The effects of mu-, delta- and kappa-opioid receptor activation on in vitro prolactin secretion by anterior pituitary cells of cyclic gilts
K. Kościukiewicz 1,   B. Wylot 1,   W. Czelejewska 1,   P. Gilun 2,   S. Okrasa 1  
More details
Hide details
University of Warmia and Mazury in Olsztyn, Faculty of Biology and Biotechnology, Department of Animal Anatomy and Physiology, Oczapowskiego 1A, 10-719 Olsztyn, Poland
Institute of Animal Reproduction and Food Research of PAS, Department of Local Physiological Regulations, Tuwima 10, 10-748 Olsztyn, Poland
S. Okrasa   

University of Warmia and Mazury in Olsztyn, Faculty of Biology and Biotechnology, Department of Animal Anatomy and Physiology, Oczapowskiego 1A, 10-719 Olsztyn, Poland
Publication date: 2018-06-13
J. Anim. Feed Sci. 2018;27(2):114–122
The aim of the study was to determine an in vitro effect of specific agonists of opioid receptors on basal prolactin secretion and in the presence of dopamine or thyreoliberin (TRH) by porcine anterior pituitary cells. The cells were isolated from anterior pituitaries of gilts on days 8–10, 15–17 and 19–21 of the oestrous cycle and submitted to in vitro culture with mu-, delta- and kappa opioid receptor agonists – FK 33-824, DPLPE and U 50,488, respectively. Differentiated effects of the opioid agonists on prolactin secretion by isolated pituitary cells of gilts in chosen days of the oestrous cycle were shown. In the midluteal phase (days 8–10), a reduced prolactin secretion was demonstrated after activation of mu-, delta- and kappa-opioid receptors under all tested conditions. In the early follicular phase (days 15–17), the activation of mu-, delta- and kappa-opioid receptors increased prolactin secretion under basal conditions, as well as mu- and delta-opioid receptors – in the presence of TRH, but the stimulation of mu- and kappa-opioid receptors reduced the hormone secretion in the presence of dopamine. In the late follicular phase (days 19–21), kappa-opioid receptor agonist stimulated prolactin secretion under all tested conditions. The activation of mu- and delta-opioid receptors increased prolactin secretion under basal conditions and in the presence of dopamine, but decreased – in the presence of TRH. The results suggest a possibility of diverse participation of endogenous opioids, depending on stage of the oestrous cycle, in the modulation of prolactin secretion at the pituitary level in gilts during the oestrous cycle.
Akil H., Owens C., Gutstein H., Taylor L., Curran E., Watson S., 1998. Endogenous opioids: overview and current issues. Drug Alcohol Depend. 51, 127–140, https://doi.org/10.1016/S0376-....
Akil H., Watson S.J., Young E., Lewis M.E., Khachaturian H., Walker J.M., 1984. Endogenous opioids: biology and function. Ann. Rev. Neurosci. 7, 223–255, https://doi.org/10.1146/annure....
Akins E.L., Morrissette M.C., 1968. Gross ovarian changes during estrous cycle of swine. Am. J. Vet. Res. 29, 1953–1957.
Armstrong J.D., Kraeling R.R., Britt J.H., 1988. Effects of naloxone or transient weaning on secretion of LH and prolactin in lactating sows. J. Reprod. Fertil. 83, 301–308, https://doi.org/10.1530/jrf.0.....
Barb C.R., Barrett J.B., Wright J.T., Kraeling R.R., Rampacek G.B., 1990. Opioid modulation of LH secretion by pig pituitary cells in vitro. J. Reprod. Fertil. 90, 213–219, https://doi.org/10.1530/jrf.0.....
Barb C.R., Kraeling R.R., Rampacek G.B., 1991. Opioid modulation of gonadotropin and prolactin secretion in domestic farm animals. Domest. Anim. Endocrinol. 8, 15–27, https://doi.org/10.1016/0739-7....
Barb C.R., Kraeling R.R., Rampacek G.B., Whisnant C.S., 1986. Influence of stage of the estrous cycle on endogenous opioid modulation of luteinizing hormone, prolactin, and cortisol secretion in the gilt. Biol. Reprod. 35, 1162–1167, https://doi.org/10.1095/biolre....
Bentley A.M., Wallis M., 1986. Effects of two enkephalin analogues, morphine sulphate, dopamine and naloxone on prolactin secretion from rat anterior pituitary glands in vitro. J. Endocrinol. 109, 313–320, https://doi.org/10.1677/joe.0.....
Bogacka I., Siawrys G., Okrasa S., Kaminski T., Przala J., 2002. The influences of GnRH, oxytocin and vasoactive intestinal peptide on LH and PRL secretion by porcine pituitary cells. J. Physiol. Pharmacol. 53, 439–451.
Brinkley H.J., 1981. Endocrine signaling and female reproduction. Biol. Reprod. 24, 22–43, https://doi.org/10.1095/biolre....
Buydens P., Velkeniers B., Golstein J., Vanhaelst L., 1986. Dissociation of the central and peripheral effects of naloxone on PRL secretion. Horm. Metab. Res. 18, 575–576, https://doi.org/10.1055/s-2007....
