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01-04-2015 | Review Article

Regulation of gonadotropin secretion by monitoring energy availability

Published in: Reproductive Medicine and Biology | Issue 2/2015

Abstract

Nutrition is a principal environmental factor influencing fertility in animals. Energy deficit causes amenorrhea, delayed puberty, and suppression of copulatory behaviors by inhibiting gonadal activity. When gonadal activity is impaired by malnutrition, the signals originating from an undernourished state are ultimately conveyed to the gonadotropin-releasing hormone (GnRH) pulse generator, leading to suppressed secretion of GnRH and luteinizing hormone (LH). The mechanism responsible for energetic control of gonadotropin release is believed to involve metabolic signals, sensing mechanisms, and neuroendocrine pathways. The availabilities of blood-borne energy substrates such as glucose, fatty acids, and ketone bodies, which fluctuate in parallel with changes in nutritional status, act as metabolic signals that regulate the GnRH pulse generator activity and GnRH/LH release. As components of the specific sensing system, the ependymocytes lining the cerebroventricular wall in the lower brainstem integrate the information derived from metabolic signals to control gonadotropin release. One of the pathways responsible for the energetic control of gonadal activity consists of noradrenergic neurons from the solitary tract nucleus in the lower brainstem, projecting to the paraventricular nucleus of the hypothalamus. Further studies are needed to elucidate the mechanisms underlying energetic control of reproductive function.

Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev. 1992;16:235–72.PubMedCrossRef

Santoro N, Filicori M, Crowley WF Jr. Hypogonadotropic disorders in men and women: diagnosis and therapy with pulsatile gonadotropin-releasing hormone. Endocr Rev. 1986;7:11–23.PubMedCrossRef

Reame NE, Sauder SE, Case GD, Kelch RP, Marshall JC. Pulsatile gonadotropin secretion in women with hypothalamic amenorrhea: evidence that reduced frequency of gonadotropin-releasing hormone secretion is the mechanism of persistent anovulation. J Clin Endocrinol Metab. 1985;61:851–8.PubMedCrossRef

Loucks AB, Verdun M, Heath EM. Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol. 1998;84:37–46.PubMed

Frisch RE, McArthur JW. Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science. 1974;185:949–51.PubMedCrossRef

Lujan ME, Krzemien AA, Reid RL, Van Vugt DA. Developing a model of nutritional amenorrhea in rhesus monkeys. Endocrinology. 2006;147:483–92.PubMedCrossRef

Sisk CL, Bronson FH. Effects of food restriction and restoration on gonadotropin and growth hormone secretion in immature male rats. Biol Reprod. 1986;35:554–61.PubMedCrossRef

Kennedy GC, Mitra J. Body weight and food intake as initiating factors for puberty in the rat. J Physiol. 1963;166:408–18.PubMedCentralPubMedCrossRef

Fitzgerald J, Michel F, Butler WR. Growth and sexual maturation in ewes: dietary and seasonal effects modulating luteinizing hormone secretion and first ovulation. Biol Reprod. 1982;27:864–70.PubMedCrossRef

10.

Foster DL, Olster DH. Effect of restricted nutrition on puberty in the lamb: patterns of tonic luteinizing hormone (LH) secretion and competency of the LH surge system. Endocrinology. 1985;116:375–81.PubMedCrossRef

11.

Nebel RL, McGilliard ML. Interactions of high milk yield and reproductive performance in dairy cows. J Dairy Sci. 1993;76:3257–68.PubMedCrossRef

12.

Rossetti L, Giaccari A, DeFronzo RA. Glucose toxicity. Diabetes Care. 1990;13:610–30.PubMedCrossRef

13.

Griffin ML, South SA, Yankov VI, Booth RA Jr, Asplin CM, Veldhuis JD, Evans WS. Insulin-dependent diabetes mellitus and menstrual dysfunction. Ann Med. 1994;26:331–40.PubMedCrossRef

14.

