Cell type-specific endometrial transcriptome changes during initial recognition of pregnancy in the mare
Iside Scaravaggi A B , Nicole Borel C , Rebekka Romer A , Isabel Imboden A , Susanne E. Ulbrich B , Shuqin Zeng A B , Heinrich Bollwein A and Stefan Bauersachs
A B D
+ Author Affiliations
- Author Affiliations
A Clinic of Reproductive Medicine, Department for Farm Animals, University of Zurich, Winterthurerstrasse 260, 8057 Zurich, Switzerland.
B Animal Physiology, Institute of Agricultural Sciences, ETH Zurich, Universitätstrasse 2, 8092 Zurich, Switzerland.
C Institute of Veterinary Pathology, University of Zurich, Winterthurerstrasse 260, 8057 Zurich, Switzerland.
D Corresponding author. Email: stefan.bauersachs@uzh.ch
Reproduction, Fertility and Development 31(3) 496-508 https://doi.org/10.1071/RD18144
Submitted: 17 April 2018 Accepted: 27 August 2018 Published: 26 September 2018
Abstract
Previous endometrial gene expression studies during the time of conceptus migration did not provide final conclusions on the mechanisms of maternal recognition of pregnancy (MRP) in the mare. This called for a cell type-specific endometrial gene expression analysis in response to embryo signals to improve the understanding of gene expression regulation in the context of MRP. Laser capture microdissection was used to collect luminal epithelium (LE), glandular epithelium and stroma from endometrial biopsies from Day 12 of pregnancy and Day 12 of the oestrous cycle. RNA sequencing (RNA-Seq) showed greater expression differences between cell types than between pregnant and cyclic states; differences between the pregnant and cyclic states were mainly found in LE. Comparison with a previous RNA-Seq dataset for whole biopsy samples revealed the specific origin of gene expression differences. Furthermore, genes specifically differentially expressed (DE) in one cell type were found that were not detectable as DE in biopsies. Overall, this study revealed spatial information about endometrial gene expression during the phase of initial MRP. The conceptus induced changes in the expression of genes involved in blood vessel development, specific spatial regulation of the immune system, growth factors, regulation of prostaglandin synthesis, transport prostaglandin receptors, specifically prostaglandin F receptor (PTGFR) in the context of prevention of luteolysis.
Additional keywords: Equus caballus, laser capture microdissection, maternal recognition of pregnancy, RNA-seq, uterus.
References
Ababneh, M. M., and Troedsson, M. H. (2013). Ovarian steroid regulation of endometrial phospholipase A2 isoforms in horses. Reprod. Domest. Anim. 48, 311–316.| Ovarian steroid regulation of endometrial phospholipase A2 isoforms in horses.Crossref | GoogleScholarGoogle Scholar |
Agrotis, A., Kanellakis, P., Kostolias, G., Di Vitto, G., Wei, C., Hannan, R., Jennings, G., and Bobik, A. (2004). Proliferation of neointimal smooth muscle cells after arterial injury. Dependence on interactions between fibroblast growth factor receptor-2 and fibroblast growth factor-9. J. Biol. Chem. 279, 42221–42229.
| Proliferation of neointimal smooth muscle cells after arterial injury. Dependence on interactions between fibroblast growth factor receptor-2 and fibroblast growth factor-9.Crossref | GoogleScholarGoogle Scholar |
Allen, W. R. (2001a). Fetomaternal interactions and influences during equine pregnancy. Reproduction 121, 513–527.
| Fetomaternal interactions and influences during equine pregnancy.Crossref | GoogleScholarGoogle Scholar |
Allen, W. R. (2001b). Luteal deficiency and embryo mortality in the mare. Reprod. Domest. Anim. 36, 121–131.
| Luteal deficiency and embryo mortality in the mare.Crossref | GoogleScholarGoogle Scholar |
Allen, W. R., and Wilsher, S. (2009). A review of implantation and early placentation in the mare. Placenta 30, 1005–1015.
| A review of implantation and early placentation in the mare.Crossref | GoogleScholarGoogle Scholar |
Atli, M. O., Kurar, E., Kayis, S. A., Aslan, S., Semacan, A., Celik, S., and Guzeloglu, A. (2010). Evaluation of genes involved in prostaglandin action in equine endometrium during estrous cycle and early pregnancy. Anim. Reprod. Sci. 122, 124–132.
| Evaluation of genes involved in prostaglandin action in equine endometrium during estrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar |
Aurich, C. (2008) Manipulation des Sexualzyklus bei der Stute. In ‘Reproduktionsmedizin beim Pferd’. (Ed. X. Parey.) pp 53–70. (Thieme: Stuttgart, Germany.)
