Short-term modulation of prolactin secretion by melatonin in anestrous ewes following dopamine- and opiate receptor blockade

Summary:

This study tested the hypothesis that the dopaminergic and opioidergic systems are not involved in the short-term stimulatory action of melatonin (MLT) on the secretion of prolactin in anestrous ewes. Thus, MLT should stimulate prolactin release after blockade of either dopamine (DA) or opiate receptors with specific antagonists at the level of the pituitary gland and central nervous system (CNS), respectively. During afternoon intracerebroventricular (icv.) infusion of MLT, the mean plasma prolactin concentration increased significantly (P < 0.001) as compared with the concentrations noted before and during the infusion of the vehicle (veh.). As a result of subcutaneous (sc.) injection of sulpiride (SULP, DA antagonist), an increase in plasma prolactin concentration was observed, followed by a gradual decrease during the icv. infusion of the vehicle. MLT infused icv. significantly increased (P < 0.001) the secretion of prolactin in SULP + MLT-treated ewes, as compared with the concentration of prolactin noted during infusion of the vehicle in SULP + veh.-treated ewes. Naloxone (NAL, opioid antagonist) infused icv. did not significantly affect the secretion of prolactin, however, a significant (P < 0.01) increase in the concentration was observed after the infusion. In MLT + NAL-treated ewes, the plasma prolactin concentration increased significantly (P < 0.001) during the infusion, as compared with the concentration noted before and that in NAL-alone infused ewes. These results demonstrate that melatonin stimulates prolactin release after the pharmacological exclusion of the dopaminergic input with the DA antagonist sulpiride and also despite the presence of DA activity in the hypothalamus after NAL treatment. Secondly, endogenous opioid peptides are not a major component of this melatonin action.

Key words:

