeneration‐associated disability progression in patients with multiple sclerosis (MS) remains an unmet therapeutic need. As remyelination prevents axonal degeneration, promoting this process in patients might enhance neuroprotection. In demyelinating mouse lesions, local overexpression of semaphorin 3F (Sema3F), an oligodendrocyte progenitor cell (OPC) attractant, increases remyelination. However, molecular targeting to MS lesions is a challenge. A clinically relevant paradigm for delivering Sema3F to demyelinating lesions could be to use blood‐derived macrophages as vehicles. Thus, we chose transplantation of genetically modified hematopoietic stem cells (HSCs) as means of obtaining chimeric mice with circulating Sema3F‐overexpressing monocytes. We demonstrated that Sema3F‐transduced HSCs stimulate OPC migration in a neuropilin 2 (Nrp2, Sema3F receptor)‐dependent fashion, which was conserved in middle‐aged OPCs. While demyelinating lesions induced in mice with Sema3F‐expressing blood cells showed no changes in inflammation and OPC survival, OPC recruitment was enhanced which accelerated the onset of remyelination. Our results provide a proof of concept that blood cells, particularly monocytes/macrophages, can be used to deliver pro‐remyelinating agents “at the right time and place,” suggesting novel means for remyelination‐promoting strategies in MS.https://doi.org/10.15252/emmm.202114759gene therapymultiple sclerosisoligodendrocyte progenitor cellsremyelinationsemaphorin 3F
spellingShingle Marie‐Stéphane Aigrot
Clara Barthelemy
Sarah Moyon
Gaelle Dufayet‐Chaffaud
Leire Izagirre‐Urizar
Beatrix Gillet‐Legrand
Satoru Tada
Laura Bayón‐Cordero
Juan‐Carlos Chara
Carlos Matute
Nathalie Cartier
Catherine Lubetzki
Vanja Tepavčević
Genetically modified macrophages accelerate myelin repair
EMBO Molecular Medicine
gene therapy
multiple sclerosis
oligodendrocyte progenitor cells
remyelination
semaphorin 3F
title Genetically modified macrophages accelerate myelin repair
title_full Genetically modified macrophages accelerate myelin repair
title_fullStr Genetically modified macrophages accelerate myelin repair
title_full_unstemmed Genetically modified macrophages accelerate myelin repair
title_short Genetically modified macrophages accelerate myelin repair
title_sort genetically modified macrophages accelerate myelin repair
topic gene therapy
multiple sclerosis
oligodendrocyte progenitor cells
remyelination
semaphorin 3F
url https://doi.org/10.15252/emmm.202114759
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