Baker, C. B., Adams, M. H., and McDowell, K. J. (1991). Lack of expression of alpha or omega interferons by the horse conceptus. J. Reprod. Fertil. Suppl. 44, 439–443.
Bardou, P., Mariette, J., Escudie, F., Djemiel, C., and Klopp, C. (2014). jvenn: an interactive Venn diagram viewer. BMC Bioinformatics 15, 293.
| jvenn: an interactive Venn diagram viewer.Crossref | GoogleScholarGoogle Scholar |
Bauersachs, S., and Wolf, E. (2012). Transcriptome analyses of bovine, porcine and equine endometrium during the pre-implantation phase. Anim. Reprod. Sci. 134, 84–94.
| Transcriptome analyses of bovine, porcine and equine endometrium during the pre-implantation phase.Crossref | GoogleScholarGoogle Scholar |
Bauersachs, S., and Wolf, E. (2015). Uterine responses to the preattachment embryo in domestic ungulates: recognition of pregnancy and preparation for implantation. Annu. Rev. Anim. Biosci. 3, 489–511.
| Uterine responses to the preattachment embryo in domestic ungulates: recognition of pregnancy and preparation for implantation.Crossref | GoogleScholarGoogle Scholar |
Bauersachs, S., Ulbrich, S. E., Gross, K., Schmidt, S. E., Meyer, H. H., Wenigerkind, H., Vermehren, M., Sinowatz, F., Blum, H., and Wolf, E. (2006). Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity. Reproduction 132, 319–331.
| Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity.Crossref | GoogleScholarGoogle Scholar |
Bazer, F. W. (2013). Pregnancy recognition signaling mechanisms in ruminants and pigs. J. Anim. Sci. Biotechnol. 4, 23.
| Pregnancy recognition signaling mechanisms in ruminants and pigs.Crossref | GoogleScholarGoogle Scholar |
Beinrohr, L., Murray-Rust, T. A., Dyksterhuis, L., Zavodszky, P., Gal, P., Pike, R. N., and Wijeyewickrema, L. C. (2011). Serpins and the complement system. Methods Enzymol. 499, 55–75.
| Serpins and the complement system.Crossref | GoogleScholarGoogle Scholar |
Betteridge, K. J. (2000). Comparative aspects of equine embryonic development. Anim. Reprod. Sci. 60–61, 691–702.
| Comparative aspects of equine embryonic development.Crossref | GoogleScholarGoogle Scholar |
Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P., Tosolini, M., Kirilovsky, A., Fridman, W. H., Pages, F., Trajanoski, Z., and Galon, J. (2009). ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25, 1091–1093.
| ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks.Crossref | GoogleScholarGoogle Scholar |
Brooks, K., Burns, G. W., Moraes, J. G., and Spencer, T. E. (2016). Analysis of the uterine epithelial and conceptus transcriptome and luminal fluid proteome during the peri-implantation period of pregnancy in sheep. Biol. Reprod. 95, 88.
| Analysis of the uterine epithelial and conceptus transcriptome and luminal fluid proteome during the peri-implantation period of pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |
Clark, D. A., Arredondo, J. L., and Dhesy-Thind, S. (2015). The CD200 tolerance-signaling molecule and its receptor, CD200R1, are expressed in human placental villus trophoblast and in peri-implant decidua by 5 weeks’ gestation. J. Reprod. Immunol. 112, 20–23.
| The CD200 tolerance-signaling molecule and its receptor, CD200R1, are expressed in human placental villus trophoblast and in peri-implant decidua by 5 weeks’ gestation.Crossref | GoogleScholarGoogle Scholar |
Cochet, M., Vaiman, D., and Lefevre, F. (2009). Novel interferon delta genes in mammals: cloning of one gene from the sheep, two genes expressed by the horse conceptus and discovery of related sequences in several taxa by genomic database screening. Gene 433, 88–99.
| Novel interferon delta genes in mammals: cloning of one gene from the sheep, two genes expressed by the horse conceptus and discovery of related sequences in several taxa by genomic database screening.Crossref | GoogleScholarGoogle Scholar |
Cross, J. C., Simmons, D. G., and Watson, E. D. (2003). Chorioallantoic morphogenesis and formation of the placental villous tree. Ann. N. Y. Acad. Sci. 995, 84–93.
| Chorioallantoic morphogenesis and formation of the placental villous tree.Crossref | GoogleScholarGoogle Scholar |
Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., and Lempicki, R. A. (2003). DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, 3.
| DAVID: Database for Annotation, Visualization, and Integrated Discovery.Crossref | GoogleScholarGoogle Scholar |
de Ruijter-Villani, M., van Boxtel, P. R., and Stout, T. A. (2013). Fibroblast growth factor-2 expression in the preimplantation equine conceptus and endometrium of pregnant and cyclic mares. Theriogenology 80, 979–989.
