The excitatory peptide kisspeptin restores the luteinizing hormone surge and modulates amino acid neurotransmission in the medial preoptic area of middle-aged rats

Endocrinology

Volumn 150, Issue 8, 2009, Pages 3699-3708

  Neal Perry, Genevieve ^a   Lebesgue, Diane ^a   Lederman, Matthew ^a   Shu, Jun ^a   Zeevalk, Gail D ^b   Etgen, Anne M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; DIZOCILPINE; ESTROGEN; KISSPEPTIN; LUTEINIZING HORMONE; MESSENGER RNA;

AGED; AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME REGULATION; FEMALE; LUTEINIZING HORMONE RELEASE; MEDIAL PREOPTIC AREA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

AGE FACTORS; AMINO ACIDS; ANIMALS; DIZOCILPINE MALEATE; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; LUTEINIZING HORMONE; NEUROPROTECTIVE AGENTS; PREOPTIC AREA; PROGESTERONE; PROGESTINS; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYNAPTIC TRANSMISSION;

EID: 67651151321     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1667     Document Type: Article

References (84)

1. Clarkson J, d'Anglemont de Tassigny X, Moreno AS, Colledge WH, Herbison AE 2008 Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci 28:8691-8697
2. d'Anglemont de Tassigny X, Fagg LA, Carlton MB, Colledge WH 2008 Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology 149:3926-3932
3. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE 2005 Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 25:11349-11356
4. Navarro VM, Castellano JM, Fernández-Fernández R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M 2004 Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 145:4565-4574
5. Ojeda SR, Lomniczi A, Mastronardi C, Heger S, Roth C, Parent AS, Matagne V, Mungenast AE 2006 Minireview: the neuroendocrine regulation of puberty: is the time ripe for a systems biology approach? Endocrinology 147:1166-1174
6. Le WW, Berghorn KA, Rassnick S, Hoffman GE 1999 Periventricular preoptic area neurons coactivated with luteinizing hormone (LH)-releasing hormone (LHRH) neurons at the time of the LH surge are LHRH afferents. Endocrinology 140:510-519
7. Wiegand SJ, Terasawa E, Bridson WE 1978 Persistent estrus and blockade of progesterone-induced LH release follows lesions which do not damage the suprachiasmatic nucleus. Endocrinology 102:1645-1648
8. Moguilevsky JA, Wuttke W 2001 Changes in the control of gonadotrophin secretion by neurotransmitters during sexual development in rats. Exp Clin Endocrinol Diabetes 109:188-195
9. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K 2005 Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 146:4431-4436
10. Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA 2006 Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 26:6687-6694
11. Adachi S, Yamada S, Takatsu Y, Matsui H, Kinoshita M, Takase K, Sugiura H, Ohtaki T, Matsumoto H, Uenoyama Y, Tsukamura H, Inoue K, Maeda K 2007 Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 53:367-378
12. Clarkson J, Herbison AE 2009 Oestrogen, kisspeptin, GPR54 and the preovulatory luteinising hormone surge. J Neuroendocrinol 21:305-311
13. Plant TM, Ramaswamy S 2009 Kisspeptin and the regulation of the hypothalamic-pituitary-gonadal axis in the rhesus monkey (Macaca mulatta). Peptides 30:67-75
14. Downs JL, Wise PM 2009 The role of the brain in female reproductive aging. Mol Cell Endocrinol 299:32-38
15. Mitsushima D, Tin-Tin-Win-Shwe, Kimura F 2003 Sexual dimorphism in the GABAergic control of gonadotropin release in intact rats. Neurosci Res 46:399-405
16. Ping L, Mahesh VB, Wiedmeier VT, Brann DW 1994 Release of glutamate and aspartate from the preoptic area during the progesterone-induced LH surge: in vivo microdialysis studies. Neuroendocrinology 59:318-324
17. Mitsushima D, Shwe TT, Funabashi T, Shinohara K, Kimura F 2002 GABA release in the medial preoptic area of cyclic female rats. Neuroscience 113:109-114
18. Brann DW 1995 Glutamate: a major excitatory transmitter in neuroendocrine regulation. Neuroendocrinology 61:213-225
19. Funabashi T, Jinnai K, Kimura F 1997 Bicuculline infusion advances the timing of Fos expression in LHRH neurons in the preoptic area of proestrous rats. Neuroreport 8:771-774
20. Neal-Perry GS ZG, Shu J, Santoro NF, Etgen AM, Reduced medial preoptic area glutamate and increased GABA levels on the day of the LH surge: a hypothalamic cause for reproductive senescence. Program of the 89th Annual Meeting of The Endocrine Society, San Francisco, CA, 2007 p686 (Abstract P4-76)
