Impact of Porcine Arterivirus, Influenza B, and Their Coinfection on Antiviral Response in the Porcine Lung
Interferon (IFN) cytokines induce an autonomous antiviral state in cells of the infected site to restrict virus spreading and critically regulate overall antiviral response. The antiviral state leads to host protection through expression of hundreds of IFN-stimulated genes that restrict viral infect...
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MDPI AG
2020-11-01
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| Series: | Pathogens |
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| Online Access: | https://www.mdpi.com/2076-0817/9/11/934 |
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| author | Damarius S. Fleming Laura C. Miller Yun Tian Yonghai Li Wenjun Ma Yongming Sang |
| author_facet | Damarius S. Fleming Laura C. Miller Yun Tian Yonghai Li Wenjun Ma Yongming Sang |
| author_sort | Damarius S. Fleming |
| collection | DOAJ |
| description | Interferon (IFN) cytokines induce an autonomous antiviral state in cells of the infected site to restrict virus spreading and critically regulate overall antiviral response. The antiviral state leads to host protection through expression of hundreds of IFN-stimulated genes that restrict viral infection through multiple mechanisms, for example, directly in viral genome degradation and indirectly through cellular metabolic inhibition. Young pigs were split into four treatment groups: control, porcine reproductive and respiratory syndrome virus (PRRSV, also known as porcine arterivirus) infected, influenza B virus (IBV) infected, and IBV/PRRSV coinfection. Lung tissue was collected at 3, 5, and 7 days post infection (dpi) for control, PRRSV and IBV/PRRSV coinfection, and at 3 and 5 dpi for IBV. Transcriptomic analysis, using usegalaxy.org tools, was performed against the S.scrofa 11.1 reference genome. Differentially expressed gene (DEG) analysis was carried out using DeSeq2 based on the model treatment + dpi + treatment:dpi + E. Downstream analysis examined the interaction of DEG at each dpi for over-enriched gene ontology (G.O.) terms and pathways. Comparisons of the infected groups vs. the controls yielded a total of (<i>n</i> = 1412) DEGs for the PRRSV group and (<i>n</i> = 1578) for the IBV/PRRSV group across all timepoints. The IBV group had (<i>n</i> = 64) total DEGs across 3 and 5 dpi. Expression data were considered statistically significant based on false discovery rate (FDR) ⫹ 0.1. Venn diagram comparisons of the DEGs across dpi showed that groups shared only 16 DEGs at 3 dpi, no DEGs were shared at 5 dpi, and for 7 dpi, only the PRRSV and IBV/PRRSV groups were compared and shared a total of 43 DEGs. Across the comparisons, differential expression was observed in antiviral genes such as IRF1, MX1, and OAS2. The IBV and IBV/PRRSV groups showed higher expression of antiviral genes at earlier dpi than the PRRSV group. Additionally, downregulated genes from the comparisons clustered around Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways effecting lung development and cellular integrity. Early expression of host IFN and antiviral genes may lead to viral RNA degradation, and assembly and transcription inhibition in the IBV infections. In comparison, expression of antiviral genes in the PRRSV group decreased across time. The decrease may explain why PRRSV infections persist, while IBV clears. Moreover, all infected groups showed prolonged upregulation in neutrophil degranulation pathway activity, possibly exacerbating symptomatic lung lesion pathology seen in these respiratory infections. |
| first_indexed | 2024-03-10T14:55:37Z |
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| issn | 2076-0817 |
| language | English |
| last_indexed | 2024-03-10T14:55:37Z |
| publishDate | 2020-11-01 |
