Steroids in the equine oviduct: synthesis, local concentrations and receptor expression
Hilde Nelis A , Julie Vanden Bussche B , Bartosz Wojciechowicz E , Anita Franczak E , Lynn Vanhaecke B , Bart Leemans A , Pieter Cornillie D , Luc Peelman C , Ann Van Soom A and Katrien Smits A F
+ Author Affiliations
- Author Affiliations
A Ghent University, Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Salisburylaan 133, 9820 Merelbeke, Belgium.
B Ghent University, Department of Veterinary Public Health and Food Safety, Laboratory of Chemical Analysis, Faculty of Veterinary Medicine, Salisburylaan 133, 9820 Merelbeke, Belgium.
C Ghent University, Department of Nutrition, Genetics and Ethology, Faculty of Veterinary Medicine, Heidestraat 19 , 9820 Merelbeke, Belgium.
D Ghent University, Department of Morphology, Faculty of Veterinary Medicine, Salisburylaan 133, 9820 Merelbeke, Belgium.
E University of Warmia and Mazury, Department of Animal Physiology, Faculty of Biology and Biotechnology, Oczapowskiego St. 1A, 10-719 Olsztyn, Poland.
F Corresponding author. Email: katrien.smits@ugent.be
Reproduction, Fertility and Development 28(9) 1390-1404 https://doi.org/10.1071/RD14483
Submitted: 4 December 2014 Accepted: 20 January 2015 Published: 10 March 2015
Abstract
Steroids play an important role in mammalian reproduction and early pregnancy. Although systemic changes in steroid concentrations have been well documented, it is not clear how these correlate with local steroid concentrations in the genital tract. We hypothesised that, in the horse, the preimplantation embryo may be subjected to high local steroid concentrations for several days. Therefore, we measured progesterone, 17-hydroxyprogesterone, 17β-oestradiol, testosterone and 17α-testosterone concentrations in equine oviductal tissue by ultra-HPLC coupled with tandem mass spectrometry, and progesterone, 17β-oestradiol, oestrone and testosterone concentrations in oviduct fluid by radioimmunoassay, with reference to cycle stage and side of ovulation. Progesterone concentrations were high in oviductal tissue and fluid ipsilateral to the ovulation side during dioestrus, whereas other steroid hormone concentrations were not influenced by the side of ovulation. These results suggest that the high ipsilateral progesterone concentration is caused by: (1) contributions from the follicular fluid in the oviduct and diffusion of follicular fluid steroids after ovulation; (2) local transfer of steroids via blood or lymph; (3) local synthesis of progesterone in the oviduct, as evidenced by the expression of steroidogenic enzymes; and (4) a paracrine contribution from follicular cells. These data provide a basis for the study of the importance of endocrine and paracrine signalling during early embryonic development in the horse.
Additional keywords: aromatase, cytochrome P450scc, follicular fluid, 3β-hydroxysteroid dehydrogenase, mare, oviductal fluid, progesterone receptor, serum, steroidogenesis, steroidogenic acute regulatory protein.
References
Abu-Hijleh, M. F., Habbal, O. A., and Moqattash, S. T. (1995). The role of the diaphragm in lymphatic absorption from the peritoneal cavity. J. Anat. 186, 453–467.| 7559120PubMed |
Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402.
| 1:CAS:528:DyaK2sXlvFyhu7w%3D&md5=245e7bbb3d93900bbc757a9778bf41f2CAS | 9254694PubMed |
Ballester, L., Romero-Aguirregomezcorta, J., Soriano-Ubeda, C., Matas, C., Romar, R., and Coy, P. (2014). Timing of oviductal fluid collection, steroid concentrations, and sperm preservation method affect porcine in vitro fertilization efficiency. Fertil. Steril. 102, 1762–1768.e1.
| Timing of oviductal fluid collection, steroid concentrations, and sperm preservation method affect porcine in vitro fertilization efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1SqurrM&md5=904616b18102be0a0fc3e78dd88e3a58CAS | 25241366PubMed |
Barone, R. (2001). Anatomie comparée des mammifères domestiques. In: ‘Anatomie comparée des mammifères domestiques’. (Ed. Vigot.) p. 322. (Editions Vigot: Paris.)
Bauersachs, S., Blum, H., Mallok, S., Wenigerkind, H., Rief, S., Prelle, K., and Wolf, E. (2003). Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: A transcriptomics approach. Biol. Reprod. 68, 1170–1177.
| Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: A transcriptomics approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVert7g%3D&md5=3d571bcec52907f88c755dbe68e42f35CAS | 12606461PubMed |
Bendz, A. (1977). Anatomical basis for a possible counter current exchange mechanism in human adnex. Prostaglandins 13, 355–362.
| Anatomical basis for a possible counter current exchange mechanism in human adnex.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s7kvFOktg%3D%3D&md5=9cf542e818974d4bf4235adb89e04ea6CAS | 847239PubMed |
Bendz, A., Einerjensen, N., Lundgren, O., and Janson, P. O. (1979). Exchange of Kr-85 between the blood-vessels of the human uterine adnexa. J. Reprod. Fertil. 57, 137–142.
