Expression of steroidogenic proteins in bovine placenta during the first half of gestation
Adriana Verduzco A , Gilles Fecteau B , Réjean Lefebvre A B , Lawrence C. Smith A and Bruce D. Murphy A C
+ Author Affiliations
- Author Affiliations
A Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, 3200 Sicotte, Saint Hyacinthe, Québec, J2S 7C6, Canada.
B Département de Sciences Cliniques, Faculté de Médecine Vétérinaire, Université de Montréal, 3200 Sicotte, Saint Hyacinthe, Québec, J2S 7C6, Canada.
C Corresponding author. Email: bruce.d.murphy@umontreal.ca
Reproduction, Fertility and Development 24(2) 392-404 https://doi.org/10.1071/RD10303
Abstract
The aim of the present study was to determine the occurrence and localisation of the principal steroidogenic proteins in bovine placenta from Day 50 to Day 120 of pregnancy. Immunohistochemistry revealed that, at all stages investigated, bovine steroidogenic acute regulatory protein (StAR), cytochrome P45011A1 and hydroxy-δ-5-steroid dehydrogenase, 3β- and steroid δ-isomerase 1 proteins were found principally at the fetomaternal interdigitations: the chorionic villus and maternal septum. Moreover, caruncular epithelial cells and uninucleate trophoblast cells were the principal cells detected that were positive for the three markers. Western blot analysis showed that only caruncular tissue expressed all three steroidogenic markers; in contrast, cotyledons only expressed StAR and cytochrome P45011A1. Immunoblot results showed a complementary pattern of StAR and cytochrome P45011A1 expression between caruncles and cotyledons at different stages. These observations suggest that, in early pregnancy, the maternal compartment contributes significantly to bovine placental steroidogenesis, particularly for the synthesis of progesterone. Furthermore, the variation in StAR and cytochrome P45011A1 expression between caruncular and cotyledonary tissues across gestation suggests that placental steroidogenesis requires cell-to-cell communication between maternal and fetal cells.
Additional keywords: placental steroids, steroidogenesis.
References
Arensburg, J., Payne, A., and Orly, J. (1999). Expression of steroidogenic genes in maternal and extraembryonic cells during early pregnancy in mice. Endocrinology 140, 5220–5232.| Expression of steroidogenic genes in maternal and extraembryonic cells during early pregnancy in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFemtL4%3D&md5=84bb57fc0e966ee9819611668a68e870CAS | 10537152PubMed |
Beckers, J. F., Zarrouk, A., Batalha, E. S., Garbayo, J. M., Mester, L., and Szenci, O. (1998). Endocrinology of pregnancy: chorionic somatomammotropins and pregnancy-associated glycoproteins Acta Vet. Hung. 46, 175–189.
| 1:CAS:528:DyaK1cXlt1aqur4%3D&md5=953933465d806ad9c94377a0368a4accCAS | 9704521PubMed |
Ben-David, E., and Shemesh, M. (1990). Ultrastructural localization of cytochrome P-450scc in the bovine placentome using protein A-goldtechnique. Biol. Reprod. 42, 131–138.
| Ultrastructural localization of cytochrome P-450scc in the bovine placentome using protein A-goldtechnique.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c7otFGlug%3D%3D&md5=3939540476db7753a4d70140e3b7c740CAS | 2310813PubMed |
Ben-Zimra, M., Koler, M., Melamed-Book, N., Arensburg, J., Payne, A., and Orly, J. (2002). Uterine and placental expression of steroidogenic genes during rodent pregnancy. Mol. Cell. Endocrinol. 187, 223–231.
| Uterine and placental expression of steroidogenic genes during rodent pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Sqt70%3D&md5=a5978f9ea6f73a70f802510355649e27CAS | 11988331PubMed |
Campbell, J. W., Hallford, D. M., and Wise, M. E. (1994). Serum progesterone and luteinizing hormone in ewes treated with PGF2α during mid-gestation and gonadotropin releasing hormone after parturition. Prostaglandins 47, 333–344.
