Biology of Reproduction 61, 1575-1580 (1999)
©Copyright 1999 Society for the Study of Reproduction, Inc.
Seasonal Variation and Opioidergic Regulation of Growth Hormone Release in Cyclic, Ovariectomized, and Pregnant Pony Mares1
Christine Aurich2,a,
Tanja Gerlachb,
Jörg E. Aurichc, and
Nahid Parvizib
a Institute for Animal Breeding and Genetics, University of Veterinary Sciences, 1210 Vienna, Austria
b Institute for Animal Science and Animal Behaviour (FAL), Mariensee, 31535 Neustadt, Germany
c Clinic for Obstetrics, Gynecology and Andrology, University of Veterinary Sciences, 1210 Vienna, Austria
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ABSTRACT
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Modulation of reproductive functions is one of the multiple effects of growth hormone (GH). To investigate effects of reproductive functions on GH release in the horse, plasma GH concentrations in ovary-intact (n = 7) and ovariectomized (n = 8) mares during the anovulatory and breeding seasons and in pregnant mares (n = 6) at various stages of gestation were determined. To analyze an opioidergic regulation of GH release, repeated blood samples were taken over 3 h, and mares were injected with the opioid antagonist naloxone (0.5 mg/kg i.v.) or saline. GH was determined by RIA with an antiserum raised against porcine GH and equine GH as standard. In ovariectomized and ovary-intact, cyclic mares, GH concentrations were low and not different between the two groups in November and December. GH concentrations increased significantly (P < 0.05) in cyclic mares during May and June but were not affected by stage of the cycle and were low in ovariectomized mares. In pregnant mares, plasma GH concentrations remained high throughout pregnancy and did not decrease during winter but increased significantly (P < 0.05) postpartum. Naloxone induced a significant GH release in ovary-intact mares; this response was most pronounced (P < 0.05) during the breeding season. Naloxone did not affect GH in ovariectomized mares. During pregnancy, naloxone induced a significant release of GH around Day 280 (P < 0.05) but not at other times of pregnancy. In conclusion, GH release is influenced by season. The seasonal changes depend on ovarian factors, are absent in ovariectomized mares, and can be modulated by pregnancy. GH release is regulated at least in part by opioidergic pathways.
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INTRODUCTION
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There is substantial evidence that growth hormone (GH, somatotropin) modulates reproductive functions by acting at different levels including the central nervous system, pituitary, and ovaries. In women treated for amenorrhea, the ovarian response to gonadotropins was improved by the concomitant use of GH [1]; in 50% of gilts treated with recombinant GH, ovulation rate was increased [2]. It has been suggested that GH increases LH binding in the follicles and thus prevents follicular atresia and increases ovulation rate [3]. In contrast, prolonged exposure to high GH levels in women [4] and mice [5] can also negatively affect fertility. GH release from the anterior pituitary is stimulated by GH-releasing hormone and inhibited by somatostatin. The regulation of GH release is affected by gonadal steroids. A reduction in plasma GH concentrations following castration was found in male rats [6], bulls [7], and bitches [8, 9]. Testosterone and estradiol replacement in castrated rats [6], progesterone treatment in ovariectomized bitches [9], and estradiol treatment in intact heifers [10] stimulated GH release. In addition, endogenous and exogenous opioids or their antagonists have been shown to influence GH release in rats, cattle, and pigs. In these studies, opioid antagonists either decreased [11–15] or increased [16] plasma GH concentrations. In Holstein calves, the opioidergic regulation of GH secretion undergoes seasonal changes, and the opioid antagonist naloxone enhances GH release in October and November but not in April [17]. The aim of the present study was to investigate the opioidergic regulation of GH release and the possible influence of seasonal changes, the state of the estrous cycle, and pregnancy in the horse. Ovariectomized and ovary-intact pony mares were used during the anovulatory and the breeding season, and pregnant mares were studied at various stages of pregnancy.
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MATERIALS AND METHODS
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Animals
The animals used in this study were nonlactating Shetland pony mares, aged 8.9 ± 2.6 yr (± SD) and weighing 165 ± 7 kg (± SD). Ponies were kept as a single group in a spacious stable and had permanent access to an outdoor paddock. They were fed hay and mineral supplements, and water was freely available. Seven mares were ovary intact, and eight mares had been ovariectomized by laparotomy using standard surgical procedures between 12 and 14 mo before the first experiment. After completion of the first series of experiments, all cyclic mares were mated to a Shetland stallion. Six of the seven mares became pregnant between 23 June and 30 July 1997 and foaled between 18 May and 14 June 1998. The average gestation length was 329.8 ± 8.5 days (± SD).
