*(A R R Cáceres, F Campo Verde Arboccó, A S Vega Orozco and M R Laconi contributed equally to this work)
Neuroactive steroids can rapidly regulate multiple physiological functions in the central and peripheral nervous systems. The aims of the present study were to determine whether allopregnanolone (ALLO), administered in low nanomolar and high micromolar concentrations, can: (i) induce changes in the ovarian progesterone (P4) and estradiol (E2) release; (ii) modify the ovarian mRNA expression of Hsd3b1 (3β-hydroxysteroid dehydrogenase, 3β-HSD)3β-, Akr1c3 (20α-hydroxysteroid dehydrogenase, 20α-HSD), and Akr1c14 (3α-hydroxy steroid oxidoreductase, 3α-HSOR)); and (iii) modulate the ovarian expression of progesterone receptors A and B, α and β estrogenic receptors, luteinizing hormone receptor (LHR) and follicle-stimulating hormone receptor (FSHR). To further characterize ALLO peripheral actions, the effects were evaluated using a superior mesenteric ganglion–ovarian nervous plexus–ovary (SMG–ONP–O) and a denervated ovary (DO) systems. ALLO SMG administration increased P4 concentration in the incubation liquid by decreasing ovarian 20α-HSD mRNA, and it also increased ovarian 3α-HSOR mRNA expression. In addition, ALLO neural peripheral modulation induced an increase in the expression of ovarian LHR, PRA, PRB, and ERα. Direct ALLO administration to the DO decreased E2 and increased P4 concentration in the incubation liquid. The mRNA expression of 3β-HSD decreased and 20α-HSD increased. Further, ALLO in the OD significantly changed ovarian FSHR and PRA expression. This is the first evidence of ALLO’s direct effect on ovarian steroidogenesis. Our results provide important insights about how this neuroactive steroid interacts both with the PNS and the ovary, and these findings might help devise some of the pleiotropic effects of neuroactive steroids on female reproduction. Moreover, ALLO modulation of ovarian physiology might help uncover novel treatment approaches for reproductive diseases.
Journal of Endocrinology is committed to supporting researchers in demonstrating the impact of their articles published in the journal.
The two types of article metrics we measure are (i) more traditional full-text views and pdf downloads, and (ii) Altmetric data, which shows the wider impact of articles in a range of non-traditional sources, such as social media.
More information is on the Reasons to publish page.
Sept 2018 onwards | Past Year | Past 30 Days | |
---|---|---|---|
Full Text Views | 102 | 50 | 0 |
PDF Downloads | 110 | 73 | 0 |
Acuña E, Fornes R, Fernandois D, Garrido MP, Greiner M, Lara HE & & Paredes AH 2009 Increases in norepinephrine release and ovarian cyst formation during ageing in the rat. Reproductive Biology and Endocrinology: RB&E 7 64. (https://doi.org/10.1186/1477-7827-7-64)
Aguado LI 2002 Role of the central and peripheral nervous system in the ovarian function. Microscopy Research and Technique 59 462–473. (https://doi.org/10.1002/jemt.10232)
Akison LK & & Robker RL 2012 The critical roles of progesterone receptor (PGR) in ovulation, oocyte developmental competence and oviductal transport in mammalian reproduction. Reproduction in Domestic Animals 47(Supplement 4) 288–296. (https://doi.org/10.1111/J.1439-0531.2012.02088.X)
Andréen L, Nyberg S, Turkmen S, van Wingen G, Fernández G & & Bäckström T 2009 Sex steroid induced negative mood may be explained by the paradoxical effect mediated by GABAA modulators. Psychoneuroendocrinology 34 1121–1132. (https://doi.org/10.1016/j.psyneuen.2009.02.003)
Asensio JA, Cáceres ARR, Pelegrina LT, Sanhueza MLÁ, Scotti L, Parborell F & & Laconi MR 2018 Allopregnanolone alters follicular and luteal dynamics during the estrous cycle. Reproductive Biology and Endocrinology 16 35. (https://doi.org/10.1186/s12958-018-0353-y)
Bäckström T, Bixo M, Johansson M, Nyberg S, Ossewaarde L, Ragagnin G, Savic I, Strömberg J, Timby E, van Broekhoven F, et al.2014 Allopregnanolone and mood disorders. Progress in Neurobiology 113. (https://doi.org/10.1016/j.pneurobio.2013.07.005)
