Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Neuromodulatory effect of oestradiol in the metabolism of ovarian progesterone and oestradiol during dioestrus II: participation of the superior mesenteric ganglion

Adriana Vega Orozco A , Cynthia Bronzi A B , Sandra Vallcaneras A B , Zulema Sosa A and Marilina Casais A B C
+ Author Affiliations
- Author Affiliations

A Laboratorio de Biología de la Reproducción (LABIR), Facultad de Química, Bioquímica y Farmacia, Universidad Nacional de San Luis. Ejercito de Los Andes 950. San Luis, República Argentina.

B Instituto Multidisciplinario de Investigaciones Biológicas (IMIBIO-SL), Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Ejercito de Los Andes 950 – 1er Bloque 1er piso ala Norte D5700HHW, San Luis, República Argentina.

C Corresponding author. Email: mcasais@unsl.edu.ar

Reproduction, Fertility and Development 29(11) 2175-2182 https://doi.org/10.1071/RD16378
Submitted: 26 September 2016  Accepted: 1 February 2017   Published: 26 April 2017

Abstract

The aims of the present study were to determine: (1) whether oestradiol (E2) in the superior mesenteric ganglion (SMG) modifies the release of ovarian progesterone (P4), androstenedione (A2) and E2, the activity and gene expression of 3β-hydroxysteroid dehydrogenase (3β-HSD) and 20α-HSD and the expression of P450 aromatase (Cyp19a1) and (2) whether any such modifications are related to changes in ovarian nitric oxide (NO) and noradrenaline (NA) levels during dioestrus II. Using an ex vivo SMG–ovarian nervous plexus–ovary system, ovarian P4 release was measured following the addition E2 plus tamoxifen (Txf) (10−6M) to the ganglion, whereas A2, E2, NA and NO were measured following the addition of E2 alone. Steroids were measured by radioimmunoassay, NA concentrations were determined by HPLC and gene expression was evaluated using reverse transcription–polymerase chain reaction. Oestradiol in the ganglion decreased ovarian P4, E2 and NA release, as well as 3β-HSD activity, but increased the release of A2 and nitrites, as well as the 20α-HSD expression and its activity. No changes were observed in Cyp19a1 gene expression. The addition of E2 plus Txf to the ganglion reversed the effects of E2 alone. The action of oestradiol in SMG favours the beginning of functional luteolysis, due to an increase in NO release and a decrease in NA in the ovary. These results may help elucidate the role of E2 in hormone-dependent pathologies in women.

Additional keywords: nitric oxide, noradrenaline, ovary, steroidogenesis.


References

Aguado, L. I., and Ojeda, S. R. (1984). Ovarian adrenergic nerves play a role in maintaining preovulatory steroid secretion. Endocrinology 114, 1944–1946.
Ovarian adrenergic nerves play a role in maintaining preovulatory steroid secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXitVCitLs%3D&md5=e5f36be17b745e10c0bd5300a85b775cCAS |

Anesetti, G., Lombide, P., and Chavez-Genaro, R. (2009). Prepubertal estrogen exposure modifies neurotrophin receptor expression in celiac neurons and alters ovarian innervation. Auton. Neurosci. 145, 35–43.
Prepubertal estrogen exposure modifies neurotrophin receptor expression in celiac neurons and alters ovarian innervation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVersQ%3D%3D&md5=ddfa6e3f3947a85d179e7e693d22abe3CAS |

Banerjee, A., Anjum, S., Verma, R., and Krishna, A. (2012). Alteration in expression of estrogen receptor isoforms alpha and beta, and aromatase in the testis and its relation with changes in nitric oxide during aging in mice. Steroids 77, 609–620.
Alteration in expression of estrogen receptor isoforms alpha and beta, and aromatase in the testis and its relation with changes in nitric oxide during aging in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1OqtL4%3D&md5=ddbf34b0bd04113d5acbdee4e08b850aCAS |

Berman, J. R., McCarthy, M. M., and Kyprianou, N. (1998). Effect of estrogen withdrawal on nitric oxide synthase expression and apoptosis in the rat vagina. Urology 51, 650–656.
Effect of estrogen withdrawal on nitric oxide synthase expression and apoptosis in the rat vagina.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3ks1SgtA%3D%3D&md5=05ae0d650577a72e31f047be2df49114CAS |

