The Neural Signals of the Superior Ovarian Nerve Modulate in an Asymmetric Way the Ovarian Steroidogenic Response to the Vasoactive Intestinal Peptide

Rosas, Gabriela; Linares, Román; Ramírez, Deyra A.; Vieyra, Elizabeth; Hernández, Adán; Domı́nguez, Roberto; Morales‐Ledesma, Leticia

doi:10.3389/fphys.2018.01142

Cited by 16 publications

(14 citation statements)

References 56 publications

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“…These results suggest that the asymmetric response of the ovaries to VIP treatment is modulated, at least in part, by the innervation received by each ovary [ 51 ]. The effects of VIP on steroid hormones release by the ovaries are modulated by neural signals arriving through the SON (NE and/or NPY) ([ 52 ], in press). According to Lara et al [ 31 ] there is no information on whether VIP-containing nerves in the SON or VIP-producing ovarian cells remain functional in GTD-treated rats.…”

Section: Discussionmentioning

confidence: 99%

Pharmacological sympathetic denervation prevents the development of polycystic ovarian syndrome in rats injected with estradiol valerate

Espinoza¹,

Alvarado²,

Venegas

et al. 2018

Reprod Biol Endocrinol

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BackgroundThe injection of estradiol valerate in female rats induces polycystic ovary syndrome, which is characterized by polycystic ovaries, anovulation, and hyperandrogenism. These characteristics have been associated with an increase in the ovarian concentration of norepinephrine, which occurs before establishing the polycystic ovary syndrome. The bilateral section of the superior ovarian nerve restores ovarian functions in animals with polycystic ovary syndrome. The superior ovarian nerve provides norepinephrine and vasoactive intestinal peptide to the ovary. An increase in the activity of both neurotransmitters has been associated with the development of polycystic ovary syndrome. The purpose of the present study was analyzed the participation of the noradrenergic nervous system in the development of polycystic ovary syndrome using guanethidine as a pharmacological tool that destroys peripheral noradrenergic nerve fibers.MethodsFourteen-day old female rats of the CIIZ-V strain were injected with estradiol valerate or vehicle solution. Rats were randomly allotted to one of three guanethidine treatment groups for denervation: 1) guanethidine treatment at age 7 to 27-days, 2) guanethidine treatment at age 14 to 34- days, and 3) guanethidine treatment at age 70 to 90- days. All animals were sacrificed when presenting vaginal oestrus at age 90 to 94-days. The parameters analyzed were the number of ova shed by ovulating animals, the ovulation rate (i.e., the numbers of ovulating animals/the numbers of used animals), the serum concentration of progesterone, testosterone, oestradiol and the immunoreactivity for tyrosine hydroxylase enzyme. All data were analyzed statistically. A p-value of less than 0.05 was considered significant.ResultsOur results show that the elimination of noradrenergic fibers before the establishment of polycystic ovary syndrome prevents two characteristics of the syndrome, blocking of ovulation and hyperandrogenism. We also found that in animals that have already developed polycystic ovary syndrome, sympathetic denervation restores ovulatory capacity, but it was not as efficient in reducing hyperandrogenism.ConclusionThe results of the present study suggest that the noradrenergic fibers play a stimulant role in the establishment of polycystic ovary syndrome.

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Section: Discussionmentioning

confidence: 99%

Pharmacological sympathetic denervation prevents the development of polycystic ovarian syndrome in rats injected with estradiol valerate

Espinoza¹,

Alvarado²,

Venegas

et al. 2018

Reprod Biol Endocrinol

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“…Growing evidence suggests that ovarian function is under the control of the autonomic nervous system, which works in parallel with the hypothalamic-pituitarygonadal axis (HPG axis) (Ojeda 2012, Uchida 2015, Pastelín et al 2017. Sympathetic nerves originating in the celiac ganglia project to the ovarian follicles, principally to its theca layer, and its transmitter, noradrenalin (NA), then acts on beta-adrenergic receptors located in theca and granulosa cells (Aguado 2002, Lara et al 2002, Manni et al 2005, Rosas et al 2018. Both neural and endocrine signals converge to regulate steroidogenesis and ovarian follicular development.…”

Section: Introductionmentioning

confidence: 99%

Role of ovarian sympathetic nerves and cholinergic local system during cold stress