| Serum progesterone and luteinizing hormone in ewes treated with PGF2α during mid-gestation and gonadotropin releasing hormone after parturition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVWhsbs%3D&md5=c9d793424e13f0bb93af48f462be2e2bCAS | 8066182PubMed |
Challis, J. R., and Patrick, J. E. (1981). Fetal and maternal estrogen concentrations throughout pregnancy in the sheep. Can. J. Physiol. Pharmacol. 59, 970–978.
| Fetal and maternal estrogen concentrations throughout pregnancy in the sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlsVOqsb8%3D&md5=169841f8cb11e344a171bb22e38a4525CAS | 7296398PubMed |
Chew, B. P., Erb, R. E., Fessler, J. F., Callahan, C. J., and Malven, P. V. (1979). Effects of ovariectomy during pregnancy and of prematurely induced parturition on progesterone, estrogens, and calving traits. J. Dairy Sci. 62, 557–566.
| Effects of ovariectomy during pregnancy and of prematurely induced parturition on progesterone, estrogens, and calving traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXktFOqtrk%3D&md5=30888709a766f9fa6208b590936130ebCAS | 457986PubMed |
Choi, I., Kim, J. Y., Lee, E. J., Kim, Y. Y., Chung, C. S., Chang, J., Choi, N. J., Chung, H. J., and Lee, K. H. (2009). Ontogeny of expression and localization of steroidogenic enzymes in the neonatal and prepubertal pig testes. J. Androl. 30, 57–74.
| Ontogeny of expression and localization of steroidogenic enzymes in the neonatal and prepubertal pig testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFSqtbY%3D&md5=bf43e387171f57e62c2833f3840c7c04CAS | 18772489PubMed |
Conley, A. J., and Ford, S. P. (1987). Effect of prostaglandin F2α-induced luteolysis on in vivo and in vitro progesterone production by individual placentomes of cows. J. Anim. Sci. 65, 500–507.
| 1:CAS:528:DyaL2sXkvFShur8%3D&md5=8f684ed9631751b8b9d23ce97d0ec4b6CAS | 3476483PubMed |
Conley, A. J., Head, J. R., Stirling, D. T., and Mason, J. I. (1992). Expression of steroidogenic enzymes in the bovine placenta and fetal adrenal glands throughout gestation. Endocrinology 130, 2641–2650.
| Expression of steroidogenic enzymes in the bovine placenta and fetal adrenal glands throughout gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktVWhsr0%3D&md5=38ef23d826322f742733232da2ea76faCAS | 1374010PubMed |
Day, A. M. (1977). Cloprostenol for termination of pregnancy in cattle. B) The induction of abortion. N. Z. Vet. J. 25, 139–144.
| Cloprostenol for termination of pregnancy in cattle. B) The induction of abortion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c3gtVGiug%3D%3D&md5=268a0e8e1d4377617f5aa45b7f8c2b9aCAS | 275710PubMed |
Douglas, D. A., Song, J. H., Houde, A., Cooke, G. M., and Murphy, B. D. (1997). Luteal and placental characteristics of carnivore gestation: expression of genes for luteotrophic receptors and steroidogenic enzymes. J. Reprod. Fertil. Suppl. 51, 153–166.
| 1:CAS:528:DyaK2sXmvFClu7o%3D&md5=fc0a74ec7611090699387cad086c769dCAS | 9404281PubMed |
Duello, T. M., Byatt, J. C., and Bremel, R. D. (1986). Immunohistochemical localization of placental lactogen in binucleate cells of bovine placentomes. Endocrinology 119, 1351–1355.
| Immunohistochemical localization of placental lactogen in binucleate cells of bovine placentomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XlsVKnurc%3D&md5=4197ae67121795084a59f7cac8da221dCAS | 3525130PubMed |
Evans, G., and Wagner, W. C. (1981). In vitro oestrogen synthesis by bovine placenta during pregnancy and induced parturition. Acta Endocrinol. 98, 119–125.