Experimental Procedures
Ovary-intact pony mares were checked for ovarian activity by monitoring plasma progesterone concentrations in blood samples taken at weekly intervals, beginning on 31 October 1996. When plasma progesterone concentrations after 1 January 1997 in at least one sample had reached a value > 3 nM, indicating the presence of a corpus luteum, blood samples were taken twice weekly. In addition, mares were checked for estrous behavior every second day with a vigorous Shetland stallion. Because of the size of the animals, ovarian function in nonpregnant mares was not examined by repeated transrectal palpation. For the experiment in pregnant mares, pregnancy was confirmed by transrectal ultrasonography on Days 18 and 45 after mating.
Experiments in nonpregnant mares were performed in November and December 1996 (nonbreeding season), in May and June 1997 (breeding season) and, in pregnant mares, on Days 26.4 ± 0.6, 75.4 ± 5.4, 171.8 ± 2.4, 226.2 ± 4.8, 282.7 ± 3.4, and 319.8 ± 2.1 of gestation as well as at 2 days postpartum. Experiments in ovary-intact, cyclic mares were performed during the second estrus and diestrus of the breeding season.
Experiments always began between 0800 and 0900 h, and during blood sampling the ponies remained in their stable. An indwelling catheter was placed in a jugular vein 15 min before the first blood sample was withdrawn. Blood for determination of GH was withdrawn at 15-min intervals for 180 min. After 60 min of sampling, 80 mg naloxone-hydrochloride (Sigma Chemicals, Deisenhofen, Germany) per animal or 6 ml saline was injected i.v. via the catheter. Naloxone was freshly dissolved in 6 ml saline and filter sterilized immediately before the injection. The dose of naloxone corresponded to 0.5 mg/kg body weight. Immediately after withdrawal, blood samples were centrifuged for 20 min at 1000 x g, and plasma was frozen at -20°C until hormone analysis. Mares were used as their own controls and were treated with both naloxone and saline. The interval between these two treatments in the same animal was 2–4 days. The order of treatments was always randomized, with half of the animals receiving naloxone first and half receiving saline injections first. In ovary-intact mares during the breeding season, the saline and naloxone applications were performed during both estrus and diestrus. On Day 2 after foaling, basal GH concentration but not the GH response to naloxone was determined.
Hormone Assays
Concentrations of GH in plasma were determined in duplicate by a double-antibody RIA as described by Bauer and Parvizi [18] with the modification that highly purified equine GH (Dr. A.F. Parlow, Harbor-UCLA Medical Center, Torrance, CA) was used as standard and for iodination. An antibody raised against porcine GH (Biogenesis, Poole, England) was used as first antibody. All reagents were diluted in assay buffer (0.01 M PBS, 0.025 M EDTA, 0.01% [w:v] thimerosal, 1% [w:v] egg albumin, pH 7.4). Measurements were performed using 100 µl plasma. Cross-reactivity with equine GH was 95%, and intra- and interassay coefficients of variation were 7.5% and 15.0%, respectively. The lower limit of detection was 0.2 ng/ml. The recovery rate of standard added to equine plasma ranged between 89% and 104%. Samples from each of the animals were analyzed in one assay.
Progesterone was determined by RIA after extraction from plasma with n-hexane as described previously [19]. The intra- and interassay coefficients of variation were 4.5% and 7.9%, respectively, and the minimal detectable concentration was 0.16 nM.
Statistical Analysis
For comparisons of basal GH concentrations, values from control experiments were used, and basal GH concentrations were calculated as the mean of the three samples taken before injection of saline. GH release in response to naloxone or saline in individual mares was calculated as the area under the curve (ng/ml per min) for the time period from immediately before to 120 min after injection of naloxone and saline. The preinjection baseline was subtracted from the value for each postinjection sample. All statistical comparisons were made with the SPSS/PC/+ statistics package [20]. Because no assumption was made about the distribution of data, nonparametric tests were used throughout. Basal hormone concentrations in ovary-intact, ovariectomized, and pregnant mares were compared by Friedman's two-way ANOVA. Comparisons of basal GH concentrations in the same animals at different times of the year, as well as comparisons between GH release in response to naloxone and saline, were made by Wilcoxon matched pairs rank sum test. Data given are means ± SEM.
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RESULTS
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Estrous Cycle and Plasma Progesterone Concentrations
Of the 7 mares, 3 had low plasma progesterone concentrations from the beginning of the experimental period (on 31 October). In the remaining mares, plasma progesterone concentrations fell below 3 nM between 5 and 15 November. Plasma progesterone concentrations of more than 3 nM, indicating the presence of a corpus luteum after the first ovulation of the breeding season, were found on 12 (n = 4), 22 (n = 2), and 24 May (n = 1). Progesterone levels were, as expected, significantly higher during the luteal phase than during either estrus or the anovulatory season (P < 0.01; Table 1). Naloxone treatment during estrus had no effects on subsequent progesterone secretion.
