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Distinct transcriptomic response to Newcastle disease virus infection during heat stress in chicken tracheal epithelial tissue.

ABSTRACT: Newcastle disease (ND) has a great impact on poultry health and welfare with its most virulent (velogenic) strain. In addition, issues exacerbated by the increase in global temperatures necessitates a greater understanding of the host immune response when facing a combination of biotic and abiotic stress factors in poultry production. Previous investigations have revealed that the host immune response is tissue-specific. The goal of this study was to identify genes and/or signaling pathways associated with immune response to NDV (Newcastle disease virus) in the trachea, an essential organ where NDV replicate after the infection, by profiling the tissue specific transcriptome response in two genetically distinct inbred chicken lines when exposed to both abiotic and biotic stressors. Fayoumis appear to be able to respond more effectively (lower viral titer, higher antibody levels, immune gene up-regulation) and earlier than Leghorns. Our results suggest NDV infection in Fayoumis appears to elicit proinflammatory processes, and pathways such as the inhibition of cell viability, cell proliferation of lymphocytes, and transactivation of RNA, more rapidly than in Leghorns. These differences in immune response converge at later timepoints which may indicate that Leghorns eventually regulate its immune response to infection. The profiling of the gene expression response in the trachea adds to our understanding of the chicken host response to NDV infection and heat stress on a whole genome level and provides potential candidate genes and signaling pathways for further investigation into the characterization of the time-specific and pathway specific responses in Fayoumis and Leghorns.

SUBMITTER: Saelao P

PROVIDER: S-EPMC8018950 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Heat stress results in reduced productivity, anorexia, and mortality in chickens. The objective of the study was to identify genes and signal pathways associated with heat stress and Newcastle disease virus (NDV) infection in the liver of chickens through RNA-seq analysis, using two highly inbred chicken lines (Leghorn and Fayoumi). All birds were held in the same environment until 14 days of age. On day 14, half the birds were exposed to 38 °C with 50% relative humidity for 4 h, then 35 °C until the end of the experiment. The remaining birds were kept at 25 °C throughout the experiment. The heat-treated birds were inoculated at 21 days of age with 107 EID50 (One EID50 unit is the amount of virus that will infect 50 percent of inoculated embryos) NDV La Sota strain to investigate the effects of both heat stress and NDV infection. Physiological parameters were recorded as blood phenotypes at three stages: acute heat (AH), chronic heat (CH1), and chronic heat combined with NDV infection (CH&NDV), at 4 h, 7 days, and 10 days post-initiation of heat treatment, respectively. Our previous work revealed that the heat-resilient Fayoumi line maintained a more stable acid-base balance in their blood compared to the Leghorn line. Liver samples were harvested on both AH and CH&NDV to characterize the transcriptome profiles of these two inbred lines. Both genetic lines and treatments had large impact on the liver transcriptome. Fayoumi birds had more differentially expressed genes (DEGs) than Leghorn birds for both treatments. Metabolic and immune-related genes were on the DEG list, with Fayoumi having more immune-related DEGs than Leghorns, which was confirmed by gene functional enrichment analysis. Weighted correlation network analysis (WGCNA) indicated that the driver genes such as Solute Carrier Family genes could be very important for stabilizing the acid-base balance in Fayoumi birds during heat stress. Therefore, candidate genes such solute carrier family genes could be potential genetic targets that are regulated by Fayoumis to maintain physical hemostasis under heat stress. Differential gene expression showed that Leghorns mainly performed metabolic regulation in response to heat stress and NDV infection, while Fayoumis regulated both immune and metabolic functions. This study provides novel insights and enhances our understandings of liver response to heat stress of heat resilient and susceptible inbred chicken lines.

Project description:BackgroundNewcastle disease virus, in its most pathogenic form, threatens the livelihood of rural poultry farmers where there is a limited infrastructure and service for vaccinations to prevent outbreaks of the virus. Previously reported studies on the host response to Newcastle disease in chickens have not examined the disease under abiotic stressors, such as heat, which commonly experienced by chickens in regions such as Africa. The objective of this study was to elucidate the underlying biological mechanisms that contribute to disease resistance in chickens to the Newcastle disease virus while under the effects of heat stress.ResultsDifferential gene expression analysis identified genes differentially expressed between treated and non-treated birds across three time points (2, 6, and 10 days post-infection) in Fayoumi and Leghorn birds. Across the three time points, Fayoumi had very few genes differentially expressed between treated and non-treated groups at 2 and 6 days post-infection. However, 202 genes were differentially expressed at 10 days post-infection. Alternatively, Leghorn had very few genes differentially expressed at 2 and 10 days post-infection but had 167 differentially expressed genes at 6 days post-infection. Very few differentially expressed genes were shared between the two genetic lines, and pathway analysis found unique signaling pathways specific to each genetic line. Fayoumi had significantly lower viral load, higher viral clearance, higher anti-NDV antibody levels, and fewer viral transcripts detected compared to Leghorns. Fayoumis activated immune related pathways including SAPK/JNK and p38 MAPK signaling pathways at earlier time points, while Leghorn would activate these same pathways at a later time. Further analysis revealed activation of the GP6 signaling pathway that may be responsible for the susceptible Leghorn response.ConclusionsThe findings in this study confirmed our hypothesis that the Fayoumi line was more resistant to Newcastle disease virus infection compared to the Leghorn line. Within line and interaction analysis demonstrated substantial differences in response patterns between the two genetic lines that was not observed from the within line contrasts. This study has provided novel insights into the transcriptome response of the Harderian gland tissue during Newcastle disease virus infection while under heat stress utilizing a unique resistant and susceptible model.