Curlewis J.D., Naylor A.M., Rhind S.M., McNeilly A.S., 1991. Effects of beta-endorphin on pulsatile luteinizing hormone and prolactin secretion during the follicular phase in the ewe. J. Neuroendocrinol. 3, 123–126, https://doi.org/10.1111/j.1365....
De Rensis F., Cosgrove J.R., Foxcroft G.R., 1993. Luteinizing hormone and prolactin responses to naloxone vary with stage of lactation in the sow. Biol. Reprod. 48, 970–976, https://doi.org/10.1095/biolre....
Dusza L., Ciereszko R., 2007. Gonadotropins and prolactin: regulation of secretion and action on target cells. In: T. Krzymowski (Editor). Biology of animal reproduction. Physiological Regulation of Reproductive Processes in Females (in Polish). University of Warmia and Mazury, Olsztyn (Poland), pp. 95–138.
Dusza L., Okrasa S., Ciereszko R., Kotwica G., Tilton J.E., 1988. Endocrine changes associated with spontaneous luteolysis in sows. I. Temporal relationships among prolactin, prostaglandin F2α, progesterone and LH. Anim. Reprod. Sci. 17, 115–122, https://doi.org/10.1016/0378-4....
Dusza L., Krzymowska H., 1979. Plasma prolactin concentrations during the oestrous cycle of sows. J. Reprod. Fertil. 57, 511–514, https://doi.org/10.1530/jrf.0.....
Dziekoński M., Żmijewska A., Franczak A., Kotwica G., Czelejewska W., Okrasa S., 2015a. The expression of mRNAs for opioid precursors in endometrium of cyclic and early pregnant pigs; effects of IL-1β, IL-6 and TNFα. J. Anim. Feed Sci. 24, 118–126, https://doi.org/10.22358/jafs/....
Dziekoński M., Żmijewska A., Franczak A., Kotwica G., Kościukiewicz K., Czelejewska W., Okrasa S., 2015b. The expression of mRNAs for opioid receptors in endometrium of cyclic and early pregnant pigs; effects of IL-1β, IL-6 and TNFα. J. Anim. Feed Sci. 24, 332–340, https://doi.org/10.22358/jafs/....
Enjalbert A., Ruberg M., Arancibia S., Priam M., Kordon C., 1979. Endogenous opiates block dopamine inhibition of prolactin secretion in vitro. Nature 280, 595–597, https://doi.org/10.1038/280595....
Freeman M.E., Kanyicska B., Lerant A., Nagy G., 2000. Prolactin: structure, function, and regulation of secretion. Physiol. Rev. 80, 1523–1631, https://doi.org/10.1152/physre....
Giudici D., D’Urso R., Falaschi P., Negri L., Melchiorri P., Motta M., 1984. Dermorphin stimulates prolactin secretion in the rat. Neuroendocrinology 39, 236–244, https://doi.org/10.1159/000123....
Guivarc’h D., Vincent J.-D., Vernier P., 1998. Alternative splicing of the D2 dopamine receptor messenger ribonucleic acid is modulated by activated sex steroid receptors in the MMQ prolactin cell line. Endocrinology 139, 4213–4221, https://doi.org/10.1210/endo.1....
Ignacak A., Kasztelnik M., Sliwa T., Korbut R.A., Rajda K., Guzik T.J., 2012. Prolactin – not only lactotrophin. a “new” view of the “old” hormone. J. Physiol. Pharmacol. 63, 435–443.
Joubert-Bression D., Brandi A.M., Birman P., Peillon F., 1990. Effect of oestradiol on dopamine receptors and protein kinase C activity in the rat pituitary: binding of oestradiol to pituitary membranes. Ciba Found Symp. 153, 156–168.
Kaminski T., Siawrys G., Bogacka I., Okrasa S., Przala J., 2004. The influence of opioid peptides on steroidogenesis in porcine granulosa cells. Reprod. Domest. Anim. 39, 25–32, https://doi.org/10.1046/j.1439....
Kimura N., Arai K., Sahara Y., Suzuki H., Kimura N., 1994. Estradiol transcriptionally and posttranscriptionally up-regulates thyrotropin-releasing hormone receptor messenger ribonucleic acid in rat pituitary cells. Endocrinology 134, 432–440, https://doi.org/10.1210/endo.1....
Kotwica G., Staszkiewicz J., Skowroński M.T., Siawrys G., Bogacka I., Franczak A., Kurowicka B., Kraziński B., Okrasa S., 2006. Effects of oxytocin alone and in combination with selected hypothalamic hormones on ACTH, β-endorphin, LH and PRL secretion by anterior pituitary cells of cyclic pigs. Reprod. Biol. 6, 115–131.
Login I.S., Macleod R.M., 1979. Failure of opiates to reverse dopamine inhibition of prolactin secretion in vitro. Eur. J. Pharmacol. 60, 253–255, https://doi.org/10.1016/0014-2....