Hotchkiss J, Knobil E. The menstrual cycle and its neuroendocrine control. In: Knobil E, Neill JD, editors. The physiology of reproduction, second edition. New York: Raven Press; 1994. p. 659–709.

15.

Carmel PW, Araki S, Ferin M. Pituitary stalk portal blood collection in rhesus monkeys: evidence for pulsatile release of gonadotropin-releasing hormone (GnRH). Endocrinology. 1976;99:243–8.PubMedCrossRef

16.

Belchetz PE, Plant TM, Nakai Y, Keogh EJ, Knobil E. Hypophysial responses to continuous and intermittent delivery of hypopthalamic gonadotropin-releasing hormone. Science. 1978;202:631–3.PubMedCrossRef

17.

Dierschke DJ, Bhattacharya AN, Atkinson LE, Knobil E. Circhoral oscillations of plasma LH levels in the ovariectomized rhesus monkey. Endocrinology. 1970;87:850–3.PubMedCrossRef

18.

Butler WR, Malven PV, Willett LB, Bolt DJ. Patterns of pituitary release and cranial output of LH and prolactin in ovariectomized ewes. Endocrinology. 1972;91:793–801.PubMedCrossRef

19.

Gay VL, Sheth NA. Evidence for a periodic release of LH in castrated male and female rats. Endocrinology. 1972;90:158–62.PubMedCrossRef

20.

Forrest DW, Fleeger JL, Long CR, Sorensen AM Jr, Harms PG. Effect of exogenous prolactin on peripheral luteinizing hormone levels in ovariectomized cows. Biol Reprod. 1980;22:197–201.PubMedCrossRef

21.

Levine JE, Norman RL, Gliessman PM, Oyama TT, Bangsberg DR, Spies HG. In vivo gonadotropin-releasing hormone release and serum luteinizing hormone measurements in ovariectomized, estrogen-treated rhesus macaques. Endocrinology. 1985;117:711–21.PubMedCrossRef

22.

Van Vugt DA, Diefenbach WD, Alston E, Ferin M. Gonadotropin-releasing hormone pulses in third ventricular cerebrospinal fluid of ovariectomized rhesus monkeys: correlation with luteinizing hormone pulses. Endocrinology. 1985;117:1550–8.PubMedCrossRef

23.

Xia L, Van Vugt D, Alston EJ, Luckhaus J, Ferin M. A surge of gonadotropin-releasing hormone accompanies the estradiol-induced gonadotropin surge in the rhesus monkey. Endocrinology. 1992;131:2812–20.PubMed

24.

Clarke IJ, Cummins JT. The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinizing hormone (LH) secretion in ovariectomized ewes. Endocrinology. 1982;111:1737–9.PubMedCrossRef

25.

Levine JE, Pau KY, Ramirez VD, Jackson GL. Simultaneous measurement of luteinizing hormone-releasing hormone and luteinizing hormone release in unanesthetized, ovariectomized sheep. Endocrinology. 1982;111:1449–55.PubMedCrossRef

26.

Moenter SM, Brand RM, Midgley AR, Karsch FJ. Dynamics of gonadotropin-releasing hormone release during a pulse. Endocrinology. 1992;130:503–10.PubMed

27.

Levine JE, Duffy MT. Simultaneous measurement of luteinizing hormone (LH)-releasing hormone, LH, and follicle-stimulating hormone release in intact and short-term castrate rats. Endocrinology. 1988;122:2211–21.PubMedCrossRef

28.

Urbanski HF, Pickle RL, Ramirez VD. Simultaneous measurement of gonadotropin-releasing hormone, luteinizing hormone, and follicle-stimulating hormone in the orchidectomized rat. Endocrinology. 1988;123:413–9.PubMedCrossRef

29.

Lincoln DW, Fraser HM, Lincoln GA, Martin GB, McNeilly AS. Hypothalamic pulse generators. Recent Prog Horm Res. 1985;41:369–419.PubMed

30.

Okamura H, Tsukamura H, Ohkura S, Uenoyama Y, Wakabayashi Y, Maeda K. Kisspeptin and GnRH pulse generation. Adv Exp Med Biol. 2013;784:297–323.PubMedCrossRef

31.

Maeda K, Ohkura S, Uenoyama Y, Wakabayashi Y, Oka Y, Tsukamura H, Okamura H. Neurobiological mechanisms underlying GnRH pulse generation by the hypothalamus. Brain Res. 2010;1364:103–15.PubMedCrossRef

32.

Day ML, Imakawa K, Zalesky DD, Kittok RJ, Kinder JE. Effects of restriction of dietary energy intake during the prepubertal period on secretion of luteinizing hormone and responsiveness of the pituitary to luteinizing hormone-releasing hormone in heifers. J Anim Sci. 1986;62:1641–8.PubMed

33.

Randel RD. Nutrition and postpartum rebreeding in cattle. J Anim Sci. 1990;68:853–62.PubMed

34.

Richards MW, Wettemann RP, Schoenemann HM. Nutritional anestrus in beef cows: body weight change, body condition, luteinizing hormone in serum and ovarian activity. J Anim Sci. 1989;67:1520–6.PubMed

35.

Ichimaru T, Mori Y, Okamura H. A possible role of neuropeptide Y as a mediator of undernutrition to the hypothalamic gonadotropin-releasing hormone pulse generator in goats. Endocrinology. 2001;142:2489–98.PubMed

36.

Matsuyama S, Ohkura S, Ichimaru T, Sakurai K, Tsukamura H, Maeda K, Okamura H. Simultaneous observation of the GnRH pulse generator activity and plasma concentrations of metabolites and insulin during fasting and subsequent refeeding periods in Shiba goats. J Reprod Dev. 2004;50:697–704.PubMedCrossRef

37.

Nagatani S, Guthikonda P, Thompson RC, Tsukamura H, Maeda KI, Foster DL. Evidence for GnRH regulation by leptin: leptin administration prevents reduced pulsatile LH secretion during fasting. Neuroendocrinology. 1998;67:370–6.PubMedCrossRef

38.

Cagampang FRA, Maeda KI, Tsukamura H, Ohkura S, Ota K. Involvement of ovarian steroids and endogenous opioids in the fasting-induced suppression of pulsatile LH release in ovariectomized rats. J Endocrinol. 1991;129:321–8.PubMedCrossRef

39.

Thomas GB, Mercer JE, Karalis T, Rao A, Cummins JT, Clarke IJ. Effect of restricted feeding on the concentrations of growth hormone (GH), gonadotropins, and prolactin (PRL) in plasma, and on the amounts of messenger ribonucleic acid for GH, gonadotropin subunits, and PRL in the pituitary glands of adult ovariectomized ewes. Endocrinology. 1990;126:1361–7.PubMedCrossRef

40.

McShane TM, Petersen SL, McCrone S, Keisler DH. Influence of food restriction on neuropeptide-Y, proopiomelanocortin, and luteinizing hormone-releasing hormone gene expression in sheep hypothalami. Biol Reprod. 1993;49:831–9.PubMedCrossRef

41.

I’Anson H, Manning JM, Herbosa CG, Pelt J, Friedman CR, Wood RI, Bucholtz DC, Foster DL. Central inhibition of gonadotropin-releasing hormone secretion in the growth-restricted hypogonadotropic female sheep. Endocrinology. 2000;141:520–7.PubMedCrossRef

42.

Schillo KK. Effects of dietary energy on control of luteinizing hormone secretion in cattle and sheep. J Anim Sci. 1992;70:1271–82.PubMed

43.

Wade GN, Schneider JE, Li HY. Control of fertility by metabolic cues. Am J Physiol. 1996;270:E1–19.PubMed

44.

Blache D, Chagas LM, Blackberry MA, Vercoe PE, Martin GB. Metabolic factors affecting the reproductive axis in male sheep. J Reprod Fertil. 2000;120:1–11.PubMedCrossRef

45.

Schneider JE. Energy balance and reproduction. Physiol Behav. 2004;81:289–317.PubMedCrossRef

46.

Wade GN, Jones JE. Neuroendocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol. 2004;287:R1277–96.PubMedCrossRef

47.

Schneider JE, Wade GN. Availability of metabolic fuels controls estrous cyclicity of Syrian hamsters. Science. 1989;244:1326–8.PubMedCrossRef

48.

Murahashi K, Bucholtz DC, Nagatani S, Tsukahara S, Tsukamura H, Foster DL, Maeda KI. Suppression of luteinizing hormone pulses by restriction of glucose availability is mediated by sensors in the brain stem. Endocrinology. 1996;137:1171–6.PubMed

49.

Nagatani S, Bucholtz DC, Murahashi K, Estacio MAC, Tsukamura H, Foster DL, Maeda KI. Reduction of glucose availability suppresses pulsatile luteinizing hormone release in female and male rats. Endocrinology. 1996;137:1166–70.PubMed

50.

Goubillon ML, Thalabard JC. Insulin-induced hypoglycemia decreases luteinizing hormone secretion in the castrated male rat: involvement of opiate peptides. Neuroendocrinology. 1996;64:49–56.PubMedCrossRef

51.

Cagampang FRA, Cates PS, Sandhu S, Strutton PH, McGarvey C, Coen CW, O’Byrne KT. Hypoglycaemia-induced inhibition of pulsatile luteinizing hormone secretion in female rats: role of oestradiol, endogenous opioids and the adrenal medulla. J Neuroendocrinol. 1997;9:867–72.PubMedCrossRef

52.

Chen MD, O’Byrne KT, Chiappini SE, Hotchkiss J, Knobil E. Hypoglycemic ‘stress’ and gonadotropin-releasing hormone pulse generator activity in the rhesus monkey: role of the ovary. Neuroendocrinology. 1992;56:666–73.PubMedCrossRef

53.

Heisler LE, Pallotta CM, Reid RL, Van Vugt DA. Hypoglycemia-induced inhibition of luteinizing hormone secretion in the rhesus monkey is not mediated by endogenous opioid peptides. J Clin Endocrinol Metab. 1993;76:1280–5.PubMed

54.

Clarke IJ, Horton RJ, Doughton BW. Investigation of the mechanism by which insulin-induced hypoglycemia decreases luteinizing hormone secretion in ovariectomized ewes. Endocrinology. 1990;127:1470–6.PubMedCrossRef

55.

Medina CL, Nagatani S, Darling TA, Bucholtz DC, Tsukamura H, Maeda K, Foster DL. Glucose availability modulates the timing of the luteinizing hormone surge in the ewe. J Neuroendocrinol. 1998;10:785–92.PubMedCrossRef

56.

Ohkura S, Tanaka T, Nagatani S, Bucholtz DC, Tsukamura H, Maeda K, Foster DL. Central, but not peripheral, glucose-sensing mechanisms mediate glucoprivic suppression of pulsatile luteinizing hormone secretion in the sheep. Endocrinology. 2000;141:4472–80.PubMed

57.

Ohkura S, Ichimaru T, Itoh F, Matsuyama S, Okamura H. Further evidence for the role of glucose as a metabolic regulator of hypothalamic gonadotropin-releasing hormone pulse generator activity in goats. Endocrinology. 2004;145:3239–46.PubMedCrossRef

58.

Shahab M, Sajapitak S, Tsukamura H, Kinoshita M, Matsuyama S, Ohkura S, Yamada S, Uenoyama Y, I’Anson H, Maeda K. Acute lipoprivation suppresses pulsatile luteinizing hormone secretion without affecting food intake in female rats. J Reprod Dev. 2006;52:763–72.PubMedCrossRef

59.

Boukhliq R, Martin GB. Administration of fatty acids and gonadotrophin secretion in the mature ram. Anim Reprod Sci. 1997;49:143–59.PubMedCrossRef

60.

Heitmann RN, Dawes DJ, Sensenig SC. Hepatic ketogenesis and peripheral ketone body utilization in the ruminant. J Nutr. 1987;117:1174–80.PubMed

61.

Bergman EN, Roe WE, Kon K. Quantitative aspects of propionate metabolism and gluconeogenesis in sheep. Am J Physiol. 1966;211:793–9.PubMed

62.

Owen OE, Reichard GA Jr, Boden G, Shuman C. Comparative measurements of glucose, beta-hydroxybutyrate, acetoacetate, and insulin in blood and cerebrospinal fluid during starvation. Metabolism. 1974;23:7–14.PubMedCrossRef

63.

Pan JW, Rothman TL, Behar KL, Stein DT, Hetherington HP. Human brain beta-hydroxybutyrate and lactate increase in fasting-induced ketosis. J Cereb Blood Flow Metab. 2000;20:1502–7.PubMedCrossRef

64.

Gjedde A, Crone C. Induction processes in blood-brain transfer of ketone bodies during starvation. Am J Physiol. 1975;229:1165–9.PubMed

65.

Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill GF Jr. Brain metabolism during fasting. J Clin Invest. 1967;46:1589–95.PubMedCentralPubMedCrossRef

66.

Hawkins RA, Mans AM, Davis DW. Regional ketone body utilization by rat brain in starvation and diabetes. Am J Physiol. 1986;250:E169–78.PubMed

67.

Lundman B, Asplund K, Norberg A. Metabolic control, food intake and mood during the menstrual cycle in patients with insulin-dependent diabetes. Int J Nurs Stud. 1994;31:391–401.PubMedCrossRef

68.

Roche JF. The effect of nutritional management of the dairy cow on reproductive efficiency. Anim Reprod Sci. 2006;96:282–96.PubMedCrossRef

69.

Iwata K, Kinoshita M, Susaki N, Uenoyama Y, Tsukamura H, Maeda K. Central injection of ketone body suppresses luteinizing hormone release via the catecholaminergic pathway in female rats. J Reprod Dev. 2011;57:379–84.PubMedCrossRef

70.

Anand BK, Brobeck JR. Hypothalamic control of food intake in rats and cats. Yale J Biol Med. 1951;24:123–40.PubMedCentralPubMed

71.

Oomura Y, Ono T, Ooyama H, Wayner MJ. Glucose and osmosensitive neurones of the rat hypothalamus. Nature. 1969;222:282–4.PubMedCrossRef

72.

Oomura Y, Ooyama H, Sugimori M, Nakamura T, Yamada Y. Glucose inhibition of the glucose-sensitive neurone in the rat lateral hypothalamus. Nature. 1974;247:284–6.PubMedCrossRef

73.

Anand BK, Chhina GS, Sharma KN, Dua S, Singh B. Activity of single neurons in the hypothalamic feeding centers: effect of glucose. Am J Physiol. 1964;207:1146–54.PubMed

74.

Ritter RC, Slusser PG, Stone S. Glucoreceptors controlling feeding and blood glucose: location in the hindbrain. Science. 1981;213:451–2.PubMedCrossRef

75.

Ritter S, Dinh TT, Zhang Y. Localization of hindbrain glucoreceptive sites controlling food intake and blood glucose. Brain Res. 2000;856:37–47.PubMedCrossRef

76.

Matschinsky FM. Glucokinase as glucose sensor and metabolic signal generator in pancreatic beta-cells and hepatocytes. Diabetes. 1990;39:647–52.PubMedCrossRef

77.

Johnson JH, Newgard CB, Milburn JL, Lodish HF, Thorens B. The high Km glucose transporter of islets of Langerhans is functionally similar to the low affinity transporter of liver and has an identical primary sequence. J Biol Chem. 1990;265:6548–51.PubMed

78.

Giroix M-H, Sener A, Pipeleers DG, Malaisse WJ. Hexose metabolism in pancreatic islets. Inhibition of hexokinase. Biochem J. 1984;223:447–53.PubMedCentralPubMed

79.

Jetton TL, Liang Y, Pettepher CC, Zimmerman EC, Cox FG, Horvath K, Matschinsky FM, Magnuson MA. Analysis of upstream glucokinase promoter activity in transgenic mice and identification of glucokinase in rare neuroendocrine cells in the brain and gut. J Biol Chem. 1994;269:3641–54.PubMed

80.

Navarro M, Rodriquez de Fonseca F, Alvarez E, Chowen JA, Zueco JA, Gomez R, Eng J, Blazquez E. Colocalization of glucagon-like peptide-1 (GLP-1) receptors, glucose transporter GLUT-2, and glucokinase mRNAs in rat hypothalamic cells: evidence for a role of GLP-1 receptor agonists as an inhibitory signal for food and water intake. J Neurochem. 1996;67:1982–91.PubMedCrossRef

81.

Yang XJ, Kow LM, Funabashi T, Mobbs CV. Hypothalamic glucose sensor: similarities to and differences from pancreatic beta-cell mechanisms. Diabetes. 1999;48:1763–72.PubMedCrossRef

82.

Lynch RM, Tompkins LS, Brooks HL, Dunn-Meynell AA, Levin BE. Localization of glucokinase gene expression in the rat brain. Diabetes. 2000;49:693–700.PubMedCrossRef

83.

Maekawa F, Toyoda Y, Torii N, Miwa I, Thompson RC, Foster DL, Tsukahara S, Tsukamura H, Maeda K-I. Localization of glucokinase-like immunoreactivity in the rat lower brain stem: for possible location of brain glucose-sensing mechanisms. Endocrinology. 2000;141:375–84.PubMed

84.

Roncero I, Alvarez E, Vazquez P, Blazquez E. Functional glucokinase isoforms are expressed in rat brain. J Neurochem. 2000;74:1848–57.PubMedCrossRef

85.

Dunn-Meynell AA, Routh VH, Kang L, Gaspers L, Levin BE. Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes. 2002;51:2056–65.PubMedCrossRef

86.

Moriyama R, Tsukamura H, Kinoshita M, Okazaki H, Kato Y, Maeda KI. In vitro increase in intracellular calcium concentrations induced by low or high extracellular glucose levels in ependymocytes and serotonergic neurons of the rat lower brainstem. Endocrinology. 2004;145:2507–15.PubMedCrossRef

87.

Kinoshita M, I’Anson H, Tsukamura H, Maeda K-I. Fourth ventricular alloxan injection suppresses pulsatile luteinizing hormone release in female rats. J Reprod Dev. 2004;50:279–85.PubMedCrossRef

88.

Sajapitak S, Iwata K, Shahab M, Uenoyama Y, Yamada S, Kinoshita M, Bari FY, I’Anson H, Tsukamura H, Maeda K. Central lipoprivation-induced suppression of luteinizing hormone pulses is mediated by paraventricular catecholaminergic inputs in female rats. Endocrinology. 2008;149:3016–24.PubMedCrossRef

89.

Ritter S, Taylor JS. Vagal sensory neurons are required for lipoprivic but not glucoprivic feeding in rats. Am J Physiol. 1990;258:R1395–401.PubMed

90.

Ritter S, Dinh TT. 2-Mercaptoacetate and 2-deoxy-d-glucose induce Fos-like immunoreactivity in rat brain. Brain Res. 1994;641:111–20.PubMedCrossRef

91.

Schneider JE, Hall AJ, Wade GN. Central vs. peripheral metabolic control of estrous cycles in Syrian hamsters. I. Lipoprivation. Am J Physiol. 1997;272:R400–5.PubMed

92.

Cremer JE, Cunningham VJ, Pardridge WM, Braun LD, Oldendorf WH. Kinetics of blood-brain barrier transport of pyruvate, lactate and glucose in suckling, weanling and adult rats. J Neurochem. 1979;33:439–45.PubMedCrossRef

93.

Cremer JE, Teal HM, Cunningham VJ. Inhibition, by 2-oxo acids that accumulate in maple-syrup-urine disease, of lactate, pyruvate, and 3-hydroxybutyrate transport across the blood-brain barrier. J Neurochem. 1982;39:674–7.PubMedCrossRef

94.

Iwata K, Kinoshita M, Yamada S, Imamura T, Uenoyama Y, Tsukamura H, Maeda K. Involvement of brain ketone bodies and the noradrenergic pathway in diabetic hyperphagia in rats. J Physiol Sci. 2011;61:103–13.PubMedCrossRef

95.

Cunningham ET Jr, Sawchenko PE. Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus. J Comp Neurol. 1988;274:60–76.PubMedCrossRef

96.

Plotsky PM. Facilitation of immunoreactive corticotropin-releasing factor secretion into the hypophysial-portal circulation after activation of catecholaminergic pathways or central norepinephrine injection. Endocrinology. 1987;121:924–30.PubMedCrossRef

97.

Nagatani S, Tsukamura H, Murahashi K, Bucholtz DC, Foster DL, Maeda K. Paraventricular norepinephrine release mediates glucoprivic suppression of pulsatile luteinizing hormone secretion. Endocrinology. 1996;137:3183–6.PubMed

98.

Tsukamura H, Nagatani S, Cagampang FRA, Kawakami S, Maeda K. Corticotropin-releasing hormone mediates suppression of pulsatile luteinizing hormone secretion induced by activation of alpha-adrenergic receptors in the paraventricular nucleus in female rats. Endocrinology. 1994;134:1460–6.PubMed

99.

Tsukahara S, Tsukamura H, Foster DL, Maeda K-I. Effect of corticotropin-releasing hormone antagonist on oestrogen-dependent glucoprivic suppression of luteinizing hormone secretion in female rats. J Neuroendocrinol. 1999;11:101–5.PubMedCrossRef

100.

Sajapitak S, Uenoyama Y, Yamada S, Kinoshita M, Iwata K, Bari FY, I’Anson H, Tsukamula H, Maeda K. Paraventricular alpha1- and alpha2-adrenergic receptors mediate hindbrain lipoprivation-induced suppression of luteinizing hormone pulses in female rats. J Reprod Dev. 2008;54:198–202.PubMedCrossRef

101.

Reyes BA, Estacio MA, I’Anson H, Tsukamura H, Maeda KI. Glucoprivation increases estrogen receptor alpha immunoreactivity in the brain catecholaminergic neurons in ovariectomized rats. Neurosci Lett. 2001;299:109–12.PubMedCrossRef

102.

Estacio MA, Tsukamura H, Reyes BA, Uenoyama Y, I’Anson H, Maeda K. Involvement of brainstem catecholaminergic inputs to the hypothalamic paraventricular nucleus in estrogen receptor alpha expression in this nucleus during different stress conditions in female rats. Endocrinology. 2004;145:4917–26.PubMedCrossRef

Title: Regulation of gonadotropin secretion by monitoring energy availability
Publication date: 01-04-2015
Published in: Reproductive Medicine and Biology / Issue 2/2015
Print ISSN: 1445-5781
Electronic ISSN: 1447-0578
DOI: https://doi.org/10.1007/s12522-014-0194-0

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Regulation of gonadotropin secretion by monitoring energy availability

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

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