MicroRNA gga-miR-10a-mediated transcriptional regulation of the immune genes in necrotic enteritis afflicted chickens
miRNAs are involved in both adaptive and innate immune systems of host animals; and play important roles in many immune-related pathways. The systemic biological roles of gga-miR-10a-5p chicken microRNA on immune response were investigated in two necrotic enteritis (NE) induced chicken lines, Marek&...
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Veröffentlicht in: | Developmental and comparative immunology 2020-01, Vol.102, p.103472-103472, Article 103472 |
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creator | Pham, Thu Thao Ban, Jihye Lee, Kyungbaek Hong, Yeojin Lee, Jiae Truong, Anh Duc Lillehoj, Hyun S. Hong, Yeong Ho |
description | miRNAs are involved in both adaptive and innate immune systems of host animals; and play important roles in many immune-related pathways. The systemic biological roles of gga-miR-10a-5p chicken microRNA on immune response were investigated in two necrotic enteritis (NE) induced chicken lines, Marek's disease (MD) resistant (line 6.3) and susceptible (line 7.2). We determined the expression patterns of gga-miR-10a in the intestinal mucosal layer of chickens upon NE induction, and identified the target genes (MyD88, and SKP1) related to the host immune response to pathogens. We found that gga-miR-10a expression in the intestinal mucosal layer of MD-resistant chicken line 6.3 gga-miR-10a was significantly down-regulated (p |
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•Gga-miR-10a significantly down-regulated in the resistant line 6.3 compared to the susceptible line 7.2 induced by NE.•Gga-miR-10a directly suppressed the expression level of its target gene MyD88.•Gga-miR-10a inhibited the expression of the signaling molecules as the downstream of MyD88-dependent pathway.•Gga-miR-10a indirectly repressed Th1, and pro-inflammatory cytokine production.</description><identifier>ISSN: 0145-305X</identifier><identifier>EISSN: 1879-0089</identifier><identifier>DOI: 10.1016/j.dci.2019.103472</identifier><identifier>PMID: 31437523</identifier><language>eng</language><publisher>United States: Elsevier Ltd</publisher><subject>3' Untranslated regions ; Adaptive systems ; Animals ; Biotechnology ; Chicken ; Chickens ; Cytokines ; Domestic animals ; Enteritis ; Gene expression ; Gene regulation ; Genes ; IL-1β ; Immune response ; Immune system ; Inflammation ; Innate immunity ; Interleukin 12 ; Intestine ; Macrophages ; Marek's disease ; MicroRNAs ; miR-10a ; miRNA ; Mucosa ; MyD88 ; MyD88 protein ; Necrotic enteritis ; Poultry ; Reporter gene ; Ribonucleic acid ; RNA ; Signal transduction ; Signaling ; TAK1 protein ; Target recognition ; Toll-like receptor signaling pathway ; Toll-like receptors ; TRAF6 protein ; Transcription ; Translation ; γ-Interferon</subject><ispartof>Developmental and comparative immunology, 2020-01, Vol.102, p.103472-103472, Article 103472</ispartof><rights>2019 Elsevier Ltd</rights><rights>Copyright © 2019 Elsevier Ltd. All rights reserved.</rights><rights>Copyright Elsevier Science Ltd. Jan 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c424t-bb920745834743d79ff325188bab8792949d8a4499d5942fef5ea9c08818a9933</citedby><cites>FETCH-LOGICAL-c424t-bb920745834743d79ff325188bab8792949d8a4499d5942fef5ea9c08818a9933</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.dci.2019.103472$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31437523$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pham, Thu Thao</creatorcontrib><creatorcontrib>Ban, Jihye</creatorcontrib><creatorcontrib>Lee, Kyungbaek</creatorcontrib><creatorcontrib>Hong, Yeojin</creatorcontrib><creatorcontrib>Lee, Jiae</creatorcontrib><creatorcontrib>Truong, Anh Duc</creatorcontrib><creatorcontrib>Lillehoj, Hyun S.</creatorcontrib><creatorcontrib>Hong, Yeong Ho</creatorcontrib><title>MicroRNA gga-miR-10a-mediated transcriptional regulation of the immune genes in necrotic enteritis afflicted chickens</title><title>Developmental and comparative immunology</title><addtitle>Dev Comp Immunol</addtitle><description>miRNAs are involved in both adaptive and innate immune systems of host animals; and play important roles in many immune-related pathways. The systemic biological roles of gga-miR-10a-5p chicken microRNA on immune response were investigated in two necrotic enteritis (NE) induced chicken lines, Marek's disease (MD) resistant (line 6.3) and susceptible (line 7.2). We determined the expression patterns of gga-miR-10a in the intestinal mucosal layer of chickens upon NE induction, and identified the target genes (MyD88, and SKP1) related to the host immune response to pathogens. We found that gga-miR-10a expression in the intestinal mucosal layer of MD-resistant chicken line 6.3 gga-miR-10a was significantly down-regulated (p < 0.01) during NE. Overexpression analysis of gga-miR-10a and reporter gene analysis using a wild- or mutant-type MyD88 3′ untranslated region (3′ UTR)-luciferase construct in chicken macrophage cell line HD11 and chicken fibroblast cell line OU2 showed that gga-miR-10a acted as a direct translational repressor of MyD88 by targeting the 3′ UTR of this gene. Furthermore, miR-10a indirectly negatively influenced the expression of signaling molecules related to the MyD88-dependent pathway, including TRAF6, TAK1, and NF-κB1 at both transcriptional and translational levels. Downstream of the MyD88-dependent pathway, several proinflammatory cytokines such as IL-1β, IFN-γ, IL-12p40, TNFSF15, and LITAF were down-regulated by overexpression of gga-miR-10a. These results suggest that gga-miR-10a is an important regulator of the Toll-like receptor signaling pathway. The findings of this study improve our understanding of the biological functions of miR-10a and the mechanisms underlying the TLR signaling pathway upon NE afflicted chickens, as well improving the overall understanding of the immune system function in domestic animals.