| Exchange of Kr-85 between the blood-vessels of the human uterine adnexa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c%2FnsVOmtA%3D%3D&md5=899d44f874512e10afd6e152142c6780CAS | 512996PubMed |
Bennett, W. A., Watts, T. L., Blair, W. D., Waldhalm, S. J., and Fuquay, J. W. (1988). Patterns of oviducal motility in the cow during the estrous-cycle. J. Reprod. Fertil. 83, 537–543.
| Patterns of oviducal motility in the cow during the estrous-cycle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1czhs1yiuw%3D%3D&md5=a4e608e46377015c6e55cdd230620884CAS | 3411549PubMed |
Bologna-Molina, R., Damian-Matsumura, P., and Molina-Frechero, N. (2011). An easy cell counting method for immunohistochemistry that does not use an image analysis program. Histopathology 59, 801–803.
| An easy cell counting method for immunohistochemistry that does not use an image analysis program.Crossref | GoogleScholarGoogle Scholar | 21939456PubMed |
Burry, R. W. (2011). Controls for immunocytochemistry: an update. J. Histochem. Cytochem. 59, 6–12.
| Controls for immunocytochemistry: an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvVOlsLs%3D&md5=409c47667ef7cf6385a0331bd0f798d2CAS | 20852036PubMed |
Campbell, D. L., Douglas, L. W., and Ramge, J. C. (1979). Cannulation of the equine oviduct and chemical-analysis of oviduct fluid. Theriogenology 12, 47–59.
| Cannulation of the equine oviduct and chemical-analysis of oviduct fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXlsFCru70%3D&md5=0f3091d6e1017c8927090c9ad4ba578fCAS | 16725431PubMed |
Chabrolle, C., Tosca, L., Rame, C., Lecomte, P., Royere, D., and Dupont, J. (2009). Adiponectin increases insulin-like growth factor I-induced progesterone and estradiol secretion in human granulosa cells. Fertil. Steril. 92, 1988–1996.
| Adiponectin increases insulin-like growth factor I-induced progesterone and estradiol secretion in human granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFGisLs%3D&md5=6e6605bd5200ee124a4974a452664bc1CAS | 19081562PubMed |
Chen, S., Einspanier, R., and Schoen, J. (2013). Long-term culture of primary porcine oviduct epithelial cells: validation of a comprehensive in vitro model for reproductive science. Theriogenology 80, 862–869.
| Long-term culture of primary porcine oviduct epithelial cells: validation of a comprehensive in vitro model for reproductive science.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlagsrzM&md5=8c1e17368ae32a79047e3072a3b9312aCAS | 23973051PubMed |
Cicinelli, E., Einer-Jensen, N., Cignarelli, M., Mangiacotti, L., Luisi, D., and Schonauer, S. (2004). Preferential transfer of endogenous ovarian steroid hormones to the uterus during both the follicular and luteal phases. Hum. Reprod. 19, 2001–2004.
| Preferential transfer of endogenous ovarian steroid hormones to the uterus during both the follicular and luteal phases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsVyisLc%3D&md5=a588d6a2ad481e80a42d55739a3f0cf9CAS | 15243001PubMed |
Ciereszko, R. (1999). Radioimmunologiczne oznaczanie stężenia hormonów steroidowych w płynach biologicznych [Radioimmunoassay of steroid hormones in biological fluids]. In: ‘Animal Physiology’. (Ed. J. Przala.) pp. 157–163. (UWM Press: Olsztyn.)
Daels, P., and Hughes, J. P. (1993). The normal oestrous cycle. In: ‘Equine Reproduction’. (Eds A. McKinnon and P. L. A. M. Vos.) pp. 121–133. (Lea & Febiger: Philadelphia.)
De Bosschere, H., Ducatelle, R., Vermeirsch, H., Simoens, P., and Coryn, M. (2002). Estrogen-alpha and progesterone receptor expression in cystic endometrial hyperplasia and pyometra in the bitch. Anim. Reprod. Sci. 70, 251–259.
| Estrogen-alpha and progesterone receptor expression in cystic endometrial hyperplasia and pyometra in the bitch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis1ensro%3D&md5=5c4e33434c16744304be79fe473ec03fCAS | 11943494PubMed |
Desantis, S., Ventriglia, G., Zizza, S., Guaricci, A. C., Losurdo, M., Zarrilli, A., and Albrizio, M. (2010). Changes in the expression of the mu-opioid receptor in the mare oviduct during oestrus and anoestrus. Anim. Reprod. Sci. 119, 40–49.
| Changes in the expression of the mu-opioid receptor in the mare oviduct during oestrus and anoestrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1Kjs7c%3D&md5=869dbfc88b92fa870c14fa824b009d78CAS | 20036785PubMed |
Einer-Jensen, N. (1988). Countercurrent transfer in the ovarian pedicle and its physiological implications. Oxf. Rev. Reprod. Biol. 10, 348–381.
| 1:STN:280:DyaL1M3itVSksg%3D%3D&md5=c37226f00f7c63955c1192584d997a1fCAS | 3072505PubMed |
Einer-Jensen, N., and Hunter, R. H. F. (2000). Physiological and pharmacological aspects of local transfer of substances in the ovarian adnexa in women. Hum. Reprod. Update 6, 132–138.
| Physiological and pharmacological aspects of local transfer of substances in the ovarian adnexa in women.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3kt1Kltw%3D%3D&md5=5025135b950a5a4cc57a167e7f6625c5CAS | 10782571PubMed |
Einer-Jensen, N., and Hunter, R. H. F. (2005). Counter-current transfer in reproductive biology. Reproduction 129, 9–18.