21. Neal-Perry GS, Zeevalk GD, Shu J, Etgen AM 2008 Restoration of the luteinizing hormone surge in middle-aged female rats by altering the balance of GABA and glutamate transmission in the medial preoptic area. Biol Reprod 79:878 -888
22. Wagner EJ, Ronnekleiv OK, Bosch MA, Kelly MJ 2001 Estrogen biphasically modifies hypothalamic GABAergic function concomitantly with negative and positive control of luteinizing hormone release. J Neurosci 21:2085-2093
23. Brann DW, Mahesh VB 1991 Endogenous excitatory amino acid involvement in the preovulatory and steroid-induced surge of gonadotropins in the female rat. Endocrinology 128:1541-1547
24. Urbanski HF, Ojeda SR 1990 A role for N-methyl-D- aspartate (NMDA) receptors in the control of LH secretion and initiation of female puberty. Endocrinology 126:1774-1776
25. Seltzer AM, Donoso AO 1992 Restraining action of GABA on estradiol-induced LH surge in the rat: GABA activity in brain nuclei and effects of GABA mimetics in the medial preoptic nucleus. Neuroendocrinology 55:28-34
26. Pielecka-Fortuna J, Chu Z, Moenter SM 2008 Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol. Endocrinology 149:1979-1986
27. Dumalska I, Wu M, Morozova E, Liu R, van den Pol A, Alreja M 2008 Excitatory effects of the puberty-initiating peptide kisspeptin and group I metabotropic glutamate receptor agonists differentiate two distinct subpopulations of gonadotropin-releasing hormone neurons. J Neurosci 28:8003-8013
28. Zhang C, Bosch MA, Ronnekleiv OK, Kelly MJ 2009 GABAB receptor mediated inhibition of GnRH neurons is suppressed by kisspeptin-GPR54 signaling. Endocrinology 150:2388-2394
29. Arias P, Carbone S, Szwarcfarb B, Feleder C, Rodríguez M, Scacchi P, Moguilevsky JA 1996 Effects of aging on N-methyl- D-aspartate (NMDA)-induced GnRH and LH release in female rats. Brain Res 740:234-238
30. Cashion AB, Smith MJ, Wise PM 2004 Glutamic acid decarboxylase 67 (GAD67) gene expression in discrete regions of the rostral preoptic area change during the oestrous cycle and with age. J Neuroendocrinol 16:711-716
31. Neal-Perry GS, Zeevalk GD, Santoro NF, Etgen AM 2005 Attenuation of preoptic area glutamate release correlates with reduced luteinizing hormone secretion in middle-aged female rats. Endocrinology 146:4331-4339
32. Grove-Strawser D, Jimenez-Linan M, Rubin BS 2007 Middle-aged female rats lack the dynamic changes in GAD(67) mRNA levels observed in young females on the day of a luteinising hormone surge. J Neuroendocrinol 19:708-716
33. Maffucci JA, Walker DM, Ikegami A, Woller MJ, Gore AC 2008 NMDA receptor subunit NR2b: effects on LH release and GnRH gene expression in young and middle-aged female rats, with modulation by estradiol. Neuroendocrinology 87:129-141
34. Le WW, Wise PM, Murphy AZ, Coolen LM, Hoffman GE 2001 Parallel declines in Fos activation of the medial anteroventral periventricular nucleus and LHRH neurons in middle-aged rats. Endocrinology 142:4976-4982
35. Kim W, Jessen HM, Auger AP, Terasawa E 2009 Postmenopausal increase in KiSS-1, GPR54, and luteinizing hormone releasing hormone (LHRH-1) mRNA in the basal hypothalamus of female rhesus monkeys. Peptides 30:103-110
36. Rometo AM, Krajewski SJ, Voytko ML, Rance NE 2007 Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys. J Clin Endocrinol Metab 92:2744-2750
37. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brézillon S, Tyldesley R, Suarez-Huerta N, Vandeput F, Blanpain C, Schiffmann SN, Vassart G, Parmentier M 2001 The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 276:34631-34636
38. Lee WS, Abbud R, Hoffman GE, Smith MS 1993 Effects of N-methyl-D-aspartate receptor activation on cFos expression in luteinizing hormone-releasing hormone neurons in female rats. Endocrinology 133:2248-2254
39. Horvath JE, Bajo AM, Schally AV, Kovacs M, Herbert F, Groot K 2002 Effects of long-term treatment with the luteinizing hormone-releasing hormone (LHRH) agonist Decapeptyl and the LHRH antagonist Cetrorelix on the levels of pituitary LHRH receptors and their mRNA expression in rats. Proc Natl Acad Sci USA 99:15048-15053
40. Kovacs M, Schally AV 2001 Comparison of mechanisms of action of luteinizing hormone-releasing hormone (LHRH) antagonist cetrorelix and LHRH agonist triptorelin on the gene expression of pituitary LHRH receptors in rats. Proc Natl Acad Sci USA 98:12197-12202
