Download PDF
Exp Clin Endocrinol Diabetes 2008; 116(6): 357-362
DOI: 10.1055/s-2008-1042406
Article

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

Implication of Dopaminergic Systems on GnRH and GnRHR Genes Expression in the Hypothalamus and GnRH-R Gene Expression in the Anterior Pituitary Gland of Anestrous Ewes

M. Ciechanowska 1 , M. Łapot 1 , T. Malewski 2 , K. Mateusiak 1 , T. Misztal 1 , F. Przekop 1
  • 1The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Jabłonna
  • 2Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 3, Warsaw
Further Information

Publication History

received 28.08.2007 first decision 29.10.2007

accepted 09.01.2008

Publication Date:
05 June 2008 (online)

Also available at
    Permissions and Reprints

Abstract

We examined by Real-time PCR how prolonged inhibition of dopaminergic D-2 receptors (DA-2) in the hypothalamus of anestrous ewes by infusion of sulpiride into the third cerebral ventricle affected GnRH and GnRH-R gene expression in discrete parts of this structure and GnRH-R gene expression in the anterior pituitary. Blockaded DA-2 receptors significantly decreased GnRH mRNA levels in the ventromedial hypothalamus but did not evidently affect GnRH mRNA in the preoptic/anterior hypothalamic area. Blockaded DA-2 receptors led to different responses in GnRH-R mRNA in various parts of the hypothalamus; increased GnRH-R mRNA levels in the preoptic/anterior hypothalamic area, and decreased GnRH-R mRNA amounts in the ventromedial hypothalamus stalk/median eminence. An infusion of sulpiride into the III-rd ventricle increased GnRH mRNA levels in the anterior pituitary gland and LH secretion. It is suggested that the increase of GnRH gene expression in the anterior pituitary gland and LH secretion in sulpiride-treated ewes are related with an increase of biosynthesis GnRH with concomitant decreased biosynthesis of GnRH-R protein in the ventromedial hypothalamus/stalk median eminence allowing to an increase of GnRH release.

Key words

receptors - signal transduction - luteininzing hormone - hormones - gonadotrophins - hormones

