Novel equine conceptus–endometrial interactions on Day 16 of pregnancy based on RNA sequencing
C. KleinFaculty of Veterinary Medicine, University of Calgary, 3280 Hospital Dr NW, Calgary, AB T2N 4Z6, Canada. Email: claudia.klein@ucalgary.ca
Reproduction, Fertility and Development 28(11) 1712-1720 https://doi.org/10.1071/RD14489
Submitted: 10 December 2014 Accepted: 1 April 2015 Published: 5 May 2015
Abstract
Maintenance of pregnancy is dependent on the exchange of signals between the conceptus and the endometrium. The objective of this study was to use next-generation sequencing to determine transcriptome blueprints of the conceptus and endometrium 16 days after ovulation in the horse. There were 7760 and 10 182 genes expressed in the conceptus and endometrium, respectively, of which 7029 were present in both. Genes related to developmental processes were enriched among conceptus-specific transcripts, whereas many endometrium-specific genes had known roles in cell communication, cell adhesion and response to stimuli. The integrin signalling pathway was overrepresented in both transcriptomes. In that regard, it was hypothesised that integrins ITGA5B1 and ITGAVB3 interact with conceptus-derived fibrinogen, potentially contributing to cessation of conceptus mobility. That several growth factors and their corresponding receptors (e.g. HDGF, NOV, CYR61, CTGF, HBEGF) were expressed by conceptus and endometrium were attributed to cross-talk. In addition, Cytoscape interaction analysis revealed a plethora of interactions between genes expressed by the conceptus and endometrium, during a period when the former had substantial movement within the uterus. This is the first report of concurrent transcriptome analysis of conceptus and endometrium in the mare, with numerous findings to provide rationale for further investigation.
Additional keywords: endometrium, mare, maternal recognition of pregnancy, signalling.
References
Anokye-Danso, F., Trivedi, C. M., Juhr, D., Gupta, M., Cui, Z., Tian, Y., Zhang, Y., Yang, W., Gruber, P. J., Epstein, J. A., and Morrisey, E. E. (2011). Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8, 376–388.| Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFGns74%3D&md5=86d7f2760a48be198aea64e01552d115CAS | 21474102PubMed |
Bazer, F. W., and Thatcher, W. W. (1977). Theory of maternal recognition of pregnancy in swine based on oestrogen-controlled endocrine versus exocrine secretion of prostaglandin F2alpha by the uterine endometrium. Prostaglandins 14, 397–401.
| Theory of maternal recognition of pregnancy in swine based on oestrogen-controlled endocrine versus exocrine secretion of prostaglandin F2alpha by the uterine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXls1WrtL8%3D&md5=0d42ba01c6987d58a91f80d3d7692eb9CAS | 897228PubMed |
Bazer, F. W., Spencer, T. E., and Ott, T. L. (1997). Interferon tau: a novel pregnancy recognition signal. Am. J. Reprod. Immunol. 37, 412–420.
| Interferon tau: a novel pregnancy recognition signal.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2sznt1Sgsw%3D%3D&md5=a2fa40ef0c88f073c6fac2376e377e54CAS | 9228295PubMed |
Brakebusch, C., and Fassler, R. (2003). The integrin–actin connection, an eternal love affair. EMBO J. 22, 2324–2333.
| The integrin–actin connection, an eternal love affair.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvV2gsbY%3D&md5=9d6b1b66fc4991a28645731b87377770CAS | 12743027PubMed |
Chen, C. C., and Lau, L. F. (2009). Functions and mechanisms of action of CCN matricellular proteins. Int. J. Biochem. Cell Biol. 41, 771–783.
| Functions and mechanisms of action of CCN matricellular proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitFSmtL0%3D&md5=562ad4d9e3a461e15b519dcc9ccb4e24CAS | 18775791PubMed |
Chiappe, M. E., Lattanzi, M. L., Colman-Lerner, A. A., Baranao, J. L., and Saragueta, P. (2002). Expression of 3 beta-hydroxysteroid dehydrogenase in early bovine embryo development. Mol. Reprod. Dev. 61, 135–141.
