Protective effect of TCR-mediated MAIT cell activation during experimental autoimmune encephalomyelitis.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
28 Oct 2024
Historique:
received: 08 07 2023
accepted: 18 10 2024
medline: 29 10 2024
pubmed: 29 10 2024
entrez: 29 10 2024
Statut: epublish

Résumé

Mucosal-associated invariant T (MAIT) cells express semi-invariant T cell receptors (TCR) for recognizing bacterial and yeast antigens derived from riboflavin metabolites presented on the non-polymorphic MHC class I-related protein 1 (MR1). Neuroinflammation in multiple sclerosis (MS) is likely initiated by autoreactive T cells and perpetuated by infiltration of additional immune cells, but the precise role of MAIT cells in MS pathogenesis remains unknown. Here, we use experimental autoimmune encephalomyelitis (EAE), a mouse model of MS, and find an accumulation of MAIT cells in the inflamed central nervous system (CNS) enriched for MAIT17 (RORγt

Identifiants

pubmed: 39468055
doi: 10.1038/s41467-024-53657-9
pii: 10.1038/s41467-024-53657-9
doi:

Substances chimiques

Receptors, Antigen, T-Cell 0
Histocompatibility Antigens Class I 0
Minor Histocompatibility Antigens 0
Cytokines 0
5-(2-oxopropylideneamino)-6-d-ribitylaminouracil 0
Ribitol 488-81-3
Nuclear Receptor Subfamily 1, Group F, Member 3 0
Uracil 56HH86ZVCT

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

9287

Subventions

Organisme : Bundesministerium für Bildung und Forschung (Federal Ministry of Education and Research)
ID : 01GI1605C
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Grant No. 470154978; WI 5322/2-1

Informations de copyright

© 2024. The Author(s).

