Cited by 211Neuroinflammation and Neurodegeneration MechanismsMultiple Sclerosis Research StudiesAutoimmune Neurological Disorders and Treatments

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Neurons under T Cell Attack Coordinate Phagocyte-Mediated Synaptic Stripping

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Di Liberto, Giovanni, Pantelyushin, Stanislav, Kreutzfeldt, Mario, Page, Nicolas, Musardo, Stefano, Coras, Roland, Steinbach, Karin, Vincenti, Ilena, Klimek, Bogna, Lingner, Thomas, Salinas, Gabriela, Lin-Marq, Nathalie, Staszewski, Ori, Costa Jordão, Marta Joana, Wagner, Ingrid, Egervari, Kristof, Mack, Matthias, Bellone, Camilla, Blümcke, Ingmar, Prinz, Marco, Pinschewer, Daniel D., Merkler, Doron·2018·Cell

DOI 10.1016/j.cell.2018.07.049

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Abstract

Inflammatory disorders of the CNS are frequently accompanied by synaptic loss, which is thought to involve phagocytic microglia and complement components. However, the mechanisms accounting for aberrant synaptic connectivity in the context of CD8+ T cell-driven neuronal damage are poorly understood. Here, we profiled the neuronal translatome in a murine model of encephalitis caused by CD8+ T cells targeting antigenic neurons. Neuronal STAT1 signaling and downstream CCL2 expression were essential for apposition of phagocytes, ensuing synaptic loss and neurological disease. Analogous observations were made in the brains of Rasmussen's encephalitis patients. In this devastating CD8+ T cell-driven autoimmune disease, neuronal STAT1 phosphorylation and CCL2 expression co-clustered with infiltrating CD8+ T cells as well as phagocytes. Taken together, our findings uncover an active role of neurons in coordinating phagocyte-mediated synaptic loss and highlight neuronal STAT1 and CCL2 as critical steps in this process that are amenable to pharmacological interventions.

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Additional file 14 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711651
Additional file 4 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711621
Additional file 10 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711639
Additional file 15 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711654
Additional file 5 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711624
Additional file 21 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711672
Additional file 9 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711636
Additional file 11 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711642
Additional file 16 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711657
Additional file 18 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711663
Additional file 7 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711630
Additional file 13 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711648
Additional file 2 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25687615
Additional file 8 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711633
Additional file 12 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711645
Additional file 1 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25687445
Additional file 3 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711618
Additional file 20 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711669
Additional file 6 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711627
Additional file 19 of Adaptive immune changes associate with clinical progression of Alzheimer’s disease
van Olst, L., Kamermans, A., Halters, S., van der Pol, S. M. A., Rodríguez, E., Verberk, I. M. W., Verberk, S. G. S., Wessels, D. W. R., Rodriguez-Mogeda, C., Verhoeff, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26711666

Authors: Di Liberto, G., Pantelyushin, S., Kreutzfeldt, M., Page, N., Musardo, S., Coras, R., Steinbach, K., Vincenti, I., Klimek, B., Lingner, T., Salinas, G., Lin-Marq, N., Staszewski, O., Costa Jordão, M. J., Wagner, I., Egervari, K., Mack, M., Bellone, C., Blümcke, I., Prinz, M., Pinschewer, D. D., & Merkler, D.
Affiliations: University of Geneva (CH)
Universitätsklinikum Erlangen (DE)
Universitätsmedizin Göttingen (DE)
University Hospital of Geneva (CH)
University of Freiburg (DE)
University of Basel (CH)
Corresponding author: Merkler, Doron
ORCID: Pantelyushin, Stanislav
Kreutzfeldt, Mario
Musardo, Stefano
Coras, Roland
Steinbach, Karin
Vincenti, Ilena
Klimek, Bogna
Salinas, Gabriela
Staszewski, Ori
Wagner, Ingrid
Egervari, Kristof
Mack, Matthias
Bellone, Camilla
Blümcke, Ingmar
Prinz, Marco
Pinschewer, Daniel D.
Merkler, Doron
Venue: Cell
Publisher: Elsevier BV
Published: 2018-10
Volume: 175
Issue: 2
Pages: 458-471.e19
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2018.07.049
OpenAlex: W2888970970
Cited by: 195
References: 55
Citations by year: 2026: 15 · 2025: 20 · 2024: 34 · 2023: 25 · 2022: 34 · 2021: 27 · 2020: 18 · 2019: 19 · 2018: 2
FWCI: 7.40
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 368 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Archive ouverte UNIGE (University of Geneva) (publishedVersion)
edoc (University of Basel) (submittedVersion)
University of Regensburg Publication Server (University of Regensburg) (submittedVersion)
GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
Funders: Gebert-Rüf Foundation (GRS-049/13)
Klaus-Tschira Foundation
Swiss National Science Foundation
Swiss MS Society
Helmut Horten Foundation
BMBF
Competence Network of Multiple Sclerosis
Sobek-Stiftung
DFG (SFB 992, SFB1160, SFB/TRR167, Reinhart-Koselleck grant)
Ministry of Science, Research and the Arts, Baden-Wuerttemberg (Sonderlinie “Neuroinflammation”)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Health Sciences › Medicine › Clinical Neurology › Autoimmune Neurological Disorders and Treatments
Keywords: synaptic stripping, CD8+ T cells, MCP-1, microglia, Rasmussen encephalitis, encephalitis, neuroinflammation, autoimmune neurodegeneration
MeSH terms: Animals, Brain, Disease Models, Animal, Encephalitis, Female, Humans, Inflammation, Male, Mice, Inbred C57BL, Nervous System Diseases, Neurons, Phagocytes, Phagocytosis, Phosphorylation, Synapses, Microglia, CD8-Positive T-Lymphocytes, Chemokine CCL2, STAT1 Transcription Factor, Mice, Transcriptome

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Neurons under T Cell Attack Coordinate Phagocyte-Mediated Synaptic Stripping

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