Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effects of testosterone and prolactin on steroidogenesis in post-ovulatory cumuli oophori and on in vitro oocyte fertilisation in the rat

Agnieszka Starowicz A C , Jerzy Galas A , Małgorzata Duda A , Zbigniew Tabarowski B and Maria Szołtys A
+ Author Affiliations
- Author Affiliations

A Department of Endocrinology, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland.

B Department of Experimental Haematology, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland.

C Corresponding author. Email: aga.starowicz@uj.edu.pl

Reproduction, Fertility and Development 29(2) 406-418 https://doi.org/10.1071/RD15050
Submitted: 6 February 2015  Accepted: 21 July 2015   Published: 9 September 2015

Abstract

The main objective of these studies was to determine the in vitro effects of prolactin (PRL) and testosterone (T) on steroidogenic function in post-ovulatory cumuli oophori containing unfertilised (ufCOCs) or fertilised (fCOCs) oocytes and to determine the differences between ufCOCs and fCOCs. In vivo, progesterone (P4) content was distinctly higher in isolated ampullae containing ufCOCs than in those containing fCOCs. Moreover, the expression of androgen (ARs) and prolactin (PRL-Rs) receptors was distinctly higher in ufCOCs than in fCOCs. Also, in vitro P4 profiles were generally higher in incubated ufCOCs, which had very high secretion rates of this steroid, especially after treatment with PRL+T. Testosterone significantly increased P4 levels only in incubated fCOCs, while the anti-androgen dihydroxyflutamide (2-Hf) markedly decreased P4 levels in both ufCOCs and fCOCs. Among post-incubation ufCOCs fertilised in vitro, the highest fertilisation rate was observed for oocytes in ufCOCs exposed to PRL+T, while those incubated with 2-Hf or T+2-Hf were not fertilisable. These studies establish differences in steroidogenic function and expression of ARs and PRL-Rs between post-ovulatory ufCOCs and fCOCs, with higher concentrations of P4 being observed in the microenvironment of ufCOCs. PRL+T stimulated P4 production by ufCOCs and increased in vitro fertilisation rate.

Additional keywords: androgen receptor, androgens, dihydroxyflutamide, oestradiol, PRL-RL and PRL-RS isoforms.


References

Amor, H., Ajina, M., Saad, A., and Ben Ali, H. (2014). Study of gonadic growth factors: seminal transforming growth factor-β1, epidermal growth factor and insulin-like growth factor-I and their relationship with male infertility. ARSci. 2, 16–23.
Study of gonadic growth factors: seminal transforming growth factor-β1, epidermal growth factor and insulin-like growth factor-I and their relationship with male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaltb7N&md5=7116b53b671bb3c4d991a61c3ffde2c0CAS |

Amsterdam, A., and Rotmensch, S. (1987). Structure–function relationships during granulosa cell differentiation. Endocr. Rev. 8, 309–337.
Structure–function relationships during granulosa cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlslaqu74%3D&md5=d39866c8eba7b7ee41c212722aeffd1aCAS | 2820706PubMed |

Anderiesz, C., and Trounson, A. O. (1995). The effect of testosterone on the maturation and developmental capacity of murine oocytes in vitro. Hum. Reprod. 10, 2377–2381.
The effect of testosterone on the maturation and developmental capacity of murine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XivVeg&md5=8ded97ec68b7634cf11dd60390dc15cbCAS | 8530669PubMed |

Armstrong, D. T., and Dorrington, J. H. (1976). Androgens augment FSH-induced progesterone secretion by cultured rat granulosa cells. Endocrinology 99, 1411–1414.
Androgens augment FSH-induced progesterone secretion by cultured rat granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXis1agtQ%3D%3D&md5=499b8a4a2fba4afdb061364bc8791145CAS | 1033061PubMed |