Project description:Whole transcriptome analysis of two genetically distinctinct inbred chicken lines during NDV infection and heat stress. Background: Newcastle disease virus, in its most pathogenic form, threatens the livelihood of rural poultry farmers where there is a limited infrastructure and service for vaccinations to prevent outbreaks of the virus. Previously reported studies on the host response to Newcastle disease in chickens have not examined the disease under abiotic stressors, such as heat, which commonly experienced by chickens in regions such as Africa. The objective of this study was to elucidate the underlying biological mechanisms that contribute to disease resistance in chickens to the Newcastle disease virus while under the effects of heat stress. Results: Differential gene expression analysis identified genes differentially expressed between treated and non-treated birds across three time points (2, 6, and 10 days post-infection) in Fayoumi and Leghorn birds. Across the three time points, Fayoumi had very few genes differentially expressed between treated and non-treated groups at 2 and 6 days post-infection. However, 202 genes were differentially expressed at 10 days post-infection. Alternatively, Leghorn had very few genes differentially expressed at 2 and 10 days post-infection but had 167 differentially expressed genes at 6 days post-infection. Very few differentially expressed genes were shared between the two genetic lines, and pathway analysis found unique signaling pathways specific to each genetic line. Conclusions: The findings in this study confirmed our hypothesis that the Fayoumi line was more resistant to Newcastle disease virus infection compared to the Leghorn line. Fayoumi had significantly lower viral load, higher viral clearance, higher anti-NDV antibody levels, and fewer viral transcripts detected compared to Leghorns. Fayoumis activated immune related pathways including SAPK/JNK and p38 MAPK signaling pathways at earlier time points, while Leghorn would activate these same pathways at a later time. Further analysis revealed activation of the GP6 signaling pathway that may be responsible for the susceptible Leghorn response. Interaction analysis demonstrated substantial differences in response patterns between the two genetic lines that was not observed from the within line contrasts. This study has provided novel insights into the transcriptome response of the Harderian gland tissue during Newcastle disease virus infection while under heat stress utilizing a unique resistant and susceptible model.

Project description:BackgroundExposure to heat stress suppresses poultry immune responses, which can increase susceptibility to infectious diseases and, thereby, intensify the negative effects of heat on poultry welfare and performance. Identifying genes and pathways that are affected by high temperatures, especially heat-induced changes in immune responses, could provide targets to improve disease resistance in chickens. This study utilized RNA-sequencing (RNA-seq) to investigate transcriptome responses in the bursa of Fabricius, a primary immune tissue, after exposure to acute heat stress and/or subcutaneous immune stimulation with lipopolysaccharide (LPS) in a 2 × 2 factorial design: Thermoneutral + Saline, Heat + Saline, Thermoneutral + LPS and Heat + LPS. All treatments were investigated in two chicken lines: a relatively heat- and disease-resistant Fayoumi line and a more susceptible broiler line.ResultsDifferential expression analysis determined that Heat + Saline had limited impact on gene expression (N = 1 or 63 genes) in broiler or Fayoumi bursa. However, Thermoneutral + LPS and Heat + LPS generated many expression changes in Fayoumi bursa (N = 368 and 804 genes). Thermoneutral + LPS was predicted to increase immune-related cell signaling and cell migration, while Heat + LPS would activate mortality-related functions and decrease expression in WNT signaling pathways. Further inter-treatment comparisons in the Fayoumi line revealed that heat stress prevented many of the expression changes caused by LPS. Although fewer significant expression changes were observed in the broiler bursa after exposure to Thermoneutral + LPS (N = 59 genes) or to Heat + LPS (N = 146 genes), both treatments were predicted to increase cell migration. Direct comparison between lines (broiler to Fayoumi) confirmed that each line had distinct responses to treatment.ConclusionsTranscriptome analysis identified genes and pathways involved in bursal responses to heat stress and LPS and elucidated that these effects were greatest in the combined treatment. The interaction between heat and LPS was line dependent, with suppressive expression changes primarily in the Fayoumi line. Potential target genes, especially those involved in cell migration and immune signaling, can inform future research on heat stress in poultry and could prove useful for improving disease resistance.

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Distinct transcriptomic response to Newcastle disease virus infection during heat stress in chicken tracheal epithelial tissue.

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