Exp Clin Endocrinol Diabetes 2004; 112(4): 215-221
DOI: 10.1055/s-2004-817942
Article

J. A. Barth Verlag in Georg Thieme Verlag KG Stuttgart · New York

The Effects of Prolonged, Intracerebroventricular Prolactin Treatment on Luteinizing Hormone Secretion, Catecholaminergic Activity and Estrous Behavior in Ewes

T. Misztal1 , K. Romanowicz1 , D. Tomaszewska-Zaremba1 , A. Wójcik-Gładysz1 , B. Barcikowski1
  • 1The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Jabłonna near Warsaw, Poland
Further Information

Publication History

Received: January 27, 2003 First decision: June 16, 2003

Accepted: October 6, 2003

Publication Date:
04 May 2004 (online)

Abstract

Searching for the role of prolactin (PRL) in controlling gonadotropic axis activity in sheep, we studied the effects of prolonged, intracerebroventricular (icv) PRL infusion on luteinizing hormone (LH) secretion and catecholaminergic activity in the hypothalamic infundibular nuclei/median eminence (IN/ME) in sexually active ewes during the periovulatory period. Three groups of animals received the following treatments: 1) icv infusion of PRL at a dose of 200 µg/day (Lower dose, n = 5); 2) icv infusion of PRL at a dose of 400 µg/day (Higher dose, n = 6), and 3) icv infusion of the vehicle (control, n = 5). Each dose of PRL was infused in a pulsatile manner, 4 × 50 µg/h and 4 × 100 µg/h, in 30-min intervals, respectively, during four consecutive days before oncoming ovulation. The estrous behavior of ewes following treatments was also monitored as a determinant of the GnRH/LH surge. Two series of blood collections were made in every ewe, the first on the day preceding the infusion (day 0 of the experiment), the second on the day after the infusion (day 5 of the experiment). In addition, on day 5 of the experiment, perfusions of the IN/ME were made by the push-pull method, either in control or lower dose-treated animals. It was shown that a significant (p < 0.01, p < 0.001) increase in tonic LH secretion during the periovulatory period remained in ewes irrespective of the kind of infusion. No statistical differences were found in LH pulse frequency, amplitude, or in the length of the pulse when compared with values from day 0 and 5 of the experiment within each group. A significant (p < 0.001) increase in IN/ME perfusate concentrations of dopamine and noradrenaline metabolites was noted in PRL-treated ewes in comparison with those in the control. The estrous behavior in PRL-treated animals was delayed for a few days, 3.80 ± 0.80 days at the lower dose (p < 0.01), and 2.83 ± 0.98 days at the higher dose (p < 0.05) in comparison with the control, 0.20 ± 0.20 days. These data indicate that maintenance of an increased PRL concentration within the central nervous system (CNS) for a few days before oncoming ovulation has no inhibitory effect on tonic LH secretion. A few-day shift of the preovulatory GnRH/LH surge, as determined by estrous behavior, might, however, be a consequence of the PRL-induced increase in catecholamine turnover in the IN/ME.

