Up-regulation of oxytocin receptor gene and protein in the sheep anterior pituitary by a dopamine derivative (salsolinol)

https://doi.org/10.17221/30/2016-CJASCitation:Górski K., Hasiec M., Zielińska-Górska M., Fülöp F., Misztal T. (2017): Up-regulation of oxytocin receptor gene and protein in the sheep anterior pituitary by a dopamine derivative (salsolinol). Czech J. Anim. Sci., 62: 150-156.
download PDF
Specific oxytocin receptors (OTR) have been identified in the anterior pituitary (AP), and their expression has been shown to change in relation to the animal physiological stage, whereas salsolinol (a derivative of dopamine) has been shown to stimulate the synthesis and release of oxytocin (OT) in lactating sheep. In the present study, the expression of both OTR mRNA and OTR protein in the AP were examined by real-time quantitative PCR and enzyme-linked immunosorbent assay, either in anestrous or lactating sheep 48 h after weaning lambs. Moreover, the effect of salsolinol administered via an intracerebroventricular (i.c.v.) infusion was tested in additional sheep at the same physiological stages. The i.c.v. infusions of Ringer-Locke (control) and salsolinol solutions were carried out from 10:00 to 15:00 h in a serial manner, i.e. five 30-min infusions at 30-min intervals. We observed both OTR gene and OTR protein expression in the AP, in both anestrous and lactating sheep, but it was significantly (< 0.01 and P < 0.05, respectively) higher in the AP of lactating animals compared to anestrous animals. Salsolinol i.c.v. treatment in anestrous sheep evoked a significant (P < 0.05) increase in both OTR gene and OTR protein expression compared to control animals. In contrast, salsolinol did not affect either OTR gene or OTR protein expression in lactating sheep. In conclusion, the expression of OTR in the sheep AP is upregulated by salsolinol. The effect of salsolinol was more pronounced in non-lactating sheep, with a reduced response due to ongoing OTR expression in lactating animals. Increased expression of OTR in the AP of lactating sheep may be related to the stimulation of pituitary lactotrophs by OT following the release of prolactin during suckling.
Adan R A, Van Leeuwen F W, Sonnemans M A, Brouns M, Hoffman G, Verbalis J G, Burbach J P (1995): Rat oxytocin receptor in brain, pituitary, mammary gland, and uterus: partial sequence and immunocytochemical localization.. Endocrinology, 136, 4022-4028 https://doi.org/10.1210/endo.136.9.7649111
Bealer S. L., Armstrong W. E., Crowley W. R. (): Oxytocin release in magnocellular nuclei: neurochemical mediators and functional significance during gestation. AJP: Regulatory, Integrative and Comparative Physiology, 299, R452-R458 https://doi.org/10.1152/ajpregu.00217.2010
Breton C. (1997): Expression and Region-Specific Regulation of the Oxytocin Receptor Gene in Rat Brain. Endocrinology, 138, 1857-1862 https://doi.org/10.1210/en.138.5.1857
Breton C, Pechoux C, Morel G, Zingg H H (1995): Oxytocin receptor messenger ribonucleic acid: characterization, regulation, and cellular localization in the rat pituitary gland.. Endocrinology, 136, 2928-2936 https://doi.org/10.1210/endo.136.7.7540544
GIBBS DANIEL M. (1984): High Concentrations of Oxytocin in Hypophysial Portal Plasma*. Endocrinology, 114, 1216-1218 https://doi.org/10.1210/endo-114-4-1216
Gimpl G., Fahrenholz F. (2001): The oxytocin receptor system: structure, function, and regulation. Physiological Reviews, 81, 629–683.
Gonzalez-Iglesias Arturo E., Fletcher Patrick A., Arias-Cristancho José A., Cristancho-Gordo Ruth, Helena Cleyde V., Bertram Richard, Tabak Joël (2015): Direct Stimulatory Effects of Oxytocin in Female Rat Gonadotrophs and Somatotrophs In Vitro: Comparison With Lactotrophs. Endocrinology, 156, 600-612 https://doi.org/10.1210/en.2014-1543
Gorski K., Romanowicz K., Herman A., Molik E., Gajewska A., Tomaszewska-Zaremba D., Misztal T. (2010): The possible involvement of salsolinol and hypothalamic prolactin in the central regulatory processes in ewes during lactation. Reproduction in Domestic Animals, 45, e54–e60.
