Acquisition of residency programs by T cells entering the human brain

Summary: T cell surveillance is mandatory for maintaining central nervous system (CNS) homeostasis, while aberrant accumulation is linked to neuroinflammation. To explore the residency programs acquired by T cells through different anatomical locations of the human brain, we isolated CD8+ and CD4+ T...

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Main Authors: Cheng-Chih Hsiao, Hendrik J. Engelenburg, Jasper Rip, Annet F. Wierenga-Wolf, Fabiënne van Puijfelik, Marvin M. van Luijn, Inge Huitinga, Jörg Hamann, Joost Smolders
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725007314
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author Cheng-Chih Hsiao
Hendrik J. Engelenburg
Jasper Rip
Annet F. Wierenga-Wolf
Fabiënne van Puijfelik
Marvin M. van Luijn
Inge Huitinga
Jörg Hamann
Joost Smolders
author_facet Cheng-Chih Hsiao
Hendrik J. Engelenburg
Jasper Rip
Annet F. Wierenga-Wolf
Fabiënne van Puijfelik
Marvin M. van Luijn
Inge Huitinga
Jörg Hamann
Joost Smolders
author_sort Cheng-Chih Hsiao
collection DOAJ
description Summary: T cell surveillance is mandatory for maintaining central nervous system (CNS) homeostasis, while aberrant accumulation is linked to neuroinflammation. To explore the residency programs acquired by T cells through different anatomical locations of the human brain, we isolated CD8+ and CD4+ T cells from CNS border compartments (choroid plexus and leptomeninges), intrathecal compartments (cerebrospinal fluid [CSF] and subcortical white matter [WM]), and paired peripheral blood of brain donors. Flow cytometry revealed a shared effector memory phenotype across CNS compartments that was partially induced in circulating T cells interacting with brain endothelium in vitro. Intrathecal T cells expressed full tissue-residency traits, yet T cells from WM, compared to CSF, showed reduced expression of migratory, co-stimulatory, and recent activation markers despite a similar cytokine response upon ex vivo activation. This work demonstrates the versatility of T cell phenotypes across CNS compartments and provides insight into the programs regulating their recruitment and maintenance within the CNS.
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institution OA Journals
issn 2211-1247
language English
publishDate 2025-07-01
publisher Elsevier
record_format Article
series Cell Reports
spelling doaj-art-35f6591efb1e48ee85272a50898b56172025-08-20T02:36:09ZengElsevierCell Reports2211-12472025-07-0144711596010.1016/j.celrep.2025.115960Acquisition of residency programs by T cells entering the human brainCheng-Chih Hsiao0Hendrik J. Engelenburg1Jasper Rip2Annet F. Wierenga-Wolf3Fabiënne van Puijfelik4Marvin M. van Luijn5Inge Huitinga6Jörg Hamann7Joost Smolders8Neuroimmunology Research Group, Netherlands Institute for Neuroscience, 1105 BA Amsterdam, the Netherlands; Department of Experimental Immunology, Amsterdam Institute for Immunology and Infectious Diseases, Amsterdam University Medical Center, 1105 AZ Amsterdam, the Netherlands; Corresponding authorNeuroimmunology Research Group, Netherlands Institute for Neuroscience, 1105 BA Amsterdam, the NetherlandsDepartment of Immunology, MS Center ErasMS, Erasmus MC, University Medical Center Rotterdam, 3015 GD Rotterdam, the NetherlandsDepartment of Immunology, MS Center ErasMS, Erasmus MC, University Medical Center Rotterdam, 3015 GD Rotterdam, the NetherlandsDepartment of Immunology, MS Center ErasMS, Erasmus MC, University Medical Center Rotterdam, 3015 GD Rotterdam, the NetherlandsDepartment of Immunology, MS Center ErasMS, Erasmus MC, University Medical Center Rotterdam, 3015 GD Rotterdam, the NetherlandsNeuroimmunology Research Group, Netherlands Institute for Neuroscience, 1105 BA Amsterdam, the Netherlands; Swammerdam Institute for Life Sciences, Center for Neuroscience, University of Amsterdam, 1098 XH Amsterdam, the NetherlandsNeuroimmunology Research Group, Netherlands Institute for Neuroscience, 1105 BA Amsterdam, the Netherlands; Department of Experimental Immunology, Amsterdam Institute for Immunology and Infectious Diseases, Amsterdam University Medical Center, 1105 AZ Amsterdam, the Netherlands; Corresponding authorNeuroimmunology Research Group, Netherlands Institute for Neuroscience, 1105 BA Amsterdam, the Netherlands; Department of Immunology, MS Center ErasMS, Erasmus MC, University Medical Center Rotterdam, 3015 GD Rotterdam, the Netherlands; Department of Neurology, MS Center ErasMS, Erasmus MC, University Medical Center Rotterdam, 3015 GD Rotterdam, the Netherlands; Corresponding authorSummary: T cell surveillance is mandatory for maintaining central nervous system (CNS) homeostasis, while aberrant accumulation is linked to neuroinflammation. To explore the residency programs acquired by T cells through different anatomical locations of the human brain, we isolated CD8+ and CD4+ T cells from CNS border compartments (choroid plexus and leptomeninges), intrathecal compartments (cerebrospinal fluid [CSF] and subcortical white matter [WM]), and paired peripheral blood of brain donors. Flow cytometry revealed a shared effector memory phenotype across CNS compartments that was partially induced in circulating T cells interacting with brain endothelium in vitro. Intrathecal T cells expressed full tissue-residency traits, yet T cells from WM, compared to CSF, showed reduced expression of migratory, co-stimulatory, and recent activation markers despite a similar cytokine response upon ex vivo activation. This work demonstrates the versatility of T cell phenotypes across CNS compartments and provides insight into the programs regulating their recruitment and maintenance within the CNS.http://www.sciencedirect.com/science/article/pii/S2211124725007314CP: NeuroscienceCP: Immunology
spellingShingle Cheng-Chih Hsiao
Hendrik J. Engelenburg
Jasper Rip
Annet F. Wierenga-Wolf
Fabiënne van Puijfelik
Marvin M. van Luijn
Inge Huitinga
Jörg Hamann
Joost Smolders
Acquisition of residency programs by T cells entering the human brain
Cell Reports
CP: Neuroscience
CP: Immunology
title Acquisition of residency programs by T cells entering the human brain
title_full Acquisition of residency programs by T cells entering the human brain
title_fullStr Acquisition of residency programs by T cells entering the human brain
title_full_unstemmed Acquisition of residency programs by T cells entering the human brain
title_short Acquisition of residency programs by T cells entering the human brain
title_sort acquisition of residency programs by t cells entering the human brain
topic CP: Neuroscience
CP: Immunology
url http://www.sciencedirect.com/science/article/pii/S2211124725007314
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