Blood immunophenotyping of multiple sclerosis patients at diagnosis identifies a classical monocyte subset associated to disease evolution

IntroductionMyeloid cells trafficking from the periphery to the central nervous system are key players in multiple sclerosis (MS) through antigen presentation, cytokine secretion and repair processes.MethodsCombination of mass cytometry on blood cells from 60 MS patients at diagnosis and 29 healthy...

Full description

Saved in:
Bibliographic Details
Main Authors: Stéphane Rodriguez, Laura Couloume, Juliette Ferrant, Nicolas Vince, Marion Mandon, Rachel Jean, Celine Monvoisin, Simon Leonard, Simon Le Gallou, Nayane S. B. Silva, Sonia Bourguiba-Hachemi, David Laplaud, Alexandra Garcia, Romain Casey, Helene Zephir, Anne Kerbrat, Gilles Edan, Emmanuelle Lepage, Eric Thouvenot, Aurelie Ruet, Guillaume Mathey, Pierre-Antoine Gourraud, Karin Tarte, Celine Delaloy, Patricia Amé, Mikael Roussel, Laure Michel
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2024.1494842/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1841554927970680832
author Stéphane Rodriguez
Stéphane Rodriguez
Laura Couloume
Juliette Ferrant
Juliette Ferrant
Nicolas Vince
Marion Mandon
Marion Mandon
Rachel Jean
Rachel Jean
Celine Monvoisin
Simon Leonard
Simon Le Gallou
Simon Le Gallou
Nayane S. B. Silva
Nayane S. B. Silva
Sonia Bourguiba-Hachemi
David Laplaud
David Laplaud
Alexandra Garcia
Romain Casey
Romain Casey
Romain Casey
Romain Casey
Helene Zephir
Anne Kerbrat
Gilles Edan
Emmanuelle Lepage
Eric Thouvenot
Eric Thouvenot
Aurelie Ruet
Aurelie Ruet
Guillaume Mathey
Guillaume Mathey
Pierre-Antoine Gourraud
Pierre-Antoine Gourraud
Karin Tarte
Karin Tarte
Celine Delaloy
Patricia Amé
Patricia Amé
Mikael Roussel
Mikael Roussel
Laure Michel
Laure Michel
Laure Michel
author_facet Stéphane Rodriguez
Stéphane Rodriguez
Laura Couloume
Juliette Ferrant
Juliette Ferrant
Nicolas Vince
Marion Mandon
Marion Mandon
Rachel Jean
Rachel Jean
Celine Monvoisin
Simon Leonard
Simon Le Gallou
Simon Le Gallou
Nayane S. B. Silva
Nayane S. B. Silva
Sonia Bourguiba-Hachemi
David Laplaud
David Laplaud
Alexandra Garcia
Romain Casey
Romain Casey
Romain Casey
Romain Casey
Helene Zephir
Anne Kerbrat
Gilles Edan
Emmanuelle Lepage
Eric Thouvenot
Eric Thouvenot
Aurelie Ruet
Aurelie Ruet
Guillaume Mathey
Guillaume Mathey
Pierre-Antoine Gourraud
Pierre-Antoine Gourraud
Karin Tarte
Karin Tarte
Celine Delaloy
Patricia Amé
Patricia Amé
Mikael Roussel
Mikael Roussel
Laure Michel
Laure Michel
Laure Michel
author_sort Stéphane Rodriguez
collection DOAJ
description IntroductionMyeloid cells trafficking from the periphery to the central nervous system are key players in multiple sclerosis (MS) through antigen presentation, cytokine secretion and repair processes.MethodsCombination of mass cytometry on blood cells from 60 MS patients at diagnosis and 29 healthy controls, along with single cell RNA sequencing on paired blood and cerebrospinal fluid (CSF) samples from 5 MS patients were used for myeloid cells detailing.ResultsMyeloid compartment study demonstrated an enrichment of a peculiar classical monocyte population in 22% of MS patients at the time of diagnosis. Notably, this patients’ subgroup exhibited a more aggressive disease phenotype two years post-diagnosis. This monocytic population, detected in both the CSF and blood, was characterized by CD206, CD209, CCR5 and CCR2 expression, and was found to be more frequent in MS patients carrying the HLA-DRB1*15:01 allele. Furthermore, pathways analysis predicted that these cells had antigen presentation capabilities coupled with pro-inflammatory phenotype.DiscussionAltogether, these results point toward the amplification of a specific and pathogenic myeloid cell subset in MS patients with genetic susceptibilities.