Références

Woo, M. S., Engler, J. B. & Friese, M. A. The neuropathology of multiple sclerosis. Nat. Rev. Neurosci. https://doi.org/10.1038/s41583-024-00823-z (2024).
Attfield, K. E., Jensen, L. T., Kaufmann, M., Friese, M. A. & Fugger, L. The immunology of multiple sclerosis. Nat. Rev. Immunol. 22, 734–750 (2022).
pubmed: 35508809 doi: 10.1038/s41577-022-00718-z
Simmons, S. B., Pierson, E. R., Lee, S. Y. & Goverman, J. M. Modeling the heterogeneity of multiple sclerosis in animals. Trends Immunol. 34, 410–422 (2013).
pubmed: 23707039 pmcid: 3752929 doi: 10.1016/j.it.2013.04.006
Lee, Y. et al. Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 13, 991–999 (2012).
pubmed: 22961052 pmcid: 3459594 doi: 10.1038/ni.2416
Pierson, E., Simmons, S. B., Castelli, L. & Goverman, J. M. Mechanisms regulating regional localization of inflammation during CNS autoimmunity. Immunol. Rev. 248, 205–215 (2012).
pubmed: 22725963 pmcid: 3678350 doi: 10.1111/j.1600-065X.2012.01126.x
Tilloy, F. et al. An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J. Exp. Med 189, 1907–1921 (1999).
pubmed: 10377186 pmcid: 2192962 doi: 10.1084/jem.189.12.1907
Treiner, E. et al. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422, 164–169 (2003).
pubmed: 12634786 doi: 10.1038/nature01433
Kjer-Nielsen, L. et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491, 717–723 (2012).
pubmed: 23051753 doi: 10.1038/nature11605
Corbett, A. J. et al. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 509, 361–365 (2014).
pubmed: 24695216 doi: 10.1038/nature13160
Ito, E. et al. Sulfated bile acid is a host-derived ligand for MAIT cells. Sci. Immunol. 9, eade6924 (2024).
pubmed: 38277465 pmcid: 11147531 doi: 10.1126/sciimmunol.ade6924
Ussher, J. E. et al. CD161 + + CD8 + T cells, including the MAIT cell subset, are specifically activated by IL-12 + IL-18 in a TCR-independent manner. Eur. J. Immunol. 44, 195–203 (2014).
pubmed: 24019201 doi: 10.1002/eji.201343509
Le Bourhis, L. et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 11, 701–708 (2010).
pubmed: 20581831 doi: 10.1038/ni.1890
Chen, Z. et al. Mucosal-associated invariant T-cell activation and accumulation after in vivo infection depends on microbial riboflavin synthesis and co-stimulatory signals. Mucosal Immunol. 10, 58–68 (2017).
pubmed: 27143301 doi: 10.1038/mi.2016.39
van Wilgenburg, B. et al. MAIT cells are activated during human viral infections. Nat. Commun. 7, 11653 (2016).
pubmed: 27337592 pmcid: 4931007 doi: 10.1038/ncomms11653
van Wilgenburg, B. et al. MAIT cells contribute to protection against lethal influenza infection in vivo. Nat. Commun. 9, 4706 (2018).
pubmed: 30413689 pmcid: 6226485 doi: 10.1038/s41467-018-07207-9
Rahimpour, A. et al. Identification of phenotypically and functionally heterogeneous mouse mucosal-associated invariant T cells using MR1 tetramers. J. Exp. Med. 212, 1095–1108 (2015).
pubmed: 26101265 pmcid: 4493408 doi: 10.1084/jem.20142110
Dusseaux, M. et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17–secreting T cells. Blood 117, 1250–1259 (2011).
pubmed: 21084709 doi: 10.1182/blood-2010-08-303339
Rouxel, O. et al. Cytotoxic and regulatory roles of mucosal-associated invariant T cells in type 1 diabetes. Nat. Immunol. 18, 1321–1331 (2017).
pubmed: 28991267 pmcid: 6025738 doi: 10.1038/ni.3854
Constantinides, M. G. et al. MAIT cells are imprinted by the microbiota in early life and promote tissue repair. Science 366, eaax6624 (2019).
Cui, Y. et al. Mucosal-associated invariant T cell–rich congenic mouse strain allows functional evaluation. J. Clin. Investig. 125, 4171–4185 (2015).
pubmed: 26524590 pmcid: 4639991 doi: 10.1172/JCI82424
Lamichhane, R. et al. TCR- or Cytokine-Activated CD8+ Mucosal-Associated Invariant T Cells Are Rapid Polyfunctional Effectors That Can Coordinate Immune Responses. Cell Rep. 28, 3061–3076.e5 (2019).
pubmed: 31533031 doi: 10.1016/j.celrep.2019.08.054