Górski K., Marciniak E., Zielińska-Górska M., Misztal T. (2016): Salsolinol Up-Regulates Oxytocin Expression and Release During Lactation in Sheep. Journal of Neuroendocrinology, 28, n/a-n/a https://doi.org/10.1111/jne.12362
Hashizume T., Shida R., Suzuki S., Nonaka S., Yonezawa C., Yamashita T., Kasuya E., Sutoh M., Oláh M., Székács D., Nagy G.M. (2008): Salsolinol is present in the bovine posterior pituitary gland and stimulates the release of prolactin both in vivo and in vitro in ruminants. Domestic Animal Endocrinology, 34, 146-152 https://doi.org/10.1016/j.domaniend.2006.12.003
Hasiec Małgorzata, Herman Andrzej P., Molik Edyta, Dobek Elżbieta, Romanowicz Katarzyna, Fülöp Ferenc, Misztal Tomasz (2012): The stimulatory effect of salsolinol on prolactin gene expression within the anterior pituitary of lactating sheep: In vivo and in vitro study. Small Ruminant Research, 102, 202-207 https://doi.org/10.1016/j.smallrumres.2011.07.011
Homicskó Krisztián Gy, Kertész István, Radnai Balázs, Tóth Béla E, Tóth Géza, Fülöp Ferenc, Fekete Márton I.K, Nagy György M (2003): Binding site of salsolinol: its properties in different regions of the brain and the pituitary gland of the rat. Neurochemistry International, 42, 19-26 https://doi.org/10.1016/S0197-0186(02)00063-3
Ivell Richard, Kimura Tadashi, Müller Dieter, Augustin Kai, Abend Nicole, Bathgate Ross, Telgmann Ralph, Balvers Marga, Tillmann Gina, Fuchs Anna-Riitta (): The structure and regulation of the oxytocin receptor. Experimental Physiology, 86, 289-296 https://doi.org/10.1113/eph8602185
Jeng Y.-J., Soloff M. S. (): Characterization of the Cyclic Adenosine Monophosphate Target Site in the Oxytocin Receptor Gene in Rabbit Amnion. Biology of Reproduction, 81, 473-479 https://doi.org/10.1095/biolreprod.109.077941
Kennett J. E., McKee D. T. (2012): Oxytocin: An Emerging Regulator of Prolactin Secretion in the Female Rat. Journal of Neuroendocrinology, 24, 403-412 https://doi.org/10.1111/j.1365-2826.2011.02263.x
Kennett Jessica E., Poletini Maristela O., Fitch Cheryl A., Freeman Marc E. (2009): Antagonism of Oxytocin Prevents Suckling- and Estradiol-Induced, But Not Progesterone-Induced, Secretion of Prolactin. Endocrinology, 150, 2292-2299 https://doi.org/10.1210/en.2008-1611
Kochman K. (2013): Neurohormones: oxytocin, vasopressin and related peptides – structure, genes, receptors, and evolution. Journal of Animal and Feed Sciences, 22, 283-294 https://doi.org/10.22358/jafs/65915/2013
Marnet Pierre-Guy, Negrao Joao-Alberto, Labussière Jacques (1998): Oxytocin release and milk ejection parameters during milking of dairy ewes in and out of natural season of lactation. Small Ruminant Research, 28, 183-191 https://doi.org/10.1016/S0921-4488(97)00075-8
McKee De’Nise T., Poletini Maristela O., Bertram Richard, Freeman Marc E. (2007): Oxytocin Action at the Lactotroph Is Required for Prolactin Surges in Cervically Stimulated Ovariectomized Rats. Endocrinology, 148, 4649-4657 https://doi.org/10.1210/en.2007-0646
Misztal T., Gorski K., Tomaszewska-Zaremba D., Molik E., Romanowicz K. (2008): Identification of salsolinol in the mediobasal hypothalamus of lactating ewes and its relation to suckling-induced prolactin and GH release. Journal of Endocrinology, 198, 83-89 https://doi.org/10.1677/JOE-07-0640
Misztal Tomasz, Górski Konrad, Tomaszewska-Zaremba Dorota, Fülöp Ferenc, Romanowicz Katarzyna (2010): Effects of a structural analogue of salsolinol, 1-MeDIQ, on pituitary prolactin release and dopaminergic activity in the mediobasal hypothalamus in nursing sheep. Brain Research, 1307, 72-77 https://doi.org/10.1016/j.brainres.2009.10.033
