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Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity

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  • Amy H. Buck

    (Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
    Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh)

  • Gillian Coakley

    (Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
    Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh)

  • Fabio Simbari

    (Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
    Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh)

  • Henry J. McSorley

    (Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
    Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh)

  • Juan F. Quintana

    (Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
    Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh)

  • Thierry Le Bihan

    (Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh
    SynthSys, Centre for Synthetic and Systems Biology, School of Biological Sciences, University of Edinburgh)

  • Sujai Kumar

    (Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh)

  • Cei Abreu-Goodger

    (Laboratorio Nacional de Genómica para la Biodiversidad, Langebio-CINVESTAV)

  • Marissa Lear

    (Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
    Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh)

  • Yvonne Harcus

    (Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
    Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh)

  • Alessandro Ceroni

    (Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
    Present address: Target Discovery Institute, University of Oxford, Nuffield Department of Medicine Research Building, Oxford OX3 7FZ, UK.)

  • Simon A. Babayan

    (Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh
    Present address: Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK (S.A.B.))

  • Mark Blaxter

    (Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh
    SynthSys, Centre for Synthetic and Systems Biology, School of Biological Sciences, University of Edinburgh
    Edinburgh Genomics, School of Biological Sciences, University of Edinburgh)

  • Alasdair Ivens

    (Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh)

  • Rick M. Maizels

    (Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
    Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh)

Abstract

In mammalian systems RNA can move between cells via vesicles. Here we demonstrate that the gastrointestinal nematode Heligmosomoides polygyrus, which infects mice, secretes vesicles containing microRNAs (miRNAs) and Y RNAs as well as a nematode Argonaute protein. These vesicles are of intestinal origin and are enriched for homologues of mammalian exosome proteins. Administration of the nematode exosomes to mice suppresses Type 2 innate responses and eosinophilia induced by the allergen Alternaria. Microarray analysis of mouse cells incubated with nematode exosomes in vitro identifies Il33r and Dusp1 as suppressed genes, and Dusp1 can be repressed by nematode miRNAs based on a reporter assay. We further identify miRNAs from the filarial nematode Litomosoides sigmodontis in the serum of infected mice, suggesting that miRNA secretion into host tissues is conserved among parasitic nematodes. These results reveal exosomes as another mechanism by which helminths manipulate their hosts and provide a mechanistic framework for RNA transfer between animal species.

Suggested Citation

  • Amy H. Buck & Gillian Coakley & Fabio Simbari & Henry J. McSorley & Juan F. Quintana & Thierry Le Bihan & Sujai Kumar & Cei Abreu-Goodger & Marissa Lear & Yvonne Harcus & Alessandro Ceroni & Simon A. , 2014. "Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms6488
    DOI: 10.1038/ncomms6488
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    Cited by:

    1. Baoye He & Huan Wang & Guosheng Liu & Angela Chen & Alejandra Calvo & Qiang Cai & Hailing Jin, 2023. "Fungal small RNAs ride in extracellular vesicles to enter plant cells through clathrin-mediated endocytosis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Maxim V. Zagoskin & Jianbin Wang & Ashley T. Neff & Giovana M. B. Veronezi & Richard E. Davis, 2022. "Small RNA pathways in the nematode Ascaris in the absence of piRNAs," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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