Bronzi, C. D., Daneri, C., Vega, O. A., Delsouc, B., Rastrilla, A. M., Casais, M., and Sosa, Z. (2013). Protective effect of oestradiol in the coeliac ganglion against ovarian apoptotic mechanism on dioestrus. J. Steroid Biochem. Mol. Biol. 135, 60–66.
Protective effect of oestradiol in the coeliac ganglion against ovarian apoptotic mechanism on dioestrus.Crossref | GoogleScholarGoogle Scholar |

Bronzi, C. D., Vega Orozco, A. S., Rodriguez, D., Rastrilla, A. M., Sosa, Z. Y., and Casais, M. (2015). Noradrenaline modulates the presence of gonadotropin-releasing hormone in ovary. The importance of its interrelation on the ovarian steroidogenesis and apoptosis on dioestrus II in rat. J. Steroid Biochem. Mol. Biol. 154, 39–46.
Noradrenaline modulates the presence of gonadotropin-releasing hormone in ovary. The importance of its interrelation on the ovarian steroidogenesis and apoptosis on dioestrus II in rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtF2rtr%2FI&md5=208ef3e5eb0a05f03fd8500994fe274bCAS |

Casais, M., Delgado, S. M., Sosa, Z. Y., Telleria, C. M., and Rastrilla, A. M. (2006). The celiac ganglion modulates LH-induced inhibition of androstenedione release in late pregnant rat ovaries. Reprod. Biol. Endocrinol. 4, 66–72.
The celiac ganglion modulates LH-induced inhibition of androstenedione release in late pregnant rat ovaries.Crossref | GoogleScholarGoogle Scholar |

Casais, M., Vallcaneras, S. S., Campo Verde Arbocco, F., Delgado, S. M., Hapon, M. B., Sosa, Z., Telleria, C. M., and Rastrilla, A. M. (2012). Estradiol promotes luteal regression through a direct effect on the ovary and an indirect effect from the celiac ganglion via the superior ovarian nerve. Reprod. Sci. 19, 416–422.
Estradiol promotes luteal regression through a direct effect on the ovary and an indirect effect from the celiac ganglion via the superior ovarian nerve.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1Ortbc%3D&md5=6442bf481dd64283cb77df5dfd1564c2CAS |

Chomczynski, P. A. (1993). A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 15, 532–534, 536–537.
| 1:CAS:528:DyaK3sXms1Grtrs%3D&md5=11196d04384986fad0634cdbadcddae0CAS |

Couse, J. F., Yates, M. M., Walker, V. R., and Korach, K. S. (2003). Characterization of the hypothalamic–pituitary–gonadal axis in estrogen receptor (ER) null mice reveals hypergonadism and endocrine sex reversal in females lacking ERalpha but not ERbeta. Mol. Endocrinol. 17, 1039–1053.
Characterization of the hypothalamic–pituitary–gonadal axis in estrogen receptor (ER) null mice reveals hypergonadism and endocrine sex reversal in females lacking ERalpha but not ERbeta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlymsbY%3D&md5=adaa4c05a902e0eebb4ea9f0a3f6119bCAS |

Daneri, C., Orozco, A. V., Bronzi, D., Mohn, C., Rastrilla, A. M., and Sosa, Z. Y. (2013). Involvement of the ganglion cholinergic receptors in gonadotropin-releasing hormone, catecholamines, and progesterone release in the rat ovary. Fertil. Steril. 99, 2062–2070.
Involvement of the ganglion cholinergic receptors in gonadotropin-releasing hormone, catecholamines, and progesterone release in the rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktlGit7w%3D&md5=ec9b05ef3fb4b07915a2224fcc94daceCAS |

De Bortoli, M. A., Garraza, M. H., and Aguado, L. I. (1998). Adrenergic intracerebroventricular stimulation affects progesterone concentration in the ovarian vein of the rat: participation of the superior ovarian nerve. J. Endocrinol. 159, 61–68.
Adrenergic intracerebroventricular stimulation affects progesterone concentration in the ovarian vein of the rat: participation of the superior ovarian nerve.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsFOntb4%3D&md5=f57078932ed5278fc6314f21d068a713CAS |

