Seminal Plasma Modifies the Transcriptional Pattern of the Endometrium and Advances Embryo Development in Pigs

Martínez, Cristina A.; Cambra, Josep M.; Parrilla, Inmaculada; Roca, Jordi; Ferreira‐Dias, Graça; Pallarés, F. J.; Lucas, Xiomara; Vázquez, J.M.; Martı́nez, Emilio A.; Gil, M.A.; Rodriguez‐Martinez, Heriberto; Cuello, C.; Álvarez‐Rodríguez, Manuel

doi:10.3389/fvets.2019.00465

Cited by 30 publications

(34 citation statements)

References 88 publications

(87 reference statements)

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“…These findings suggest that application of SP in ET-protocols could increase ET-outcomes by increasing the number of embryos succeeding during the crucial implantation window. Such a statement is based on the confirmation of previous findings [18,19,21], indicating that the effects of SP remain influential over time. Particularly, SP infusions at estrus advance embryonic development, and alters the expression of the endometrial genes and pathways potentially involved in embryonic development and maternal immune system tolerance during early pregnancy [19].…”

Section: Discussionmentioning

confidence: 52%

“…In pigs, SP infusions during estrus influenced the uterine environment during at least the first nine days of pregnancy, with changes of specific endometrial cytokines known to promote embryo development and implantation [18]. Our own findings revealed that SP infusions during estrus not only advance embryo development in pigs, but also change the global endometrial transcriptome at Day 6 of pregnancy [19]. This particular study showed >1600 endometrial transcripts differentially expressed in SP-treated endometrium compared to controls, depicting overrepresentation of genes and pathways potentially involved in embryo development and implantation, such as immune response, cytokine signaling, cell cycle, cell adhesion and hormone response [19].…”

Section: Introductionmentioning

confidence: 60%

“…Our own findings revealed that SP infusions during estrus not only advance embryo development in pigs, but also change the global endometrial transcriptome at Day 6 of pregnancy [19]. This particular study showed >1600 endometrial transcripts differentially expressed in SP-treated endometrium compared to controls, depicting overrepresentation of genes and pathways potentially involved in embryo development and implantation, such as immune response, cytokine signaling, cell cycle, cell adhesion and hormone response [19]. These results re-confirmed the long-lasting effects of porcine SP estrus-infusions throughout the preimplantation period, suggesting SP-use has a potential application value in ET technology, optimizing ET procedures in both donor and recipient females.…”

Section: Introductionmentioning

confidence: 74%

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

Martínez

Cambra

Gil

et al. 2020

IJMS

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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.

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Section: Discussionmentioning

confidence: 52%

Section: Introductionmentioning

confidence: 60%

Section: Introductionmentioning

confidence: 74%

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

Martínez

Cambra

Gil

et al. 2020

IJMS

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“…Nevertheless, several factors could be involved in this fact. First, it has been shown that seminal plasma proteins and other components activated changes in the gene expression of the endometrium [44,46,47]; but in our study, the level of seminal plasma in the insemination dose was low because the ejaculate was diluted in commercial extender, so its impact on the genomic expression of the endometrium could be limited. Second, although uterus is colonized by the sperm within minutes after deposition [48] the differences detected in gene expression were evaluated 24 h after semen deposition [43][44][45], while our measurements were carried out only 2 hours after insemination.…”

Section: Discussionmentioning

confidence: 67%

In vivo measurement of pH, CO2 and HCO3- levels in the uterus of non-anesthetized sows through the estrous cycle and after insemination

