Cytokine and antibody subclass responses in the intestinal lymph of sheep during repeated experimental infections with the nematode parasite Trichostrongylus colubriformis

• Published in: Veterinary Immunology and Immunopathology 2006-11, Vol.114 (1), p.135-148
• Main Authors: Pernthaner, Anton, Cole, Sally-Ann, Morrison, Lilian, Green, Richard, Shaw, Richard J., Hein, Wayne R.
• Format: Article
• Language: English
• Subjects: Afferent lymph; animal parasitic nematodes; Animals; Antibodies, Helminth - biosynthesis; Antibodies, Helminth - immunology; Antibody subclass; Cytokines; Cytokines - genetics; Cytokines - immunology; Efferent lymph; Feces - parasitology; food animals; gene expression; Gene Expression Regulation - immunology; genetic resistance; genotype; immune response; immunity; Immunoglobulin Isotypes - biosynthesis; Immunoglobulin Isotypes - immunology; immunoglobulins; interferons; interleukins; Intestinal Diseases, Parasitic - genetics; Intestinal Diseases, Parasitic - immunology; Intestinal Diseases, Parasitic - parasitology; Intestinal Diseases, Parasitic - veterinary; Intestinal immune response; intestines; lymph; Lymph - immunology; Lymph - parasitology; Male; messenger RNA; Nematoda; Nematode infection; nematode infections; Parasite Egg Count - veterinary; pest resistance; Reverse Transcriptase Polymerase Chain Reaction - veterinary; RNA - chemistry; RNA - genetics; Sheep; Sheep - immunology; Sheep Diseases - genetics; Sheep Diseases - immunology; Sheep Diseases - parasitology; Statistics, Nonparametric; Trichostrongylosis - genetics; Trichostrongylosis - immunology; Trichostrongylosis - parasitology; Trichostrongylosis - veterinary; Trichostrongylus; Trichostrongylus - immunology; Trichostrongylus colubriformis; tumor necrosis factor-alpha
• ISSN: 0165-2427; 1873-2534; 1365-2567
• DOI: 10.1016/j.vetimm.2006.08.004

The expression of interleukin (IL)-4, IL-5, IL-10, IL-13, TNF-α and IFN-γ genes, and parasite-specific IgM, IgG1, IgG2, IgA and total IgE levels, were monitored daily in intestinal lymph of sheep infected repeatedly with the nematode parasite Trichostrongylus colubriformis. Host genotype had a significant influence on IL-13 gene activity, with resistant-line (R) sheep consistently expressing higher levels of mRNA than susceptible-line (S) sheep. Mean gene expression of IL-13, IL-4 and IFN-γ did not differ significantly between the first and second nematode challenge. Field-primed R and S as well as field-primed R and naïve S sheep had lower mean gene expression of IL-5 and IL-10, respectively, during the second when compared to primary challenge. Genes for IL-13 and IL-5 were transiently and strongly up-regulated after nematode infection, particularly in animals with previous exposure to nematodes. Genes for TNF-α and IFN-γ were also transiently up-regulated, but to a lesser extent and more typically after primary challenge. Naïve sheep of both genotypes produced relatively little antibody response after primary challenge. A second nematode challenge resulted in large increases in the lymphatic levels of all antibody sub-classes which were significant for adult antigen-specific IgA and larval antigen-specific IgG1. In naïve S line sheep, the larval-specific IgA and IgG2 response appeared delayed when compared to the R line animals. Field-primed R and S line sheep had relatively high lymphatic IgG1 levels prior to experimental infection and these did not change significantly afterwards. These results demonstrate that during nematode infections, the intestinal micro-environment of sheep is transiently skewed towards Th2 cytokine dominance, although IFN-γ gene expression continues. This response is accompanied by increases of nematode-specific IgG1, IgA, IgG2 and IgM, as well as of total IgE in lymph plasma.