Delgado, S. M., Sosa, Z., Dominguez, N. S., Casais, M., Aguado, L., and Rastrilla, A. M. (2004). Effect of the relation between neural cholinergic action and nitric oxide on ovarian steroidogenesis in prepubertal rats. J. Steroid Biochem. Mol. Biol. 91, 139–145.
Effect of the relation between neural cholinergic action and nitric oxide on ovarian steroidogenesis in prepubertal rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVCju70%3D&md5=89b68a0ea45fd8b0570b2b9ba0da0c6fCAS |

Egami, F., and Taniguchi, S. (1974). Nitrate. In ‘Methods of Enzymatic Analysis’, 2nd edn. (Ed. H. U. Bergmeyr.) pp. 2260–2265. (Academic Press: New York.)

Eisenhofer, G., Goldstein, D. S., Stull, R., Keiser, H. R., Sunderland, T., Murphy, D. L., and Kopin, I. J. (1986). Simultaneous liquid-chromatographic determination of 3, 4-dihydroxyphenylglycol, catecholamines, and 3,4-dihydroxyphenylalanine in plasma, and their responses to inhibition of monoamine oxidase. Clin. Chem. 32, 2030–2033.
| 1:CAS:528:DyaL2sXhtlSntA%3D%3D&md5=9e0a6b84fb7d384953c9ceea53ad7568CAS |

Erickson, G. F., Magofin, D. A., Dyer, C. A., and Hofeditz, C. (1985). The ovarian androgen-producing cells: a review of structure/function relationships. Endocr. Rev. 6, 371–399.
The ovarian androgen-producing cells: a review of structure/function relationships.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvV2qsb0%3D&md5=4a7e606f484c2db65561e58d32cf5adbCAS |

Fridén, B. E., Runesson, E., Hahlin, M., and Brännström, M. (2000). Evidence for nitric oxide acting as a luteolytic factor in the human corpus luteum. Mol. Hum. Reprod. 6, 397–403.
Evidence for nitric oxide acting as a luteolytic factor in the human corpus luteum.Crossref | GoogleScholarGoogle Scholar |

Hazell, G. G. J., Yao, S. T., Roper, J. A., Prossnitz, E. R., O’Carroll, A.-M., and Lolait, S. J. (2009). Localization of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues. J. Endocrinol. 202, 223–236.
Localization of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsFOgsbo%3D&md5=197701f1a136c3d63cbc050484ac31c0CAS |

Hickey, G. J., Chen, S. A., Besman, M. J., Shively, J. E., Hall, P. F., Gaddy-Kurten, D., and Richards, J. S. (1988). Hormonal regulation, tissue distribution, and content of aromatase cytochrome P450 messenger ribonucleic acid and enzyme in rat ovarian follicles and corpora lutea: relationship to estradiol biosynthesis. Endocrinology 122, 1426–1436.
Hormonal regulation, tissue distribution, and content of aromatase cytochrome P450 messenger ribonucleic acid and enzyme in rat ovarian follicles and corpora lutea: relationship to estradiol biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhvVSgtro%3D&md5=6ddeda1074f263e361099a74a62c4461CAS |

Jaroszewski, J. J., and Hansel, W. (2000). Intraluteal administration of a nitric oxide synthase blocker stimulates progesterone and oxytocin secretion and prolongs the life span of the bovine corpus luteum. Proc. Soc. Exp. Biol. Med. 224, 50–55.
Intraluteal administration of a nitric oxide synthase blocker stimulates progesterone and oxytocin secretion and prolongs the life span of the bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislyqt7Y%3D&md5=596bb84c530d54467ae19f5737df30e7CAS |

Järvi, R. (1989). Localization of bombesin, neuropeptide Y, enkephalin, and tyrosine hydroxylase-like inmunoreactivities in rats coeliac-superior mesenteric ganglion. Histochemistry 92, 231–236.
Localization of bombesin, neuropeptide Y, enkephalin, and tyrosine hydroxylase-like inmunoreactivities in rats coeliac-superior mesenteric ganglion.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. C., Diaz, H. A., Stocco, C., Palomino, A., Devoto, L., and Vega, M. (1999). Antisteroidogenic action of nitric oxide on human corpus luteum in vitro: mechanism of action. Endocrine 11, 31–36.
Antisteroidogenic action of nitric oxide on human corpus luteum in vitro: mechanism of action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1eit7s%3D&md5=0ce5e6d957f56d11414bc5d2df280351CAS |