| Fibroblast growth factor-2 expression in the preimplantation equine conceptus and endometrium of pregnant and cyclic mares.Crossref | GoogleScholarGoogle Scholar |
de Ruijter-Villani, M., van Tol, H. T., and Stout, T. A. (2015). Effect of pregnancy on endometrial expression of luteolytic pathway components in the mare. Reprod. Fertil. Dev. 27, 834–845.
| Effect of pregnancy on endometrial expression of luteolytic pathway components in the mare.Crossref | GoogleScholarGoogle Scholar |
Dorniak, P., Bazer, F. W., and Spencer, T. E. (2011). Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biol. Reprod. 84, 1119–1127.
| Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium.Crossref | GoogleScholarGoogle Scholar |
Dorniak, P., Bazer, F. W., Wu, G., and Spencer, T. E. (2012). Conceptus-derived prostaglandins regulate endometrial function in sheep. Biol. Reprod. 87, 9.
| Conceptus-derived prostaglandins regulate endometrial function in sheep.Crossref | GoogleScholarGoogle Scholar |
Field, S. L., Cummings, M., and Orsi, N. M. (2015). Epithelial and stromal-specific immune pathway activation in the murine endometrium post-coitum. Reproduction 150, 127–138.
| Epithelial and stromal-specific immune pathway activation in the murine endometrium post-coitum.Crossref | GoogleScholarGoogle Scholar |
Filant, J., and Spencer, T. E. (2013). Cell-specific transcriptional profiling reveals candidate mechanisms regulating development and function of uterine epithelia in mice. Biol. Reprod. 89, 86.
| Cell-specific transcriptional profiling reveals candidate mechanisms regulating development and function of uterine epithelia in mice.Crossref | GoogleScholarGoogle Scholar |
Frontini, M. J., Nong, Z., Gros, R., Drangova, M., O’Neil, C., Rahman, M. N., Akawi, O., Yin, H., Ellis, C. G., and Pickering, J. G. (2011). Fibroblast growth factor 9 delivery during angiogenesis produces durable, vasoresponsive microvessels wrapped by smooth muscle cells. Nat. Biotechnol. 29, 421–427.
| Fibroblast growth factor 9 delivery during angiogenesis produces durable, vasoresponsive microvessels wrapped by smooth muscle cells.Crossref | GoogleScholarGoogle Scholar |
Garrido-Gomez, T., Dominguez, F., Quinonero, A., Estella, C., Vilella, F., Pellicer, A., and Simon, C. (2012). Annexin A2 is critical for embryo adhesiveness to the human endometrium by RhoA activation through F-actin regulation. FASEB J. 26, 3715–3727.
| Annexin A2 is critical for embryo adhesiveness to the human endometrium by RhoA activation through F-actin regulation.Crossref | GoogleScholarGoogle Scholar |
Giardine, B., Riemer, C., Hardison, R. C., Burhans, R., Elnitski, L., Shah, P., Zhang, Y., Blankenberg, D., Albert, I., Taylor, J., Miller, W., Kent, W. J., and Nekrutenko, A. (2005). Galaxy: a platform for interactive large-scale genome analysis. Genome Res. 15, 1451–1455.
| Galaxy: a platform for interactive large-scale genome analysis.Crossref | GoogleScholarGoogle Scholar |
Goff, A. K., Pontbriand, D., and Sirois, J. (1987). Oxytocin stimulation of plasma 15-keto-13,14-dihydro prostaglandin F-2 alpha during the oestrous cycle and early pregnancy in the mare. J. Reprod. Fertil. Suppl. 35, 253–260.
Guo, L., Li, S. Y., Ji, F. Y., Zhao, Y. F., Zhong, Y., Lv, X. J., Wu, X. L., and Qian, G. S. (2014). Role of Angptl4 in vascular permeability and inflammation. Inflamm. Res. 63, 13–22.
| Role of Angptl4 in vascular permeability and inflammation.Crossref | GoogleScholarGoogle Scholar |
Hayes, M. A., Quinn, B. A., Keirstead, N. D., Katavolos, P., Waelchli, R. O., and Betteridge, K. J. (2008). Proteins associated with the early intrauterine equine conceptus. Reprod. Domest. Anim. 43, 232–237.
| Proteins associated with the early intrauterine equine conceptus.Crossref | GoogleScholarGoogle Scholar |
Hayes, A. M., Quinn, B. A., Lillie, B. N., Côté, O., Bienzle, D., Waelchli, R. O., and Betteridge, K. J. (2012). Changes in various endometrial proteins during cloprostenol-induced failure of early pregnancy in mares. Anim. Reprod. 9, 723–741.
