Seminal Plasma Induces Overexpression of Genes Associated with Embryo Development and Implantation in Day-6 Porcine Blastocysts

Abstract

The infusion of boar seminal plasma (SP) before artificial insemination (AI) positively alters the expression of endometrial genes and pathways involved in embryo development. This study aimed to determine which transcriptome changes occur in preimplantation embryos in response to SP infusions during estrus. Postweaning estrus sows received 40-mL intrauterine infusions of either SP (N = 6) or BTS extender (control group; N = 6) 30 min before each of two post-cervical AIs. On Day 6, embryos were surgically collected and analyzed for differential gene expression. Microarray analysis of embryos revealed 210 annotated genes, differentially expressed (p-value < 0.05 and fold change </> 2) in SP-blastocysts, compared to controls. Most of these genes were associated with biological, cellular, metabolic and developmental processes. The pathways enriched among the upregulated genes related to signal transduction, cellular processes and the endocrine system. Among altered genes involved in these pathways, the SP-group showed a conspicuous overexpression of ApoA-I, CDK1, MAPK1, SMAD2, PRKAA1 and RICTOR, with reported key roles in embryo development, implantation, or progression of pregnancy. In conclusion, the results demonstrate that SP infusions prior to AI upregulates the expression of embryo development related genes in Day 6 pig embryos.

Intrauterine Infusion of TGF-β1 Prior to Insemination, Alike Seminal Plasma, Influences Endometrial Cytokine Responses but Does Not Impact the Timing of the Progression of Pre-Implantation Pig Embryo Development

“…Our results further indicate that cytokine production by endometrial explants was affected by the different infusion treatments administered prior to AI and that different patterns of expression between experimental groups were detected as far out as 6 days after the treatments. These results were not unexpected, as SP infusions pre-AI also altered the transcriptome of the endometrium and blastocysts six days later [ 22 , 23 ].…”

“…These findings confirmed previous studies indicating that the effect of SP administration at estrus is not only immediate [ 20 , 21 ] but also remains during the preimplantation time [ 22 , 24 ] and modifies the timing of embryo development [ 22 ]. Although the advanced embryo development detected in the SP group might be related to the influence that SP has on the time of ovulation [ 5 , 6 , 7 ], recent studies suggest that the timing of embryo development is controlled and modified at the molecular level by a possible direct effect of SP [ 22 , 23 ]. First, SP infused during estrus modifies the endometrial transcriptome on day 6 of gestation, upregulating the genes and pathways that are closely related to embryo development and maternal immune system tolerance [ 22 ]; second, such SP infusions also upregulate the expression of genes and pathways in day 6 blastocysts that are linked to processes that control embryonic development, implantation, or the progression of pregnancy [ 23 ].…”

“…Although the advanced embryo development detected in the SP group might be related to the influence that SP has on the time of ovulation [ 5 , 6 , 7 ], recent studies suggest that the timing of embryo development is controlled and modified at the molecular level by a possible direct effect of SP [ 22 , 23 ]. First, SP infused during estrus modifies the endometrial transcriptome on day 6 of gestation, upregulating the genes and pathways that are closely related to embryo development and maternal immune system tolerance [ 22 ]; second, such SP infusions also upregulate the expression of genes and pathways in day 6 blastocysts that are linked to processes that control embryonic development, implantation, or the progression of pregnancy [ 23 ]. Altogether, these molecular modifications might modulate the endometrial secretions of embryotrophic molecules that protect and nurture the conceptuses during its free-floating period prior to implantation.…”

“…Thus, among other actions, the SP promotes the release of cytokines that support the development of preimplantation embryos and the induction of the expression of factors related to angiogenesis and attachment processes, all of which relates to the attainment of the status of maternal immune tolerance to hemiallogeneic embryos [ 19 ]. Interestingly, the exposure of the uterus to SP during estrus not only induced endometrial changes in multiple genes and pathways during the periovulation time [ 20 , 21 ] but also modified the endometrial and the blastocyst transcriptomes on day 6 of pregnancy by upregulating numerous genes related to immune pathways, embryonic development, and implantation [ 22 , 23 ]. These and other results [ 24 ] clearly demonstrate that the effects of SP infusions during estrus remain influential over time and affect subsequent events related to pre-implantation embryo development and implantation.…”

Seminal Plasma Triggers the Differential Expression of the Glucocorticoid Receptor (NR3C1/GR) in the Rabbit Reproductive Tract

“…SP is produced by sexual accessory glands together with secretions from the epididymis [ 54 ] and, in rabbits, it seems to play a role in spermatozoa protection, fertilization [ 55 ] and also immune modulation during development [ 56 ]. After natural mating and sperm-free SP infusion [ 17 ], the female reproductive tract undergoes a variety of modifications that influence the initiation of controlled inflammatory response, ovulation stimulation, changes in the transcription of genes related to reproductive stages [ 50 ] and early embryonic development [ 57 , 58 ]. Thus, even when the SP, deposited in the cervix, does not directly reach the upper regions of the oviduct such as the infundibulum, proteins of this fluid may be absorbed by the endometrium and achieve the ovary via lymphatic route or, alternatively, by activating signaling cascades [ 59 ] that may modify the ovulation in rabbit [ 60 ].…”