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Journal articles
A proliferation‐inducing ligand–mediated anti‐inflammatory response of astrocytes in multiple sclerosis
Laurie Baert
1
Mahdia Benkhoucha
2
Natalia Popa
3
Mashal Ahmed
1
Benoit Manfroi
1
Jean Boutonnat
4
Nathalie Sturm
4
Gilda Raguenez
3
Marine Tessier
3
Olivier Casez
5
Romain Marignier
6
Mitra Ahmadi
7
Alexis Broisat
7
Catherine Ghezzi
7
Cyril Rivat
8
Corinne Sonrier
8
Michael Hahne
9
Dominique Baeten
10
Romain R Vivès
11
Hugues Lortat-Jacob
11
Patrice Marche
1
Pascal Schneider
12
Hans Lassmann
13
José Boucraut
3
Patrice Lalive
2, 14
Bertrand Huard
1, *
*
Corresponding author
Michael Hahne 9
Author
Dominique L. Baeten 10
Author
Romain R Vivès 11
Author
Hugues Lortat-Jacob 11
Author
Patrice N. Marche 1
Author IdHAL : patrice-marche ResearcherId : http://www.researcherid.com/rid/K-5060-2013 ORCID : https://orcid.org/0000-0002-8930-9340
Pascal Schneider 12
Author
Hans P Lassmann 13
Author
José Boucraut 3
Author
Patrice H Lalive 2, 14
Author
Bertrand Huard 1
Correspondent author
1
IAB - Institute for Advanced Biosciences / Institut pour l'Avancée des Biosciences (Grenoble) (Institut pour l'Avancée des Biosciences
Centre de Recherche UGA / Inserm U 1209 / CNRS UMR 5309
Site Santé - Allée des Alpes
38700 La Tronche - France)
- CHU - Centre Hospitalier Universitaire [Grenoble] (CS 10217 38043 Grenoble cedex 9 - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale : U1209 (101, rue de Tolbiac, 75013 Paris - France)
- CNRS - Centre National de la Recherche Scientifique : UMR5309 (France)
- EFS - Etablissement français du sang - Auvergne-Rhône-Alpes (France)
- UGA [2016-2019] - Université Grenoble Alpes [2016-2019] (CS 40700 - 38058 Grenoble cedex - France)
2
Clinical Pathology Division - Department of Pathology and Immunology [Geneva, Switzerland] (Geneva University Hospital - 1211 Geneva 4. - Switzerland)
- University of Geneva [Switzerland] (Bd du Pont-d'Arve 40, CH-1211 Geneva 4 - Switzerland)
- Geneva University Hospitals - HUG [Switzerland] (Rue Gabrielle-Perret-Gentil 4, 1205 Genève. - Switzerland)
3
CRN2M - Centre de recherche en neurobiologie - neurophysiologie de Marseille (Faculté de Médecine
Secteur Nord
Boulevard Pierre Dramard
13916 MARSEILLE CEDEX 20 - France)
- AMU - Aix Marseille Université : UMR7286 (Aix-Marseille Université Jardins du Pharo 58 Boulevard Charles Livon 13284 Marseille cedex 7 - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale : UMR7286 (101, rue de Tolbiac, 75013 Paris - France)
- CNRS - Centre National de la Recherche Scientifique : UMR7286 (France)
4
Département d'anatomie et cythologie pathologique (France)
- CHU Grenoble (France)
- Hôpital Michallon (CHU Grenoble-Alpes - France)
5
CHU - Centre Hospitalier Universitaire [Grenoble] (CS 10217
38043 Grenoble cedex 9 - France)
6
CRNL - Centre de recherche en neurosciences de Lyon (CH Le vinatier, 95 bd Pinel, bat B13 59 69677 Bron cedex - France)
- UCBL - Université Claude Bernard Lyon 1 (43, boulevard du 11 novembre 1918, 69622 Villeurbanne cedex - France)
- Université de Lyon (92 rue Pasteur - CS 30122, 69361 Lyon Cedex 07 - France)
- UJM - Université Jean Monnet [Saint-Étienne] (10 rue Tréfilerie - 42100 Saint-Étienne - France)
- Université de Lyon (92 rue Pasteur - CS 30122, 69361 Lyon Cedex 07 - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale : U1028 (101, rue de Tolbiac, 75013 Paris - France)
- CNRS - Centre National de la Recherche Scientifique : UMR5292 (France)
7
LRB - Radiopharmaceutiques biocliniques (Faculté de médecine et pharmacie, Domaine de la Merci, Bat Jean Roget 38700 La Tronche - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale : U1039 (101, rue de Tolbiac, 75013 Paris - France)
- UGA [2016-2019] - Université Grenoble Alpes [2016-2019] (CS 40700 - 38058 Grenoble cedex - France)
8
INM - Institut des Neurosciences de Montpellier - Déficits sensoriels et moteurs (Hôpital Saint Eloi - Bâtiment INM - 80, rue Augustin Fliche - BP 74103 - 34091 Montpellier cedex 5 - France)
- INSERM - Institut National de la Santé et de la Recherche Médicale : U 1051 (101, rue de Tolbiac, 75013 Paris - France)
- UM - Université de Montpellier (163 rue Auguste Broussonnet - 34090 Montpellier - France)
9
IGMM - Institut de Génétique Moléculaire de Montpellier (1919 Route de Mende - 34293 Montpellier Cedex 5 - France)
- UM - Université de Montpellier (163 rue Auguste Broussonnet - 34090 Montpellier - France)
- CNRS - Centre National de la Recherche Scientifique : UMR5535 (France)
10
Department of Clinical Immunology and Rheumatology [Academic Medical Center, Amsterdam] (Netherlands)