Arowojolu, A. O., Akinloye, O., and Shittu, O. B. (2004). Serum and seminal plasma prolactin levels in male attenders of an infertility clinic in Ibadan. J. Obstet. Gynaecol. 24, 306–309.
Serum and seminal plasma prolactin levels in male attenders of an infertility clinic in Ibadan.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2czgvF2jug%3D%3D&md5=d7c2322a994ea2dcad3ac01d18610f54CAS | 15203635PubMed |

Ayub, M., and Levell, M. J. (1987). Inhibition of rat testicular 17 alpha-hydroxylase and 17,20-lyase activities by anti-androgens (flutamide, hydroxyflutamide, RU23908, cyproterone acetate) in vitro. J. Steroid Biochem. 28, 43–47.
Inhibition of rat testicular 17 alpha-hydroxylase and 17,20-lyase activities by anti-androgens (flutamide, hydroxyflutamide, RU23908, cyproterone acetate) in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXltV2ltro%3D&md5=a932b7d17a9918f6c3127ed5b2d68998CAS | 2956461PubMed |

Bagnell, C. A., Mills, T. M., Costoff, A., and Mahesh, V. B. (1982). A model for the study of androgen effects on follicular atresia and ovulation. Biol. Reprod. 27, 903–914.
A model for the study of androgen effects on follicular atresia and ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXntVw%3D&md5=f08d9149d1f590c169013d09d53e0953CAS | 7171673PubMed |

Bar-Ami, S., Regev, A., and Gitay-Goren, H. (1997). Effect of androgen substrates on the steroid pattern of cumulus cells: correlation with cumulus culture morphology. J. Assist. Reprod. Genet. 14, 270–276.
Effect of androgen substrates on the steroid pattern of cumulus cells: correlation with cumulus culture morphology.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3pt1Ohuw%3D%3D&md5=69c36e5ed9ee6f10ad583246b6a87d3aCAS | 9147240PubMed |

Billig, H., Furuta, I., and Hsueh, A. J. (1993). Oestrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology 133, 2204–2212.
| 1:CAS:528:DyaK2cXosVY%3D&md5=405f0b468514077b7dbfdde7a2a75fd0CAS | 8404672PubMed |

Cameron, N., Ha, G. K., and Erskine, M. S. (2003). Effect of adrenalectomy on mating-induced prolactin surges and pseudopregnancy in the female rat. Neuroendocrinology 78, 138–146.
Effect of adrenalectomy on mating-induced prolactin surges and pseudopregnancy in the female rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsFeks7c%3D&md5=fb4e887dc63f28854c32d74c92586af6CAS | 14512706PubMed |

Clarke, D. L., Areyp, B. J., and Linzers, D. I. H. (1993). Prolactin receptor messenger ribonucleic acid expression in the ovary during the rat oestrous cycle. Endocrinology 133, 2594–2603.
| 1:CAS:528:DyaK2cXks1aktQ%3D%3D&md5=9cb7b8edd5f4aee39639445dbed4de13CAS | 8243282PubMed |

Conway, B. A., Mahesh, V. B., and Mills, T. M. (1990). Effect of dihydrotestosterone on the growth and function of ovarian follicles in intact immature female rats primed with PMSG. J. Reprod. Fertil. 90, 267–277.
Effect of dihydrotestosterone on the growth and function of ovarian follicles in intact immature female rats primed with PMSG.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXjs1WmtQ%3D%3D&md5=461fc94415a08da0b3320e004c9db044CAS | 2121972PubMed |

Devi, Y. S., and Halperin, J. (2014). Reproductive actions of prolactin mediated through short and long receptor isoforms. Mol. Cell. Endocrinol. 382, 400–410.
Reproductive actions of prolactin mediated through short and long receptor isoforms.Crossref | GoogleScholarGoogle Scholar | 24060636PubMed |

Duda, M., Durlej, M., Knet, M., Knapczyk-Stwora, K., Tabarowski, Z., and Slomczynska, M. (2012). Does 2-hydroxyflutamide inhibit apoptosis in porcine granulosa cells? – an in vitro study. J. Reprod. Dev. 58, 438–444.
Does 2-hydroxyflutamide inhibit apoptosis in porcine granulosa cells? – an in vitro study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVOhur%2FL&md5=fce83e1bc23df96160a3497162a49228CAS | 22522230PubMed |

