Estradiol modulates Kiss1 neuronal response to ghrelin

American Journal of Physiology - Endocrinology and Metabolism

Volumn 306, Issue 6, 2014, Pages

  Frazao, Renata ^a,b   Dungan Lemko, Heather M ^a   da Silva, Regina P ^b   Ratra, Dhirender V ^c   Lee, Charlotte E ^a   Williams, Kevin W ^a   Zigman, Jeffrey M ^a   Elias, Carol F ^a,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Growth hormone secretagogue receptor; Hypothalamus; Kisspeptin; Metabolism; Reproduction

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GHRELIN; GHRELIN RECEPTOR; KISSPEPTIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARCUATE NUCLEUS; ARTICLE; BRAIN FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; FEMALE; HYPOTHALAMUS; MOUSE; NERVE CELL; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

GROWTH HORMONE SECRETAGOGUE RECEPTOR; HYPOTHALAMUS; KISSPEPTIN; METABOLISM; REPRODUCTION;

ACYLATION; ANIMALS; ARCUATE NUCLEUS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN REPLACEMENT THERAPY; FEMALE; GENE EXPRESSION REGULATION; GHRELIN; GREEN FLUORESCENT PROTEINS; HYPOTHALAMUS; KISSPEPTINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; OVARIECTOMY; RATS; RECEPTORS, GHRELIN; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84900556544     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00211.2013     Document Type: Article

References (51)

