IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31074-0.html
   My bibliography  Save this article

Airway Prevotella promote TLR2-dependent neutrophil activation and rapid clearance of Streptococcus pneumoniae from the lung

Author

Listed:
  • Kadi J. Horn

    (University of Colorado School of Medicine, Department of Otolaryngology)

  • Melissa A. Schopper

    (University of Colorado School of Medicine, Department of Otolaryngology)

  • Zoe G. Drigot

    (University of Colorado School of Medicine, Department of Otolaryngology
    University of Colorado Boulder, College of Arts and Sciences)

  • Sarah E. Clark

    (University of Colorado School of Medicine, Department of Otolaryngology)

Abstract

This study investigates how specific members of the lung microbiome influence the early immune response to infection. Prevotella species are a major component of the endogenous airway microbiota. Increased abundance of Prevotella melaninogenica correlates with reduced infection with the bacterial pathogen Streptococcus pneumoniae, indicating a potentially beneficial role. Here, we show that P. melaninogenica enhances protection against S. pneumoniae, resulting in rapid pathogen clearance from the lung and improved survival in a mouse lung co-infection model. This response requires recognition of P. melaninogenica lipoproteins by toll-like receptor (TLR)2, the induction of TNFα, and neutrophils, as the loss of any of these factors abrogates Prevotella-induced protection. Improved clearance of S. pneumoniae is associated with increased serine protease-mediated killing by lung neutrophils and restraint of P. melaninogenica-induced inflammation by IL-10 in co-infected mice. Together, these findings highlight innate immune priming by airway Prevotella as an important protective feature in the respiratory tract.

Suggested Citation

  • Kadi J. Horn & Melissa A. Schopper & Zoe G. Drigot & Sarah E. Clark, 2022. "Airway Prevotella promote TLR2-dependent neutrophil activation and rapid clearance of Streptococcus pneumoniae from the lung," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31074-0
    DOI: 10.1038/s41467-022-31074-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31074-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-31074-0?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Sudip Das & Eric Bernasconi & Angela Koutsokera & Daniel-Adrien Wurlod & Vishwachi Tripathi & Germán Bonilla-Rosso & John-David Aubert & Marie-France Derkenne & Louis Mercier & Céline Pattaroni & Alex, 2021. "A prevalent and culturable microbiota links ecological balance to clinical stability of the human lung after transplantation," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    2. Rebecca L. Brown & Richard P. Sequeira & Thomas B. Clarke, 2017. "The microbiota protects against respiratory infection via GM-CSF signaling," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    3. Beom Seok Park & Dong Hyun Song & Ho Min Kim & Byong-Seok Choi & Hayyoung Lee & Jie-Oh Lee, 2009. "The structural basis of lipopolysaccharide recognition by the TLR4–MD-2 complex," Nature, Nature, vol. 458(7242), pages 1191-1195, April.
    4. Evelyn Balsells & Laurence Guillot & Harish Nair & Moe H Kyaw, 2017. "Serotype distribution of Streptococcus pneumoniae causing invasive disease in children in the post-PCV era: A systematic review and meta-analysis," PLOS ONE, Public Library of Science, vol. 12(5), pages 1-20, May.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Peter Francis Raguindin, 2020. "The changing epidemiology of pneumococcal diseases: new challenges after widespread routine immunization," International Journal of Public Health, Springer;Swiss School of Public Health (SSPH+), vol. 65(6), pages 709-710, July.
    2. Martin Boström & Erik Larsson, 2022. "Somatic mutation distribution across tumour cohorts provides a signal for positive selection in cancer," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    3. Carsten Eriksen & Janne Marie Moll & Pernille Neve Myers & Ana Rosa Almeida Pinto & Niels Banhos Danneskiold-Samsøe & Rasmus Ibsen Dehli & Lisbeth Buus Rosholm & Marlene Danner Dalgaard & John Penders, 2023. "IgG and IgM cooperate in coating of intestinal bacteria in IgA deficiency," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    4. Anastasiia Petenkova & Shelby A. Auger & Jeffrey Lamb & Daisy Quellier & Cody Carter & On Tak To & Jelena Milosevic & Rana Barghout & Abirami Kugadas & Xiaoxiao Lu & Jennifer Geddes-McAlister & Raina , 2023. "Prenylcysteine oxidase 1 like protein is required for neutrophil bactericidal activities," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Peter Francis Raguindin, 0. "The changing epidemiology of pneumococcal diseases: new challenges after widespread routine immunization," International Journal of Public Health, Springer;Swiss School of Public Health (SSPH+), vol. 0, pages 1-2.
    6. Uri Obolski & Todd D. Swarthout & Akuzike Kalizang’oma & Thandie S. Mwalukomo & Jia Mun Chan & Caroline M. Weight & Comfort Brown & Rory Cave & Jen Cornick & Arox Wadson Kamng’ona & Jacquline Msefula , 2023. "The metabolic, virulence and antimicrobial resistance profiles of colonising Streptococcus pneumoniae shift after PCV13 introduction in urban Malawi," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. F. D. Kornilov & A. V. Shabalkina & Cong Lin & P. E. Volynsky & E. F. Kot & A. L. Kayushin & V. A. Lushpa & M. V. Goncharuk & A. S. Arseniev & S. A. Goncharuk & Xiaohui Wang & K. S. Mineev, 2023. "The architecture of transmembrane and cytoplasmic juxtamembrane regions of Toll-like receptors," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31074-0. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.