| 1:CAS:528:DyaL3MXltlSntb4%3D&md5=2b1e5926fe4f7246cf9f9f8818dc2294CAS | 7282265PubMed |
Evans, H., and Sack, W. (1973). Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references. Anat. Histol. Embryol. 2, 11–45.
| Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c%2FhtVGquw%3D%3D&md5=fb84839a35655130aea65a2651cca4eaCAS |
Gabai, G., Marinelli, L., Simontacchi, C., and Bono, G. G. (2004). The increase in plasma C19Delta5 steroids in subcutaneous abdominal and jugular veins of dairy cattle during pregnancy is unrelated to estrogenic activity. Steroids 69, 121–127.
| The increase in plasma C19Delta5 steroids in subcutaneous abdominal and jugular veins of dairy cattle during pregnancy is unrelated to estrogenic activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFamu7k%3D&md5=d07383e664143b92b4790d5a01552986CAS | 15013690PubMed |
Gross, T. S., and Williams, W. F. (1988). In-vitro steroid synthesis by the placenta of cows in late gestation and at parturition. J. Reprod. Fertil. 83, 565–573.
| In-vitro steroid synthesis by the placenta of cows in late gestation and at parturition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkvVKmsbk%3D&md5=7862fb9cb65e56fd4110d84fdc3ec321CAS | 3411551PubMed |
Hashizume, K., Ushizawa, K., Patel, O. V., Kizaki, K., Imai, K., Yamada, O., Nakano, H., and Takahashi, T. (2007). Gene expression and maintenance of pregnancy in bovine: roles of trophoblastic binucleate cell-specific molecules. Reprod. Fertil. Dev. 19, 79–90.
| Gene expression and maintenance of pregnancy in bovine: roles of trophoblastic binucleate cell-specific molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhtleitr%2FP&md5=4ed3dc48c9b2bd7ce9d89df0afd74f26CAS | 17389137PubMed |
Hoffmann, B., and Schuler, G. (2002). The bovine placenta; a source and target of steroid hormones: observations during the second half of gestation. Domest. Anim. Endocrinol. 23, 309–320.
| The bovine placenta; a source and target of steroid hormones: observations during the second half of gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1Wktbc%3D&md5=3da73681c047f43a2b197f3c7f457c96CAS | 12142247PubMed |
Hoffmann, B., Falter, K., Vielemeier, A., Failing, K., and Schuler, G. (2001). Investigations on the activity of bovine placental oestrogen sulfotransferase and -sulfatase from midgestation to parturition. Exp. Clin. Endocrinol. Diabetes 109, 294–301.
| Investigations on the activity of bovine placental oestrogen sulfotransferase and -sulfatase from midgestation to parturition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlslOisbs%3D&md5=51fa18d6ebd28e45ff5e32156d8b1534CAS | 11507654PubMed |
Izhar, M., Pasmanik, M., and Shemesh, M. (1992). Bovine placental progesterone synthesis: comparison of first and second trimesters of gestation. Biol. Reprod. 46, 846–852.
| Bovine placental progesterone synthesis: comparison of first and second trimesters of gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xit1ymsbc%3D&md5=4e4de33c859f61bb926f2109c893d57aCAS | 1591339PubMed |
Kim, H., Kang, S., Cho, G., and Choi, W. (2004). Steroidogenic acute regulatory protein: its presence and function in brain neurosteroidogenesis. Arch. Histol. Cytol. 67, 383–392.
| Steroidogenic acute regulatory protein: its presence and function in brain neurosteroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFWnt78%3D&md5=4a6fa042e1d840f0ca94372d2621b360CAS | 15781980PubMed |
Klisch, K., Hecht, W., Pfarrer, C., Schuler, G., Hoffmann, B., and Leiser, R. (1999a). DNA content and ploidy level of bovine placentomal trophoblast giant cells. Placenta 20, 451–458.