| Expression of 3 beta-hydroxysteroid dehydrogenase in early bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Gjtw%3D%3D&md5=18fed1ad373188a5d098d14a9386acdeCAS | 11803547PubMed |
Doty, A., Buhi, W. C., Benson, S., Scoggin, K. E., Pozor, M., Macpherson, M., Mutz, M., and Troedsson, M. H. (2011). Equine CRISP3 modulates interaction between spermatozoa and polymorphonuclear neutrophils. Biol. Reprod. 85, 157–164.
| Equine CRISP3 modulates interaction between spermatozoa and polymorphonuclear neutrophils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFOlsL8%3D&md5=e97e204d242952916d752ee56769a9b9CAS | 21389342PubMed |
Gallitzendoerfer, R., Abouzied, M. M., Hartmann, D., Dobrowolski, R., Gieselmann, V., and Franken, S. (2008). Hepatoma-derived growth factor (HDGF) is dispensable for normal mouse development. Dev. Dyn. 237, 1875–1885.
| Hepatoma-derived growth factor (HDGF) is dispensable for normal mouse development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVOgs7w%3D&md5=b33cac7c6b512190ba070dbee900ed79CAS | 18570251PubMed |
Geisert, R. D., Zavy, M. T., Moffatt, R. J., Blair, R. M., and Yellin, T. (1990). Embryonic steroids and the establishment of pregnancy in pigs. J. Reprod. Fertil. Suppl. 40, 293–305.
| 1:CAS:528:DyaK3MXlt1Oju7s%3D&md5=1bf9e6d604d9317634e1c3695ad3468dCAS | 2192045PubMed |
Goldsmith, L. T., Weiss, G., Palejwala, S., Plant, T. M., Wojtczuk, A., Lambert, W. C., Ammur, N., Heller, D., Skurnick, J. H., Edwards, D., and Cole, D. M. (2004). Relaxin regulation of endometrial structure and function in the rhesus monkey. Proc. Natl. Acad. Sci. USA 101, 4685–4689.
| Relaxin regulation of endometrial structure and function in the rhesus monkey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtFKisbo%3D&md5=b98eae5d9d00dfeabd657dedf56b7b41CAS | 15070778PubMed |
Gómez, E., Correia, E., Caamaño, J. N., Díez, C., Carrocera, S., Peynot, N., Martín Gonzalez, D., Giraud-Delville, C., Duranthon, V., Sandra, O., and Muñoz, M. (2014). Hepatoma-derived growth factor: from the bovine uterus to the in vitro embryo culture. Reproduction 148, 353–365.
| Hepatoma-derived growth factor: from the bovine uterus to the in vitro embryo culture.Crossref | GoogleScholarGoogle Scholar | 25009202PubMed |
Herrler, A., Stewart, F., Crossett, B., Pell, J. M., Ellis, P. D., Beier, H. M., and Allen, W. R. (2000). Identification of proteins in the equine embryonic capsule. J. Reprod. Fertil. Suppl. 56, 601–606.
| 20681175PubMed |
Jin, W., and Dong, C. (2013). IL-17 cytokines in immunity and inflammation. Emerg. Microbes Infect. 2, e60.
| IL-17 cytokines in immunity and inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVyqu7nO&md5=1c75a07a5e86271005cbb7f918fb4641CAS |
Jung, C. J., Iyengar, S., Blahnik, K. R., Ajuha, T. P., Jiang, J. X., Farnham, P. J., and Zern, M. (2011). Epigenetic modulation of miR-122 facilitates human embryonic stem cell self-renewal and hepatocellular carcinoma proliferation. PLoS One 6, e27740.
