RNA sequencing reveals dynamic expression of genes related to innate immune responses in canine small intestinal epithelial cells induced by Echinococcus granulosus protoscoleces
BackgroundDogs are definitive hosts of Echinococcus granulosus, with the small intestine being the only site of parasitic infections. However, the immunomodulatory processes that occur during interactions between E. granulosus and its definitive host remain unclear. Therefore, this study aimed to ev...
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Frontiers Media S.A.
2024-11-01
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| author | Zhengrong Wang Zhengrong Wang Na Pu Na Pu Na Pu Wenqing Zhao Wenqing Zhao Wenqing Zhao Xuke Chen Xuke Chen Xuke Chen Yanyan Zhang Yanyan Zhang Yan Sun Yan Sun Xinwen Bo Xinwen Bo Xinwen Bo |
| author_facet | Zhengrong Wang Zhengrong Wang Na Pu Na Pu Na Pu Wenqing Zhao Wenqing Zhao Wenqing Zhao Xuke Chen Xuke Chen Xuke Chen Yanyan Zhang Yanyan Zhang Yan Sun Yan Sun Xinwen Bo Xinwen Bo Xinwen Bo |
| author_sort | Zhengrong Wang |
| collection | DOAJ |
| description | BackgroundDogs are definitive hosts of Echinococcus granulosus, with the small intestine being the only site of parasitic infections. However, the immunomodulatory processes that occur during interactions between E. granulosus and its definitive host remain unclear. Therefore, this study aimed to evaluate gene transcription patterns in canine small intestinal epithelial cells (CIECs) following stimulation by E. granulosus protoscoleces (PSCs). Particularly, this study investigated the roles of pattern recognition receptors (PRRs), involved in recognizing pathogen-associated molecular patterns (PAMPs) and mediating the host innate immune response to the tapeworm E. granulosus.MethodsRNA sequencing (RNA-seq) was used to examine gene transcription patterns in CIECs following stimulation with PSCs for 12 and 24 h. The potential roles of differentially expressed (DE) genes were inferred through Gene Ontology (GO) enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses.ResultsRNA-seq analysis identified 78,206,492–90,548,214 clean reads in 12 RNA samples. This included six samples stimulated with PSCs for 12 h (PSC1_12h–PSC3_12h) and 24 h (PSC1_24h–PSC3_24h) and six corresponding control samples (PBS1_12h–PBS3_12h and PBS1_24h–PBS3_24h). In the PSC_12h vs. PBS_12h and PSC_24h vs. PBS_24h groups, 3,520 (2,359 upregulated and 1,161 downregulated) and 3,287 (1765 upregulated and 1,522 downregulated) DEgenes were identified, respectively. The expression of 45 PRRs genes was upregulated in the PSC_12h and PSC_24h groups compared to those in the control groups, including 4 Toll-like receptors (TLRs), 4C-type lectin receptors (CLRs), 3 NOD-like receptors (NLRs), 17 G protein-coupled receptors (GPCRs), 4 scavenger receptors (SRs), and 13 leucine-rich repeat-containing proteins (LRRCs). GO enrichment and KEGG analyses revealed that these DEgenes were mainly involved in the regulation of host immune response processes and molecules. These included antigen processing and presentation, Th17, PI3K-Akt, Th1, and Th2 cell differentiation, neutrophil extracellular trap formation, NOD- and Toll-like receptors, TNF, intestinal immune network for IgA production and IL-17 signaling pathway. Furthermore, the identified DEgenes were involved in the regulation of signaling molecules and interaction (e.g., cell adhesion molecules and ECM-receptor interaction).ConclusionThese preliminary findings provide novel perspectives on the host innate immune response to E. granulosus PSC stimulation, with a focus on the involvement of E. granulosus-specific PRRs in host defense mechanisms against infection. |
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| publishDate | 2024-11-01 |
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| spelling | doaj-art-bbb0eff610b04d498440a3ba02c425352025-08-20T02:48:53ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692024-11-011110.3389/fvets.2024.15039951503995RNA sequencing reveals dynamic expression of genes related to innate immune responses in canine small intestinal epithelial cells induced by Echinococcus granulosus protoscolecesZhengrong Wang0Zhengrong Wang1Na Pu2Na Pu3Na Pu4Wenqing Zhao5Wenqing Zhao6Wenqing Zhao7Xuke Chen8Xuke Chen9Xuke Chen10Yanyan Zhang11Yanyan Zhang12Yan Sun13Yan Sun14Xinwen Bo15Xinwen Bo16Xinwen Bo17State Key Laboratory of Sheep Genetic Improvement and Healthy Production, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaInstitute of Animal Husbandry and Veterinary Medicine, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaState Key Laboratory of Sheep Genetic Improvement and Healthy Production, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaInstitute of Animal Husbandry and Veterinary Medicine, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaCollege of Animal Science and Technology, Shihezi University, Shihezi, ChinaState Key Laboratory of Sheep Genetic Improvement and Healthy Production, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaInstitute of Animal Husbandry and Veterinary Medicine, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaCollege of Animal Science and Technology, Tarim University, Alar, ChinaState Key Laboratory of Sheep Genetic Improvement and Healthy Production, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaInstitute of Animal Husbandry and Veterinary Medicine, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaCollege of Animal Science and Technology, Shihezi