Transcriptional profiling of the ovine abomasal lymph node reveals a role for timing of the immune response in gastrointestinal nematode resistance

Article English OPEN
McRae, KM ; Good, B ; Hanrahan, JP ; McCabe, MS ; Cormican, P ; Sweeney, T ; O'Connell, MJ ; Keane, OM (2016)
  • Publisher: Elsevier
  • Subject:
    mesheuropmc: parasitic diseases | animal diseases

Gastrointestinal nematodes are a serious cause of morbidity and mortality in grazing ruminants. The major ovine defence mechanism is acquired immunity, with protective immunity developing over time in response to infection. Nematode resistance varies both within and between breeds and is moderately heritable. A detailed understanding of the genes and mechanisms involved in protective immunity, and the factors that regulate this response, is required to aid both future breeding strategies and the development of effective and sustainable nematode control methods. The aim of this study was to compare the abomasal lymph node transcriptome of resistant and susceptible lambs in order to determine biological processes differentially expressed between resistant and susceptible individuals. Scottish Blackface lambs, with divergent phenotypes for resistance, were challenged with 30,000 Teladorsagia circumcincta larvae (L3), and abomasal lymph nodes recovered at 7 and 14 days post-infection (dpi). High-throughput sequencing of cDNA from the abomasal lymph node was used to quantitatively sample the transcriptome with an average of 32 million reads per sample. A total of 194 and 144 genes were differentially expressed between resistant and susceptible lambs at 7 and 14 dpi respectively. Differentially expressed networks and biological processes were identified using Ingenuity Pathway Analysis. Genes involved in the inflammatory response, attraction of T lymphocytes and binding of leukocytes were more highly expressed in resistant animals at 7 dpi and in susceptible animals at 14 dpi indicating that resistant animals respond to infection earlier than susceptible animals. Twenty-four Single Nucleotide Polymorphisms (SNP) within 11 differentially expressed genes, were tested for association with gastrointestinal nematode resistance in the Scottish Blackface lambs. Four SNP, in 2 genes (SLC30A2 and ALB), were suggestively associated with faecal egg count. In conclusion, a large number of genes were differentially expressed in the abomasal lymph node of resistant and susceptible lambs responding to gastrointestinal nematode challenge. Resistant Scottish Blackface lambs appear to generate an earlier immune response to T. circumcincta. In susceptible lambs this response appears to be delayed. SNP in 2 differentially expressed genes were suggestively associated with faecal egg count indicating that differentially expressed genes may be considered candidate loci for mediating nematode resistance.
  • References (66)
    66 references, page 1 of 7

    Ahmed, A.M., 2013. Immunological and transcriptomic analysis of genetically resistant and susceptible sheep to gastrointestinal nematodes. Doctoral Thesis. University College Dublin, Dublin, Ireland.

    Allen, J.E., Maizels, R.M., 2011, Diversity and dialogue in immunity to helminths. Nature Reviews Immunology 11, 375-388.

    Andronicos, N.M., Hunt, P., Windon, R., 2010, Expression of genes in gastrointestinal and lymphatic tissues during parasite infection in sheep genetically resistant or susceptible to Trichostrongylus colubriformis and Haemonchus contortus. International Journal for Parasitology 40, 417-429.

    Anon, 1986, Modified McMaster Method. In Ministry of Agriculture Fisheries and Food: Manual of Veterinary Parasitological Laboratory Techniques. (Reference book 418) London.

    Banerji, S., Ni, J., Wang, S.-X., Clasper, S., Su, J., Tammi, R., Jones, M., Jackson, D.G., 1999, LYVE-1, a New Homologue of the CD44 Glycoprotein, Is a Lymph-specific Receptor for Hyaluronan. The Journal of Cell Biology 144, 789-801.

    Benjamini, Y., Hochberg, Y., 1995, Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society. Series B Methodological 57, 289-300.

    Bishop, S.C., Morris, C.A., 2007, Genetics of disease resistance in sheep and goats. Small Ruminant Research 70, 48-59.

    Buitkamp, J., Filmether, P., Stear, M.J., Epplen, J.T., 1996, Class I and class II major histocompatibility complex alleles are associated with faecal egg counts following natural, predominantly Ostertagia circumcincta infection. Parasitology Research 82, 693-696.

    Craig, N.M., Miller, H.R.P., Smith, W.D., Knight, P.A., 2007, Cytokine expression in naïve and previously infected lambs after challenge with Teladorsagia circumcincta. Veterinary Immunology and Immunopathology 120, 47-54.

    Culhane, A.C., Thioulouse, J., Perrière, G., Higgins, D.G., 2005, MADE4: an R package for multivariate analysis of gene expression data. Bioinformatics 21, 2789-2790.

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