| DNA content and ploidy level of bovine placentomal trophoblast giant cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzltVGruw%3D%3D&md5=ea1d76ef95dd1da874d40cfc318f49e6CAS | 10419810PubMed |
Klisch, K., Pfarrer, C., Schuler, G., Hoffmann, B., and Leiser, R. (1999b). Tripolar acytokinetic mitosis and formation of feto-maternal syncytia in the bovine placentome: different modes of the generation of multinuclear cells. Anat. Embryol. 200, 229–237.
| Tripolar acytokinetic mitosis and formation of feto-maternal syncytia in the bovine placentome: different modes of the generation of multinuclear cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cvnvVylsg%3D%3D&md5=c6e5ce0486f2de16b6dfbab2e47b17a3CAS | 10424879PubMed |
Lee, C. S., Gogolin-Ewens, K., White, T. R., and Brandon, M. R. (1985). Studies on the distribution of binucleate cells in the placenta of the sheep with a monoclonal antibody SBU-3. J. Anat. 140, 565–576.
| 4077697PubMed |
Lee, C. S., Ralph, M. M., Gogolin-Ewens, K. J., and Brandon, M. R. (1990). Monoclonal antibody (SBU-1 and SBU-3) identification of cells dissociated from the sheep placentomal trophoblast. J. Histochem. Cytochem. 38, 649–652.
| Monoclonal antibody (SBU-1 and SBU-3) identification of cells dissociated from the sheep placentomal trophoblast.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c3jslCmtQ%3D%3D&md5=d5fb745c328b5cdee393e30aa5b6f864CAS | 1692053PubMed |
Li, Y., Isomaaa, V., Pulkka, A., Herva, R., Peltoketo, H., and Vihko, P. (2005). Expression of 3β-hydroxysteroid dehydrogenase type 1, P450 aromatase, and 17β-hydroxysteroid dehydrogenase types 1, 2, 5 and 7 mRNAs in human early and mid-gestation placentas. Placenta 26, 387–392.
| Expression of 3β-hydroxysteroid dehydrogenase type 1, P450 aromatase, and 17β-hydroxysteroid dehydrogenase types 1, 2, 5 and 7 mRNAs in human early and mid-gestation placentas.Crossref | GoogleScholarGoogle Scholar | 15850643PubMed |
Linzell, J. L., and Heap, R. B. (1968). A comparison of progesterone metabolism in the pregnant sheep and goat: sources of production and an estimation of uptake by some target organs. J. Endocrinol. 41, 433-NP.
| A comparison of progesterone metabolism in the pregnant sheep and goat: sources of production and an estimation of uptake by some target organs.Crossref | GoogleScholarGoogle Scholar |
Liu, J., Rone, M. B., and Papadopoulos, V. (2006). Protein–protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J. Biol. Chem. 281, 38 879–38 893.
| Protein–protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12msrvL&md5=23219b9b22014351dd383cdd95f519f9CAS |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) Method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) Method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=e0ea026c02920b4196beca401ea8984bCAS | 11846609PubMed |
Manna, P. R., Dyson, M. T., and Stocco, D. M. (2009). Regulation of the steroidogenic acute regulatory protein gene expression: present and future perspectives. Mol. Hum. Reprod. 15, 321–333.
| Regulation of the steroidogenic acute regulatory protein gene expression: present and future perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVWktLc%3D&md5=a20a241284a9aad2acb96d14b0e5bfb2CAS | 19321517PubMed |
Matamoros, R. A., Caamano, L., Lamb, S. V., and Reimers, T. J. (1994). Estrogen production by bovine binucleate and mononucleate trophoblastic cells in vitro. Biol. Reprod. 51, 486–492.
| Estrogen production by bovine binucleate and mononucleate trophoblastic cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsV2gt7c%3D&md5=93afca2c78866ad75f09855379d65dacCAS | 7803620PubMed |
Miller, W. L. (2007). Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter. Biochim. Biophys. Acta 1771, 663–676.
