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Differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge

BACKGROUND: Accompanied with rapid growth and high density aquaculture, gibel carp has been seriously threatened by Carassius auratus herpesvirus (CaHV) since 2012. In previous study, distinct CaHV resistances and immune responses were revealed in the diseased individuals of three gibel carp gynogen...

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Autores principales: Lu, Wei-Jia, Gao, Fan-Xiang, Wang, Yang, Zhang, Qi-Ya, Li, Zhi, Zhang, Xiao-Juan, Zhou, Li, Gui, Jian-Fang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6540555/
https://www.ncbi.nlm.nih.gov/pubmed/31138127
http://dx.doi.org/10.1186/s12864-019-5777-z
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author Lu, Wei-Jia
Gao, Fan-Xiang
Wang, Yang
Zhang, Qi-Ya
Li, Zhi
Zhang, Xiao-Juan
Zhou, Li
Gui, Jian-Fang
author_facet Lu, Wei-Jia
Gao, Fan-Xiang
Wang, Yang
Zhang, Qi-Ya
Li, Zhi
Zhang, Xiao-Juan
Zhou, Li
Gui, Jian-Fang
author_sort Lu, Wei-Jia
collection PubMed
description BACKGROUND: Accompanied with rapid growth and high density aquaculture, gibel carp has been seriously threatened by Carassius auratus herpesvirus (CaHV) since 2012. In previous study, distinct CaHV resistances and immune responses were revealed in the diseased individuals of three gibel carp gynogenetic clones (A(+), F and H). However, little is known about the gene expression changes in the survivors after CaHV challenge, particularly their differences of innate and adaptive immune system between susceptible clone and resistant clone. RESULTS: We firstly confirmed the CaHV carrier state in the survivors of three gibel carp clones after CaHV challenge by evaluating the abundances of five CaHV genes. The assay of viral loads indicated the resistant clone H possessed not only stronger resistance but also higher tolerance to CaHV. Then, 2818, 4047 and 3323 differentially expressed unigenes (DEUs) were screened from the head-kidney transcriptome profiles of survivors compared with controls from clone A(+), F and H. GO and KEGG analysis suggested that a persistent immune response might sustain in resistant clone H and F, while susceptible clone A(+) had a long-term impact on the circulatory system which was consistent with the major symptoms of bleeding caused by CaHV. Among the top 30 enriched pathways of specifically up-regulated DEUs in respective clones, 26, 7 and 15 pathways in clone H, F and A(+) were associated with infections, diseases, or immune-related pathways respectively. In addition, 20 pathways in clone F belonged to “metabolism” or “biogenesis”, and 7 pathways involved in “circulatory system” were enriched in clone A(+). Significantly, we revealed the differential expression changes of IFN system genes and immunoglobulin (Ig) genes among the survivors of three clones. Finally, myosins and Igs were identified as co-expression modules which were positively or negatively correlated to CaHV viral loads respectively. CONCLUSIONS: Our results revealed the common and distinct gene expression changes in immune and circulatory system in the survivors of three gibel carp gynogenetic clones with different CaHV resistances. The current study represents a paradigm of differential innate and adaptive immune reactions in teleost, and will be beneficial to the disease-resistance breeding of gibel carp. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5777-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-65405552019-06-03 Differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge Lu, Wei-Jia Gao, Fan-Xiang Wang, Yang Zhang, Qi-Ya Li, Zhi Zhang, Xiao-Juan Zhou, Li Gui, Jian-Fang BMC Genomics Research Article BACKGROUND: Accompanied with rapid growth and high density aquaculture, gibel carp has been seriously threatened by Carassius auratus herpesvirus (CaHV) since 2012. In previous study, distinct CaHV resistances and immune responses were revealed in the diseased individuals of three gibel carp gynogenetic clones (A(+), F and H). However, little is known about the gene expression changes in the survivors after CaHV challenge, particularly their differences of innate and adaptive immune system between susceptible clone and resistant clone. RESULTS: We firstly confirmed the CaHV carrier state in the survivors of three gibel carp clones after CaHV challenge by evaluating the abundances of five CaHV genes. The assay of viral loads indicated the resistant clone H possessed not only stronger resistance but also higher tolerance to CaHV. Then, 2818, 4047 and 3323 differentially expressed unigenes (DEUs) were screened from the head-kidney transcriptome profiles of survivors compared with controls from clone A(+), F and H. GO and KEGG analysis suggested that a persistent immune response might sustain in resistant clone H and F, while susceptible clone A(+) had a long-term impact on the circulatory system which was consistent with the major symptoms of bleeding caused by CaHV. Among the top 30 enriched pathways of specifically up-regulated DEUs in respective clones, 26, 7 and 15 pathways in clone H, F and A(+) were associated with infections, diseases, or immune-related pathways respectively. In addition, 20 pathways in clone F belonged to “metabolism” or “biogenesis”, and 7 pathways involved in “circulatory system” were enriched in clone A(+). Significantly, we revealed the differential expression changes of IFN system genes and immunoglobulin (Ig) genes among the survivors of three clones. Finally, myosins and Igs were identified as co-expression modules which were positively or negatively correlated to CaHV viral loads respectively. CONCLUSIONS: Our results revealed the common and distinct gene expression changes in immune and circulatory system in the survivors of three gibel carp gynogenetic clones with different CaHV resistances. The current study represents a paradigm of differential innate and adaptive immune reactions in teleost, and will be beneficial to the disease-resistance breeding of gibel carp. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5777-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-28 /pmc/articles/PMC6540555/ /pubmed/31138127 http://dx.doi.org/10.1186/s12864-019-5777-z Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Lu, Wei-Jia
Gao, Fan-Xiang
Wang, Yang
Zhang, Qi-Ya
Li, Zhi
Zhang, Xiao-Juan
Zhou, Li
Gui, Jian-Fang
Differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge
title Differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge
title_full Differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge
title_fullStr Differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge
title_full_unstemmed Differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge
title_short Differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge
title_sort differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6540555/
https://www.ncbi.nlm.nih.gov/pubmed/31138127
http://dx.doi.org/10.1186/s12864-019-5777-z
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