| Counter-current transfer in reproductive biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1eltb4%3D&md5=01769c10940819692d983ceda7f08a7fCAS | 15615894PubMed |
Einerjensen, N., and McCracken, J. A. (1981). Physiological-aspects of corpus-luteum blood-flow and of the counter system in the ovarian pedicle of the sheep. Acta Vet. Scand. Suppl. 77, 89–101.
| 1:STN:280:DyaL38%2FmsFWgtA%3D%3D&md5=b3937fad24f157596996a2e9c50e204eCAS |
Eisenbach, M., and Giojalas, L. C. (2006). Sperm guidance in mammals: an unpaved road to the egg. Nat. Rev. Mol. Cell Biol. 7, 276–285.
| Sperm guidance in mammals: an unpaved road to the egg.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt12qsLY%3D&md5=0c188eec62ff400edd8ac3eae05a2588CAS | 16607290PubMed |
Faul, F., Erdfelder, E., Lang, A. G., and Buchner, A. (2007). G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 39, 175–191.
| G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences.Crossref | GoogleScholarGoogle Scholar | 17695343PubMed |
Franczak, A., and Bogacki, M. (2009). Local and systemic effects of embryos on uterine tissues during early pregnancy in pigs. J. Reprod. Dev. 55, 262–272.
| Local and systemic effects of embryos on uterine tissues during early pregnancy in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFehtb0%3D&md5=d99e643b7c14921a3fed1896fe5d516aCAS | 19293562PubMed |
Franczak, A., Kotwica, G., Kurowicka, B., Oponowicz, A., Woclawek-Potocka, I., and Petroff, B. K. (2006). Expression of enzymes of cyclooxygenase pathway and secretion of prostaglandin E-2 and F-2 alpha by porcine myometrium during luteolysis and early pregnancy. Theriogenology 66, 1049–1056.
| Expression of enzymes of cyclooxygenase pathway and secretion of prostaglandin E-2 and F-2 alpha by porcine myometrium during luteolysis and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotleqsL0%3D&md5=743670f48de0457dea76a732909cbeb5CAS | 16616952PubMed |
Franczak, A., Wojciechowicz, B., Zmijewska, A., Kolakowska, J., and Kotwica, G. (2013). The effect of interleukin 1 beta and interleukin 6 on estradiol-17 beta secretion in the endometrium of pig during early pregnancy and the estrous cycle. Theriogenology 80, 90–98.
| The effect of interleukin 1 beta and interleukin 6 on estradiol-17 beta secretion in the endometrium of pig during early pregnancy and the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmsFagtb4%3D&md5=03ac77cc177823ff262a6f651249432bCAS | 23615429PubMed |
Fukuda, M., Fukuda, K., Andersen, C. Y., and Byskov, A. G. (1997). Does corpus luteum locally affect follicular growth negatively? Hum. Reprod. 12, 1024–1027.
| Does corpus luteum locally affect follicular growth negatively?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szjsl2rug%3D%3D&md5=873bccccfca992675bbeb255b9d08851CAS | 9194659PubMed |
Gabler, C., Einspanier, A., Schams, D., and Einspanier, R. (1999). Expression of vascular endothelial growth factor (VEGF) and its corresponding receptors (flt-1 and flk-1) in the bovine oviduct. Mol. Reprod. Dev. 53, 376–383.
| Expression of vascular endothelial growth factor (VEGF) and its corresponding receptors (flt-1 and flk-1) in the bovine oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVOlsrY%3D&md5=597cced0e96bfbae7d33c4d7d6187c41CAS | 10398412PubMed |
Gardner, D. K., Lane, M., Calderon, I., and Leeton, J. (1996). Environment of the preimplantation human embryo in vivo: Metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells. Fertil. Steril. 65, 349–353.
| 1:STN:280:DyaK287lsVSitA%3D%3D&md5=31b3bc16b76b68d1a98ad401b22e1d1eCAS | 8566260PubMed |
Georgiou, A. S., Sostaric, E., Wong, C. H., Snijders, A. P. L., Wright, P. C., Moore, H. D., and Fazeli, A. (2005). Gametes alter the oviductal secretory proteome. Mol. Cell. Proteomics 4, 1785–1796.
| Gametes alter the oviductal secretory proteome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Cgtb%2FK&md5=510c164d30b93ac876edfd2fc1ee1373CAS | 16105986PubMed |
Ginther, O. J. (1974). Internal regulation of physiological processes through local venoarterial pathways: review. J. Anim. Sci. 39, 550–564.
| 1:STN:280:DyaE2M%2FhtFamsQ%3D%3D&md5=5735d4cc841b892e8c778a2238a4715dCAS | 4213194PubMed |
Ginther, O. J. (1976). Comparative anatomy of the uteroovarian vasculature. In ‘Veterinary Scope. Vol. 20’. pp. 1–17. (Upjohn Co.: Kalamazoo, Michigan.)
