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Sex steroid modulation of cortisol secretion in sheep

Published online by Cambridge University Press:  04 April 2014

E. van Lier ,
M. Carriquiry  and
A. Meikle
E. van Lier*
Affiliation:
Dpto. de Producción Animal y Pasturas, Facultad de Agronomía, Universidad de la República, Avda. E. Garzón 780, 12900 Montevideo, Uruguay Estación Experimental Facultad de Agronomía Salto, Ruta 31 Km 21, 50000 Salto, Uruguay
M. Carriquiry
Affiliation:
Dpto. de Producción Animal y Pasturas, Facultad de Agronomía, Universidad de la República, Avda. E. Garzón 780, 12900 Montevideo, Uruguay
A. Meikle
Affiliation:
Laboratorio de Técnicas Nucleares, Facultad de Veterinaria, Universidad de la República, Lasplaces 1550, 11600 Montevideo, Uruguay
*
†E-mail: evanlier@fagro.edu.uy
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Abstract

There is strong evidence that the gonads modulate the hypothalamic–pituitary–adrenal axis. To investigate these sex differences at the adrenal glands of sheep we compared the cortisol response to ACTH (experiment 1) and measured the relative expression of oestrogen receptor alpha (ERS1), androgen receptor (AR), melanocortin 2 receptor (MC2R) and steroid acute regulatory protein (STAR) mRNA in adrenal glands (experiment 2) of gonadectomised rams and ewes either with or without sex steroid replacement. In experiment 1 six castrated adult rams and four ovariectomised adult ewes were used in two ACTH trials. On each trial blood samples were taken every 15 min for 4 h through an indwelling jugular catheter and each animal received 0.5 mg of an ACTH analogue i.v., immediately after the sample at 1 h from the beginning of the trial. Four days after the first trial the males received 100 mg of Testosterone Cyclopentilpropionate (TC) i.m. and the females received 2.5 mg of Oestradiol Benzoate (EB) i.m. At 72 h after TC or EB administration the second trial was performed. In experiment 2 the adrenal glands were obtained from gonadectomised adult rams (n=8) and adult ewes (n=8). Four rams received 100 mg of TC i.m. and four females received 0.5 mg of EB i.m. Blood samples were taken at 0, 12, 24, 48 and 72 h relative to steroid replacement and the animals were thereafter slaughtered. Cortisol, testosterone and 17β-oestradiol were determined by radioimmunoanalysis. The transcripts of ERS1, AR, MC2R and STAR were determined by real-time reverse transcription PCR in adrenal tissue. Cortisol secretion was higher in female sheep than in male sheep, and higher in EB-treated than non-treated ewes. No difference in cortisol secretion was observed between TC-treated and non-treated rams. Gonadectomised rams treated with TC presented greater AR mRNA and MC2R mRNA expression than males without the steroid replacement. Gonadectomised ewes treated with EB tended to present lower AR mRNA than the ones without steroid replacement. Gonadectomised rams with TC also had greater AR mRNA, ERS1 mRNA and MC2R mRNA expression than ewes treated with EB. The relative amount of STAR transcript was not different among the different groups. The results confirm sex differences in ACTH-induced cortisol secretion in sheep, as well as in the expression of the receptor proteins for both 17β-oestradiol and testosterone in the sheep adrenal gland. However, the underlying mechanisms for sex steroid modulation remain unresolved.

Keywords

sex steroidsgonadectomyadrenalreceptorssheep
Type
Full Paper
Information
animal , Volume 8 , Issue 6 , June 2014 , pp. 960 - 967
Copyright
© The Animal Consortium 2014 

