Neuronal pSTAT1 hallmarks synaptic pathology in autoimmune encephalitis against intracellular antigens
Autoimmune encephalitis (AE) is an inflammatory syndrome of the central nervous system (CNS) triggered by aberrant immune responses against neuronal intracellular (IC-AE) or surface (NS-AE) autoantigens. The resulting neuronal alterations and clinical trajectories differ, with IC-AE often leading to...
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| Vydané v: | Acta neuropathologica Ročník 149; číslo 1; s. 35 |
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| Médium: | Journal Article |
| Jazyk: | English |
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Berlin/Heidelberg
Springer Berlin Heidelberg
25.04.2025
Springer Nature B.V |
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| ISSN: | 1432-0533, 0001-6322, 1432-0533 |
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| Abstract | Autoimmune encephalitis (AE) is an inflammatory syndrome of the central nervous system (CNS) triggered by aberrant immune responses against neuronal intracellular (IC-AE) or surface (NS-AE) autoantigens. The resulting neuronal alterations and clinical trajectories differ, with IC-AE often leading to fatal outcomes. Unfortunately, the scarce availability of tissue from AE cases has hampered systematic analyses that would allow an understanding of the pathogenesis underlying neuronal alterations in T cell-mediated AE syndromes. Here, we assembled a cohort comprising both NS-AE (n = 8) and IC-AE (n = 12) from multiple institutions to delineate key histopathological features that distinguish neuronal pathology between IC-AE and NS-AE. In contrast to NS-AE, IC-AE lesions present a prominent neuronal pSTAT1 signature, accompanied by a high proportion of brain-resident memory CD8 + T cells and neurodegenerative GPNMB + phagocytes which show synaptic engulfment with little C3-complement deposition. Our findings highlight distinct histopathological features of IC-AE compared to NS-AE, providing actionable biomarkers for diagnostics and treatment strategies. |
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| AbstractList | Autoimmune encephalitis (AE) is an inflammatory syndrome of the central nervous system (CNS) triggered by aberrant immune responses against neuronal intracellular (IC-AE) or surface (NS-AE) autoantigens. The resulting neuronal alterations and clinical trajectories differ, with IC-AE often leading to fatal outcomes. Unfortunately, the scarce availability of tissue from AE cases has hampered systematic analyses that would allow an understanding of the pathogenesis underlying neuronal alterations in T cell-mediated AE syndromes. Here, we assembled a cohort comprising both NS-AE (n = 8) and IC-AE (n = 12) from multiple institutions to delineate key histopathological features that distinguish neuronal pathology between IC-AE and NS-AE. In contrast to NS-AE, IC-AE lesions present a prominent neuronal pSTAT1 signature, accompanied by a high proportion of brain-resident memory CD8 + T cells and neurodegenerative GPNMB + phagocytes which show synaptic engulfment with little C3-complement deposition. Our findings highlight distinct histopathological features of IC-AE compared to NS-AE, providing actionable biomarkers for diagnostics and treatment strategies. Autoimmune encephalitis (AE) is an inflammatory syndrome of the central nervous system (CNS) triggered by aberrant immune responses against neuronal intracellular (IC-AE) or surface (NS-AE) autoantigens. The resulting neuronal alterations and clinical trajectories differ, with IC-AE often leading to fatal outcomes. Unfortunately, the scarce availability of tissue from AE cases has hampered systematic analyses that would allow an understanding of the pathogenesis underlying neuronal alterations in T cell-mediated AE syndromes. Here, we assembled a cohort comprising both NS-AE (n = 8) and IC-AE (n = 12) from multiple institutions to delineate key histopathological features that distinguish neuronal pathology between IC-AE and NS-AE. In contrast to NS-AE, IC-AE lesions present a prominent neuronal pSTAT1 signature, accompanied by a high proportion of brain-resident memory CD8 + T cells and neurodegenerative GPNMB + phagocytes which show synaptic engulfment with little C3-complement deposition. Our findings highlight distinct histopathological features of IC-AE compared to NS-AE, providing actionable biomarkers for diagnostics and treatment strategies.Autoimmune encephalitis (AE) is an inflammatory syndrome of the central nervous system (CNS) triggered by aberrant immune responses against neuronal intracellular (IC-AE) or surface (NS-AE) autoantigens. The resulting neuronal alterations and clinical trajectories differ, with IC-AE often leading to fatal outcomes. Unfortunately, the scarce availability of tissue from AE cases has hampered systematic analyses that would allow an understanding of the pathogenesis underlying neuronal alterations in T cell-mediated AE syndromes. Here, we assembled a cohort comprising both NS-AE (n = 8) and IC-AE (n = 12) from multiple institutions to delineate key histopathological features that distinguish neuronal pathology between IC-AE and NS-AE. In contrast to NS-AE, IC-AE lesions present a prominent neuronal pSTAT1 signature, accompanied by a high proportion of brain-resident memory CD8 + T cells and neurodegenerative GPNMB + phagocytes which show synaptic engulfment with little C3-complement deposition. Our findings highlight distinct histopathological features of IC-AE compared to NS-AE, providing actionable biomarkers for diagnostics and treatment strategies. |
| ArticleNumber | 35 |
| Author | Irani, Sarosh R. Vogrig, Alberto Meyronet, David Dickson, Dennis W. Höftberger, Romana Prinz, Marco de Leval, Laurence Endmayr, Verena Frank, Stephan Parkkinen, Laura Egervari, Kristof Draganski, Bogdan Vicino, Alex Di Liberto, Giovanni Ostertag, Karoline Hewer, Ekkehard Spatola, Marianna Vincenti, Ilena Honnorat, Jérôme Pröbstel, Anne-Katrin Piccinno, Margot Roemer, Shanu F. Kreutzfeldt, Mario Merkler, Doron Dubey, Divyanshu Rahimi, Jasmin Desestret, Virginie Wagner, Ingrid Brouland, Jean-Philippe Pittock, Sean J. Du Pasquier, Renaud |
