Cargando…

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

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 act...

Descripción completa

Detalles Bibliográficos
Autores principales: Waberski, Dagmar, Schäfer, Jana, Bölling, Alexandra, Scheld, Manon, Henning, Heiko, Hambruch, Nina, Schuberth, Hans-Joachim, Pfarrer, Christiane, Wrenzycki, Christine, Hunter, Ronald H. F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6112639/
https://www.ncbi.nlm.nih.gov/pubmed/30153288
http://dx.doi.org/10.1371/journal.pone.0202654
_version_ 1783350881920483328
author Waberski, Dagmar
Schäfer, Jana
Bölling, Alexandra
Scheld, Manon
Henning, Heiko
Hambruch, Nina
Schuberth, Hans-Joachim
Pfarrer, Christiane
Wrenzycki, Christine
Hunter, Ronald H. F.
author_facet Waberski, Dagmar
Schäfer, Jana
Bölling, Alexandra
Scheld, Manon
Henning, Heiko
Hambruch, Nina
Schuberth, Hans-Joachim
Pfarrer, Christiane
Wrenzycki, Christine
Hunter, Ronald H. F.
author_sort Waberski, Dagmar
collection PubMed
description 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.
format Online
Article
Text
id pubmed-6112639
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-61126392018-09-17 Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles Waberski, Dagmar Schäfer, Jana Bölling, Alexandra Scheld, Manon Henning, Heiko Hambruch, Nina Schuberth, Hans-Joachim Pfarrer, Christiane Wrenzycki, Christine Hunter, Ronald H. F. PLoS One Research Article 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. Public Library of Science 2018-08-28 /pmc/articles/PMC6112639/ /pubmed/30153288 http://dx.doi.org/10.1371/journal.pone.0202654 Text en © 2018 Waberski et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Waberski, Dagmar
Schäfer, Jana
Bölling, Alexandra
Scheld, Manon
Henning, Heiko
Hambruch, Nina
Schuberth, Hans-Joachim
Pfarrer, Christiane
Wrenzycki, Christine
Hunter, Ronald H. F.
Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles
title Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles
title_full Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles
title_fullStr Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles
title_full_unstemmed Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles
title_short Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles
title_sort seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6112639/
https://www.ncbi.nlm.nih.gov/pubmed/30153288
http://dx.doi.org/10.1371/journal.pone.0202654
work_keys_str_mv AT waberskidagmar seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles
AT schaferjana seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles
AT bollingalexandra seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles
AT scheldmanon seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles
AT henningheiko seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles
AT hambruchnina seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles
AT schuberthhansjoachim seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles
AT pfarrerchristiane seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles
AT wrenzyckichristine seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles
AT hunterronaldhf seminalplasmamodulatestheimmunecytokinenetworkintheporcineuterinetissueandpreovulatoryfollicles