Jang, H., Choi, Y., Yoo, I., Han, J., Kim, M., and Ka, H. (2017). Expression and regulation of prostaglandin transporters, ATP-binding cassette, subfamily C, member 1 and 9, and solute carrier organic anion transporter family, member 2A1 and 5A1 in the uterine endometrium during the estrous cycle and pregnancy in pigs. Asian-Australas. J. Anim. Sci. 30, 643–652.
| Expression and regulation of prostaglandin transporters, ATP-binding cassette, subfamily C, member 1 and 9, and solute carrier organic anion transporter family, member 2A1 and 5A1 in the uterine endometrium during the estrous cycle and pregnancy in pigs.Crossref | GoogleScholarGoogle Scholar |
Ka, H., Seo, H., Kim, M., Choi, Y., and Lee, C. K. (2009). Identification of differentially expressed genes in the uterine endometrium on day 12 of the estrous cycle and pregnancy in pigs. Mol. Reprod. Dev. 76, 75–84.
| Identification of differentially expressed genes in the uterine endometrium on day 12 of the estrous cycle and pregnancy in pigs.Crossref | GoogleScholarGoogle Scholar |
Kenney, R. M., and Doig, P. A. (1986) Equine endometrial biopsy. In ‘Current Therapy in Theriogenology’. (Eds RM Kenney, PA Doig.) pp. 723–729. (W.B. Saunders: Philadelphia, PA, USA.)
Klein, C. (2015). Novel equine conceptus–endometrial interactions on Day 16 of pregnancy based on RNA sequencing. Reprod. Fertil. Dev. 28, 1712–1720.
| Novel equine conceptus–endometrial interactions on Day 16 of pregnancy based on RNA sequencing.Crossref | GoogleScholarGoogle Scholar |
Klein, C., Scoggin, K. E., Ealy, A. D., and Troedsson, M. H. (2010). Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy. Biol. Reprod. 83, 102–113.
| Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Klohonatz, K. M., Hess, A. M., Hansen, T. R., Squires, E. L., Bouma, G. J., and Bruemmer, J. E. (2015). Equine endometrial gene expression changes during and after maternal recognition of pregnancy. J. Anim. Sci. 93, 3364–3376.
| Equine endometrial gene expression changes during and after maternal recognition of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Kozai, K., Tokuyama, S., Szóstek, A. Z., Toishi, Y., Tsunoda, N., Taya, K., Sakatani, M., Takahashi, M., Nambo, Y., Skarzynski, D. J., Yamamoto, Y., Kimura, K., and Okuda, K. (2016). Evidence for a PGF2α auto-amplification system in the endometrium in mares. Reproduction 151, 517–526.
| Evidence for a PGF2α auto-amplification system in the endometrium in mares.Crossref | GoogleScholarGoogle Scholar |
Kradolfer, D., Floter, V. L., Bick, J. T., Furst, R. W., Rode, K., Brehm, R., Henning, H., Waberski, D., Bauersachs, S., and Ulbrich, S. E. (2016). Epigenetic effects of prenatal estradiol-17beta exposure on the reproductive system of pigs. Mol. Cell. Endocrinol. 430, 125–137.
| Epigenetic effects of prenatal estradiol-17beta exposure on the reproductive system of pigs.Crossref | GoogleScholarGoogle Scholar |
Laubli, H., Alisson-Silva, F., Stanczak, M. A., Siddiqui, S. S., Deng, L., Verhagen, A., Varki, N., and Varki, A. (2014). Lectin galactoside-binding soluble 3 binding protein (LGALS3BP) is a tumor-associated immunomodulatory ligand for CD33-related Siglecs. J. Biol. Chem. 289, 33481–33491.
| Lectin galactoside-binding soluble 3 binding protein (LGALS3BP) is a tumor-associated immunomodulatory ligand for CD33-related Siglecs.Crossref | GoogleScholarGoogle Scholar |
Lee, W. Y., Wang, C. J., Lin, T. Y., Hsiao, C. L., and Luo, C. W. (2013). CXCL17, an orphan chemokine, acts as a novel angiogenic and anti-inflammatory factor. Am. J. Physiol. Endocrinol. Metab. 304, E32–E40.
| CXCL17, an orphan chemokine, acts as a novel angiogenic and anti-inflammatory factor.Crossref | GoogleScholarGoogle Scholar |
Lin, C. G., Leu, S. J., Chen, N., Tebeau, C. M., Lin, S. X., Yeung, C. Y., and Lau, L. F. (2003). CCN3 (NOV) is a novel angiogenic regulator of the CCN protein family. J. Biol. Chem. 278, 24200–24208.