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| spelling | doaj.art-26c61b41bb0a4e9aa5ea8b29d218aeb52023-11-20T20:33:25ZengMDPI AGPathogens2076-08172020-11-0191193410.3390/pathogens9110934Impact of Porcine Arterivirus, Influenza B, and Their Coinfection on Antiviral Response in the Porcine LungDamarius S. Fleming0Laura C. Miller1Yun Tian2Yonghai Li3Wenjun Ma4Yongming Sang5Oak Ridge Institute for Science and Education Oakridge, Oak Ridge Associated Universities, Oak Ridge, TN 37830, USAVirus and Prion Research Unit, National Animal Disease Center, USDA, Agricultural Research Service, Ames, IA 50161, USADepartment of Agricultural and Environmental Sciences, Tennessee State University, Nashville, TN 37209, USADepartment of Diagnostic Medicine and Pathobiology, Kansas State University, Manhattan, KS 66506, USADepartment of Diagnostic Medicine and Pathobiology, Kansas State University, Manhattan, KS 66506, USADepartment of Agricultural and Environmental Sciences, Tennessee State University, Nashville, TN 37209, USAInterferon (IFN) cytokines induce an autonomous antiviral state in cells of the infected site to restrict virus spreading and critically regulate overall antiviral response. The antiviral state leads to host protection through expression of hundreds of IFN-stimulated genes that restrict viral infection through multiple mechanisms, for example, directly in viral genome degradation and indirectly through cellular metabolic inhibition. Young pigs were split into four treatment groups: control, porcine reproductive and respiratory syndrome virus (PRRSV, also known as porcine arterivirus) infected, influenza B virus (IBV) infected, and IBV/PRRSV coinfection. Lung tissue was collected at 3, 5, and 7 days post infection (dpi) for control, PRRSV and IBV/PRRSV coinfection, and at 3 and 5 dpi for IBV. Transcriptomic analysis, using usegalaxy.org tools, was performed against the S.scrofa 11.1 reference genome. Differentially expressed gene (DEG) analysis was carried out using DeSeq2 based on the model treatment + dpi + treatment:dpi + E. Downstream analysis examined the interaction of DEG at each dpi for over-enriched gene ontology (G.O.) terms and pathways. Comparisons of the infected groups vs. the controls yielded a total of (<i>n</i> = 1412) DEGs for the PRRSV group and (<i>n</i> = 1578) for the IBV/PRRSV group across all timepoints. The IBV group had (<i>n</i> = 64) total DEGs across 3 and 5 dpi. Expression data were considered statistically significant based on false discovery rate (FDR) ⫹ 0.1. Venn diagram comparisons of the DEGs across dpi showed that groups shared only 16 DEGs at 3 dpi, no DEGs were shared at 5 dpi, and for 7 dpi, only the PRRSV and IBV/PRRSV groups were compared and shared a total of 43 DEGs. Across the comparisons, differential expression was observed in antiviral genes such as IRF1, MX1, and OAS2. The IBV and IBV/PRRSV groups showed higher expression of antiviral genes at earlier dpi than the PRRSV group. Additionally, downregulated genes from the comparisons clustered around Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways effecting lung development and cellular integrity. Early expression of host IFN and antiviral genes may lead to viral RNA degradation, and assembly and transcription inhibition in the IBV infections. In comparison, expression of antiviral genes in the PRRSV group decreased across time. The decrease may explain why PRRSV infections persist, while IBV clears. Moreover, all infected groups showed prolonged upregulation in neutrophil degranulation pathway activity, possibly exacerbating symptomatic lung lesion pathology seen in these respiratory infections.https://www.mdpi.com/2076-0817/9/11/934PRRSVIBV-Slungimmune responsedifferential expression |
| spellingShingle | Damarius S. Fleming Laura C. Miller Yun Tian Yonghai Li Wenjun Ma Yongming Sang Impact of Porcine Arterivirus, Influenza B, and Their Coinfection on Antiviral Response in the Porcine Lung Pathogens PRRSV IBV-S lung immune response differential expression |
| title | Impact of Porcine Arterivirus, Influenza B, and Their Coinfection on Antiviral Response in the Porcine Lung |
| title_full | Impact of Porcine Arterivirus, Influenza B, and Their Coinfection on Antiviral Response in the Porcine Lung |
| title_fullStr | Impact of Porcine Arterivirus, Influenza B, and Their Coinfection on Antiviral Response in the Porcine Lung |
| title_full_unstemmed | Impact of Porcine Arterivirus, Influenza B, and Their Coinfection on Antiviral Response in the Porcine Lung |
| title_short | Impact of Porcine Arterivirus, Influenza B, and Their Coinfection on Antiviral Response in the Porcine Lung |
| title_sort | impact of porcine arterivirus influenza b and their coinfection on antiviral response in the porcine lung |
| topic | PRRSV IBV-S lung immune response differential expression |
| url | https://www.mdpi.com/2076-0817/9/11/934 |
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