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Disruption of early embryo-maternal crosstalk via peptidoglycan in the infected uterus in the cow

Mohammad Ali ZINNAH 帯広畜産大学

2021.06.09

概要

Bidirectional embryo-maternal communication is critically important for appropriate maternal recognition of pregnancy and thereby establishing a successful gestation. Any alteration in maternal recognition of pregnancy may result in early embryonic loss. Bio-molecular dialogue between the embryo and mother should be started by developing bovine embryo in order to establish a suitable uterine environment that could support the growth of developing embryo leading to successful pregnancy. In case of ruminant, interferon tau (IFNT) is secreted from the trophoectoderm and acts as a signaling molecule for recognition of pregnancy.

After parturition, natural orifice such as vaginal opening remains open. Soon after parturition, bacteria present in feces, urine, and bedding materials can enter into the uterus and may cause infection.

Moreover, biodegradable materials present within the uterus after partition serve as a good media for the growth of a variety of aerobic and anaerobic bacteria. These perceptions become more complicated with the fact that the gravid uterus is not germ-free as it has been thought for many years, and it may be colonized with numerous bacteria including Trueperella pyogenes. These bacteria persistently remain within the uterus and continue to grow. As a result, peptidoglycan (PGN), the important cell component of bacteria is continuously producing as byproduct which remains within the uterine environment. It has been reported that PGN administered after 5 days of mating interrupts early pregnancy in ewes in vivo.

Therefore, I hypothesized that presence of PGN within the uterine environment has deleterious effects on embryo-derived IFNT mediated embryo-maternal immune crosstalk.

In chapter 1, I used embryo conditioned media (ECM) to see the effect of embryo culture media on bovine endometrium epithelial cells (BEECs) in presence or absence of PGN. I used this model to mimic in vivo real situation where the uterus contains persistent bacterial infection and the embryo is coming and/or transferring to that uterus. Healthy bovine uteri of luteal phage (D 7-8) were collected from local slaughterhouse for isolation and culture of epithelial cells. When the cells from second passage reached at 80-90% confluence, then cells were cultured in ECM in presence or absence of PGN for 24 h in a 38.50C incubator with 5% CO2 in humidified air. Cells without ECM or PGN served as control. BEECs were analyzed to see the mRNA expressions of ISGs (OAS1 and ISG15) and STAT1, a key factor for IFNT signaling by real-time PCR. Real-time PCR result demonstrated that ECM induced mRNA expression of ISGs (OAS1 and ISG15) and STAT1, a crucial molecule for IFNT signaling. On the other hand, presence of PGN significantly suppressed the upregulation of ISGs (OAS1 and ISG15) and STAT1 in BEECs.

Surprisingly, no modulatory effects on the mRNA expression of pro-inflammatory cytokine (TNFA and IL1B) or TLR2 were observed by PGN. The findings strongly suggest that ECM contains IFNT secreted from cultured embryos, and that PGN blocks IFNT signaling in BEEC.

In chapter 2, I investigated the direct effect of IFNT, secreted from embryos, on BEECs in vitro and endometrial explants ex-vivo in presence or absence of PGN. Similar to chapter 1, when the cells from second passage reached 80-90% confluence, cells were stimulated with IFNT in the presence or absence of PGN for 24 h. Healthy uteri of the same stage were obtained and using an 8 mm biopsy punch, disks of endometrial tissue (2 mm thick) were separated from the intercaruncular regions ipsilateral to the corpus luteum. Then explants were cultivated in Roswell Park Memorial Institute (RPMI)-1640 media supplemented with 10% fetal bovine serum (FBS) with IFNT in the presence or absence of PGN for 12 h in a 38.50C incubator with 5% CO2 in humidified air. Cells/explants without IFNT and PGN served as control. BEECs and endometrial tissues were analyzed for mRNA expressions of ISGs (OAS1 and ISG15) and STAT1, a key factor for IFNT signaling, by real-time PCR. OAS1 protein was identified by immunofluorescence in LE of endometrial explants. Gene analysis results showed that IFNT stimulated the expression of interferon stimulated genes (ISGs: OAS1, ISG15) and STAT1 in BEECs in vitro and explants ex-vivo. While the presence of PGN significantly suppressed the upregulation of ISGs and STAT1 in both models. Interestingly, PGN did not stimulate mRNA expressions of the pro-inflammatory cytokines (TNFA and IL1B) or TLR2 in BEECs or explants. I also analyzed interferon receptor 1 (IFNAR1) and IFNAR2 to see the any fold expression changes in explant. Real-time-PCR result showed no changes of mRNA expression of IFNAR1 and IFNAR2 among all groups. Further, OAS1 protein expression was detected using immunofluorescence (IF) staining in the luminal epithelia of endometrial tissue, and PGN suppressed the IFNT-triggered intensive OAS1 protein expression throughout the whole luminal epithelium.

It can be concluded that the findings of this study demonstrate that the presence of low levels of PGN suppresses early embryo-derived IFNT signals for ISGs expression in the bovine endometrium and thereby, interferes with endometrial epithelium receptivity and early embryo-maternal crosstalk in cows, which leads to pregnancy failure.

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