Bali A & & Jaggi AS 2014 Multifunctional aspects of allopregnanolone in stress and related disorders. Progress in Neuro-Psychopharmacology and Biological Psychiatry 48 64–78. (https://doi.org/10.1016/j.pnpbp.2013.09.005)
Baljet B & & Drukker J 1979 The extrinsic innervation of the abdominal organs in the female rat. Acta Anatomica 104 243–267. (https://doi.org/10.1159/000145073)
Belelli D & & Lambert JJ 2005 Neurosteroids: endogenous regulators of the GABAA receptor. Nature Reviews. Neuroscience 6 565–575. (https://doi.org/10.1038/nrn1703)
Bendix M, Bixo M, Wihlbäck AC, Ahokas A & & Jokinen J 2019 Allopregnanolone and progesterone in estradiol treated severe postpartum depression and psychosis – preliminary findings. Neurology, Psychiatry and Brain Research 34 50–57. (https://doi.org/10.1016/J.NPBR.2019.10.003)
Benitez A, Riquelme R, del Campo M, Araya C & & Lara HE 2021 Nerve growth factor: A dual activator of noradrenergic and cholinergic systems of the rat ovary. Frontiers in Endocrinology 12 636600. (https://doi.org/10.3389/fendo.2021.636600)
Boero G, Porcu P & & Morrow AL 2020 Pleiotropic actions of allopregnanolone underlie therapeutic benefits in stress-related disease. Neurobiology of Stress 12 100203. (https://doi.org/10.1016/j.ynstr.2019.100203)
Bonalume V, Caffino L, Castelnovo LF, Faroni A, Giavarini F, Liu S, Caruso D, Schmelz M, Fumagalli F, Carr RW, et al.2020 Schwann cell autocrine and paracrine regulatory mechanisms, mediated by allopregnanolone and BDNF, modulate PKCε in peripheral sensory neurons. Cells 9. (https://doi.org/10.3390/cells9081874)
Bossard C, Busson M, Vindrieux D, Gaudin F, Machelon V, Brigitte M, Jacquard C, Pillon A, Balaguer P, Balabanian K, et al.2012 Potential role of estrogen receptor beta as a tumor suppressor of epithelial ovarian cancer. PLoS One 7 e44787. (https://doi.org/10.1371/JOURNAL.PONE.0044787)
Bravo-Benitez JM, Cruz Y, Lucio RA, Venegas B, Díaz A, Morales-Ledesma L, Domínguez R & & Morán C 2022 Intrinsic innervation of the ovary and its variations in the rat senescence process. Journal of Molecular Histology 53 347–356. (https://doi.org/10.1007/s10735-022-10069-7)
Bullock AE, Clark AL, Grady SR, Robinson SF, Slobe BS, Marks MJ & & Collins AC 1997 Neurosteroids modulate nicotinic receptor function in mouse striatal and thalamic synaptosomes. Journal of Neurochemistry 68 2412–2423. (https://doi.org/10.1046/j.1471-4159.1997.68062412.x)
Cáceres ARR, Campo Verde Arboccó F, Cardone DA & & Sanhueza M 2021 Superior mesenteric ganglion neural modulation of ovarian angiogenesis, apoptosis and proliferation by the neuroactive steroid allopregnanolone. Journal of Neuroendocrinology e13056. (https://doi.org/10.1111/jne.13056)
Cáceres ARR, Orozco V, Cabrera RJ & & Laconi MR 2020 Rapid actions of the neurosteroid allopregnanolone on ovarian and hypothalamic steroidogenesis: central and peripheral modulation. Journal of Neuroendocrinology 32 1–13. (https://doi.org/10.1111/jne.12836)
Cai Z & & Stocco C 2005 Expression and regulation of progestin membrane receptors in the rat corpus luteum. Endocrinology 146 5522–5532. (https://doi.org/10.1210/en.2005-0759)
Camille Melón L & & Maguire J 2016 GABAergic regulation of the HPA and HPG axes and the impact of stress on reproductive function. Journal of Steroid Biochemistry and Molecular Biology 160. (https://doi.org/10.1016/j.jsbmb.2015.11.019)
Camp TA, Rahal JO & & Mayo KE 1991 Cellular localization and hormonal regulation of follicle-stimulating hormone and luteinizing hormone receptor messenger RNAs in the rat ovary. Molecular Endocrinology 5 1405–1417. (https://doi.org/10.1210/mend-5-10-1405)
Colciago A, Bonalume V, Melfi V & & Magnaghi V 2020 Genomic and non-genomic action of neurosteroids in the peripheral nervous system. Frontiers in Neuroscience 14 796. (https://doi.org/10.3389/fnins.2020.00796)
Corpéchot C, Young J, Calvel M, Wehrey C, Veltz JN, Touyer G, Mouren M, Prasad VVK, Banner C, Sjövall J, et al.1993 Neurosteroids: 3α-hydroxy-5α-pregnan-20-one and its precursor in the brain, plasma, and steroidogenic glands of male, and female rats. Endocrinology 133 1003–1009. (https://doi.org/10.1210/endo.133.3.8365352)
