The production of the chemokine CCL2 by corneal sensory neurons initiates anti-viral immunity at the cornea and trigeminal ganglion

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The cornea is an epithelial tissue densely innervated by sensory neurons but devoid of autonomic innervation, lymphatics, and vasculature. The simplicity of the cellular composition suggests that corneal afferents participate in tissue homeostasis by regulating immune cells. Transcriptomic analysis of retrogradely labeled corneal afferents in the trigeminal ganglion (TG) found that they express many immune-related genes. Optogenetic activation of corneal afferents increased neutrophils and monocytes in both the cornea and TG, as well as inducing phenotypic changes in natural killer (NK) cells. Unsupervised pathway analysis indicated neuronally expressed Ccl2 as a modulator of immune cell responses. Selective deletion of neuronal Ccl2 decreased the number of myeloid cells in the cornea and TG in response to herpes simplex virus (HSV) infection, resulting in compromised viral clearance during primary infection. These experiments demonstrate that corneal afferent activation is sufficient to trigger inflammatory responses that can assist the host in initiating anti-viral immunity.

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