A Role for Catecholaminergic Neurons in the Suppression of Pulsatile Luteinizing Hormone Secretion in the Prepubertal Ewe Lamb

Brango, C.; Whisnant, Scott; Goodman, Robert L.

doi:10.1159/000125627

Cited by 12 publications

(9 citation statements)

References 27 publications

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“…In mammals, DA has been shown in several species to be involved in the modulation of pulsatile LH release through direct or indirect actions. This has been extensively studied in sheep, in which DA participates in the inhibition of gonadotrophic activity before puberty as well as in the adult during seasonal anestrus by acting on GnRH neurons [59][60][61]. A direct inhibitor action of DA at the pituitary level was reported in the rabbit, in which DA inhibits GnRH-stimulated LH release in normal as well as in stalk-sectioned animals [62].…”

Section: Discussionmentioning

confidence: 99%

Dopamine Inhibits Luteinizing Hormone Synthesis and Release in the Juvenile European Eel: A Neuroendocrine Lock for the Onset of Puberty1

Vidal¹,

Pasqualini²,

Belle³

et al. 2004

Biology of Reproduction

154

113

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In various adult teleost fishes, LH ovulatory peak is under a dual neurohormonal control that is stimulatory by GnRH and inhibitory by dopamine (DA). We investigated whether DA could also be involved in the inhibitory control of LH at earlier steps of gametogenesis by studying the model of the European eel, Anguilla anguilla, which remains at a prepubertal stage until the oceanic reproductive migration. According to a protocol previously developed in the striped bass, eels received sustained treatments with GnRH agonist (GnRHa), DA-receptor antagonist (pimozide), and testosterone (T) either alone or in combination. Only the triple treatment with T, GnRHa, and pimozide could trigger dramatic increases in LH synthesis and release as well as in plasma vitellogenin levels and a stimulation of ovarian vitellogenesis. Thus, in the prepubertal eel, removal of DA inhibition is required for triggering GnRH-stimulated LH synthesis and release as well as ovarian development. To locate the anatomical support for DA inhibition, the distribution of tyrosine hydroxylase (TH) in the brain and pituitary was studied by immunocytochemistry. Numerous TH-immunoreactive cell bodies were observed in the preoptic anteroventral nucleus, with a dense tract of immunoreactive fibers reaching the pituitary proximal pars distalis, where the gonadotrophs are located. This pathway corresponds to that mediating the inhibition of LH and ovulation in adult teleosts. To our knowledge, this is the first demonstration of a pivotal role for DA in the control of LH and puberty in a juvenile teleost. These data support the view that DA inhibition on LH secretion is an ancient evolutionary component in the neuroendocrine regulation of reproduction that may have been partially maintained throughout vertebrate evolution.

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Section: Discussionmentioning

confidence: 99%

Dopamine Inhibits Luteinizing Hormone Synthesis and Release in the Juvenile European Eel: A Neuroendocrine Lock for the Onset of Puberty1

Vidal¹,

Pasqualini²,

Belle³

et al. 2004

Biology of Reproduction

154

113

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“…Other neurotransmitters (e.g. catecholamines) [41] undoubtedly act in concert with opioids to inhibit LH pulses in prepubertal male and female lambs.…”

Section: Discussionmentioning

confidence: 99%

Opioid Inhibition of Luteinizing Hormone Secretion Compared in Developing Male and Female Sheep