Duda, M., Grzesiak, M., Knet, M., Knapczyk-Stwora, K., Tabarowski, Z., Michna, A., and Slomczynska, M. (2014). The impact of anti-androgen 2-hydroxyflutamide on the expression of steroidogenic enzymes in cultured porcine ovarian follicles. Mol. Biol. Rep. 41, 4213–4222.
The impact of anti-androgen 2-hydroxyflutamide on the expression of steroidogenic enzymes in cultured porcine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsVChsbk%3D&md5=e22cd0cfccf160e2b653a35794d5607cCAS | 24584661PubMed |

Dunaif, A. E., Zimmerman, E. A., Friesen, H. G., and Frantz, A. G. (1982). Intracellular localisation of prolactin receptor and prolactin in the rat ovary by immunocytochemistry. Endocrinology 110, 1465–1471.
Intracellular localisation of prolactin receptor and prolactin in the rat ovary by immunocytochemistry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XitFWisL4%3D&md5=312b14f6344c5e8cfd9d289d801b9d05CAS | 6280962PubMed |

Dunning, K. R., Watson, L. N., Sharkey, D. J., Brown, H. M., Norman, R. J., Thompson, J. G., Robker, R. L., and Russell, D. L. (2012). Molecular filtration properties of the mouse expanded cumulus matrix: controlled supply of metabolites and extracellular signals to cumulus cells and the oocyte. Biol. Reprod. 87, 89.
Molecular filtration properties of the mouse expanded cumulus matrix: controlled supply of metabolites and extracellular signals to cumulus cells and the oocyte.Crossref | GoogleScholarGoogle Scholar | 22837478PubMed |

Ecay, T. W., and Powers, R. D. (1990). Differential effects of testosterone and dibutyryl cyclic AMP on the meiotic maturation of mouse oocytes in vitro. J. Exp. Zool. 253, 88–98.
Differential effects of testosterone and dibutyryl cyclic AMP on the meiotic maturation of mouse oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhtFagsL0%3D&md5=ca082cea9962c8a5f6e6824548919145CAS | 2155990PubMed |

Egli, M., Leeners, B., and Kruger, T. H. C. (2010). Prolactin secretion patterns: basic mechanisms and clinical implications for reproduction. Reproduction 140, 643–654.
Prolactin secretion patterns: basic mechanisms and clinical implications for reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCnsbfO&md5=7b3d61f3a6dd0e820d51459e8bf95388CAS | 20733016PubMed |

Eppig, J. J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–838.
Oocyte control of ovarian follicular development and function in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVWjsw%3D%3D&md5=ffd18350627634c0ed9a22155739f770CAS | 11732978PubMed |

Erickson, G. F., and Shimasaki, S. (2000). The role of the oocyte in the folliculogenesis. Trends Endocrinol. Metab. 11, 193–198.
The role of the oocyte in the folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFChtbk%3D&md5=8c9bcd09b6387c61d3b424372c490b63CAS | 10856922PubMed |

Fortune, J. E., and Vincent, S. E. (1986). Prolactin modulates steroidogenesis by rat granulosa cells: I. Effects on progesterone. Biol. Reprod. 35, 84–91.
Prolactin modulates steroidogenesis by rat granulosa cells: I. Effects on progesterone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xlt1Oru70%3D&md5=54c94013dd4f4f12fb12a7a0f6fbfdadCAS | 3091106PubMed |

Fortune, J. E., Wissler, R. N., and Vincent, S. E. (1986). Prolactin modulates steroidogenesis by rat granulosa cells: II. Effects on oestradiol. Biol. Reprod. 35, 92–99.
Prolactin modulates steroidogenesis by rat granulosa cells: II. Effects on oestradiol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xlt1Oru7o%3D&md5=b3da218610aef5f2ceed42b85f9bd102CAS | 3091107PubMed |