Kawano, T., Okamura, H., Tajima, C., Fukuma, K., and Katabuchi, H. (1988). Effect of RU 486 on luteal function in the early pregnant rat. J. Reprod. Fertil. 83, 279–285.
Effect of RU 486 on luteal function in the early pregnant rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktlagt7k%3D&md5=7d03251f2f0f73b60de6d332e62ce945CAS |

Klein, C. M., and Burden, H. W. (1988a). Anatomical localization of afferent and postganglionic sympathetic neurons innervating the rat ovary. Neurosci. Lett. 85, 217–222.
Anatomical localization of afferent and postganglionic sympathetic neurons innervating the rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3jtlegsQ%3D%3D&md5=3d336e4e5145f2a4426a971c7124551fCAS |

Klein, C. M., and Burden, H. W. (1988b). Substance P and vasoactive intestinal polypeptide (VIP) inmunoreactive nerve fibers in relation to ovarian postganglionic perikarya in para- and prevertebral ganglia: evidence from combined retrograde tracing and immunocytochemistry. Cell Tissue Res. 252, 403–410.
Substance P and vasoactive intestinal polypeptide (VIP) inmunoreactive nerve fibers in relation to ovarian postganglionic perikarya in para- and prevertebral ganglia: evidence from combined retrograde tracing and immunocytochemistry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXitFKltb4%3D&md5=0a2223653b5c42891b43f1fb35bd51f4CAS |

Koh, D. S., and Hille, B. (1997). Modulation by neurotransmitters of catecholamine secretion from sympathetic ganglion neurons detected by amperometry. Proc. Natl Acad. Sci. USA 94, 1506–1511.
Modulation by neurotransmitters of catecholamine secretion from sympathetic ganglion neurons detected by amperometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtl2ntLg%3D&md5=e575528558a7f541e21a17779ad33686CAS |

Korzekwa, A. J., Okuda, K., Woclawek-Potocka, I., Murakami, S., and Skarzynski, D. J. (2006). Nitric oxide induces apoptosis in bovine luteal cells. J. Reprod. Dev. 52, 353–361.
Nitric oxide induces apoptosis in bovine luteal cells.Crossref | GoogleScholarGoogle Scholar |

Lara, H. E., Dorfman, M., Venegas, M., Luza, S. M., Luna, S. L., Mayerhofer, A., and Guimaraes, M. A. (2002). Changes in sympathetic nerve activity of the mammalian ovary during a normal estrous cycle and in polycystic ovary syndrome: studies on norepinephrine release. Microsc. Res. Tech. 59, 495–502.
Changes in sympathetic nerve activity of the mammalian ovary during a normal estrous cycle and in polycystic ovary syndrome: studies on norepinephrine release.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVKnsQ%3D%3D&md5=acf2caf74442d8373601e1b0b99b127dCAS |

Lars-Gösta, E., Holmberg, K., Emson, P., Schemmann, M., and Hokfelt, T. (1997). Nitric oxide synthase, choline acetyltransferase, catecholamine enzymes and neuropeptides and their colocalization in the anterior pelvic ganglion and hypogastryc nerve of the male guinea pig. J. Chem Neuroanat 14, 33–49.
Nitric oxide synthase, choline acetyltransferase, catecholamine enzymes and neuropeptides and their colocalization in the anterior pelvic ganglion and hypogastryc nerve of the male guinea pig.Crossref | GoogleScholarGoogle Scholar |

Lawrence, I. E., and Burden, H. W. (1980). The origin of the extrinsic adrenergic innervation to the ovary. Anat. Rec. 196, 51–59.
The origin of the extrinsic adrenergic innervation to the ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXktVGjs7g%3D&md5=f690fa5769d2a24664ddccb70fea702eCAS |

Lowry, O. H., Rosebrough, H. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275.
| 1:CAS:528:DyaG38XhsVyrsw%3D%3D&md5=543feb0ae4d03a840b0d5387fc0cd0f1CAS |