| Epigenetic modulation of miR-122 facilitates human embryonic stem cell self-renewal and hepatocellular carcinoma proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1eqtLfI&md5=53f4721e67c9c9520e67514595ab7752CAS | 22140464PubMed |
Kaczmarek, M. M., Blitek, A., Kaminska, K., Bodek, G., Zygmunt, M., Schams, D., and Ziecik, A. J. (2008). Assessment of VEGF-receptor system expression in the porcine endometrial stromal cells in response to insulin-like growth factor-I, relaxin, oxytocin and prostaglandin E2. Mol. Cell. Endocrinol. 291, 33–41.
| Assessment of VEGF-receptor system expression in the porcine endometrial stromal cells in response to insulin-like growth factor-I, relaxin, oxytocin and prostaglandin E2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsValsbs%3D&md5=c125baaf590ab6e93445cd32c5806bb6CAS | 18562087PubMed |
Kent, L. N., Konno, T., and Soares, M. J. (2010). Phosphatidylinositol 3 kinase modulation of trophoblast cell differentiation. BMC Dev. Biol. 10, 97.
| Phosphatidylinositol 3 kinase modulation of trophoblast cell differentiation.Crossref | GoogleScholarGoogle Scholar | 20840781PubMed |
Klein, C., and Troedsson, M. H. (2011). Transcriptional profiling of equine conceptuses reveals new aspects of embryo–maternal communication in the horse. Biol. Reprod. 84, 872–885.
| Transcriptional profiling of equine conceptuses reveals new aspects of embryo–maternal communication in the horse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGju7Y%3D&md5=ba1141a76fb40f320ddae9cf60ed5641CAS | 21209420PubMed |
Klein, C., and Troedsson, M. (2012). Equine pre-implantation conceptuses express neuraminidase 2 – a potential mechanism for desialylation of the equine capsule. Reprod. Domest. Anim. 47, 449–454.
| Equine pre-implantation conceptuses express neuraminidase 2 – a potential mechanism for desialylation of the equine capsule.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsVKmtLk%3D&md5=ef066ca3733f9762c3f570c9f2f45924CAS | 22022932PubMed |
Klein, C., and Troedsson, M. H. (2013). Macrophage migration inhibitory factor is expressed by equine conceptuses and endometrium. Reprod. Domest. Anim. 48, 297–304.
| Macrophage migration inhibitory factor is expressed by equine conceptuses and endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlWqu7w%3D&md5=fa0a32c404956505ded67bed548574aeCAS | 22805597PubMed |
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 | 1:CAS:528:DC%2BC3cXotlWqtLc%3D&md5=d6d7284abf9226ea3a0234e3a2ab8a65CAS | 20335638PubMed |
Klonisch, T., Mathias, S., Cambridge, G., Hombach-Klonisch, S., Ryan, P. L., and Allen, W. R. (1997). Placental localisation of relaxin in the pregnant mare. Placenta 18, 121–128.
| Placental localisation of relaxin in the pregnant mare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXislansro%3D&md5=8044d5058b75239cdd7edd875d359126CAS | 9089772PubMed |
Leith, G. S., and Ginther, O. J. (1984). Characterisation of intrauterine mobility of the early equine conceptus. Theriogenology 22, 401–408.
| Characterisation of intrauterine mobility of the early equine conceptus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVOnsA%3D%3D&md5=f881b47469a31d0d296c6cedcaa751c2CAS | 16725972PubMed |
Lessey, B. A. (1998). Endometrial integrins and the establishment of uterine receptivity. Hum. Reprod. 13, 247–258.
| Endometrial integrins and the establishment of uterine receptivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtVCnu7o%3D&md5=f931e6066971ddf82ade84be0477ee6aCAS | 9755427PubMed |
Lim, H. J., and Dey, S. K. (2009). HB-EGF: a unique mediator of embryo–uterine interactions during implantation. Exp. Cell Res. 315, 619–626.
| HB-EGF: a unique mediator of embryo–uterine interactions during implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXis1alur0%3D&md5=d585e3d95c300e7b1d480809e813e654CAS | 18708050PubMed |
Mamo, S., Mehta, J. P., Forde, N., McGettigan, P., and Lonergan, P. (2012). Conceptus–endometrium crosstalk during maternal recognition of pregnancy in cattle. Biol. Reprod. 87, 6.
