Nociceptor sensory neurons suppress neutrophil and γδ T cell responses in bacterial lung infections and lethal pneumonia

Nociceptor sensory neurons suppress innate immunity during bacterial lung infection. Lung-innervating nociceptor sensory neurons detect noxious or harmful stimuli and consequently protect organisms by mediating coughing, pain, and bronchoconstriction. However, the role of sensory neurons in pulmonar...

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Published inNature medicine Vol. 24; no. 4; pp. 417 - 426
Main Authors Baral, Pankaj, Umans, Benjamin D, Li, Lu, Wallrapp, Antonia, Bist, Meghna, Kirschbaum, Talia, Wei, Yibing, Zhou, Yan, Kuchroo, Vijay K, Burkett, Patrick R, Yipp, Bryan G, Liberles, Stephen D, Chiu, Isaac M
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.05.2018
Nature Publishing Group
Subjects
13/21
13/51
14/63
14/69
631/250/255
631/250/371
631/326/41
631/378/371
64/60
96/106
96/31
Ablation
Biomedicine
Body temperature
Bronchoconstriction
Bronchopulmonary infection
Calcitonin
Calcitonin gene-related peptide
Cancer Research
Capsaicin receptors
Cell survival
Critical care
Defense
Drug dosages
Ganglia
Heat
Hospitals
Immunity (Disease)
Immunosuppression
Infectious Diseases
Innate immunity
Leukocytes (neutrophilic)
Lungs
Lymphocytes
Lymphocytes T
Medicine
Metabolic Diseases
Molecular Medicine
Neurons
Neurosciences
Neutrophils
Nociceptors
Nosocomial infections
Pain perception
Pathogens
Pneumonia
Sensory neurons
Staphylococcus infections
Streptococcus infections
Toxins
Vagus nerve
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Abstract Nociceptor sensory neurons suppress innate immunity during bacterial lung infection. Lung-innervating nociceptor sensory neurons detect noxious or harmful stimuli and consequently protect organisms by mediating coughing, pain, and bronchoconstriction. However, the role of sensory neurons in pulmonary host defense is unclear. Here, we found that TRPV1 + nociceptors suppressed protective immunity against lethal Staphylococcus aureus pneumonia. Targeted TRPV1 + -neuron ablation increased survival, cytokine induction, and lung bacterial clearance. Nociceptors suppressed the recruitment and surveillance of neutrophils, and altered lung γδ T cell numbers, which are necessary for immunity. Vagal ganglia TRPV1 + afferents mediated immunosuppression through release of the neuropeptide calcitonin gene–related peptide (CGRP). Targeting neuroimmunological signaling may be an effective approach to treat lung infections and bacterial pneumonia.
AbstractList Nociceptor sensory neurons suppress innate immunity during bacterial lung infection. Lung-innervating nociceptor sensory neurons detect noxious or harmful stimuli and consequently protect organisms by mediating coughing, pain, and bronchoconstriction. However, the role of sensory neurons in pulmonary host defense is unclear. Here, we found that TRPV1 + nociceptors suppressed protective immunity against lethal Staphylococcus aureus pneumonia. Targeted TRPV1 + -neuron ablation increased survival, cytokine induction, and lung bacterial clearance. Nociceptors suppressed the recruitment and surveillance of neutrophils, and altered lung γδ T cell numbers, which are necessary for immunity. Vagal ganglia TRPV1 + afferents mediated immunosuppression through release of the neuropeptide calcitonin gene–related peptide (CGRP). Targeting neuroimmunological signaling may be an effective approach to treat lung infections and bacterial pneumonia.
Lung-innervating nociceptor sensory neurons detect noxious or harmful stimuli and consequently protect organisms by mediating coughing, pain, and bronchoconstriction. However, the role of sensory neurons in pulmonary host defense is unclear. Here, we found that TRPV1 nociceptors suppressed protective immunity against lethal Staphylococcus aureus pneumonia. Targeted TRPV1 -neuron ablation increased survival, cytokine induction, and lung bacterial clearance. Nociceptors suppressed the recruitment and surveillance of neutrophils, and altered lung γδ T cell numbers, which are necessary for immunity. Vagal ganglia TRPV1 afferents mediated immunosuppression through release of the neuropeptide calcitonin gene-related peptide (CGRP). Targeting neuroimmunological signaling may be an effective approach to treat lung infections and bacterial pneumonia.
Nociceptor sensory neurons suppress innate immunity during bacterial lung infection.Lung-innervating nociceptor sensory neurons detect noxious or harmful stimuli and consequently protect organisms by mediating coughing, pain, and bronchoconstriction. However, the role of sensory neurons in pulmonary host defense is unclear. Here, we found that TRPV1+ nociceptors suppressed protective immunity against lethal Staphylococcus aureus pneumonia. Targeted TRPV1+-neuron ablation increased survival, cytokine induction, and lung bacterial clearance. Nociceptors suppressed the recruitment and surveillance of neutrophils, and altered lung γδ T cell numbers, which are necessary for immunity. Vagal ganglia TRPV1+ afferents mediated immunosuppression through release of the neuropeptide calcitonin gene–related peptide (CGRP). Targeting neuroimmunological signaling may be an effective approach to treat lung infections and bacterial pneumonia.