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References

Adams, NR, Atkinson, HC, Hoskinson, RM, Abordi, JA, Briegel, JR, Jones, M and Sanders, MR 1990. Immunization of ovariectomized ewes against progesterone, oestrogen or cortisol to detect effects of adrenal steroids on reproduction. Journal of Reproduction and Fertility 89, 477–483.CrossRefGoogle ScholarPubMed
Atkinson, HC and Waddell, BJ 1997. Circadian variation in basal plasma corticosterone and adrenocorticotropin in the rat: sexual dimorphism and changes across the estrous cycle. Endocrinology 138, 3842–3848.Google Scholar
Bentvelsen, FM, McPhaul, MJ, Wilson, CM, Wilson, JD and George, FW 1996. Regulation of immunoreactive androgen receptor in the adrenal gland of the adult rat. Endocrinology 137, 2659–2663.Google Scholar
Broadbear, JH, Pierce, BN, Clarke, IJ and Canny, BJ 2005. Role of sex and sex steroids in mediating pituitary-adrenal responses to acute buspirone treatment in sheep. Journal of Neuroendocrinology 17, 804–810.Google Scholar
Burgess, LH and Handa, RJ 1992. Chronic estrogen-induced alterations in adrenocorticotropin and corticosterone secretion, and glucocorticoid receptor-mediated functions in female rats. Endocrinology 131, 1261–1269.Google Scholar
Calandra, RS, Purvis, K, Naess, O, Attramadal, A, Djøseland, O and Hansson, V 1978. Androgen receptors in the rat adrenal gland. Journal of Steroid Biochemistry 9, 1009–1015.CrossRefGoogle ScholarPubMed
Canny, BJ, O’Farrell, KA, Clarke, IJ and Tilbrook, AJ 1999. The influence of sex and gonadectomy on the hypothalamo-pituitary-adrenal axis of the sheep. Journal of Endocrinology 162, 215–225.CrossRefGoogle ScholarPubMed
Carriquiry, M, Weber, WJ, Fahrenkrug, SC and Crooker, BA 2009. Hepatic gene expression in multiparous Holstein cows treated with bovine somatotropin and fed n-3 fatty acids in early lactation. Journal of Dairy Science 92, 4889–4900.CrossRefGoogle ScholarPubMed
Chen, Y, Green, JA, Antoniou, E, Ealy, AD, Mathialagan, N, Walker, AM, Avalle, MP, Rosenfeld, CS, Hearne, LB and Roberts, RM 2006. Effect of interferon-tau administration on endometrium of nonpregnant ewes: a comparison with pregnant ewes. Endocrinology 147, 2127–2137.Google Scholar
Clark, JH, Schrader, WT and O’Malley, BW 1992. Mechanisms of steroid hormone action. In Textbook of endocrinology (ed. JD Wilson and DW Foster), pp. 35–90. WB Saunders, Philadelphia, PA, USA.Google Scholar
Cutler, GB Jr, Barnes, KM, Sauer, MA and Loriaux, DL 1978. Estrogen receptor in rat adrenal gland. Endocrinology 102, 252–257.CrossRefGoogle ScholarPubMed
Dyson, MT, Kowalewski, MP, Manna, PR and Stocco, DM 2009. The differential regulation of steroidogenic acute regulatory protein-mediated steroidogenesis by type I and type II PKA in MA-10 cells. Molecular and Cellular Endocrinology 300, 94–103.Google Scholar
Figueiredo, HF, Ulrich-Lai, YM, Choi, DC and Herman, JP 2007. Estrogen potentiates adrenocortical responses to stress in female rats. American Journal of Physiology Endocrinology and Metabolism 292, E1173–E1182.Google Scholar
Gay, E, Campbell, S, McNeilly, A and Duncan, WC 2007. Sexually dimorphic expression of androgen receptors in the fetal sheep adrenal gland. Biology of Reproduction 77, 119–120.Google Scholar
Handa, RJ, Burgess, LH, Kerr, JE and O’Keefe, JA 1994. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Hormones and Behavior 28, 464–476.Google Scholar
Hiroi, H, Christenson, LK and Strauss, JF III 2004. Regulation of transcription of the steroidogenic acute regulatory protein (StAR) gene: temporal and spatial changes in transcription factor binding and histone modification. Molecular and Cellular Endocrinology 215, 119–126.Google Scholar
Hirst, JJ, West, NB, Brenner, RM and Novy, MJ 1992. Steroid hormone receptors in the adrenal glands of fetal and adult Rhesus monkeys. Journal of Clinical Endocrinology and Metabolism 75, 308–314.Google Scholar
Jaquiery, AL, Oliver, MH, Bloomfield, FH, Connor, KL, Challis, JRG and Harding, JE 2006. Fetal exposure to excess glucocorticoid is unlikely to explain the effects of periconceptional undernutrition in sheep. Journal of Physiology 572, 109–118.Google Scholar
Kitay, JI 1961. Sex differences in adrenal cortical secretion in the rat. Endocrinology 68, 818–824.Google Scholar
Kitay, JI 1963. Pituitary-adrenal function in the rat after gonadectomy and gonadal hormone replacement. Endocrinology 73, 253–260.Google Scholar
Korte, SM, Koolhaas, JM, Wingfield, JC and McEwen, BS 2005. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neuroscience and Biobehavioral Reviews 29, 3–38.CrossRefGoogle ScholarPubMed