Fuentealba, B., Nieto, M., and Croxatto, H. B. (1988). Progesterone abbreviates the nuclear retention of oestrogen receptor in the rat oviduct and counteracts oestrogen action on egg transport. Biol. Reprod. 38, 63–69.
Progesterone abbreviates the nuclear retention of oestrogen receptor in the rat oviduct and counteracts oestrogen action on egg transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXht1Cksbg%3D&md5=18c28203ed6f5834c79c319784257078CAS | 3365472PubMed |

Galas, J., Słomczyńska, M., Knapczyk-Stwora, K., Durlej, M., Starowicz, A., Tabarowski, Z., Rutka, K., and Szołtys, M. (2012). Steroid levels and the spatiotemporal expression of steroidogenic enzymes and androgen receptor in developing ovaries of immature rats. Acta Histochem. 114, 207–216.
Steroid levels and the spatiotemporal expression of steroidogenic enzymes and androgen receptor in developing ovaries of immature rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVWit70%3D&md5=9646ab696208c6868c9e73e6085a127eCAS | 21620445PubMed |

Gaytán, F., Bellido, C., Morales, C., and Sánchez-Criado, J. E. (2001). Cyclic changes in the responsiveness of regressing corpora lutea to the luteolytic effects of prolactin in rats. Reproduction 122, 411–417.
Cyclic changes in the responsiveness of regressing corpora lutea to the luteolytic effects of prolactin in rats.Crossref | GoogleScholarGoogle Scholar | 11603369PubMed |

Gilchrist, R. B., Ritter, L. J., and Armstrong, D. T. (2004). Oocyte–somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82–83, 431–446.
Oocyte–somatic cell interactions during follicle development in mammals.Crossref | GoogleScholarGoogle Scholar | 15271471PubMed |

Goldschmit, D., Kraicer, P., and Orly, J. (1989). Peri-ovulatory expression of cholesterol side-chain cleavage cytochrome P450 in cumulus cells. Endocrinology 124, 369–378.
Peri-ovulatory expression of cholesterol side-chain cleavage cytochrome P450 in cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXmvFKksA%3D%3D&md5=fdb36901bb90185daa312c5535f6dd6eCAS | 2535811PubMed |

Grosdemouge, I., Bachelot, A., Lucas, A., Baran, N., Kelly, P. A., and Binart, N. (2003). Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod. Biol. Endocrinol. 1, 12.
Effects of deletion of the prolactin receptor on ovarian gene expression.Crossref | GoogleScholarGoogle Scholar | 12646063PubMed |

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 |

Hampl, R., Kubátová, J., Sobotka, V., and Heráček, J. (2013). Steroids in semen, their role in spermatogenesis and the possible impact of endocrine disruptors. Horm. Mol. Biol. Clin. Investig. 13, 1–5.
Steroids in semen, their role in spermatogenesis and the possible impact of endocrine disruptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsVekurY%3D&md5=2b80722f649092fcbabed303ad34cec5CAS | 25436708PubMed |

Harlow, Ch. R., Bradshaw, A. C., Rae, M. T., Shearer, K. D., and Hillier, S. G. (2007). Oestrogen formation and connective tissue growth factor expression in rat granulosa cells. J. Endocrinol. 192, 41–52.
Oestrogen formation and connective tissue growth factor expression in rat granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktlKqtLs%3D&md5=aebfc3829c12651998448d87e2252171CAS |

Hillier, S. G., Knazek, R. A., and Ross, G. T. (1977). Androgenic stimulation of progesterone production by granulosa cells from pre-antral ovarian follicles: further in vitro studies using replicate cell cultures. Endocrinology 100, 1539–1549.
Androgenic stimulation of progesterone production by granulosa cells from pre-antral ovarian follicles: further in vitro studies using replicate cell cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXkslyksbk%3D&md5=6ed250c511465af6e838aa7f27784b92CAS | 870305PubMed |