| Conceptus–endometrium crosstalk during maternal recognition of pregnancy in cattle.Crossref | GoogleScholarGoogle Scholar | 22517619PubMed |
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 | 1:CAS:528:DyaL1cXls1ektr8%3D&md5=1269691d85847b2f88f7b98a57eee5f4CAS | 3179385PubMed |
Merk, M., Zierow, S., Leng, L., Das, R., Du, X., Schulte, W., Fan, J., Lue, H., Chen, Y., Xiong, H., Chagnon, F., Bernhagen, J., Lolis, E., Mor, G., Lesur, O., and Bucala, R. (2011). The D-dopachrome tautomerase (DDT) gene product is a cytokine and functional homologue of macrophage migration inhibitory factor (MIF). Proc. Natl. Acad. Sci. USA 108, E577–E585.
| The D-dopachrome tautomerase (DDT) gene product is a cytokine and functional homologue of macrophage migration inhibitory factor (MIF).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFamsLjP&md5=b3e478e776fb14c5a37143fb8a894585CAS | 21817065PubMed |
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 | 1:CAS:528:DC%2BC3cXhtlGls7%2FF&md5=526ceb5ff21beb93456f8d2e8c0ffba6CAS | 20631402PubMed |
Moussad, E. E., Rageh, M. A., Wilson, A. K., Geisert, R. D., and Brigstock, D. R. (2002). Temporal and spatial expression of connective tissue growth factor (CCN2; CTGF) and transforming growth factor beta type 1 (TGF-beta1) at the utero–placental interface during early pregnancy in the pig. Mol. Pathol. 55, 186–192.
| Temporal and spatial expression of connective tissue growth factor (CCN2; CTGF) and transforming growth factor beta type 1 (TGF-beta1) at the utero–placental interface during early pregnancy in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1yrt74%3D&md5=554758b2c5afd93dce5b47f24d88405eCAS | 12032230PubMed |
Oriol, J. G., Betteridge, K. J., Clarke, A. J., and Sharom, F. J. (1993a). Mucin-like glycoproteins in the equine embryonic capsule. Mol. Reprod. Dev. 34, 255–265.
| Mucin-like glycoproteins in the equine embryonic capsule.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktVGlsr8%3D&md5=ba0afdf62726f5cabf58cfa836c08483CAS | 8471247PubMed |
Oriol, J. G., Sharom, F. J., and Betteridge, K. J. (1993b). Developmentally regulated changes in the glycoproteins of the equine embryonic capsule. J. Reprod. Fertil. 99, 653–664.
| Developmentally regulated changes in the glycoproteins of the equine embryonic capsule.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFentbc%3D&md5=979538a68bf391c21eaacedfe359829cCAS | 8107051PubMed |
Orr, A. W., Ginsberg, M. H., Shattil, S. J., Deckmyn, H., and Schwartz, M. A. (2006). Matrix-specific suppression of integrin activation in shear stress signalling. Mol. Biol. Cell 17, 4686–4697.
| Matrix-specific suppression of integrin activation in shear stress signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFygtr%2FO&md5=354dbd6b75a7bb482ceaa734f15896f4CAS | 16928957PubMed |
Passey, R. J., Williams, E., Lichanska, A. M., Wells, C., Hu, S., Geczy, C. L., Little, M. H., and Hume, D. A. (1999a). A null mutation in the inflammation-associated S100 protein S100A8 causes early resorption of the mouse embryo. J. Immunol. 163, 2209–2216.
| 1:CAS:528:DyaK1MXltFagsbg%3D&md5=3576717031573df4f740aca9dd1456fbCAS | 10438963PubMed |
Passey, R. J., Xu, K., Hume, D. A., and Geczy, C. L. (1999b). S100A8: emerging functions and regulation. J. Leukoc. Biol. 66, 549–556.