Manna, P, Dyson, M and Stocco, D 2009. Regulation of the steroidogenic acute regulatory protein gene expression: present and future perspectives. Molecular Human Reproduction 15, 321–333.Google Scholar
McCormick, CM, Furey, BF, Child, M, Sawyer, MJ and Donohue, SM 1998. Neonatal sex hormones have ‘organizational’ effects on the hypothalamic-pituitary-adrenal axis of male rats. Developmental Brain Research 105, 295–307.Google Scholar
Medlock, KL, Forrester, MT and Sheehan, DM 1994. Progesterone and estradiol interaction in the regulation of rat uterine weight and estrogen receptor concentrations. Proceedings of the Society for Experimental Biology and Medicine 205, 145–153.Google Scholar
Meikle, A, Tasende, C, Rodríguez, M and Garófalo, EG 1997. Effects of oestradiol and progesterone on the reproductive tract and on uterine sex steroid receptors in female lambs. Theriogenology 48, 1105–1113.Google Scholar
Meikle, A, Forsberg, M, Sahlin, L, Masironi, B, Tasende, C, Rodriguez-Pinon, M and Garófalo, E 2000. A biphasic action of estradiol on estrogen and progesterone receptor expression in the lamb uterus. Reproduction Nutrition Development 40, 283–294.Google Scholar
Myers, DA, Hyatt, K, Mlynarczyk, M, Bird, IM and Ducsay, CA 2005. Long-term hypoxia represses the expression of key genes regulating cortisol biosynthesis in the near-term ovine fetus. American Journal of Physiology Regulatory Integrative and Comparative Physiology 289, R1707–R1714.Google Scholar
Nowak, KW, Neri, G, Nussdorfer, GG and Malendowicz, LK 1995. Effects of sex hormones on the steroidogenic activity of dispersed adrenocortical cells of the rat adrenal cortex. Life Sciences 57, 833–837.CrossRefGoogle ScholarPubMed
Ogilvie, KM and Rivier, C 1997. Gender difference in hypothalamic-pituitary-adrenal axis response to alcohol in the rat: activational role of gonadal steroids. Brain Research 766, 19–28.Google Scholar
Rifka, SM, Cutler, GB Jr, Sauer, MA and Loriaux, DL 1978. Rat adrenal androgen receptor: a possible mediator of androgen-induced decrease in rat adrenal weight. Endocrinology 103, 1103–1110.Google Scholar
Sanford, LM, Palmer, WM and Howland, BE 1977. Changes in the profiles of serum LH, FSH and testosterone, and in mating performance and ejaculate volume in the ram during the ovine breeding season. Journal of Animal Science 45, 1382–1391.Google Scholar
Schams, D, Kohlenberg, S, Amselgruber, W, Berisha, B, Pfaffl, MW and Sinowatz, F 2003. Expression and localisation of oestrogen and progesterone receptors in the bovine mammary gland during development, function and involution. Journal of Endocrinology 177, 305–317.Google Scholar
Spencer, TE and Bazer, FW 1995. Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe. Biology of Reproduction 53, 1527–1543.Google Scholar
Tilbrook, AJ, Canny, BJ, Serapiglia, MD, Ambrose, TJ and Clarke, IJ 1999. Suppression of the secretion of luteinizing hormone due to isolation/restraint stress in gonadectomised rams and ewes is influenced by sex steroids. Journal of Endocrinology 160, 469–481.Google Scholar
Turner, A, Canny, BJ, Hobbs, RJ, Bond, JD, Clarke, IJ and Tilbrook, AJ 2002. Influence of sex and gonadal status of sheep on cortisol secretion in response to ACTH and on cortisol and LH secretion in response to stress: importance of different stressors. Journal of Endocrinology 173, 113–122.Google Scholar
Uhart, M, Chong, RY, Oswald, L, Lin, P-I and Wand, GS 2006. Gender differences in hypothalamic-pituitary-adrenal (HPA) axis reactivity. Psychoneuroendocrinology 31, 642–652.Google Scholar
Van Lier, E, Pérez-Clariget, R and Forsberg, M 2003a. Sex differences in cortisol secretion after administration of an ACTH analogue in sheep during the breeding and non-breeding season. Animal Reproduction Science 79, 81–92.Google Scholar
Van Lier, E, Meikle, A, Bielli, A, Akerberg, S, Forsberg, M and Sahlin, L 2003b. Sex differences in oestrogen receptor levels in adrenal glands of sheep during the breeding season. Domestic Animal Endocrinology 25, 373–387.Google Scholar
Verkerk, GA and Mcmillan, KL 1997. Adrenocortical responses to an adrenocorticotropic hormone in bulls and steers. Journal of Animal Science 75, 2520–2525.Google Scholar
Viau, V and Meaney, MJ 1991. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 129, 2503–2511.CrossRefGoogle ScholarPubMed
Viau, V and Meaney, MJ 1996. The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area. Journal of Neuroscience 16, 1866–1876.Google Scholar
Young, EA 1995. The role of gonadal steroids in hypothalamic-pituitary-adrenal axis regulation. Critical Reviews in Neurobiology 9, 371–381.Google Scholar
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