Heat stress modulates polymorphonuclear cell response in early pregnancy cows: I. interferon pathway and oxidative stress

Abstract

One of the major causes of early pregnancy loss is heat stress. In ruminants, interferon tau (IFNT) is the embryo signal to the mother. Once the interferon signaling pathway is activated, it drives gene expression for interferon-stimulated genes (ISGs) and alters neutrophils responses. The aim of the present study was to evaluate interferon (IFN) pathway, ISGs and gene expression in polymorphonuclear leukocytes (PMN) and oxidative stress in dairy cows under heat stress. Pregnant cows had their estrous cycle synchronized and randomly assigned to a comfort or heat stress group. Blood samples were collected at artificial insemination (AI) and on Days 10, 14 and 18 following AI. Pregnant cows were pregnancy checked by ultrasound on Day 30 and confirmed on Day 60 post-AI. Results are presented as mean ± SEM. The corpus luteum (CL) diameter was not different between groups of pregnant cows; concentration of progesterone of pregnant cows on Day 18 following AI was greater in comfort group compared to heat stressed group. Comfort pregnant cows had higher expression of all analyzed genes from interferon pathway, except for IFNAR1, on both Days 14 and 18. Conversely, heat stressed cows did not show altered expression of IFNT pathway genes and ISGs between Days 10, 14, and 18 after AI. The oxidative stress, determined as malondialdehyde (MDA) levels, was greater in heat stress group on Days 10, 14 and 18, independent of pregnancy status. Heat stress negatively influences expression of ISGs, IFN pathway gene expression in neutrophils, and oxidative stress. Our data suggest that lower conception rates in cows under heat stress are multifactorial, with the association of interferon pathway activation and the unbalanced oxidative stress being main contributing factors.

Factors affecting first service conception rate in Holstein cows synchronized with double-ovsynch

“…A possible explanation for these results relies on the negative environmental impact of heat stress and the presence of higher humidity in the environment on fertility, which has been previously reported (Astiz and Fargas, 2013;Schüller et al, 2016). Heat stress reduces oocyte quality, compromises the uterine environment, and alters ovarian function, which is detrimental to embryonic development (Wolfenson and Roth, 2019;Amaral et al, 2021). Additionally, humidity in the environment deteriorates the general health of the cows, increasing their risk of suffering metritis and endometritis and thus compromising fertility (Adnane et al, 2017).…”

Oxidative activity of corpus luteum and ovarian parenchyma in Bos taurus indicus heifers

“…Mammalian CL contains two types of steroidogenic cells, designated as small and large luteal cells ( Al-Gubory et al, 2012 ). Although, the mechanisms of cell death and maintenance of progesterone production are complex and vary among mammalian species, it has been suggested that antioxidants play a significant role in CL during estrous cycle ( Al-Gubory et al, 2005 , 2006 ; Sugino, 2006 ; Amaral et al, 2021 ).…”

“…The production and propagation of reactive oxygen species (ROS) by CL depends on several regulatory factors, such as luteal antioxidants, steroid hormones, and cytokines ( Al-Gubory et al, 2012 ; Amaral et al, 2021 ). However, the factor that has the greatest contribution to CL function is unknown.…”

“…In vivo studies on the CL of rats ( Sugino et al, 1993 ), women ( Sugino et al, 2000 ), sheep ( Al-Gubory et al, 2004 ; Arianmanesh et al, 2011 ), and cows ( Amaral et al, 2021 ) have shown the importance of antioxidant enzymes in controlling CL function during pre-implantation period. The presence of relevant amounts of antioxidants in CL has already been described in bovine and swine females, with emphases on β-carotene and ascorbic acid ( Miszkiel et al, 1999 ; Al-Gubory et al, 2012 ).…”

“…β-carotene can act on ovaries and uterus, protecting them against oxidative damage and ensuring a favorable environment for the development of follicles and embryos, respectively. The ascorbic acid content of mature CL is high in cattle, remains high during pregnancy, and decreases during CL regression ( Petroff et al, 1997 ; Amaral et al, 2021 ).…”