Identification of Potential Immune-Related circRNA–miRNA–mRNA Regulatory Network in Intestine of Paralichthys olivaceus During Edwardsiella tarda Infection

Olive flounder (Paralichthys olivaceus) is an important economical flatfish in Japan, Korea, and China, but its production has been greatly threatened by disease outbreaks. In this research, we aimed to explore the immune responsive mechanism of P. olivaceus against Edwardsiella tarda infection by p...

Full description

Bibliographic Details
Main Authors: Yunji Xiu, Guangpeng Jiang, Shun Zhou, Jing Diao, Hongjun Liu, Baofeng Su, Chao Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-08-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2019.00731/full
_version_ 1818293387574378496
author Yunji Xiu
Yunji Xiu
Guangpeng Jiang
Shun Zhou
Jing Diao
Hongjun Liu
Baofeng Su
Chao Li
author_facet Yunji Xiu
Yunji Xiu
Guangpeng Jiang
Shun Zhou
Jing Diao
Hongjun Liu
Baofeng Su
Chao Li
author_sort Yunji Xiu
collection DOAJ
description Olive flounder (Paralichthys olivaceus) is an important economical flatfish in Japan, Korea, and China, but its production has been greatly threatened by disease outbreaks. In this research, we aimed to explore the immune responsive mechanism of P. olivaceus against Edwardsiella tarda infection by profiling the expression of circRNA, miRNA, and mRNA by RNA-seq and constructing a regulatory circular circRNA–miRNA–mRNA network. Illumina sequencing of samples from normal control (H0), 2 h (H2), 8 h (H8), and 12 h (H12) post-challenge was conducted. Differentially expressed (DE) circRNA (DE–circRNAs), miRNAs (DE–miRNAs), and mRNAs [differential expression genes (DEGs)] between challenge and control groups were identified, resulting in a total of 62 DE–circRNAs, 39 DE–miRNAs, and 3,011 DEGs. Based on the differentially expressed gene results, miRNA target interactions (circRNA–miRNA pairs and miRNA–mRNA pairs) were predicted by MiRanda software. Once these paired were combined, a preliminary circRNA–miRNA–mRNA network was generated with 198 circRNA–miRNA edges and 3,873 miRNA–mRNA edges, including 44 DE–circRNAs, 32 DE–miRNAs, and 1,774 DEGs. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis was performed to evaluate the function of the DEGs in this network, and we focused and identified two important intestinal immune pathways (herpes simplex infection and intestinal immune network for IgA production) that showed statistical significance between the challenge and control groups. Furthermore, three critical DEGs (nectin2, MHC II α-chain, and MHC II β-chain) were identified, mapped into the preliminary circRNA–miRNA–mRNA network, and new circRNA–miRNA–mRNA regulatory networks were constructed. In conclusion, we, for the first time, identified circRNA–miRNA–mRNA network from P. olivaceus in the pathogenesis of E. tarda and provided valuable resources for further analyses of the molecular mechanisms and signaling networks.
first_indexed 2024-12-13T03:15:03Z
format Article
id doaj.art-7e16bf6cc85d4e44a9cf33f9bf163c07
institution Directory Open Access Journal
issn 1664-8021
language English
last_indexed 2024-12-13T03:15:03Z
publishDate 2019-08-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Genetics
spelling doaj.art-7e16bf6cc85d4e44a9cf33f9bf163c072022-12-22T00:01:30ZengFrontiers Media S.A.Frontiers in Genetics1664-80212019-08-011010.3389/fgene.2019.00731441798Identification of Potential Immune-Related circRNA–miRNA–mRNA Regulatory Network in Intestine of Paralichthys olivaceus During Edwardsiella tarda InfectionYunji Xiu0Yunji Xiu1Guangpeng Jiang2Shun Zhou3Jing Diao4Hongjun Liu5Baofeng Su6Chao Li7School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, ChinaShandong Key Laboratory of Disease Control in Mariculture, Marine Biology Institute of Shandong Province, Qingdao, ChinaSchool of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, ChinaSchool of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, ChinaShandong Key Laboratory of Disease Control in Mariculture, Marine Biology Institute of Shandong Province, Qingdao, ChinaShandong Key Laboratory of Disease Control in Mariculture, Marine Biology Institute of Shandong Province, Qingdao, ChinaSchool of Fisheries, Aquaculture and Aquatic Sciences, Auburn University, Auburn, AL, United StatessSchool of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, ChinaOlive flounder (Paralichthys olivaceus) is an important economical flatfish in Japan, Korea, and China, but its production has been greatly threatened by disease outbreaks. In this research, we aimed to explore the immune responsive mechanism