Comparative RNA-Seq analysis reveals insights in Salmonella disease resistance of chicken; and database development as resource for gene expression in poultry

Dar, Muneer Ahmad; Ahmad, Syed Mudasir; Bhat, Basharat Ahmad; Dar, Tanveer Ali; Haq, Zulfqar Ul; Wani, B.A.; Shabir, Nadeem; Kashoo, Zahid Amin; Shah, Rehan Ali; Ganai, Nazir Ahmad; Heidari, Mohammad

doi:10.1016/j.ygeno.2022.110475

Cited by 11 publications

(13 citation statements)

References 84 publications

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“…We found genes such as, TOLLIP, RASD1 and SOCS1, which are involved in the negative regulation of downstream TLR4 signalling, NFĸB activation and cytokine activities, were upregulated across all models. Collectively, the modulation of a majority of the shared genes resemble the immune landscape similar to in vivo studies (Berndt et al, 2007;Fasina et al, 2008;Khan and Chousalkar, 2020;Bescucci et al, 2022;Dar et al, 2022). Overall, the data suggests a tight balance between pro-and anti-inflammatory responses is taking place in both 2D and 3D enteroids during STm infection.…”

Section: Discussionsupporting

confidence: 56%

Disentangling the Innate Immune Responses of Intestinal Epithelial Cells and Lamina Propria Cells toSalmonellaTyphimurium Infection in Chickens

Sutton

Nash

Sives

et al. 2023

Preprint

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Salmonella enterica serovar Typhimurium (STm) is a major foodborne pathogen and poultry are a key reservoir of human infections. To understand the host responses to early stages of Salmonella infection in poultry, we infected 2D and 3D enteroids, the latter of which contains leukocytes, neurons, and mesenchymal cells that are characteristic of the lamina propria. We infected these enteroids with wild-type (WT STm), a non-invasive mutant lacking the prgH gene (delta STm), or treated them with STm lipopolysaccharide (LPS) and analysed the expression of innate immune related genes by qPCR at 4 and 8 h. The localisation of ZO-1 expression was disrupted in WT STm infected enteroids but not delta prgH STm or LPS treated enteroids, suggesting a loss of barrier integrity. The innate immune response to LPS was more pronounced in 2D enteroids compared to 3D enteroids and by 8 hpi, the response in 3D enteroids was almost negligible. However, when STm adhered to or invaded the enteroids, both 2D and 3D enteroids exhibited an upregulation of inflammatory responses. The presence of lamina propria cells in 3D enteroids resulted in the unique expression of genes associated with immune functions involved in regulating inflammation. Moreover, 2D and 3D enteroids showed temporal differences in response to bacterial invasion or adherence. At 8 hpi, innate responses in 3D but not 2D enteroids continued to increase after infection with WT STm, whereas the responses to the non-invasive strain decreased at 8 hpi in both 2D and 3D enteroids. In conclusion, STm infection of chicken enteroids recapitulated several observations from in vivo studies of Salmonella-infected chickens, including altered epithelial barrier integrity based on ZO-1 expression and inflammatory responses. Our findings provide evidence that Salmonella-infected enteroids serve as effective models for investigating host-pathogen interactions and exploring the molecular mechanisms of microbial virulence although the 3D model mimics the host more accurately due to the presence of a lamina propria.

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Section: Discussionsupporting

confidence: 56%

Disentangling the Innate Immune Responses of Intestinal Epithelial Cells and Lamina Propria Cells toSalmonellaTyphimurium Infection in Chickens

Sutton

Nash

Sives

et al. 2023

Preprint

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“…Our study revealed that S. enterica BNCC186354 triggers host cellular responses through the RAS, MAPK, and RAP1 pathways, among others. These pathways are involved in processes, including inflammation and apoptosis, and some have been reported as being involved in regulating the infection process of S. enterica [ 58 ]. Interestingly, we found that the expression trend of genes was restored by L. reuteri ATCC 53,608 after S. enterica BNCC186354 infection; that is, these genes were mostly down-regulated under S. enterica BNCC186354 treatment only, while the addition of L. reuteri ATCC 53,608 inhibited this trend.…”

Section: Discussionmentioning

confidence: 99%

Chromatin Accessibility and Transcriptional Landscape during Inhibition of Salmonella enterica by Lactobacillus reuteri in IPEC-J2 Cells