Hu, Y. C., Wang, P. H., Yeh, S., Wang, S., Xie, C., Xu, Q., Zhou, X., Chao, H. T., Tsai, M. Y., and Chang, C. (2004). Subfertility and defective folliculogenesis in female mice lacking androgen receptor. Proc. Natl. Acad. Sci. USA 101, 11209–11214.
Subfertility and defective folliculogenesis in female mice lacking androgen receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvVKgtro%3D&md5=9da4c8e63e8500a69dd543b0d394a9b6CAS | 15277682PubMed |

Kiapekou, E., Loutradis, D., Mastorakos, D., Bletsa, R., Beretsos, P., Zapanti, E., Drakakis, P., Antsteidis, A., and Kiessling, A. A. (2009). Effect of PRL on in vitro follicle growth, in vitro oocyte maturation, fertilisation and early embryonic development in mice. Cloning Stem Cells 11, 293–300.
Effect of PRL on in vitro follicle growth, in vitro oocyte maturation, fertilisation and early embryonic development in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnt1CisrY%3D&md5=b8e7b03ad0cce66433bcea343dc63bb7CAS | 19522676PubMed |

Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFags7s%3D&md5=8e6d2f0feb3d7e17e4113a8ccd82296cCAS | 5432063PubMed |

Malven, P. V. (1969). Luteotrophic and luteolytic responses to prolactin in hypophysectomised rats. Endocrinology 84, 1224–1229.
Luteotrophic and luteolytic responses to prolactin in hypophysectomised rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXktF2hs7k%3D&md5=e094eff4791be7bc2f140144ae528390CAS | 5777417PubMed |

Miyoshi, K., Kono, T., and Niwa, K. (1997). Stage-dependent development of rat one-cell embryos in a chemically defined medium after fertilisation in vivo and in vitro. Biol. Reprod. 56, 180–185.
Stage-dependent development of rat one-cell embryos in a chemically defined medium after fertilisation in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXis1Kkuw%3D%3D&md5=ee63128851e439513eb61ee4ee660984CAS | 9002647PubMed |

Nakamura, E., Otsuka, F., Inagaki, K., Miyoshi, T., Yamanaka, R., Tsukamoto, N., Suzuki, J., Ogura, T., and Makino, H. (2010). A novel antagonistic effect of the bone morphogenetic protein system on prolactin actions in regulating steroidogenesis by granulosa cells. Endocrinology 151, 5506–5518.
A novel antagonistic effect of the bone morphogenetic protein system on prolactin actions in regulating steroidogenesis by granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVKks7fI&md5=7559dc61ab7cdfcc0e67ccde56f8f0ccCAS | 20810564PubMed |

Oh, S. H., Miyoshi, K., and Funahashi, H. (1998). Rat oocytes fertilised in modified rat one-cell embryo culture medium containing a high sodium chloride concentration and bovine serum albumin maintain developmental ability to the blastocyst stage. Biol. Reprod. 59, 884–889.
Rat oocytes fertilised in modified rat one-cell embryo culture medium containing a high sodium chloride concentration and bovine serum albumin maintain developmental ability to the blastocyst stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVGrsbY%3D&md5=824812e7fa19fc56e83c96c396a22a28CAS | 9746739PubMed |

Ormandy, Ch. J., Camus, A., Barra, J., Damotte, D., Lucas, B., Buteau, H., Edery, M., Brousse, N., Babinet, Ch., Binart, N., and Kelly, P. A. (1997). Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev. 11, 167–178.
Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXpsVKmsg%3D%3D&md5=277cf779054e9856c9e4e0ccc01cf1bdCAS |

Prizant, H., Gleicher, N., and Sen, A. (2014). Androgen actions in the ovary: balance is key. J. Endocrinol. 222, R141–R151.
Androgen actions in the ovary: balance is key.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1CgurjN&md5=293b38ce8178bf0db5b91a43b15c6c61CAS | 25037707PubMed |