| CCN3 (NOV) is a novel angiogenic regulator of the CCN protein family.Crossref | GoogleScholarGoogle Scholar |
Liu, H. C., Mele, C., Catz, D., Noyes, N., and Rosenwaks, Z. (1995). Production of insulin-like growth factor binding proteins (IGFBPs) by human endometrial stromal cell is stimulated by the presence of embryos. J. Assist. Reprod. Genet. 12, 78–87.
| Production of insulin-like growth factor binding proteins (IGFBPs) by human endometrial stromal cell is stimulated by the presence of embryos.Crossref | GoogleScholarGoogle Scholar |
Liu, J., Na, S., Glasebrook, A., Fox, N., Solenberg, P. J., Zhang, Q., Song, H. Y., and Yang, D. D. (2001). Enhanced CD4+ T cell proliferation and Th2 cytokine production in DR6-deficient mice. Immunity 15, 23–34.
| Enhanced CD4+ T cell proliferation and Th2 cytokine production in DR6-deficient mice.Crossref | GoogleScholarGoogle Scholar |
Liu, J., Ren, Y., Kang, L., and Zhang, L. (2014). Overexpression of CCN3 inhibits inflammation and progression of atherosclerosis in apolipoprotein E-deficient mice. PLoS One 9, e94912.
| Overexpression of CCN3 inhibits inflammation and progression of atherosclerosis in apolipoprotein E-deficient mice.Crossref | GoogleScholarGoogle Scholar |
Mattijssen, F., and Kersten, S. (2012). Regulation of triglyceride metabolism by angiopoietin-like proteins. Biochim. Biophys. Acta 1821, 782–789.
| Regulation of triglyceride metabolism by angiopoietin-like proteins.Crossref | GoogleScholarGoogle Scholar |
McDowell, K. J., Sharp, D. C., Grubaugh, W., Thatcher, W. W., and Wilcox, C. J. (1988). Restricted conceptus mobility results in failure of pregnancy maintenance in mares. Biol. Reprod. 39, 340–348.
| Restricted conceptus mobility results in failure of pregnancy maintenance in mares.Crossref | GoogleScholarGoogle Scholar |
Merkl, M., Ulbrich, S. E., Otzdorff, C., Herbach, N., Wanke, R., Wolf, E., Handler, J., and Bauersachs, S. (2010). Microarray analysis of equine endometrium at Days 8 and 12 of pregnancy. Biol. Reprod. 83, 874–886.
| Microarray analysis of equine endometrium at Days 8 and 12 of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Moza Jalali, B., Likszo, P., and Skarzynski, D. J. (2016). Proteomic and network analysis of pregnancy-induced changes in the porcine endometrium on Day 12 of gestation. Mol. Reprod. Dev. 83, 827–841.
| Proteomic and network analysis of pregnancy-induced changes in the porcine endometrium on Day 12 of gestation.Crossref | GoogleScholarGoogle Scholar |
Murphy, J. F., Lennon, F., Steele, C., Kelleher, D., Fitzgerald, D., and Long, A. C. (2005). Engagement of CD44 modulates cyclooxygenase induction, VEGF generation, and proliferation in human vascular endothelial cells. FASEB J. 19, 446–448.
| Engagement of CD44 modulates cyclooxygenase induction, VEGF generation, and proliferation in human vascular endothelial cells.Crossref | GoogleScholarGoogle Scholar |
Muthana, M., Hawtree, S., Wilshaw, A., Linehan, E., Roberts, H., Khetan, S., Adeleke, G., Wright, F., Akil, M., Fearon, U., Veale, D., Ciani, B., and Wilson, A. G. (2015). C5orf30 is a negative regulator of tissue damage in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 112, 11618–11623.
| C5orf30 is a negative regulator of tissue damage in rheumatoid arthritis.Crossref | GoogleScholarGoogle Scholar |
Niklaus, A. L., and Pollard, J. W. (2006). Mining the mouse transcriptome of receptive endometrium reveals distinct molecular signatures for the luminal and glandular epithelium. Endocrinology 147, 3375–3390.
| Mining the mouse transcriptome of receptive endometrium reveals distinct molecular signatures for the luminal and glandular epithelium.Crossref | GoogleScholarGoogle Scholar |
Ohashi, K., Fujiwara, S., and Mizuno, K. (2017). Roles of the cytoskeleton, cell adhesion and rho signalling in mechanosensing and mechanotransduction. J. Biochem. 161, 245–254.