Ginther, O. J., Garcia, M. C., Squires, E. L., and Steffenhagen, W. P. (1972). Anatomy of vasculature of uterus and ovaries in mare. Am. J. Vet. Res. 33, 1561–1568.
| 1:STN:280:DyaE383kt1SjsA%3D%3D&md5=7446cabe4160132a355b66d6b29d33c1CAS | 5047115PubMed |
Ginther, O. J., Gastal, E. L., Gastal, M. O., Utt, M. D., and Beg, M. A. (2007). Luteal blood flow and progesterone production in mares. Anim. Reprod. Sci. 99, 213–220.
| Luteal blood flow and progesterone production in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1GmsL4%3D&md5=5a5207728b30b97c52c08bb66510e828CAS | 16815650PubMed |
Ginther, O. J., Gastal, E. L., Gastal, M. O., and Beg, M. A. (2008). Passage of postovulatory follicular fluid into the peritoneal cavity and the effect on concentrations of circulating hormones in mares. Anim. Reprod. Sci. 107, 1–8.
| Passage of postovulatory follicular fluid into the peritoneal cavity and the effect on concentrations of circulating hormones in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlyhsro%3D&md5=cc0f1725299824b692265e39a5d285c8CAS | 18448279PubMed |
Guidobaldi, H. A., Teves, M. E., Unates, D. R., Anastasia, A., and Giojalas, L. C. (2008). Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex. PLoS ONE 3, e3040.
| Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex.Crossref | GoogleScholarGoogle Scholar | 18725941PubMed |
Hai, M. T. V., Logeat, F., Warembourg, M., and Milgrom, E. (1977). Hormonal-control of progesterone receptors. Ann. N. Y. Acad. Sci. 286, 199–209.
| Hormonal-control of progesterone receptors.Crossref | GoogleScholarGoogle Scholar |
Hartt, L. S., Carling, S. J., Joyce, M. M., Johnson, G. A., Vanderwall, D. K., and Ott, T. L. (2005). Temporal and spatial associations of oestrogen receptor alpha and progesterone receptor in the endometrium of cyclic and early pregnant mares. Reproduction 130, 241–250.
| Temporal and spatial associations of oestrogen receptor alpha and progesterone receptor in the endometrium of cyclic and early pregnant mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVSksbvF&md5=f1c90504cdd9fa06e3b47412dbecece7CAS | 16049162PubMed |
Hayes, K. E. N., Pierson, R. A., Scraba, S. T., and Ginther, O. J. (1985). Effects of estrous-cycle and season on ultrasonic uterine anatomy in mares. Theriogenology 24, 465–477.
| Effects of estrous-cycle and season on ultrasonic uterine anatomy in mares.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVylug%3D%3D&md5=95b0cb9697e246f60cf973a11d37a415CAS |
Heggland, S. J., Signs, S. A., and Stalvey, J. R. D. (1997). Testosterone decreases 3 beta-hydroxysteroid dehydrogenase-isomerase messenger ribonucleic acid in cultured mouse Leydig cells by a strain-specific mechanism. J. Androl. 18, 646–655.
| 1:CAS:528:DyaK1cXjtlOnug%3D%3D&md5=a718e4feb4ef5748fac7fef5c38bbaaaCAS | 9432137PubMed |
Hillier, S. G., Vandenboogaard, A. M. J., Reichert, L. E., and Vanhall, E. V. (1980). Alterations in granulosa-cell aromatase-activity accompanying preovulatory follicular development in the rat ovary with evidence that 5-alpha-reduced c-19 steroids inhibit the aromatase reaction in vitro. J. Endocrinol. 84, 409–419.
| Alterations in granulosa-cell aromatase-activity accompanying preovulatory follicular development in the rat ovary with evidence that 5-alpha-reduced c-19 steroids inhibit the aromatase reaction in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXktVCrsbg%3D&md5=9158537256004de8f8d259e92874d1beCAS | 7190181PubMed |
Hunter, R. H. F. (2012). Components of oviduct physiology in eutherian mammals. Biol. Rev. Camb. Philos. Soc. 87, 244–255.
| Components of oviduct physiology in eutherian mammals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC387htFKitw%3D%3D&md5=f188947b15a93b3b38691ce6b8c1eb5bCAS |
Hunter, R. H. F., Cook, B., and Poyser, N. L. (1983). Regulation of oviduct function in pigs by local transfer of ovarian-steroids and prostaglandins: a mechanism to influence sperm transport. Eur. J. Obstet. Gynecol. Reprod. Biol. 14, 225–232.
| Regulation of oviduct function in pigs by local transfer of ovarian-steroids and prostaglandins: a mechanism to influence sperm transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhslersbc%3D&md5=a2e938884c668aaa19f59e66cf6f1ecdCAS |
Kendle, K. E., and Lee, B. (1980). Investigation of the influence of progesterone on mouse embryo transport by using anti-progestational steroids. J. Reprod. Fertil. 58, 253–258.
| Investigation of the influence of progesterone on mouse embryo transport by using anti-progestational steroids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXovVartA%3D%3D&md5=6ca69568202c02cde498a4eb73c36a9bCAS | 6898668PubMed |
Kobayashi, F., Zimniski, S. J., and Smalley, K. N. (1996). Characterization of oviductal aromatase in the northern leopard frog, Rana pipens. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 113, 653–657.