| 1:CAS:528:DyaK1MXmvVaisbY%3D&md5=28352e50fa3eec5784941ce8a441a854CAS | 10534107PubMed |
Pongcharoen, S., and Supalap, K. (2009). Interleukin-17 increased progesterone secretion by JEG-3 human choriocarcinoma cells. Am. J. Reprod. Immunol. 61, 261–264.
| Interleukin-17 increased progesterone secretion by JEG-3 human choriocarcinoma cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvVGqsrk%3D&md5=73bca1898548470a430c2746e5382ffaCAS | 19260856PubMed |
Pongcharoen, S., Niumsup, P., Sanguansermsri, D., Supalap, K., and Butkhamchot, P. (2006). The effect of interleukin-17 on the proliferation and invasion of JEG-3 human choriocarcinoma cells. Am. J. Reprod. Immunol. 55, 291–300.
| The effect of interleukin-17 on the proliferation and invasion of JEG-3 human choriocarcinoma cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFCksr4%3D&md5=f294e8a311da8602fe1574d5006777f5CAS | 16533341PubMed |
Ramsköld, D., Wang, E. T., Burge, C. B., and Sandberg, R. (2009). An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLOS Comput. Biol. 5, e1000598.
| An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data.Crossref | GoogleScholarGoogle Scholar | 20011106PubMed |
Rhéaume, E., Lachance, Y., Zhao, H. F., Breton, N., Dumont, M., de Launoit, Y., Trudel, C., Luu-The, V., Simard, J., and Labrie, F. (1991). Structure and expression of a new complementary DNA encoding the almost exclusive 3β-hydroxysteroid dehydrogenase/Δ5-Δ4-isomerase in human adrenals and gonads. Mol. Endocrinol. 5, 1147–1157.
| Structure and expression of a new complementary DNA encoding the almost exclusive 3β-hydroxysteroid dehydrogenase/Δ5-Δ4-isomerase in human adrenals and gonads.Crossref | GoogleScholarGoogle Scholar | 1944309PubMed |
Robinson, E. E., Foty, R. A., and Corbett, S. A. (2004). Fibronectin matrix assembly regulates alpha5beta1-mediated cell cohesion. Mol. Biol. Cell 15, 973–981.
| Fibronectin matrix assembly regulates alpha5beta1-mediated cell cohesion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitlGhuro%3D&md5=6de84984cde534c7eba28cc8351149daCAS | 14718567PubMed |
Schmitz, C., Yu, L., Bocca, S., Anderson, S., Cunha-Filho, J. S., Rhavi, B. S., and Oehninger, S. (2014). Role for the endometrial epithelial protein MFG-E8 and its receptor integrin alphavbeta3 in human implantation: results of an in vitro trophoblast attachment study using established human cell lines. Fertil. Steril. 101, 874–882.
| Role for the endometrial epithelial protein MFG-E8 and its receptor integrin alphavbeta3 in human implantation: results of an in vitro trophoblast attachment study using established human cell lines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlSqsro%3D&md5=89eed884383c66087f405c6a9fa4fcbcCAS | 24424369PubMed |
Short, R. V. 1969 Implantation and the maternal recognition of pregnancy. In ‘Ciba Foundation Symposium on Foetal Autonomy’. (Eds G. E. W. Wolstenholme and M. O’Connor.) pp. 2–26. (Churchill: London.)
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 immunolocalisation 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 immunolocalisation and gene expression study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlyitbzM&md5=d22f933de8432bcee4d984b054fb8a39CAS | 21757474PubMed |
Simpson, K. S., Adams, M. H., Behrendt-Adam, C. Y., Baker, C. B., and McDowell, K. J. (1999). Identification and initial characterisation of calcyclin and phospholipase A2 in equine conceptuses. Mol. Reprod. Dev. 53, 179–187.