Leng, T. et al. TCR and Inflammatory Signals Tune Human MAIT Cells to Exert Specific Tissue Repair and Effector Functions. Cell Rep. 28, 3077–3091.e5 (2019).
pubmed: 31533032 pmcid: 6899450 doi: 10.1016/j.celrep.2019.08.050
Hinks, T. S. C. et al. Activation and In Vivo Evolution of the MAIT Cell Transcriptome in Mice and Humans Reveals Tissue Repair Functionality. Cell Rep. 28, 3249–3262.e5 (2019).
pubmed: 31533045 pmcid: 6859474 doi: 10.1016/j.celrep.2019.07.039
Leeansyah, E. et al. Arming of MAIT Cell Cytolytic Antimicrobial Activity Is Induced by IL-7 and Defective in HIV-1 Infection. PLoS Pathog. 11, e1005072 (2015).
pubmed: 26295709 pmcid: 4546682 doi: 10.1371/journal.ppat.1005072
Willing, A., Jäger, J., Reinhardt, S., Kursawe, N. & Friese, M. A. Production of IL-17 by MAIT Cells Is Increased in Multiple Sclerosis and Is Associated with IL-7 Receptor Expression. J. Immunol. 200, 974–982 (2018).
pubmed: 29298833 doi: 10.4049/jimmunol.1701213
Miyazaki, Y., Miyake, S., Chiba, A., Lantz, O. & Yamamura, T. Mucosal-associated invariant T cells regulate Th1 response in multiple sclerosis. Int Immunol. 23, 529–535 (2011).
pubmed: 21712423 doi: 10.1093/intimm/dxr047
Annibali, V. et al. CD161(high)CD8 + T cells bear pathogenetic potential in multiple sclerosis. Brain 134, 542–554 (2011).
pubmed: 21216829 doi: 10.1093/brain/awq354
Salou, M. et al. Neuropathologic, phenotypic and functional analyses of Mucosal Associated Invariant T cells in Multiple Sclerosis. Clin. Immunol. 166–167, 1–11 (2016).
pubmed: 27050759 doi: 10.1016/j.clim.2016.03.014
Illés, Z., Shimamura, M., Newcombe, J., Oka, N. & Yamamura, T. Accumulation of Valpha7.2-Jalpha33 invariant T cells in human autoimmune inflammatory lesions in the nervous system. Int Immunol. 16, 223–230 (2004).
pubmed: 14734607 doi: 10.1093/intimm/dxh018
Willing, A. et al. CD8
pubmed: 25043505 doi: 10.1002/eji.201344160
Held, K. et al. αβ T-cell receptors from multiple sclerosis brain lesions show MAIT cell-related features. Neurol.(R.) Neuroimmunol. neuroinflammation 2, e107 (2015).
doi: 10.1212/NXI.0000000000000107
Croxford, J. L., Miyake, S., Huang, Y.-Y., Shimamura, M. & Yamamura, T. Invariant V(alpha)19i T cells regulate autoimmune inflammation. Nat. Immunol. 7, 987–994 (2006).
pubmed: 16878136 doi: 10.1038/ni1370
Smith, A. D. et al. Microbiota of MR1 deficient mice confer resistance against Clostridium difficile infection. PLoS One 14, e0223025 (2019).
pubmed: 31560732 pmcid: 6764671 doi: 10.1371/journal.pone.0223025
Koay, H.-F. et al. A three-stage intrathymic development pathway for the mucosal-associated invariant T cell lineage. Nat. Immunol. 17, 1300–1311 (2016).
pubmed: 27668799 doi: 10.1038/ni.3565
Wang, H. et al. IL-23 costimulates antigen-specific MAIT cell activation and enables vaccination against bacterial infection. Sci. Immunol. 4, eaaw0402 (2019).
Linehan, J. L. et al. Non-classical Immunity Controls Microbiota Impact on Skin Immunity and Tissue Repair. Cell 172, 784–796.e18 (2018).
pubmed: 29358051 pmcid: 6034182 doi: 10.1016/j.cell.2017.12.033
Yanai, H. et al. Tissue repair genes: the TiRe database and its implication for skin wound healing. Oncotarget 7, 21145–21155 (2016).
pubmed: 27049721 pmcid: 5008274 doi: 10.18632/oncotarget.8501
Wagner, C. A., Roqué, P. J. & Goverman, J. M. Pathogenic T cell cytokines in multiple sclerosis. J. Exp. Med. 217, e20190460 (2020).
Bettelli, E., Oukka, M. & Kuchroo, V. K. T(H)−17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8, 345–350 (2007).
pubmed: 17375096 doi: 10.1038/ni0407-345
Eken, A. et al. Temporal overexpression of IL-22 and Reg3γ differentially impacts the severity of experimental autoimmune encephalomyelitis. Immunology 164, 73–89 (2021).
pubmed: 33876425 pmcid: 8358722 doi: 10.1111/imm.13340
Ito, M. et al. Brain regulatory T cells suppress astrogliosis and potentiate neurological recovery. Nature 565, 246–250 (2019).
pubmed: 30602786 doi: 10.1038/s41586-018-0824-5