Mani, S. K., Mermelstein, P. G., Tetel, M. J., and Anesetti, G. (2012). Convergence of multiple mechanisms of steroid hormone action. Horm. Metab. Res. 44, 569–576.
Convergence of multiple mechanisms of steroid hormone action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVGisbfL&md5=4c81e72a4e4c0bbbe634850b9d77e2c3CAS |

Motta, A. B., Estevez, A., Tognetti, T., Gimeno, M. A., and Franchi, A. M. (2001). Dual effects of nitric oxide in functional and regressing rat corpus luteum. Mol. Hum. Reprod. 7, 43–47.
Dual effects of nitric oxide in functional and regressing rat corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtVeisrc%3D&md5=ca8e0771ac1b9a7074421b77d64414bbCAS |

Olson, L. M., Jones-Burton, C. M., and Jablonka-Shariff, A. (1996). Nitric oxide decreases estradiol synthesis of rats luteinized ovarian cells: possible role for nitric oxide in functional luteal regression. Endocrinology 137, 3531–3539.
| 1:CAS:528:DyaK28XksVChsbk%3D&md5=317fdd1a663a351006cc295c449e5223CAS |

Orozco, A. V., Sosa, Z., Fillipa, V., Mohamed, F., and Rastrilla, A. M. (2006). The cholinergic influence on the mesenteric ganglion affects the liberation of ovarian steroids and nitric oxide in oestrus day rats: characterization of an ex vivo system. J. Endocrinol. 191, 587–598.
The cholinergic influence on the mesenteric ganglion affects the liberation of ovarian steroids and nitric oxide in oestrus day rats: characterization of an ex vivo system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1egu7o%3D&md5=7ff3e0f73f63668df0c50eeac2048d27CAS |

Poole, T. (1999). ‘The UFAW Handbook on the Care and Management of Laboratory Animals. Vol. 1: Terrestrial Vertebrates, 7th edition.’ (UFAW: Herts.)

Rosa-e-Silva, A., Guimaraes, M. A., Padmanabhan, V., and Lara, H. E. (2003). Prepubertal administration of estradiol valerate disrupts cyclicity and leads to cystic ovarian morphology during adult life in the rat: role of sympathetic innervation. Endocrinology 144, 4289–4297.
Prepubertal administration of estradiol valerate disrupts cyclicity and leads to cystic ovarian morphology during adult life in the rat: role of sympathetic innervation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1SrtL0%3D&md5=8d9f0d84bdf13a8b395979d9e1da7c4aCAS |

Shinohara, Y., Matsumoto, A., and Mori, T. (1998). Effects of prenatal exposure to diethylstilbestrol on the sympathetic nervous system in the rat ovary. Neurosci. Lett. 255, 123–126.
Effects of prenatal exposure to diethylstilbestrol on the sympathetic nervous system in the rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmvFWmur8%3D&md5=511f7617dae995da5721afd143eb57d4CAS |

Shirasuna, K. (2010). Nitric oxide and luteal blood flow in the luteolytic cascade in the cow. J. Reprod. Dev. 56, 9–14.
Nitric oxide and luteal blood flow in the luteolytic cascade in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVymsbg%3D&md5=57a585bd2b8ad86b2e960d41472c0582CAS |

Skarzynski, D. J., and Okuda, K. (2000). Different actions of noradrenaline and nitric oxide on the output of prostaglandins and progesterone in cultured bovine luteal cells. Prostaglandins Other Lipid Mediat. 60, 35–47.
Different actions of noradrenaline and nitric oxide on the output of prostaglandins and progesterone in cultured bovine luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosFeksg%3D%3D&md5=37ca679b4948047a4dcbac807a4de9c2CAS |

Skarzynski, D. J., Kobayashi, S., and Okuda, K. (2000). Influence of nitric oxide and noradrenaline on prostaglandin F(2)(alpha)-induced oxytocin secretion and intracellular calcium mobilization in cultured bovine luteal cells. Biol. Reprod. 63, 1000–1005.
Influence of nitric oxide and noradrenaline on prostaglandin F(2)(alpha)-induced oxytocin secretion and intracellular calcium mobilization in cultured bovine luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmslyltLo%3D&md5=74ee194c2a9287e14faaf23c1ac01ed3CAS |

Snedecor, W. G., and Cochram, W. G. (1976). ‘Statistical Methods.’ (The Iowa State University Press: Ames, IA.)