format Article
id doaj-art-39dcf655253348839790e0e5abb3f93b
institution Kabale University
issn 1664-3224
language English
publishDate 2025-01-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj-art-39dcf655253348839790e0e5abb3f93b2025-01-08T08:14:48ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-01-011510.3389/fimmu.2024.14948421494842Blood immunophenotyping of multiple sclerosis patients at diagnosis identifies a classical monocyte subset associated to disease evolutionStéphane Rodriguez0Stéphane Rodriguez1Laura Couloume2Juliette Ferrant3Juliette Ferrant4Nicolas Vince5Marion Mandon6Marion Mandon7Rachel Jean8Rachel Jean9Celine Monvoisin10Simon Leonard11Simon Le Gallou12Simon Le Gallou13Nayane S. B. Silva14Nayane S. B. Silva15Sonia Bourguiba-Hachemi16David Laplaud17David Laplaud18Alexandra Garcia19Romain Casey20Romain Casey21Romain Casey22Romain Casey23Helene Zephir24Anne Kerbrat25Gilles Edan26Emmanuelle Lepage27Eric Thouvenot28Eric Thouvenot29Aurelie Ruet30Aurelie Ruet31Guillaume Mathey32Guillaume Mathey33Pierre-Antoine Gourraud34Pierre-Antoine Gourraud35Karin Tarte36Karin Tarte37Celine Delaloy38Patricia Amé39Patricia Amé40Mikael Roussel41Mikael Roussel42Laure Michel43Laure Michel44Laure Michel45Institut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FrancePole Biologie-Centre Hospitalier Universitaire (CHU) Rennes, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FrancePole Biologie-Centre Hospitalier Universitaire (CHU) Rennes, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Nantes, Nantes University, Center for Research in Transplantation and Translational Immunology, UMR 1064, Nantes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FrancePole Biologie-Centre Hospitalier Universitaire (CHU) Rennes, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FrancePole Biologie-Centre Hospitalier Universitaire (CHU) Rennes, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FrancePole Biologie-Centre Hospitalier Universitaire (CHU) Rennes, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Nantes, Nantes University, Center for Research in Transplantation and Translational Immunology, UMR 1064, Nantes, FranceSão Paulo State University, Molecular Genetics and Bioinformatics Laboratory, School of Medicine, Botucatu, BrazilInstitut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Nantes, Nantes University, Center for Research in Transplantation and Translational Immunology, UMR 1064, Nantes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Nantes, Nantes University, Center for Research in Transplantation and Translational Immunology, UMR 1064, Nantes, FranceService de Neurologie, Centre Hospitalier Universitaire (CHU) Nantes, CRC-SEP Pays de la Loire, CIC 1413, Nantes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Nantes, Nantes University, Center for Research in Transplantation and Translational Immunology, UMR 1064, Nantes, FranceLyon University, University Claude Bernard Lyon 1, Lyon, FranceHospices Civils de Lyon, Neurology Department, Sclérose en Plaques, Pathologies de la Myéline et Neuro-Inflammation, Bron, FranceObservatoire Français de la Sclérose en Plaques, Centre de Recherche en Neurosciences de Lyon, INSERM 1028 and CNRS UMR 5292, Lyon, FranceEUGENE DEVIC EDMUS Foundation against Multiple Sclerosis, State-Approved Foundation, Bron, France0Lille University, Inserm U1172, Lille University Hospital, Lille, France1Neurology Department, Rennes Clinical Investigation Centre, Rennes University Hospital-Rennes University-Institut National de la Santé et de la Recherche Médicale (INSERM), Rennes, France1Neurology Department, Rennes Clinical Investigation Centre, Rennes University Hospital-Rennes University-Institut National de la Santé et de la Recherche Médicale (INSERM), Rennes, France1Neurology Department, Rennes Clinical Investigation Centre, Rennes University Hospital-Rennes University-Institut National de la Santé et de la Recherche Médicale (INSERM), Rennes, France2Department of Neurology, Nimes University Hospital, Nimes, France3Institut de Génomique Fonctionnelle, UMR5203, Inserm 1191, Université de Montpellier, Montpellier, France4Neurocentre Magendie, Institut National de la Santé et de la Recherche Médicale (INSERM) U1215, Bordeaux, France5CHU de Bordeaux, Department of Neurology, Bordeaux, France6Department of Neurology, Nancy University Hospital, Nancy, France7Université de Lorraine, Inserm, INSPIIRE, Nancy, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Nantes, Nantes University, Center for Research in Transplantation and Translational Immunology, UMR 1064, Nantes, FranceService de Neurologie, Centre Hospitalier Universitaire (CHU) Nantes, CRC-SEP Pays de la Loire, CIC 1413, Nantes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FrancePole Biologie-Centre Hospitalier Universitaire (CHU) Rennes, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FrancePole Biologie-Centre Hospitalier Universitaire (CHU) Rennes, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FrancePole Biologie-Centre Hospitalier Universitaire (CHU) Rennes, Rennes, FranceInstitut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche U1236, Université Rennes, Etablissement Français du Sang Bretagne, LabEx IGO, Rennes, FrancePole Biologie-Centre Hospitalier Universitaire (CHU) Rennes, Rennes, FranceObservatoire Français de la Sclérose en Plaques, Centre de Recherche en Neurosciences de Lyon, INSERM 1028 and CNRS UMR 5292, Lyon, FranceIntroductionMyeloid cells trafficking from the periphery to the central nervous system are key players in multiple sclerosis (MS) through antigen presentation, cytokine secretion and repair processes.MethodsCombination of mass cytometry on blood cells from 60 MS patients at diagnosis and 29 healthy controls, along with single cell RNA sequencing on paired blood and cerebrospinal fluid (CSF) samples from 5 MS patients were used for myeloid cells detailing.ResultsMyeloid compartment study demonstrated an enrichment of a peculiar classical monocyte population in 22% of MS patients at the time of diagnosis. Notably, this patients’ subgroup exhibited a more aggressive disease phenotype two years post-diagnosis. This monocytic population, detected in both the CSF and blood, was characterized by CD206, CD209, CCR5 and CCR2 expression, and was found to be more frequent in MS patients carrying the HLA-DRB1*15:01 allele. Furthermore, pathways analysis predicted that these cells had antigen presentation capabilities coupled with pro-inflammatory phenotype.DiscussionAltogether, these results point toward the amplification of a specific and pathogenic myeloid cell subset in MS patients with genetic susceptibilities.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1494842/fullmultiple sclerosiscerebrospinal fluidclassical monocytedisabilityantigen presentation