- UvA - University of Amsterdam [Amsterdam] (Spui 21 1012 WX Amsterdam - Netherlands)
11
IBS - UMR 5075 - Institut de biologie structurale (Institut de Biologie Structurale, 71 avenue des martyrs, CS 10090, 38044 Grenoble Cedex 9 - France)
- CNRS - Centre National de la Recherche Scientifique : UMR5075 (France)
- UGA [2016-2019] - Université Grenoble Alpes [2016-2019] (CS 40700 - 38058 Grenoble cedex - France)
- IRIG - Institut de Recherche Interdisciplinaire de Grenoble : DRF/IRIG/DBSC (France)
- DRF (CEA) - Direction de Recherche Fondamentale (CEA) : DRF/IRIG (Direction de Recherche Fondamentale
Fundamental Research Division
CEA Saclay
91191 Gif-sur-Yvette
- France)
- CEA - Commissariat à l'énergie atomique et aux énergies alternatives (Centre de Saclay Centre de Grenoble Centre de Cadarache etc - France)
- DRF (CEA) - Direction de Recherche Fondamentale (CEA) : DRF/IRIG (Direction de Recherche Fondamentale
Fundamental Research Division
CEA Saclay
91191 Gif-sur-Yvette
- France)
12
Department of Biochemistry [Lausanne] (Université de Lausanne, Boveresses 155, CH-1066 Epalinges - Switzerland)
- UNIL - Université de Lausanne (CH-1015 Lausanne - Switzerland)
13
University of Vienna [Vienna] (Universitätsring 1, 1010 Wien - Austria)
14
Department of Clinical Neurosciences [Geneva, Switzerland] (Geneva University Hospital - 1211 Geneva 4. - Switzerland)
- Division of Neurology - Unit of Neuroimmunology and Neuromuscular Diseases [Geneva, Switzerland] (Geneva University Hospital - 1211 Geneva 4. - Switzerland)
- Geneva University Hospitals - HUG [Switzerland] (Rue Gabrielle-Perret-Gentil 4, 1205 Genève. - Switzerland)
Abstract : OBJECTIVE:
The two related tumor necrosis factor members a proliferation-inducing ligand (APRIL) and B-cell activation factor (BAFF) are currently targeted in autoimmune diseases as B-cell regulators. In multiple sclerosis (MS), combined APRIL/BAFF blockade led to unexpected exacerbated inflammation in the central nervous system (CNS) of patients. Here, we investigate the role of the APRIL/BAFF axis in the CNS.
METHODS:
APRIL expression was analyzed in MS lesions by immunohistochemistry. The in vivo role of APRIL was assessed in the murine MS model, experimental autoimmune encephalitis (EAE). Functional in vitro studies were performed with human and mouse astrocytes.
RESULTS:
APRIL was expressed in lesions from EAE. In its absence, the disease was worst. Lesions from MS patients also showed APRIL expression upon infiltration of macrophages. Notably, all the APRIL secreted by these macrophages specifically targeted astrocytes. The upregulation of chondroitin sulfate proteoglycan, sometimes bearing chondroitin sulfate of type E sugar moieties, binding APRIL, in reactive astrocytes explained the latter selectivity. Astrocytes responded to APRIL by producing a sufficient amount of IL-10 to dampen antigen-specific T-cell proliferation and pathogenic cytokine secretion. Finally, an intraspinal delivery of recombinant APRIL before disease onset, shortly reduced EAE symptoms. Repeated intravenous injections of recombinant APRIL before and even at disease onset also had an effect.
INTERPRETATION:
Our data show that APRIL mediates an anti-inflammatory response from astrocytes in MS lesions. This protective activity is not shared with BAFF. ANN NEUROL 2019;85:406-420.
© 2019 American Neurological Association.
Document type :
Journal articles
Complete list of metadatas
https://www.hal.inserm.fr/inserm-02332844
Contributor : Patrice Marche <>
Submitted on : Friday, October 25, 2019 - 10:02:10 AM
Last modification on : Friday, November 20, 2020 - 1:00:06 PM
Long-term archiving on: : Sunday, January 26, 2020 - 1:39:30 PM
Contributor : Patrice Marche <>
Submitted on : Friday, October 25, 2019 - 10:02:10 AM
Last modification on : Friday, November 20, 2020 - 1:00:06 PM
Long-term archiving on: : Sunday, January 26, 2020 - 1:39:30 PM
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Identifiers
- HAL Id : inserm-02332844, version 1
- PUBMED : 30635946
- DOI : 10.1002/ana.25415
Collections
INSERM | CNRS | CEA | BS | UNIV-MONTPELLIER | CEA-DRF | UNIV-AMU | IRIG | CEA-GRE | IBS | IBS-SAG | UNIV-ST-ETIENNE | UNIV-LYON1 | UDL | UGA
Citation
Laurie Baert, Mahdia Benkhoucha, Natalia Popa, Mashal Ahmed, Benoit Manfroi, et al.. A proliferation‐inducing ligand–mediated anti‐inflammatory response of astrocytes in multiple sclerosis. Annals of Neurology, Wiley, 2019, 85 (3), pp.406-420. ⟨10.1002/ana.25415⟩. ⟨inserm-02332844⟩
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