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Early alveolar macrophage response and IL-1R-dependent T cell priming determine transmissibility of Mycobacterium tuberculosis strains

Author

Listed:
  • Arianne Lovey

    (Rutgers-New Jersey Medical School)

  • Sheetal Verma

    (Rutgers-New Jersey Medical School)

  • Vaishnavi Kaipilyawar

    (Rutgers-New Jersey Medical School)

  • Rodrigo Ribeiro-Rodrigues

    (Núcleo de Doenças Infecciosas, NDI/Universidade Federal do Espirito Santo-UFES)

  • Seema Husain

    (The Genomics Center, Rutgers—New Jersey Medical School)

  • Moises Palaci

    (Núcleo de Doenças Infecciosas, NDI/Universidade Federal do Espirito Santo-UFES)

  • Reynaldo Dietze

    (Núcleo de Doenças Infecciosas, NDI/Universidade Federal do Espirito Santo-UFES
    Global Health & Tropical Medicine—Instituto de Higiene e Medicina Tropical—Universidade Nova de Lisboa)

  • Shuyi Ma

    (Seattle Children’s Research Institute
    University of Washington
    University of Washington
    University of Washington)

  • Robert D. Morrison

    (National Institute of Allergy and Infectious Diseases, NIH)

  • David. R. Sherman

    (University of Washington)

  • Jerrold J. Ellner

    (Rutgers-New Jersey Medical School)

  • Padmini Salgame

    (Rutgers-New Jersey Medical School)

Abstract

Mechanisms underlying variability in transmission of Mycobacterium tuberculosis strains remain undefined. By characterizing high and low transmission strains of M.tuberculosis in mice, we show here that high transmission M.tuberculosis strain induce rapid IL-1R-dependent alveolar macrophage migration from the alveolar space into the interstitium and that this action is key to subsequent temporal events of early dissemination of bacteria to the lymph nodes, Th1 priming, granulomatous response and bacterial control. In contrast, IL-1R-dependent alveolar macrophage migration and early dissemination of bacteria to lymph nodes is significantly impeded in infection with low transmission M.tuberculosis strain; these events promote the development of Th17 immunity, fostering neutrophilic inflammation and increased bacterial replication. Our results suggest that by inducing granulomas with the potential to develop into cavitary lesions that aids bacterial escape into the airways, high transmission M.tuberculosis strain is poised for greater transmissibility. These findings implicate bacterial heterogeneity as an important modifier of TB disease manifestations and transmission.

Suggested Citation

  • Arianne Lovey & Sheetal Verma & Vaishnavi Kaipilyawar & Rodrigo Ribeiro-Rodrigues & Seema Husain & Moises Palaci & Reynaldo Dietze & Shuyi Ma & Robert D. Morrison & David. R. Sherman & Jerrold J. Elln, 2022. "Early alveolar macrophage response and IL-1R-dependent T cell priming determine transmissibility of Mycobacterium tuberculosis strains," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28506-2
    DOI: 10.1038/s41467-022-28506-2
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    References listed on IDEAS

    as
    1. Michael B. Reed & Pilar Domenech & Claudia Manca & Hua Su & Amy K. Barczak & Barry N. Kreiswirth & Gilla Kaplan & Clifton E. Barry, 2004. "A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response," Nature, Nature, vol. 431(7004), pages 84-87, September.
    2. Francesc Coll & Ruth McNerney & José Afonso Guerra-Assunção & Judith R. Glynn & João Perdigão & Miguel Viveiros & Isabel Portugal & Arnab Pain & Nigel Martin & Taane G. Clark, 2014. "A robust SNP barcode for typing Mycobacterium tuberculosis complex strains," Nature Communications, Nature, vol. 5(1), pages 1-5, December.
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    Cited by:

    1. Davide Pisu & Luana Johnston & Joshua T. Mattila & David G. Russell, 2024. "The frequency of CD38+ alveolar macrophages correlates with early control of M. tuberculosis in the murine lung," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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