Secretion of an Argonaute protein by a parasitic nematode and the evolution of its siRNA guides.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
23 04 2019
Historique:
accepted: 25 02 2019
revised: 16 02 2019
received: 24 08 2018
pubmed: 2 3 2019
medline: 11 10 2019
entrez: 2 3 2019
Statut: ppublish

Résumé

Extracellular RNA has been proposed to mediate communication between cells and organisms however relatively little is understood regarding how specific sequences are selected for export. Here, we describe a specific Argonaute protein (exWAGO) that is secreted in extracellular vesicles (EVs) released by the gastrointestinal nematode Heligmosomoides bakeri, at multiple copies per EV. Phylogenetic and gene expression analyses demonstrate exWAGO orthologues are highly conserved and abundantly expressed in related parasites but highly diverged in free-living genus Caenorhabditis. We show that the most abundant small RNAs released from the nematode parasite are not microRNAs as previously thought, but rather secondary small interfering RNAs (siRNAs) that are produced by RNA-dependent RNA Polymerases. The siRNAs that are released in EVs have distinct evolutionary properties compared to those resident in free-living or parasitic nematodes. Immunoprecipitation of exWAGO demonstrates that it specifically associates with siRNAs from transposons and newly evolved repetitive elements that are packaged in EVs and released into the host environment. Together this work demonstrates molecular and evolutionary selectivity in the small RNA sequences that are released in EVs into the host environment and identifies a novel Argonaute protein as the mediator of this.

Identifiants

pubmed: 30820541
pii: 5366476
doi: 10.1093/nar/gkz142
pmc: PMC6468290
doi:

Substances chimiques

Argonaute Proteins 0
RNA, Small Interfering 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3594-3606

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.

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Auteurs

Franklin Wang-Ngai Chow (FW)

Institute of Immunology and Infection Research, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.

Georgios Koutsovoulos (G)

Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.

Cesaré Ovando-Vázquez (C)

Unidad de Genómica Avanzada (Langebio), Centro de Investigación y de Estudios Avanzados del IPN, Irapuato, Guanajuato 36824, México.

Kyriaki Neophytou (K)

Institute of Immunology and Infection Research, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.

Jose R Bermúdez-Barrientos (JR)

Unidad de Genómica Avanzada (Langebio), Centro de Investigación y de Estudios Avanzados del IPN, Irapuato, Guanajuato 36824, México.

Dominik R Laetsch (DR)

Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.

Elaine Robertson (E)

Institute of Immunology and Infection Research, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.

Sujai Kumar (S)

Institute of Immunology and Infection Research, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.

Julie M Claycomb (JM)

Department of Molecular Genetics, University of Toronto, Toronto, ON M5G 1M1, Canada.

Mark Blaxter (M)

Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.
Centre for Immunity, Infection and Evolution, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.

Cei Abreu-Goodger (C)

Unidad de Genómica Avanzada (Langebio), Centro de Investigación y de Estudios Avanzados del IPN, Irapuato, Guanajuato 36824, México.

Amy H Buck (AH)

Institute of Immunology and Infection Research, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.
Centre for Immunity, Infection and Evolution, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3JT, UK.

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Classifications MeSH