| 1:CAS:528:DC%2BD2sXmtlWgtr4%3D&md5=62d8fae8b8cfb33740c0ce935fc839ccCAS | 17433772PubMed |
Murayama, C., Miyazaki, H., Miyamoto, A., and Shimizu, T. (2008). Involvement of Ad4BP/SF-1, DAX-1, and COUP-TFII transcription factor on steroid production and luteinization in ovarian theca cells. Mol. Cell. Biochem. 314, 51–58.
| Involvement of Ad4BP/SF-1, DAX-1, and COUP-TFII transcription factor on steroid production and luteinization in ovarian theca cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFKnu7g%3D&md5=ead14d77f1ae1da841c2eb3748c84d4cCAS | 18409030PubMed |
Nara, B. S., Darmadja, D., and First, N. L. (1981). Effect of removal of follicles, corpora lutea or ovaries on maintenance of pregnancy in swine. J. Anim. Sci. 52, 794–801.
| 1:CAS:528:DyaL3MXitVKns70%3D&md5=e672ff99f4f0defbfb83935c7423d4c5CAS | 7263538PubMed |
Nash, A. R., Glenn, W. K., Moore, S. S., Kerr, J., Thompson, A. R., and Thompson, E. O. (1988). Oestrogen sulfotransferase: molecular cloning and sequencing of cDNA for the bovine placental enzyme. Aust. J. Biol. Sci. 41, 507–516.
| 1:CAS:528:DyaK3cXntFantQ%3D%3D&md5=14a36baf9e2f8dbeb3dc1a7a365be087CAS | 3271383PubMed |
Nicol, M., Wang, H., Ivell, R., Morley, S., Walker, S., and Mason, J. (1998). The expression of steroidogenic acute regulatory protein (StAR) in bovine adrenocortical cells. Endocr. Res. 24, 565–569.
| The expression of steroidogenic acute regulatory protein (StAR) in bovine adrenocortical cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvVSjsw%3D%3D&md5=efd88dfdfa3672e04708307f8022b5f5CAS | 9888538PubMed |
Nishimura, R., Sakumoto, R., Tatsukawa, Y., Acosta, T. J., and Okuda, K. (2006). Oxygen concentration is an important factor for modulating progesterone synthesis in bovine corpus luteum. Endocrinology 147, 4273–4280.
| Oxygen concentration is an important factor for modulating progesterone synthesis in bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xpt1SjtbY%3D&md5=3173d8e999294c129cb386e5996c084eCAS | 16740971PubMed |
Orisaka, M., Tajima, K., Mizutani, T., Miyamoto, K., Tsang, B. K., Fukuda, S., Yoshida, Y., and Kotsuji, F. (2006). Granulosa cells promote differentiation of cortical stromal cells into theca cells in the bovine ovary. Biol. Reprod. 75, 734–740.
| Granulosa cells promote differentiation of cortical stromal cells into theca cells in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCgt7nN&md5=424345ed92ad8176800f5f5ce8e26d9fCAS | 16914692PubMed |
Pace, M. M., Augenstein, M. L., Betthauser, J. M., Childs, L. A., Eilertsen, K. J., Enos, J. M., Forsberg, E. J., Golueke, P. J., Graber, D. F., Kemper, J. C., Koppang, R. W., Lange, G., Lesmeister, T. L., Mallon, K. S., Mell, G. D., Misica, P. M., Pfister-Genskow, M., Strelchenko, N. S., Voelker, G. R., Watt, S. R., and Bishop, M. D. (2002). Ontogeny of cloned cattle to lactation. Biol. Reprod. 67, 334–339.
| Ontogeny of cloned cattle to lactation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvV2iurk%3D&md5=1c25534805af1a6f5f9ec9babe28f25bCAS | 12080037PubMed |
Pasqualini, J. R. (2005). Enzymes involved in the formation and transformation of steroid hormones in the fetal and placental compartments. J. Steroid Biochem. Mol. Biol. 97, 401–415.