University, Shihezi, ChinaState Key Laboratory of Sheep Genetic Improvement and Healthy Production, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaInstitute of Animal Husbandry and Veterinary Medicine, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaState Key Laboratory of Sheep Genetic Improvement and Healthy Production, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaInstitute of Animal Husbandry and Veterinary Medicine, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaState Key Laboratory of Sheep Genetic Improvement and Healthy Production, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaInstitute of Animal Husbandry and Veterinary Medicine, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi, ChinaCollege of Animal Science and Technology, Shihezi University, Shihezi, ChinaBackgroundDogs are definitive hosts of Echinococcus granulosus, with the small intestine being the only site of parasitic infections. However, the immunomodulatory processes that occur during interactions between E. granulosus and its definitive host remain unclear. Therefore, this study aimed to evaluate gene transcription patterns in canine small intestinal epithelial cells (CIECs) following stimulation by E. granulosus protoscoleces (PSCs). Particularly, this study investigated the roles of pattern recognition receptors (PRRs), involved in recognizing pathogen-associated molecular patterns (PAMPs) and mediating the host innate immune response to the tapeworm E. granulosus.MethodsRNA sequencing (RNA-seq) was used to examine gene transcription patterns in CIECs following stimulation with PSCs for 12 and 24 h. The potential roles of differentially expressed (DE) genes were inferred through Gene Ontology (GO) enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses.ResultsRNA-seq analysis identified 78,206,492–90,548,214 clean reads in 12 RNA samples. This included six samples stimulated with PSCs for 12 h (PSC1_12h–PSC3_12h) and 24 h (PSC1_24h–PSC3_24h) and six corresponding control samples (PBS1_12h–PBS3_12h and PBS1_24h–PBS3_24h). In the PSC_12h vs. PBS_12h and PSC_24h vs. PBS_24h groups, 3,520 (2,359 upregulated and 1,161 downregulated) and 3,287 (1765 upregulated and 1,522 downregulated) DEgenes were identified, respectively. The expression of 45 PRRs genes was upregulated in the PSC_12h and PSC_24h groups compared to those in the control groups, including 4 Toll-like receptors (TLRs), 4C-type lectin receptors (CLRs), 3 NOD-like receptors (NLRs), 17 G protein-coupled receptors (GPCRs), 4 scavenger receptors (SRs), and 13 leucine-rich repeat-containing proteins (LRRCs). GO enrichment and KEGG analyses revealed that these DEgenes were mainly involved in the regulation of host immune response processes and molecules. These included antigen processing and presentation, Th17, PI3K-Akt, Th1, and Th2 cell differentiation, neutrophil extracellular trap formation, NOD- and Toll-like receptors, TNF, intestinal immune network for IgA production and IL-17 signaling pathway. Furthermore, the identified DEgenes were involved in the regulation of signaling molecules and interaction (e.g., cell adhesion molecules and ECM-receptor interaction).ConclusionThese preliminary findings provide novel perspectives on the host innate immune response to E. granulosus PSC stimulation, with a focus on the involvement of E. granulosus-specific PRRs in host defense mechanisms against infection.https://www.frontiersin.org/articles/10.3389/fvets.2024.1503995/fullEchinococcus granulosusdefinitive hostinnate immunitypattern recognition receptorsRNA sequencing |
| spellingShingle | Zhengrong Wang Zhengrong Wang Na Pu Na Pu Na Pu Wenqing Zhao Wenqing Zhao Wenqing Zhao Xuke Chen Xuke Chen Xuke Chen Yanyan Zhang Yanyan Zhang Yan Sun Yan Sun Xinwen Bo Xinwen Bo Xinwen Bo RNA sequencing reveals dynamic expression of genes related to innate immune responses in canine small intestinal epithelial cells induced by Echinococcus granulosus protoscoleces Frontiers in Veterinary Science Echinococcus granulosus definitive host innate immunity pattern recognition receptors RNA sequencing |
| title | RNA sequencing reveals dynamic expression of genes related to innate immune responses in canine small intestinal epithelial cells induced by Echinococcus granulosus protoscoleces |
| title_full | RNA sequencing reveals dynamic expression of genes related to innate immune responses in canine small intestinal epithelial cells induced by Echinococcus granulosus protoscoleces |
| title_fullStr | RNA sequencing reveals dynamic expression of genes related to innate immune responses in canine small intestinal epithelial cells induced by Echinococcus granulosus protoscoleces |
| title_full_unstemmed | RNA sequencing reveals dynamic expression of genes related to innate immune responses in canine small intestinal epithelial cells induced by Echinococcus granulosus protoscoleces |
| title_short | RNA sequencing reveals dynamic expression of genes related to innate immune responses in canine small intestinal epithelial cells induced by Echinococcus granulosus protoscoleces |
| title_sort | rna sequencing reveals dynamic expression of genes related to innate immune responses in canine small intestinal epithelial cells induced by echinococcus granulosus protoscoleces |
| topic | Echinococcus granulosus definitive host innate immunity pattern recognition receptors RNA sequencing |
| url | https://www.frontiersin.org/articles/10.3389/fvets.2024.1503995/full |
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