Intrathecal activation of CD8+ memory T cells in IgG4‐related disease of the brain parenchyma

Abstract IgG4‐related disease (IgG4‐RD) is a fibroinflammatory disorder signified by aberrant infiltration of IgG4‐restricted plasma cells into a variety of organs. Clinical presentation is heterogeneous, and pathophysiological mechanisms of IgG4‐RD remain elusive. There are very few cases of IgG4‐R...

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Main Authors: Mirco Friedrich, Niklas Kehl, Niko Engelke, Josephine Kraus, Katharina Lindner, Philipp Münch, Iris Mildenberger, Christoph Groden, Achim Gass, Nima Etminan, Marc Fatar, Andreas von Deimling, David Reuss, Michael Platten, Lukas Bunse
Format: Article
Language:English
Published: Springer Nature 2021-07-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202113953
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author Mirco Friedrich
Niklas Kehl
Niko Engelke
Josephine Kraus
Katharina Lindner
Philipp Münch
Iris Mildenberger
Christoph Groden
Achim Gass
Nima Etminan
Marc Fatar
Andreas von Deimling
David Reuss
Michael Platten
Lukas Bunse
author_facet Mirco Friedrich
Niklas Kehl
Niko Engelke
Josephine Kraus
Katharina Lindner
Philipp Münch
Iris Mildenberger
Christoph Groden
Achim Gass
Nima Etminan
Marc Fatar
Andreas von Deimling
David Reuss
Michael Platten
Lukas Bunse
author_sort Mirco Friedrich
collection DOAJ
description Abstract IgG4‐related disease (IgG4‐RD) is a fibroinflammatory disorder signified by aberrant infiltration of IgG4‐restricted plasma cells into a variety of organs. Clinical presentation is heterogeneous, and pathophysiological mechanisms of IgG4‐RD remain elusive. There are very few cases of IgG4‐RD with isolated central nervous system manifestation. By leveraging single‐cell sequencing of the cerebrospinal fluid (CSF) of a patient with an inflammatory intracranial pseudotumor, we provide novel insights into the immunopathophysiology of IgG4‐RD. Our data illustrate an IgG4‐RD‐associated polyclonal T‐cell response in the CSF and an oligoclonal T‐cell response in the parenchymal lesions, the latter being the result of a multifaceted cell–cell interaction between immune cell subsets and pathogenic B cells. We demonstrate that CD8+ T effector memory cells might drive and sustain autoimmunity via macrophage migration inhibitory factor (MIF)‐CD74 signaling to immature B cells and CC‐chemokine ligand 5 (CCL5)‐mediated recruitment of cytotoxic CD4+ T cells. These findings highlight the central role of T cells in sustaining IgG4‐RD and open novel avenues for targeted therapies.
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spelling doaj-art-2092b8d7df0b40dfac224be28ccddb6d2025-08-20T03:05:53ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842021-07-0113811010.15252/emmm.202113953Intrathecal activation of CD8+ memory T cells in IgG4‐related disease of the brain parenchymaMirco Friedrich0Niklas Kehl1Niko Engelke2Josephine Kraus3Katharina Lindner4Philipp Münch5Iris Mildenberger6Christoph Groden7Achim Gass8Nima Etminan9Marc Fatar10Andreas von Deimling11David Reuss12Michael Platten13Lukas Bunse14DKTK Clinical Cooperation Unit (CCU) Neuroimmunology and Brain Tumor Immunology, German Cancer Research Center (DKFZ)DKTK Clinical Cooperation Unit (CCU) Neuroimmunology and Brain Tumor Immunology, German Cancer Research Center (DKFZ)Department of Neurology, MCTN, Medical Faculty Mannheim, Heidelberg UniversityDepartment of Neurology, MCTN, Medical Faculty Mannheim, Heidelberg UniversityDKTK Clinical Cooperation Unit (CCU) Neuroimmunology and Brain Tumor Immunology, German