Extracellular Vesicle-Contained microRNA of C. elegans as a Tool to Decipher the Molecular Basis of Nematode Parasitism

Among the fundamental biological processes affected by microRNAs, small regulators of gene expression, a potential role in host-parasite communication is intriguing. We compared the miRNA complement of extracellular vesicles released by the free-living nematode Caenorhabditis elegans in culture to t...

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Main Authors: Thomas B. Duguet, Julien Soichot, Rostyslav Kuzyakiv, Lars Malmström, Lucienne Tritten
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcimb.2020.00217/full
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spelling doaj-ef9df0d334b041b18214aefd2a6b5a872020-11-25T03:21:22ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882020-05-011010.3389/fcimb.2020.00217536974Extracellular Vesicle-Contained microRNA of C. elegans as a Tool to Decipher the Molecular Basis of Nematode ParasitismThomas B. Duguet0Julien Soichot1Rostyslav Kuzyakiv2Rostyslav Kuzyakiv3Lars Malmström4Lars Malmström5Lars Malmström6Lars Malmström7Lucienne Tritten8Institute of Parasitology, McGill University, Sainte-Anne-de-Bellevue, QC, CanadaInstitute of Parasitology, University of Zurich, Zurich, SwitzerlandS3IT, University of Zurich, Zurich, SwitzerlandSIB Swiss Institute of Bioinformatics, Lausanne, SwitzerlandS3IT, University of Zurich, Zurich, SwitzerlandSIB Swiss Institute of Bioinformatics, Lausanne, SwitzerlandInstitute for Computational Science, University of Zurich, Zurich, SwitzerlandDivision of Infection Medicine, Lund University, Lund, SwedenInstitute of Parasitology, University of Zurich, Zurich, SwitzerlandAmong the fundamental biological processes affected by microRNAs, small regulators of gene expression, a potential role in host-parasite communication is intriguing. We compared the miRNA complement of extracellular vesicles released by the free-living nematode Caenorhabditis elegans in culture to that of other adult parasitic nematodes. Expecting convergent functional roles for secreted miRNAs due to the common parasitic lifestyle of the organisms under investigation, we performed a miRNA sequence analysis as well as target search and pathway enrichment for potential mRNA targets within host immune functions. We found that the parasite miRNA seed sequences were more often identical to those of C. elegans, rather than to those of their hosts. However, we observed that the nematode-secreted miRNA fractions shared more often seed sequences with host miRNAs than those that are not found in the extracellular environment. Development and proliferation of immune cells was predicted to be affected several-fold by nematode miRNA release. In addition, we identified the AGE-RAGE signaling as a convergent targeted pathway by species-specific miRNAs from several parasitic species. We propose a multi-species comparative approach to differentiate those miRNAs that may have critical functions in host modulation, from those that may not. With our simple analysis, we put forward a workflow to study traits of parasitism at the miRNA level. This work will find even more resonance and significance, as an increasing amount of parasite miRNA collections are expected to be produced in the future.https://www.frontiersin.org/article/10.3389/fcimb.2020.00217/fullnematodehostmicroRNAsecretedextracellular vesiclescomputational analysis
collection DOAJ
language English
format Article
sources DOAJ
author Thomas B. Duguet
Julien Soichot
Rostyslav Kuzyakiv
Rostyslav Kuzyakiv
Lars Malmström
Lars Malmström
Lars Malmström
Lars Malmström
Lucienne Tritten
spellingShingle Thomas B. Duguet
Julien Soichot
Rostyslav Kuzyakiv
Rostyslav Kuzyakiv
Lars Malmström
Lars Malmström
Lars Malmström
Lars Malmström
Lucienne Tritten
Extracellular Vesicle-Contained microRNA of C. elegans as a Tool to Decipher the Molecular Basis of Nematode Parasitism
Frontiers in Cellular and Infection Microbiology
nematode
host
microRNA
secreted
extracellular vesicles
computational analysis
author_facet Thomas B. Duguet
Julien Soichot
Rostyslav Kuzyakiv
Rostyslav Kuzyakiv
Lars Malmström
Lars Malmström
Lars Malmström
Lars Malmström
Lucienne Tritten
author_sort Thomas B. Duguet
title Extracellular Vesicle-Contained microRNA of C. elegans as a Tool to Decipher the Molecular Basis of Nematode Parasitism
title_short Extracellular Vesicle-Contained microRNA of C. elegans as a Tool to Decipher the Molecular Basis of Nematode Parasitism
title_full Extracellular Vesicle-Contained microRNA of C. elegans as a Tool to Decipher the Molecular Basis of Nematode Parasitism
title_fullStr Extracellular Vesicle-Contained microRNA of C. elegans as a Tool to Decipher the Molecular Basis of Nematode Parasitism
title_full_unstemmed Extracellular Vesicle-Contained microRNA of C. elegans as a Tool to Decipher the Molecular Basis of Nematode Parasitism
title_sort extracellular vesicle-contained microrna of c. elegans as a tool to decipher the molecular basis of nematode parasitism
publisher Frontiers Media S.A.
series Frontiers in Cellular and Infection Microbiology
issn 2235-2988
publishDate 2020-05-01
description Among the fundamental biological processes affected by microRNAs, small regulators of gene expression, a potential role in host-parasite communication is intriguing. We compared the miRNA complement of extracellular vesicles released by the free-living nematode Caenorhabditis elegans in culture to that of other adult parasitic nematodes. Expecting convergent functional roles for secreted miRNAs due to the common parasitic lifestyle of the organisms under investigation, we performed a miRNA sequence analysis as well as target search and pathway enrichment for potential mRNA targets within host immune functions. We found that the parasite miRNA seed sequences were more often identical to those of C. elegans, rather than to those of their hosts. However, we observed that the nematode-secreted miRNA fractions shared more often seed sequences with host miRNAs than those that are not found in the extracellular environment. Development and proliferation of immune cells was predicted to be affected several-fold by nematode miRNA release. In addition, we identified the AGE-RAGE signaling as a convergent targeted pathway by species-specific miRNAs from several parasitic species. We propose a multi-species comparative approach to differentiate those miRNAs that may have critical functions in host modulation, from those that may not. With our simple analysis, we put forward a workflow to study traits of parasitism at the miRNA level. This work will find even more resonance and significance, as an increasing amount of parasite miRNA collections are expected to be produced in the future.
topic nematode
host
microRNA
secreted
extracellular vesicles
computational analysis
url https://www.frontiersin.org/article/10.3389/fcimb.2020.00217/full
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