1. Balthazart J, Ball GF. Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front Neuroendocrinol 28: 161-178, 2007.
2. Burke MC, Letts PA, Krajewski SJ, Rance NE. Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: Morphologic evidence of interrelated function within the arcuate nucleus. J Comp Neurol 498: 712-726, 2006.
3. Butera PC, Wojcik DM, Clough SJ. Effects of estradiol on food intake and meal patterns for diets that differ in flavor and fat content. Physiol Behav 99: 142-145, 2010.
4. Castaneda TR, Tong J, Datta R, Culler M, Tschop MH. Ghrelin in the regulation of body weight and metabolism. Front Neuroendocrinol 31: 44-60, 2010.
5. Chuang JC, Sakata I, Kohno D, Perello M, Osborne-Lawrence S, Repa JJ, Zigman JM. Ghrelin directly stimulates glucagon secretion from pancreatic alpha-cells. Mol Endocrinol 25: 1600-1611, 2011.
6. Clegg DJ, Brown LM, Zigman JM, Kemp CJ, Strader AD, Benoit SC, Woods SC, Mangiaracina M, Geary N. Estradiol-dependent decrease in the orexigenic potency of ghrelin in female rats. Diabetes 56: 1051-1058, 2007.
7. Cravo RM, Margatho LO, Osborne-Lawrence S, Donato J Jr, Atkin S, Bookout AL, Rovinsky S, Frazao R, Lee CE, Gautron L, Zigman JM, Elias CF. Characterization of Kiss1 neurons using transgenic mouse models. Neuroscience 173: 37-56, 2011.
8. Dungan HM, Gottsch ML, Zeng H, Gragerov A, Bergmann JE, Vassilatis DK, Clifton DK, Steiner RA. The role of kisspeptin-GPR54 signaling in the tonic regulation and surge release of gonadotropinreleasing hormone/luteinizing hormone. J Neurosci 27: 12088-12095, 2007.
9. Elias CF, Purohit D. Leptin signaling and circuits in puberty and fertility. Cell Mol life Sci 70: 841-862, 2013.
10. Fernández-Fernández R, Tena-Sempere M, Aguilar E, Pinilla L. Ghrelin effects on gonadotropin secretion in male and female rats. Neurosci Lett 362: 103-107, 2004.
11. Fernández-Fernández R, Tena-Sempere M, Navarro VM, Barreiro ML, Castellano JM, Aguilar E, Pinilla L. Effects of ghrelin upon gonadotropin-releasing hormone and gonadotropin secretion in adult female rats: in vivo and in vitro studies. Neuroendocrinology 82: 245-255, 2005.
12. Flanagan-Cato LM. Sex differences in the neural circuit that mediates female sexual receptivity. Front Neuroendocrinol 32: 124-136, 2011.
13. Forbes S, Li XF, Kinsey-Jones J, O'Byrne K. Effects of ghrelin on Kisspeptin mRNA expression in the hypothalamic medial preoptic area and pulsatile luteinising hormone secretion in the female rat. Neurosci Lett 460: 143-147, 2009.
14. Frazao R, Cravo RM, Donato J Jr, Ratra DV, Clegg DJ, Elmquist JK, Zigman JM, Williams KW, Elias CF. Shift in Kiss1 cell activity requires estrogen receptor alpha. J Neurosci 33: 2807-2820, 2013.
15. Furuta M, Funabashi T, Kimura F. Intracerebroventricular administration of ghrelin rapidly suppresses pulsatile luteinizing hormone secretion in ovariectomized rats. Biochem Biophys Res Commun 288: 780-785, 2001.
16. Gavériaux-Ruff C, Kieffer BL. Conditional gene targeting in the mouse nervous system: Insights into brain function and diseases. Pharmacol Ther 113: 619-634, 2007.
17. Gottsch ML, Popa SM, Lawhorn JK, Qiu J, Tonsfeldt KJ, Bosch MA, Kelly MJ, Ronnekleiv OK, Sanz E, McKnight GS, Clifton DK, Palmiter RD, Steiner RA. Molecular properties of Kiss1 neurons in the arcuate nucleus of the mouse. Endocrinology 152: 4298-4309, 2011.
18. Grachev P, Li XF, Kinsey-Jones JS, di Domenico AL, Millar RP, Lightman SL, O'Byrne KT. Suppression of the GnRH pulse generator by neurokinin B involves a kappa-opioid receptor-dependent mechanism. Endocrinology 153: 4894-4904, 2012.
19. Harrison JL, Miller DW, Findlay PA, Adam CL. Photoperiod influences the central effects of ghrelin on food intake, GH and LH secretion in sheep. Neuroendocrinology 87: 182-192, 2008.
20. Herbison AE. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: The case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 57: 277-287, 2008.
21. Herbison AE, Moenter SM. Depolarising and hyperpolarising actions of GABA(A) receptor activation on gonadotrophin-releasing hormone neurones: towards an emerging consensus. J Neuroendocrinol 23: 557-569, 2011.
22. Higgins SC, Gueorguiev M, Korbonits M. Ghrelin, the peripheral hunger hormone. Ann Med 39: 116-136, 2007.
23. Hill JW, Elmquist JK, Elias CF. Hypothalamic pathways linking energy balance and reproduction. Am J Physiol Endocrinol Metab 294: E827-E832, 2008.
24. Iremonger KJ, Constantin S, Liu X, Herbison AE. Glutamate regulation of GnRH neuron excitability. Brain Res 1364: 35-43, 2010.