Covaleda AMS, Van den Berg H, Vervoort J, Van der Saag P, Ström A, Gustafsson JÅ, Rietjens I & & Murk AJ 2008 Influence of cellular ERα/ERβ ratio on the ERα-agonist induced proliferation of human T47D breast cancer cells. Toxicological Sciences 105 303–311. (https://doi.org/10.1093/TOXSCI/KFN141)
D’Albora H, Anesetti G, Lombide P, Les Dees WL & & Ojeda SR 2002 Intrinsic neurons in the mammalian ovary. Microscopy Research and Technique 59 484–489. (https://doi.org/10.1002/jemt.10231)
Daneri C, Orozco AV, Bronzi D, Mohn C, Rastrilla AM & & Sosa ZY 2013 Involvement of the ganglion cholinergic receptors in gonadotropin-releasing hormone, catecholamines, and progesterone release in the rat ovary. Fertility and Sterility 99 2062–2070. (https://doi.org/10.1016/j.fertnstert.2013.02.037)
Del Campo M, Piquer B, Witherington J, Sridhar A & & Lara HE 2019 Effect of superior ovarian nerve and plexus nerve sympathetic denervation on ovarian-derived infertility provoked by estradiol exposure to rats. Frontiers in Physiology 10 349. (https://doi.org/10.3389/fphys.2019.00349)
Delgado SM, Casais M, Sosa Z & & Rastrilla AM 2006 Ganglionic adrenergic action modulates ovarian steroids and nitric oxide in prepubertal rat. Endocrine Journal 53 547–554. (https://doi.org/10.1507/endocrj.K05-130)
Delgado SM, Escudero CG, Casais M, Gordillo M, Anzulovich AC, Sosa Z & & Rastrilla AM 2010 Ovaric physiology in the first oestral cycle: influence of noradrenergic and cholinergic neural stimuli from coeliac ganglion. Steroids 75 685–694. (https://doi.org/10.1016/J.STEROIDS.2010.04.005)
Delsouc MB, Bronzi CD, Becerra CD, Bonaventura MM, Mohamed FH & & Casais M 2019 Ganglionic and ovarian action of acetylcholine during diestrous II in rats. Neuroendocrine control of the luteal regression. Steroids 148 19–27. (https://doi.org/10.1016/j.steroids.2019.04.005)
Diep CH, Daniel AR, Mauro LJ, Knutson TP & & Lange CA 2015 Progesterone action in breast, uterine, and ovarian cancers. Journal of Molecular Endocrinology 54 R31–R53. (https://doi.org/10.1530/JME-14-0252)
Dinny Graham JD & & Clarke CL 2002 Expression and transcriptional activity of progesterone receptor A and progesterone receptor B in mammalian cells. Breast Cancer Research 4 187–190. (https://doi.org/10.1186/bcr450)
Domínguez R & & Cruz-Morales SE 2011 The ovarian innervation participates in the regulation of ovarian functions. Endocrinology and Metabolic Syndrome 4 1. (https://doi.org/10.4172/2161-1017.S4-001)
Dunkel L, Tilly JL, Shikone T, Nishimori K & & Hsueh AJW 1994 Follicle-stimulating hormone receptor expression in the rat ovary: increases during prepubertal development and regulation by the opposing actions of transforming growth factors β and α. Biology of Reproduction 50 940–948. (https://doi.org/10.1095/biolreprod50.4.940)
Erdö SL, Joo F & & Wolff JR 1989 Immunohistochemical localization of glutamate decarboxylase in the rat oviduct and ovary: further evidence for non-neural GABA systems. Cell and Tissue Research 255 431–434. (https://doi.org/10.1007/BF00224128)
Falvo E, Diviccaro S, Melcangi RC & & Giatti S 2020 Physiopathological role of neuroactive steroids in the peripheral nervous system. International Journal of Molecular Sciences 21. (https://doi.org/10.3390/ijms21239000)
Faroni A & & Magnaghi V 2011 The neurosteroid allopregnanolone modulates specific functions in central and peripheral glial cells. Frontiers in Endocrinology 2 103. (https://doi.org/10.3389/fendo.2011.00103)
Farrant M & & Nusser Z 2005 Variations on an inhibitory theme: phasic and tonic activation of GABA A receptors. Nature Reviews. Neuroscience 6 215–229. (https://doi.org/10.1038/nrn1625)
Fasano C & & Niel JP 2009 The mammalian sympathetic prevertebral ganglia: models for the study of neuronal networks and basic neuronal properties. Autonomic Neuroscience: Basic and Clinical 150 8–20. (https://doi.org/10.1016/j.autneu.2009.06.006)
Forneris ML & & Aguado LI 2002 Neonatal superior ovarian nerve transection disturbs the cyclic activity of the female rats. Journal of Steroid Biochemistry and Molecular Biology 82 75–82. (https://doi.org/10.1016/S0960-0760(0200149-8)
