- Open Access
The celiac ganglion modulates LH-induced inhibition of androstenedione release in late pregnant rat ovaries
© Casais et al; licensee BioMed Central Ltd. 2006
- Received: 04 August 2006
- Accepted: 21 December 2006
- Published: 21 December 2006
Although the control of ovarian production of steroid hormones is mainly of endocrine nature, there is increasing evidence that the nervous system also influences ovarian steroidogenic output. The purpose of this work was to study whether the celiac ganglion modulates, via the superior ovarian nerve, the anti-steroidogenic effect of LH in the rat ovary. Using mid- and late-pregnant rats, we set up to study: 1) the influence of the noradrenergic stimulation of the celiac ganglion on the ovarian production of the luteotropic hormone androstenedione; 2) the modulatory effect of noradrenaline at the celiac ganglion on the anti-steroidogenic effect of LH in the ovary; and 3) the involvement of catecholaminergic neurotransmitters released in the ovary upon the combination of noradrenergic stimulation of the celiac ganglion and LH treatment of the ovary.
The ex vivo celiac ganglion-superior ovarian nerve-ovary integrated system was used. This model allows studying in vitro how direct neural connections from the celiac ganglion regulate ovarian steroidogenic output. The system was incubated in buffer solution with the ganglion and the ovary located in different compartments and linked by the superior ovarian nerve. Three experiments were designed with the addition of: 1) noradrenaline in the ganglion compartment; 2) LH in the ovarian compartment; and 3) noradrenaline and LH in the ganglion and ovarian compartments, respectively. Rats of 15, 19, 20 and 21 days of pregnancy were used, and, as an end point, the concentration of the luteotropic hormone androstenedione was measured in the ovarian compartment by RIA at various times of incubation. For some of the experimental paradigms the concentration of various catecholamines (dihydroxyphenylalanine, dopamine, noradrenaline and adrenaline) was also measured in the ovarian compartment by HPLC.
The most relevant result concerning the action of noradrenaline in the celiac ganglion was found on day 21 of pregnancy resulting in the inhibition of androstenedione release from the ovarian compartment. In addition on day 15 of pregnancy, LH placed in the ovarian compartment led to an inhibition of the release of androstenedione, and this inhibitory effect was further reinforced by the joint action of noradrenaline in the celiac ganglion and LH in the ovary. The levels of catecholamines in the ovarian compartment showed differences among the experiments; of significance, the joint treatment of noradrenaline in the celiac ganglion and LH in the ovary resulted in a remarkable increase in the ovarian levels of noradrenaline and adrenaline when compared to the effect achieved by either one of the compounds added alone.
Our results demonstrate that the noradrenergic stimulation of the celiac ganglion reinforces the LH-induced inhibition of androstenedione production by the ovary of late pregnant rats, and that this effect is associated with marked changes in the release of catecholamines in the ovary.
- Luteinizing Hormone
- Corpus Luteum
- Progesterone Production
The ovary is innervated by the ovarian plexus nerve and the superior ovarian nerve , the latter being the most related to ovarian steroidogenesis . Most of the fibers of the superior ovarian nerve come from the postganglionic sympathetic neurons of the celiac ganglion . They directly innervate the ovarian theca and secondary interstitial cells and exert an indirect action on the luteal cells . Neurotransmitters of peptidergic and catecholaminergic nature have been detected in the ovarian nervous terminals of the superior ovarian nerve , some of which are also present in the celiac ganglion . Moreover, the presence of intrinsic ovarian neurons in several mammalian species, including rats, has been demonstrated [7–9]. Among the neurotransmitters expressed in these cells are nitric oxide (NO), neuropeptide Y (NPY) and catecholamines . The celiac ganglion is part of the sympathetic prevertebral chain possessing a great variety of specific receptors and neurotransmitters such as catecholamines, neuropeptides, and nitric oxide [3, 11, 12], and constitutes a modulation center in the pathway of the afferent and efferent fibers between the central nervous system and the ovary . The main preganglion neurotransmitter of the celiac ganglion is acetylcholine [13–15], yet the celiac ganglion-mesenteric complex also contain α and β adrenergic receptors and is innervated by fibers of adrenergic nature that come from other preaortic ganglia [6, 16]. The presence of such receptors in the celiac ganglion has been demonstrated physiologically in adult [17, 18] and prepubertal rats .