Melatonin - prolactin - dopamine receptor - opiate receptor

References

• 1 Arbogast L A, Voogt J L. Endogenous opioid peptides contribute to suckling-induced prolactin release by suppression tyrosine hydroxylase activity and messenger ribonucleic acid levels in tuberoinfundibular dopaminergic neurons.  Endocrinology. 139 2857-2862 1998; 
• 2 Arey B J, Burris T P, Basco P, Freeman M E. Infusion of dopamine at low concentrations stimulates the release of prolactin from alfa-methyl-p-tyrosine-treated rats.  PSEBM. 203 60-63 1993; 
• 3 Barrell G K, Lapwood K R. Effects of pinealectomy in rams on secretory profiles of luteinizing hormone, testosterone, prolactin and cortisol.  Neuroendocrinology. 27 216-227 1978; 
• 4 Bjorklund A, Moore R Y, Nobin A, Stenevi U. The organization of tubero-hypophysical and reticulo-infundibular catecholamine neuron systems in the rat brain.  Brain Res. 51 171-191 1973; 
• 5 Burris T P, Nguyen D N, Smith S G, Freeman M E. Stimulatory and inhibitory effects of dopamine on prolactin secretion involve different G-protein.  Endocrinology. 130 926-932 1992; 
• 6 Cuello A C. Central distribution of opioid peptides.  Br Med Bull. 39 11-16 1983; 
• 7 Curlewis J D, Naylor A M, Rhind S M, McNeilly A S. Effects of β-endorphin on pulsatile luteinizing hormone and prolactin secretion during the follicular phase in the ewe.  J Neuroendocrinol. 3 123-126 1991; 
• 8 Denef C, Manet D, Dewals R. Dopaminergic stimulation of prolactin release.  Nature. 285 243-246 1980; 
• 9 DeMaria J E, Livingstone J D, Freeman M E. Characterization of the dopaminergic input to the pituitary gland throughout the estrous cycle of the rat.  Neuroendocrinology. 67 377-383 1998; 
• 10 Domanski E, Romanowicz K, Kerdelhue B. Enhancing effect of intracerebrally infused β-endorphin antiserum on the secretion of cortisol in foot-shocked sheep.  Neuroendocrinology. 57 127-131 1993; 
• 11 Dupont A, Cusan L, Labrie F, Coy D H, Li C H. Stimulation of prolactin release in the rat by intraventricular injection of β-endorphin and methionine-enkephalin.  Biochem Biophys Res Commun. 75 76-82 1977; 
• 12 Ebling F JP, Lincoln G A. β-endorphin secretion in rams related to season and photoperiod.  Endocrinology. 120 809-818 1987; 
• 13 Fuxe K. Cellular localization of monoamines in the median eminence and in the infundibular stem of some mammals.  Acta Physiol Scand. 58 383-384 1963; 
• 14 Goudreau J L, Lindley S E, Lookingland K J, Moore K E. Evidence that hypothalamic periventricular dopamine neurons innervate the intermediate lobe of the rat pituitary.  Neuroendocrinology. 56 100-105 1992; 
• 15 Goudreau J L, Falls W M, Lookingland K J, Moore K E. Periventricular-hypophysical dopaminergic neurons innervate the intermediate but not the neural lobe of the rat pituitary gland.  Neuroendocrinology. 62 147-154 1995; 
• 16 Gudelsky G A, Porter J C. Morphine- and opioid peptide-induced inhibition of the release of dopamine from tuberoinfundibular neurons.  Life Sci. 25 1697-1702 1979; 
• 17 Hazlerigg D G, Hastings M H, Morgan P J. Production of a prolactin releasing factor by the ovine pars tuberalis.  J Neuroendocrinol. 8 489-492 1996; 
• 18 Kennaway D J, Gilmore T A, Seamark R E. Effect of melatonin feeding on serum prolactin and gonadotropin and the onset of seasonal estrous cyclicity in sheep.  Endocrinology. 110 1766-1772 1982; 
• 19 Kennaway D J, Obst J M, Dunstan E A, Friesen H G. Ultradian and seasonal rhythms in plasma gonadotropins, prolactin, cortisol and testosterone in pinealectomized rams.  Endocrinology. 108 639-646 1981; 
• 20 Kochman H, Kochman K. Purification of ovine and bovine prolactins on DEAE cellulose chromatography and preparative polyacrylamide gel electrophoresis.  Bull Acad Sci Polon. 25 67-70 1977; 
• 21 Lamberts S WJ, MacLeod R M. Regulation of prolactin secretion at the level of the lactotrophs.  Physiol Rev. 70 279-318 1990; 
• 22 Lincoln G A, Maeda K-I. Effects of placing micro-implants of melatonin in the mediobasal hypothalamus and preoptic area on the secretion of prolactin and β-endorphin in rams.  J Endocrinol. 134 437-448 1992; 
• 23 Lincoln G A, Clarke I J. Photoperiodically-induced cycles in the secretion of prolactin in hypothalamo-pituitary disconnected rams: evidence for translation of the melatonin signal in the pituitary gland.  J Neuroendocrinol. 6 251-260 1994; 