Fortune JE & & Vincent SE 1983 Progesterone inhibits the induction of aromatase activity in rat granulosa cells in vitro. Biology of Reproduction 28 1078–1089. (https://doi.org/10.1095/BIOLREPROD28.5.1078)
Fritz S, Wessler I, Breitling R, Rossmanith W, Ojeda SR, Dissen GA, Amsterdam A & & Mayerhofer A 2001 Expression of muscarinic receptor types in the primate ovary and evidence for nonneuronal acetylcholine Synthesis1. Journal of Clinical Endocrinology and Metabolism 86 349–354. (https://doi.org/10.1210/jcem.86.1.7146)
Genazzani AD, Luisi M, Malavasi B, Strucchi C, Luisi S, Casarosa E, Bernardi F, Genazzani AR & & Petraglia F 2002 Pulsatile secretory characteristics of allopregnanolone, a neuroactive steroid, during the menstrual cycle and in amenorrheic subjects. European Journal of Endocrinology 146 347–356. (https://doi.org/10.1530/eje.0.1460347)
Genazzani AR, Bernardi F, Stomati M, Monteleone P, Luisi S, Rubino S, Farzati A, Casarosa E, Luisi M & & Petraglia F 2000 Effects of estradiol and raloxifene analog on brain, adrenal and serum allopregnanolone content in fertile and ovariectomized female rats. Neuroendocrinology 72 162–170. (https://doi.org/10.1159/000054583)
Genazzani AR, Palumbo MA, De Micheroux AA, Artini PG, Criscuolo M, Ficarra G, Guo AL, Benelli A, Bertolini A, Pertraglia F, et al.1995 Evidence for a role for the neurosteroid allopregnanolone in the modulation of reproductive function in female rats. European Journal of Endocrinology 133 375–380. (https://doi.org/10.1530/eje.0.1330375)
George JW, Dille EA & & Heckert LL 2011 Current concepts of follicle-stimulating hormone receptor gene regulation. Biology of Reproduction 84 7–17. (https://doi.org/10.1095/BIOLREPROD.110.085043)
Gerendai I, Banczerowski P & & Halász B 2005 Functional significance of the innervation of the gonads. Endocrine 28 309–318. (https://doi.org/10.1385/ENDO:28:3:309)
Gerendai I, Tóth IE, Boldogkői Z & & Halász B 2009 Recent findings on the organization of central nervous system structures involved in the innervation of endocrine glands and other organs; observations obtained by the transneuronal viral double-labeling technique. Endocrine 36 179–188. (https://doi.org/10.1007/s12020-009-9189-8)
Ghersa F, Burdisso J, Vallcaneras SS, Fuentes F, de la Vega M, Delgado SM, Telleria CM & & Casais M 2015 Neuromodulation of the luteal regression: presence of progesterone receptors in coeliac ganglion. Experimental Physiology 100 935–946. (https://doi.org/10.1113/EP085261)
González S & & Ferreyra S 2022 Neurosteroids and neuropathic pain: an up-to-date perspective. Current Opinion in Endocrine and Metabolic Research 22 100314. (https://doi.org/10.1016/J.COEMR.2021.100314)
Goyeneche AA, Deis RP, Gibori G & & Telleria CM 2003 Progesterone promotes survival of the rat corpus luteum in the absence of cognate receptors. Biology of Reproduction 68 151–158. (https://doi.org/10.1095/biolreprod.102.007898)
Häppölä O, Karhula T, Päivärinta H, Soinila S, Wu J-Y & & Ahonen M 1992 L-glutamate decarboxylase immunoreactivity in the sympathoadrenal system. In GABA Outside the CNS. Berlin Heidelberg: Springer, pp. 65–82. (https://doi.org/10.1007/978-3-642-76915-3_5)
Hardy DB, Janowski BA, Chen CC & & Mendelson CR 2008 Progesterone receptor inhibits aromatase and inflammatory response pathways in breast cancer cells via ligand-dependent and ligand-independent mechanisms. Molecular Endocrinology 22 1812–1824. (https://doi.org/10.1210/ME.2007-0443)
Holzbauer M 1975 Physiological variations in the ovarian production of 5α-pregnane derivatives with sedative properties in the rat. Journal of Steroid Biochemistry 6 1307–1310. (https://doi.org/10.1016/0022-4731(7590357-X)
Ichikawa S, Sawada T, Nakamura Y & & Morioka H 1974 Ovarian secretion of pregnane compounds during the estrous cycle and pregnancy in rats. Endocrinology 94 1615–1620. (https://doi.org/10.1210/endo-94-6-1615)