Riquelme

Ruz

Mayerhofer

et al. 2019

Journal of Endocrinology

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An increase in the sympathetic tone in the rat ovary induces a polycystic ovary (PCOS-like) phenotype. No information exists about its impact on fertility. In contrast, increased follicular development and improved fertility in rats were found after pharmacological inhibition of acetylcholinesterase, which increased intraovarian acetylcholine (ACh). Now, we studied the impact of sympathetic stress, followed by a recovery period without stress, on the cholinergic and noradrenergic systems of the rat ovary and on fertility. To activate ovarian sympathetic nerves, female Sprague–Dawley rats were exposed to cold stress (4°C/3 h day for 28 days; first period), followed by a 28-day period without cold stress (second period). No changes in estrous cyclicity during the first period was found. At the end of this period, ovarian levels of NA and ACh were increased. Morphometric analysis showed lower numbers of secondary and antral follicles, enhanced follicular atresia and fewer corpora lutea. Plasma progesterone was lower and testosterone was higher than that in controls. At end of the second period, ovarian ACh levels had returned to control levels, but NA levels remained elevated. The second period was also characterized by the presence of cystic follicles in the ovary, by elevated plasma testosterone and estradiol levels, while progesterone levels were decreased. Estrous cyclicity and ovulation during that period were irregular and fertility decreased. Thus, cold stress initially activated both ovarian noradrenergic and cholinergic system. After stress, the ovary did not fully recover and activation of the noradrenergic system persisted and correlated with cystic ovarian morphology and decreased fertility.

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“…All the rats were hemiovariectomized (ULO) during the surgical denervation process (or sham operation) to eliminate a putative effect of the contralateral ovary on the hypothalamus. Some asymmetry was described between the right and left ovary regarding the hypothalamic control of the ovary (Pastelin et al, 2017; Rosas et al, 2018). It was described that each ovary has a different capacity to release steroids; thus, a hormonal signal from one ovary could affect the contralateral ovary by altering the hormonal signals that after arrive to the ovary through the circulation.…”

Section: Methodsmentioning

confidence: 99%

Effect of Superior Ovarian Nerve and Plexus Nerve Sympathetic Denervation on Ovarian-Derived Infertility Provoked by Estradiol Exposure to Rats

et al. 2019

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Sympathetic innervation of the ovary in rodents occurs via two routes: the superior ovarian nerve (SON), which runs along the ovarian ligament, and the plexus nerve (PN), which is mainly associated with the vasculature. SON and ovarian norepinephrine (NE) levels play a major role in regulating ovarian cystic health. Although it was previously described that the polycystic ovarian phenotype (PCO) is causally related to hyperstimulation of the sympathetic nerves of the ovary, much less is known, however, regarding the role of PN in ovarian physiology. We studied the role of SON and PN in relation to the maintenance of the PCO phenotype induced in the rat by exposure to estradiol valerate (EV). EV exposure at 24 days old (juvenile exposure) increases NE in the ovary for up to 90 days after EV injection. SON or PN denervation (SONX and PNX) decreased NE. SONXreversed the acyclic condition from 30 days after surgery ( p < 0.05), but PNXdid not. SONX was more effective than PNX to downregulate the increased number of cysts induced by EV, with the presence of the corpora lutea (CL, signifying ovulation) in the SONX group. Seventy percent of SONX rats presented with pregnancy at 60 days post-EV (6 of the 7 sperm-positive rats were pregnant); however, SONX rats had a reduced number (half) of pups compared with vehicle-treated rats and 60% more pups than EV rats. These data suggest that the SON plays a predominant role in follicular development, ovulation and pregnancy during ovarian diseases.

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The Neural Signals of the Superior Ovarian Nerve Modulate in an Asymmetric Way the Ovarian Steroidogenic Response to the Vasoactive Intestinal Peptide

Cited by 16 publications

References 56 publications

Pharmacological sympathetic denervation prevents the development of polycystic ovarian syndrome in rats injected with estradiol valerate

Pharmacological sympathetic denervation prevents the development of polycystic ovarian syndrome in rats injected with estradiol valerate

Role of ovarian sympathetic nerves and cholinergic local system during cold stress

Effect of Superior Ovarian Nerve and Plexus Nerve Sympathetic Denervation on Ovarian-Derived Infertility Provoked by Estradiol Exposure to Rats

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