References

  • 1 Adams VL, Goodman RL, Salm AK, Coolen LM, Karsch FJ, Lehman MN. Morphological plasticity in the neural circuitry responsible for seasonal breeding in the ewe.  Endocrinology. 2006;  147 4843-4851
    CrossrefPubMedSearch in Google Scholar
  • 2 Adams BM, Sukarai H, Adams TE. Concentration of gonadotropin-releasing hormone (GnRH) receptor messenger ribonucleic acid in pituitary tissue of orchidectomized sheep: effect of estradiol and GnRH.  Biol Reprod. 1996;  54 407-412
    CrossrefPubMedSearch in Google Scholar
  • 3 Anderson ST, Walsh JP, Tillet Y, Clarke IJ, Curlevis JD. Dopaminergic input to the ventromedial hypothalamus facilitates the estrogen-induced luteinizing hormone surge in ewes.  Neuroendocrinology. 2001;  73 91-101
    CrossrefPubMedSearch in Google Scholar
  • 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 Endocr. 1999;  163 293-254
    PubMedSearch in Google Scholar
  • 5 Curlewis JD, Naylor AM, Mac Neilly AS. Evaluation of a possible role for the dopamine D1 and D2 receptors in the steroid-dependent suppression of luteinizing hormone secretion in the seasonally anestrous ewes.  J Neuroendocrinol. 1991;  3 387-391
    CrossrefPubMedSearch in Google Scholar
  • 6 Paolo LV De, King RA, Carollo AJ. In vivo and in vitro examination of an autoregulatory mechanism for luteinizing hormone-releasing hormone.  Endocrinology. 1987;  120 272-279
    PubMedSearch in Google Scholar
  • 7 Gajewska A, Kochman K, Lerrant Y, Kochman H, Cunis R. Modulation of luteinizing hormone subunit gene expression by intracerebroventricular microinjection of gonadotropin releasing hormone or β-endorphin in female rats.  Biochimical Biophisica Acta. 2000;  1523 217-224
    PubMedSearch in Google Scholar
  • 8 Gallegos-Sandez J, Delaleu B, Caraty A, Malpaux B, Thiery JC. Estradiol acts locally within the retrochiasmatic area to inhibit pulsatile luteinizing hormone release in the female sheep during anestrus.  Biol Reprod. 1997;  56 1544-1549
    CrossrefPubMedSearch in Google Scholar
  • 9 Goodman RL. Neural systems mediating the negative feedback actions of estradiol and progesterone in the ewe.  Acta Neurobiol Exp. 1996;  56 727-741
    PubMedSearch in Google Scholar
  • 10 Goodman RL, Inskeep EK. The neuroendocrine control of the ovarian cycle of sheep. In: Neill JD, ed Knobil and Neill's Physiology and Reproduction. 3rd ed. Amsterdam: Elsevier 2006 Vol. 2 2389-2447
    Search in Google Scholar
  • 11 Goodman RL, Robinson JE, Kendrick KM, Dyer RG. Is the inhibitory action of estradiol on luteinizing hormone pulse frequency in anestrous ewes mediated by noradrenergic neurons in the preoptic area?.  Neuroendocrinology. 1995;  61 284-292
    PubMedSearch in Google Scholar
  • 12 Goodman RL, Thiery JC, Delaleu B, Malpaux B. Estradiol increases multi-unit activity in the A15 area of ewes exposed to inhibitory photoperiod.  Biol Reprod. 2000;  63 1352-1357
    CrossrefPubMedSearch in Google Scholar
  • 13 Gore AC, Roberts JL. Regulation of gonadotropin-releasing hormone gene expression in vivo and in vitro.  Front Neuroendocrinol. 1997;  18 209-245
    PubMedSearch in Google Scholar
  • 14 Hardy SL, Anderson GM, Valent M, Connors JM, Goodman RL. Evidence that estrogen receptor α but not β, mediates seasonal changes in the response of the ovine retrochiasmatic area to estradiol.  Biol Reprod. 2003;  68 846-852
    PubMedSearch in Google Scholar
  • 15 Harris TG, Robinson JE, Evans NP, Skinner DC, Herbison AE. Gonadotropin-releasing hormone messenger ribonucleic acid expression changes prior to onset of LH surge in the ewe.  Endocrinology. 1998;  139 57-64
    CrossrefPubMedSearch in Google Scholar
  • 16 Havern RL, Whisnant CS, Goodman RL. Hypothalamic sites of catecholamine inhibition of luteinizing hormone in the anestrous ewe.  Biol Reprod. 1991;  44 476-482
    CrossrefPubMedSearch in Google Scholar
  • 17 Herbison AE. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons.  Endocr Rev. 1998;  19 302-330
    CrossrefPubMedSearch in Google Scholar
  • 18 Horwath TL, Naftolin F, Leranth C. B-endorphin innervation of dopamine neurons in the rat hypothalamus: a light and electron microscopic double immunostaining study.  Endocrinology. 1992;  131 1547-1557
    CrossrefPubMedSearch in Google Scholar