Ilenchuk TT & & Walters MR 1987 Rat uterine progesterone receptor analyzed by [3h]R5020 photoaffinity labeling: evidence that the a and b subunits are not equimolar. Endocrinology 120 1449–1456. (https://doi.org/10.1210/endo-120-4-1449)
Itoh MT & & Ishizuka B 2005 alpha1-Adrenergic receptor in rat ovary: Presence and localization. Molecular and Cellular Endocrinology 240 58–63. (https://doi.org/10.1016/j.mce.2005.05.012)
Jana B, Dzienis A, Wojtkiewicz J, Kaczmarek M & & Majewski M 2007 Surgical denervation of porcine ovaries during the middle luteal phase of the oestrous cycle changes their morphology and steroidogenic activity. Acta Veterinaria Hungarica 55 107–122. (https://doi.org/10.1556/AVet.55.2007.1.11)
Jayaraman A & & Pike CJ 2009 Progesterone attenuates oestrogen neuroprotection via downregulation of oestrogen receptor expression in cultured neurones. Journal of Neuroendocrinology 21 77–81. (https://doi.org/10.1111/J.1365-2826.2008.01801.X)
Jure I, De Nicola AF & & Labombarda F 2019 Progesterone effects on the oligodendrocyte linage: all roads lead to the progesterone receptor. Neural Regeneration Research 14 2029–2034. (https://doi.org/10.4103/1673-5374.262570)
Kagitani F, Uchida S & & Hotta H 2008 Effects of electrical stimulation of the superior ovarian nerve and the ovarian plexus nerve on the ovarian estradiol secretion rate in rats. Journal of Physiological Sciences 58 133–138. (https://doi.org/10.2170/physiolsci.RP001508)
Kannisto P, Håkanson R, Owman C, Schmidt G & & Wahlestedt C 1987 GABA suppresses stimulation‐induced release of [3H]‐noradrenaline from sympathetic nerve fibres in bovine ovarian follicles. Journal of Autonomic Pharmacology 7 339–347. (https://doi.org/10.1111/j.1474-8673.1987.tb00162.x)
Klein CM & & Burden HW 1988 Anatomical localization of afferent and postganglionic sympathetic neurons innervating the rat ovary. Neuroscience Letters 85 217–222. (https://doi.org/10.1016/0304-3940(8890354-0)
Laconi MR & & Cabrera RJ 2002 Effect of centrally injected allopregnanolone on sexual receptivity, luteinizing hormone release, hypothalamic dopamine turnover, and release in female rats. Endocrine 17 77–83. (https://doi.org/10.1385/ENDO:17:2:077)
Laconi MR, Chavez C, Cavicchia JC, Fóscolo M, Sosa Z, Yunes RF & & Cabrera RJ 2012 Allopregnanolone alters the luteinizing hormone, prolactin, and progesterone serum levels interfering with the regression and apoptosis in rat corpus luteum. Hormone and Metabolic Research 44 632–638. (https://doi.org/10.1055/s-0032-1314834)
Lambert JJ, Peters JA, Sturgess NC & & Hales TG 1990 Steroid modulation of the GABAA receptor complex: electrophysiological studies. Ciba Foundation Symposium 153 56–71. (https://doi.org/10.1002/9780470513989.ch4)
Langdon SP, Herrington CS, Hollis RL & & Gourley C 2020 Estrogen signaling and its potential as a target for therapy in ovarian cancer. Cancers 12 1647. (https://doi.org/10.3390/CANCERS12061647)
Lawrence IE & & Burden HW 1980 The origin of the extrinsic adrenergic innervation to the rat ovary. Anatomical Record 196 51–59. (https://doi.org/10.1002/ar.1091960106)
Lee S, Kang HG, Jeong PS, Kim MJ, Park SH, Song BS, Sim BW & & Kim SU 2021 Heat stress impairs oocyte maturation through ceramide-mediated apoptosis in pigs. Science of the Total Environment 755 144144. (https://doi.org/10.1016/J.SCITOTENV.2020.144144)
Madeira M, Mattar A, Logullo AF, Soares FA & & Gebrim LH 2013 Estrogen receptor alpha/beta ratio and estrogen receptor beta as predictors of endocrine therapy responsiveness-a randomized neoadjuvant trial comparison between anastrozole and tamoxifen for the treatment of postmenopausal breast cancer. BMC Cancer 13 425. (https://doi.org/10.1186/1471-2407-13-425)
Majewska MD 1992 Neurosteroids: endogenous bimodal modulators of the GABAA receptor mechanism of action and physiological significance. Progress in Neurobiology 38 379–395. (https://doi.org/10.1016/0301-0082(9290025-A)
Mal R, Magner A, David J, Datta J, Vallabhaneni M, Kassem M, Manouchehri J, Willingham N, Stover D, Vandeusen J, et al.2020 Estrogen receptor beta (ERβ): a ligand activated tumor suppressor. Frontiers in Oncology 10 587386. (https://doi.org/10.3389/FONC.2020.587386)