41. Richard N, Galmiche G, Corvaisier S, Caraty A, Kottler ML 2008 KiSS-1 and GPR54 genes are co-expressed in rat gonadotrophs and differentially regulated in vivo by oestradiol and gonadotrophin-releasing hormone. J Neuroendocrinol 20:381-393
42. Pellegrino LJ 1979 A stereotaxic atlas of the rat brain. 2nd ed. New York: Plenum Press
43. Freeman MC, Dupke KC, Croteau CM 1976 Extinction of the estrogen-induced daily signal for LH release in the rat: a role for the proestrous surge of progesterone. Endocrinology 99:223-229
44. Smith JT 2009 Sex steroid control of hypothalamic Kiss1 expression in sheep and rodents: comparative aspects. Peptides 30:94-102
45. Gutiérrez-Pascual E, Martínez-Fuentes AJ, Pinilla L, Tena-Sempere M, Malagón MM, Castaño JP 2007 Direct pituitary effects of kisspeptin: activation of gonadotrophs and somatotrophs and stimulation of luteinising hormone and growth hormone secretion. J Neuroendocrinol 19:521-530
46. Carbone S, Szwarcfarb B, Otero Losada ME, Moguilevsky JA 1992 Effects of ovarian steroids on the gonadotropin response to N-methyl- D-aspartate and on hypothalamic excitatory amino acid levels during sexual maturation in female rats. Endocrinology 130:1365-1370
47. Lloyd JM, Hoffman GE, Wise PM 1994 Decline in immediate early gene expression in gonadotropin-releasing hormone neurons during proestrus in regularly cycling, middle-aged rats. Endocrinology 134:1800-1805
48. Krajnak K, Rosewell KL, Wise PM 2001 Fos-induction in gonadotropin-releasing hormone neurons receiving vasoactive intestinal polypeptide innervation is reduced in middle-aged female rats. Biol Reprod 64:1160-1164
49. Wiegand SJ, Terasawa E, Bridson WE, Goy RW 1980 Effects of discrete lesions of preoptic and suprachiasmatic structures in the female rat. Alterations in the feedback regulation of gonadotropin secretion. Neuroendocrinology 31:147-157
50. Hahn JD, Coen CW 2006 Comparative study of the sources of neuronal projections to the site of gonadotrophin-releasing hormone perikarya and to the anteroventral periventricular nucleus in female rats. J Comp Neurol 494:190-214
51. Mikkelsen JD, Bentsen AH, Ansel L, Simonneaux V, Juul A 2009 Comparison of the effects of peripherally administered kisspeptins. Regul Peptides 152:95-100
52. Gu G, Varoqueaux F, Simerly RB 1999 Hormonal regulation of glutamate receptor gene expression in the anteroventral periventricular nucleus of the hypothalamus. J Neurosci 19:3213-3222
53. Wise PM, Smith MJ, Dubal DB, Wilson ME, Rau SW, Cashion AB, Böttner M, Rosewell KL 2002 Neuroendocrine modulation and repercussions of female reproductive aging. Recent Prog Horm Res 57:235-256
54. Roa J, Vigo E, Castellano JM, Gaytan F, Navarro VM, Aguilar E, Dijcks FA, Ederveen AG, Pinilla L, van Noort PI, Tena-Sempere M 2008 Opposite roles of estrogen receptor (ER)-α and ERβ in the modulation of luteinizing hormone responses to kisspeptin in the female rat: implications for the generation of the preovulatory surge. Endocrinology 149:1627-1637
55. Dungan HM, Gottsch ML, Zeng H, Gragerov A, Bergmann JE, Vassilatis DK, Clifton DK, Steiner RA 2007 The role of kisspeptin-GPR54 signaling in the tonic regulation and surge release of gonadotropin-releasing hormone/luteinizing hormone. J Neurosci 27:12088-12095
56. de la Iglesia HO, Schwartz WJ 2006 Minireview: timely ovulation: circadian regulation of the female hypothalamo-pituitary-gonadal axis. Endocrinology 147:1148-1153
57. Christian CA, Moenter SM 2008 Vasoactive intestinal polypeptide can excite gonadotropin-releasing hormone neurons in a manner dependent on estradiol and gated by time of day. Endocrinology 149:3130-3136
58. van der Beek EM, Swarts HJ, Wiegant VM 1999 Central administration of antiserum to vasoactive intestinal peptide delays and reduces luteinizing hormone and prolactin surges in ovariectomized, estrogen-treated rats. Neuroendocrinology 69:227-237
59. Harney JP, Scarbrough K, Rosewell KL, Wise PM 1996 In vivo antisense antagonism of vasoactive intestinal peptide in the suprachiasmatic nuclei causes aging-like changes in the estradiol-induced luteinizing hormone and prolactin surges. Endocrinology 137:3696-3701
60. van der Beek EM, Wiegant VM, van der Donk HA, van den Hurk R, Buijs RM 1993 Lesions of the suprachiasmatic nucleus indicate the presence of a direct vasoactive intestinal polypeptide-containing projection to gonadotrophin-releasing hormone neurons in the female rat. J Neuroendocrinol 5:137-144
