Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shasta

© 2021 by the authors.

Detalles Bibliográficos
Autores: Barrett, Damien E., Estensoro, Itziar, Sitjà-Bobadilla, Ariadna, Bartholomew, J. L.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2021
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/267104
Acceso en línea:http://hdl.handle.net/10261/267104
Access Level:acceso abierto
Palabra clave:Oncorhynchus mykiss
Steelhead
Ceratonova shasta
Myxozoan
Parasites
RNA-seq
Transcriptomics
Immune response
Host–parasite interaction
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spelling Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shastaBarrett, Damien E.Estensoro, ItziarSitjà-Bobadilla, AriadnaBartholomew, J. L.Oncorhynchus mykissSteelheadCeratonova shastaMyxozoanParasitesRNA-seqTranscriptomicsImmune responseHost–parasite interaction© 2021 by the authors.Background: Myxozoan parasites infect fish worldwide causing significant disease or death in many economically important fish species, including rainbow trout and steelhead trout (Oncorhynchus mykiss). The myxozoan Ceratonova shasta is a parasite of salmon and trout that causes ceratomyxosis, a disease characterized by severe inflammation in the intestine resulting in hemorrhaging and necrosis. Populations of O. mykiss that are genetically fixed for resistance or susceptibility to ceratomyxosis exist naturally, offering a tractable system for studying the immune response to myxozoans. The aim of this study was to understand how steelhead trout that are resistant to the disease respond to C. shasta once it has become established in the intestine and identify potential mechanisms of resistance. Results: Sequencing of intestinal mRNA from resistant steelhead trout with severe C. shasta infections identified 417 genes differentially expressed during the initial stage of the infection compared to uninfected control fish. A strong induction of interferon-gamma and interferon-stimulated genes was evident, along with genes involved in cell adhesion and migration. A total of 11,984 genes were differentially expressed during the late stage of the infection, most notably interferon-gamma, interleukin-6, and immunoglobulin transcripts. A distinct hardening of the intestinal tissue and a strong inflammatory reaction in the intestinal submucosa including severe hyperplasia and inflammatory cell infiltrates were observed in response to the infection. The massive upregulation of caspase-14 early in the infection, a protein involved in keratinocyte differentiation might reflect the rapid onset of epithelial repair mechanisms, and the collagenous stratum compactum seemed to limit the spread of C. shasta within the intestinal layers. These observations could explain the ability of resistant fish to eventually recover from the infection. Conclusions: Our results suggest that resistance to ceratomyxosis involves both a rapid induction of key immune factors and a tissue response that limits the spread of the parasite and the subsequent tissue damage. These results improve our understanding of the myxozoan–host dialogue and provide a framework for future studies investigating the infection dynamics of C. shasta and other myxozoans.This work was funded by the Bureau of Reclamation, U.S. Department of Interior through Interagency Agreement # R19PG00027, awarded to J.L.B.Multidisciplinary Digital Publishing InstituteU. S. Department of the InteriorConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2022202220212022info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/267104reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttp://dx.doi.org/10.3390/pathogens10091179Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2671042026-05-22T06:33:51Z
dc.title.none.fl_str_mv Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shasta
title Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shasta
spellingShingle Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shasta
Barrett, Damien E.
Oncorhynchus mykiss
Steelhead
Ceratonova shasta
Myxozoan
Parasites
RNA-seq
Transcriptomics
Immune response
Host–parasite interaction
title_short Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shasta
title_full Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shasta
title_fullStr Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shasta
title_full_unstemmed Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shasta
title_sort Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite ceratonova shasta
dc.creator.none.fl_str_mv Barrett, Damien E.
Estensoro, Itziar
Sitjà-Bobadilla, Ariadna
Bartholomew, J. L.
author Barrett, Damien E.
author_facet Barrett, Damien E.
Estensoro, Itziar
Sitjà-Bobadilla, Ariadna
Bartholomew, J. L.
author_role author
author2 Estensoro, Itziar
Sitjà-Bobadilla, Ariadna
Bartholomew, J. L.
author2_role author
author
author
dc.contributor.none.fl_str_mv U. S. Department of the Interior
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Oncorhynchus mykiss
Steelhead
Ceratonova shasta
Myxozoan
Parasites
RNA-seq
Transcriptomics
Immune response
Host–parasite interaction
topic Oncorhynchus mykiss
Steelhead
Ceratonova shasta
Myxozoan
Parasites
RNA-seq
Transcriptomics
Immune response
Host–parasite interaction
description © 2021 by the authors.
publishDate 2021
dc.date.none.fl_str_mv 2021
2022
2022
2022
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/267104
url http://hdl.handle.net/10261/267104
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv http://dx.doi.org/10.3390/pathogens10091179
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Multidisciplinary Digital Publishing Institute
publisher.none.fl_str_mv Multidisciplinary Digital Publishing Institute
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.812429

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