| Enzymes involved in the formation and transformation of steroid hormones in the fetal and placental compartments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1OntL3K&md5=ed888da44cf7f50593f0b442b0230943CAS | 16202579PubMed |
Pescador, N., Soumano, K., Stocco, D., Price, C., and Murphy, B. (1996). Steroidogenic acute regulatory protein in bovine corpora lutea. Biol. Reprod. 55, 485–491.
| Steroidogenic acute regulatory protein in bovine corpora lutea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltlGrur0%3D&md5=c93fee164be29faf1364e8ee00b2a5b9CAS | 8828859PubMed |
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
| A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=3cfd2ff99dae9a87dc2a76cece195022CAS | 11328886PubMed |
Pilon, N., Daneau, I., Brisson, C., Ethier, J., Lussier, J., and Silversides, D. (1997). Porcine and bovine steroidogenic acute regulatory protein (StAR) gene expression during gestation. Endocrinology 138, 1085–1091.
| Porcine and bovine steroidogenic acute regulatory protein (StAR) gene expression during gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1OqtLg%3D&md5=1fe0ca1f310e6c0e9d0cd2789cca8c47CAS | 9048613PubMed |
Schuler, G., Wirth, C., Klisch, K., Pfarrer, C., Leiser, R., and Hoffmann, B. (1999). Immunolocalization of progesterone receptors in bovine placentomes throughout mid and late gestation and at parturition. Biol. Reprod. 61, 797–801.
| Immunolocalization of progesterone receptors in bovine placentomes throughout mid and late gestation and at parturition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFCqtrY%3D&md5=7eec8b1eaa1835222fa2e94bdfbf6bc0CAS | 10456859PubMed |
Schuler, G., Teichmann, U., Taubert, A., Failing, K., and Hoffmann, B. (2005). Estrogen receptor beta (ERbeta) is expressed differently from ERalpha in bovine placentomes. Exp. Clin. Endocrinol. Diabetes 113, 107–114.
| Estrogen receptor beta (ERbeta) is expressed differently from ERalpha in bovine placentomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivVaiu7g%3D&md5=696a3752785c51f7ca1331464af0cc8aCAS | 15772903PubMed |
Schuler, G., Ozalp, G. R., Hoffmann, B., Harada, N., Browne, P., and Conley, A. J. (2006). Reciprocal expression of 17alpha-hydroxylase-C17,20-lyase and aromatase cytochrome P450 during bovine trophoblast differentiation: a two-cell system drives placental oestrogen synthesis. Reproduction 131, 669–679.
| Reciprocal expression of 17alpha-hydroxylase-C17,20-lyase and aromatase cytochrome P450 during bovine trophoblast differentiation: a two-cell system drives placental oestrogen synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltV2jtr0%3D&md5=8f5b04e4ed7d0ec7882efa876bfc994eCAS | 16595718PubMed |
Schuler, G., Greven, H., Kowalewski, M. P., Doring, B., Ozalp, G. R., and Hoffmann, B. (2008). Placental steroids in cattle: hormones, placental growth factors or by-products of trophoblast giant cell differentiation? Exp. Clin. Endocrinol. Diabetes 116, 429–436.
| Placental steroids in cattle: hormones, placental growth factors or by-products of trophoblast giant cell differentiation?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Sgtb3P&md5=c6d2f52402f9df6973ebffdd6e5ee518CAS | 18704836PubMed |
Shemesh, M., Izhar, M., Pasmanik, M., and Shore, L. S. (1992). Regulation of steroidogenesis in the bovine placenta. J. Physiol. Pharmacol. 43, 153–163.
| 1:CAS:528:DyaK2cXktVGmtbo%3D&md5=c479d2e0f07f54b4ee259dab652316ceCAS | 1343967PubMed |
Simpson, E. R., and Boyd, G. S. (1966). The cholesterol side-chain cleavage system of the adrenal cortex: a mixed-function oxidase. Biochem. Biophys. Res. Commun. 24, 10–17.
