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KIR3DL1 and Tox identify clonally expanded encephalitogenic neuron-specific CD8+ T cells in autoimmune encephalitis

Perriot, S.; Jones, S.; Genolet, R.; Mathias, A.; Lindsay, H.; Bobisse, S.; Di Liberto, G.; Canales, M.; Queiroz, L.; Sauvage, C.; Wagner, I.; Oberholster, L.; Gimenez, M.; Begarie, D.; Theaudin, M.; Pot, C.; Merkler, D.; Gottardo, R.; Harari, A.; Du Pasquier, R.

2024-03-29 immunology
10.1101/2024.03.25.586688 bioRxiv
Show abstract

Autoreactive CD8+ T cells are the principal suspects in autoimmune encephalitis (AIE) with antibodies targeting intracellular neuronal antigens So far, the search for neuron-autoreactive CD8+ T cells has been focused on a few autoantigens and did not yield convincing results. Here, we leveraged natural antigen presentation by hiPSC-derived neurons to look at the global autoreactive CD8+ T cell response, independently of pre-conceived hypothesis of the autoantigens involved in the disease. This unbiased approach allowed for the identification of rare polyclonal neuron-reactive CD8+ T cells in healthy donors, and contrastingly, expanded clonotypes in two patients with anti-Ri AIE. Detailed ex vivo phenotypic characterization of these clonotypes revealed a specific transcriptional program suggestive of a pathogenic potential. In particular, this subset can be identified by the expression of KIR3DL1 and TOX. Strikingly, we could also demonstrate that CD8+ T cells found in the brain of an anti-Ri AIE patient display a similar phenotype associated with cytotoxicity and encephalitogenic features.

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