Our laboratory has previously demonstrated that modifications in the adrenergic activity of the celiac ganglion results in an altered capacity of the ovary of pregnant rats to produce progesterone , suggesting that the celiac ganglion-superior ovarian nerve-ovarian axis provides a direct link between the autonomic nervous system and the physiology of pregnancy (reviewed in ). More recently, we have also shown that modifications in the cholinergic input at the celiac ganglion also led, via the superior ovarian nerve, to modifications in ovarian steroidogenesis . Adding a level of complexity to the understanding of the neuroendocrine interactions between the celiac ganglion and the physiology of the ovary we showed that modifications in the hormonal environment that surrounds the celiac ganglion affects its behavior, ultimately affecting ovarian steroidogenesis [2, 21].
Androstenedione is a major luteotropic hormone for the pregnant rat ovary. The involvement of androstenedione is widely accepted in the maintenance of luteal function upon its intraluteal conversion to estradiol . Moreover, it has been demonstrated in different experimental schemes that androstenedione has also a direct luteotropic effect stimulating luteal progesterone production – an effect not mediated by its previous conversion to estradiol – [23–25], and interfering with the programmed cell death process that accompanies the regression of the corpus luteum . More recently, our laboratory demonstrated that androstenedione can also indirectly exert a luteotropic effect by regulating the activity of the celiac ganglion .
In pregnant rats LH has a peculiar dual effect controlling ovarian function. During the first half of pregnancy LH is essential, together with prolactin, to sustain the corpus luteum , whereas its increase in late pregnancy is detrimental for luteal function, promoting the regression of the corpora lutea that accompanies parturition [26–28]. Considering the relevant role of androstenedione in rat pregnancy and the fine modulatory control exerted by the peripheral neural system throughout the celiac ganglion on pregnant rat ovarian steroidogenesis, we set up to study whether the celiac ganglion modulates, via the superior ovarian nerve, the anti-steroidogenic effect of LH in late pregnant rats as assessed by measuring the production of androstenedione by the ovary.
Pregnant (day 0 = sperm positive) Holtzman rats were used in the studies. They were housed under controlled conditions of light (lights on 07:00 – 19:00 h) and temperature (24 ± 2°C) with free access to standard rat chow and water. Animals were handled in accordance with to the procedures approved in the UFAW Handbook on the Care and Management of Laboratory Animals . The experimental protocol was approved by the University of San Luis Animal Care and Use Committee (ordinance CD 006/02).
The following chemicals were purchased from Sigma Chemical Co. (St. Louis, MO, USA): L-D-noradrenaline hydrochloride (NA), dextrose, ascorbic acid, bovine serum albumin fraction V (BSA), and luteinizing hormone (LH). 1, 2, 6, 7-[3H] androst-4-ene-3, 17-dione (115.0 Ci/mmol) was provided by New England Nuclear Products (Boston, MA, USA). Other reagents were of analytical grade.
The samples of liquid from the ovarian compartment were stored at -20°C until hormone assay. Androstenedione was measured by radioimmunoassay (RIA); the variability and cross-reaction of this RIA have been previously reported . The assay sensitivity was less than 10 pg/ml androstenedione and the intra-assay coefficient of variation was less than 10.0%. The results were expressed as pg of androstenedione per mg of ovarian tissue (A2 pg/mg ovary) against time of incubation. The corresponding corrections were made in all cases, taking into consideration the volume extracted in each tested period.
Determination of catecholamines by HPLC
The catecholamines measured were dihydroxyphenylalanine (DOPA), dopamine (DA), noradrenaline (NA) and adrenaline (A). The catechols in 20 μl aliquots of liquid from the ovarian cuvette (180 min) were partially purified by batch alumina extraction, separated by reverse-phase high-pressure liquid chromatography using a 4.6 mm × 250 mm Zorbax RxC18 column (Du Pont, USA) and quantified by current produced upon exposure of the column effluent to oxidizing and then reducing potentials in series using a triple-electrode system (Coulochem II, ESA, Bedford, MA) . Recovery through the alumina extraction step averaged 70–80% for catecholamines and 45–55% for DOPA. Catecholamine concentrations, in each sample, were corrected for recovery of an internal standard dihydroxybenzylamine. Levels of DOPA were further corrected for differences in recovery of the internal standard and this catechol in a mixture of external standards. The results were expressed as pg of catecholamine per mg of ovarian tissue/180 min incubation (Catechol pg/mg ovary/180 min incubation).
