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Abstract
Vitamin D is a secosteroid hormone with many varied functions including regulation of blood calcium levels, cell proliferation, immunity, and reproduction in mammals. Vitamin D is activated by 25-hydroxylase (CYP2R1) and 1-alpha-hydroxylase (CYP27B1) and is degraded by 24-hydroxylase (CYP24A1). Vitamin D is transported by vitamin D-binding protein (group-specific component, GC) through the bloodstream and regulates cellular actions by binding to vitamin D receptor (VDR). In this study, we determined the expression and regulation of vitamin D-related molecules and the role of vitamin D at the maternal-conceptus interface in pigs. Vitamin D-metabolizing enzymes CYP2R1, CYP27B1, and CYP24A1, vitamin D binding protein GC, and vitamin D receptor VDR were expressed in the endometrium in a pregnancy stage-specific manner as well as in conceptus and chorioallantoic tissues during pregnancy. VDR protein was localized to endometrial and trophoblastic cells. Concentrations of calcitriol, the active form of vitamin D, in the endometrial tissues were higher during early pregnancy than in mid- to late pregnancy, while plasma concentrations of calcitriol were highest during late pregnancy. Furthermore, calcitriol affected the expression of several genes related to conceptus implantation, vitamin D metabolism, calcium ion regulation, PG metabolism, and calcium-binding proteins in endometrial tissue explants. These results show that CYP2R1, CYP27B1, CYP24A1, GC, and VDR were expressed at the maternal-conceptus interface, endometrial calcitriol levels were regulated during pregnancy, and calcitriol modulated the expression of endometrial genes, suggesting that calcitriol may play an important role in the establishment and maintenance of pregnancy by regulating endometrial function in pigs.
Highlights
Appropriate interactions between the developing conceptus and the maternal endometrium are essential for the establishment and maintenance of pregnancy and are tightly regulated by many factors including steroid hormones, prostaglandins (PGs), cytokines, enzymes, and ions [1, 2]
On Days 12 and 15 post-estrus, the expression of CYP27B1 was not affected by day, status, or day × status, while steady-state levels of CYP27B1 mRNA during pregnancy changed with the increased levels during mid- to late pregnancy
The significant findings of this study are: 1) vitamin D-metabolizing enzymes CYP2R1, CYP27B1, and CYP24A1, vitamin D binding protein, GC, and vitamin D receptor, VDR are expressed in the endometrium in a pregnancy status- and/or stage-specific manner; 2) CYP2R1, CYP27B1, CYP24A1, GC, and VDR mRNAs are expressed in conceptuses on Days 12 and 15 of pregnancy and in chorioallantoic tissues from Day 30 to term pregnancy; 3) levels of calcitriol in the uterine endometrial tissues are higher on Days 12 and 15 of pregnancy than in the later stage of pregnancy, while calcitriol levels in plasma are high during late pregnancy; and 4) calcitriol affects the expression of several genes related to conceptus implantation, vitamin D metabolism, calcium ion regulation, PG metabolism, and calcium-binding proteins
Summary
Appropriate interactions between the developing conceptus (embryo/fetus and associated extraembryonic membranes) and the maternal endometrium are essential for the establishment and maintenance of pregnancy and are tightly regulated by many factors including steroid hormones, prostaglandins (PGs), cytokines, enzymes, and ions [1, 2]. The conceptus-derived estrogen redirects PGF2α secretion from the uterine vasculature to the uterine lumen for corpora lutea (CL) maintenance and induces the expression of many endometrial genes including aldo-keto reductase 1B1 (AKR1B1) [3], fibroblast growth factor 7 (FGF7) [4], lysophosphatidic acid receptor 3 (LPAR3) [5]), S100 calcium binding protein G (S100G) [6], secreted phosphoprotein 1 (SPP1) [7], signal transducer and activator of transcription 1 (STAT1) [8], stanniocalcin 1 (STC1) [9], and transient receptor potential cation channel subfamily V member 6 (TRPV6) [10]. Cholecalciferol is circulated bound with vitamin D binding protein ( known as group-specific component; GC) or albumin in blood and is hydroxylated to calcifediol [25(OH)D3], the major circulating form, by CYP2R1 (25-hydroxylase) in the liver [14]. In the genomic signaling pathway, calcitriol binds to VDR with a partner receptor, retinoid X receptor, to regulate transcription of vitamin D target genes, whereas calcitriol binds to VDR associated with caveolae to activate various intracellular signaling cascades in the non-genomic pathway [19]
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