Oka, T., Sugaya, M., Takahashi, N., Takahashi, T., Shibata, S., Miyagaki, T., Asano, Y., and Sato, S. (2017). CXCL17 attenuates imiquimod-induced psoriasis-like skin inflammation by recruiting myeloid-derived suppressor cells and regulatory T cells. J. Immunol. 198, 3897–3908.
| CXCL17 attenuates imiquimod-induced psoriasis-like skin inflammation by recruiting myeloid-derived suppressor cells and regulatory T cells.Crossref | GoogleScholarGoogle Scholar |
Østrup, E., Bauersachs, S., Blum, H., Wolf, E., and Hyttel, P. (2010). Differential endometrial gene expression in pregnant and nonpregnant sows. Biol. Reprod. 83, 277–285.
| Differential endometrial gene expression in pregnant and nonpregnant sows.Crossref | GoogleScholarGoogle Scholar |
Palomino, W. A., Argandona, F., Azua, R., Kohen, P., and Devoto, L. (2013). Complement C3 and decay-accelerating factor expression levels are modulated by human chorionic gonadotropin in endometrial compartments during the implantation window. Reprod. Sci. 20, 1103–1110.
| Complement C3 and decay-accelerating factor expression levels are modulated by human chorionic gonadotropin in endometrial compartments during the implantation window.Crossref | GoogleScholarGoogle Scholar |
Piccolo, E., Tinari, N., Semeraro, D., Traini, S., Fichera, I., Cumashi, A., La Sorda, R., Spinella, F., Bagnato, A., Lattanzio, R., D’Egidio, M., Di Risio, A., Stampolidis, P., Piantelli, M., Natoli, C., Ullrich, A., and Iacobelli, S. (2013). LGALS3BP, lectin galactoside-binding soluble 3 binding protein, induces vascular endothelial growth factor in human breast cancer cells and promotes angiogenesis. J. Mol. Med. 91, 83–94.
| LGALS3BP, lectin galactoside-binding soluble 3 binding protein, induces vascular endothelial growth factor in human breast cancer cells and promotes angiogenesis.Crossref | GoogleScholarGoogle Scholar |
Rebordão, M. R., Galvão, A., Pinto-Bravo, P., Pinheiro, J., Gamboa, S., Silva, E., Mateus, L., and Ferreira-Dias, G. (2017). Endometrial prostaglandin synthases, ovarian steroids, and oxytocin receptors in mares with oxytocin-induced luteal maintenance. Theriogenology 87, 193–204.
| Endometrial prostaglandin synthases, ovarian steroids, and oxytocin receptors in mares with oxytocin-induced luteal maintenance.Crossref | GoogleScholarGoogle Scholar |
Rivera del Alamo, M. M., Reilas, T., Kindahl, H., and Katila, T. (2008). Mechanisms behind intrauterine device-induced luteal persistence in mares. Anim. Reprod. Sci. 107, 94–106.
| Mechanisms behind intrauterine device-induced luteal persistence in mares.Crossref | GoogleScholarGoogle Scholar |
Roberts, R. M. (1996). Interferon-tau and pregnancy. J. Interferon Cytokine Res. 16, 271–273.
| Interferon-tau and pregnancy.Crossref | GoogleScholarGoogle Scholar |
Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140.
| edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.Crossref | GoogleScholarGoogle Scholar |
Roker, L. A., Nemri, K., and Yu, J. (2017). Wnt7b signaling from the ureteric bud epithelium regulates medullary capillary development. J. Am. Soc. Nephrol. 28, 250–259.
| Wnt7b signaling from the ureteric bud epithelium regulates medullary capillary development.Crossref | GoogleScholarGoogle Scholar |
Romero, J. J., Liebig, B. E., Broeckling, C. D., Prenni, J. E., and Hansen, T. R. (2017). Pregnancy-induced changes in metabolome and proteome in ovine uterine flushings. Biol. Reprod. 97, 273–287.
| Pregnancy-induced changes in metabolome and proteome in ovine uterine flushings.Crossref | GoogleScholarGoogle Scholar |
Ronchetti, S., Ricci, E., Petrillo, M. G., Cari, L., Migliorati, G., Nocentini, G., and Riccardi, C. (2015). Glucocorticoid-induced tumour necrosis factor receptor-related protein: a key marker of functional regulatory T cells. J. Immunol. Res. 2015, 171520.
| Glucocorticoid-induced tumour necrosis factor receptor-related protein: a key marker of functional regulatory T cells.Crossref | GoogleScholarGoogle Scholar |
Rosario, G. X., Cheng, J. G., and Stewart, C. L. (2016). Gene expression analysis in the compartments of the murine uterus. Differentiation 91, 42–49.
| Gene expression analysis in the compartments of the murine uterus.Crossref | GoogleScholarGoogle Scholar |
Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E., Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., and Quackenbush, J. (2003). TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374–378.