| Characterization of oviductal aromatase in the northern leopard frog, Rana pipens.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK283gvV2ntw%3D%3D&md5=0292460687cfe522cc3601ce9158492fCAS | 8829814PubMed |
Kotwica, J., Williams, G. L., and Marchello, M. J. (1982). Countercurrent transfer of testosterone by the ovarian vascular pedicle of the cow: evidence for a relationship to follicular steroidogenesis. Biol. Reprod. 27, 778–789.
| Countercurrent transfer of testosterone by the ovarian vascular pedicle of the cow: evidence for a relationship to follicular steroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXivVWlsg%3D%3D&md5=ca3113c66f76fc2224198f3e2ddeea2fCAS | 7171665PubMed |
Kunz, G., Herbertz, M., Noe, M., and Leyendecker, G. (1998). Sonographic evidence for the involvement of the utero-ovarian counter-current system in the ovarian control of directed uterine sperm transport. Hum. Reprod. Update 4, 667–672.
| Sonographic evidence for the involvement of the utero-ovarian counter-current system in the ovarian control of directed uterine sperm transport.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7kvFyltA%3D%3D&md5=9f3b2bb323bf5f4c5c0310def12777f9CAS | 10027620PubMed |
Lavoie, H. A., and King, S. R. (2009). Transcriptional regulation of steroidogenic genes: STARD1, CYP11A1 and HSD3B. Exp. Biol. Med. (Maywood) 234, 880–907.
| Transcriptional regulation of steroidogenic genes: STARD1, CYP11A1 and HSD3B.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt1WksLs%3D&md5=d5cf632e44ffb116cf9e3d53285d2535CAS | 19491374PubMed |
Leak, L. V., and Rahil, K. (1978). Permeability of diaphragmatic mesothelium: ultrastructural basis for stomata. Am. J. Anat. 151, 557–593.
| Permeability of diaphragmatic mesothelium: ultrastructural basis for stomata.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c7mtlamtg%3D%3D&md5=491cae88200a7b4712207c2586bf3b5dCAS | 645618PubMed |
Li, Y., Qin, L., Xiao, Z. H., Wang, Y. L., Herva, R., Leng, J. H., Lang, J. H., Isomaa, V., and Piao, Y. S. (2003). Expression of P450 aromatase and 17 beta-hydroxysteroid dehydrogenase type 1 at fetal-maternal interface during tubal pregnancy. J. Steroid Biochem. Mol. Biol. 87, 241–246.
| Expression of P450 aromatase and 17 beta-hydroxysteroid dehydrogenase type 1 at fetal-maternal interface during tubal pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSjtbjL&md5=6693296395be291d65e9f5d076b901ecCAS | 14698204PubMed |
McCracken, J. A., Schramm, W., and Einer-Jensen, N. (1984). The structure of steroids and their diffusion through blood-vessel walls in a countercurrent system. Steroids 43, 293–303.
| The structure of steroids and their diffusion through blood-vessel walls in a countercurrent system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktVSluw%3D%3D&md5=3e3c65eb474d03ce7c0f5b96df1e65c2CAS | 6523546PubMed |
McDonald, M., Malone, E., and McBride, J. (2010). Confirmation of hormones in animal serum by liquid chromatography/tandem mass spectrometry according to European Commission Decision 2002/657. J. AOAC Int. 93, 343–349.
| 1:CAS:528:DC%2BC3cXjtVajtbY%3D&md5=eb6a7d1f85f3ed59d4422fc44815e0d7CAS | 20334197PubMed |
Munabi, A. K., Cassorla, F. G., Pfeiffer, D. G., Albertson, B. D., and Loriaux, D. L. (1983). The effects of estradiol and progesterone on rat ovarian 17-hydroxylase and 3β-hydroxysteroid dehydrogenase activities. Steroids 41, 95–98.
| The effects of estradiol and progesterone on rat ovarian 17-hydroxylase and 3β-hydroxysteroid dehydrogenase activities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhsl2hug%3D%3D&md5=32c8a1c7bc6fd3509f48e91a133bf314CAS | 6606868PubMed |
Nelis, H. M., Goossens, K., Leemans, B., Peelman, L., and Van Soom, A. (2013). Steroid-regulated mRNA expression in oviduct epithelial cells in the mare. Reprod. Fertil. Dev. 25, 258.
| Steroid-regulated mRNA expression in oviduct epithelial cells in the mare.Crossref | GoogleScholarGoogle Scholar |
Nguyen, D. H., Zhou, T., Shu, J., and Mao, J.-H. (2013). Quantifying chromogen intensity in immunohistochemistry via reciprocal intensity. Cancer InCytes 2, .
| Quantifying chromogen intensity in immunohistochemistry via reciprocal intensity.Crossref | GoogleScholarGoogle Scholar |
Olson, S. H., Bandera, E. V., and Orlow, I. (2007). Variants in estrogen biosynthesis genes, sex steroid hormone levels, and endometrial cancer: a HuGE review. Am. J. Epidemiol. 165, 235–245.
| Variants in estrogen biosynthesis genes, sex steroid hormone levels, and endometrial cancer: a HuGE review.Crossref | GoogleScholarGoogle Scholar | 17110639PubMed |
Pattison, M. L., Chen, C. L., Kelley, S. T., and Brandt, G. W. (1974). Luteinizing-hormone and estradiol in peripheral-blood of mares during estrous-cycle. Biol. Reprod. 11, 245–250.
