Long noncoding RNA profiling reveals that LncRNA BTN3A2 inhibits the host inflammatory response to Eimeria tenella infection in chickens

Coccidiosis is a widespread parasitic disease that causes serious economic losses to the poultry industry every year. Long noncoding RNAs (lncRNAs) play important roles in transcriptional regulation and are involved in a variety of diseases and immune responses. However, the lncRNAs associated with...

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Main Authors: Hailiang Yu, Changhao Mi, Qi Wang, Guojun Dai, Tao Zhang, Genxi Zhang, Kaizhou Xie, Zhenhua Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2022.891001/full
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author Hailiang Yu
Changhao Mi
Qi Wang
Guojun Dai
Tao Zhang
Genxi Zhang
Kaizhou Xie
Zhenhua Zhao
author_facet Hailiang Yu
Changhao Mi
Qi Wang
Guojun Dai
Tao Zhang
Genxi Zhang
Kaizhou Xie
Zhenhua Zhao
author_sort Hailiang Yu
collection DOAJ
description Coccidiosis is a widespread parasitic disease that causes serious economic losses to the poultry industry every year. Long noncoding RNAs (lncRNAs) play important roles in transcriptional regulation and are involved in a variety of diseases and immune responses. However, the lncRNAs associated with Eimeria tenella (E. tenella) resistance have not been identified in chickens. In addition, the expression profiles and functions of lncRNAs during E. tenella infection remain unclear. In the present study, high-throughput sequencing was applied to identify lncRNAs in chicken cecal tissues from control (JC), resistant (JR), and susceptible (JS) groups on day 4.5 post-infection (pi), and functional tests were performed. A total of 564 lncRNAs were differentially expressed, including 263 lncRNAs between the JS and JC groups, 192 between the JR and JS groups, and 109 between the JR and JC groups. Functional analyses indicated that these differentially expressed lncRNAs were involved in pathways related to E. tenella infection, including the NF-kappa B signaling, B cell receptor signaling and natural killer cell-mediated cytotoxicity pathways. Moreover, through cis regulation network analysis of the differentially expressed lncRNAs, we found that a novel lncRNA termed lncRNA BTN3A2 was significantly increased in both cecum tissue and DF-1 cells after coccidia infection or sporozoite stimulation. Functional test data showed that the overexpression of lncRNA BTN3A2 reduced the production of inflammatory cytokines, including IL-6, IL-1β, TNF-α and IL-8, while lncRNA BTN3A2 knockdown promoted the production of these inflammatory cytokines. Taken together, this study identify the differentially expressed lncRNAs during E. tenella infection in chickens for the first time and provide the direct evidence that lncRNA BTN3A2 regulates the host immune response to coccidia infection.
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spelling doaj.art-697bfb6541a44613b1e20552f32788612022-12-22T04:02:49ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-08-011310.3389/fimmu.2022.891001891001Long noncoding RNA profiling reveals that LncRNA BTN3A2 inhibits the host inflammatory response to Eimeria tenella infection in chickensHailiang Yu0Changhao Mi1Qi Wang2Guojun Dai3Tao Zhang4Genxi Zhang5Kaizhou Xie6Zhenhua Zhao7College of Animal Science and Technology, Yangzhou University, Yangzhou, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou, ChinaPoultry Institute, Chinese Academy of Agricultural Sciences, Yangzhou, ChinaCoccidiosis is a widespread parasitic disease that causes serious economic losses to the poultry industry every year. Long noncoding RNAs (lncRNAs) play important roles in transcriptional regulation and are involved in a variety of diseases and immune responses. However, the lncRNAs associated with Eimeria tenella (E. tenella) resistance have not been identified in chickens. In addition, the expression profiles and functions of lncRNAs during E. tenella infection remain unclear. In the present study, high-throughput sequencing was applied to identify lncRNAs in chicken cecal tissues from control (JC), resistant (JR), and susceptible (JS) groups on day 4.5 post-infection (pi), and functional tests were performed. A total of 564 lncRNAs were differentially expressed, including 263 lncRNAs between the JS and JC groups, 192 between the JR and JS groups, and 109 between the JR and JC groups. Functional analyses indicated that these differentially expressed lncRNAs were involved in pathways related to E. tenella infection, including the NF-kappa B signaling, B cell receptor signaling and natural killer cell-mediated cytotoxicity pathways. Moreover, through cis regulation network analysis of the differentially expressed lncRNAs, we found that a novel lncRNA termed lncRNA BTN3A2 was significantly increased in both cecum tissue and DF-1 cells after coccidia infection or sporozoite stimulation. Functional test data showed that the overexpression of lncRNA BTN3A2 reduced the production of inflammatory cytokines, including IL-6, IL-1β, TNF-α and IL-8, while lncRNA BTN3A2 knockdown promoted the production of these inflammatory cytokines. Taken together, this study identify the differentially expressed lncRNAs during E. tenella infection in chickens for the first time and provide the direct evidence that lncRNA BTN3A2 regulates the host immune response to coccidia infection.https://www.frontiersin.org/articles/10.3389/fimmu.2022.891001/fullchickenE. tenellalncRNA BTN3A2inflammatory responsehost resistance
spellingShingle Hailiang Yu
Changhao Mi
Qi Wang
Guojun Dai
Tao Zhang
Genxi Zhang
Kaizhou Xie
Zhenhua Zhao
Long noncoding RNA profiling reveals that LncRNA BTN3A2 inhibits the host inflammatory response to Eimeria tenella infection in chickens
Frontiers in Immunology
chicken
E. tenella
lncRNA BTN3A2
inflammatory response
host resistance
title Long noncoding RNA profiling reveals that LncRNA BTN3A2 inhibits the host inflammatory response to Eimeria tenella infection in chickens
title_full Long noncoding RNA profiling reveals that LncRNA BTN3A2 inhibits the host inflammatory response to Eimeria tenella infection in chickens
title_fullStr Long noncoding RNA profiling reveals that LncRNA BTN3A2 inhibits the host inflammatory response to Eimeria tenella infection in chickens
title_full_unstemmed Long noncoding RNA profiling reveals that LncRNA BTN3A2 inhibits the host inflammatory response to Eimeria tenella infection in chickens
title_short Long noncoding RNA profiling reveals that LncRNA BTN3A2 inhibits the host inflammatory response to Eimeria tenella infection in chickens
title_sort long noncoding rna profiling reveals that lncrna btn3a2 inhibits the host inflammatory response to eimeria tenella infection in chickens
topic chicken
E. tenella
lncRNA BTN3A2
inflammatory response
host resistance
url https://www.frontiersin.org/articles/10.3389/fimmu.2022.891001/full
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