Stress increases gonadotropin inhibitory hormone cell activity and input to gnrh cells in ewes

Endocrinology

Volumn 157, Issue 11, 2016, Pages 4339-4350

  Clarke, Iain J ^a   Bartolini, Danielle ^a   Conductier, Gregory ^a   Henry, Belinda A ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GONADORELIN; GONADOTROPIN; GONADOTROPIN INHIBITORY HORMONE; INSULIN; LIPOPOLYSACCHARIDE; TETRACOSACTIDE ZINC PHOSPHATE; UNCLASSIFIED DRUG; HYPOTHALAMUS HORMONE; LUTEINIZING HORMONE;

ACUTE STRESS; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CHRONIC STRESS; CONTROLLED STUDY; EXPERIMENTAL SHEEP; GENE EXPRESSION; GONADOTROPIN RELEASE; HORMONE BLOOD LEVEL; HYPOGLYCEMIA; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NERVE CELL; NONHUMAN; ONCOGENE C FOS; PORTAL VEIN BLOOD; PREDATOR STRESS; PRIORITY JOURNAL; PSEUDOSTRESS; QUANTITATIVE ANALYSIS; STRESS; ANIMAL; BLOOD; DRUG EFFECTS; FEMALE; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RADIOIMMUNOASSAY; SHEEP;

ANIMALS; FEMALE; GONADOTROPIN-RELEASING HORMONE; GONADOTROPINS; HYPOTHALAMIC HORMONES; HYPOTHALAMUS; IN SITU HYBRIDIZATION; LIPOPOLYSACCHARIDES; LUTEINIZING HORMONE; NEURONS; RADIOIMMUNOASSAY; SHEEP; STRESS, PHYSIOLOGICAL;

EID: 84994201239     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2016-1513     Document Type: Article

References (47)