of P. olivaceus against Edwardsiella tarda infection by profiling the expression of circRNA, miRNA, and mRNA by RNA-seq and constructing a regulatory circular circRNA–miRNA–mRNA network. Illumina sequencing of samples from normal control (H0), 2 h (H2), 8 h (H8), and 12 h (H12) post-challenge was conducted. Differentially expressed (DE) circRNA (DE–circRNAs), miRNAs (DE–miRNAs), and mRNAs [differential expression genes (DEGs)] between challenge and control groups were identified, resulting in a total of 62 DE–circRNAs, 39 DE–miRNAs, and 3,011 DEGs. Based on the differentially expressed gene results, miRNA target interactions (circRNA–miRNA pairs and miRNA–mRNA pairs) were predicted by MiRanda software. Once these paired were combined, a preliminary circRNA–miRNA–mRNA network was generated with 198 circRNA–miRNA edges and 3,873 miRNA–mRNA edges, including 44 DE–circRNAs, 32 DE–miRNAs, and 1,774 DEGs. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis was performed to evaluate the function of the DEGs in this network, and we focused and identified two important intestinal immune pathways (herpes simplex infection and intestinal immune network for IgA production) that showed statistical significance between the challenge and control groups. Furthermore, three critical DEGs (nectin2, MHC II α-chain, and MHC II β-chain) were identified, mapped into the preliminary circRNA–miRNA–mRNA network, and new circRNA–miRNA–mRNA regulatory networks were constructed. In conclusion, we, for the first time, identified circRNA–miRNA–mRNA network from P. olivaceus in the pathogenesis of E. tarda and provided valuable resources for further analyses of the molecular mechanisms and signaling networks.https://www.frontiersin.org/article/10.3389/fgene.2019.00731/fullcircRNAmiRNAmRNAcircRNA–miRNA–mRNA networkimmune responseParalichthys olivaceus
spellingShingle Yunji Xiu
Yunji Xiu
Guangpeng Jiang
Shun Zhou
Jing Diao
Hongjun Liu
Baofeng Su
Chao Li
Identification of Potential Immune-Related circRNA–miRNA–mRNA Regulatory Network in Intestine of Paralichthys olivaceus During Edwardsiella tarda Infection
Frontiers in Genetics
circRNA
miRNA
mRNA
circRNA–miRNA–mRNA network
immune response
Paralichthys olivaceus
title Identification of Potential Immune-Related circRNA–miRNA–mRNA Regulatory Network in Intestine of Paralichthys olivaceus During Edwardsiella tarda Infection
title_full Identification of Potential Immune-Related circRNA–miRNA–mRNA Regulatory Network in Intestine of Paralichthys olivaceus During Edwardsiella tarda Infection
title_fullStr Identification of Potential Immune-Related circRNA–miRNA–mRNA Regulatory Network in Intestine of Paralichthys olivaceus During Edwardsiella tarda Infection
title_full_unstemmed Identification of Potential Immune-Related circRNA–miRNA–mRNA Regulatory Network in Intestine of Paralichthys olivaceus During Edwardsiella tarda Infection
title_short Identification of Potential Immune-Related circRNA–miRNA–mRNA Regulatory Network in Intestine of Paralichthys olivaceus During Edwardsiella tarda Infection
title_sort identification of potential immune related circrna mirna mrna regulatory network in intestine of paralichthys olivaceus during edwardsiella tarda infection
topic circRNA
miRNA
mRNA
circRNA–miRNA–mRNA network
immune response
Paralichthys olivaceus
url https://www.frontiersin.org/article/10.3389/fgene.2019.00731/full
work_keys_str_mv AT yunjixiu identificationofpotentialimmunerelatedcircrnamirnamrnaregulatorynetworkinintestineofparalichthysolivaceusduringedwardsiellatardainfection
AT yunjixiu identificationofpotentialimmunerelatedcircrnamirnamrnaregulatorynetworkinintestineofparalichthysolivaceusduringedwardsiellatardainfection
AT guangpengjiang identificationofpotentialimmunerelatedcircrnamirnamrnaregulatorynetworkinintestineofparalichthysolivaceusduringedwardsiellatardainfection
AT shunzhou identificationofpotentialimmunerelatedcircrnamirnamrnaregulatorynetworkinintestineofparalichthysolivaceusduringedwardsiellatardainfection
AT jingdiao identificationofpotentialimmunerelatedcircrnamirnamrnaregulatorynetworkinintestineofparalichthysolivaceusduringedwardsiellatardainfection
AT hongjunliu identificationofpotentialimmunerelatedcircrnamirnamrnaregulatorynetworkinintestineofparalichthysolivaceusduringedwardsiellatardainfection
AT baofengsu identificationofpotentialimmunerelatedcircrnamirnamrnaregulatorynetworkinintestineofparalichthysolivaceusduringedwardsiellatardainfection
AT chaoli identificationofpotentialimmunerelatedcircrnamirnamrnaregulatorynetworkinintestineofparalichthysolivaceusduringedwardsiellatardainfection