25. Kennedy GC, Mitra J. Body weight and food intake as initiating factors for puberty in the rat. J Physiol 166: 408-418, 1963.
26. Kinsey-Jones JS, Grachev P, Li XF, Lin YS, Milligan SR, Lightman SL, O'Byrne KT. The inhibitory effects of neurokinin B on GnRH pulse generator frequency in the female rat. Endocrinology 153: 307-315, 2012.
27. Kluge M, Schussler P, Schmidt D, Uhr M, Steiger A. Ghrelin suppresses secretion of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in women. J Clin Endocrinol Metab 97: E448-E451, 2012.
28. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402: 656-660, 1999.
29. Kollack-Walker S, Newman SW. Mating and agonistic behavior produce different patterns of Fos immunolabeling in the male Syrian hamster brain. Neuroscience 66: 721-736, 1995.
30. Martini AC, Fernández-Fernández R, Tovar S, Navarro VM, Vigo E, Vazquez MJ, Davies JS, Thompson NM, Aguilar E, Pinilla L, Wells T, Dieguez C, Tena-Sempere M. Comparative analysis of the effects of ghrelin and unacylated ghrelin on luteinizing hormone secretion in male rats. Endocrinology 147: 2374-2382, 2006.
31. Mayer C, Acosta-Martinez M, Dubois SL, Wolfe A, Radovick S, Boehm U, Levine JE. Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc Natl Acad Sci USA 107: 22693-22698, 2010.
32. Moenter SM, Chu Z, Christian CA. Neurobiological mechanisms underlying oestradiol negative and positive feedback regulation of gonadotrophin-releasing hormone neurones. J Neuroendocrinol 21: 327-333, 2009.
33. Moenter SM, DeFazio RA. Endogenous gamma-aminobutyric acid can excite gonadotropin-releasing hormone neurons. Endocrinology 146: 5374-5379, 2005.
34. Muccioli G, Lorenzi T, Lorenzi M, Ghe C, Arnoletti E, Raso GM, Castellucci M, Gualillo O, Meli R. Beyond the metabolic role of ghrelin: a new player in the regulation of reproductive function. Peptides 32: 2514-2521, 2011.
35. Musatov S, Chen W, Pfaff DW, Kaplitt MG, Ogawa S. RNAi-mediated silencing of estrogen receptor {alpha} in the ventromedial nucleus of hypothalamus abolishes female sexual behaviors. Proc Natl Acad Sci USA 103: 10456-10460, 2006.
36. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 29: 11859-11866, 2009.
37. Numan M, Woodside B. Maternity: neural mechanisms, motivational processes, and physiological adaptations. Behav Neurosci 124: 715-741, 2010.
38. Paredes RG, Baum MJ. Role of the medial preoptic area/anterior hypothalamus in the control of masculine sexual behavior. Annu Rev Sex Res 8: 68-101, 1997.
39. Paxinos G, Franklin C. The Mouse Brain in Stereotaxic Coordinates. Sydney, Australia: Academic, 2001.
40. Sakata I, Park WM, Walker AK, Piper PK, Chuang JC, Osborne-Lawrence S, Zigman JM. Glucose-mediated control of ghrelin release from primary cultures of gastric mucosal cells. Am J Physiol Endocrinol Metab 302: E1300-E1310, 2012.
41. Simerly RB, Carr AM, Zee MC, Lorang D. Ovarian steroid regulation of estrogen and progesterone receptor messenger ribonucleic acid in the anteroventral periventricular nucleus of the rat. J Neuroendocrinol 8: 45-56, 1996.
42. Simerly RB, Young BJ. Regulation of estrogen receptor messenger ribonucleic acid in rat hypothalamus by sex steroid hormones. Mol Endocrinol 5: 424-432, 1991.
43. Smith HR, Pang KC. Orexin-saporin lesions of the medial septum impair spatial memory. Neuroscience 132: 261-271, 2005.
44. Smith JT, Clay CM, Caraty A, Clarke IJ. KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 148: 1150-1157, 2007.
45. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 146: 3686-3692, 2005.
46. Tena-Sempere M. Ghrelin and reproduction: ghrelin as novel regulator of the gonadotropic axis. Vitam Horm 77: 285-300, 2008.
47. Tschop M, Smiley DL, Heiman ML. Ghrelin induces adiposity in rodents. Nature 407: 908-913, 2000.
48. Vulliemoz NR, Xiao E, Xia-Zhang L, Germond M, Rivier J, Ferin M. Decrease in luteinizing hormone pulse frequency during a five-hour peripheral ghrelin infusion in the ovariectomized rhesus monkey. J Clin Endocrinol Metab 89: 5718-5723, 2004.
49. Wade GN, Schneider JE, Li HY. Control of fertility by metabolic cues. Am J Physiol Endocrinol Metab 270: E1-E19, 1996.
50. Wiegand SJ, Terasawa E. Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology 34: 395-404, 1982.
51. Williams KW, Margatho LO, Lee CE, Choi M, Lee S, Scott MM, Elias CF, Elmquist JK. Segregation of acute leptin and insulin effects in distinct populations of arcuate proopiomelanocortin neurons. J Neurosci 30: 2472-2479, 2010.