Wheeler, M. A. et al. Droplet-based forward genetic screening of astrocyte–microglia cross-talk. Science (1979) 379, 1023–1030 (2023).
Salou, M. & Lantz, O. A TCR-Dependent Tissue Repair Potential of MAIT Cells. Trends Immunol. 40, 975–977 (2019).
pubmed: 31623980 doi: 10.1016/j.it.2019.09.001
Osborne, B. A. et al. Identification of genes induced during apoptosis in T lymphocytes. Immunol. Rev. 142, 301–320 (1994).
pubmed: 7698798 doi: 10.1111/j.1600-065X.1994.tb00894.x
Moran, A. E. et al. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med 208, 1279–1289 (2011).
pubmed: 21606508 pmcid: 3173240 doi: 10.1084/jem.20110308
Lange, J. et al. The Chemical Synthesis, Stability, and Activity of MAIT Cell Prodrug Agonists That Access MR1 in Recycling Endosomes. ACS Chem. Biol. 15, 437–445 (2020).
pubmed: 31909966 doi: 10.1021/acschembio.9b00902
Yamana, S. et al. Mucosal-associated invariant T cells have therapeutic potential against ocular autoimmunity. Mucosal Immunol. 15, 351–361 (2022).
pubmed: 34775490 doi: 10.1038/s41385-021-00469-5
Felderhoff-Mueser, U., Schmidt, O. I., Oberholzer, A., Bührer, C. & Stahel, P. F. IL-18: a key player in neuroinflammation and neurodegeneration? Trends Neurosci. 28, 487–493 (2005).
pubmed: 16023742 doi: 10.1016/j.tins.2005.06.008
Nicoletti, F. et al. Increased serum levels of interleukin-18 in patients with multiple sclerosis. Neurology 57, 342–344 (2001).
pubmed: 11468327 doi: 10.1212/WNL.57.2.342
Elkjaer, M. L. et al. Hypothesis of a potential BrainBiota and its relation to CNS autoimmune inflammation. Front Immunol. 13, 1043579 (2022).
pubmed: 36532064 pmcid: 9756883 doi: 10.3389/fimmu.2022.1043579
Patel, O. et al. Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat. Commun. 4, 2142 (2013).
pubmed: 23846752 doi: 10.1038/ncomms3142
Crowther, M. D. et al. Genome-wide CRISPR-Cas9 screening reveals ubiquitous T cell cancer targeting via the monomorphic MHC class I-related protein MR1. Nat. Immunol. 21, 178–185 (2020).
pubmed: 31959982 pmcid: 6983325 doi: 10.1038/s41590-019-0578-8
Lepore, M. et al. Functionally diverse human T cells recognize non-microbial antigens presented by MR1. Elife 6, e24476 (2017).
Legoux, F. et al. Microbial metabolites control the thymic development of mucosal-associated invariant T cells. Science 366, 494–499 (2019).
pubmed: 31467190 doi: 10.1126/science.aaw2719
Salou, M., Legoux, F. & Lantz, O. MAIT cell development in mice and humans. Mol. Immunol. 130, 31–36 (2021).
pubmed: 33352411 doi: 10.1016/j.molimm.2020.12.003
Wang, H. et al. The balance of interleukin-12 and interleukin-23 determines the bias of MAIT1 versus MAIT17 responses during bacterial infection. Immunol. Cell Biol. 100, 547–561 (2022).
pubmed: 35514192 pmcid: 9539875 doi: 10.1111/imcb.12556
Mondal, S. et al. IL-12 p40 monomer is different from other IL-12 family members to selectively inhibit IL-12Rβ1 internalization and suppress EAE. Proc. Natl Acad. Sci. USA 117, 21557–21567 (2020).
pubmed: 32817415 pmcid: 7474649 doi: 10.1073/pnas.2000653117
Li, Y. et al. Increased IL-23p19 expression in multiple sclerosis lesions and its induction in microglia. Brain 130, 490–501 (2007).
pubmed: 17003070 doi: 10.1093/brain/awl273
Yan, M., Hu, Y., Yao, M., Bao, S. & Fang, Y. GM-CSF ameliorates microvascular barrier integrity via pericyte-derived Ang-1 in wound healing. Wound Repair Regen. 25, 933–943 (2017).
pubmed: 29328541 doi: 10.1111/wrr.12608
Kinugasa, T., Sakaguchi, T., Gu, X. & Reinecker, H. C. Claudins regulate the intestinal barrier in response to immune mediators. Gastroenterology 118, 1001–1011 (2000).
pubmed: 10833473 doi: 10.1016/S0016-5085(00)70351-9
Simmons, S. B., Liggitt, D. & Goverman, J. M. Cytokine-regulated neutrophil recruitment is required for brain but not spinal cord inflammation during experimental autoimmune encephalomyelitis. J. Immunol. 193, 555–563 (2014).
pubmed: 24913979 doi: 10.4049/jimmunol.1400807
