Relationship between susceptibility of Blackface sheep to Teladorsagia circumcincta infection and an inflammatory mucosal T cell response

Anton G Gossner,Darren J Shaw,Josephine M Pemberton,Virginia M Venturina,John Hopkins

doi:10.1186/1297-9716-43-26

Anton G Gossner, Darren J Shaw + Show 3 more

Open Access

https://doi.org/10.1186/1297-9716-43-26

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Journal: Veterinary Research	Publication Date: Jan 1, 2012
Citations: 85	License type: cc-by

Affiliation: Roslin Institute, University of Edinburgh

Abstract

Teladorsagia circumcincta is the most economically important gastrointestinal (abomasal) nematode parasite of sheep in cool temperate regions, to which sheep show genetically-varying resistance to infection. Lambs, from parents with genetic variation for resistance, were trickle infected with L3 larvae over 12 weeks. 45 lambs were identified with a range of susceptibilities as assessed by: adult worm count at post mortem, faecal egg count (FEC) and IgA antibody levels. This project investigated the correlation of T cell cytokine expression and resistance to infection at the mature stage of response, when the resistant lambs had excluded all parasites.Histopathology showed only minor changes in resistant animals with a low level lymphocyte infiltration; but in susceptible lambs, major pathological changes were associated with extensive infiltration of lymphocytes, eosinophils and neutrophils.Absolute quantitative RT-qPCR assays on the abomasal lymph node (ALN) revealed a significant positive correlation between IL6, IL21 and IL23A transcript levels with adult worm count and FEC. IL23A was also negatively correlated with IgA antibody levels. Significantly positive correlation of TGFB1 levels with adult worm count and FEC were also seen in the abomasal mucosa. These data are consistent with the hypothesis that the inability to control L3 larval colonization, adult worm infection and egg production is due to the activation of the inflammatory Th17 T cell subset.

Highlights

The dominant gastrointestinal parasite of farmed sheep in cool temperate regions is the abomasal strongylid nematode Teladorsagia circumcincta [1,2]
In comparison to the uninfected control group (Figure 1A), only minor pathological changes were noted in resistant animals with a low level lymphocytic infiltrate and few eosinophils and neutrophils associated with the gastric glands (Figure 1B); nematodes were not detected within the gastric glands
The aim of this study was to investigate the relationship between the host immune response and parasite infection in sheep selected to have a range of predicted genetic resistance to the abomasal nematode parasite T. circumcincta

Summary

Introduction

The dominant gastrointestinal parasite of farmed sheep in cool temperate regions is the abomasal strongylid nematode Teladorsagia circumcincta [1,2]. Many sheep eventually control worm development and egg production through the acquisition of protective immunity [6,7], largely through the generation of parasite specific IgE and IgA. Our data and others [11,12] show a significant linkage between IgA antibody levels, adult worm numbers, worm length and faecal egg counts (FEC). The original breeding programmes for the development of resistant and susceptible lines to Haemonchus contortus, Trichostrongylus colubriformis as well as T. circumcincta were based on FEC [14,15,16]. Microsatellite and quantitative trait locus (QTL) analyses [17,18] have identified a number of markers associated with resistance, including alleles of Ovar-DRB1 [19] and IFNG [20]

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