| The cholesterol side-chain cleavage system of the adrenal cortex: a mixed-function oxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28XksV2htbw%3D&md5=11c6c8f4ac8700ee94f1647e325ba5c4CAS | 5966391PubMed |
Słomczyńska, M., and Woźniak, J. (2001). Differential distribution of estrogen receptor-beta and estrogen receptor-alpha in the porcine ovary. Exp. Clin. Endocrinol. Diabetes 109, 238–244.
| Differential distribution of estrogen receptor-beta and estrogen receptor-alpha in the porcine ovary.Crossref | GoogleScholarGoogle Scholar | 11453037PubMed |
Stocco, D. M. (2000). Intramitochondrial cholesterol transfer. Biochim. Biophys. Acta 1486, 184–197.
| 1:CAS:528:DC%2BD3cXlt1SntLw%3D&md5=5236390873af117c1f02a75b10609965CAS | 10856721PubMed |
Takagi, M., Yamamoto, D., Ohtani, M., and Miyamoto, A. (2007). Quantitative analysis of messenger RNA expression of matrix metalloproteinases (MMP-2 and MMP-9), tissue inhibitor-2 of matrix metalloproteinases (TIMP-2), and steroidogenic enzymes in bovine placentomes during gestation and postpartum. Mol. Reprod. Dev. 74, 801–807.
| Quantitative analysis of messenger RNA expression of matrix metalloproteinases (MMP-2 and MMP-9), tissue inhibitor-2 of matrix metalloproteinases (TIMP-2), and steroidogenic enzymes in bovine placentomes during gestation and postpartum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtlKlsb4%3D&md5=9edfe2d5d3e27eb10f024f2b772f95c2CAS | 17154296PubMed |
Tsumagari, S., Kamata, J., Takagi, K., Tanemura, K., Yosai, A., and Takeishi, M. (1994). 3 beta-Hydroxysteroid dehydrogenase activity and gestagen concentrations in bovine cotyledons and caruncles during gestation and parturition. J. Reprod. Fertil. 102, 35–39.
| 3 beta-Hydroxysteroid dehydrogenase activity and gestagen concentrations in bovine cotyledons and caruncles during gestation and parturition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit12rt7w%3D&md5=260f74df4ba7f8ca0d8a4f3857d1e0deCAS | 7799323PubMed |
Ushizawa, K., Takahashi, T., Hosoe, M., Ishiwata, H., Kaneyama, K., Kizaki, K., and Hashizume, K. (2007). Global gene expression analysis and regulation of the principal genes expressed in bovine placenta in relation to the transcription factor AP-2 family. Reprod. Biol. Endocrinol. 5, 17.
| Global gene expression analysis and regulation of the principal genes expressed in bovine placenta in relation to the transcription factor AP-2 family.Crossref | GoogleScholarGoogle Scholar | 17462098PubMed |
Weems, C. W., Vincent, D. L., and Weems, Y. S. (1992). Roles of prostaglandins (PG) F2 alpha, E1, E2, adenosine, oestradiol-17 beta, histone-H2A and progesterone of conceptus, uterine or ovarian origin during early and mid pregnancy in the ewe. Reprod. Fertil. Dev. 4, 289–295.
| Roles of prostaglandins (PG) F2 alpha, E1, E2, adenosine, oestradiol-17 beta, histone-H2A and progesterone of conceptus, uterine or ovarian origin during early and mid pregnancy in the ewe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXjtlShsw%3D%3D&md5=d227bc90a24723c3a749b261464273cfCAS | 1438960PubMed |
Wooding, F. B. (1992). Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta 13, 101–113.
| Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XkvVenurg%3D&md5=38b4e9bb5985036f096b3e399ed492c8CAS | 1631024PubMed |
Zirkin, B. (1998). Spermatogenesis: its regulation by testosterone and FSH. Semin. Cell Dev. Biol. 9, 417–421.
| Spermatogenesis: its regulation by testosterone and FSH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFyk&md5=f3cbd5fc4f1039511b95aff9ea5685c7CAS | 9813188PubMed |
