Analysis of cysteine-X-cysteine motif chemokine ligands 9, 10, and 11, their receptor CXCR3, and their possible role on the recruitment of immune cells at the maternal–conceptus interface in pigs†

Han, Jisoo; Gu, Min; Yoo, Inkyu; Choi, Yunseon; Jang, Hyejeong; Kim, Minjeong; Yun, Cheol‐Heui; Ka, Hakhyun

doi:10.1093/biolre/iox074

Cited by 42 publications

(25 citation statements)

References 47 publications

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“…Th1 cytokines activate cell-mediated immunity that is deleterious for pregnancy, while Th2 cytokines are involved in humoral immunity that is beneficial for fetal survival and leads to maternal immune tolerance to the developing fetus [ 52 ]. In the porcine endometrium, there are many immune cells recruited into the endometrium during early pregnancy [ 53 ] and recruitment of T cells and NK cells into the endometrium is greatest on Day 15 of pregnancy [ 54 ], when the conceptus attachment to the endometrial epithelial cells occurs. Our results indicate that IL10 production increases and IL12 production decreases in the endometrium during early pregnancy (Han and Ka, unpublished data).…”

Section: Discussionmentioning

confidence: 99%

Vitamin D-metabolic enzymes and related molecules: Expression at the maternal-conceptus interface and the role of vitamin D in endometrial gene expression in pigs

et al. 2017

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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 maternalconceptus 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.PLOS ONE | https://doi.org/10.1371/journal.pone

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Section: Discussionmentioning

confidence: 99%

Vitamin D-metabolic enzymes and related molecules: Expression at the maternal-conceptus interface and the role of vitamin D in endometrial gene expression in pigs

et al. 2017

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“…Unlike IFN-τ (IFNT), a type I IFN produced by the conceptus and acting as a signal for maternal recognition of pregnancy by preventing endometrial production of luteolytic PGF 2α in ruminants [ 17 ], IFND and IFNG do not have an anti-luteolytic effect in pigs [ 18 ]. IFNs secreted by the conceptus trophectoderm induce many IFN-stimulated genes and class I and II major histocompatibility complex (MHC) molecules in the endometrium [ 19 – 22 ], but detailed function of IFNs at the maternal-conceptus interface is not fully understood in pigs.…”

Section: Introductionmentioning

confidence: 99%

Endometrial response to conceptus-derived estrogen and interleukin-1β at the time of implantation in pigs

Seo

Choi

et al. 2018

J Animal Sci Biotechnol

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The establishment of pregnancy is a complex process that requires a well-coordinated interaction between the implanting conceptus and the maternal uterus. In pigs, the conceptus undergoes dramatic morphological and functional changes at the time of implantation and introduces various factors, including estrogens and cytokines, interleukin-1β2 (IL1B2), interferon-γ (IFNG), and IFN-δ (IFND), into the uterine lumen. In response to ovarian steroid hormones and conceptus-derived factors, the uterine endometrium becomes receptive to the implanting conceptus by changing its expression of cell adhesion molecules, secretory activity, and immune response. Conceptus-derived estrogens act as a signal for maternal recognition of pregnancy by changing the direction of prostaglandin (PG) F2α from the uterine vasculature to the uterine lumen. Estrogens also induce the expression of many endometrial genes, including genes related to growth factors, the synthesis and transport of PGs, and immunity. IL1B2, a pro-inflammatory cytokine, is produced by the elongating conceptus. The direct effect of IL1B2 on endometrial function is not fully understood. IL1B activates the expression of endometrial genes, including the genes involved in IL1B signaling and PG synthesis and transport. In addition, estrogen or IL1B stimulates endometrial expression of IFN signaling molecules, suggesting that estrogen and IL1B act cooperatively in priming the endometrial function of conceptus-produced IFNG and IFND that, in turn, modulate endometrial immune response during early pregnancy. This review addresses information about maternal-conceptus interactions with respect to endometrial gene expression in response to conceptus-derived factors, focusing on the roles of estrogen and IL1B during early pregnancy in pigs.

