IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52846-w.html
   My bibliography  Save this article

The frequency of CD38+ alveolar macrophages correlates with early control of M. tuberculosis in the murine lung

Author

Listed:
  • Davide Pisu

    (Cornell University)

  • Luana Johnston

    (Cornell University)

  • Joshua T. Mattila

    (University of Pittsburgh School of Public Health)

  • David G. Russell

    (Cornell University)

Abstract

Tuberculosis, caused by Mycobacterium tuberculosis, remains an enduring global health challenge due to the limited efficacy of existing treatments. Although much research has focused on immune failure, the role of host macrophage biology in controlling the disease remains underappreciated. Here we show, through multi-modal single-cell RNA sequencing in a murine model, that different alveolar macrophage subsets play distinct roles in either advancing or controlling the disease. Initially, alveolar macrophages that are negative for the CD38 marker are the main infected population. As the infection progresses, CD38+ monocyte-derived and tissue-resident alveolar macrophages emerge as significant controllers of bacterial growth. These macrophages display a unique chromatin organization pre-infection, indicative of epigenetic priming for pro-inflammatory responses. Moreover, intranasal BCG immunization increases the numbers of CD38+ macrophages, enhancing their capability to restrict Mycobacterium tuberculosis growth. Our findings highlight the dynamic roles of alveolar macrophages in tuberculosis and open pathways for improved vaccines and therapies.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52846-w
    DOI: 10.1038/s41467-024-52846-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52846-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-52846-w?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. 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.
    2. Patricia A. Darrah & Joseph J. Zeppa & Pauline Maiello & Joshua A. Hackney & Marc H. Wadsworth & Travis K. Hughes & Supriya Pokkali & Phillip A. Swanson & Nicole L. Grant & Mark A. Rodgers & Megha Kam, 2020. "Prevention of tuberculosis in macaques after intravenous BCG immunization," Nature, Nature, vol. 577(7788), pages 95-102, January.
    3. M. Büttner & J. Ostner & C. L. Müller & F. J. Theis & B. Schubert, 2021. "scCODA is a Bayesian model for compositional single-cell data analysis," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    4. M. Tovar & Y. Moreno & J. Sanz, 2023. "Addressing mechanism bias in model-based impact forecasts of new tuberculosis vaccines," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    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. Dennis Lapuente & Jana Fuchs & Jonas Willar & Ana Vieira Antão & Valentina Eberlein & Nadja Uhlig & Leila Issmail & Anna Schmidt & Friederike Oltmanns & Antonia Sophia Peter & Sandra Mueller-Schmucker, 2021. "Protective mucosal immunity against SARS-CoV-2 after heterologous systemic prime-mucosal boost immunization," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. Jonas Engesser & Robin Khatri & Darius P. Schaub & Yu Zhao & Hans-Joachim Paust & Zeba Sultana & Nariaki Asada & Jan-Hendrik Riedel & Varshi Sivayoganathan & Anett Peters & Anna Kaffke & Saskia-Lariss, 2024. "Immune profiling-based targeting of pathogenic T cells with ustekinumab in ANCA-associated glomerulonephritis," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Abigail R. Gress & Christine E. Ronayne & Joshua M. Thiede & David K. Meyerholz & Samuel Okurut & Julia Stumpf & Tailor V. Mathes & Kenneth Ssebambulidde & David B. Meya & Fiona V. Cresswell & David R, 2023. "Recently activated CD4 T cells in tuberculosis express OX40 as a target for host-directed immunotherapy," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Yi Huang & Anyongqi Wang & Wenjiang Zhou & Baoguo Li & Linshan Zhang & Agata M. Rudolf & Zengguang Jin & Catherine Hambly & Guanlin Wang & John R. Speakman, 2024. "Maternal dietary fat during lactation shapes single nucleus transcriptomic profile of postnatal offspring hypothalamus in a sexually dimorphic manner in mice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Zhenlin Yang & He Tian & Xiaowei Chen & Bozhao Li & Guangyu Bai & Qingyuan Cai & Jiachen Xu & Wei Guo & Shuaibo Wang & Yue Peng & Qing Liang & Liyan Xue & Shugeng Gao, 2024. "Single-cell sequencing reveals immune features of treatment response to neoadjuvant immunochemotherapy in esophageal squamous cell carcinoma," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Kaya J. E. Matson & Daniel E. Russ & Claudia Kathe & Isabelle Hua & Dragan Maric & Yi Ding & Jonathan Krynitsky & Randall Pursley & Anupama Sathyamurthy & Jordan W. Squair & Boaz P. Levi & Gregoire Co, 2022. "Single cell atlas of spinal cord injury in mice reveals a pro-regenerative signature in spinocerebellar neurons," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Eduardo Moreo & Aitor Jarit-Cabanillas & Iñaki Robles-Vera & Santiago Uranga & Claudia Guerrero & Ana Belén Gómez & Pablo Mata-Martínez & Luna Minute & Miguel Araujo-Voces & María José Felgueres & Glo, 2023. "Intravenous administration of BCG in mice promotes natural killer and T cell-mediated antitumor immunity in the lung," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Ivan V. Kuzmin & Ruben Soto Acosta & Layne Pruitt & Perry T. Wasdin & Kritika Kedarinath & Keziah R. Hernandez & Kristyn A. Gonzales & Kharighan Hill & Nicole G. Weidner & Chad Mire & Taylor B. Engdah, 2024. "Comparison of uridine and N1-methylpseudouridine mRNA platforms in development of an Andes virus vaccine," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    9. Sebastian Schmidt & Malte D. Luecken & Dietrich Trümbach & Sina Hembach & Kristina M. Niedermeier & Nicole Wenck & Klaus Pflügler & Constantin Stautner & Anika Böttcher & Heiko Lickert & Ciro Ramirez-, 2022. "Primary cilia and SHH signaling impairments in human and mouse models of Parkinson’s disease," Nature Communications, Nature, vol. 13(1), pages 1-25, December.
    10. Richard F. Silver & Mei Xia & Chad E. Storer & Jessica R. Jarvela & Michelle C. Moyer & Azra Blazevic & David A. Stoeckel & Erin K. Rakey & Jan M. Tennant & Johannes B. Goll & Richard D. Head & Daniel, 2023. "Distinct gene expression signatures comparing latent tuberculosis infection with different routes of Bacillus Calmette-Guérin vaccination," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    11. Andrew Gibson & Ramesh Ram & Rama Gangula & Yueran Li & Eric Mukherjee & Amy M. Palubinsky & Chelsea N. Campbell & Michael Thorne & Katherine C. Konvinse & Phuti Choshi & Pooja Deshpande & Sarah Pedre, 2024. "Multiomic single-cell sequencing defines tissue-specific responses in Stevens-Johnson syndrome and toxic epidermal necrolysis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. Venkata S. Bollimpelli & Pradeep B. J Reddy & Sailaja Gangadhara & Tysheena P. Charles & Samantha L. Burton & Gregory K. Tharp & Tiffany M. Styles & Celia C. Labranche & Justin C. Smith & Amit A. Upad, 2023. "Intradermal but not intramuscular modified vaccinia Ankara immunizations protect against intravaginal tier2 simian-human immunodeficiency virus challenges in female macaques," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Joshua S. Woodworth & Helena Strand Clemmensen & Hannah Battey & Karin Dijkman & Thomas Lindenstrøm & Raquel Salvador Laureano & Randy Taplitz & Jeffrey Morgan & Claus Aagaard & Ida Rosenkrands & Ceci, 2021. "A Mycobacterium tuberculosis-specific subunit vaccine that provides synergistic immunity upon co-administration with Bacillus Calmette-Guérin," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    14. Drew R. Neavin & Angela M. Steinmann & Nona Farbehi & Han Sheng Chiu & Maciej S. Daniszewski & Himanshi Arora & Yasmin Bermudez & Cátia Moutinho & Chia-Ling Chan & Monique Bax & Mubarika Tyebally & Vi, 2023. "A village in a dish model system for population-scale hiPSC studies," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    15. Atienza-Diez, Iker & Seoane, Luís F., 2023. "Long- and short-term effects of cross-immunity in epidemic dynamics," Chaos, Solitons & Fractals, Elsevier, vol. 174(C).
    16. Alok K. Maity & Andrew E. Teschendorff, 2023. "Cell-attribute aware community detection improves differential abundance testing from single-cell RNA-Seq data," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    17. Seongryong Kim & Ji Hyang Jeon & Myeonghwan Kim & Yeji Lee & Yun-Ho Hwang & Myungsun Park & C. Han Li & Taeyoung Lee & Jung-Ah Lee & You-Me Kim & Dokeun Kim & Hyukjin Lee & You-Jin Kim & V. Narry Kim , 2024. "Innate immune responses against mRNA vaccine promote cellular immunity through IFN-β at the injection site," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    18. One B. Dintwe & Lamar Ballweber Fleming & Valentin Voillet & John McNevin & Aaron Seese & Anneta Naidoo & Saleha Omarjee & Linda-Gail Bekker & James G. Kublin & Stephen C. Rosa & Evan W. Newell & Andr, 2024. "Adolescent BCG revaccination induces a phenotypic shift in CD4+ T cell responses to Mycobacterium tuberculosis," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Praveen Weeratunga & Laura Denney & Joshua A. Bull & Emmanouela Repapi & Martin Sergeant & Rachel Etherington & Chaitanya Vuppussetty & Gareth D. H. Turner & Colin Clelland & Jeongmin Woo & Amy Cross , 2023. "Single cell spatial analysis reveals inflammatory foci of immature neutrophil and CD8 T cells in COVID-19 lungs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    20. Sara G. Danielli & Yun Wei & Michael A. Dyer & Elizabeth Stewart & Heather Sheppard & Marco Wachtel & Beat W. Schäfer & Anand G. Patel & David M. Langenau, 2024. "Single cell transcriptomic profiling identifies tumor-acquired and therapy-resistant cell states in pediatric rhabdomyosarcoma," Nature Communications, Nature, vol. 15(1), pages 1-14, 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:15:y:2024:i:1:d:10.1038_s41467-024-52846-w. 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.