| Luteinizing-hormone and estradiol in peripheral-blood of mares during estrous-cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXlsFaiug%3D%3D&md5=815df01e88ee1e7a45ca3e0882d73e61CAS | 4477029PubMed |
Pope, W. F., Maurer, R. R., and Stormshak, F. (1982). Distribution of progesterone in the uterus, broad ligament, and uterine arteries of beef cows. Anat. Rec. 203, 245–249.
| Distribution of progesterone in the uterus, broad ligament, and uterine arteries of beef cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XksFSjs7w%3D&md5=c53014dba0039c2e01ea962dcb003b06CAS | 7114497PubMed |
Reischl, J., Prelle, K., Schol, H., Neumuller, C., Einspanier, R., Sinowatz, F., and Wolf, E. (1999). Factors affecting proliferation and dedifferentiation of primary bovine oviduct epithelial cells in vitro. Cell Tissue Res. 296, 371–383.
| Factors affecting proliferation and dedifferentiation of primary bovine oviduct epithelial cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitlyiu7c%3D&md5=c710260e8d27b32c5c614a1f3731e774CAS | 10382279PubMed |
Reverchon, M., Cornuau, M., Rame, C., Guerif, F., Royere, D., and Dupont, J. (2012). Chemerin inhibits IGF-1-induced progesterone and estradiol secretion in human granulosa cells. Hum. Reprod. 27, 1790–1800.
| Chemerin inhibits IGF-1-induced progesterone and estradiol secretion in human granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnvVOlsLY%3D&md5=e9d21e04c237fb73b4b33d738a7c2234CAS | 22447628PubMed |
Richardson, L. L., and Oliphant, G. (1981). Steroid concentrations in rabbit oviducal fluid during estrus and pseudopregnancy. J. Reprod. Fertil. 62, 427–431.
| Steroid concentrations in rabbit oviducal fluid during estrus and pseudopregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXksF2hsrg%3D&md5=7f8fe5a29b289dab09ff2015765efbb4CAS | 7195938PubMed |
Rottmayer, R., Ulbrich, S. E., Kolle, S., Prelle, K., Neumueller, C., Sinowatz, F., Meyer, H. H. D., Wolf, E., and Hiendleder, S. (2006). A bovine oviduct epithelial cell suspension culture system suitable for studying embryo–maternal interactions: morphological and functional characterization. Reproduction 132, 637–648.
| A bovine oviduct epithelial cell suspension culture system suitable for studying embryo–maternal interactions: morphological and functional characterization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1ahs7rJ&md5=9f7be6d73e8d0da6eff37d5bc90d9dedCAS | 17008475PubMed |
Ruckebusch, Y., and Bayard, F. (1975). Motility of oviduct and uterus of cow during estrous-cycle. J. Reprod. Fertil. 43, 23–32.
| Motility of oviduct and uterus of cow during estrous-cycle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2M7ltlekuw%3D%3D&md5=20559c516ecd6c16027cd935a1973323CAS | 1168710PubMed |
Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKntb7P&md5=b185f20c8797a84cfbb62751d93dfd7cCAS | 22930834PubMed |
Schuetz, A. W., and Dubin, N. H. (1981). Progesterone and prostaglandin secretion by ovulated rat cumulus cell–oocyte complexes. Endocrinology 108, 457–463.
| Progesterone and prostaglandin secretion by ovulated rat cumulus cell–oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhtVSnsbc%3D&md5=382e247d5bb7ed8bb29bed8ecb4543c5CAS | 7449734PubMed |
Seytanoglu, A., Georgiou, A. S., Sostaric, E., Watson, P. F., Holt, W. V., and Fazeli, A. (2008). Oviductal cell proteome alterations during the reproductive cycle in pigs. J. Proteome Res. 7, 2825–2833.
| Oviductal cell proteome alterations during the reproductive cycle in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvFCit7s%3D&md5=e7f065cd453905fae0bd3123fff42765CAS | 18540664PubMed |
Shao, R., Ljungström, K., Weijdegård, B., Egecioglu, E., Fernandez-Rodriguez, J., Zhang, F. P., Thurin-Kjellberg, A., Bergh, C., and Billig, H. (2007). Estrogen-induced upregulation of AR expression and enhancement of AR nuclear translocation in mouse fallopian tubes in vivo. Am. J. Physiol. Endocrinol. Metab. 292, E604–E614.
| Estrogen-induced upregulation of AR expression and enhancement of AR nuclear translocation in mouse fallopian tubes in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjt1Glsb8%3D&md5=b65de0b6ca7d43196e4f87f6e27dcc3cCAS | 17047162PubMed |
Silva, E. S., Scoggin, K. E., Canisso, I. F., Troedsson, M. H. T., Squires, E. L., and Ball, B. A. (2014). Expression of receptors for ovarian steroids and prostaglandin E2 in the endometrium and myometrium of mares during estrus, diestrus and early pregnancy. Anim. Reprod. Sci. 151, 169–181.
| Expression of receptors for ovarian steroids and prostaglandin E2 in the endometrium and myometrium of mares during estrus, diestrus and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFeisrnL&md5=de2c486be62bc8df34ccf1ea387c7b91CAS | 25465360PubMed |
Simard, J., Ricketts, M. L., Gingras, B., Soucy, P., Feltus, F. A., and Melner, M. H. (2005). Molecular biology of the 3 beta-hydroxysteroid dehydrogenase/Delta(5)-Delta(4) isomerase gene family. Endocr. Rev. 26, 525–582.