Mattioli M., Conte F., Galeati G., Seren E., 1986. Effect of naloxone on plasma concentrations of prolactin and LH in lactating sows. J. Reprod. Fertil. 76, 167–173, https://doi.org/10.1530/jrf.0.....
Okrasa S., Weigl R., Jeng M., Tilton J., 1990. Concentrations of prolactin, LH and FSH after naloxone administration in follicular- phase gilts. Anim. Reprod. Sci. 22, 39–46, https://doi.org/10.1016/0378-4....
Okrasa S.C., Tilton J.E., 1992. Concentrations of prolactin and LH after administration of Met-enkephalin analogue (FK 33-824) to gilts during the follicular phase. Anim. Reprod. Sci. 27, 195–207, https://doi.org/10.1016/0378-4....
Satoh M., Minami M., 1995. Molecular pharmacology of the opioid receptors. Pharmacol. Ther. 68, 343–364, https://doi.org/10.1016/0163-7....
Sengupta A., Sarkar D.K., 2012. Estrogen inhibits D2S receptor-regulated Gi3 and Gs protein interactions to stimulate prolactin production and cell proliferation in lactotropic cells. J. Endocrinol. 214, 67–78, https://doi.org/10.1530/JOE-12....
Siawrys G., Bogacka I., Okrasa S., Kamiński T., Przała J., 2003. The effects of GnRH and adrenergic agents on PRL and β-endorphin secretion by porcine pituitary cells in vitro. Acta Vet. Hung. 51, 353–369, https://doi.org/10.1556/AVet.5....
Sosa L.d.V., Gutiérrez S., Petiti J.P., Palmeri C.M., Mascanfroni I.D., Soaje M., De Paul A.L., Torres A.I., 2012. 17β-Estradiol modulates the prolactin secretion induced by TRH through membrane estrogen receptors via PI3K/Akt in female rat anterior pituitary cell culture. Am. J. Physiol. Endocrinol. Metab. 302, 1189–1197, https://doi.org/10.1152/ajpend....
Staszkiewicz J., Skowronski M.T., Siawrys G., Kaminski T., Krazinski B.E., Plonka K., Wylot B., Przala J., Okrasa S., 2007. Expression of proopiomelanocortin, proenkephalin and prodynorphin genes in porcine luteal cells. Acta Vet. Hung. 55, 435–449, https://doi.org/10.1556/AVet.5....
Szafranska B., Tilton J.E., 2000. Free intracellular calcium ([Ca2+]i) in opioid sensitive cells of the porcine anterior pituitary. J. Physiol. Pharmacol. 51, 541–554.
Szafranska B., Ziecik A., Okrasa S., 2002. Primary antisera against selected steroids or proteins and secondary antisera against γ-globulins – an available tool for studies of reproductive processes. Reprod. Biol. 2, 187–204.
Tavakoli-Nezhad M., Arbogast L.A., 2010. Mu and kappa opioid receptor expression in the mediobasal hypothalamus and effectiveness of selective antagonists on prolactin release during lactation. Neuroscience 166, 359–367, https://doi.org/10.1016/j.neur....
Van de Wiel D.F.M., Erkens J., Koops W., Vos E., Van Landeghem A.A., 1981. Periestrous and midluteal time courses of circulating LH, FSH, prolactin, estradiol-17β and progesterone in the domestic pig. Biol. Reprod. 24, 223–233, https://doi.org/10.1095/biolre....
Voigt K.H., Frank D., Düker E., Martin R., Wuttke W., 1983. Dopamine-inhibited release of prolactin and intermediate lobe-POMC-peptides: different modulation by opioids. Life Sci. 33, Suppl. 1, 507–510, https://doi.org/10.1016/0024-3....
Vuong C., Van Uum S.H.M., O’Dell L.E., Lutfy K., Friedman T.C., 2010. The effects of opioids and opioid analogs on animal and human endocrine systems. Endocr. Rev. 31, 98–132, https://doi.org/10.1210/er.200....
Willis H.J., Cosgrove J.R., Foxcroft G.R., 1996. Opioidergic control of luteinizing hormone and prolactin secretion in late gestation in the sow. Biol. Reprod. 55, 318–324, https://doi.org/10.1095/biolre....
Wylot B., Staszkiewicz J., Okrasa S., 2008. The expression of genes coding for opioid precursors, opioid receptors, β-LH subunit and GnRH receptor in the anterior pituitary of cyclic gilts. J. Physiol. Pharmacol. 59, 745–758.
Wylot B., Tworus K., Okrasa S., 2013. The effects of mu-, delta- and kappa-opioid receptor activation on luteinizing and folliclestimulating hormone secretion from porcine pituitary cells. J. Physiol. Pharmacol. 64, 505–511.
The role of neurokinin A and its receptor in the regulation of prolactin secretion by the anterior pituitary of cyclic pigs
Wioleta Czelejewska, Agata Zmijewska, Mariusz Dziekonski, Stanislaw Okrasa
Reproduction in Domestic Animals
Methionine-enkephalin-treatment suppresses the pituitary-ovary axis in the cichlid fish Oreochromis mossambicus
C.B. Ganesh, Vijayalaxmi
Aquaculture Reports