  • 19 James MD, Mac Kenzie FJ, Tuohy-Jones PA, Wilson CA. Dopaminergic neurons in the zona incerta exert a stimulatory control of gonadotropin release via D1-dopamine receptors.  Neuroendocrinology. 1987;  45 348-355
    PubMedSearch in Google Scholar
  • 20 Jansen HT, Cutter C, Hardy S, Lehman MN, Goodman RL. Seasonal plasticity within gonadotropin-releasing hormone (GnRH) system of the ewe: changes in identified GnRH inputs and glial association.  Endocrinology. 2003;  144 3663-3676
    CrossrefPubMedSearch in Google Scholar
  • 21 Kaiser UB, Jakubowiak A, Steinberger A, Chin WW. Differential effect of gonadotropin-releasing hormone (GnRH) pulse frequency on gonadotropin subunit and GnRH receptor messenger ribonucleic acid levels in vitro.  Endocrinology. 1997;  138 1224-1231
    CrossrefPubMedSearch in Google Scholar
  • 22 Kalia V, Fenske C, Holc RD, Wilson CA. Effect of gonadal steroid and gamma -aminobutyric acid on LH release and dopamine expression and activity in the zona incerta in rats.  J Reprod Fertil. 1999;  117 189-197
    PubMedSearch in Google Scholar
  • 23 Kirkpatrick BL, Esquivel E, Moss GE, Hamernik DL, Wise ME. Estradiol and gonadotropin-releasing hormone (GnRH) interact to increase GnRH receptor expression in ovariectomized ewes after hypothalamic-pituitary disconnection.  Endocrine. 1998;  8 225-229
    CrossrefPubMedSearch in Google Scholar
  • 24 Kuljis RO, Advis JP. Immunocytochemical and physiological evidence of a synapse between dopamine- and luteinizing hormone-releasing hormone - containing neurons in the ewe median eminence.  Endocrinology. 1989;  124 1579-1581
    PubMedSearch in Google Scholar
  • 25 Le Corre S, Chemineau P. Control of photoperiodic inhibition of luteinizing hormone secretion by dopaminergic and serotoninergic systems in ovariectomized Ile-de-France ewes supplemented with estradiol.  J Reprod Fertil. 1993;  97 367-373
    PubMedSearch in Google Scholar
  • 26 Lehman MN, Durham DM, Jansen HT, Adrian B, Goodman RL. Dopaminergic A14/A15 neurons are activated during estradiol negative feedback in anestrous, but not breeding season, ewes.  Endocrinology. 1996;  137 4443-4450
    CrossrefPubMedSearch in Google Scholar
  • 27 Lehman MN, Karsch FJ. Do gonadotropin-releasing hormone, tyrosine hydroxylase-, and β-endorphin-immunoreactive neurons contain estrogen receptors? A double-label immunocytochemical study in the Suffolk ewe.  Endocrinology. 1993;  133 887-895
    CrossrefPubMedSearch in Google Scholar
  • 28 Lincoln GA. Neuroendocrine regulation of seasonal gonadotrophin and prolactin rhythms: lesson from the Soay ram model.  Reproduction, Suppl. 2002;  59 131-141
    PubMedSearch in Google Scholar
  • 29 Livak KJ, Smittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and 2-ΔΔC T method.  Methods. 2001;  25 402-408
    CrossrefPubMedSearch in Google Scholar
  • 30 Malpaux B, Daveau A, Maurice-Mandon F, Duarte G, Chemineau P. Evidence that melatonin acts in the premammilary hypothalamic area to control reproduction in the ewe: presence of binding sites and stimulation of luteinizing hormone by in situ micrimplant delivery.  Endocrinology. 1995;  139 1508-1516
    PubMedSearch in Google Scholar
  • 31 Marriam GR, Wachter KW. Algorithms for study of episodic hormone secretion.  Amer J Physiol. 1982;  243 E310-E318
    PubMedSearch in Google Scholar
  • 32 Moore KL, Lookingland KJ. Dopaminergic neuronal systems in the hypothalamus. Bloom FE and Kupfer DJ, eds. Psychopharmacology: The fourth generation of progress (Chapter 22). New York: Raven Press, Ltd 1995: 245-256
    Search in Google Scholar
  • 33 Pau K, Kuchl DE, Jackson GL. Effect of frontal hypothalamic deafferentation on luteinizing hormone secretion and seasonal breeding in the ewe.  Biol Reprod. 1982;  27 999-1009
    CrossrefPubMedSearch in Google Scholar
  • 34 Przekop F. Effect of anterior deafferentation of the hypothalamus on the hypothalamus on the release of luteinizing hormone (LH and reproductive function in sheep).  Acta Physiol Pol. 1978;  29 393-407
    PubMedSearch in Google Scholar
  • 35 Robinson JE, Healey AE, Harris TG, Messent AE, Skinner DC, Taylor JA, Evans NP. The negative feedback action of progesterone on luteinizing hormone release is not associated with changes in GnRHmRNA expression in the ewe.  J Neuroendocrinol. 2000;  12 121-129