| Molecular biology of the 3 beta-hydroxysteroid dehydrogenase/Delta(5)-Delta(4) isomerase gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFejt7c%3D&md5=5750f3f01114498780b975ef71481c1eCAS | 15632317PubMed |
Smith, O. F., Ogunsola, A. A., Ladokun, A. O., and Ajadi, R. (2011). Synergistic effects of insulin-like growth factor II (IGF-II) and leutinizing hormone (LH) on steroid hormone secretion by cultured bovine granulosa cells. Indian J. Anim. Sci. 81, 1116–1120.
| 1:CAS:528:DC%2BC3MXhs1ynsLbE&md5=dd73b1f819011bcd22fc22c8ee4811b6CAS |
Spilman, C. H., and Wilks, J. W. (1976). Peripheral plasma progesterone during egg transport in rabbit. Proc. Soc. Exp. Biol. Med. 151, 726–729.
| Peripheral plasma progesterone during egg transport in rabbit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XhslOlsL0%3D&md5=963fe25a16bae62d231a8a5661e8d4e0CAS | 1265057PubMed |
Squires, E. L., and Ginther, O. J. (1975). Collection technique and progesterone concentration of ovarian and uterine venous-blood in mares. J. Anim. Sci. 40, 275–281.
| 1:CAS:528:DyaE2MXhsFaqtbg%3D&md5=30d6d0e3d55054907c7acb769c2fe75dCAS | 1116964PubMed |
Staples, L. D., Fleet, I. R., and Heap, R. B. (1982). Anatomy of the utero-ovarian lymphatic network and the composition of afferent lymph in relation to the establishment of pregnancy in the sheep and goat. J. Reprod. Fertil. 64, 409–420.
| Anatomy of the utero-ovarian lymphatic network and the composition of afferent lymph in relation to the establishment of pregnancy in the sheep and goat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xhs1Sjtbs%3D&md5=c764e46a82bd7d1d9739e9c258938ce7CAS | 7069659PubMed |
Stefañczyk-Krzymowska, S., Krzymowski, T., Wasowska, B., and Chlopek, J. (2002). Retrograde transfer of ovarian steroid hormones to the ovary in the porcine periovarian vascular complex. Exp. Physiol. 87, 361–371.
| Retrograde transfer of ovarian steroid hormones to the ovary in the porcine periovarian vascular complex.Crossref | GoogleScholarGoogle Scholar | 12089604PubMed |
Stoklosowa, S., Gregoraszczuk, E., and Channing, C. P. (1982). Estrogen and progesterone secretion by isolated cultured porcine thecal and granulosa-cells. Biol. Reprod. 26, 943–952.
| Estrogen and progesterone secretion by isolated cultured porcine thecal and granulosa-cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktFOmtLY%3D&md5=2e5ad24a72ca9e2255b2ffaf77e661e8CAS | 7093409PubMed |
Suarez, S. S. (2008). Regulation of sperm storage and movement in the mammalian oviduct. Int. J. Dev. Biol. 52, 455–462.
| Regulation of sperm storage and movement in the mammalian oviduct.Crossref | GoogleScholarGoogle Scholar | 18649258PubMed |
Suarez, S. S., and Ho, H. C. (2003). Hyperactivated motility in sperm. Reprod. Domest. Anim. 38, 119–124.
| Hyperactivated motility in sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s7nvFyitQ%3D%3D&md5=de82a01f2563ea9112cde71f8d39bebfCAS | 12654022PubMed |
Szafranska, B., Ziecik, A., and Okrasa, S. (2002). Primary antisera against selected steroids or proteins and secondary antisera against gamma-globulins—an available tool for studies of reproductive processes. Reprod. Biol. 2, 187–204.
| 14666157PubMed |
Takeda, T., Tsutsumi, Y., Hara, S., and Ida, M. (1978). Effects of prostaglandin-F2-alpha on egg transport and in vivo egg recovery from vaginas of rabbits. Fertil. Steril. 30, 79–85.
| 1:CAS:528:DyaE1cXmtV2lsr4%3D&md5=35ebb2d8b7951714ab3ff2841d846004CAS | 680187PubMed |
Tetsuka, M., Milne, M., and Hillier, S. G. (1998). Expression of oestrogen receptor isoforms in relation to enzymes of oestrogen synthesis in rat ovary. Mol. Cell. Endocrinol. 141, 29–35.
| Expression of oestrogen receptor isoforms in relation to enzymes of oestrogen synthesis in rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltlKrsro%3D&md5=d1fe8494a27e69817ef251a8eff4fa51CAS | 9723882PubMed |
Teves, M. E., Barbano, F., Guidobaldi, H. A., Sanchez, R., Miska, W., and Giojalas, L. C. (2006). Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa. Fertil. Steril. 86, 745–749.
| Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCqsLzJ&md5=6b730087ee068e8fe6a4a22527182944CAS | 16784744PubMed |
Ulbrich, S. E., Kettler, A., and Einspanier, R. (2003). Expression and localization of estrogen receptor α, estrogen receptor β and progesterone receptor in the bovine oviduct in vivo and in vitro. J. Steroid Biochem. Mol. Biol. 84, 279–289.