Randall, G. W., Awadalla, S. G., and Shivers, C. A. (1990). Isolation, in vitro maturation and fertilisation of germinal vesicle oocytes obtained from the intact murine ovary. J. In Vitro Fert. Embryo Transf. 7, 314–320.
Isolation, in vitro maturation and fertilisation of germinal vesicle oocytes obtained from the intact murine ovary.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7ntVymuw%3D%3D&md5=7570a9b4014254069fb61255f5d5cbb9CAS | 2127601PubMed |

Regucka, J., Szołtys, M., Wójtowicz, A., and Walocha, A. (2000). Effects of testosterone, FSH and LH on oestradiol and progesterone secretion by pre-ovulatory cumulus oophorus complexes of the rat. Exp. Clin. Endocrinol. Diabetes 108, 44–48.
| 1:CAS:528:DC%2BD3cXitFejt7g%3D&md5=cfad7d548edfe755f592b79628a5741dCAS | 10768831PubMed |

Russell, D. L., and Richards, J. S. (1999). Differentiation-dependent prolactin responsiveness and StAT (signal transducers and activators of transcription) signalling in rat ovarian cells. Mol. Endocrinol. 13, 2049–2064.
Differentiation-dependent prolactin responsiveness and StAT (signal transducers and activators of transcription) signalling in rat ovarian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnvVantrg%3D&md5=b8012e59a2a16a88e0b4c61ec0e8faa8CAS | 10598581PubMed |

Salustri, A., Fulop, C., Camaion, A., and Hascall, V. C. (2004). Oocyte–granulosa cell interaction. In ‘The Ovary’. (Eds P. C. K. Leung and E. Y. Adashi.) pp. 131-43. (Elsevier Academic Press: Boston.)

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 |

Sherizly, I., and Kraicer, P. F. (1980). Progesterone secretion by the post-ovulatory rat cumulus oophorus. Gamete Res. 3, 115–119.
Progesterone secretion by the post-ovulatory rat cumulus oophorus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXlt12ns7k%3D&md5=b01c7ced12f6c5ebe6d584df3788e19cCAS |

Sidhu, K. S., and Gill, H. K. (1992). Immunoreactive prolactin, progesterone and luteinising hormone in the seminal plasma of buffalo (Bubalus bubalis). Acta Vet. Hung. 40, 27–32.
| 1:CAS:528:DyaK3sXhsVShsr4%3D&md5=fcdfb7c95a8ed534db44f77fb0d23fa8CAS | 1476086PubMed |

Silva, C. C., and Knight, P. G. (2000). Effects of androgens, progesterone and their antagonists on the developmental competence of in vitro-matured bovine oocytes. J. Reprod. Fertil. 119, 261–269.
| 1:CAS:528:DC%2BD3cXltlyltrw%3D&md5=fe002aa3b5107f43277b669e4d5193a1CAS | 10864838PubMed |

Smith, D. M., and Tenney, D. Y. (1980). Effects of steroids on mouse oocyte maturation in vitro. J. Reprod. Fertil. 60, 331–338.
Effects of steroids on mouse oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlsVM%3D&md5=c661260854dcbfac346330e205686b02CAS | 7431342PubMed |

Suzuki, O., Koura, O., Noguch, Y., Uchio-Yamada, K., and Matsuda, J. (2013). Reduced superovulation efficiency by high-dose treatment of dehydroepiandrosterone in mice. Reprod. Fertil. Dev. 25, 307–319.
Reduced superovulation efficiency by high-dose treatment of dehydroepiandrosterone in mice.Crossref | GoogleScholarGoogle Scholar |

Szołtys, M., and Słomczyńska, M. (2000). Changes in distribution of androgen receptor during maturation of rat ovarian follicles. Exp. Clin. Endocrinol. Diabetes 108, 228–234.
Changes in distribution of androgen receptor during maturation of rat ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 10926321PubMed |

Szołtys, M., Galas, J., Jabłonka, A., and Tabarowski, Z. (1994). Some morphological and hormonal aspects of ovulation and superovulation. J. Endocrinol. 141, 91–100.
Some morphological and hormonal aspects of ovulation and superovulation.Crossref | GoogleScholarGoogle Scholar | 8014608PubMed |