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TABLE 1. Progesterone (P) concentrations (mean ± SEM) in plasma of ovary-intact mares (n = 7) during estrus and diestrus (May/June) and during the anovulatory season (November/December)
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Basal GH Concentrations
In ovary-intact mares, basal plasma GH concentrations were significantly lower outside the breeding season (November/December) than during the breeding season (May/June: P < 0.05). In ovariectomized pony mares, GH concentrations remained low throughout the year. Therefore, in May, plasma GH concentrations were significantly higher in ovary-intact than in ovariectomized mares (P < 0.05). During pregnancy, basal plasma GH concentrations remained significantly higher than in nonpregnant cyclic mares in December and in ovariectomized mares throughout the year (P < 0.05). Two days postpartum, plasma GH concentrations had increased and were significantly higher than in the same animals during pregnancy (Fig. 1; P < 0.05).
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FIG. 1. Basal plasma GH concentrations (ng/ml; mean ± SEM) in ovary-intact, nonpregnant (hatched bars, n = 7), pregnant (black bars, n = 6), 2-day-postpartum (June, hatched bars, n = 6), and ovariectomized mares (open bars, n = 8) at different times of the year. Values with different superscript letters were significantly different (P < 0.05)
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GH Release in Response to Naloxone
Treatment with the opioid antagonist naloxone induced a significant (P < 0.05 vs. controls) GH release at all times of the year in ovary-intact mares (Fig. 2). GH release in response to naloxone calculated as area under the curve was 141.8 ± 37.2 ng/ml per min in estrus, 132.9 ± 24.7 ng/ml per min in diestrus, and 33.9 ± 5.1 ng/ml per min in seasonally anovulatory mares. Respective values for control experiments were -21.0 ± 15.0, -46.5 ± 28.5, and -3.0 ± 6.0 ng/ml per min. GH release in response to naloxone was significantly (P < 0.05) more pronounced in cyclic mares than in ovary-intact, seasonally anovulatory mares. Naloxone did not significantly affect GH release in ovariectomized mares, either during or outside the breeding season (Fig. 3). In pregnant mares, naloxone induced a significant release of GH only around Day 280 (P < 0.05) and not at other times of gestation (Fig. 4). Calculated as area under the curve around Day 280, GH release was 113.8 ± 64.1 ng/ml per min in response to naloxone and 8.8 ± 23.1 ng/ml per min in response to saline. At Day 170 of gestation, the difference between naloxone (area under the curve 91.1 ± 32.1 ng/ml per min) and saline experiments (area under the curve 10.4 ± 13.3 ng/ml per min) approached statistical significance (P = 0.1).
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FIG. 2. Plasma GH concentration (ng/ml; mean ± SEM) before and after injections (arrows) of naloxone (solid circles) and saline (open circles) in ovary-intact mares (a) during the anovulatory season and during the breeding season in estrus (b) and diestrus (c) (n = 7). a–c) GH release in response to naloxone was significantly different from that in respective saline treatments (P < 0.05)
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FIG. 3. Plasma GH concentration (ng/ml; mean ± SEM) before and after injections (arrows) of naloxone (solid circles) and saline (open circles) in ovariectomized mares (n = 8) in a) May (breeding season) and b) November (nonbreeding season). GH release was not significantly different between naloxone and respective saline treatments
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FIG. 4. Plasma GH concentration (ng/ml; mean ± SEM) before and after injections (arrows) of naloxone (solid circles) and saline (open circles) in pregnant mares (n = 6) on Days a) 26.4 ± 0.6, b) 75.4 ± 5.4, c) 171.8 ± 2.4, d) 226.2 ± 4.8, e) 282.7 ± 3.4, and f) 319.8 ± 2.1 of gestation. e) GH release in response to naloxone was significantly different from that in respective saline treatments (P < 0.05); c, P = 0.01
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DISCUSSION
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The results of this study indicate that GH release in mares is affected by season, ovarian factors, and pregnancy. In ovary-intact, nonpregnant mares, GH concentrations were higher during the breeding than during the nonbreeding season. These changes occurred neither in ovariectomized mares, in which GH concentrations remained low during the breeding season, nor in pregnant mares, in which GH concentration were high during winter. Circannual changes in GH release in ovary-intact, nonpregnant mares are therefore not simply a function of season. Estradiol has been shown to stimulate GH release in heifers [10], and progesterone treatment increased GH release in ovariectomized bitches [9]. The increase in plasma GH concentrations in May and June is therefore most likely stimulated by ovarian steroids and linked to the enhanced ovarian activity during the breeding season. In agreement with our results in ovariectomized mares, a marked reduction in GH concentrations was found following castration in rats [6], bulls [7], and bitches [9]. The high GH concentrations in pregnant mares could be stimulated by progestagens of ovarian and/or placental origin. However, the possibility cannot be excluded that at least during part of pregnancy, not only GH released from the pituitary but also GH-related peptides of placental origin were measured. Expression of a GH-related protein that might be a placental lactogen has been found in endometrial cup tissue [21]. Although in the present study, plasma GH concentrations were elevated throughout pregnancy and not only during the period of endometrial cup activity, a certain contribution of GH-related placental peptides to GH immunoreactivity cannot be totally ruled out. The high plasma GH concentrations 2 days after foaling could be stimulated in conjunction with the onset of lactation. Elevated plasma GH concentrations have also been found in lactating ewes [22, 23], gilts [24], and rats [25]. Furthermore, in ewes, early lactogenesis is in part controlled by GH [22]. GH also is involved in nutrient partitioning in the lactating ewe [26]. Such effects can be assumed in the postpartum mare. In our study, samples were taken for 1 h before and 2 h after injections of either naloxone or saline. Therefore our data allow analysis only of mean plasma GH concentrations and not of GH pulse frequency and amplitude.
