Abstract
Dendritic cells (DCs) are essential for successful embryo implantation. However, the properties of uterine DCs (uDCs) during the implantation period are not well characterized. In this study, we investigated the dynamic changes in the uDC phenotypes during the period between coitus and implantation. In virgin mice, we evaluated the expressions of CD103 and XCR1, this is the first report to demonstrate uDCs expressing CD103 in XCR1+cDC1s and XCR1+cDC2s. On day 0.5 post coitus (pc), the number of uterine CD11c+CD103–MHC classIIhighCD86high–mature DCs rapidly increased and then decreased to non-pregnancy levels on days 1.5 and 2.5 pc. On day 3.5 pc just before implantation, the number of CD11c+CD103+MHC class IIdimCD86dim–immature DCs increased in the uterus. The increase in mature uDCs on day 1.5 pc was observed in both allogeneic- and syngeneic mating, suggesting that sexual intercourse, or semen, play a role in this process. Meanwhile, the increase in immature uDCs on day 3.5 pc was only observed in allogeneic mating, suggesting that allo-antigens in the semen contribute to this process. Next, to understand the turnover and migration of uDCs, we monitored DC movement in the uterus and uterine draining lymph nodes (dLNs) using photoconvertible protein Kikume Green Red (KikGR) mice. On day 0.5 pc, uDCs were composed of equal numbers of remaining DCs and migratory DCs. However, on day 3.5 pc, uDCs were primarily composed of migratory DCs, suggesting that most of the uDCs migrate from the periphery just before implantation. Finally, we studied the expression of PD-L2—which induces immunoregulation—on DCs. On day 3.5 pc, PD-L2 was expressed on CD103+-mature and CD103–-mature DCs in the uterus. However, PD-L2 expression on CD103–-immature DCs and CD103+-immature DCs was very low. Furthermore, both remaining and migratory DCs in the uterus and uterus-derived-DCs in the dLNs on day 3.5 pc highly expressed PD-L2 on their surface. Therefore, our study findings provide a better understanding of the dynamic changes occurring in uterine DCs and dLNs in preparation for implantation following allogeneic- and syngeneic mating.
Highlights
Dendritic cells (DCs) play an essential role in successful implantation and placentation in allogeneic- and syngeneic pregnancy [1,2,3,4]
The proportion of each DC subset in virgin mice showed that the majority of uterine DCs (uDCs) were CD103− DCs (79.0%), followed by CD103+ DCs (17.8%), while plasmacytoid DCs (pDCs) (3.3%) were in minority (Supplementary Figure 1C)
We showed that there is a transient increase in CD11c+ CD86high MHC class IIhigh Ly6C− PDCA-1dim CD11b+ CD103−-mature uDCs on day 0.5 pc, and CD11c+ CD86dim MHC class IIdim Ly6C− PDCA-1dim CD11b− CD103+immature uDCs on day 3.5 pc
Summary
Dendritic cells (DCs) play an essential role in successful implantation and placentation in allogeneic- and syngeneic pregnancy [1,2,3,4]. The essential role of uDCs in the maintenance of feto-maternal tolerance during pregnancy has been examined. IDO-expressing DCs and plasmacytoid DCs (pDCs) act as tolerogenic DCs (tDCs) [4]. These tDCs have been shown to possess the capability of immunoregulation by inducing Tregs, as well as T cell, anergy and deletion [6, 14, 15]. Few reports have examined the characteristics of uDC subsets in murine pregnancy [2, 4, 16,17,18,19,20,21,22]
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