Szołtys, M., Słomczyńska, M., Galas, J., Duda, M., and Sakiewicz, A. (2007). Expression of androgen receptor and 3β-hydroxysteroid dehydrogenase in corpora lutea during pregnancy in the rat. Reprod. Fertil. Dev. 19, 356–365.
Expression of androgen receptor and 3β-hydroxysteroid dehydrogenase in corpora lutea during pregnancy in the rat.Crossref | GoogleScholarGoogle Scholar | 17257522PubMed |

Szołtys, M., Słomczyńska, M., Knapczyk-Stwora, K., Durlej, M., and Lechowska, A. (2010). Immunolocalisation of androgen receptor and steroidogenic enzymes in cumuli oophori of pre- and post-ovulatory rats. Acta Histochem. 112, 576–582.
Immunolocalisation of androgen receptor and steroidogenic enzymes in cumuli oophori of pre- and post-ovulatory rats.Crossref | GoogleScholarGoogle Scholar | 19775733PubMed |

Telleria, C. M., Parmer, T. G., Zhong, L., Clarke, D. L., Albarracin, C. T., Duan, W. R., Linzer, D. I., and Gibori, G. (1997). The different forms of the prolactin receptor in the rat corpus luteum: developmental expression and hormonal regulation in pregnancy. Endocrinology 138, 4812–4820.
| 1:CAS:528:DyaK2sXmslGqtLw%3D&md5=73bbcc30197a730b4bed1dbc4285b719CAS | 9348210PubMed |

Tetsuka, M., and Hillier, S. G. (1997). Differential regulation of aromatase and androgen receptor in granulosa cells. J. Steroid Biochem. Mol. Biol. 61, 233–239.
Differential regulation of aromatase and androgen receptor in granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnt1Cku78%3D&md5=2d3a7f23dfee439ec0f73a547e9317afCAS | 9365195PubMed |

Tetsuka, M., Whitelaw, P. F., Bremne, W., Milla, M. R., Smyth, C., and Hillier, S. G. (1995). Developmental regulation of androgen receptor in rat ovary. J. Endocrinol. 145, 535–543.
Developmental regulation of androgen receptor in rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtV2gtrw%3D&md5=7d1c88d10e377dfd78e446d8e785510cCAS | 7636438PubMed |

Turner, K. J., Macpherson, S., Millar, S. M., McNeilly, A. S., Williams, K., Cranfield, M., Groome, N. P., Sharpe, R. M., Fraser, H. M., and Saunders, P. T. K. (2002). Development and validation of a new monoclonal antibody to mammalian aromatase. J. Endocrinol. 172, 21–30.
Development and validation of a new monoclonal antibody to mammalian aromatase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsFWlsw%3D%3D&md5=6aaf0b5837275980fb731f227f3d43c1CAS | 11786371PubMed |

Walters, K. A., Allan, C. M., and Handelsman, D. J. (2008). Androgen actions and the ovary. Biol. Reprod. 78, 380–389.
Androgen actions and the ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFSltb8%3D&md5=3c2c7c908100e9cf06b1fc28c73cbc8dCAS | 18003945PubMed |

Wang, C., and Chan, V. (1982). Divergent effects of prolactin on oestrogen and progesterone production by granulosa cells of rat Graafian follicles. Endocrinology 110, 1085–1093.
Divergent effects of prolactin on oestrogen and progesterone production by granulosa cells of rat Graafian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhsFGqu74%3D&md5=4eae7e6ff96085a9b4aac1b668ee4796CAS | 6800769PubMed |

Wånggren, K., Stavreus-Evers, A., Olsson, C., Andersson, E., and Gemzell-Danielsson, K. (2008). Regulation of muscular contractions in the human Fallopian tube through prostaglandins and progestagens. Hum. Reprod. 23, 2359–2368.
Regulation of muscular contractions in the human Fallopian tube through prostaglandins and progestagens.Crossref | GoogleScholarGoogle Scholar | 18621753PubMed |

