Local immune response of Canarian Majorera goats infected with Teladorsagia circumcincta

Abstract

Background: Due to increased anthelmintic resistance, alternative methods to drugs are necessary to control gastrointestinal nematodes (GINs). Some of the most promising alternatives are based on the immune response of the host, such as the selection of genetically resistant breeds or the use of vaccines against these parasites. Given the limited information available on the immune response against GINs in goats, this study investigated the local immune response of goat kids of an indigenous Canary Islands breed (Majorera breed) experimentally infected with Teladorsagia circumcincta, one of the most pathogenic and prevalent GIN species.

Methods: For this purpose, the relationship between different parasitological (number of mature and immature worms, worm length, and number of intrauterine eggs) and immunological parameters at the local level (related to both the humoral and cellular immune response) was analyzed at early (1 week post-infection [wpi]) and late (8 wpi) stages of infection.

Results: Primary infection of goat kids with T. circumcincta infective larvae (L3) generated a complex immune response that could be defined as Th2 type, characterized by increased infiltration in abomasal tissues of several effector cells as well as a progressive presence of specific antibodies against parasitic antigens in the gastric mucus. Cellular responses were evidenced from 1 wpi onward, showing an increase in antigen-presenting cells and various lymphocyte subsets in the gastric mucosa.

Conclusions: The complexity of the host response was evidenced by statistically significant changes in the number of all these subpopulations (MHCII⁺, CD4⁺, CD8⁺, γδ⁺, CD45R⁺, IgA⁺, and IgG⁺), as well as in the evolution of the relative cytokine gene expression. From a functional point of view, negative associations were observed between the number of most of the immune cells (CD4, IgA, IgG, and CD45R cells) and parameters that could be related to the fecundity of worms, a phenomenon that was especially evident when the number of IgG and CD45R cells or the specific IgA levels of the gastric mucus were compared with parasitological parameters such as the female worm length or fecal egg counts at 8 wpi.

Keywords: Abomasal mucosa; Cellular response; Goat; Immunoglobulins; Teladorsagia circumcincta.

Fig. 1

Eggs per gram of feces (EPG) expressed as mean EPG ± SEM in goats orally infected with 8000 T. circumcincta L3 (group 2)

Fig. 2

Total IgG and IgA anti-T. circumcincta in mucus from groups 1 and 2 (orally infected with 8000 T. circumcincta L3 and slaughtered at 1 or 8 wpi, respectively) and the uninfected control group. Results are mean optical density (OD) at 492 nm ± SEM

Fig. 3

Immunorecognition of mucosal IgA of T. circumcincta adult worms somatic antigen in goats from group 2 (orally inoculated with 8000 T. circumcincta L3) (P) and uninfected control group (C) at 8 wpi. kDa molecular weight markers in kilodaltons

Fig. 4

Levels of effector cells (eosinophils, mast cells, and globule leucocyte counts) in the gastric mucosa in goats from groups 1, 2 (orally infected with 8000 T. circumcincta L3 and slaughtered at 1 or 8 weeks pi, respectively) and uninfected control group. Results are mean number cells/mm² ± SEM

Fig. 5

Levels of cellular subpopulations in the gastric mucosa in goats from groups 1 and 2 (orally infected with 8000 T. circumcincta L3 and slaughtered at 1 or 8 wpi, respectively) and the uninfected control group. Results are mean number of cells/mm² ± SEM. Abbreviations: Mann–Whitney U-test group 1 vs. control: a Z = −2.193, P = 0.028. b Z = −1.984, P = 0.047. c Z = −2.402, P = 0.016. d Z = −2.601, P = 0.09. Mann–Whitney U-test group 2 vs. control: e Z = −2.193, P = 0.028. f Z = −2.402, P = 0.016. g Z = −2.611, P = 0.009. MHCII⁺: antigen-presenting cells MHCII. CD4: lymphocyte subset CD4⁺. CD8: lymphocyte subset CD8⁺. γδ: lymphocyte subset γδ⁺. WC1: lymphocyte subset WC1⁺. CD45R: lymphocyte subset CD45R⁺. IgA⁺: anti-IgA immunoreactive cells. IgG⁺: anti-IgG immunoreactive cells

Fig. 6

Gene transcription levels of IL-2, IL-4, IL-10, IL-17, and INF-γ in abomasal lymph nodes (LN) and gastric mucosa (GM) from groups 1 and 2 (goats orally infected with 8000 T. circumcincta L3 and slaughtered at 1 or 8 wpi, respectively). Results are mean relative units (RU) ± SEM after applying the ΔΔCt method (giving a value of 1 RU to the control group) and using β-actin as housekeeping gene