Expression network analysis of bovine skin infested with Rhipicephalus australis identifies pro-inflammatory genes contributing to tick susceptibility
Abstract The skin is the primary feeding site of ticks that infest livestock animals such as cattle. The highly specialised functions of skin at the molecular level may be a factor contributing to variation in susceptibility to tick infestation; but these remain to be well defined. The aim of this s...
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Nature Portfolio
2024-02-01
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| Ráidu: | Scientific Reports |
| Fáttát: | |
| Liŋkkat: | https://doi.org/10.1038/s41598-024-54577-w |
| _version_ | 1827327669331558400 |
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| author | Emily F. Mantilla Valdivieso Elizabeth M. Ross Ali Raza Loan Nguyen Ben J. Hayes Nicholas N. Jonsson Peter James Ala E. Tabor |
| author_facet | Emily F. Mantilla Valdivieso Elizabeth M. Ross Ali Raza Loan Nguyen Ben J. Hayes Nicholas N. Jonsson Peter James Ala E. Tabor |
| author_sort | Emily F. Mantilla Valdivieso |
| collection | DOAJ |
| description | Abstract The skin is the primary feeding site of ticks that infest livestock animals such as cattle. The highly specialised functions of skin at the molecular level may be a factor contributing to variation in susceptibility to tick infestation; but these remain to be well defined. The aim of this study was to investigate the bovine skin transcriptomic profiles of tick-naïve and tick-infested cattle and to uncover the gene expression networks that influence contrasting phenotypes of host resistance to ticks. RNA-Seq data was obtained from skin of Brangus cattle with high (n = 5) and low (n = 6) host resistance at 0 and 12 weeks following artificial tick challenge with Rhipicephalus australis larvae. No differentially expressed genes were detected pre-infestation between high and low resistance groups, but at 12-weeks there were 229 differentially expressed genes (DEGs; FDR < 0.05), of which 212 were the target of at least 1866 transcription factors (TFs) expressed in skin. Regulatory impact factor (RIF) analysis identified 158 significant TFs (P < 0.05) of which GRHL3, and DTX1 were also DEGs in the experiment. Gene term enrichment showed the significant TFs and DEGs were enriched in processes related to immune response and biological pathways related to host response to infectious diseases. Interferon Type 1-stimulated genes, including MX2, ISG15, MX1, OAS2 were upregulated in low host resistance steers after repeated tick challenge, suggesting dysregulated wound healing and chronic inflammatory skin processes contributing to host susceptibility to ticks. The present study provides an assessment of the bovine skin transcriptome before and after repeated tick challenge and shows that the up-regulation of pro-inflammatory genes is a prominent feature in the skin of tick-susceptible animals. In addition, the identification of transcription factors with high regulatory impact provides insights into the potentially meaningful gene–gene interactions involved in the variation of phenotypes of bovine host resistance to ticks. |
| first_indexed | 2024-03-07T15:03:41Z |
| format | Article |
| id | doaj.art-cddafb15d8d442aa81049b1047a7b51e |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-07T15:03:41Z |
| publishDate | 2024-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-cddafb15d8d442aa81049b1047a7b51e2024-03-05T18:59:51ZengNature PortfolioScientific Reports2045-23222024-02-0114111410.1038/s41598-024-54577-wExpression network analysis of bovine skin infested with Rhipicephalus australis identifies pro-inflammatory genes contributing to tick susceptibilityEmily F. Mantilla Valdivieso0Elizabeth M. Ross1Ali Raza2Loan Nguyen3Ben J. Hayes4Nicholas N. Jonsson5Peter James6Ala E. Tabor7Queensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, The University of QueenslandQueensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, The University of QueenslandQueensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, The University of QueenslandQueensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, The University of QueenslandQueensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, The University of QueenslandInstitute of Biodiversity One Health and Veterinary Medicine, University of GlasgowQueensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, The University of QueenslandQueensland Alliance for Agriculture and Food Innovation, Centre for Animal Science, The University of QueenslandAbstract The skin is the primary feeding site of ticks that infest livestock animals such as cattle. The highly specialised functions of skin at the molecular level may be a factor contributing to variation in susceptibility to tick infestation; but these remain to be well defined. The aim of this study was to investigate the bovine skin transcriptomic profiles of tick-naïve and tick-infested cattle and to uncover the gene expression networks that influence contrasting phenotypes of host resistance to ticks. RNA-Seq data was obtained from skin of Brangus cattle with high (n = 5) and low (n = 6) host resistance at 0 and 12 weeks following artificial tick challenge with Rhipicephalus australis larvae. No differentially expressed genes were detected pre-infestation between high and low resistance groups, but at 12-weeks there were 229 differentially expressed genes (DEGs; FDR < 0.05), of which 212 were the target of at least 1866 transcription factors (TFs) expressed in skin. Regulatory impact factor (RIF) analysis identified 158 significant TFs (P < 0.05) of which GRHL3, and DTX1 were also DEGs in the experiment. Gene term enrichment showed the significant TFs and DEGs were enriched in processes related to immune response and biological pathways related to host response to infectious diseases. Interferon Type 1-stimulated genes, including MX2, ISG15, MX1, OAS2 were upregulated in low host resistance steers after repeated tick challenge, suggesting dysregulated wound healing and chronic inflammatory skin processes contributing to host susceptibility to ticks. The present study provides an assessment of the bovine skin transcriptome before and after repeated tick challenge and shows that the up-regulation of pro-inflammatory genes is a prominent feature in the skin of tick-susceptible animals. In addition, the identification of transcription factors with high regulatory impact provides insights into the potentially meaningful gene–gene interactions involved in the variation of phenotypes of bovine host resistance to ticks.https://doi.org/10.1038/s41598-024-54577-wGene expressionCattleBovineHost resistanceRNA-Seq |
| spellingShingle | Emily F. Mantilla Valdivieso Elizabeth M. Ross Ali Raza Loan Nguyen Ben J. Hayes Nicholas N. Jonsson Peter James Ala E. Tabor Expression network analysis of bovine skin infested with Rhipicephalus australis identifies pro-inflammatory genes contributing to tick susceptibility Scientific Reports Gene expression Cattle Bovine Host resistance RNA-Seq |
| title | Expression network analysis of bovine skin infested with Rhipicephalus australis identifies pro-inflammatory genes contributing to tick susceptibility |
| title_full | Expression network analysis of bovine skin infested with Rhipicephalus australis identifies pro-inflammatory genes contributing to tick susceptibility |
| title_fullStr | Expression network analysis of bovine skin infested with Rhipicephalus australis identifies pro-inflammatory genes contributing to tick susceptibility |
| title_full_unstemmed | Expression network analysis of bovine skin infested with Rhipicephalus australis identifies pro-inflammatory genes contributing to tick susceptibility |
| title_short | Expression network analysis of bovine skin infested with Rhipicephalus australis identifies pro-inflammatory genes contributing to tick susceptibility |
| title_sort | expression network analysis of bovine skin infested with rhipicephalus australis identifies pro inflammatory genes contributing to tick susceptibility |
| topic | Gene expression Cattle Bovine Host resistance RNA-Seq |
| url | https://doi.org/10.1038/s41598-024-54577-w |
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