Witte, T. S., and Schäfer-Somi, S. (2007). Involvement of cholesterol, calcium and progesterone in the induction of capacitation and acrosome reaction of mammalian spermatozoa. Anim. Reprod. Sci. 102, 181–193.
Involvement of cholesterol, calcium and progesterone in the induction of capacitation and acrosome reaction of mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKiurvN&md5=603f4061edb3eaa678f3e7df9fb38facCAS | 17870257PubMed |

Wuttke, W., and Meites, J. (1971). Luteolytic role of prolactin during the oestrous cycle of the rat. Proc. Soc. Exp. Biol. Med. 137, 988–991.
Luteolytic role of prolactin during the oestrous cycle of the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXksF2hsbk%3D&md5=76c584849839650751fc8bbcfe62e2dcCAS | 5105378PubMed |

Yohkaichiya, T., Fukaya, T., Hoshiai, H., and Yajima, A. (1988). Improvement of mouse embryo development in vitro by prolactin. Tohoku J. Exp. Med. 155, 241–246.
Improvement of mouse embryo development in vitro by prolactin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlsVaqsLs%3D&md5=c5ded8b6dd93cade161f90ec78ec41a3CAS | 3176020PubMed |

Yoshida, M., and Yoshida, K. (2011). Sperm chemotaxis and regulation of flagellar movement by Ca2+. Mol. Hum. Reprod. 17, 457–465.
Sperm chemotaxis and regulation of flagellar movement by Ca2+.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFCnsbg%3D&md5=a3df7c9c7a7b685385f351e21b87c180CAS | 21610215PubMed |

Yoshimura, Y., Hosoi, Y., Iritani, A., Nakamura, Y., Atlas, S. J., and Wallach, E. E. (1989). Developmental potential of rabbit oocyte matured in vitro: the possible contribution of prolactin. Biol. Reprod. 41, 26–33.
Developmental potential of rabbit oocyte matured in vitro: the possible contribution of prolactin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXls1Oks7Y%3D&md5=4728685508148af60d87c05c62d7e8fbCAS | 2804207PubMed |

Yu, F. H., Yun, Y. W., Yuen, B. H., and Moon, Y. S. (1991). Effects of hydroxyflutamide on rats treated with a superovulatory dose of pregnant mare serum gonadotrophin. Can. J. Physiol. Pharmacol. 69, 185–190.
Effects of hydroxyflutamide on rats treated with a superovulatory dose of pregnant mare serum gonadotrophin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhslymsr8%3D&md5=228c34e38d58b52a2b78a85fb1e6d7c4CAS | 2054733PubMed |

Yun, Y. W., Yuen, B. H., and Moon, Y. S. (1987). Effects of superovulatory doses of pregnant mare serum gonadotrophin on oocyte quality and ovulatory and steroid hormone responses in rats. Gamete Res. 16, 109–120.
Effects of superovulatory doses of pregnant mare serum gonadotrophin on oocyte quality and ovulatory and steroid hormone responses in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXitVOrt7s%3D&md5=431c549e558af694449d528c33a052a0CAS | 3506903PubMed |

Yun, Y. W., Yu, F. H., Yuen, B. H., and Moon, Y. S. (1989). Effects of a superovulatory dose of pregnant mare serum gonadotrophin on follicular steroid contents and oocyte maturation in rats. Gamete Res. 23, 289–298.
Effects of a superovulatory dose of pregnant mare serum gonadotrophin on follicular steroid contents and oocyte maturation in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltV2hsLg%3D&md5=0fb0664ed9a54724561213f35b0dfa8bCAS | 2777168PubMed |

Zoller, L. (1991). Quantitative analysis of the membrane granulosa in developing and ovulatory follicle. In ‘Ultrastructure of the Ovary’. (Eds G. Familiari, P. Makabe and M. Motta.) pp. 73-89. (Kluver Academic Publishers: Boston.)