Song, R. X., Zhang, Z., and Santen, R. J. (2005). Estrogen rapid action via protein complex formation involving ERalpha and Src. Trends Endocrinol. Metab. 16, 347–353.
Estrogen rapid action via protein complex formation involving ERalpha and Src.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVart7fN&md5=4239b8efc40a20ff81a8488f12fd7d0cCAS |

Sosa, Z. Y., Casais, M., Rastrilla, A. M., and Aguado, L. (2000). Adrenergic influences on coeliac ganglion affect the release of progesterone from cycling ovaries: characterisation of an in vitro system. J. Endocrinol. 166, 307–318.
Adrenergic influences on coeliac ganglion affect the release of progesterone from cycling ovaries: characterisation of an in vitro system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFOqt78%3D&md5=08d27c455af77ce32ff5b4ac93846d94CAS |

Stocco, C. O., Chedrese, J., and Deis, R. P. (2001). Luteal expression of cytochrome P450 side-chain cleavage, steroidogenic acute regulatory protein, 3beta-hydroxysteroid dehydrogenase, and 20alpha-hydroxysteroid dehydrogenase genes in late pregnant rats: effect of luteinizing hormone and RU486. Biol. Reprod. 65, 1114–1119.
Luteal expression of cytochrome P450 side-chain cleavage, steroidogenic acute regulatory protein, 3beta-hydroxysteroid dehydrogenase, and 20alpha-hydroxysteroid dehydrogenase genes in late pregnant rats: effect of luteinizing hormone and RU486.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1Cms78%3D&md5=ae78d6060f072fa3d61e12bae6448ed7CAS |

Stocco, C., Telleria, C., and Gibori, G. (2007). The molecular control of corpus luteum formation, function, and regression. Endocr. Rev. 28, 117–149.
The molecular control of corpus luteum formation, function, and regression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtFCgsrc%3D&md5=f2ee08d96fd8585609a4e401c67201f4CAS |

Vallcaneras, S. S., Casais, M., Delgado, S. M., Filippa, V., Mohamed, F., Sosa, Z., and Rastrilla, A. M. (2009). Androgen receptors in coeliac ganglion in late pregnant rat. Steroids 74, 526–534.
Androgen receptors in coeliac ganglion in late pregnant rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFajtbc%3D&md5=98238b58521f121a07d9e509cd367becCAS |

Van Voorhis, B. J., Dunn, M. S., Snyder, G. D., and Weiner, C. P. (1994). Nitric oxide: an autocrine regulator of human granulosa–luteal cell steroidogenesis. Endocrinology 135, 1799–1806.
| 1:CAS:528:DyaK2MXitVyqtbk%3D&md5=e811891e92d365f450ddac75ffdf44ffCAS |

Vega Orozco, A., Sosa, Z., Delgado, S., Casais, M., and Rastrilla, A. M. (2010). Involvement of ganglionic cholinergic receptors on the steroidogenesis in the luteal phase in rat. J. Steroid Biochem. Mol. Biol. 120, 45–52.
Involvement of ganglionic cholinergic receptors on the steroidogenesis in the luteal phase in rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFGksLg%3D&md5=7c579e0f2804e9f697ad810fa4d27bbfCAS |

Vega Orozco, A. S., Daneri, C., Anesetti, G., Cabrera, R., Sosa, Z., and Rastrilla, A. M. (2012). Involvement of the oestrogenic receptors in superior mesenteric ganglion on the ovarian steroidogenesis in rat. Reproduction 143, 183–193.
Involvement of the oestrogenic receptors in superior mesenteric ganglion on the ovarian steroidogenesis in rat.Crossref | GoogleScholarGoogle Scholar |

Weihua, Z., Andersson, S., Cheng, G., Simpson, E. R., Warner, M., and Gustafsson, J. A. (2003). Update on estrogen signaling. FEBS Lett. 546, 17–24.
Update on estrogen signaling.Crossref | GoogleScholarGoogle Scholar |