References

  • 1 Anderson S T, Walsh J P, Tillet Y, Clarke I J, Curlewis F D. Dopaminergic input to the ventromedial hypothalamus facilitates the oestrogen-induced luteinizing hormone surge in ewes.  Neuroendocrinology. 2001;  73 91-101
  • 2 Arbogast L A, Voogt J L. Prolactin (PRL) receptors are colocalized in dopaminergic neurons in fetal hypothalamic cell cultures: Effect of PRL on tyrosine hydroxylase activity.  Endocrinology. 1997;  138 3016-3023
  • 3 Ben-Jonathan N, Mershon J L, Allen D L, Steinmetz R W. Extrapituitary prolactin: distribution, regulation, functions and clinical aspects.  Endocrine Rev. 1996;  17 639-669
  • 4 Bertrand F, Thiery J-C, Picard S, Malpaux B. Implication of D2-like dopaminergic receptors in the median eminence during the establishment of long-day inhibition of LH secretion in the ewe.  J Endocrinol. 1999;  163 243-254
  • 5 Cheung C Y. Prolactin suppresses luteinizing hormone secretion and pituitary responsiveness to luteinizing hormone-releasing hormone by a direct action at the anterior pituitary.  Endocrinology. 1983;  113 632-638
  • 6 Chomicka L K. Biogenic amines and the activity of the hypothalamo-pituitary-ovarian axis in ewes.  J Physiol Pharmacol. 1992;  43 (Suppl 1) 57-68
  • 7 Chomicka L K, Wolińska-Witort E, Przekop F. Release of LHRH, β-endorphin and dopamine by nucleus infundibularis/median eminence during the estrous cycle in the ewe.  European J Endocrinol. 1994;  130 (Suppl 2) 43
  • 8 Ciereszko R, Opalka M, Kaminska B, Kaminski T, Dusza L. Prolactin involvement in the regulation of the hypothalamic-pituitary-ovarian axis during the early luteal phase of the porcine estrous cycle.  Anim Reprod Sci. 2002;  69 99-115
  • 9 Cramer O M, Parker C R, Porter J C. Estrogen inhibition of dopamine release into hypophysial portal blood.  Endocrinology. 1979;  104 419-422
  • 10 Curlewis J D, McNeilly A S. Prolactin short-loop feedback and prolactin inhibition of luteinizing hormone secretion during the breeding season and seasonal anoestrus in the ewe.  Neuroendocrinology. 1991;  54 279-285
  • 11 Deaver D R, Dailey R A. Effect of dopamine, norepinephrine and serotonin on plasma concentrations of luteinizing hormone and prolactin in ovariectomized and anestrous ewes.  Biol Reprod. 1982;  27 624-632
  • 12 Deaver D R, Dailey R A. Effects of dopamine and serotonin on concentration of luteinizing hormone and estradiol 17-β in plasma of cycling ewes.  Biol Reprod. 1983;  28 870-877
  • 13 Domański E, Chomicka L K, Ostrowska A, Gajewska A, Mateusiak K. Release of luteinizing hormone-releasing hormone, β-endorphin and noradrenaline by the nucleus infundibularis/median eminence during periovulatory period in the sheep.  Neuroendocrinology. 1991;  54 151-158
  • 14 Fox S R, Hoefer M T, Bartke A, Smith M S. Suppression of pulsatile LH secretion, pituitary GnRH receptor content and pituitary responsiveness to GnRH by hyperprolactinemia in the male rat.  Neuroendocrinology. 1987;  46 350-359
  • 15 Freeman M E, Kanyicska B, Lerant A, Nagy G. Prolactin: structure, function and regulation of secretion.  Physiol Rev. 2000;  80 1523-1631
  • 16 Gallegoz-Sanchez J, Malpaux B, Thiery J-C. Control of pulsatile LH secretion during seasonal anoestrus in the ewe.  Reprod Nutr Dev. 1998;  38 3-15
  • 17 Garcia A, Herbon L, Barkan A, Papavasiliou S, Marshall J C. Hyperprolactinemia inhibits gonadotropin releasing-hormone (GnRH) stimulation of the number of pituitary GnRH receptors.  Endocrinology. 1985;  117 954-959
  • 18 Goodman R L. Neuroendocrine control of the ovine estrous cycle. Knobil E, Neill JD The Physiology of Reproduction. 2nd ed., Vol. 2. New York; Raven Press 1994: 659-710
  • 19 Grattan D. The actions of prolactin in the brain during pregnancy and lactation.  Prog Brain Res. 2001;  133 153-171
  • 20 Kann G, Denamur R. Possible role of prolactin during the estrous cycle and gestation in the ewe.  J Reprod Fertil. 1974;  39 473-483
  • 21 Kochman H, Kochman K. Purification of ovine and bovine prolactins on DEAE cellulose chromatography and preparative polyacrylamide gel electrophoresis.  Bull Acad Sci Polon. 1977;  25 67-70
  • 22 Kuljis R O, Advis J P. Immunocytochemical and physiological evidence of a synapse between dopamine and luteinizing hormone-releasing hormone-containing neurons in the ewe median eminence.  Endocrinology. 1989;  124 1579-1587