| Expression and localization of estrogen receptor α, estrogen receptor β and progesterone receptor in the bovine oviduct in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFWgs7o%3D&md5=1d5588f04c04e6f5e9837069e51fd9acCAS | 12711014PubMed |
Van den Broeck, W., D’haeseleer, M., Coryn, M., and Simoens, P. (2002). Cell-specific distribution of progesterone receptors in the bovine ovary. Reprod. Domest. Anim. 37, 164–170.
| Cell-specific distribution of progesterone receptors in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlslygtrY%3D&md5=f9c428b1a1c9bbbe5c774d810acdea1bCAS | 12071891PubMed |
Vanhaecke, L., Bussche, J. V., Wille, K., Bekaert, K., and De Brabander, H. F. (2011). Ultra-high performance liquid chromatography–tandem mass spectrometry in high-throughput confirmation and quantification of 34 anabolic steroids in bovine muscle. Anal. Chim. Acta 700, 70–77.
| Ultra-high performance liquid chromatography–tandem mass spectrometry in high-throughput confirmation and quantification of 34 anabolic steroids in bovine muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXoslWqsLw%3D&md5=7cce0f0c4964a730e0ed380f2a090720CAS | 21742119PubMed |
Watson, E. D., Skolnik, S. B., and Zanecosky, H. G. (1992). Progesterone and estrogen-receptor distribution in the endometrium of the mare. Theriogenology 38, 575–580.
| Progesterone and estrogen-receptor distribution in the endometrium of the mare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs1Cqsw%3D%3D&md5=230af8682dccd47d164b21be93b6926aCAS | 16727160PubMed |
Watson, E. D., Thomassen, R., Steele, M., Heald, M., Leask, R., Groome, N. P., and Riley, S. C. (2002). Concentrations of inhibin, progesterone and oestradiol in fluid from dominant and subordinate follicles from mares during spring transition and the breeding season. Anim. Reprod. Sci. 74, 55–67.
| Concentrations of inhibin, progesterone and oestradiol in fluid from dominant and subordinate follicles from mares during spring transition and the breeding season.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVKisrw%3D&md5=0ae12dc53e93e97417bc04c46a29f14aCAS | 12379375PubMed |
Weems, C. W., Weems, Y. S., Lee, C. N., and Vincent, D. L. (1989). Progesterone in uterine and arterial tissue and in jugular and uterine venous plasma of sheep. Biol. Reprod. 41, 1–6.
| Progesterone in uterine and arterial tissue and in jugular and uterine venous plasma of sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXls1OlsLg%3D&md5=7c6426fef4511e3c100e843af03c949cCAS | 2804199PubMed |
Wijayagunawardane, M. P. B., Cerbito, W. A., Miyamoto, A., Acosta, T. J., Takagi, M., Miyazawa, K., and Sato, K. (1996). Oviductal progesterone concentration and its spatial distribution in cyclic and early pregnant cows. Theriogenology 46, 1149–1158.
| Oviductal progesterone concentration and its spatial distribution in cyclic and early pregnant cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmslKlt7Y%3D&md5=67b3170120c06f44a81f9e555f3bfb1cCAS |
Wijayagunawardane, M. P. B., Choi, Y. H., Miyamoto, A., Kamishita, H., Fujimoto, S., Takagi, M., and Sato, K. (1999). Effect of ovarian steroids and oxytocin on the production of prostaglandin E-2, prostaglandin F-2 alpha and endothelin-1 from cow oviductal epithelial cell monolayers in vitro. Anim. Reprod. Sci. 56, 11–17.
| Effect of ovarian steroids and oxytocin on the production of prostaglandin E-2, prostaglandin F-2 alpha and endothelin-1 from cow oviductal epithelial cell monolayers in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVSlsbg%3D&md5=69adf46952a5eae0c461cf465fda2e32CAS |
Wildt, L., Kissler, S., Licht, P., and Becker, W. (1998). Sperm transport in the human female genital tract and its modulation by oxytocin as assessed by hysterosalpingoscintigraphy, hysterotonography, electrohysterography and Doppler sonography. Hum. Reprod. Update 4, 655–666.
| Sperm transport in the human female genital tract and its modulation by oxytocin as assessed by hysterosalpingoscintigraphy, hysterotonography, electrohysterography and Doppler sonography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvVShtro%3D&md5=12b0a909488527bdade5adaeb55f5e5dCAS | 10027619PubMed |
Wilsher, S., Gower, S., and Allen, W. R. (2011). Immunohistochemical localisation of progesterone and oestrogen receptors at the placental interface in mares during early pregnancy. Anim. Reprod. Sci. 129, 200–208.
| Immunohistochemical localisation of progesterone and oestrogen receptors at the placental interface in mares during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1OmsLY%3D&md5=2fe76a05ea02c4f845689a25abe5143dCAS | 22176887PubMed |
Yaniz, J. L., Lopez-Bejar, M., Santolaria, P., Rutllant, J., and Lopez-Gatius, F. (2002). Intraperitoneal insemination in mammals: a review. Reprod. Domest. Anim. 37, 75–80.
| Intraperitoneal insemination in mammals: a review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383mvFGgsA%3D%3D&md5=7f73cfc8c52961a95d9a655703f490a9CAS | 11975743PubMed |
