Abstract
Neospora caninum is an apicomplexan cyst-forming parasite that is considered one of the main causes of abortion. The pathogenic mechanisms associated with parasite virulence at the maternal-foetal interface that are responsible for the outcome of infection are largely unknown. Here, utilizing placentomes from cattle experimentally infected with high-virulence (Nc-Spain7) and low-virulence (Nc-Spain1H) isolates, we studied key elements of the innate and adaptive immune responses, as well as components of the extracellular matrix (ECM), at 10 and 20 days post-infection (dpi). The low-virulence isolate elicited a robust immune response characterized by upregulation of genes involved in pathogen recognition, chemokines and pro-inflammatory cytokines, crucial for its adequate control. In addition, Nc-Spain1H triggered the expression of anti-inflammatory cytokines and other mechanisms implicated in the maintenance of ECM integrity to ensure foetal survival. In contrast, local immune responses were initially (10 dpi) impaired by Nc-Spain7, allowing parasite multiplication. Subsequently (20 dpi), a predominantly pro-inflammatory Th1-based response and an increase in leucocyte infiltration were observed. Moreover, Nc-Spain7-infected placentomes from animals carrying non-viable foetuses exhibited higher expression of the IL-8, TNF-α, iNOS and SERP-1 genes and lower expression of the metalloproteases and their inhibitors than Nc-Spain7-infected placentomes from animals carrying viable foetuses. In addition, profound placental damage characterized by an alteration in the ECM organization in necrotic foci, which could contribute to foetal death, was found. Two different host-parasite interaction patterns were observed at the bovine placenta as representative examples of different evolutionary strategies used by this parasite for transmission to offspring.
Highlights
Neospora caninum is an apicomplexan cyst-forming protozoan parasite that is considered one of the main causes of abortion and one of the organisms most efficiently transmitted by the transplacental route in cattle [1, 2]
The parasite isolate determined a time‐dependent expression pattern of pathogen recognition receptors (PRRs) chemokines and endothelial adhesion molecule genes in placentomes We found that the expression of all investigated PRRs (Figure 1A) was upregulated in the placentas infected by the low-virulence isolate Nc-Spain1H (P < 0.05–0.0001) at 10 and 20 dpi
Both isolates induced the upregulation of Chemokine ligand (CCL), Intercellular adhesion molecule (ICAM)-1 and Vascular cell adhesion molecule (VCAM)-1 RNA in placental tissues at the late stages of infection (20 dpi); placentomes from animals infected with Nc-Spain7 exhibited higher CCL2, CCL4 and ICAM-1 expression levels than those infected with Nc-Spain1H (P < 0.05–0.001), especially in CO samples (Figure 1B)
Summary
Neospora caninum is an apicomplexan cyst-forming protozoan parasite that is considered one of the main causes of abortion and one of the organisms most efficiently transmitted by the transplacental route in cattle [1, 2]. The factors that enable some isolates to be more effectively transmitted or cause foetal death than others are still unclear. Jiménez‐Pelayo et al Vet Res (2020) 51:83 and in vivo models to characterize two N. caninum isolates with marked differences in virulence: Nc-Spain and Nc-Spain1H, previously classified as high- and lowvirulence isolates, respectively [6,7,8]. We used an in vivo model of bovine infection at mid-gestation to study the early infection dynamics (10 and 20 days postinfection, dpi) after experimental challenge with highand low-virulence isolates of N. caninum (Nc-Spain and Nc-Spain1H, respectively) [13]. Nc-Spain induced foetal death and vertical transmission, with increased dissemination, parasite burdens and lesion severity in placental and foetal tissues. The infection with the low-virulence isolate Nc-Spain1H did not result in foetal death and lesional development
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