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“…Works of Joyce et al (Joyce et al, ; Joyce, Burghardt, Burghardt et al, ; Joyce, Burghardt, Geisert et al, ) indicate that conceptus secretory proteins from the conceptus‐conditioned culture medium increase endometrial expression of STAT1, STAT2, IRF1, SLA1,2,3,6,7,8 , and B2M (β2 microglobulin), suggesting that IFNG and/or IFND stimulate expression of these genes in the endometrium. Our recent studies on pigs have shown that IFNG induces the endometrial expression of SLA‐DQA and SLA‐DQB (Kim et al, ), TLR7 (Yoo et al, ), and chemokines cysteine‐X‐cysteine motif chemokine ligand 9 (CXCL9), CXCL10, CXCL11, and CXCL12 (Han et al, ). These molecules are involved in endometrial immune responses and CXCL9, CXCL10, CXCL11, and CXCL12 have been indicated to regulate the recruitment of immune cells into the endometrium at the time of conceptus implantation.…”

Section: Discussionmentioning

confidence: 99%

Analysis of interferon‐γ receptor IFNGR1 and IFNGR2 expression and regulation at the maternal‐conceptus interface and the role of interferon‐γ on endometrial expression of interferon signaling molecules during early pregnancy in pigs

Yoo

Seo

Choi

et al. 2019

Molecular Reproduction Devel

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It has long been known that pig conceptuses produce interferon‐γ (IFNG) at the time of implantation, but the role of IFNG and its mechanism of action at the maternal‐conceptus interface are not fully understood. Accordingly, we analyzed the expression and regulation of IFNG receptors IFNGR1 and IFNGR2 in the endometrium during the estrous cycle and pregnancy in pigs. Levels of IFNGR1 and IFNGR2 messenger RNA (mRNA) expression changed in the endometrium, with the highest levels during mid pregnancy for IFNGR1 and on Day 12 of pregnancy for IFNGR2. The expression of IFNGR1 and IFNGR2 mRNAs was also detected in conceptuses during early pregnancy and chorioallantoic tissues during mid to late pregnancy. IFNGR1 and IFNGR2 mRNAs were localized to endometrial epithelial and stromal cells and to the chorionic membrane during pregnancy. IFNGR2 protein was also localized to endometrial epithelial and stromal cells, and increased epithelial expression of IFNGR2 mRNA and protein was detectable during early pregnancy than the estrous cycle. Explant culture studies showed that estrogen increased levels of IFNGR2, but not IFNGR1, mRNAs, while interleukin‐1β did not affect levels of IFNGR1 and IFNGR2 mRNAs. Furthermore, IFNG increased levels of IRF1, IRF2, STAT1, and STAT2 mRNAs in the endometrial explants. These results in pigs indicate that IFNGR1 and IFNGR2 are expressed in a stage of pregnancy‐ and cell‐type specific manner in the endometrium and that sequential cooperative action of conceptus signals estrogen and IFNG may be critical for endometrial responsiveness to IFNs for the establishment of pregnancy in pigs.

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Analysis of cysteine-X-cysteine motif chemokine ligands 9, 10, and 11, their receptor CXCR3, and their possible role on the recruitment of immune cells at the maternal–conceptus interface in pigs†

Cited by 42 publications

References 47 publications

Vitamin D-metabolic enzymes and related molecules: Expression at the maternal-conceptus interface and the role of vitamin D in endometrial gene expression in pigs

Vitamin D-metabolic enzymes and related molecules: Expression at the maternal-conceptus interface and the role of vitamin D in endometrial gene expression in pigs

Endometrial response to conceptus-derived estrogen and interleukin-1β at the time of implantation in pigs

Analysis of interferon‐γ receptor IFNGR1 and IFNGR2 expression and regulation at the maternal‐conceptus interface and the role of interferon‐γ on endometrial expression of interferon signaling molecules during early pregnancy in pigs

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