Cancer Research Center (DKFZ)DKTK Clinical Cooperation Unit (CCU) Neuroimmunology and Brain Tumor Immunology, German Cancer Research Center (DKFZ)DKTK Clinical Cooperation Unit (CCU) Neuroimmunology and Brain Tumor Immunology, German Cancer Research Center (DKFZ)Department of Neuroradiology, Medical Faculty Mannheim, Heidelberg UniversityDepartment of Neurology, MCTN, Medical Faculty Mannheim, Heidelberg UniversityDepartment of Neurosurgery, Medical Faculty Mannheim, Heidelberg UniversityDepartment of Neurology, MCTN, Medical Faculty Mannheim, Heidelberg UniversityDepartment of Neuropathology, Heidelberg University HospitalDepartment of Neuropathology, Heidelberg University HospitalDKTK Clinical Cooperation Unit (CCU) Neuroimmunology and Brain Tumor Immunology, German Cancer Research Center (DKFZ)DKTK Clinical Cooperation Unit (CCU) Neuroimmunology and Brain Tumor Immunology, German Cancer Research Center (DKFZ)Abstract IgG4‐related disease (IgG4‐RD) is a fibroinflammatory disorder signified by aberrant infiltration of IgG4‐restricted plasma cells into a variety of organs. Clinical presentation is heterogeneous, and pathophysiological mechanisms of IgG4‐RD remain elusive. There are very few cases of IgG4‐RD with isolated central nervous system manifestation. By leveraging single‐cell sequencing of the cerebrospinal fluid (CSF) of a patient with an inflammatory intracranial pseudotumor, we provide novel insights into the immunopathophysiology of IgG4‐RD. Our data illustrate an IgG4‐RD‐associated polyclonal T‐cell response in the CSF and an oligoclonal T‐cell response in the parenchymal lesions, the latter being the result of a multifaceted cell–cell interaction between immune cell subsets and pathogenic B cells. We demonstrate that CD8+ T effector memory cells might drive and sustain autoimmunity via macrophage migration inhibitory factor (MIF)‐CD74 signaling to immature B cells and CC‐chemokine ligand 5 (CCL5)‐mediated recruitment of cytotoxic CD4+ T cells. These findings highlight the central role of T cells in sustaining IgG4‐RD and open novel avenues for targeted therapies.https://doi.org/10.15252/emmm.202113953CSF single‐cell sequencingcytotoxic T helper cellIgG4‐related diseaseinflammatory pseudotumorpathogenic B‐cell
spellingShingle Mirco Friedrich
Niklas Kehl
Niko Engelke
Josephine Kraus
Katharina Lindner
Philipp Münch
Iris Mildenberger
Christoph Groden
Achim Gass
Nima Etminan
Marc Fatar
Andreas von Deimling
David Reuss
Michael Platten
Lukas Bunse
Intrathecal activation of CD8+ memory T cells in IgG4‐related disease of the brain parenchyma
EMBO Molecular Medicine
CSF single‐cell sequencing
cytotoxic T helper cell
IgG4‐related disease
inflammatory pseudotumor
pathogenic B‐cell
title Intrathecal activation of CD8+ memory T cells in IgG4‐related disease of the brain parenchyma
title_full Intrathecal activation of CD8+ memory T cells in IgG4‐related disease of the brain parenchyma
title_fullStr Intrathecal activation of CD8+ memory T cells in IgG4‐related disease of the brain parenchyma
title_full_unstemmed Intrathecal activation of CD8+ memory T cells in IgG4‐related disease of the brain parenchyma
title_short Intrathecal activation of CD8+ memory T cells in IgG4‐related disease of the brain parenchyma
title_sort intrathecal activation of cd8 memory t cells in igg4 related disease of the brain parenchyma
topic CSF single‐cell sequencing
cytotoxic T helper cell
IgG4‐related disease
inflammatory pseudotumor
pathogenic B‐cell
url https://doi.org/10.15252/emmm.202113953
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