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Abstract
Bovine viral diarrhea virus (BVDV) can evade host detection by downregulation of interferon signaling pathways. Infection of cows with noncytopathic (ncp) BVDV can cause early embryonic mortality. Upregulation of type I interferon stimulated genes (ISGs) by blastocyst-secreted interferon tau (IFNT) is a crucial component of the maternal recognition of pregnancy (MRP) in ruminants. This study investigated the potential of acute BVDV infection to disrupt MRP by modulating endometrial ISG expression. Endometrial cells from 10 BVDV-free cows were cultured and treated with 0 or 100 ng/ml IFNT for 24 h in the absence or presence of ncpBVDV infection to yield four treatment groups: CONT, ncpBVDV, IFNT, or ncpBVDV+IFNT. ncpBVDV infection alone only upregulated TRIM56, but reduced mRNA expression of ISG15, MX2, BST2, and the proinflammatory cytokine IL1B. As anticipated, IFNT treatment alone significantly increased expression of all 17 ISGs tested. In contrast to the limited effect of ncpBVDV alone, the virus markedly inhibited IFNT-stimulated expression of 15 ISGs tested (ISG15, HERC5, USP18, DDX58, IFIH1, IFIT1, IFIT3, BST2, MX1, MX2, RSAD2, OAS1Y, SAMD9, GBP4, and PLAC8), together with ISG15 secreted protein. Only TRIM56 and IFI27 expression was unaltered. IL1B expression was reduced by the combined treatment. These results indicate that acute ncpBVDV infection may decrease uterine immunity and lead to MRP failure through inhibition of IFNT-stimulated endometrial ISG production. This in turn could reduce fertility and predispose cows to uterine disease, while evasion of the normal uterine immune response by ncpBVDV may contribute to maintenance and spreading of this economically important disease.
Highlights
Embryonic death is a major cause of poor reproductive performance in cattle, with most losses occurring before day 16 of pregnancy [1]
We showed previously that infection of cultured bovine endometrial cells with a non-cytopathic strain of bovine viral diarrhoea virus (BVDV) inhibited many of the immune pathways normally activated in response to a challenge with bacterial lipopolysaccharide (LPS), including downregulation of many interferon stimulated genes (ISGs) [19]
At the end of culture, ncpBVDV RNA was detected by PCR in the endometrial cultures treated with ncpBVDV or ncpBVDV+interferon tau (IFNT)
Summary
Embryonic death is a major cause of poor reproductive performance in cattle, with most losses occurring before day 16 of pregnancy [1]. We showed previously that infection of cultured bovine endometrial cells with a non-cytopathic strain of BVDV inhibited many of the immune pathways normally activated in response to a challenge with bacterial lipopolysaccharide (LPS), including downregulation of many interferon stimulated genes (ISGs) [19]. This observation is pertinent as pregnancy recognition in cows is initiated by interferon tau (IFNT), which is a Type I interferon. This is not an ISG but represented a major pro-inflammatory cytokine which is thought to participate in signalling between the conceptus and endometrium during MRP in cows [39]
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