1. Tilbrook AJ, Clarke IJ. Neuroendocrine mechanisms of innate states of attenuated responsiveness of the hypothalamo-pituitary adrenal axis to stress. Front Neuroendocrin . 2006;27:285-307.
2. Tilbrook AJ, Canny BJ, Serapiglia MD, Ambrose TJ, Clarke IJ. Suppression of the secretion of luteinizing hormone due to isolation/ restraint stress in gonadectomised rams and ewes is influenced by sex steroids. J Endocrinol . 1999;160:469-481.
3. Papargiris MM, Rivalland ET, Clarke IJ, Smith JT, Pereira A, Tilbrook AJ. Evidence that RF-Amide related peptide-3 is not a mediator of the inhibitory effects of psychosocial stress on gonadotrophin secretion in ovariectomised ewes. J Neuroendocrinol . 2011;23: 208-215.
4. Kirby ED, Geraghty AC, Ubuka T, Bentley GE, Kaufer D. Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc Natl Acad Sci USA. 2009; 106:11324-11329.
5. Clarke IJ, Sari IP, Qi Y, et al. Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology . 2008;149:5811-5821.
6. Smith JT, Coolen LM, Kriegsfeld LJ, et al. Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology. 2008;149:5770-5782.
7. Qi Y, Oldfield BJ, Clarke IJ. Projections of RFamide-related peptide-3 neurones in the ovine hypothalamus, with special reference to regions regulating energy balance and reproduction. J Neuroendocrinol. 2009;21:690-697.
8. Ubuka T, Lai H, Kitani M, et al. Gonadotropin-inhibitory hormone identificati on, cDNA cloning, and distribution in rhesus macaque brain. J Comp Neurol. 2009;517:841-855.
9. Smith JT, Young IR, Veldhuis JD, Clarke IJ. Gonadotropin-inhibitory hormone (GnIH) secretion into t he ovine hypophyseal portal system. Endocrinology. 2012;153:3368-3375.
10. Rizwan MZ, Porteous R, Herbison AE, Anderson GM. Cells expressing RFamide-related peptide-1/3, the mammalian gonadotropin-inhibitory hormone orthologs, are not hypophysiotropic neuroendocrine neurons in the rat. Endocrinology . 2009;150:1413-1420.
11. Kriegsfeld LJ, Mei DF, Bentley GE, et al. Identification and char acterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci USA. 2006;103:2410-2415.
12. Henry BA, Blache D, Dunshea FR, Clarke IJ. Altered " set-point" of the hypothalamus determines effects of cortisol on food intake, adiposity, and metabolic substrates in sheep. Domest Anim Endocrinol. 2010;38:46-56.
13. Ubuka T, Morgan K, Pawson AJ, et al. Identificatio n of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. PLoS One. 2009;4:e8400.
14. Lehman MN, Robinson JE, Karsch FJ, Silverman AJ. Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) pathways in the sheep brain during anestrus and the midluteal phase of the estrous cycle. J Comp Neurol . 1986;244:19-35.
15. Clarke IJ. Two decades of measuring GnRH secretion. Reprod Suppl . 2002;59:1-13.
16. Engler D, Pham T, Fullerton MJ, Ooi G, Funder JW, Clarke IJ. Studies of the secretion of corticotropin-rel easing factor and arginine vasopressin into the hypophysial-portal circulation of the conscious sheep. I. Effect of an audiovisual stimulus and insulin-induced hypoglycemia. Neuroendocrinology . 1989;49:367-381.
17. Saifullizam AK, Routly JE, Smith RF, Dobson H. Effect of insulin on the relationship of estrous behaviors to estradiol and LH surges in intact ewes. Physiol Behav. 2010;99:555-561.
18. Lee VW, Cumming IA, de Kretser DM, Findlay JK, Hudson B, Keogh EJ. Regulation of gonadotrophin secretion in rams from birth to sexual maturity. I. Plasma LH, FSHand testosterone levels. J Reprod Fertil. 1976;46:1-6.
19. Burger HG, Lee VW, Rennie GC. A generalized computer program for the treatment of data from competitive protein-binding assays including radioimmunoassays. J Lab Clin Med . 1972;80:302-312.
20. Clarke IJ, Cummins JT. Increased gonadotropin-releasing hormone pulse frequency associated with estrogen-induced luteinizing hormone surges in ovariectomized ewes. Endocrinology . 1985;116: 2376-2383.
21. Clarke IJ. Evidence that the switch from negative to positive feedback at the level of the pituitary gland is an important timing event for the onset of the preovulatory surge in LH in the ewe. J Endocrinol . 1995;145:271-282.
22. Bocking AD, McMillen IC, Harding R, Thorburn GD. Effect of reduced uterine blood flow on fetal and maternal cortisol. J Dev Physiol. 1986;8:237-245.
23. Tilbrook AJ, Rivalland EA, Turner AI, Lambert GW, Clarke IJ. Responses of the hypothalamopituitary adrenal axis and the sympathoadrenal system to isolation/restraint stress in sheep of different adiposity. Neuroendocrinology. 2008; 87:193-205.