61. Krajnak K, Kashon ML, Rosewell KL, Wise PM 1998 Aging alters the rhythmic expression of vasoactive intestinal polypeptide mRNA but not arginine vasopressin mRNA in the suprachiasmatic nuclei of female rats. J Neurosci 18:4767-4774
62. Krajnak K, Kashon ML, Rosewell KL, Wise PM 1998 Sex differences in the daily rhythm of vasoactive intestinal polypeptide but not arginine vasopressin messenger ribonucleic acid in the suprachiasmatic nuclei. Endocrinology 139:4189-4196
63. Roa J, Vigo E, Castellano JM, Navarro VM, Fernández- Fernández R, Casanueva FF, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M 2006 Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female rat. Endocrinology 147:2864-2878
64. Seminara SB, Dipietro MJ, Ramaswamy S, Crowley Jr WF, Plant TM 2006 Continuous human metastin 45-54 infusion desensitizes G protein-coupled receptor 54-induced gonadotropin-releasing hormone release monitored indirectly in the juvenile male Rhesus monkey (Macaca mulatta): a finding with therapeutic implications. Endocrinology 147:2122-2126
65. Clarkson J, Herbison AE 2006 Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 147:5817-5825
66. Brann DW, Mahesh VB 2005 The aging reproductive neuroendocrine axis. Steroids 70:273-283
67. Liu X, Lee K, Herbison AE 2008 Kisspeptin excites gonadotropin-releasing hormone neurons through a phospholipase C/calcium-dependent pathway regulating multiple ion channels. Endocrinology 149:4605-4614
68. Gore AC, Wu TJ, Rosenberg JJ, Roberts JL 1996 Gonadotropin- releasing hormone and NMDA receptor gene expression and colocalization change during puberty in female rats. J Neurosci 16:5281-5289
69. Dhandapani KM, Brann DW 2000 The role of glutamate and nitric oxide in the reproductive neuroendocrine system. Biochem Cell Biol 78:165-179
70. Herbison AE 1997 Noradrenergic regulation of cyclic GnRH secretion. Rev Reprod 2:1-6
71. Moenter SM, DeFazio RA 2005 Endogenous γ-aminobutyric acid can excite gonadotropin-releasing hormone neurons. Endocrinology 146:5374-5379
72. Spergel DJ, Krüth U, Hanley DF, Sprengel R, Seeburg PH 1999 GABA- and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J Neurosci 19:2037-2050
73. Roa J, Vigo E, García-Galiano D, Castellano JM, Navarro VM, Pineda R, Diéguez C, Aguilar E, Pinilla L, Tena-Sempere M 2008 Desensitization of gonadotropin responses to kisspeptin in the female rat: analyses of LH and FSH secretion at different developmental and metabolic states. Am J Physiol Endocrinol Metab 294:E1088-E1096
74. Miller BH, Gore AC 2002 N-methyl-D-aspartate receptor subunit expression in GnRH neurons changes during reproductive senescence in the female rat. Endocrinology 143:3568-3574
75. Adjan V, Centers A, Jennes L 2008 Expression and activation of NMDAR1 receptor subunits in gonadotrophin releasing hormone (GnRH) neurones of young and middle-aged mice during the LH surge. J Neuroendocrinol 20:1147-1154
76. Zhang C, Roepke TA, Kelly MJ, Rønnekleiv OK 2008 Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 28:4423-4434
77. Petersen SL, Ottem EN, Carpenter CD 2003 Direct and indirect regulation of gonadotropin-releasing hormone neurons by estradiol. Biol Reprod 69:1771-1778
78. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA 2004 Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 80:264-272
79. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA 2004 A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145:4073-4077
80. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR 2004 Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 16:850-858
81. Paxinos G, Watson C 2007 The rat brain in stereotaxic coordinates. Burlington, MA: Academic Press of Elsevier
82. Adler BA, Crowley WR 1986 Evidence for gamma-aminobutyric acid modulation of ovarian hormonal effects on luteinizing hormone secretion and hypothalamic catecholamine activity in the female rat. Endocrinology 118:91-97
83. Mohankumar PS, Thyagarajan S, Quadri SK 1995 Cyclic and age-related changes in norepinephrine concentrations in the medial preoptic area and arcuate nucleus. Brain Res Bull 38:561-564
84. Wise PM 1982 Norepinephrine and dopamine activity in microdissected brain areas of the middle-aged and young rat on proestrus. Biol Reprod 27:562-574