Chicken gga-miR-1306-5p targets Tollip and plays an important role in host response against Salmonella enteritidis infection

Abstract Background Increasing evidence indicates that microRNAs (miRNAs) are involved in inflammatory response and immune regulation following pathogen invasion. The purpose of this study was to elucidate the roles played by Gallus gallus microRNA-1306-5p (gga-miR-1306-5p) in host responses against...

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Main Authors: Weiwei Sun, Ranran Liu, Peng Li, Qinghe Li, Huanxian Cui, Maiqing Zheng, Jie Wen, Guiping Zhao
Format: Article
Language:English
Published: BMC 2019-07-01
Series:Journal of Animal Science and Biotechnology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40104-019-0365-2
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author Weiwei Sun
Ranran Liu
Peng Li
Qinghe Li
Huanxian Cui
Maiqing Zheng
Jie Wen
Guiping Zhao
author_facet Weiwei Sun
Ranran Liu
Peng Li
Qinghe Li
Huanxian Cui
Maiqing Zheng
Jie Wen
Guiping Zhao
author_sort Weiwei Sun
collection DOAJ
description Abstract Background Increasing evidence indicates that microRNAs (miRNAs) are involved in inflammatory response and immune regulation following pathogen invasion. The purpose of this study was to elucidate the roles played by Gallus gallus microRNA-1306-5p (gga-miR-1306-5p) in host responses against potential invasion by Salmonella enteritidis (SE) in chickens and the underlying mechanisms. Results In present study, the expression levels of gga-miR-1306-5p were determined in both tissues and HD11 cells. The results showed that gga-miR-1306-5p was significantly increased following SE infection or lipopolysaccharide (LPS) stimulation. The dual luciferase reporter assay further validated that gga-miR-1306-5p targeted the Toll-interacting protein (Tollip), and thereby participated in the regulation of immune response against SE or LPS stimulation through binding with the 3′-untranslated region (3’UTR) of Tollip. Additionally, the expression of Tollip was significantly blocked by over-expressed gga-miR-1306-5p. The underlying mechanisms by which gga-miR-1306-5p modulated the production of pro-inflammatory cytokines were also investigated. Molecular biological assays demonstrated that overexpression of gga-miR-1306-5p promoted the production of pro-inflammatory mediators, including NF-κB, TNF-α, IL-6, and IL-1β, which produced effects similar to those of Tollip knockdown. Conclusions Taken together, gga-miR-1306-5p induced by SE or LPS, regulates the immune response by inhibiting Tollip, which activates the production of inflammatory cytokines. This study has provided the first direct evidence that gga-miR-1306-5p targets Tollip, and is involved in the host response against SE.
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spelling doaj.art-5eb4818bc8fe4ca087bb2d5e2867e3cd2022-12-21T18:41:16ZengBMCJournal of Animal Science and Biotechnology2049-18912019-07-0110111110.1186/s40104-019-0365-2Chicken gga-miR-1306-5p targets Tollip and plays an important role in host response against Salmonella enteritidis infectionWeiwei Sun0Ranran Liu1Peng Li2Qinghe Li3Huanxian Cui4Maiqing Zheng5Jie Wen6Guiping Zhao7Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, State Key Laboratory of Animal NutritionInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, State Key Laboratory of Animal NutritionInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, State Key Laboratory of Animal NutritionInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, State Key Laboratory of Animal NutritionInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, State Key Laboratory of Animal NutritionInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, State Key Laboratory of Animal NutritionInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, State Key Laboratory of Animal NutritionInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, State Key Laboratory of Animal NutritionAbstract Background Increasing evidence indicates that microRNAs (miRNAs) are involved in inflammatory response and immune regulation following pathogen invasion. The purpose of this study was to elucidate the roles played by Gallus gallus microRNA-1306-5p (gga-miR-1306-5p) in host responses against potential invasion by Salmonella enteritidis (SE) in chickens and the underlying mechanisms. Results In present study, the expression levels of gga-miR-1306-5p were determined in both tissues and HD11 cells. The results showed that gga-miR-1306-5p was significantly increased following SE infection or lipopolysaccharide (LPS) stimulation. The dual luciferase reporter assay further validated that gga-miR-1306-5p targeted the Toll-interacting protein (Tollip), and thereby participated in the regulation of immune response against SE or LPS stimulation through binding with the 3′-untranslated region (3’UTR) of Tollip. Additionally, the expression of Tollip was significantly blocked by over-expressed gga-miR-1306-5p. The underlying mechanisms by which gga-miR-1306-5p modulated the production of pro-inflammatory cytokines were also investigated. Molecular biological assays demonstrated that overexpression of gga-miR-1306-5p promoted the production of pro-inflammatory mediators, including NF-κB, TNF-α, IL-6, and IL-1β, which produced effects similar to those of Tollip knockdown. Conclusions Taken together, gga-miR-1306-5p induced by SE or LPS, regulates the immune response by inhibiting Tollip, which activates the production of inflammatory cytokines. This study has provided the first direct evidence that gga-miR-1306-5p targets Tollip, and is involved in the host response against SE.http://link.springer.com/article/10.1186/s40104-019-0365-2gga-miR-1306-5pLPSPro-inflammatory cytokineSalmonella enteritidisTollip
spellingShingle Weiwei Sun
Ranran Liu
Peng Li
Qinghe Li
Huanxian Cui
Maiqing Zheng
Jie Wen
Guiping Zhao
Chicken gga-miR-1306-5p targets Tollip and plays an important role in host response against Salmonella enteritidis infection
Journal of Animal Science and Biotechnology
gga-miR-1306-5p
LPS
Pro-inflammatory cytokine
Salmonella enteritidis
Tollip
title Chicken gga-miR-1306-5p targets Tollip and plays an important role in host response against Salmonella enteritidis infection
title_full Chicken gga-miR-1306-5p targets Tollip and plays an important role in host response against Salmonella enteritidis infection
title_fullStr Chicken gga-miR-1306-5p targets Tollip and plays an important role in host response against Salmonella enteritidis infection
title_full_unstemmed Chicken gga-miR-1306-5p targets Tollip and plays an important role in host response against Salmonella enteritidis infection
title_short Chicken gga-miR-1306-5p targets Tollip and plays an important role in host response against Salmonella enteritidis infection
title_sort chicken gga mir 1306 5p targets tollip and plays an important role in host response against salmonella enteritidis infection
topic gga-miR-1306-5p
LPS
Pro-inflammatory cytokine
Salmonella enteritidis
Tollip
url http://link.springer.com/article/10.1186/s40104-019-0365-2
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