Malomouzh A, Ilyin V & & Nikolsky E 2019 Components of the GABAergic signaling in the peripheral cholinergic synapses of vertebrates: a review. Amino Acids 51 1093–1102. (https://doi.org/10.1007/s00726-019-02754-x)
McEvoy K & & Osborne LM 2019 Allopregnanolone and reproductive psychiatry: an overview. International Review of Psychiatry 31 237–244. (https://doi.org/10.1080/09540261.2018.1553775)
Melcangi RC & & Panzica GC 2014 Allopregnanolone: state of the art. Progress in Neurobiology 113 1–5. (https://doi.org/10.1016/j.pneurobio.2013.09.005)
Melfi S, Montt Guevara MM, Bonalume V, Ruscica M, Colciago A, Simoncini T & & Magnaghi V 2017 Src and phospho-FAK kinases are activated by allopregnanolone promoting Schwann cell motility, morphology and myelination. Journal of Neurochemistry 141 165–178. (https://doi.org/10.1111/jnc.13951)
Mellon SH, Griffin LD & & Compagnone NA 2001 Biosynthesis and action of neurosteroids. Brain Research. Brain Research Reviews 37 3–12. (https://doi.org/10.1016/S0165-0173(0100109-6)
Mody I 2001 Distinguishing between GABAA receptors responsible for tonic and phasic conductances. Neurochemical Research 26 907–913. (https://doi.org/10.1023/A:1012376215967)
Moffett SX, Klein EA, Brannigan G & & Martin JV 2019 L-3,3′,5-triiodothyronine and pregnenolone sulfate inhibit Torpedo nicotinic acetylcholine receptors. PLoS One 14 e0223272. (https://doi.org/10.1371/JOURNAL.PONE.0223272)
Morales-Ledesma L, Vieyra E, Ramírez DA, Trujillo A, Chavira R, Cárdenas M & & Domínguez R 2012 Effects on steroid hormones secretion resulting from the acute stimulation of sectioning the superior ovarian nerve to pre-pubertal rats. Reproductive Biology and Endocrinology 10 88. (https://doi.org/10.1186/1477-7827-10-88)
Morán C, Franco A, Morán JL, Handal A, Morales L & & Domínguez R 2005 Neural activity between ovaries and the prevertebral celiac-superior mesenteric ganglia varies during the estrous cycle of the rat. Endocrine 26 147–152. (https://doi.org/10.1385/ENDO:26:2:147)
Moritz CP 2017 Tubulin or not tubulin: heading toward total protein staining as loading control in Western blots. Proteomics 17 1600189. (https://doi.org/10.1002/pmic.201600189)
Morrow AL, Suzdak PD & & Paul SM 1987 Steroid hormone metabolites potentiate GABA receptor-mediated chloride ion flux with nanomolar potency. European Journal of Pharmacology 142 483–485. (https://doi.org/10.1016/0014-2999(8790094-X)
Natraj U & & Richards JS 1993 Hormonal regulation, localization, and functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinology 133 761–769. (https://doi.org/10.1210/endo.133.2.8344215)
O’Shaughnessy PJ & & Wathes DC 1985 Characteristics of bovine luteal cells in culture: morphology, proliferation and progesterone secretion in different media and effects of LH, dibutyryl cyclic AMP, antioxidants and insulin. Journal of Endocrinology 104 355–361. (https://doi.org/10.1677/JOE.0.1040355)
Ojeda SR & & Lara HE 1989 Role of the sympathetic nervous system in the regulation of ovarian function. In The Menstrual Cycle and Its Disorders. Berlin Heidelberg: Springer, pp. 26–32. (https://doi.org/10.1007/978-3-642-74631-4_4)
Orozco AV, Sosa Z, Fillipa V, Mohamed F & & Rastrilla AM 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. Journal of Endocrinology 191 587–598. (https://doi.org/10.1677/joe.1.06859)
Ottander U, Poromaa IS, Bjurulf E, Skytt A, Bäckström T & & Olofsson JI 2005 Allopregnanolone and pregnanolone are produced by the human corpus luteum. Molecular and Cellular Endocrinology 239 37–44. (https://doi.org/10.1016/j.mce.2005.04.007)
Palumbo MA, Salvestroni C, Gallo R, Guo AL, Genazzani AD, Artini PG, Petraglia F & & Genazzani AR 1995 Allopregnanolone concentration in hippocampus of prepubertal rats and female rats throughout estrous cycle. Journal of Endocrinological Investigation 18 853–856. (https://doi.org/10.1007/BF03349832)
Pasqualini JR & & Chetrite G 2008 The anti-aromatase effect of progesterone and of its natural metabolites 20α- and 5α-dihydroprogesterone in the MCF-7aro breast cancer cell line. Anticancer Research 28 2129–2133.
