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

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. Babayan, Mark Blaxter, Alasdair Ivens and Rick M. Maizels
Additional contact information
Amy H. Buck: Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
Gillian Coakley: Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
Fabio Simbari: Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
Henry J. McSorley: Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
Juan F. Quintana: Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
Thierry Le Bihan: Centre for Immunity, Infection and Evolution, 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
Yvonne Harcus: Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
Alessandro Ceroni: Institute of Immunology and Infection Research, School of Biological Sciences, University of Edinburgh
Simon A. Babayan: Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh
Mark Blaxter: Centre for Immunity, Infection and Evolution, 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

Nature Communications, 2014, vol. 5, issue 1, 1-12

Abstract: 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.

Date: 2014
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DOI: 10.1038/ncomms6488

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