• 24 Lincoln G A, Clarke I J. Evidence that melatonin acts in the pituitary gland through a dopamine-independent mechanism to mediate effects of daylength on the secretion of prolactin in the ram.  J Neuroendocrinol. 7 637-643 1995; 
• 25 Lincoln G A, McNeilly A S, Cameron C L. The effects of sudden decrease or increase in daylength on prolactin secretion in the ram.  J Reprod Fert. 52 305-311 1978; 
• 26 van Loon G R, Ho D, Kim C. β-endorphin induced decrease in hypothalamic dopamine turnover.  Endocrinology. 106 76-80 1980; 
• 27 Misztal T, Romanowicz K, Barcikowski B. Effects of melatonin infused into the III ventricle on prolactin, β-endorphin and luteotropin secretion in ewes during the different stages of the reproductive cycle.  Acta Neurobiol Exp. 56 769-778 1996; 
• 28 Misztal T, Romanowicz K, Barcikowski B. Natural and melatonin-stimulated changes in the circadian rhythm of prolactin secretion in the ewe during seasonal anestrus.  Neuroendocrinology. 66 360-367 1997; 
• 29 Misztal T, Romanowicz K, Barcikowski B. Melatonin modulation of the daily prolactin secretion in intact and ovariectomized ewes: relation to a phase of the estrous cycle and to presence of estradiol.  Neuroendocrinology. 69 105-112 1999; 
• 30 Morgan P J. The pars tuberalis as a target for melatonin action.  Adv Pin Res. 6 149-158 1991; 
• 31 Morgan P J, Williams L M. The pars tuberalis of the pituitary: a gateway for neuroendocrine output.  Rev Reprod. 1 153-161 1996; 
• 32 Morgan P J, Barrett P, Davidson G, Lawson W. Melatonin regulates the synthesis and secretion of several proteins by pars tuberalis cells of the ovine pituitary.  J Neuroendocrinol. 4 557-563 1993; 
• 33 Morgan P J, Williams L M, Davidson G, Lawson W, Howell E. Melatonin receptors on the ovine pars tuberalis: characterization and autoradiographical localization.  J Neuroendocrinol. 1 1-4 1989; 
• 34 Morgan P J, Webster C A, Mercer J G, Ross A W, Hazlerigg D G, MacLean A, Barrett P. The ovine pars tuberalis secretes a factor(s) that regulates gene expression in both lactotropic and nonlactotropic pituitary cells.  Endocrinology. 137 4018-4026 1996; 
• 35 Poulton A L, English J, Symons A M, Arendt J. Changes in plasma concentration of LH, FSH and prolactin in ewes receiving melatonin and short-photoperiod treatments to induce early onset of breeding activity.  J Endocrinol. 112 103-111 1987; 
• 36 Sagrillo C A, Voogt J L. Endogenous opioids mediate the nocturnal prolactin surge in the pregnant rat.  Endocrinology. 129 925-930 1991; 
• 37 Shieh K R, Pan J T. Sexual differences in the diurnal changes of tuberoinfundibular dopaminergic neuron activity in the rat: Role of cholinergic control.  Biol Reprod. 54 987-992 1996; 
• 38 Shin S H. Dopamine-induced inhibition of prolactin release from cultured adenohypophysial cells: spare receptor for dopamine.  Life Sci. 22 67-74 1978; 
• 39 Steger R W, Juszczak M, Fadden C, Bartke A. Photoperiod effect on neurohypophyseal and tuberoinfundibular dopamine metabolism in the male hamster.  Endocrinology. 136 3000-3006 1995; 
• 40 Thiery J-C. Monoamine content of the stalk-median eminence and hypothalamus in the adult female sheep as affected by day length.  J Neuroendocrinol. 3 407-411 1991; 
• 41 Thomas G B, Cummins J T, Smythe G A, Gleeson R M, Dow R C, Fink G, Clarke I J. Concentrations of dopamine and noradrenaline in hypophysial portal blood in the sheep and the rat.  J Endocrinol. 121 141-147 1989; 
• 42 Thomas G B, Cummins J T, Griffin N, Clarke I J. Involvement of the posterior pituitary gland in the control of prolactin secretion in the sheep. Proc Vth International Congress on Prolactin. Kyoto, Japan. Abstract P-28 1988
• 43 Traczyk W, Przekop F. Methods of investigation of the function of the hypothalamus and hypophysis in chronic experiments in sheep.  Acta Physiol Pol. 14 217-226 1963; 
• 44 van Vugt D A, Sylvester P W, Aylsworth C F, Meites J. Comparison of acute effects of dynorphin and β-endorphin on prolactin release in the rat.  Endocrinology. 108 2017-1018 1981; 
• 45 Walton J S, Evins J D, Fitzgerald B P, Cunningham F J. Abrupt decrease in daylength and short-term changes in the plasma concentrations of FSH, LH and prolactin in anoestrous ewes.  J Reprod Fert. 59 163-171 1980; 
• 46 Wolin¿ska E, Polkowska J, Doman¿ski E. The hypothalamic centers involved in the control of production and release of prolactin in sheep.  J Endocrinol. 73 21-29 1977;