Sensory neurons regulate stimulus-dependent humoral immunity in mouse models of bacterial infection and asthma

Diane Aguilar, Fengli Zhu, Antoine Millet, Nicolas Millet, Patrizia Germano, Joseph Pisegna, Omid Akbari, Taylor A. Doherty, Marc Swidergall and Nicholas Jendzjowsky ()
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Diane Aguilar: Harbor-UCLA Medical Center
Fengli Zhu: Harbor-UCLA Medical Center
Antoine Millet: Harbor-UCLA Medical Center
Nicolas Millet: The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center
Patrizia Germano: Veterans Affairs Greater Los Angeles Healthcare System
Joseph Pisegna: University of California
Omid Akbari: University of Southern California
Taylor A. Doherty: Veterans Affairs San Diego Healthcare System
Marc Swidergall: The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center
Nicholas Jendzjowsky: Harbor-UCLA Medical Center

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: Abstract Sensory neurons sense pathogenic infiltration to drive innate immune responses, but their role in humoral immunity is unclear. Here, using mouse models of Streptococcus pneumoniae infection and Alternaria alternata asthma, we show that sensory neurons are required for B cell recruitment and antibody production. In response to S. pneumoniae, sensory neuron depletion increases bacterial burden and reduces B cell numbers, IgG release, and neutrophil stimulation. Meanwhile, during A. alternata-induced airway inflammation, sensory neuron depletion decreases B cell population sizes, IgE levels, and asthmatic characteristics. Mechanistically, during bacterial infection, sensory neurons preferentially release vasoactive intestinal polypeptide (VIP). In response to asthma, sensory neurons release substance P. Administration of VIP into sensory neuron-depleted mice suppresses bacterial burden, while VIPR1 deficiency increases infection. Similarly, exogenous substance P delivery aggravates asthma in sensory neuron-depleted mice, while substance P deficiency ameliorates asthma. Our data, thus demonstrate that sensory neurons release select neuropeptides which target B cells dependent on the immunogen.

Date: 2024
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DOI: 10.1038/s41467-024-53269-3

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