•Gga-miR-10a significantly down-regulated in the resistant line 6.3 compared to the susceptible line 7.2 induced by NE.•Gga-miR-10a directly suppressed the expression level of its target gene MyD88.•Gga-miR-10a inhibited the expression of the signaling molecules as the downstream of MyD88-dependent pathway.•Gga-miR-10a indirectly repressed Th1, and pro-inflammatory cytokine production.</description><subject>3' Untranslated regions</subject><subject>Adaptive systems</subject><subject>Animals</subject><subject>Biotechnology</subject><subject>Chicken</subject><subject>Chickens</subject><subject>Cytokines</subject><subject>Domestic animals</subject><subject>Enteritis</subject><subject>Gene expression</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>IL-1β</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Inflammation</subject><subject>Innate immunity</subject><subject>Interleukin 12</subject><subject>Intestine</subject><subject>Macrophages</subject><subject>Marek's disease</subject><subject>MicroRNAs</subject><subject>miR-10a</subject><subject>miRNA</subject><subject>Mucosa</subject><subject>MyD88</subject><subject>MyD88 protein</subject><subject>Necrotic enteritis</subject><subject>Poultry</subject><subject>Reporter gene</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>TAK1 protein</subject><subject>Target recognition</subject><subject>Toll-like receptor signaling pathway</subject><subject>Toll-like receptors</subject><subject>TRAF6 protein</subject><subject>Transcription</subject><subject>Translation</subject><subject>γ-Interferon</subject><issn>0145-305X</issn><issn>1879-0089</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp9kU9rFEEQxRsxmE30A3iRBi9eZu2_O914CiEaISYQInhrenpqNr3O9KzdPYLf3lo2evBgXYqCX73i1SPkNWdrzvjm_W7dh7gWjFucpWrFM7LiprUNY8Y-JyvGlW4k099OyVkpO4ZlOHtBTiVXstVCrsjyJYY8399e0O3WN1O8bzjDDn30FXpas08l5LivcU5-pBm2y-gPA50HWh-BxmlaEtAtJCg0JpoA9WoMFFKFHGss1A_DGMNBLjzG8B1SeUlOBj8WePXUz8nXj1cPl9fNzd2nz5cXN01QQtWm66xgrdIGvSnZt3YYpNDcmM53aFNYZXvjlbK211aJAQYN3gZmDDfeWinPybuj7j7PPxYo1U2xBBhHn2BeihPCML3RylhE3_6D7uYlo2ekJMermm0MUvxIoclSMgxun-Pk8y_HmTtk4nYOM3GHTNwxE9x586S8dPjYvxt_QkDgwxEAfMXPCNmVECEFDCFDqK6f43_kfwP1zJty</recordid><startdate>202001</startdate><enddate>202001</enddate><creator>Pham, Thu Thao</creator><creator>Ban, Jihye</creator><creator>Lee, Kyungbaek</creator><creator>Hong, Yeojin</creator><creator>Lee, Jiae</creator><creator>Truong, Anh Duc</creator><creator>Lillehoj, Hyun S.</creator><creator>Hong, Yeong Ho</creator><general>Elsevier Ltd</general><general>Elsevier Science Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7T5</scope><scope>C1K</scope><scope>H94</scope><scope>7X8</scope></search><sort><creationdate>202001</creationdate><title>MicroRNA gga-miR-10a-mediated transcriptional regulation of the immune genes in necrotic enteritis afflicted chickens</title><author>Pham, Thu Thao ; Ban, Jihye ; Lee, Kyungbaek ; Hong, Yeojin ; Lee, Jiae ; Truong, Anh Duc ; Lillehoj, Hyun S. ; Hong, Yeong Ho</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c424t-bb920745834743d79ff325188bab8792949d8a4499d5942fef5ea9c08818a9933</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>3' Untranslated regions</topic><topic>Adaptive systems</topic><topic>Animals</topic><topic>Biotechnology</topic><topic>Chicken</topic><topic>Chickens</topic><topic>Cytokines</topic><topic>Domestic animals</topic><topic>Enteritis</topic><topic>Gene expression</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>IL-1β</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Inflammation</topic><topic>Innate immunity</topic><topic>Interleukin 12</topic><topic>Intestine</topic><topic>Macrophages</topic><topic>Marek's disease</topic><topic>MicroRNAs</topic><topic>miR-10a</topic><topic>miRNA</topic><topic>Mucosa</topic><topic>MyD88</topic><topic>MyD88 protein</topic><topic>Necrotic enteritis</topic><topic>Poultry</topic><topic>Reporter gene</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Signal transduction</topic><topic>Signaling</topic><topic>TAK1 protein</topic><topic>Target recognition</topic><topic>Toll-like receptor signaling pathway</topic><topic>Toll-like receptors</topic><topic>TRAF6 protein</topic><topic>Transcription</topic><topic>Translation</topic><topic>γ-Interferon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pham, Thu Thao</creatorcontrib><creatorcontrib>Ban, Jihye</creatorcontrib><creatorcontrib>Lee, Kyungbaek</creatorcontrib><creatorcontrib>Hong, Yeojin</creatorcontrib><creatorcontrib>Lee, Jiae</creatorcontrib><creatorcontrib>Truong, Anh Duc</creatorcontrib><creatorcontrib>Lillehoj, Hyun S.