24. Clarke IJ, Pereira A, Li Q, Smith JT. Sex steroid and leptin receptors in gonadotropin inhibitory hormone neurons. Endocr Rev. 2012; 33:SAT-672.
25. Seckl JR. 11β-hydroxysteroid dehydrogenase in the brain: a novel regulator of glucocorticoid action? Front Neuroendocrinol. 1997; 18:49-99.
26. Stackpole CA, Turner AI, Clarke IJ, Lambert GW, Tilbrook AJ. Seasonal differences in the effect of isolation and restraint stress on the luteinizing hormone response to gonadotropin-releasing hormone in hypothalamopituitary disconnected, gonadectomized rams and ewes. Biol Reprod. 2003;69:1158-1164.
27. Clarke IJ, Horton RJ, Doughton BW. Investigation of the mechanism by which insulin-induced hypoglycemia decreases luteinizing hormone secretion in ovariectomized ewes. Endocrinology. 19 90; 127:1470-1476.
28. Ohkura S, Tanaka T, Nagatani S, et al. Central, but not peripheral, glucose-sensing mechanisms mediate glucoprivic suppression of pulsatile luteinizing hormone secretion in the sheep. Endocrinology . 2000;141:4472-4480.
29. Son YL, Ubuka T, Narihiro M, et al. Molecular basis for the activation of gonadotropin-inhibitory hormone gene transcription by corticosterone. Endocrinology. 2014;155:1817-1826.
30. Lee TK, Lee C, Bischof R, Lambert GW, Clarke IJ, Henry BA. Stress-induced behavioral and metabolic adaptations lead to an obesity-prone phenotype in ewes with elevated cortisol responses. Psychoneuroendocrinology . 2014;47:166-177.
31. Harris TG, Battaglia DF, Brown ME, et al. Prostaglandins mediate the endotoxin-induced suppression of pulsatile gonadotropin-releasing hormone and luteinizing hormone secretion in the ewe. Endocrinology . 2000;141:1050-1058.
32. Debus N, Breen KM, Barrell GK, et al. Does cortisol mediate endotoxin-induced inhibitio n of pulsatile luteinizing hormone and gonadotropin-releasing hormone secretion? Endocrinology. 2002; 143:3748-3758.
33. Williams CY, Harris TG, Battaglia DF, Viguié C, Karsch FJ. Endo toxin inhibits pituitary responsiveness to gonadotropin-releasing hormone. Endocrinology. 2001;142:1915-1922.
34. Geraghty AC, Muroy SE, Zhao S, Bentley GE, Kriegsfeld LJ, Kaufer D. Knockdown of hypothalamic RFRP3 prevents chronic stressinduced infertility and embryo resorption. eLife. 2015;4.
35. Decourt C, Anger K, Robert V, et al. No evidence that RFamiderelated peptide 3 directly modulates LH secretion in the ewe. Endocrinology. 2016;157:1566-1575.
36. Clarke IJ, Smith JT, Henry BA, et al. Gonadotropin-inhibitory hormone is a hypothalamic peptide that provides a molecular switch between reproduction and feeding. Neuroendocrinology . 2012;95: 305-316.
37. Caraty A, Smith JT, Lomet D, et al. Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology. 2007;148:5258-5267.
38. Sari IP, Rao A, Smith JT, Tilbrook AJ, Clarke IJ. Effect of RF-Amiderelated peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology . 2009;150:5549-5556.
39. Clarke IJ, Qi Y, Puspita Sari I, Smith JT. Evidence that RF-Amide related peptides are i nhibitors of reproduction in mammals. Front Neuroendocrinol. 2009;30:371-378.
40. Smith JT, Clarke IJ. Gonadotropin inhibitory hormone function in mammals. Trends Endocrinol Metab. 2010;21:255-260.
41. Clarke IJ, Smith JT. The role of kisspeptin and gonadotropin inhibitory hormone (GnIH) in the seasonality of reproduction in sheep. Soc Reprod Fertil Suppl. 2010;67:159-169.
42. Dardente H, BirnieM, Lincoln GA, Hazlerigg DG. RFamide-related peptide and its cognate receptor in the sheep:cDNAcloning, mRNA distribution in the hypothalamus and the effect of photoperiod. J Neuroendocrinol. 2008;20:1252-1259.
43. Merkley CM, Coolen LM, Goodman RL, Lehman MN. Evidence for changes in numbers of synaptic inputs onto KNDy and GnRH neurones during the preovulatory LH surge in the ewe. J Neuroendocrinol . 2015;27:624-635.
44. Naftolin F, Mor G, Horvath TL, et al. Synaptic remodeling in the arcuate nucleus during the estrous cycle is induced by estrogen and precedes the preovulatory gonadotropin surge. Endocrinology . 1996;137:5576-5580.
45. Ubuka T, Kim S, Huang YC, et al. Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and-II neurons in European starling brain. Endocrinology . 2008;149:268-278.
46. Rizwan MZ, Poling MC, Corr M, et al. RFamide-related peptide-3 receptor gene expression in GnRH and kisspeptin neurons and GnRH-dependent mechanism of action. Endocrinology . 2012;153: 3770-3779.
47. Poling MC, Kim J, Dhamija S, Kauffman AS. Development, sex steroid regulation, and phenotypic characterization of RFamiderelated peptide (Rfrp) gene expression and RFamide receptors in the mouse hypothalamus. Endocrinology . 2012;153:1827-1840