Identification of Regulatory Functions of LncRNAs Associated With T. circumcincta Infection in Adult Sheep

Several recent studies have demonstrated the role of long non-coding RNAs (lncRNAs) in regulating the defense mechanism against parasite infections, but no studies are available that investigated their relevance for immune response to nematode infection in sheep. Thus, the aim of the current study w...

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Main Authors: Praveen Krishna Chitneedi, Rosemarie Weikard, Juan J. Arranz, María Martínez-Valladares, Christa Kuehn, Beatriz Gutiérrez-Gil
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2021.685341/full
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author Praveen Krishna Chitneedi
Rosemarie Weikard
Juan J. Arranz
María Martínez-Valladares
María Martínez-Valladares
Christa Kuehn
Christa Kuehn
Beatriz Gutiérrez-Gil
author_facet Praveen Krishna Chitneedi
Rosemarie Weikard
Juan J. Arranz
María Martínez-Valladares
María Martínez-Valladares
Christa Kuehn
Christa Kuehn
Beatriz Gutiérrez-Gil
author_sort Praveen Krishna Chitneedi
collection DOAJ
description Several recent studies have demonstrated the role of long non-coding RNAs (lncRNAs) in regulating the defense mechanism against parasite infections, but no studies are available that investigated their relevance for immune response to nematode infection in sheep. Thus, the aim of the current study was to (i) detect putative lncRNAs that are expressed in the abomasal lymph node of adult sheep after an experimental infection with the gastrointestinal nematode (GIN) Teladorsagia circumcincta and (ii) to elucidate their potential functional role associated with the differential host immune response. We hypothesized that putative lncRNAs differentially expressed (DE) between samples from animals that differ in resistance to infection may play a significant regulatory role in response to nematode infection in adult sheep. To obtain further support for our hypothesis, we performed co-expression and functional gene enrichment analyses with the differentially expressed lncRNAs (DE lncRNAs). In a conservative approach, we included for this predictive analysis only those lncRNAs that are confirmed and supported by documentation of expression in gastrointestinal tissues in the current sheep gene atlas. We identified 9,105 putative lncRNA transcripts corresponding to 7,124 gene loci. Of these, 457 were differentially expressed lncRNA loci (DELs) with 683 lncRNA transcripts. Based on a gene co-expression analysis via weighted gene co-expression network analysis, 12 gene network modules (GNMs) were found significantly correlated with at least one of 10 selected target DE lncRNAs. Based on the principle of “guilt-by-association,” the DE genes from each of the three most significantly correlated GNMs were subjected to a gene enrichment analysis. The significant pathways associated with DE lncRNAs included ERK5 Signaling, SAPK/JNK Signaling, RhoGDI Signaling, EIF2 Signaling, Regulation of eIF4 and p70S6K Signaling and Oxidative Phosphorylation pathways. They belong to signaling pathway categories like Cellular Growth, Proliferation and Development, Cellular Stress and Injury, Intracellular and Second Messenger Signaling and Apoptosis. Overall, this lncRNA study conducted in adult sheep after GIN infection provided first insights into the potential functional role of lncRNAs in the differential host response to nematode infection.