Qin

Ren

et al. 2023

Cells

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Lactobacillus reuteri is a probiotic with bacteriostatic effects, which can effectively inhibit the activity of pathogens. However, the molecular mechanism underlying the inhibition of pathogens by L. reuteri in intestinal cells remains unclear. Using the porcine intestinal cell line IPEC-J2 as a model, we combined RNA-seq and ATAC-seq methods to delineate the porcine genome-wide changes in biological processes and chromatin accessibility in IPEC-J2 cells stimulated by Salmonella enterica BNCC186354, as well as L. reuteri ATCC 53608. Overall, we found that many porcine transcripts were altered after S. enterica BNCC186354 treatment, while L. reuteri ATCC 53608 treatment partially restored this alteration, such as salmonella infection and PI3K/AKT and MAPK pathways. Combined analysis of these two datasets revealed that 26 genes with similar trends overlapped between gene expression and chromatin accessibility. In addition, we identified potential host functional transcription factors (TFs), such as GATA1, TAL1, TBP, RUNX1, Gmeb1, Gfi1b, RARA, and RXRG, in IPEC-J2 cells that might play a critical role and are targeted by L. reuteri ATCC 53608. Moreover, we verified that PI3K/AKT, MAPK, and apoptosis pathways are potentially regulated by S. enterica BNCC186354 but restored by L. reuteri ATCC 53608. The PI3K/AKT pathway was activated by L. reuteri ATCC 53608, thereby potentially inhibiting S. enterica BNCC186354 infection. In conclusion, our data provide new insights into the expression pattern of functional genes and the epigenetic alterations in IPEC-J2 cells underlying the bacteriostatic action of L. reuteri ATCC 53608.

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“…For global identification of genes and transcription factorss interacting with NF-κB1, FOXO3 and PAX5, we utilized RNA-Sequencing data from our previously published dataset NCBI GEO ID: GSE168060 [ 10 ]. The standard protocols/pipeline was utilized for RNA extraction, cDNA preparation and RNA-Sequencing [ 10 ]. Total RNA was extracted using Trizol method (Ambion, USA).…”

Section: Methodsmentioning

confidence: 99%

Identification of key transcription factors and their functional role involved in Salmonella typhimurium infection in chicken using integrated transcriptome analysis and bioinformatics approach

et al. 2023

Self Cite

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Salmonella enterica serovar typhimurium is the cause of significant morbidity and mortality worldwide that causes economic losses to poultry and is able to cause infection in humans. Indigenous chicken breeds are a potential source of animal protein and have the added advantage of being disease resistant. An indigenous chicken, Kashmir favorella and commercial broiler were selected for understanding the mechanism of disease resistance. Following infection in Kashmir favorella, three differentially expressed genes Nuclear Factor Kappa B (NF-κB1), Forkhead Box Protein O3 (FOXO3) and Paired box 5 (Pax5) were identified. FOXO3, a transcriptional activator, is the potential marker of host resistance in Salmonella infection. NF-κB1 is an inducible transcription factor which lays the foundation for studying gene network of the innate immune response of Salmonella infection in chicken. Pax5 is essential for differentiation of pre-B cells into mature B cell. The real time PCR analysis showed that in response to Salmonella Typhimurium infection a remarkable increase of NF-κB1 (P˂0.01), FOXO3 (P˂0.01) gene expression in liver and Pax5 (P˂0.01) gene expression in spleen of Kashmir favorella was observed. The protein–protein interaction (PPI) and protein-TF interaction network by STRINGDB analysis suggests that FOXO3 is a hub gene in the network and is closely related to Salmonella infection along with NF-κB1. All the three differentially expressed genes (NF-κB1, FOXO3 and PaX5) showed their influence on 12 interacting proteins and 16 TFs, where cyclic adenosine monophosphate Response Element Binding protein (CREBBP), erythroblast transformation-specific (ETSI), Tumour-protein 53(TP53I), IKKBK, lymphoid enhancer-binding factor-1 (LEF1), and interferon regulatory factor-4 (IRF4) play role in immune responses. This study shall pave the way for newer strategies for treatment and prevention of Salmonella infection and may help in increasing the innate disease resistance.

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Comparative RNA-Seq analysis reveals insights in Salmonella disease resistance of chicken; and database development as resource for gene expression in poultry

Cited by 11 publications

References 84 publications

Disentangling the Innate Immune Responses of Intestinal Epithelial Cells and Lamina Propria Cells toSalmonellaTyphimurium Infection in Chickens

Disentangling the Innate Immune Responses of Intestinal Epithelial Cells and Lamina Propria Cells toSalmonellaTyphimurium Infection in Chickens

Chromatin Accessibility and Transcriptional Landscape during Inhibition of Salmonella enterica by Lactobacillus reuteri in IPEC-J2 Cells

Identification of key transcription factors and their functional role involved in Salmonella typhimurium infection in chicken using integrated transcriptome analysis and bioinformatics approach

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