Meningeal γδ T cell-derived IL-17 controls synaptic plasticity and short-term memory
Open accessAbstract
The notion of "immune privilege" of the brain has been revised to accommodate its infiltration, at steady state, by immune cells that participate in normal neurophysiology. However, the immune mechanisms that regulate learning and memory remain poorly understood. Here, we show that noninflammatory interleukin-17 (IL-17) derived from a previously unknown fetal-derived meningeal-resident γδ T cell subset promotes cognition. When tested in classical spatial learning paradigms, mice lacking γδ T cells or IL-17 displayed deficient short-term memory while retaining long-term memory. The plasticity of glutamatergic synapses was reduced in the absence of IL-17, resulting in impaired long-term potentiation in the hippocampus. Conversely, IL-17 enhanced glial cell production of brain-derived neurotropic factor, whose exogenous provision rescued the synaptic and behavioral phenotypes of IL-17-deficient animals. Together, our work provides previously unknown clues on the mechanisms that regulate short-term versus long-term memory and on the evolutionary and functional link between the immune and nervous systems.
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Under pathological conditions, IL-17 can be secreted by several other cells in the CNS in addition to Th17 cells.
“This is largely because under pathological conditions, IL-17 can be secreted by several other cells in the CNS in addition to Th17 cells.”
From Chronic stress-induced depression requires the recruitment of peripheral Th17 cells into the brain (2022) · cites this paper as [70]
The Discussion (page unavailable) says that, during inflammation, IL-17 is produced by γδ T cells as well as recruited CD4+ T cells. This supports a source beyond Th17 cells, but the paper does not identify several other IL-17-producing CNS cell types. Its references to astrocytes and microglia describe cells that respond to IL-17, not cells that secrete it. (LLM, conf=0.85)
Experimental — accuracy not yet measuredMeningeal resident γδ17 T cells express RORγt and have been implicated in regulating anxiety-like behaviour and short-term memory via IL-17 signalling.
“Particularly, meningeal resident γδ17 T cells, which express RORγt as well, have been recently implicated in regulating anxiety-like behaviour and short-term memory via IL-17 signalling [70, 71].”
From Chronic stress-induced depression requires the recruitment of peripheral Th17 cells into the brain (2022) · cites this paper as [70]
The Results sections report that resident meningeal γδ17 T cells express RORγt and that IL-17 or γδ T-cell deficiency impairs short-term memory in mice. They do not support the anxiety-like behaviour part: the mice showed no particular signs of anxiety. No page numbers are available in our copy. (LLM, conf=0.89)
Experimental — accuracy not yet measuredFunctional immune cells can enter the CNS through the blood-brain barrier, choroid plexus, and lymphatic vessels and have been described beyond neuropathological conditions.
“However, the idea that the CNS is an immune privileged organ has been reconsidered, as the functional immune cells can enter the CNS through the BBB, the choroid plexus, and the lymphatic vessels and have been described beyond neuropathological conditions (26, 35–47).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [41]
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- Authors
- Ribeiro, M., Brigas, H. C., Temido-Ferreira, M., Pousinha, P. A., Regen, T., Santa, C., Coelho, J. E., Marques-Morgado, I., Valente, C. A., Omenetti, S., Stockinger, B., Waisman, A., Manadas, B., Lopes, L. V., Silva-Santos, B., & Ribot, J. C.
- Affiliations
- University of Lisbon (PT)
- Instituto de Medicina Molecular João Lobo Antunes, Faculdade de Medicina, Universidade de Lisboa, Lisboa, Portugal.
- Centre National de la Recherche Scientifique (FR)
- University Medical Center of the Johannes Gutenberg University Mainz (DE)
- Centro de Neurociências e Biologia Celular (PT)
- The Francis Crick Institute (GB)
- Corresponding author
- Ribot, Julie C.
- ORCID
- Venue
- Science Immunology
- Published
- 2019-10-11
- Volume
- 4
- Issue
- 40
- ISSN
- 2470-9468 (ISSN-L)
- PMC
- PMC6894940
- OpenAlex
- W2979366073
- Cited by
- 335
- References
- 71
- Citations by year
- 2026: 43 · 2025: 53 · 2024: 49 · 2023: 52 · 2022: 52 · 2021: 55 · 2020: 25 · 2019: 6
- FWCI
- 15.20
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science Immunology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- Wellcome Trust (FC001159, 100910)
- Francis Crick Institute (10159)
- Cancer Research UK (FC001159)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- γδ T cells, IL-17, meningeal immune cells, short-term memory, long-term memory, synaptic plasticity, long-term potentiation, hippocampus, brain-derived neurotrophic factor, glial cells, spatial learning, immune privilege, neuroimmunology
- MeSH terms
- Animals, Memory, Short-Term, Meninges, Mice, Inbred C57BL, Neuronal Plasticity, T-Lymphocytes, Mice, Knockout, Interleukin-17, Mice
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