spellingShingle Stéphane Rodriguez
Stéphane Rodriguez
Laura Couloume
Juliette Ferrant
Juliette Ferrant
Nicolas Vince
Marion Mandon
Marion Mandon
Rachel Jean
Rachel Jean
Celine Monvoisin
Simon Leonard
Simon Le Gallou
Simon Le Gallou
Nayane S. B. Silva
Nayane S. B. Silva
Sonia Bourguiba-Hachemi
David Laplaud
David Laplaud
Alexandra Garcia
Romain Casey
Romain Casey
Romain Casey
Romain Casey
Helene Zephir
Anne Kerbrat
Gilles Edan
Emmanuelle Lepage
Eric Thouvenot
Eric Thouvenot
Aurelie Ruet
Aurelie Ruet
Guillaume Mathey
Guillaume Mathey
Pierre-Antoine Gourraud
Pierre-Antoine Gourraud
Karin Tarte
Karin Tarte
Celine Delaloy
Patricia Amé
Patricia Amé
Mikael Roussel
Mikael Roussel
Laure Michel
Laure Michel
Laure Michel
Blood immunophenotyping of multiple sclerosis patients at diagnosis identifies a classical monocyte subset associated to disease evolution
Frontiers in Immunology
multiple sclerosis
cerebrospinal fluid
classical monocyte
disability
antigen presentation
title Blood immunophenotyping of multiple sclerosis patients at diagnosis identifies a classical monocyte subset associated to disease evolution
title_full Blood immunophenotyping of multiple sclerosis patients at diagnosis identifies a classical monocyte subset associated to disease evolution
title_fullStr Blood immunophenotyping of multiple sclerosis patients at diagnosis identifies a classical monocyte subset associated to disease evolution
title_full_unstemmed Blood immunophenotyping of multiple sclerosis patients at diagnosis identifies a classical monocyte subset associated to disease evolution
title_short Blood immunophenotyping of multiple sclerosis patients at diagnosis identifies a classical monocyte subset associated to disease evolution
title_sort blood immunophenotyping of multiple sclerosis patients at diagnosis identifies a classical monocyte subset associated to disease evolution
topic multiple sclerosis
cerebrospinal fluid
classical monocyte
disability
antigen presentation
url https://www.frontiersin.org/articles/10.3389/fimmu.2024.1494842/full
work_keys_str_mv AT stephanerodriguez bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT stephanerodriguez bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT lauracouloume bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT julietteferrant bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT julietteferrant bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT nicolasvince bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT marionmandon bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT marionmandon bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT racheljean bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT racheljean bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT celinemonvoisin bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT simonleonard bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT simonlegallou bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT simonlegallou bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT nayanesbsilva bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT nayanesbsilva bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT soniabourguibahachemi bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT davidlaplaud bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT davidlaplaud bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT alexandragarcia bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT romaincasey bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT romaincasey bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT romaincasey bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT romaincasey bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT helenezephir bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT annekerbrat bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT gillesedan bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT emmanuellelepage bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT ericthouvenot bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT ericthouvenot bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT aurelieruet bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT aurelieruet bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT guillaumemathey bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT guillaumemathey bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT pierreantoinegourraud bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT pierreantoinegourraud bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT karintarte bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT karintarte bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT celinedelaloy bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT patriciaame bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT patriciaame bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT mikaelroussel bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT mikaelroussel bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT lauremichel bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT lauremichel bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution
AT lauremichel bloodimmunophenotypingofmultiplesclerosispatientsatdiagnosisidentifiesaclassicalmonocytesubsetassociatedtodiseaseevolution