</creatorcontrib><creatorcontrib>Hong, Yeong Ho</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Developmental and comparative immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pham, Thu Thao</au><au>Ban, Jihye</au><au>Lee, Kyungbaek</au><au>Hong, Yeojin</au><au>Lee, Jiae</au><au>Truong, Anh Duc</au><au>Lillehoj, Hyun S.</au><au>Hong, Yeong Ho</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MicroRNA gga-miR-10a-mediated transcriptional regulation of the immune genes in necrotic enteritis afflicted chickens</atitle><jtitle>Developmental and comparative immunology</jtitle><addtitle>Dev Comp Immunol</addtitle><date>2020-01</date><risdate>2020</risdate><volume>102</volume><spage>103472</spage><epage>103472</epage><pages>103472-103472</pages><artnum>103472</artnum><issn>0145-305X</issn><eissn>1879-0089</eissn><abstract>miRNAs are involved in both adaptive and innate immune systems of host animals; and play important roles in many immune-related pathways. The systemic biological roles of gga-miR-10a-5p chicken microRNA on immune response were investigated in two necrotic enteritis (NE) induced chicken lines, Marek's disease (MD) resistant (line 6.3) and susceptible (line 7.2). We determined the expression patterns of gga-miR-10a in the intestinal mucosal layer of chickens upon NE induction, and identified the target genes (MyD88, and SKP1) related to the host immune response to pathogens. We found that gga-miR-10a expression in the intestinal mucosal layer of MD-resistant chicken line 6.3 gga-miR-10a was significantly down-regulated (p < 0.01) during NE. Overexpression analysis of gga-miR-10a and reporter gene analysis using a wild- or mutant-type MyD88 3′ untranslated region (3′ UTR)-luciferase construct in chicken macrophage cell line HD11 and chicken fibroblast cell line OU2 showed that gga-miR-10a acted as a direct translational repressor of MyD88 by targeting the 3′ UTR of this gene. Furthermore, miR-10a indirectly negatively influenced the expression of signaling molecules related to the MyD88-dependent pathway, including TRAF6, TAK1, and NF-κB1 at both transcriptional and translational levels. Downstream of the MyD88-dependent pathway, several proinflammatory cytokines such as IL-1β, IFN-γ, IL-12p40, TNFSF15, and LITAF were down-regulated by overexpression of gga-miR-10a. These results suggest that gga-miR-10a is an important regulator of the Toll-like receptor signaling pathway. The findings of this study improve our understanding of the biological functions of miR-10a and the mechanisms underlying the TLR signaling pathway upon NE afflicted chickens, as well improving the overall understanding of the immune system function in domestic animals.
•Gga-miR-10a significantly down-regulated in the resistant line 6.3 compared to the susceptible line 7.2 induced by NE.•Gga-miR-10a directly suppressed the expression level of its target gene MyD88.•Gga-miR-10a inhibited the expression of the signaling molecules as the downstream of MyD88-dependent pathway.•Gga-miR-10a indirectly repressed Th1, and pro-inflammatory cytokine production.</abstract><cop>United States</cop><pub>Elsevier Ltd</pub><pmid>31437523</pmid><doi>10.1016/j.dci.2019.103472</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 3' Untranslated regions Adaptive systems Animals Biotechnology Chicken Chickens Cytokines Domestic animals Enteritis Gene expression Gene regulation Genes IL-1β Immune response Immune system Inflammation Innate immunity Interleukin 12 Intestine Macrophages Marek's disease MicroRNAs miR-10a miRNA Mucosa MyD88 MyD88 protein Necrotic enteritis Poultry Reporter gene Ribonucleic acid RNA Signal transduction Signaling TAK1 protein Target recognition Toll-like receptor signaling pathway Toll-like receptors TRAF6 protein Transcription Translation γ-Interferon |
title | MicroRNA gga-miR-10a-mediated transcriptional regulation of the immune genes in necrotic enteritis afflicted chickens |
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