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

Author

Listed:
  • Diane Aguilar

    (Harbor-UCLA Medical Center
    The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center)

  • Fengli Zhu

    (Harbor-UCLA Medical Center
    The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center)

  • Antoine Millet

    (Harbor-UCLA Medical Center
    The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center)

  • Nicolas Millet

    (The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center
    Harbor-UCLA Medical Center)

  • Patrizia Germano

    (Veterans Affairs Greater Los Angeles Healthcare System
    University of California
    David Geffen School of Medicine at UCLA)

  • Joseph Pisegna

    (University of California
    VA Greater Los Angeles Healthcare System and Department of Medicine
    Veterans Affairs Greater Los Angeles Healthcare System)

  • 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
    Harbor-UCLA Medical Center
    David Geffen School of Medicine)

  • Nicholas Jendzjowsky

    (Harbor-UCLA Medical Center
    The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center
    David Geffen School of Medicine)

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.

Suggested Citation

  • Diane Aguilar & Fengli Zhu & Antoine Millet & Nicolas Millet & Patrizia Germano & Joseph Pisegna & Omid Akbari & Taylor A. Doherty & Marc Swidergall & Nicholas Jendzjowsky, 2024. "Sensory neurons regulate stimulus-dependent humoral immunity in mouse models of bacterial infection and asthma," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53269-3
    DOI: 10.1038/s41467-024-53269-3
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    1. Isaac M. Chiu & Balthasar A. Heesters & Nader Ghasemlou & Christian A. Von Hehn & Fan Zhao & Johnathan Tran & Brian Wainger & Amanda Strominger & Sriya Muralidharan & Alexander R. Horswill & Juliane B, 2013. "Bacteria activate sensory neurons that modulate pain and inflammation," Nature, Nature, vol. 501(7465), pages 52-57, September.
    2. Kimbria J. Blake & Pankaj Baral & Tiphaine Voisin & Ashira Lubkin & Felipe Almeida Pinho-Ribeiro & Kelsey L. Adams & David P. Roberson & Yuxin C. Ma & Michael Otto & Clifford J. Woolf & Victor J. Torr, 2018. "Staphylococcus aureus produces pain through pore-forming toxins and neuronal TRPV1 that is silenced by QX-314," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    3. David Julius & Allan I. Basbaum, 2001. "Molecular mechanisms of nociception," Nature, Nature, vol. 413(6852), pages 203-210, September.
    4. Xu Zhang & Bo Lei & Yuan Yuan & Li Zhang & Lu Hu & Sen Jin & Bilin Kang & Xuebin Liao & Wenzhi Sun & Fuqiang Xu & Yi Zhong & Ji Hu & Hai Qi, 2020. "Brain control of humoral immune responses amenable to behavioural modulation," Nature, Nature, vol. 581(7807), pages 204-208, May.
    5. Vânia Cardoso & Julie Chesné & Hélder Ribeiro & Bethania García-Cassani & Tânia Carvalho & Tiffany Bouchery & Kathleen Shah & Nuno L. Barbosa-Morais & Nicola Harris & Henrique Veiga-Fernandes, 2017. "Neuronal regulation of type 2 innate lymphoid cells via neuromedin U," Nature, Nature, vol. 549(7671), pages 277-281, September.
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