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The impact of influenza pulmonary infection and inflammation on vagal bronchopulmonary sensory neurons

Authors: Verzele, Nathalie A. J.; Chua, Brendon Y.; Law, Charity W.; Zhang, Albert; Ritchie, Matthew E.; Wightman, Oliver; Edwards, Isaac N.; Hulme, Katina D.; Bloxham, Conor J.; Bielefeldt‐Ohmann, Helle; Trewella, Matthew W.; Moe, Aung Aung Kywe; Chew, Keng Yih; Mazzone, Stuart B.; Short, Kirsty R.; McGovern, Alice E.

Online: https://faseb.onlinelibrary.wiley.com/doi/abs/10.1096/fj.202001509R

Issue: FASEB J . 2021 Mar;35(3):e21320.


Influenza A virus (IAV) is rapidly detected in the airways by the immune system, with resident parenchymal cells and leukocytes orchestrating viral sensing and the induction of antiviral inflammatory responses. The airways are innervated by heterogeneous populations of vagal sensory neurons which also play an important role in pulmonary defense. How these neurons respond to IAV respiratory infection remains unclear. Here, we use a murine model to provide the first evidence that vagal sensory neurons undergo significant transcriptional changes following a respiratory IAV infection. RNA sequencing on vagal sensory ganglia showed that IAV infection induced the expression of many genes associated with an antiviral and pro-inflammatory response and this was accompanied by a significant increase in inflammatory cell recruitment into the vagal ganglia. Assessment of gene expression in single-vagal sensory neurons confirmed that IAV infection induced a neuronal inflammatory phenotype, which was most prominent in bronchopulmonary neurons, and also evident in some neurons innervating other organs. The altered transcriptome could be mimicked by intranasal treatment with cytokines and the lung homogenates of infected mice, in the absence of infectious virus. These data argue that IAV pulmonary infection and subsequent inflammation induces vagal sensory ganglia neuroinflammation and this may have important implications for IAV-induced morbidity.