Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles

Abstract

Evidence is emerging that the interaction between male seminal fluid and female tissues promotes fertility, pregnancy, and health of offspring. This includes the acceleration of ovulation in a species known as a spontaneous ovulator, the domestic pig. Earlier studies revealed that seminal plasma acts by a local mechanism in the female pig. The aim of the present study was to examine local short-term and mid-term effects of seminal plasma (SP) on mRNA expression of immunoregulatory genes and transcripts associated with follicle- and oocyte maturation. In the porcine animal model, effects on mRNA expression in the female tract and preovulatory follicles were examined. SP suppressed mRNA expression of Prostaglandin-Endoperoxide Synthase 2 (PTGS2) ipsilateral to the infused uterine horn which was associated with a lower presence of immune cells in the uterine epithelium and lower PTGS2 immunoreaction. Depending on the sampling time (2 h vs. 17 h) and hormonal status, SP altered significant correlative relations of mRNA expression between PTGS2 and the transcripts Tumor Necrosis Factor Alpha, Tumor Necrosis Factor Alpha-Induced Protein 6 and Pentraxin 3 in uterus, granulosa and cumulus cells. A modulatory effect of SP on the oocyte gene network comprising eight oocyte transcripts was observed: uterine exposure to SP induced positive correlations (r >0.08, p<0.05) of maturation promoting factors among each other and with cumulus cells on the side of the treated horn. In conclusion, SP orchestrates the gene network regulating the bidirectional communication between oocytes and surrounding somatic cells. The modulation of the immune-cytokine network of the female reproductive system could contribute to the previously reported SP-induced acceleration of ovulation in the porcine species.

Granulocyte-macrophage colony stimulating factor (GM-CSF) is fully expressed in the genital tract, seminal plasma and spermatozoa of male pigs

“…The WB also revealed that the active GM-CSF was in greater quantity in the SP of particular ejaculate fractions, namely the so-called “rest of the SRF” and the post-SRF, just the two pig ejaculate portions gathering most of the secretion from prostate and seminal vesicles 35 . The GM-CSF is a key regulator of the immune and inflammatory response 36 and its presence in SP would be involved in the positive effects exerted by SP on the uterus of sows for promoting an initial, transient inflammation, probably mostly directed to eventual pathogens; but also influencing both sperm survival and embryo development 13 , 37 . In this context, it is well known that GM-CSF is a cytokine that improves embryo development and the establishment of pregnancy in rodents 38 .…”

Defining the male contribution to embryo quality and offspring health in assisted reproduction in farm animals

“…Here, unwashed boar sperm held at 15 o C for 24 to 72 hours in commercial GEPS extender showed significantly higher motility, survival and integrity of the acrosome prior to preservation when compared to washed sperm held in GEPS alone (Chutia et al, 2014). Interestingly, uterine seminal plasma deposition in the pig has been shown to not only influence uterine prostaglandin synthesis gene (PTGS2) expression but also the expression of multiple maturation promotion factors within the oocyte, cumulus and granulosa cells within the ovary (Waberski et al, 2018). Furthermore, uterine inflammatory responses persist for up to 8 days post seminal plasma infusion (O'Leary et al, 2004) and significant increases in the number of viable embryos being collected post insemination have been reported in the pig (O'Leary et al, 2004).…”

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

“…In the pig, the SP shortens the LH peak-to-ovulation interval [4], advancing ovulation [5], and supports luteal development and, consequently, the synthesis of progesterone [6]. In addition, the SP induces endometrial changes in the expression of numerous genes related to maternal immunity during the peri-ovulation period [7,8]. In rodents, SP infusions at estrus support pre-implantation embryonic development and implantation [9], by likely modifying the release of cytokines that support embryonic development, and by inducing the expression of factors associated with angiogenesis and chorionic attachment [10].…”