For multiple comparisons made along the time of incubation, repeated measures analysis of variance followed by Tukey's test was used. Instead, for multiple comparisons not involving repeated measures, one-way analysis of variance followed by Tukey's test was utilized. A difference was considered to be statistically significant at P < 0.05 .
Effect of the addition of noradrenaline in the ganglion compartment on the levels of androstenedione accumulated in the ovarian compartment of celiac ganglion-superior ovarian nerve-ovary preparations obtained from animals sacrificed on days 19, 20, and 21 of pregnancy
Effect of the addition of noradrenaline in the ganglion compartment and LH in the ovarian compartment on the levels of androstenedione accumulated in the ovarian compartment of celiac ganglion-superior ovarian nerve-ovary preparations obtained on day 15 of pregnancy
Effect of the addition of noradrenaline in the ganglion compartment and LH in the ovarian compartment on the levels of catecholaminergic neurotransmitters released in the ovarian compartment of celiac ganglion-superior ovarian nerve-ovary preparations obtained on day 15 of pregnancy
The celiac ganglion-superior ovarian nerve-ovary system utilized in this study provides an adequate ex vivo model with good resemblance to the in vivo conditions, and allows discerning endocrine-neural interactions about the regulation of the physiology of the ovary. In the present study, using this experimental approach, we present evidence demonstrating that the capacity of the ovary of late pregnant rats to produce androstenedione is modulated by neural inputs coming from the celiac ganglion via the superior ovarian nerve. This study also confirms that there is a functional inter-relationship between the adrenergic inputs on the celiac ganglion and the endocrine action of LH in the ovary and that the response of the ovary to neural stimulation varies throughout pregnancy. Furthermore, these results contribute to the understanding of the role of the peripheral nervous system in ovarian physiology and can add to the understanding of certain pathologic states of reproduction that cannot be solely explained by hormonal causes, such as polycystic ovary syndrome, whose development is profoundly influenced by the sympathetic nervous system .
In celiac ganglion-superior ovarian nerve-ovary preparations obtained on days 15, 19, and 20 of pregnancy noradrenergic stimulation of the celiac ganglion did not largely modify the capacity of the ovary to produce androstenedione; however, there was a marked inhibition in the capacity to accumulate androstenedione in the ovaries of preparations taken from day 21 pregnant rats that had been subjected to noradrenergic stimulation of the celiac ganglion. It is possible that ovaries of day 21 pregnant rats respond strongly to neural inputs because androstenedione most probably originates in the interstitial cells and the theca cells of growing preovulatory follicles found in the ovary of rats at term  and that are directly innervated by terminals from the superior ovarian nerve . The inhibitory effect of the noradrenergic stimulation of the celiac ganglion on the androstenedione producing capacity of late pregnant ovaries was further visualized by the enhancement of the anti-steroidogenic effect of LH. We have previously shown that adding LH to the ovarian compartment of celiac ganglion-superior ovarian nerve-ovary preparations obtained from day 15 pregnant rats did not affect progesterone production, yet when combined with noradrenergic stimulation of the celiac ganglion led to a decrease in the ovarian progesterone producing capacity . Overall results from the present work and previous work in our laboratory  demonstrate that the anti-steroidogenic effect of LH in late pregnant rat ovaries is modulated by the activity of the celiac ganglion. Whereas LH alone may be sufficient to impair the capacity of the ovary to produce androstenedione, it may need the contribution of neural inputs coming from the celiac ganglion via the superior ovarian nerve to also impair progesterone production.