    CrossrefPubMedSearch in Google Scholar
  • 36 Sarkar DK. In vitro secretion of LHRH in ovariectomized rats is regulated by a possible autofeedback mechanism.  Neuroendocrinology. 1987;  45 510-513
    PubMedSearch in Google Scholar
  • 37 Seong JY, Kang SS, Kam K, Han Y-G, Kwon HB, Ryu K, Kim K. Different regulation of gonadotropin-releasing hormone (GnRH) receptor expression in the posterior mediobasal hypothalamus by steroid hormones: implication of GnRH neuronal activity.  Mol Brain Res. 1998;  53 226-235
    CrossrefPubMedSearch in Google Scholar
  • 38 Skinner DC, Herbison AE. Effects of photoperiod on estrogen receptors, tyrosin hydroxylase (TH), neuropeptide Y and β-endorphin immunoreactivity in the ewe hypothalamus.  Endocrinology. 1997;  138 2585-2595
    CrossrefPubMedSearch in Google Scholar
  • 39 Stupnicki R, Madej A. Radioimmunoassay of LH in blood plasma of farm animals.  Endokrinologie. 1976;  68 6-13
    PubMedSearch in Google Scholar
  • 40 Thanky NR, Slater R, Herbison AE. Sex differences in estrogen-dependenttranscription of gonadotropin-releasing hormone (GnRH) gene revealed in GnRH transgenic mice.  Endocrinology. 2003;  144 3351-3358
    CrossrefPubMedSearch in Google Scholar
  • 41 Thiery JC, Martin GB, Tillet Y, Caldani M, Quentin M, Jamain C, Revault JP. Role of hypothalamic catecholamines in the regulation of luteinizing hormone and prolactin secretion in the ewe during seasonal anestrus.  Neuroendocrinology. 1989;  49 80-87
    PubMedSearch in Google Scholar
  • 42 Tomaszewska D, Mateusiak K, Przekop F. Extracellular concentration of monoamines and their metabolites in the mediobasal hypothalamus-median eminence of ewes during β- endorphin treatment.  Neuroendocrinology Letters. 1998;  19 43-53
    PubMedSearch in Google Scholar
  • 43 Tomaszewska-Zaremba D, Przekop F. Effects of GABAβ receptor modulation of gonadotropin-releasing hormone and β-endorphin release, and on catecholaminergic activity in the ventromedial hypothalamus-infundibular nucleus region of anestrous ewes.  J Neuroendocrinology. 2005;  17 44-56
    PubMedSearch in Google Scholar
  • 44 Tortonese DJ. Interaction between hypothalamic dopaminergic and opioidergic systems in the photoperiodic regulation of pulsatile luteinizing hormone secretion in sheep.  Endocrinology. 1999;  140 750-757
    CrossrefPubMedSearch in Google Scholar
  • 45 Tortonese DJ, Lincoln GA. Photoperiodic modulation of the dopaminergic control of pulsatile LH secretion in sheep.  J Endocrinol. 1994;  143 25-32
    PubMedSearch in Google Scholar
  • 46 Traczyk W, Przekop F. Methods of investigation of the function of hypothalamus and hypophysis in chronic experiments in sheep.  Acta Physiol Pol. 1963;  14 217-226
    PubMedSearch in Google Scholar
  • 47 Turzillo AM, Juengel JL, Nett TM. Pulsatile gonadotropin-releasing hormone (GnRH) increases concentrations of GnRH receptor messenger ribonucleic acid and numbers of GnRH receptors during luteolysis in the ewe.  Biol Reprod. 1995;  53 418-423
    PubMedSearch in Google Scholar
  • 48 Turzillo AM, Nolan TE, Nett TM. Regulation of gonadotropin-releasing hormone (GnRH) receptor gene expression in sheep: interaction of GnRH and estradiol.  Endocrinology. 1998;  139 3890-3894
    PubMedSearch in Google Scholar
  • 49 Welento J, Steyn S, Milart Z. Observation on the stereotaxic configuration of the hypothalamus nuclei in sheep.  Anat Anz. 1969;  124 1-27
    PubMedSearch in Google Scholar
  • 50 Viguié C, Caraty A, Locatelly A, Malpaux B. Regulation of luteinizing hormone- releasing hormone (LHRH) secretion by melatonin in the ewe. Simultaneous delayed increase in LHRH and luteinizing hormone pulsatile secretion.  Biol Reprod. 1995;  52 1114-1120
    PubMedSearch in Google Scholar
  • 51 Yasin M, Dalkin AC, Haisenleder DJ, Kerrigan JR, Marshall JC. Gonadotropin-releasing hormone (GnRH) pulse pattern regulates GnRH receptor gene expression: augmentation by estradiol.  Endocrinology. 1995;  136 1559-1564
    CrossrefPubMedSearch in Google Scholar

Correspondence

M. Ciechanowska

The Kielanowski Institute of Animal Physiology and Nutrition

Polish Academy of Sciences

05-110 Jabłonna n. Warsaw

Poland

Email: m.ciechanowska@ifzz.pan.pl