Nakamura Kazuaki, Fujiwara Yoko, Mizutani Reiko, Sanbe Atsushi, Miyauchi Noriko, Hiroyama Masami, Yamauchi Junji, Yamashita Tatsuya, Nakamura Shigeki, Mori Toyoki, Tsujimoto Gozoh, Tanoue Akito (2008): Effects of Vasopressin V1b Receptor Deficiency on Adrenocorticotropin Release from Anterior Pituitary Cells in Response to Oxytocin Stimulation. Endocrinology, 149, 4883-4891 https://doi.org/10.1210/en.2007-1528
Pfaffl Michael W., Tichopad Ales, Prgomet Christian, Neuvians Tanja P. (2004): Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper – Excel-based tool using pair-wise correlations. Biotechnology Letters, 26, 509-515 https://doi.org/10.1023/B:BILE.0000019559.84305.47
Qui&ntilde;ones-Jenab Vanya, Jenab Shirzad, Ogawa Sonoko, Adan Roger A.M., Burbach Peter H., Pfaff Donald W. (1997): Effects of Estrogen on Oxytocin Receptor Messenger Ribonucleic Acid Expression in the Uterus, Pituitary, and Forebrain of the Female Rat. Neuroendocrinology, 65, 9-17 https://doi.org/10.1159/000127160
Radnai Balázs, Kandár Zoltán, Somogyvári-Vigh Anikó, Mergl Zsuzsanna, Oláh Márk, Fülöp Ferenc, Vecsernyés Miklós, Nagy György M. (2005): Salsolinol induces a decrease in cyclic AMP at the median eminence and an increase at the adenohypophysis in lactating rats. Brain Research Bulletin, 65, 105-110 https://doi.org/10.1016/j.brainresbull.2004.11.007
Sabatier N., Rowe I., Leng G. (): Central release of oxytocin and the ventromedial hypothalamus. Biochemical Society Transactions, 35, 1247- https://doi.org/10.1042/BST0351247
Samson W.K., Schell D.A. (1995): Oxytocin and the anterior pituitary gland. Advances in Experimental Medicine and Biology, 395, 355–364.
SAMSON WILLIS K., LUMPKIN MICHAEL D., McCANN SAMUEL M. (1986): Evidence for a Physiological Role for Oxytocin in the Control of Prolactin Secretion*. Endocrinology, 119, 554-560 https://doi.org/10.1210/endo-119-2-554
Schlosser S F, Almeida O F, Patchev V K, Yassouridis A, Elands J (1994): Oxytocin-stimulated release of adrenocorticotropin from the rat pituitary is mediated by arginine vasopressin receptors of the V1b type.. Endocrinology, 135, 2058-2063 https://doi.org/10.1210/endo.135.5.7956927
Tabak Joël, Gonzalez-Iglesias Arturo E., Toporikova Natalia, Bertram Richard, Freeman Marc E. (2010): Variations in the Response of Pituitary Lactotrophs to Oxytocin during the Rat Estrous Cycle. Endocrinology, 151, 1806-1813 https://doi.org/10.1210/en.2009-1267
Tóth B. E., Homicskó K., Radnai B., Maruyama W., DeMaria J. E., Vecsernyés M., Fekete M. I. K., Fülöp F., Naoi M., Freeman M. E., Nagy G. M. (2001): Salsolinol is a Putative Endogenous Neuro-intermediate Lobe Prolactin-Releasing Factor. Journal of Neuroendocrinology, 13, 1042-1050 https://doi.org/10.1046/j.1365-2826.2001.00725.x
Traczyk W., Przekop F. (1963): A method for testing the function of the hypothalamus and pituitary in the sheep in chronic experiments. Acta Physiologica Polonica, 14, 227–236.
Untergasser A., Cutcutache I., Koressaar T., Ye J., Faircloth B. C., Remm M., Rozen S. G. (): Primer3--new capabilities and interfaces. Nucleic Acids Research, 40, e115-e115 https://doi.org/10.1093/nar/gks596
Welento J., Szteyn S., Milart Z. (1969): Observations on the stereotaxic configuration of the hypothalamus nuclei in the sheep. Anatomischer Anzeiger, 124, 1–27.
Yang Hai-Peng, Wang Liwei, Han Liqun, Wang Stephani C. (2013): Nonsocial Functions of Hypothalamic Oxytocin. ISRN Neuroscience, 2013, 1-13 https://doi.org/10.1155/2013/179272
Zingg Hans H., Laporte Stephane A. (2003): The oxytocin receptor. Trends in Endocrinology & Metabolism, 14, 222-227 https://doi.org/10.1016/S1043-2760(03)00080-8
download PDF

© 2019 Czech Academy of Agricultural Sciences