| Identification and initial characterisation of calcyclin and phospholipase A2 in equine conceptuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivFKmtL4%3D&md5=5906e33b33d140caed907ee0c747945bCAS | 10331456PubMed |
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 | 1:CAS:528:DC%2BD3MXktVait7w%3D&md5=94e8e009c5ffc3cc6e9d011eb053a1e0CAS | 11427165PubMed |
Suehiro, K., Mizuguchi, J., Nishiyama, K., Iwanaga, S., Farrell, D. H., and Ohtaki, S. (2000). Fibrinogen binds to integrin alpha(5)beta(1) via the carboxyl-terminal RGD site of the Aalpha-chain. J. Biochem. 128, 705–710.
| Fibrinogen binds to integrin alpha(5)beta(1) via the carboxyl-terminal RGD site of the Aalpha-chain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosFOjs7c%3D&md5=c34dffcc00ed1ba9afd8769999b46f1aCAS | 11011154PubMed |
Unemori, E. N., Erikson, M. E., Rocco, S. E., Sutherland, K. M., Parsell, D. A., Mak, J., and Grove, B. H. (1999). Relaxin stimulates expression of vascular endothelial growth factor in normal human endometrial cells in vitro and is associated with menometrorrhagia in women. Hum. Reprod. 14, 800–806.
| Relaxin stimulates expression of vascular endothelial growth factor in normal human endometrial cells in vitro and is associated with menometrorrhagia in women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisV2qtrw%3D&md5=9e05b262df82a8ce10b242df791887e4CAS | 10221717PubMed |
Vanderwall, D. K., Woods, G. L., Weber, J. A., and Lichtenwalner, A. B. (1994). Corpus luteal function in non-pregnant mares following intrauterine administration of prostaglandin E(2) or oestradiol-17beta. Theriogenology 42, 1069–1083.
| Corpus luteal function in non-pregnant mares following intrauterine administration of prostaglandin E(2) or oestradiol-17beta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXis1Giu7o%3D&md5=79d8d35e371d3fed9479a2fde5c0bc6dCAS | 16727611PubMed |
Waterhouse, P., Parhar, R. S., Guo, X., Lala, P. K., and Denhardt, D. T. (1992). Regulated temporal and spatial expression of the calcium-binding proteins calcyclin and OPN (osteopontin) in mouse tissues during pregnancy. Mol. Reprod. Dev. 32, 315–323.
| Regulated temporal and spatial expression of the calcium-binding proteins calcyclin and OPN (osteopontin) in mouse tissues during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlvVyqtLc%3D&md5=c214372201dcf2a9105e06c663e68906CAS | 1497879PubMed |
Watson, E. D., and Sertich, P. L. (1989). Prostaglandin production by horse embryos and the effect of co-culture of embryos with endometrium from pregnant mares. J. Reprod. Fertil. 87, 331–336.
| Prostaglandin production by horse embryos and the effect of co-culture of embryos with endometrium from pregnant mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlvVyiu7Y%3D&md5=244d1e1a63c7df513326548fbe186c73CAS | 2621704PubMed |
Webel, S. K., Franklin, V., Harland, B., and Dziuk, P. J. (1977). Fertility, ovulation and maturation of eggs in mares injected with HCG. J. Reprod. Fertil. 51, 337–341.
| Fertility, ovulation and maturation of eggs in mares injected with HCG.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXpvFGksQ%3D%3D&md5=bcd6e84b5b6b6fbed25381e38d870116CAS | 563450PubMed |
Woodley, S. L., Burns, P. J., Douglas, R. H., and Oxender, W. D. (1979). Prolonged interovulatory interval after oestradiol treatment in mares. J. Reprod. Fertil. Suppl. 27, 205–209.
| 289791PubMed |
Zavy, M. T., Vernon, M. W., Sharp, D. C., and Bazer, F. W. (1984). Endocrine aspects of early pregnancy in pony mares: a comparison of uterine luminal and peripheral plasma levels of steroids during the oestrous cycle and early pregnancy. Endocrinology 115, 214–219.
| Endocrine aspects of early pregnancy in pony mares: a comparison of uterine luminal and peripheral plasma levels of steroids during the oestrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXks1KhtbY%3D&md5=7b8cf94a75439f8f7c5af6ab6188cd0fCAS | 6734514PubMed |