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Dual RNA-seq transcriptome analysis of caecal tissue during primary Eimeria tenella infection in chickens

BACKGROUND: Coccidiosis is an infectious disease with large negative impact on the poultry industry worldwide. It is an enteric infection caused by unicellular Apicomplexan parasites of the genus Eimeria. The present study aimed to gain more knowledge about interactions between parasites and the hos...

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Autores principales: Sandholt, Arnar K. S., Wattrang, Eva, Lilja, Tobias, Ahola, Harri, Lundén, Anna, Troell, Karin, Svärd, Staffan G., Söderlund, Robert
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8438895/
https://www.ncbi.nlm.nih.gov/pubmed/34521339
http://dx.doi.org/10.1186/s12864-021-07959-7
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author Sandholt, Arnar K. S.
Wattrang, Eva
Lilja, Tobias
Ahola, Harri
Lundén, Anna
Troell, Karin
Svärd, Staffan G.
Söderlund, Robert
author_facet Sandholt, Arnar K. S.
Wattrang, Eva
Lilja, Tobias
Ahola, Harri
Lundén, Anna
Troell, Karin
Svärd, Staffan G.
Söderlund, Robert
author_sort Sandholt, Arnar K. S.
collection PubMed
description BACKGROUND: Coccidiosis is an infectious disease with large negative impact on the poultry industry worldwide. It is an enteric infection caused by unicellular Apicomplexan parasites of the genus Eimeria. The present study aimed to gain more knowledge about interactions between parasites and the host immune system during the early asexual replication phase of E. tenella in chicken caeca. For this purpose, chickens were experimentally infected with E. tenella oocysts, sacrificed on days 1–4 and 10 after infection and mRNA from caecal tissues was extracted and sequenced. RESULTS: Dual RNA-seq analysis revealed time-dependent changes in both host and parasite gene expression during the course of the infection. Chicken immune activation was detected from day 3 and onwards with the highest number of differentially expressed immune genes recorded on day 10. Among early (days 3–4) responses up-regulation of genes for matrix metalloproteinases, several chemokines, interferon (IFN)-γ along with IFN-stimulated genes GBP, IRF1 and RSAD2 were noted. Increased expression of genes with immune suppressive/regulatory effects, e.g. IL10, SOCS1, SOCS3, was also observed among early responses. For E. tenella a general up-regulation of genes involved in protein expression and energy metabolism as well as a general down-regulation genes for DNA and RNA processing were observed during the infection. Specific E. tenella genes with altered expression during the experiment include those for proteins in rhoptry and microneme organelles. CONCLUSIONS: The present study provides novel information on both the transcriptional activity of E. tenella during schizogony in ceacal tissue and of the local host responses to parasite invasion during this phase of infection. Results indicate a role for IFN-γ and IFN-stimulated genes in the innate defence against Eimeria replication. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07959-7.
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spelling pubmed-84388952021-09-14 Dual RNA-seq transcriptome analysis of caecal tissue during primary Eimeria tenella infection in chickens Sandholt, Arnar K. S. Wattrang, Eva Lilja, Tobias Ahola, Harri Lundén, Anna Troell, Karin Svärd, Staffan G. Söderlund, Robert BMC Genomics Research BACKGROUND: Coccidiosis is an infectious disease with large negative impact on the poultry industry worldwide. It is an enteric infection caused by unicellular Apicomplexan parasites of the genus Eimeria. The present study aimed to gain more knowledge about interactions between parasites and the host immune system during the early asexual replication phase of E. tenella in chicken caeca. For this purpose, chickens were experimentally infected with E. tenella oocysts, sacrificed on days 1–4 and 10 after infection and mRNA from caecal tissues was extracted and sequenced. RESULTS: Dual RNA-seq analysis revealed time-dependent changes in both host and parasite gene expression during the course of the infection. Chicken immune activation was detected from day 3 and onwards with the highest number of differentially expressed immune genes recorded on day 10. Among early (days 3–4) responses up-regulation of genes for matrix metalloproteinases, several chemokines, interferon (IFN)-γ along with IFN-stimulated genes GBP, IRF1 and RSAD2 were noted. Increased expression of genes with immune suppressive/regulatory effects, e.g. IL10, SOCS1, SOCS3, was also observed among early responses. For E. tenella a general up-regulation of genes involved in protein expression and energy metabolism as well as a general down-regulation genes for DNA and RNA processing were observed during the infection. Specific E. tenella genes with altered expression during the experiment include those for proteins in rhoptry and microneme organelles. CONCLUSIONS: The present study provides novel information on both the transcriptional activity of E. tenella during schizogony in ceacal tissue and of the local host responses to parasite invasion during this phase of infection. Results indicate a role for IFN-γ and IFN-stimulated genes in the innate defence against Eimeria replication. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07959-7. BioMed Central 2021-09-14 /pmc/articles/PMC8438895/ /pubmed/34521339 http://dx.doi.org/10.1186/s12864-021-07959-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Sandholt, Arnar K. S.
Wattrang, Eva
Lilja, Tobias
Ahola, Harri
Lundén, Anna
Troell, Karin
Svärd, Staffan G.
Söderlund, Robert
Dual RNA-seq transcriptome analysis of caecal tissue during primary Eimeria tenella infection in chickens
title Dual RNA-seq transcriptome analysis of caecal tissue during primary Eimeria tenella infection in chickens
title_full Dual RNA-seq transcriptome analysis of caecal tissue during primary Eimeria tenella infection in chickens
title_fullStr Dual RNA-seq transcriptome analysis of caecal tissue during primary Eimeria tenella infection in chickens
title_full_unstemmed Dual RNA-seq transcriptome analysis of caecal tissue during primary Eimeria tenella infection in chickens
title_short Dual RNA-seq transcriptome analysis of caecal tissue during primary Eimeria tenella infection in chickens
title_sort dual rna-seq transcriptome analysis of caecal tissue during primary eimeria tenella infection in chickens
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8438895/
https://www.ncbi.nlm.nih.gov/pubmed/34521339
http://dx.doi.org/10.1186/s12864-021-07959-7
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