  • 23 Merriam G R, Wachter K W. Algorithms for the study of episodic hormone secretion.  Am J Physiol. 1982;  243 E310-E318
  • 24 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. 1997;  66 360-367
  • 25 Misztal T, Romanowicz K, Barcikowski B. Effect of prolactin infused into the third brain ventricle on LH secretion in follicular-phase and ovariectomized ewes.  Anim Reprod Sci. 2003;  75 27-37
  • 26 Moenter S M, Caraty A, Lacatelli A, Karsch F J. Pattern of gonadotropin-releasing hormone (GnRH) secretion leading up to ovulation in the ewe: existence of a preovulatory GnRH surge.  Endocrinology. 1991;  129 1175-1182
  • 27 Moore K E. Interactions between prolactin and dopaminergic neurons.  Biol Reprod. 1987;  36 47-58
  • 28 Picazo R A, Gonzalez de Bulnes A, Gomez Brunet A, del Campo A, Granados B, Tresguerres J, Lopez Sebastian A. Effects of bromocriptine administration during the follicular phase of the oestrous cycle on prolactin and gonadotrophin secretion and follicular dynamics in Merino monovular ewes.  J Reprod Fert. 2000;  120 177-186
  • 29 Przekop F, Skubiszewski B, Wolińska E, Domański E. The role of catecholamines in stimulating the release of pituitary ovulating hormone(s) in sheep.  Acta Physiol Pol. 1975;  26 433-437
  • 30 Reeves J T, Arimura S, Schally A B. Serum levels of prolactin and luteinizing hormone in the ewe at various stages of the estrous cycle.  Proc Soc Exp Biol Med. 1970;  134 938-942
  • 31 Sortino M A, Wise P M. Effect of hyperprolactinemia on luteinizing hormone and prolactin secretion assessed using the reverse hemolytic plaque assay.  Biol Reprod. 1989;  41 618-625
  • 32 Smith M S. A comparison of pituitary responsiveness to luteinizing hormone-releasing hormone during lactation and the estrous cycle of the rat.  Endocrinology. 1978;  102 114-120
  • 33 Smith M S. Effect of pulsatile gonadotrophin-releasing hormone on the release of luteinizing hormone and follicle-stimulating hormone in vitro by anterior pituitaries from lactating and cycling rats.  Endocrinology. 1982;  110 882-891
  • 34 Stupnicki R, Madej A. Radioimmunoassay of LH in blood plasma of farm animals.  Endokrinologie. 1976;  68 6-13
  • 35 Stupnicki R, Kula E. Direct radioimmunoassay of progesterone in human plasma.  Endokrinologie. 1982;  80 1-7
  • 36 Thiery J-C. Monoamine content of the stalk-median eminence and hypothalamus in adult female sheep as affected by daylength.  J Neuroendocrinol. 1991;  3 407-411
  • 37 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 rat.  J Endocrinol. 1989 a;  121 141-147
  • 38 Thomas G B, Cummins J T, Doughton B W, Griffin N, Smythe G A, Gleeson R M, Clarke I J. Direct pituitary inhibition of prolactin secretion by dopamine and noradrenaline in sheep.  J Endocrinol. 1989 b;  123 393-402
  • 39 Tillet Y. Distribution of neurotransmitters in the sheep brain.  J Reprod Fertil Suppl. 1995;  49 199-220
  • 40 Tomaszewska-Zaremba D, Mateusiak K, Przekop F. The involvement of GABAA receptors in the control of GnRH and β-endorphin release, and catecholaminergic activity in the preoptic area in anestrous ewes.  Exp Clin Endocrinol Diabetes. 2002;  110 336-342
  • 41 Tortonese D J, Brooks J, McNeilly A S. Prolactin receptor gene expression in sheep hypothalamus and pituitary gland.  J Reprod Fertil Abstr Ser. 1995;  16 20
  • 42 Tortonese D J, Brooks J, Ingleton P M, McNeilly A S. Detection of prolactin receptor gene expression in the sheep pituitary gland and visualization of the specific translation of the signal in gonadotrophs.  Endocrinology. 1998;  139 5215-5223
  • 43 Traczyk W, Przekop F. Methods of investigation of the function of the hypothalamus and hypophysis in chronic experiments in sheep.  Acta Physiol Pol. 1963;  14 217-226
  • 44 Wolińska E, Polkowska J, Domański E. The hypothalamic centers involved in the control of production and release of prolactin in sheep.  J Endocrinol. 1977;  73 21-29

Ph.D. Tomasz Misztal

The Kielanowski Institute of Animal Physiology and Nutrition Polish Academy of Sciences

05-110 Jabłonna n/Warsaw

Poland

Phone: + 48227824422

Fax: + 48 2 27 74 20 38

Email: t.misztal@ifzz.pan.pl

    >