Peters, A. et al. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity 35, 986–996 (2011).
pubmed: 22177922 pmcid: 3422678 doi: 10.1016/j.immuni.2011.10.015
Codarri, L. et al. RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 12, 560–567 (2011).
pubmed: 21516112 doi: 10.1038/ni.2027
Ponomarev, E. D. et al. GM-CSF production by autoreactive T cells is required for the activation of microglial cells and the onset of experimental autoimmune encephalomyelitis. J. Immunol. 178, 39–48 (2007).
pubmed: 17182538 doi: 10.4049/jimmunol.178.1.39
Croxford, A. L. et al. The Cytokine GM-CSF Drives the Inflammatory Signature of CCR2+ Monocytes and Licenses Autoimmunity. Immunity 43, 502–514 (2015).
pubmed: 26341401 doi: 10.1016/j.immuni.2015.08.010
Sonnenberg, G. F., Fouser, L. A. & Artis, D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 12, 383–390 (2011).
pubmed: 21502992 doi: 10.1038/ni.2025
du Halgouet, A. et al. Role of MR1-driven signals and amphiregulin on the recruitment and repair function of MAIT cells during skin wound healing. Immunity 56, 78–92.e6 (2023).
pubmed: 36630919 pmcid: 9839364 doi: 10.1016/j.immuni.2022.12.004
Luo, J., Ho, P., Steinman, L. & Wyss-Coray, T. Bioluminescence in vivo imaging of autoimmune encephalomyelitis predicts disease. J. Neuroinflammation 5, 6 (2008).
pubmed: 18237444 pmcid: 2267451 doi: 10.1186/1742-2094-5-6
Zhang, Y. et al. Mucosal-associated invariant T cells restrict reactive oxidative damage and preserve meningeal barrier integrity and cognitive function. Nat. Immunol. 23, 1714–1725 (2022).
pubmed: 36411380 pmcid: 10202031 doi: 10.1038/s41590-022-01349-1
Tang, W., Zhu, H., Feng, Y., Guo, R. & Wan, D. The Impact of Gut Microbiota Disorders on the Blood-Brain Barrier. Infect. Drug Resist 13, 3351–3363 (2020).
pubmed: 33061482 pmcid: 7532923 doi: 10.2147/IDR.S254403
Provine, N. M. & Klenerman, P. MAIT Cells in Health and Disease. Annu Rev. Immunol. 38, 203–228 (2020).
pubmed: 31986071 doi: 10.1146/annurev-immunol-080719-015428
Lantz, O. & Legoux, F. MAIT cells: an historical and evolutionary perspective. Immunol. Cell Biol. 96, 564–572 (2018).
pubmed: 29363173 doi: 10.1111/imcb.1034
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886 doi: 10.1093/bioinformatics/bts635
Wu, T. et al. clusterProfiler 4.0: A universal enrichment tool for interpreting omics data. Innovation 2, 100141 (2021).
pubmed: 34557778 pmcid: 8454663
Aibar, S. et al. SCENIC: single-cell regulatory network inference and clustering. Nat. Methods 14, 1083–1086 (2017).
pubmed: 28991892 pmcid: 5937676 doi: 10.1038/nmeth.4463

Auteurs

Mark Walkenhorst (M)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Jana K Sonner (JK)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Nina Meurs (N)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Jan Broder Engler (JB)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Simone Bauer (S)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Ingo Winschel (I)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Marcel S Woo (MS)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Lukas Raich (L)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Iris Winkler (I)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Vanessa Vieira (V)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Lisa Unger (L)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Gabriela Salinas (G)

NGS-Integrative Genomics Core Unit, Institute of Pathology, University Medical Center Göttingen, Göttingen, Germany.

Olivier Lantz (O)

Institut National de la Santé et de la Recherche Médicale U932, PSL University, Institut Curie, Paris, France.

Manuel A Friese (MA)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany. manuel.friese@zmnh.uni-hamburg.de.

Anne Willing (A)

Institute of Neuroimmunology and Multiple Sclerosis, University Medical Center Hamburg-Eppendorf, Hamburg, Germany. anne.willing@zmnh.uni-hamburg.de.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH