Dynamics of the responses in secretion of luteinising hormone, leptin and insulin following an acute increase in nutrition in mature male sheep
Song Zhang A , Dominique Blache A B , Margaret A. Blackberry A and Graeme B. Martin AA School of Animal Biology, Faculty of Natural and Agricultural Sciences, University of Western Australia, Crawley, WA 6009, Australia.
B Corresponding author. Email: dblache@agric.uwa.edu.au
Reproduction, Fertility and Development 16(8) 823-829 https://doi.org/10.1071/RD04086
Submitted: 2 August 2004 Accepted: 27 October 2004 Published: 13 January 2005
Abstract
In Merino rams, an increase in the plane of nutrition increases the frequency of luteinising hormone (LH) pulses within a few days and this response is correlated with changes in the circulating concentrations of metabolic hormones. To analyse early dynamic aspects of these responses, we studied mature rams fed with diets that contained either low or high amounts of energy and protein. Jugular blood was sampled every 20 min for 96 h, including a control period of 24 h before the change of diet in the high-diet group. In the high-diet group, a significant increase in LH pulse frequency was first detected 6 h after the increase in nutrition on Day 1 and the frequency remained significantly elevated throughout the 72-h treatment period, except for a 12-h period on Day 2. Following the change of diet, insulin concentrations increased within 3 h and leptin concentrations increased within 7 h, after which time the concentrations of both hormones remained high. Dietary treatment did not affect the concentrations of thyroxine or insulin-like growth factor-I, but the high diet increased the concentrations of tri-iodothyronine. These observations are consistent with insulin and leptin playing a role in the early activation of the gonadotrophin-releasing hormone–LH axis by nutritional inputs.
Extra keywords: insulin-like growth factor-I, post-prandial hormonal increase, ram, reproduction, thyroid hormones.
Acknowledgments
The authors thank everyone in the Animal Science Group who was willing to help with the animal experiments. S. Z. was supported by an International Postgraduate Research Scholarship from the University of Western Australia. This work was supported by a National Health and Medical Research Council of Australia grant (no. 139134).
Amstalden, M. , Garcia, M. R. , Stanko, R. L. , Nizielski, S. E. , Morrison, C. D. , Keisler, D. H. , and Williams, G. L. (2002). Central infusion of recombinant ovine leptin normalizes plasma insulin and stimulates a novel hypersecretion of luteinizing hormone after short-term fasting in mature beef cows. Biol. Reprod. 66, 1555–1561.
| PubMed |
Barb, C. R. , and Kraeling, R. R. (2004). Role of leptin in the regulation of gonadotropin secretion in farm animals. Anim. Reprod. Sci. 82–83, 155–167.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Berthoud, H. R. , Kressel, M. , and Neuhuber, W. L. (1992). An anterograde tracing study of the vagal innervation of rat liver, portal vein and biliary system. Anat. Embryol. (Berl.) 186, 431–442.
| PubMed |
Blache, D. , Chagas, L. M. , Caraty, A. , Blackberry, M. A. , and Martin, G. B. (1997a). GnRH secretion into CSF in rams treated with a GnRH antagonist. J. Neuroendocrinol. 9, 887–892.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Blache, D. , Tjondronegoro, S. , Blackberry, M. A. , Anderson, S. T. , Curlewis, J. D. , and Martin, G. B. (1997b). Gonadotrophin and prolactin secretion in castrated male sheep following subcutaneous or intracranial treatment with testicular hormones. Endocrine 7, 235–243.
| PubMed |
Blache, D. , Celi, P. , Blackberry, M. A. , Dynes, R. A. , and Martin, G. B. (2000a). Decrease in voluntary feed intake and pulsatile luteinizing hormone secretion after intracerebroventricular infusion of recombinant bovine leptin in mature male sheep. Reprod. Fertil. Dev. 12, 373–381.
| PubMed |
Blache, D. , Chagas, L. M. , Blackberry, M. A. , Vercoe, P. E. , and Martin, G. B. (2000b). Metabolic factors affecting the reproductive axis in male sheep. J. Reprod. Fertil. 120, 1–11.
| PubMed |
Blache, D. , Tellam, R. L. , Chagas, L. M. , Blackberry, M. A. , Vercoe, P. E. , and Martin, G. B. (2000c). Level of nutrition affects leptin concentrations in plasma and cerebrospinal fluid in sheep. J. Endocrinol. 165, 625–637.
| PubMed |
Blache, D. , Adam, C. L. , and Martin, G. B. (2002). The mature male sheep: a model to study the effects of nutrition on the reproductive axis. Reprod. Suppl. 59, 219–233.
| PubMed |
Blache, D. , Zhang, S. , and Martin, G. B. (2003). Fertility in male sheep: modulators of the acute effects of nutrition on the reproductive axis of male sheep. Reprod. Suppl. 61, 387–402.
| PubMed |
Block, S. S. , Rhoads, R. P. , Bauman, D. E. , Ehrhardt, R. A. , and McGuire, M. A. , et al. (2003). Demonstration of a role for insulin in the regulation of leptin in lactating dairy cows. J. Dairy Sci. 86, 3508–3515.
| PubMed |
Boukhliq, R. , Martin, G. B. , White, C. L. , Blackberry, M. A. , and Murray, P. J. (1997). Role of glucose, fatty acids and protein in regulation of testicular growth and secretion of gonadotrophin, prolactin, somatotrophin and insulin in the mature ram. Reprod. Fertil. Dev. 9, 515–524.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Breier, B. H. , Gallaher, B. W. , and Gluckman, P. D. (1991). Radioimmunoassay for insulin-like growth factor-I: solutions to some potential problems and pitfalls. J. Endocrinol. 128, 347–357.
| PubMed |
Burcelin, R. , Thorens, B. , Glauser, M. , Gaillard, R. C. , and Pralong, F. P. (2003). Gonadotropin-releasing hormone secretion from hypothalamic neurons: stimulation by insulin and potentiation by leptin. Endocrinology 144, 4484–4491.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cagampang, F. R. , Maeda, K. , and Ota, K. (1992). Involvement of the gastric vagal nerve in the suppression of pulsatile luteinizing hormone release during acute fasting in rats. Endocrinology 130, 3003–3006.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dallongeville, J. , Hecquet, B. , Lebel, P. , Edme, J. L. , Le Fur, C. , Fruchart, J. C. , Auwerx, J. , and Romon, M. (1998). Short term response of circulating leptin to feeding and fasting in man: influence of circadian cycle. Int. J. Obes. Relat. Metab. Disord. 22, 728–733.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Daniel, J. A. , Thomas, M. G. , Hale, C. S. , Simmons, J. M. , and Keisler, D. H. (2000). Effect of cerebroventricular infusion of insulin and (or) glucose on hypothalamic expression of leptin receptor and pituitary secretion of LH in diet-restricted ewes. Domest. Anim. Endocrinol. 18, 177–185.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dawson, A. , Deeming, D. C. , Dick, A. C. , and Sharp, P. J. (1996). Plasma thyroxine concentrations in farmed ostriches in relation to age, body weight, and growth hormone. Gen. Comp. Endocrinol. 103, 308–315.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dyer, C. J. , Simmons, J. M. , Matteri, R. L. , and Keisler, D. H. (1997). Leptin receptor mRNA is expressed in ewe anterior pituitary and adipose tissues and is differentially expressed in hypothalamic regions of well-fed and feed-restricted ewes. Domest. Anim. Endocrinol. 14, 119–128.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fernandez-Fernandez, R. , Tena-Sempere, M. , Aguilar, E. , and Pinilla, L. (2004). Ghrelin effects on gonadotropin secretion in male and female rats. Neurosci. Lett. 362, 103–107.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gibbs, J. , Young, R. C. , and Smith, G. P. (1973). Cholecystokinin decreases food intake in rats. J. Comp. Physiol. Psychol. 84, 488–495.
| PubMed |
Gluckman, P. D. , Johnson-Barrett, J. J. , Butler, J. H. , Edgar, B. W. , and Gunn, T. R. (1983). Studies of insulin-like growth factor-I and -II by specific radioligand assays in umbilical cord blood. Clin. Endocrinol. (Oxf.) 19, 405–413.
| PubMed |
Hardie, L. J. , Rayner, D. V. , Holmes, S. , and Trayhurn, P. (1996). Circulating leptin levels are modulated by fasting, cold exposure and insulin administration in lean but not Zucker (fa/fa) rats as measured by ELISA. Biochem. Biophys. Res. Commun. 223, 660–665.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Henry, B. A. , Goding, J. W. , Tilbrook, A. J. , Dunshea, F. R. , and Clarke, I. J. (2001). Intracerebroventricular infusion of leptin elevates the secretion of luteinising hormone without affecting food intake in long-term food-restricted sheep, but increases growth hormone irrespective of bodyweight. J. Endocrinol. 168, 67–77.
| PubMed |
Hötzel, M. J. , Walkden-Brown, S. W. , Blackberry, M. A. , and Martin, G. B. (1995). The effect of nutrition on testicular growth in mature Merino rams involves mechanisms that are independent of changes in GnRH pulse frequency. J. Endocrinol. 147, 75–85.
| PubMed |
Houseknecht, K. L. , and Portocarrero, C. P. (1998). Leptin and its receptors: regulators of whole-body energy homeostasis. Domest. Anim. Endocrinol. 15, 457–475.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kimura, F. , Hashimoto, R. , and Kawakami, M. (1983). The stimulatory effect of cholecystokinin implanted in the medial preoptic area on luteinizing hormone secretion in the ovariectomized estrogen-primed rat. Endocrinol. Jpn. 30, 305–309.
| PubMed |
Marie, M. , Findlay, P. A. , Thomas, L. , and Adam, C. L. (2001). Daily patterns of plasma leptin in sheep: effects of photoperiod and food intake. J. Endocrinol. 170, 277–286.
| PubMed |
Martin, G. B. , Oldham, C. M. , and Lindsay, D. R. (1980). Increased plasma LH levels in seasonally anovular Merino ewes following the introduction of rams. Anim. Reprod. Sci. 3, 125–132.
| Crossref | GoogleScholarGoogle Scholar |
Martin, G. B. , Tjondronegoro, S. , and Blackberry, M. A. (1994). Effects of nutrition on testicular size and the concentrations of gonadotrophins, testosterone and inhibin in plasma of mature male sheep. J. Reprod. Fertil. 101, 121–128.
| PubMed |
Merriam, G. R. , and Wachter, K. W. (1982). Algorithms for the study of episodic hormone secretion. Am. J. Physiol. 243, E310–E318.
| PubMed |
Miller, D. W. , Blache, D. , and Martin, G. B. (1995). The role of intracerebral insulin in the effect of nutrition on gonadotrophin secretion in mature male sheep. J. Endocrinol. 147, 321–329.
| PubMed |
Miller, D. W. , Blache, D. , Boukhliq, R. , Curlewis, J. D. , and Martin, G. B. (1998). Central metabolic messengers and the effects of nutrition on gonadotrophin secretion in sheep. J. Reprod. Fertil. 112, 347–356.
| PubMed |
Miller, D. W. , Findlay, P. A. , Morrison, M. A. , Raver, N. , and Adam, C. L. (2002). Seasonal and dose-dependent effects of intracerebroventricular leptin on LH secretion and appetite in sheep. J. Endocrinol. 175, 395–404.
| PubMed |
Monget, P. , and Martin, G. B. (1997). Involvement of insulin-like growth factors in the interactions between nutrition and reproduction in female mammals. Hum. Reprod. 1((Suppl.)), 33–52.
Morrison, C. D. , Daniel, J. A. , Holmberg, B. J. , Djiane, J. , Raver, N. , Gertler, A. , and Keisler, D. H. (2001). Central infusion of leptin into well-fed and undernourished ewe lambs: effects on feed intake and serum concentrations of growth hormone and luteinizing hormone. J. Endocrinol. 168, 317–324.
| PubMed |
Nakazato, M. , Murakami, N. , Date, Y. , Kojima, M. , Matsuo, H. , Kangawa, K. , and Matsukura, S. (2001). A role for ghrelin in the central regulation of feeding. Nature 409, 194–198.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Perera, A. D. , Verbalis, J. G. , Mikuma, N. , Majumdar, S. S. , and Plant, T. M. (1993). Cholecystokinin stimulates gonadotropin-releasing hormone release in the monkey (Macaca mulatta). Endocrinology 132, 1723–1728.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rae, M. T. , Rhind, S. M. , Kyle, C. E. , Miller, D. W. , and Brooks, A. (2002). Maternal undernutrition alters triiodothyronine concentrations and pituitary response to GnRH in fetal sheep. J. Endocrinol. 173, 449–455.
| PubMed |
Rushing, P. A. , Hagan, M. M. , Seeley, R. J. , Lutz, T. A. , and Woods, S. C. (2000). Amylin: a novel action in the brain to reduce body weight. Endocrinology 141, 850–853.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Saladin, R. , De Vos, P. , Guerre-Millo, M. , Leturque, A. , Girard, J. , Staels, B. , and Auwerx, J. (1995). Transient increase in obese gene expression after food intake or insulin administration. Nature 377, 527–529.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schneider, J. E. (2004). Energy balance and reproduction. Physiol. Behav. 81, 289–317.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schwartz, G. J. (2000). The role of gastrointestinal vagal afferents in the control of food intake: current prospects. Nutrition 16, 866–873.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shiba, Y. , Nitta, E. , Hirono, C. , Sugita, M. , and Iwasa, Y. (2002). Evaluation of mastication-induced change in sympatho-vagal balance through spectral analysis of heart rate variability. J. Oral Rehabil. 29, 956–960.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tanaka, T. , Nagatani, S. , Bucholtz, D. C. , Ohkura, S. , Tsukamura, H. , Maeda, K. , and Foster, D. L. (2000). Central action of insulin regulates pulsatile luteinizing hormone secretion in the diabetic sheep model. Biol. Reprod. 62, 1256–1261.
| PubMed |
Tanizawa, Y. , Okuya, S. , Ishihara, H. , Asano, T. , Yada, T. , and Oka, Y. (1997). Direct stimulation of basal insulin secretion by physiological concentrations of leptin in pancreatic beta cells. Endocrinology 138, 4513–4516.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tindal, J. S. , Knaggs, G. S. , Hart, I. C. , and Blake, L. A. (1978). Release of growth hormone in lactating and non-lactating goats in relation to behaviour, stages of sleep, electroencephalographs, environmental stimuli and levels of prolactin, insulin, glucose and free fatty acids in the circulation. J. Endocrinol. 76, 333–346.
| PubMed |
Zieba, D. A. , Amstalden, M. , Maciel, M. N. , Keisler, D. H. , Raver, N. , Gertler, A. , and Williams, G. L. (2003). Divergent effects of leptin on luteinizing hormone and insulin secretion are dose dependent. Exp. Biol. Med. (Maywood) 228, 325–330.
| PubMed |