Samborski, A., Graf, A., Krebs, S., Kessler, B., and Bauersachs, S. (2013). Deep sequencing of the porcine endometrial transcriptome on Day 14 of pregnancy. Biol. Reprod. 88, 84.
| Deep sequencing of the porcine endometrial transcriptome on Day 14 of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Satterfield, M. C., Hayashi, K., Song, G., Black, S. G., Bazer, F. W., and Spencer, T. E. (2008). Progesterone regulates FGF10, MET, IGFBP1, and IGFBP3 in the endometrium of the ovine uterus. Biol. Reprod. 79, 1226–1236.
| Progesterone regulates FGF10, MET, IGFBP1, and IGFBP3 in the endometrium of the ovine uterus.Crossref | GoogleScholarGoogle Scholar |
Scott, C. A., van Huyen, D., and Bany, B. M. (2012). Angiopoietin-like gene expression in the mouse uterus during implantation and in response to steroids. Cell Tissue Res. 348, 199–211.
| Angiopoietin-like gene expression in the mouse uterus during implantation and in response to steroids.Crossref | GoogleScholarGoogle Scholar |
Seo, H., Choi, Y., Shim, J., Yoo, I., and Ka, H. (2014a). Comprehensive analysis of prostaglandin metabolic enzyme expression during pregnancy and the characterization of AKR1B1 as a prostaglandin F synthase at the maternal–conceptus interface in pigs. Biol. Reprod. 90, 99.
| Comprehensive analysis of prostaglandin metabolic enzyme expression during pregnancy and the characterization of AKR1B1 as a prostaglandin F synthase at the maternal–conceptus interface in pigs.Crossref | GoogleScholarGoogle Scholar |
Seo, H., Choi, Y., Shim, J., Yoo, I., and Ka, H. (2014b). Prostaglandin transporters ABCC4 and SLCO2A1 in the uterine endometrium and conceptus during pregnancy in pigs. Biol. Reprod. 90, 100.
| Prostaglandin transporters ABCC4 and SLCO2A1 in the uterine endometrium and conceptus during pregnancy in pigs.Crossref | GoogleScholarGoogle Scholar |
Sharp, D. C., Thatcher, M. J., Salute, M. E., and Fuchs, A. R. (1997). Relationship between endometrial oxytocin receptors and oxytocin-induced prostaglandin F2 alpha release during the oestrous cycle and early pregnancy in pony mares. J. Reprod. Fertil. 109, 137–144.
| Relationship between endometrial oxytocin receptors and oxytocin-induced prostaglandin F2 alpha release during the oestrous cycle and early pregnancy in pony mares.Crossref | GoogleScholarGoogle Scholar |
Silva, L. A., Gastal, E. L., Beg, M. A., and Ginther, O. J. (2005). Changes in vascular perfusion of the endometrium in association with changes in location of the embryonic vesicle in mares. Biol. Reprod. 72, 755–761.
| Changes in vascular perfusion of the endometrium in association with changes in location of the embryonic vesicle in mares.Crossref | GoogleScholarGoogle Scholar |
Silva, L. A., Klein, C., Ealy, A. D., and Sharp, D. C. (2011). Conceptus-mediated endometrial vascular changes during early pregnancy in mares: an anatomic, histomorphometric, and vascular endothelial growth factor receptor system immunolocalization and gene expression study. Reproduction 142, 593–603.
| Conceptus-mediated endometrial vascular changes during early pregnancy in mares: an anatomic, histomorphometric, and vascular endothelial growth factor receptor system immunolocalization and gene expression study.Crossref | GoogleScholarGoogle Scholar |
Sluysmans, S., Vasileva, E., Spadaro, D., Shah, J., Rouaud, F., and Citi, S. (2017). The role of apical cell–cell junctions and associated cytoskeleton in mechanotransduction. Biol. Cell 109, 139–161.
| The role of apical cell–cell junctions and associated cytoskeleton in mechanotransduction.Crossref | GoogleScholarGoogle Scholar |
Song, G., Bazer, F. W., Wagner, G. F., and Spencer, T. E. (2006). Stanniocalcin (STC) in the endometrial glands of the ovine uterus: regulation by progesterone and placental hormones. Biol. Reprod. 74, 913–922.
| Stanniocalcin (STC) in the endometrial glands of the ovine uterus: regulation by progesterone and placental hormones.Crossref | GoogleScholarGoogle Scholar |
Song, G., Dunlap, K. A., Kim, J., Bailey, D. W., Spencer, T. E., Burghardt, R. C., Wagner, G. F., Johnson, G. A., and Bazer, F. W. (2009). Stanniocalcin 1 is a luminal epithelial marker for implantation in pigs regulated by progesterone and estradiol. Endocrinology 150, 936–945.
| Stanniocalcin 1 is a luminal epithelial marker for implantation in pigs regulated by progesterone and estradiol.Crossref | GoogleScholarGoogle Scholar |
Spencer, T. E., and Bazer, F. W. (1996). Ovine interferon tau suppresses transcription of the estrogen receptor and oxytocin receptor genes in the ovine endometrium. Endocrinology 137, 1144–1147.
| Ovine interferon tau suppresses transcription of the estrogen receptor and oxytocin receptor genes in the ovine endometrium.Crossref | GoogleScholarGoogle Scholar |
Spencer, T. E., Johnson, G. A., Bazer, F. W., and Burghardt, R. C. (2007). Fetal–maternal interactions during the establishment of pregnancy in ruminants. Soc. Reprod. Fertil. Suppl. 64, 379–396.