Author Zhou, Yan
Baral, Pankaj
Yipp, Bryan G
Chiu, Isaac M
Wei, Yibing
Burkett, Patrick R
Kirschbaum, Talia
Wallrapp, Antonia
Bist, Meghna
Kuchroo, Vijay K
Li, Lu
Liberles, Stephen D
Umans, Benjamin D
Author_xml – sequence: 1
  givenname: Pankaj
  surname: Baral
  fullname: Baral, Pankaj
  organization: Department of Microbiology and Immunobiology, Division of Immunology, Harvard Medical School
– sequence: 2
  givenname: Benjamin D
  orcidid: 0000-0002-8209-9731
  surname: Umans
  fullname: Umans, Benjamin D
  organization: Department of Cell Biology, Harvard Medical School
– sequence: 3
  givenname: Lu
  surname: Li
  fullname: Li, Lu
  organization: Department of Critical Care, Cumming School of Medicine, University of Calgary
– sequence: 4
  givenname: Antonia
  surname: Wallrapp
  fullname: Wallrapp, Antonia
  organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women's Hospital
– sequence: 5
  givenname: Meghna
  surname: Bist
  fullname: Bist, Meghna
  organization: Department of Microbiology and Immunobiology, Division of Immunology, Harvard Medical School
– sequence: 6
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  surname: Kirschbaum
  fullname: Kirschbaum, Talia
  organization: Department of Microbiology and Immunobiology, Division of Immunology, Harvard Medical School
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  surname: Wei
  fullname: Wei, Yibing
  organization: Department of Microbiology and Immunobiology, Division of Immunology, Harvard Medical School
– sequence: 8
  givenname: Yan
  surname: Zhou
  fullname: Zhou, Yan
  organization: Department of Microbiology and Immunobiology, Division of Immunology, Harvard Medical School
– sequence: 9
  givenname: Vijay K
  surname: Kuchroo
  fullname: Kuchroo, Vijay K
  organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women's Hospital
– sequence: 10
  givenname: Patrick R
  surname: Burkett
  fullname: Burkett, Patrick R
  organization: Division of Pulmonary and Critical Care Medicine, Department of Medicine, Brigham and Women's Hospital
– sequence: 11
  givenname: Bryan G
  orcidid: 0000-0002-5887-9551
  surname: Yipp
  fullname: Yipp, Bryan G
  organization: Department of Critical Care, Cumming School of Medicine, University of Calgary
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  surname: Liberles
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  organization: Department of Cell Biology, Harvard Medical School
– sequence: 13
  givenname: Isaac M
  orcidid: 0000-0002-0723-4841
  surname: Chiu
  fullname: Chiu, Isaac M
  email: isaac_chiu@hms.harvard.edu
  organization: Department of Microbiology and Immunobiology, Division of Immunology, Harvard Medical School
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29505031$$D View this record in MEDLINE/PubMed
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10.1038/nature24029
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Copyright Springer Nature America, Inc. 2018
Copyright Nature Publishing Group Apr 2018
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Snippet Nociceptor sensory neurons suppress innate immunity during bacterial lung infection. Lung-innervating nociceptor sensory neurons detect noxious or harmful...
Lung-innervating nociceptor sensory neurons detect noxious or harmful stimuli and consequently protect organisms by mediating coughing, pain, and...
Nociceptor sensory neurons suppress innate immunity during bacterial lung infection.Lung-innervating nociceptor sensory neurons detect noxious or harmful...
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14/69
631/250/255
631/250/371
631/326/41
631/378/371
64/60
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96/31
Ablation
Biomedicine
Body temperature
Bronchoconstriction
Bronchopulmonary infection
Calcitonin
Calcitonin gene-related peptide
Cancer Research
Capsaicin receptors
Cell survival
Critical care
Defense
Drug dosages
Ganglia
Heat
Hospitals
Immunity (Disease)
Immunosuppression
Infectious Diseases
Innate immunity
Leukocytes (neutrophilic)
Lungs
Lymphocytes
Lymphocytes T
Medicine
Metabolic Diseases
Molecular Medicine
Neurons
Neurosciences
Neutrophils
Nociceptors
Nosocomial infections
Pain perception
Pathogens
Pneumonia
Sensory neurons
Staphylococcus infections
Streptococcus infections
Toxins
Vagus nerve
Title Nociceptor sensory neurons suppress neutrophil and γδ T cell responses in bacterial lung infections and lethal pneumonia
URI https://link.springer.com/article/10.1038/nm.4501
https://www.ncbi.nlm.nih.gov/pubmed/29505031
https://www.proquest.com/docview/3143148700
https://search.proquest.com/docview/2010841020
https://pubmed.ncbi.nlm.nih.gov/PMC6263165
Volume 24
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