Treatment with exogenous GH has been shown to enhance the ovarian response to gonadotropins in women and in sows [1–3]. Increased plasma GH concentrations in cyclic and in pregnant mares, via comparable mechanisms, could be involved in the stimulation of reproductive functions during the breeding season. Seasonal changes in GH release might be more pronounced in the Shetland pony, which shows a more pronounced circannual rhythm of reproductive activity than highly domesticated breeds of equines [27]. Because seasonal effects were to be investigated, a breed with strong reproductive seasonality was chosen for this study. Seasonal changes in GH release are overcome by pregnancy-associated factors, and thus plasma GH concentrations remain high throughout pregnancy. Seasonal changes in GH release have not been investigated before in horses or in other species. However, in boars, but not in sows, a diurnal rhythm in GH release exists with distinct GH pulses only during daytime [28].
The opioid antagonist naloxone stimulated GH release in ovary-intact mares and in pregnant mares around Day 280 of gestation, indicating an opioidergic inhibition of GH secretion. This is, at least in part, different from results obtained in rats, cattle, and pigs [11–15]. In these species, naloxone treatment decreased plasma GH concentrations, indicative of direct or indirect stimulatory opioidergic effects on GH release. In agreement with our study, evidence of an opioidergic inhibition of GH release comes from an experiment in Holstein calves. In that study, naloxone treatment significantly increased plasma GH concentrations in October and November but not in April. The opioid antagonist methyl levallorphan enhanced GH release also in April [17]. An involvement of more than one opioid receptor type in the regulation of GH secretion could explain the different effects of the two antagonists.
An opioidergic effect on GH release was found only in ovary-intact, not in ovariectomized mares. In the ovary-intact, nonpregnant mares, the naloxone-induced GH release was stronger in May and June than in November and December. Therefore not only the increase in basal GH release during summer, but also the opioidergic regulation of GH secretion, requires the presence of the ovaries. This could reflect a more pronounced inhibitory opioidergic tone during the breeding season. An increase in GH synthesis leading to a bigger pool of releasable GH is also feasible. Seasonal changes in opioidergic regulation have been found also for LH and prolactin in both mares and stallions [19,29–31]. In pregnant mares, a naloxone-induced GH release was absent during most of pregnancy but not around Day 280 of gestation. An opioidergic inhibition of GH release that exists in cyclic mares during both estrus and diestrus is inactivated as early as during the first month of pregnancy. The opioidergic inhibition of GH release found in cyclic mares is therefore overcome or masked by pregnancy-associated factors.
In conclusion, it could be shown that GH release is strongly influenced by reproductive state in the horse. In cyclic mares during the breeding season and in pregnant mares, endogenous GH release is enhanced. At least in part, GH release is inhibited by opioidergic systems in the horse.
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ACKNOWLEDGMENTS
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The authors are grateful to R. Wittig, M. Müller, and K. von Kittlitz for technical assistance.
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FOOTNOTES
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1 Supported by the Deutsche Forschungsgemeinschaft (AU 118/1–3). 
2 Correspondence: Christine Aurich, Institut für Tierzucht und Genetik, Veterinärmedizinische Universität Wien, Veterinärplatz 1, A-1210 Vienna, Austria. FAX: 43 1 25077 5490; joerg.aurich{at}vu-wien.ac.at
Accepted: July 28, 1999.
Received: February 22, 1999.
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ABSTRACT
INTRODUCTION