Pastelín CF, Rosas NH, Morales-Ledesma L, Linares R, Domínguez R & & Morán C 2017 Anatomical organization and neural pathways of the ovarian plexus nerve in rats. Journal of Ovarian Research 10 18. (https://doi.org/10.1186/s13048-017-0311-x)
Paul SM, Pinna G & & Guidotti A 2020 Allopregnanolone: from molecular pathophysiology to therapeutics. A historical perspective. Neurobiology of Stress 12 100215. (https://doi.org/10.1016/j.ynstr.2020.100215)
Paul SM & & Purdy RH 1992 Neuroactive steroids. FASEB Journal 6 2311–2322. (https://doi.org/10.1096/fasebj.6.6.1347506)
Pelegrina LT, Cáceres ARR, Giuliani FA, Asensio JA, Parborell F & & Laconi MR 2017 A single dose of allopregnanolone affects rat ovarian morphology and steroidogenesis. Reproduction 153 75–83. (https://doi.org/10.1530/REP-16-0463)
Pelegrina LT, Escudero C, Giuliani F, Cabrera R & & Laconi M 2015 Pharmacological effect of one icv dose of allopregnanolone in the female rat: behavioral profile. Brazilian Journal of Biological Sciences 2 39–50.
Pelletier G 2000 Localization of androgen and estrogen receptors in rat and primate tissues. Histology and Histopathology 15 1261–1270 doi:10.14670/HH-15.1261)
Pfaffl MW 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29 e45. (https://doi.org/10.1093/nar/29.9.e45)
Reddy DS & & Estes WA 2016 Clinical potential of neurosteroids for CNS disorders. Trends in Pharmacological Sciences 37 543–561. (https://doi.org/10.1016/J.TIPS.2016.04.003)
Riquelme R, Ruz F, Mayerhofer A & & Lara HE 2019 Role of ovarian sympathetic nerves and cholinergic local system during cold stress. Journal of Endocrinology 242 115–124. (https://doi.org/10.1530/JOE-19-0125)
Rivero-Gutiérrez B, Anzola A, Martínez-Augustin O & & De Medina FS 2014 Stain-free detection as loading control alternative to Ponceau and housekeeping protein immunodetection in Western blotting. Analytical Biochemistry 467 1–3. (https://doi.org/10.1016/j.ab.2014.08.027)
Robins A, Berkley KJ & & Sato Y 1992 Estrous cycle variation of afferent fibers supplying reproductive organs in the female rat. Brain Research 596 353–356. (https://doi.org/10.1016/0006-8993(9291572-V)
Romero-Calvo I, Ocón B, Martínez-Moya P, Suárez MD, Zarzuelo A, Martínez-Augustin O & & de Medina FS 2010 Reversible Ponceau staining as a loading control alternative to actin in Western blots. Analytical Biochemistry 401 318–320. (https://doi.org/10.1016/j.ab.2010.02.036)
Rupprecht R, Reul JMHM, Trapp T, Steensel van B, Wetzel C, Damm K, Zieglgänsberger W & & Holsboer F 1993 Progesterone receptor-mediated effects of neuroactive steroids. Neuron 11 523–530. (https://doi.org/10.1016/0896-6273(9390156-L)
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al.2012 Fiji: an open-source platform for biological-image analysis. Nature Methods 9 676–682. (https://doi.org/10.1038/nmeth.2019)
Shi Y, , Li Y, , Yin J, , Hu H, , Xue M, , Li X, , Cheng W, , Wang Y, , Li X, , Wang Y, et al.2019 A novel sympathetic neuronal GABAergic signalling system regulates NE release to prevent ventricular arrhythmias after acute myocardial infarction. Acta Physiologica 227 e13315. (https://doi.org/10.1111/apha.13315)
Shu HJ, Eisenman LN, Jinadasa D, Covey DF, Zorumski CF & & Mennerick S 2004 Slow actions of neuroactive steroids at GABAA receptors. Journal of Neuroscience 24 6667–6675. (https://doi.org/10.1523/JNEUROSCI.1399-04.2004)
Si W, Li H, Kang T, Ye J, Yao Z, Liu Y, Yu T, Zhang Y, Ling Y, Cao H, et al.2020 Effect of GABA-T on reproductive function in female rats. Animals 10 567. (https://doi.org/10.3390/ani10040567)