Wood

I’Anson²,

Ebling³

et al. 1992

Neuroendocrinology

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The sheep exhibits a marked sex difference in the timing of the pubertal increase in luteinizing hormone (LH). Male lambs undergo a reduction in sensitivity to inhibitory steroid feedback, leading to an increase in LH by 10 weeks of age, but females remain hypersensitive until 30 weeks of age. Endogenous opioids suppress LH secretion in the female lamb prepubertally and in adult male and female sheep. It has been suggested that a reduction in opioid inhibition of LH secretion is the signal to time puberty. Therefore, if a decrease in opioid tone occurs during sexual maturation, it should begin earlier in the male lamb than in the female. The objective of this study was to compare opioid inhibition of LH secretion in male and female lambs in relation to the timing of puberty. Our approach was to examine the response to the opioid antagonist naloxone at various ages in both sexes. To determine the timing of the pubertal LH rise in the presence of constant inhibitory steroid feedback, male and female lambs (n = 5 each) were gonadectomized at 3 weeks of age and implanted with a Silastic capsule of estradiol. They were then challenged with naloxone at 5, 11, and 23 weeks of age; blood samples were collected every 12 min for 8 hours, and lambs received naloxone (1 mg/kg i.v.) at hours 4, 5, 6, and 7. Mean LH before and during naloxone treatment was compared at each age. During the 4-hour pretreatment period, no LH pulses were evident in prepubertal females at 5, 11, or 23 weeks of age, and mean LH remained low (0.8 ± 0.05 ng/ml). In prepubertal males, mean LH was 1.5 ± 0.2 ng/ml at 5 weeks of age and rose at puberty to 6.8 ± 0.3 ng/ml by 23 weeks of age. Despite this sex difference in the timing of the pubertal LH rise, neither male nor female lambs increased LH secretion in response to naloxone until 23 wseeks of age. At this time, mean LH in females increased by 3.2 ± 0.7 ng/ml over pretreatment values in response to naloxone and increased by 5.0 ± 0.9 ng/ml in males. Thus, although opioid tone is expressed prepubertally in the female lamb, it is not evident until after puberty in the male. In a second experiment, we determined if increasing the concentration of estradiol in circulation affects the gonadotropin response to naloxone. LH pulse frequency during naloxone treatment did not differ in ovariectomized prepubertal females bearing 3-, 10-, or 30-mm implants of estradiol, although the larger implants of estradiol suppressed LH during the pretreatment period. These data suggest that increasing steroid negative feedback does not increase opioid tone, thereby reducing the gonadotropin response to a single dose of naloxone. Together, these studies provide evidence that in sheep the timing of the pubertal rise in LH secretion is not causally related to changes in opioid inhibition; rather, other factors including age or season may influence when endogenous opioids begin to serve a major role in modulating gonadotropin secretion in this species.

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“…In mammals, DA has been shown to be involved in the modulation of pulsatile LH release in some species. This effect has been extensively studied in sheep, in which DA appears to participate in the inhibition of gonadotropic activity before puberty,55 as well as in the adult during seasonal anestrus (for review, see ref. 56).…”

Section: Inhibitory Neuroendocrine Role For Dopamine In the Control Omentioning

confidence: 99%

Dopaminergic Inhibition of Reproduction in Teleost Fishes: Ecophysiological and Evolutionary Implications

Dufour¹,

Weltzien²,

Sébert³

et al. 2005

Annals of the New York Academy of Sciences

155

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In many teleosts, dopamine (DA) exerts direct inhibitory control on gonadotropes, counteracting the stimulatory effect of gonadotropin-releasing hormone (GnRH) on gonadotropin release. This dual control by GnRH and DA has been demonstrated in various adult teleosts and has major implications for aquaculture. Because of its unique life cycle, the European eel has provided a powerful model for demonstrating the key role of DA in the control of puberty. Data from tetrapods suggest that the inhibitory role of DA on reproduction is not restricted to the teleosts. Thus, DA inhibitory control could represent an ancient evolutionary component in the neuroendocrine regulation of reproduction that may have been differentially maintained throughout vertebrate evolution. The intensity of DA inhibition, its main site of action, and its involvement in the control of puberty, seasonal reproduction, ovulation, spermiation, or even sex change may differ among classes of vertebrates, as well as within smaller phylogenetic units such as teleosts or mammals. An inhibitory role for DA has been reported also in some invertebrates, indicating that neuronal DA pathways may have been recruited in various groups of metazoa to participate in the control of reproduction. In addition to the incontestable GnRH neurons, the recruitment of DA neurons for the neuroendocrine control of reproduction provides an additional brain pathway for the integration of various species-specific, internal, and environmental cues. In teleosts, the plasticity of the DA neuroendocrine role may have contributed to their large diversity of biological cycles and to their successful adaptation to various environments.

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A Role for Catecholaminergic Neurons in the Suppression of Pulsatile Luteinizing Hormone Secretion in the Prepubertal Ewe Lamb

Cited by 12 publications

References 27 publications

Dopamine Inhibits Luteinizing Hormone Synthesis and Release in the Juvenile European Eel: A Neuroendocrine Lock for the Onset of Puberty1

Dopamine Inhibits Luteinizing Hormone Synthesis and Release in the Juvenile European Eel: A Neuroendocrine Lock for the Onset of Puberty1

Opioid Inhibition of Luteinizing Hormone Secretion Compared in Developing Male and Female Sheep

Dopaminergic Inhibition of Reproduction in Teleost Fishes: Ecophysiological and Evolutionary Implications

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