Semen Modulates Cell Proliferation and Differentiation-Related Transcripts in the Pig Peri-Ovulatory Endometrium
by
, , , , , and
Jaume Gardela
1,2,†
,
Mateo Ruiz-Conca
1,2,†,
Dominic Wright
3
,
Manel López-Béjar
2,4
,
Cristina A. Martínez
1
,
Heriberto Rodríguez-Martínez
1,*,‡
and
Manuel Álvarez-Rodríguez
1,2,‡
1
Department of Biomedical & Clinical Sciences (BKV), BKH/Obstetrics & Gynecology, Faculty of Medicine and Health Sciences, Linköping University, 58185 Linköping, Sweden
2
Department of Animal Health and Anatomy, Veterinary Faculty, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain
3
Department of Physics, Chemistry and Biology, Faculty of Science and Engineering, Linköping University, 58185 Linköping, Sweden
4
College of Veterinary Medicine, Western University of Health Sciences, Pomona, CA 91766, USA
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
‡
These authors contributed equally to this work.
Biology 2022, 11(4), 616; https://doi.org/10.3390/biology11040616
Submission received: 11 March 2022
/
Revised: 6 April 2022
/
Accepted: 16 April 2022
/
Published: 18 April 2022
Simple Summary
Homeostasis of the uterus after mating is crucial for the subsequent reproductive events. The post-mating inflammatory response is restricted to the uterus, but semen also modulates the expression of other genes involved in regulation along the female reproductive tract, including the oviduct. This study aims to determine if several ejaculate fractions of the pig may modulate cell proliferation and differentiation-related transcripts in different sections of the peri-ovulatory sow reproductive tract. Our data demonstrate that most of the mRNA expression changes of the 144 transcripts tested were induced by mating. Additionally, spermatozoa and seminal plasma also triggered differential expression of the transcripts tested. Finally, our data imply that spermatozoa, seminal plasma components, and the act of mating induce differential mechanisms in the peri-ovulatory female reproductive tract, which are essential for tissue repair.
Abstract
Uterine homeostasis is maintained after mating by eliminating pathogens, foreign cells, and proteins by a transient inflammation of the uterus. Such inflammation does not occur in the oviductal sperm reservoir (utero-tubal junction, UTJ), colonized by a population of potentially fertile spermatozoa before the inflammatory changes are triggered. Semen entry (spermatozoa and/or seminal plasma) modifies the expression of regulatory genes, including cell proliferation and differentiation-related transcripts. Considering pigs display a fractionated ejaculation, this study aims to determine whether different ejaculate fractions differentially modulate cell proliferation and differentiation-related transcripts in the sow reproductive tract during the peri-ovulatory stage. Using species-specific microarray analyses, the differential expression of 144 cell proliferation and differentiation-related transcripts was studied in specific segments: cervix (Cvx), distal and proximal uterus (DistUt, ProxUt), UTJ, isthmus (Isth), ampulla (Amp), and infundibulum (Inf) of the peri-ovulatory sow reproductive tract in response to semen and/or seminal plasma cervical deposition. Most mRNA expression changes were induced by mating. In addition, while mating upregulates the fibroblast growth factor 1 (FGF1, p-value DistUt = 0.0007; ProxUt = 0.0253) transcript in the endometrium, both its receptor, the fibroblast growth factor receptor 1 (FGFR1, p-value DistUt = 2.14 e−06; ProxUt = 0.0027; UTJ = 0.0458) transcript, and a potentiator of its biological effect, the fibroblast growth factor binding protein 1 (FGFBP1), were downregulated in the endometrium (p-value DistUt = 0.0068; ProxUt = 0.0011) and the UTJ (p-value UTJ = 0.0191). The FGFBP1 was downregulated in the whole oviduct after seminal depositions (p-value Isth = 0.0007; Amp = 0.0007; Inf = 6.87 e−05) and, interestingly, FGFR1 was downregulated in the endometrium in the absence of semen (p-value DistUt = 0.0097; ProxUt = 0.0456). In conclusion, the findings suggest that spermatozoa, seminal components, and the act of mating trigger, besides inflammation, differential mechanisms in the peri-ovulatory female reproductive tract, relevant for tissue repair.