Simoni M, Gromoll J & & Nieschlag E 1997 The Follicle-Stimulating Hormone Receptor: Biochemistry, Molecular Biology, Physiology, and Pathophysiology. Endocrine Reviews 18 7 39–7 73. (https://doi.org/10.1210/edrv.18.6.0320)
Sosa ZY, Casais M, Rastrilla AM & & Aguado L 2000 Adrenergic influences on coeliac ganglion affect the release of progesterone from cycling ovaries: characterisation of an in vitro system. Journal of Endocrinology 166 307–318. (https://doi.org/10.1677/joe.0.1660307)
Stocco C, Telleria C & & Gibori G 2007 The molecular control of corpus luteum formation, function, and regression. Endocrine Reviews 28 117–149. (https://doi.org/10.1210/er.2006-0022)
Stocco CO, Chedrese J & & Deis RP 2001 Luteal expression of cytochrome P450 side-chain cleavage, steroidogenic acute regulatory protein, 3β-hydroxysteroid dehydrogenase, and 20α-hydroxysteroid dehydrogenase genes in late pregnant rats: effect of luteinizing hormone and RU486. Biology of Reproduction 65 1114–1119. (https://doi.org/10.1095/BIOLREPROD65.4.1114)
Sugino N, Telleria CM & & Gibori G 1997 Progesterone inhibits 20α-hydroxysteroid dehydrogenase expression in the rat corpus luteum through the glucocorticoid receptor. Endocrinology 138 4497–4500. (https://doi.org/10.1210/endo.138.10.5572)
Telleria CM, Stocco CO, Stati AO & & Deis RP 1999 Progesterone receptor is not required for progesterone action in the rat corpus luteum of pregnancy. Steroids 64 760–766. (https://doi.org/10.1016/S0039-128X(9900061-6)
Uchida S & & Kagitani F 2015 Autonomic nervous regulation of ovarian function by noxious somatic afferent stimulation. Journal of Physiological Sciences 65 1–9. (https://doi.org/10.1007/s12576-014-0324-9)
Vallcaneras S, Morales L, Delsouc MB, Ramirez D, Filippa V, Fernández M, Telleria CM & & Casais M 2022 Interplay between nitric oxide and gonadotrophin-releasing hormone in the neuromodulation of the corpus luteum during late pregnancy in the rat. Reproductive Biology and Endocrinology 20 19. (https://doi.org/10.1186/s12958-022-00894-6)
Vega Orozco AV, Sosa Z, Delgado S, Casais M & & Rastrilla AM 2010 Involvement of ganglionic cholinergic receptors on the steroidogenesis in the luteal phase in rat. Journal of Steroid Biochemistry and Molecular Biology 120 45–52. (https://doi.org/10.1016/j.jsbmb.2010.03.040)
Vieyra-Valdez E, Garcia-Tabla JC, Zarco-Juarez HA, Calderon-Ramos R, Morales-Ledesma L & & Dominguez R 2020 SUN-251 the effects of unilateral vagotomy in female rats with blockade of the muscarinic system of the suprachiasmatic nucleus on ovulation and estradiol serum levels. Journal of the Endocrine Society 4(Supplement 1). (https://doi.org/10.1210/JENDSO/BVAA046.1130)
Wetendorf M, Li R, Wu S-P, Liu J, Creighton CJ, Wang T, Janardhan KS, Willson CJ, Lanz RB, Murphy BD, et al.2019 Constitutive expression of the progesterone receptor isoforms promotes hormone-dependent development of ovarian neoplasms. bioRxiv 816934. (https://doi.org/10.1101/816934)
Wolff JR, Kása P, Dobó E, Párducz Á & & Joó F 1992 The GABAergic innervation of paravertebral sympathetic ganglia. In GABA Outside the CNS. Berlin Heidelberg: Springer, pp. 45–63. (https://doi.org/10.1007/978-3-642-76915-3_4)
Online ISSN: 1479-6805
Print ISSN: 0022-0795
CONTACT US
Bioscientifica Ltd | Starling House | 1600 Bristol Parkway North | Bristol BS34 8YU | UK
Bioscientifica Ltd | Registered in England no 3190519