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Institute (CRI) – sequence: 5 givenname: Margot surname: Piccinno fullname: Piccinno, Margot organization: Department of Pathology and Immunology, University of Geneva – sequence: 6 givenname: Ilena surname: Vincenti fullname: Vincenti, Ilena organization: Department of Pathology and Immunology, University of Geneva, Division of Clinical Pathology, Geneva University Hospital – sequence: 7 givenname: Ingrid surname: Wagner fullname: Wagner, Ingrid organization: Department of Pathology and Immunology, University of Geneva – sequence: 8 givenname: Mario surname: Kreutzfeldt fullname: Kreutzfeldt, Mario organization: Department of Pathology and Immunology, University of Geneva, Division of Clinical Pathology, Geneva University Hospital – sequence: 9 givenname: Verena surname: Endmayr fullname: Endmayr, Verena organization: Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Comprehensive Center for Clinical Neurosciences and Mental Health, 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Hospital and University Bonn, German Center for Neurodegenerative Diseases (DZNE) – sequence: 14 givenname: David surname: Meyronet fullname: Meyronet, David organization: Institute of Neuropathology, Hospices Civils de Lyon, Centre de Recherche en Cancérologie de Lyon, Inserm U1052, CNRS UMR5286, Université de Lyon, Université Claude Bernard Lyon 1 – sequence: 15 givenname: Stephan surname: Frank fullname: Frank, Stephan organization: Department of Neuropathology, Institute of Pathology, Basel University Hospital – sequence: 16 givenname: Marco surname: Prinz fullname: Prinz, Marco organization: Institute of Neuropathology, University of Freiburg, Signaling Research Centers BIOSS and CIBSS, University of Freiburg – sequence: 17 givenname: Ekkehard surname: Hewer fullname: Hewer, Ekkehard organization: Department of Laboratory Medicine and Pathology, Institute of Pathology, Lausanne University Hospital and University of Lausanne – sequence: 18 givenname: Jean-Philippe surname: Brouland fullname: Brouland, Jean-Philippe organization: Department of Laboratory Medicine and Pathology, Institute of Pathology, Lausanne University Hospital and University of Lausanne – sequence: 19 givenname: Laurence surname: de Leval fullname: de Leval, Laurence organization: Department of Laboratory Medicine and Pathology, Institute of Pathology, Lausanne University Hospital and University of Lausanne – sequence: 20 givenname: Laura surname: Parkkinen fullname: Parkkinen, Laura organization: Nuffield Department of Clinical Neurosciences, University of Oxford – sequence: 21 givenname: Bogdan surname: Draganski fullname: Draganski, Bogdan organization: Universitätsklinik für Neurologie, Inselspital, University of Bern, University Institute for Diagnostic and Interventional Neuroradiology, Inselspital, University of Bern – sequence: 22 givenname: Virginie surname: Desestret fullname: Desestret, Virginie organization: French Reference Center On Paraneoplastic Neurological Syndromes and 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fullname: Höftberger, Romana organization: Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Comprehensive Center for Clinical Neurosciences and Mental Health, Medical University of Vienna – sequence: 28 givenname: Sarosh R. surname: Irani fullname: Irani, Sarosh R. organization: Department of Neuroscience, Mayo Clinic, Department of Neurology, Mayo Clinic, Autoimmune Neurology Group, West Wing, Level 3, John Radcliffe Hospital, University of Oxford – sequence: 29 givenname: Jérôme surname: Honnorat fullname: Honnorat, Jérôme organization: French Reference Center On Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, MeLiS – UCBL – CNRS UMR 5284 – INSERM U1314, Université de Lyon, Université Claude Bernard Lyon 1 – sequence: 30 givenname: Renaud surname: Du Pasquier fullname: Du Pasquier, Renaud organization: Department of Clinical Neurosciences, Neurology Service, Lausanne University Hospital and University of Lausanne – sequence: 31 givenname: Doron surname: Merkler fullname: Merkler, Doron email: doron.merkler@unige.ch organization: Department of Pathology and Immunology, University of Geneva, Division of Clinical Pathology, Geneva University Hospital |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40278930$$D View this record in MEDLINE/PubMed |
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| Keywords | Phagocytes Neuroinflammation Resident memory T cells Neurodegeneration Synapses |
| Language | English |
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| SubjectTerms | Adult Aged Antibodies Antigens Autoantigens Autoantigens - immunology Autoimmune diseases Biomarkers Brain - immunology Brain - pathology CD8 antigen CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - pathology Central nervous system Complement component C3 Disease Encephalitis Encephalitis - immunology Encephalitis - metabolism Encephalitis - pathology Female Females Genotype & phenotype Hashimoto Disease - immunology Hashimoto Disease - pathology Humans Immunological memory Intracellular Lymphocytes Lymphocytes T Male Males Medical prognosis Medicine Medicine & Public Health Memory Memory cells Middle Aged Nervous system Neurodegeneration Neurons - immunology Neurons - metabolism Neurons - pathology Neurosciences Original Paper Pathogenesis Pathology Phagocytes Proteins STAT1 Transcription Factor - metabolism Synapses - immunology Synapses - metabolism Synapses - pathology Young Adult |
| Title | Neuronal pSTAT1 hallmarks synaptic pathology in autoimmune encephalitis against intracellular antigens |
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