López-Albors¹,

Llamas-López²,

Ortuño³

et al. 2020

Preprint

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Background The pH-CO2-HCO3− system is a ubiquitous biological regulator with important functional implications for reproduction. Knowledge of the physiological values of its components is relevant for reproductive biology and the optimization of Assistant Reproductive Techniques (ARTs). In vivo pH of the oviduct and uterus has been estimated by direct in situ measurements in a few species. However, regarding the levels of CO2 and HCO3−, information is very scarce and, when available, it comes from fluid samples instead of in vivo estimations. This study describes a non-invasive method to measure pH and % of CO2 in the uterus of sows with cutting-edge technology and no medication. Sows were at three different reproductive conditions, estrous with no insemination E(-)AI and after insemination E(+)AI, and diestrous (non-estrous, NE). From pH and CO2 data, HCO3− concentration was estimated. Results The designed methodology allowed for in situ time-lapse recording of pH and % of CO2 within the uterus of non-anesthetized sows. Variable oscillatory patterns of pH, CO2 and HCO3− were found independently of the estrous condition. Insemination did not changed the levels of uterine pH, % of CO2 and HCO3− concentration, -E(-)AI = E(+)AI-, but all the values were affected by the estrous cycle in a way that decreased significantly at diestrous condition - E(-)AI and E(+)AI > NE-. Conclusions A non-invasive approach to the porcine uterus with novel optical probes allowed the obtaining of in situ physiological values of pH, CO2, and HCO3− at different reproductive conditions. While the short-time presence of sperm in the uterus did not change the physiological milieu, the whole pH-CO2-HCO3− system was affected by the estrous cycle. This study contributes to a better understanding of the in vivo regulation of the pH/CO2/HCO3− system in the uterus and may help to optimize the protocols of sperm treatment for in vitro fertilization.

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“…However, semen has, by its specific sperm-and SP constituents proven able to induce major changes in the expression of genes in tissues of the internal genital tract alongside fertilization, in animal classes as disparate as insects or pigs [9]. Such changes clearly indicate pathways governing sperm transport [10], ovulation [11], sperm storage [4,6,12], sperm capacitation [12,13] and gamete encounter [14], processes that apparently continue during early embryo development and-for Eutheria-with placental development and pregnancy [11,15]. To complicate matters, while fertilization can be achieved without the intervention of immune responses, immunity modulation is apparently crucial to tolerate the presence of a foreign cell (the spermatozoon) and the proteins it and the accompanying SP carries in a female whose innate and adaptative immune system is prompt in eliminating both pathogens and foreign antigens.…”

Section: Introductionmentioning

confidence: 99%

Does the Act of Copulation per se, without Considering Seminal Deposition, Change the Expression of Genes in the Porcine Female Genital Tract?

Álvarez‐Rodríguez

Martínez

Wright

et al. 2020

IJMS

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Semen—through its specific sperm and seminal plasma (SP) constituents—induces changes of gene expression in the internal genital tract of pigs, particularly in the functional sperm reservoir at the utero-tubal junction (UTJ). Although seminal effects are similarly elicited by artificial insemination (AI), major changes in gene expression are registered after natural mating, a fact suggesting the act of copulation induces per se changes in genes that AI does not affect. The present study explored which pathways were solely influenced by copulation, affecting the differential expression of genes (DEGs) of the pre/peri-ovulatory genital tract (cervix, distal uterus, proximal uterus and UTJ) of estrus sows, 24 h after various procedures were performed to compare natural mating with AI of semen (control 1), sperm-free SP harvested from the sperm-peak fraction (control 2), sperm-free SP harvested from the whole ejaculate (control 3) or saline-extender BTS (control 4), using a microarray chip (GeneChip® porcine gene 1.0 st array). Genes related to neuroendocrine responses (ADRA1, ADRA2, GABRB2, CACNB2), smooth muscle contractility (WNT7A), angiogenesis and vascular remodeling (poFUT1, NTN4) were, among others, overrepresented with distal and proximal uterine segments exhibiting the highest number of DEGs. The findings provide novel evidence that relevant transcriptomic changes in the porcine female reproductive tract occur in direct response to the specific act of copulation, being semen-independent.

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Seminal Plasma Modifies the Transcriptional Pattern of the Endometrium and Advances Embryo Development in Pigs

Cited by 30 publications

References 88 publications

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

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

In vivo measurement of pH, CO2 and HCO3- levels in the uterus of non-anesthetized sows through the estrous cycle and after insemination

Does the Act of Copulation per se, without Considering Seminal Deposition, Change the Expression of Genes in the Porcine Female Genital Tract?

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