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Disruption of gut integrity and permeability contributes to enteritis in a fish-parasite model: a story told from serum metabolomics

2019-10-16Journal article Open access
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dc.contributor.authorSitjà-Bobadilla, Ariadna
dc.contributor.authorGil-Solsona, Rubén
dc.contributor.authorEstensoro, Itziar
dc.contributor.authorPiazzon, M. C
dc.contributor.authorMartos-Sitcha, Juan A
dc.contributor.authorPicard-Sánchez, Amparo
dc.contributor.authorFuentes, Juan
dc.contributor.authorSancho, Juan V
dc.contributor.authorCalduch-Giner, Josep A
dc.contributor.authorHernández, Félix
dc.contributor.authorPérez-Sánchez, Jaume
dc.date.accessioned2019-11-06T09:37:09Z
dc.date.available2019-11-06T09:37:09Z
dc.date.issued2019-10-16
dc.date.updated2019-11-01T08:01:03Z
dc.description.abstractBackground In the animal production sector, enteritis is responsible for serious economic losses, and intestinal parasitism is a major stress factor leading to malnutrition and lowered performance and animal production efficiency. The effect of enteric parasites on the gut function of teleost fish, which represent the most ancient bony vertebrates, is far from being understood. The intestinal myxozoan parasite Enteromyxum leei dwells between gut epithelial cells and causes severe enteritis in gilthead sea bream (Sparus aurata), anorexia, cachexia, growth impairment, reduced marketability and increased mortality. Methods This study aimed to outline the gut failure in this fish-parasite model using a multifaceted approach and to find and validate non-lethal serum markers of gut barrier dysfunction. Intestinal integrity was studied in parasitized and non-parasitized fish by immunohistochemistry with specific markers for cellular adhesion (E-cadherin) and tight junctions (Tjp1 and Cldn3) and by functional studies of permeability (oral administration of FITC-dextran) and electrophysiology (Ussing chambers). Serum samples from parasitized and non-parasitized fish were analyzed using non-targeted metabolomics and some significantly altered metabolites were selected to be validated using commercial kits. Results The immunodetection of Tjp1 and Cldn3 was significantly lower in the intestine of parasitized fish, while no strong differences were found in E-cadherin. Parasitized fish showed a significant increase in paracellular uptake measured by FITC-dextran detection in serum. Electrophysiology showed a decrease in transepithelial resistance in infected animals, which showed a diarrheic profile. Serum metabolomics revealed 3702 ions, from which the differential expression of 20 identified compounds significantly separated control from infected groups in multivariate analyses. Of these compounds, serum inosine (decreased) and creatine (increased) were identified as relevant and validated with commercial kits. Conclusions The results demonstrate the disruption of tight junctions and the loss of gut barrier function, a metabolomic profile of absorption dysfunction and anorexia, which further outline the pathophysiological effects of E. leei.pt_PT
dc.description.sponsorshipThis work has been carried out with fnancial support from the European Union under grant projects ParaFishControl (H2020-634429) to ASB and Aquaexcel2020 (652831, TNA AE10004-INTEBREAM) to JF and JPS, and from the Spanish MINECO under AGL2013-48560-R project to ASB and JPS. APS was contracted under the ParaFishControl project, MCP under CSIC PIE project no. 201740E013 and IE under APOSTD/2016/037 grant by the “Generalitat Valen‑ ciana”. Centre for Marine Sciences (CCMAR) is supported by the Portuguese Foundation for Science and Technology (FCT) through project UID/Multi 04326/2019.pt_PT
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.citationParasites & Vectors. 2019 Oct 16;12(1):486pt_PT
dc.identifier.dois13071-019-3746-7
dc.identifier.issn1756-3305
dc.identifier.urihttp://hdl.handle.net/10400.1/12866
dc.language.isoengpt_PT
dc.peerreviewedyespt_PT
dc.publisherBMCpt_PT
dc.relationAQUAculture infrastructures for EXCELlence in European fish research towards 2020
dc.rights.holderThe Author(s)
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/pt_PT
dc.subjectMyxozoapt_PT
dc.subjectEnteromyxum leeipt_PT
dc.subjectGilthead sea breampt_PT
dc.subjectTeleosteipt_PT
dc.subjectAquaculturept_PT
dc.subjectPathophysiologypt_PT
dc.subjectTight junctionspt_PT
dc.subjectGut barrierpt_PT
dc.subjectElectrophysiologypt_PT
dc.subjectMetabolomicspt_PT
dc.titleDisruption of gut integrity and permeability contributes to enteritis in a fish-parasite model: a story told from serum metabolomicspt_PT
dc.typejournal article
dspace.entity.typePublication
oaire.awardTitleAQUAculture infrastructures for EXCELlence in European fish research towards 2020
oaire.awardURIinfo:eu-repo/grantAgreement/EC/H2020/652831/EU
oaire.citation.issue1pt_PT
oaire.citation.startPage486pt_PT
oaire.citation.titleParasites and Vectorspt_PT
oaire.citation.volume12pt_PT
oaire.fundingStreamH2020
person.familyNameFuentes
person.givenNameJuan
person.identifier392998
person.identifier.ciencia-id421B-E196-2C33
person.identifier.orcid0000-0003-0430-8734
person.identifier.scopus-author-id7201832526
project.funder.identifierhttp://doi.org/10.13039/501100008530
project.funder.nameEuropean Commission
rcaap.rightsopenAccesspt_PT
rcaap.typearticlept_PT
relation.isAuthorOfPublicationd354b937-b18c-4ca5-a843-04a04269d60f
relation.isAuthorOfPublication.latestForDiscoveryd354b937-b18c-4ca5-a843-04a04269d60f
relation.isProjectOfPublicationaf2e9e71-3f77-4149-8f42-1d186fc443e4
relation.isProjectOfPublication.latestForDiscoveryaf2e9e71-3f77-4149-8f42-1d186fc443e4

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