The luteotropic effect of androstenedione in pregnant rats has been widely demonstrated in different experimental schemes [21, 23, 25]. Androstenedione appears to be a potent tropic hormone that assists corpus luteum function particularly at the end of pregnancy when the gland approaches its regression. This is supported by the fact that when the ovary is populated with corpora lutea that are approaching the time of regression (day 21 of pregnancy), they become more responsive to androstenedione in terms of progesterone production in vivo and in vitro . Our current data show that ovaries taken at end of pregnancy (day 21) are capable of producing more androstenedione in vitro than ovaries obtained on previous days of pregnancy. Consequently, in a physiological setting, it is possible that the ovarian production of androstenedione needs to be limited in order to ensure the regression of the corpus luteum. Neural inputs coming from the celiac ganglion may be in charge of fine-tuning, together with LH, the production of androstenedione at the end of pregnancy.
In the current study we also provide evidence that four metabolically related catecholamines (dihydroxyphenylalanine, dopamine, noradrenaline and adrenaline) are detected in the ovarian incubation compartment of the celiac ganglion-superior ovarian nerve-ovary tissue preparation. The increase observed in the accumulation of noradrenaline and adrenaline within the ovarian compartment upon the joint adrenergic stimulation of the celiac ganglion and the endocrine ovarian effect of LH was particularly dramatic, suggesting that they may be involved in the anti-steroidogenic effect of LH at the end of pregnancy in rats. It is not possible from our experiments to know, however, the source or location of these amines. LH may locally induce the release of catecholamines either from: i) the nervous terminals coming from the peripheral innervation (pool of catecholamines synthesized in the celiac ganglion or in the superior ovarian nerve terminals) ; ii) the intrinsic neurons of the ovary (structures from a network of neurons developed as a ganglion and located in the meso-ovarium and hilium and neurons mostly isolated in the cortex and medulla) ; or iii) a combination of both.
It was noticeable that the anti-steroidogenic effect of LH on androstenedione production was associated with elevated adrenaline and noradrenaline in the ovarian compartment; this observation is controversial because of the fact that these two catecholamines have been usually reported as favoring steroidogenesis . It is possible that any action of the catecholamines in the ovary in the presence of elevated concentrations of LH could be prevented by a desensitizing effect of the gonadotropin in the coupling of beta adrenergic receptors to adenylate cyclase . We should also consider that probably other neurotransmitters not analyzed in this work, such as NO [34, 35], GnRH [36, 37] or neuropeptides such as NPY and substance P (SP)  play roles together with catecholamines in the neural control of the function of the ovary during pregnancy; consequently they may mediate the anti-steroidogenic effect of LH in the presence of elevated catecholamines.
There is ample evidence suggesting that the sympathetic nervous system is involved in pathologies associated to the reproductive system. Evidence has been accumulating supporting the participation of sympathetic nerves in the function of the ovary under normal and pathological conditions such as polycystic ovarian syndrome [32, 39]. It is overall suggested that chronic increase in ovarian sympathetic nerve activity is related to changes in follicular development, producing an anovulatory ovary with cysts, but that the process can be reversed by attenuation of the sympathetic activity . Polycystic ovarian syndrome is a common cause of infertility in women during their reproductive years and is associated with cystic ovaries and increased capacity to produce androgens. Whether a dysregulation in the activity of the celiac ganglion and the superior ovarian nerve is involved in the dysregulated androgen production observed in polycystic ovary syndrome remains an attractive subject for future investigations. The results of the present study demonstrating that adrenergic activation of the celiac ganglion impacts ovarian androgen production in rats, certainly stimulates such future investigations.
Our results demonstrate that in the ovary of late pregnant rats the production of androstenedione is inhibited upon the joint action of noradrenaline in the celiac ganglion and LH in the ovary, and that this effect is associated with marked changes in the release of catecholamines in the ovary.
This manuscript is dedicated to the memory of Dr. Luis I. Aguado (1946–2003) and was supported by Grant 9302 from Universidad Nacional de San Luis, Argentina. We express our appreciation to the staff members of the Centro de Investigaciones Endocrinológicas (CONICET), Hospital de Niños Ricardo Gutierrez, Buenos Aires, Argentina for the measurements of catecholamines. We also thank Dr. R.P. Deis from the Laboratorio de Reproducción y Lactancia (LARLAC-CONICET) who provided the androstenedione antiserum, Ing. Mario Baudino for informatic assistance, Lic. Fabricio Penna for assistance with the statistics, Luis Villegas for technical support, and Dr. Barbara Goodman for critical revision of the manuscript. This work is part of the doctoral thesis of Marilina Casais.
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