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Pulmonary inflammation promoted by type-2 dendritic cells is a feature of human and murine schistosomiasis

Author

Listed:
  • E. L. Houlder

    (University of Manchester
    Leiden University Medical Centre)

  • A. H. Costain

    (University of Manchester
    Leiden University Medical Centre)

  • I. Nambuya

    (University of Manchester
    MRC/UVRI and LSHTM Uganda Research Unit)

  • S. L. Brown

    (University of Manchester)

  • J. P. R. Koopman

    (Leiden University Medical Centre)

  • M. C. C. Langenberg

    (Leiden University Medical Centre)

  • J. J. Janse

    (Leiden University Medical Centre)

  • M. A. Hoogerwerf

    (Leiden University Medical Centre)

  • A. J. L. Ridley

    (University of Manchester)

  • J. E. Forde-Thomas

    (Aberystwyth University)

  • S. A. P. Colombo

    (University of Manchester)

  • B. M. F. Winkel

    (Leiden University Medical Centre)

  • A. A. Galdon

    (University of Manchester)

  • K. F. Hoffmann

    (Aberystwyth University)

  • P. C. Cook

    (University of Manchester
    University of Exeter)

  • M. Roestenberg

    (Leiden University Medical Centre)

  • H. Mpairwe

    (MRC/UVRI and LSHTM Uganda Research Unit)

  • A. S. MacDonald

    (University of Manchester)

Abstract

Schistosomiasis is a parasitic disease affecting over 200 million people in multiple organs, including the lungs. Despite this, there is little understanding of pulmonary immune responses during schistosomiasis. Here, we show type-2 dominated lung immune responses in both patent (egg producing) and pre-patent (larval lung migration) murine Schistosoma mansoni (S. mansoni) infection. Human pre-patent S. mansoni infection pulmonary (sputum) samples revealed a mixed type-1/type-2 inflammatory cytokine profile, whilst a case-control study showed no significant pulmonary cytokine changes in endemic patent infection. However, schistosomiasis induced expansion of pulmonary type-2 conventional dendritic cells (cDC2s) in human and murine hosts, at both infection stages. Further, cDC2s were required for type-2 pulmonary inflammation in murine pre-patent or patent infection. These data elevate our fundamental understanding of pulmonary immune responses during schistosomiasis, which may be important for future vaccine design, as well as for understanding links between schistosomiasis and other lung diseases.

Suggested Citation

  • E. L. Houlder & A. H. Costain & I. Nambuya & S. L. Brown & J. P. R. Koopman & M. C. C. Langenberg & J. J. Janse & M. A. Hoogerwerf & A. J. L. Ridley & J. E. Forde-Thomas & S. A. P. Colombo & B. M. F. , 2023. "Pulmonary inflammation promoted by type-2 dendritic cells is a feature of human and murine schistosomiasis," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37502-z
    DOI: 10.1038/s41467-023-37502-z
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    References listed on IDEAS

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    1. Barbara Maier & Andrew M. Leader & Steven T. Chen & Navpreet Tung & Christie Chang & Jessica LeBerichel & Aleksey Chudnovskiy & Shrisha Maskey & Laura Walker & John P. Finnigan & Margaret E. Kirkling , 2020. "A conserved dendritic-cell regulatory program limits antitumour immunity," Nature, Nature, vol. 580(7802), pages 257-262, April.
    2. Peter C. Cook & Heather Owen & Aimée M. Deaton & Jessica G. Borger & Sheila L. Brown & Thomas Clouaire & Gareth-Rhys Jones & Lucy H. Jones & Rachel J. Lundie & Angela K. Marley & Vicky L. Morrison & A, 2015. "A dominant role for the methyl-CpG-binding protein Mbd2 in controlling Th2 induction by dendritic cells," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    3. Barbara Maier & Andrew M. Leader & Steven T. Chen & Navpreet Tung & Christie Chang & Jessica LeBerichel & Aleksey Chudnovskiy & Shrisha Maskey & Laura Walker & John P. Finnigan & Margaret E. Kirkling , 2020. "Author Correction: A conserved dendritic-cell regulatory program limits antitumour immunity," Nature, Nature, vol. 582(7813), pages 17-17, June.
    4. Johannes U. Mayer & Mimoza Demiri & William W. Agace & Andrew S. MacDonald & Marcus Svensson-Frej & Simon W. Milling, 2017. "Different populations of CD11b+ dendritic cells drive Th2 responses in the small intestine and colon," Nature Communications, Nature, vol. 8(1), pages 1-12, August.
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