Alemtuzumab treatment exemplifies discordant immune effects of blood and cerebrospinal fluid in multiple sclerosis.


Journal

Journal of neuroimmunology
ISSN: 1872-8421
Titre abrégé: J Neuroimmunol
Pays: Netherlands
ID NLM: 8109498

Informations de publication

Date de publication:
15 05 2023
Historique:
received: 21 02 2023
revised: 03 04 2023
accepted: 08 04 2023
medline: 8 5 2023
pubmed: 17 4 2023
entrez: 16 4 2023
Statut: ppublish

Résumé

Immune responses in the central nervous system (CNS) are highly compartmentalized and cerebrospinal fluid (CSF) in particular often reflects CNS pathology better than peripheral blood. While CSF leukocytes are known to be distinct from blood, the immediate effects of peripheral leukocyte depletion on CSF leukocytes have not been studied in humans. We here analyzed CSF and blood from two relapsing-remitting multiple sclerosis (RRMS) patients early after peripheral leukocyte depletion with the anti-CD52 antibody alemtuzumab compared to untreated RRMS and control patients using single cell RNA-sequencing. As expected for alemtuzumab, most leukocyte lineages including T cells were synchronously depleted from CSF and blood, while - surprisingly - pDCs were maintained in CSF but depleted from blood by alemtuzumab. Transcriptionally, genes associated with migration were elevated only in the CSF after alemtuzumab. Predicted cellular interactions indicated a central role of pDCs and enhanced migration signaling in the CSF after alemtuzumab. The CSF and blood compartments are thus partially uncoupled, emphasizing that the CNS is only partially accessible even for treatments profoundly affecting the blood.

Sections du résumé

BACKGROUND AND OBJECTIVES
Immune responses in the central nervous system (CNS) are highly compartmentalized and cerebrospinal fluid (CSF) in particular often reflects CNS pathology better than peripheral blood. While CSF leukocytes are known to be distinct from blood, the immediate effects of peripheral leukocyte depletion on CSF leukocytes have not been studied in humans.
METHODS
We here analyzed CSF and blood from two relapsing-remitting multiple sclerosis (RRMS) patients early after peripheral leukocyte depletion with the anti-CD52 antibody alemtuzumab compared to untreated RRMS and control patients using single cell RNA-sequencing.
RESULTS
As expected for alemtuzumab, most leukocyte lineages including T cells were synchronously depleted from CSF and blood, while - surprisingly - pDCs were maintained in CSF but depleted from blood by alemtuzumab. Transcriptionally, genes associated with migration were elevated only in the CSF after alemtuzumab. Predicted cellular interactions indicated a central role of pDCs and enhanced migration signaling in the CSF after alemtuzumab.
DISCUSSION
The CSF and blood compartments are thus partially uncoupled, emphasizing that the CNS is only partially accessible even for treatments profoundly affecting the blood.

Identifiants

pubmed: 37062182
pii: S0165-5728(23)00074-7
doi: 10.1016/j.jneuroim.2023.578088
pii:
doi:

Substances chimiques

Alemtuzumab 3A189DH42V

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

578088

Informations de copyright

Copyright © 2023 Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest GMzH received compensation for serving on scientific advisory boards (LFB) and speaker honoraria (Alexion). HW is acting as a paid consultant for AbbVie, Actelion, Biogen, IGES, Johnson & Johnson, Novartis, Roche, Sanofi-Aventis, and the Swiss Multiple Sclerosis Society. The remaining authors declare no financial interests or conflicts of interest.

Auteurs

Louisa Müller-Miny (L)

Department of Neurology with Institute of Translational Neurology, University Hospital Münster, Münster, Germany.

Michael Heming (M)

Department of Neurology with Institute of Translational Neurology, University Hospital Münster, Münster, Germany.

Tobias Lautwein (T)

Biologisch-Medizinisches Forschungszentrum (BMFZ), Genomics and Transcriptomics Labor, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany.

Tobias Ruck (T)

Department of Neurology, Medical Faculty, Heinrich-Heine-University Düsseldorf, Moorenstraße 5, 40225 Düsseldorf, Germany.

I-Na Lu (IN)

Department of Neurology with Institute of Translational Neurology, University Hospital Münster, Münster, Germany.

Heinz Wiendl (H)

Department of Neurology with Institute of Translational Neurology, University Hospital Münster, Münster, Germany.

Gerd Meyer Zu Hörste (G)

Department of Neurology with Institute of Translational Neurology, University Hospital Münster, Münster, Germany. Electronic address: gerd.mzh@uni-muenster.de.

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Classifications MeSH