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spelling doaj.art-26299c95f65c4963af97275cb67e48082022-12-21T22:00:44ZengFrontiers Media S.A.Frontiers in Genetics1664-80212021-06-011210.3389/fgene.2021.685341685341Identification of Regulatory Functions of LncRNAs Associated With T. circumcincta Infection in Adult SheepPraveen Krishna Chitneedi0Rosemarie Weikard1Juan J. Arranz2María Martínez-Valladares3María Martínez-Valladares4Christa Kuehn5Christa Kuehn6Beatriz Gutiérrez-Gil7Institute of Genome Biology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyInstitute of Genome Biology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyDepartamento de Producción Animal, Facultad de Veterinaria, Universidad de León, León, SpainDepartamento de Sanidad Animal, Facultad de Veterinaria, Universidad de León, León, SpainInstituto de Ganadería de Montaña, CSIC-Universidad de León, León, SpainInstitute of Genome Biology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, GermanyFaculty of Agricultural and Environmental Sciences, University of Rostock, Rostock, GermanyDepartamento de Producción Animal, Facultad de Veterinaria, Universidad de León, León, SpainSeveral recent studies have demonstrated the role of long non-coding RNAs (lncRNAs) in regulating the defense mechanism against parasite infections, but no studies are available that investigated their relevance for immune response to nematode infection in sheep. Thus, the aim of the current study was to (i) detect putative lncRNAs that are expressed in the abomasal lymph node of adult sheep after an experimental infection with the gastrointestinal nematode (GIN) Teladorsagia circumcincta and (ii) to elucidate their potential functional role associated with the differential host immune response. We hypothesized that putative lncRNAs differentially expressed (DE) between samples from animals that differ in resistance to infection may play a significant regulatory role in response to nematode infection in adult sheep. To obtain further support for our hypothesis, we performed co-expression and functional gene enrichment analyses with the differentially expressed lncRNAs (DE lncRNAs). In a conservative approach, we included for this predictive analysis only those lncRNAs that are confirmed and supported by documentation of expression in gastrointestinal tissues in the current sheep gene atlas. We identified 9,105 putative lncRNA transcripts corresponding to 7,124 gene loci. Of these, 457 were differentially expressed lncRNA loci (DELs) with 683 lncRNA transcripts. Based on a gene co-expression analysis via weighted gene co-expression network analysis, 12 gene network modules (GNMs) were found significantly correlated with at least one of 10 selected target DE lncRNAs. Based on the principle of “guilt-by-association,” the DE genes from each of the three most significantly correlated GNMs were subjected to a gene enrichment analysis. The significant pathways associated with DE lncRNAs included ERK5 Signaling, SAPK/JNK Signaling, RhoGDI Signaling, EIF2 Signaling, Regulation of eIF4 and p70S6K Signaling and Oxidative Phosphorylation pathways. They belong to signaling pathway categories like Cellular Growth, Proliferation and Development, Cellular Stress and Injury, Intracellular and Second Messenger Signaling and Apoptosis. Overall, this lncRNA study conducted in adult sheep after GIN infection provided first insights into the potential functional role of lncRNAs in the differential host response to nematode infection.https://www.frontiersin.org/articles/10.3389/fgene.2021.685341/fulladult sheepgastrointestinal infectionnematodeabomasal lymph nodelong non-coding RNAfunctional annotation
spellingShingle Praveen Krishna Chitneedi
Rosemarie Weikard
Juan J. Arranz
María Martínez-Valladares
María Martínez-Valladares
Christa Kuehn
Christa Kuehn
Beatriz Gutiérrez-Gil
Identification of Regulatory Functions of LncRNAs Associated With T. circumcincta Infection in Adult Sheep
Frontiers in Genetics
adult sheep
gastrointestinal infection
nematode
abomasal lymph node
long non-coding RNA
functional annotation
title Identification of Regulatory Functions of LncRNAs Associated With T. circumcincta Infection in Adult Sheep
title_full Identification of Regulatory Functions of LncRNAs Associated With T. circumcincta Infection in Adult Sheep
title_fullStr Identification of Regulatory Functions of LncRNAs Associated With T. circumcincta Infection in Adult Sheep
title_full_unstemmed Identification of Regulatory Functions of LncRNAs Associated With T. circumcincta Infection in Adult Sheep
title_short Identification of Regulatory Functions of LncRNAs Associated With T. circumcincta Infection in Adult Sheep
title_sort identification of regulatory functions of lncrnas associated with t circumcincta infection in adult sheep
topic adult sheep
gastrointestinal infection
nematode
abomasal lymph node
long non-coding RNA
functional annotation
url https://www.frontiersin.org/articles/10.3389/fgene.2021.685341/full
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