Spencer, T. E., Sandra, O., and Wolf, E. (2008). Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches. Reproduction 135, 165–179.
| Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches.Crossref | GoogleScholarGoogle Scholar |
Spencer, T. E., Forde, N., and Lonergan, P. (2016). Insights into conceptus elongation and establishment of pregnancy in ruminants. Reprod. Fertil. Dev. 29, 84–100.
| Insights into conceptus elongation and establishment of pregnancy in ruminants.Crossref | GoogleScholarGoogle Scholar |
Starbuck, G. R., Stout, T. A., Lamming, G. E., Allen, W. R., and Flint, A. P. (1998). Endometrial oxytocin receptor and uterine prostaglandin secretion in mares during the oestrous cycle and early pregnancy. J. Reprod. Fertil. 113, 173–179.
| Endometrial oxytocin receptor and uterine prostaglandin secretion in mares during the oestrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar |
Stasko, S. E., DiMattia, G. E., and Wagner, G. F. (2001). Dynamic changes in stanniocalcin gene expression in the mouse uterus during early implantation. Mol. Cell. Endocrinol. 174, 145–149.
| Dynamic changes in stanniocalcin gene expression in the mouse uterus during early implantation.Crossref | GoogleScholarGoogle Scholar |
Stout, T. A., and Allen, W. R. (2001). Role of prostaglandins in intrauterine migration of the equine conceptus. Reproduction 121, 771–775.
| Role of prostaglandins in intrauterine migration of the equine conceptus.Crossref | GoogleScholarGoogle Scholar |
Stout, T. A., and Allen, W. R. (2002). Prostaglandin E(2) and F(2 alpha) production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares. Reproduction 123, 261–268.
| Prostaglandin E(2) and F(2 alpha) production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares.Crossref | GoogleScholarGoogle Scholar |
Stout, T. A., Lamming, G. E., and Allen, W. R. (2000). The uterus as a source of oxytocin in cyclic mares. J. Reprod. Fertil. Suppl. 56, 281–287.
Stout, T. A., Meadows, S., and Allen, W. R. (2005). Stage-specific formation of the equine blastocyst capsule is instrumental to hatching and to embryonic survival in vivo. Anim. Reprod. Sci. 87, 269–281.
| Stage-specific formation of the equine blastocyst capsule is instrumental to hatching and to embryonic survival in vivo.Crossref | GoogleScholarGoogle Scholar |
Tsai, S. J., Wu, M. H., Chen, H. M., Chuang, P. C., and Wing, L. Y. (2002). Fibroblast growth factor-9 is an endometrial stromal growth factor. Endocrinology 143, 2715–2721.
| Fibroblast growth factor-9 is an endometrial stromal growth factor.Crossref | GoogleScholarGoogle Scholar |
Wang, B., Ye, T. M., Lee, K. F., Chiu, P. C., Pang, R. T., Ng, E. H., and Yeung, W. S. (2015). Annexin A2 acts as an adhesion molecule on the endometrial epithelium during implantation in mice. PLoS One 10, e0139506.
| Annexin A2 acts as an adhesion molecule on the endometrial epithelium during implantation in mice.Crossref | GoogleScholarGoogle Scholar |
Wetendorf, M., and DeMayo, F. J. (2012). The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network. Mol. Cell. Endocrinol. 357, 108–118.
| The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network.Crossref | GoogleScholarGoogle Scholar |
Wilsher, S., and Allen, W. R. (2011). Intrauterine administration of plant oils inhibits luteolysis in the mare. Equine Vet. J. 43, 99–105.
| Intrauterine administration of plant oils inhibits luteolysis in the mare.Crossref | GoogleScholarGoogle Scholar |
Wilsher, S., Gower, S., and Allen, W. R. (2013). Persistence of an immunoreactive MUC1 protein at the feto–maternal interface throughout pregnancy in the mare. Reprod. Fertil. Dev. 25, 753–761.
| Persistence of an immunoreactive MUC1 protein at the feto–maternal interface throughout pregnancy in the mare.Crossref | GoogleScholarGoogle Scholar |
