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Dermis resident macrophages orchestrate localized ILC2 eosinophil circuitries to promote non-healing cutaneous leishmaniasis

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  • Sang Hun Lee

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Byunghyun Kang

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Olena Kamenyeva

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Tiago Rodrigues Ferreira

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Kyoungin Cho

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Jaspal S. Khillan

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Juraj Kabat

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Brian L. Kelsall

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • David L. Sacks

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

Abstract

Tissue-resident macrophages are critical for tissue homeostasis and repair. We previously showed that dermis-resident macrophages produce CCL24 which mediates their interaction with IL-4+ eosinophils, required to maintain their M2-like properties in the TH1 environment of the Leishmania major infected skin. Here, we show that thymic stromal lymphopoietin (TSLP) and IL-5+ type 2 innate lymphoid cells are also required to maintain dermis-resident macrophages and promote infection. Single cell RNA sequencing reveals the dermis-resident macrophages as the sole source of TSLP and CCL24. Generation of Ccl24-cre mice permits specific labeling of dermis-resident macrophages and interstitial macrophages from other organs. Selective ablation of TSLP in dermis-resident macrophages reduces the numbers of IL-5+ type 2 innate lymphoid cells, eosinophils and dermis-resident macrophages, and ameliorates infection. Our findings demonstrate that dermis-resident macrophages are self-maintained as a replicative niche for L. major by orchestrating localized type 2 circuitries with type 2 innate lymphoid cells and eosinophils.

Suggested Citation

  • Sang Hun Lee & Byunghyun Kang & Olena Kamenyeva & Tiago Rodrigues Ferreira & Kyoungin Cho & Jaspal S. Khillan & Juraj Kabat & Brian L. Kelsall & David L. Sacks, 2023. "Dermis resident macrophages orchestrate localized ILC2 eosinophil circuitries to promote non-healing cutaneous leishmaniasis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43588-2
    DOI: 10.1038/s41467-023-43588-2
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    References listed on IDEAS

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    1. Stephan Culemann & Anika Grüneboom & José Ángel Nicolás-Ávila & Daniela Weidner & Katrin Franziska Lämmle & Tobias Rothe & Juan A. Quintana & Philipp Kirchner & Branislav Krljanac & Martin Eberhardt &, 2019. "Locally renewing resident synovial macrophages provide a protective barrier for the joint," Nature, Nature, vol. 572(7771), pages 670-675, August.
    2. Tiffany Bouchery & Ryan Kyle & Mali Camberis & Amy Shepherd & Kara Filbey & Alexander Smith & Marina Harvie & Gavin Painter & Karen Johnston & Peter Ferguson & Rohit Jain & Ben Roediger & Brett Delahu, 2015. "ILC2s and T cells cooperate to ensure maintenance of M2 macrophages for lung immunity against hookworms," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
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