17β-oestradiol regulation of gonadotrophin-releasing hormone neuronal Excitability

Journal of Neuroendocrinology

Volumn 24, Issue 1, 2012, Pages 122-130

  Ronnekleiv O K ^a,b   Bosch, M A ^a   Zhang, C ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Burst firing; Gonadotrophin releasing hormone neurones; Hyperpolarisation; T type calcium channels

Indexed keywords

4 AMINOBUTYRATE AMINOTRANSFERASE; CALCIUM CHANNEL T TYPE; ESTRADIOL; GONADORELIN; GREEN FLUORESCENT PROTEIN; KISSPEPTIN; MESSENGER RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

CALCIUM CELL LEVEL; HORMONAL REGULATION; HYPERPOLARIZATION; NEGATIVE FEEDBACK; NERVE CELL EXCITABILITY; NEUROTRANSMISSION; NONHUMAN; POSITIVE FEEDBACK; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS, T-TYPE; ESTRADIOL; GONADOTROPIN-RELEASING HORMONE; NEURONS;

EID: 84055188826     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02160.x     Document Type: Review

References (91)

1. Micevych P, Sinchak K, Mills RH, Tao L, LaPolt P, Lu JK. The luteinizing hormone surge is preceded by an estrogen-induced increase of hypothalamic progesterone in ovariectomized and adrenalectomized rats. Neuroendocrinology 2003; 78: 29-35.
2. Micevych P, Bondar G, Kuo J. Estrogen action on neuroendocrine glia. Neuroendocrinology 2010; 91: 211-222.
3. Levine JE, Ramirez VD. Luteinizing hormone-releasing hormone release during the rat estrous cycle and after ovariectomy, as estimated with push-pull cannulae. Endocrinology 1982; 111: 1439-1448.
4. Chappell PE, Levine JE. Stimulation of gonadotropin-releasing hormone surges by estrogen. I. Role of hypothalamic progesterone receptors. Endocrinology 2000; 141: 1477-1485.
5. Caraty A, Locatelli A, Martin GB. Biphasic response in the secretion of gonadotrophin-releasing hormone in ovariectomized ewes injected with oestradiol. J Endocrinol 1989; 123: 375-382.
6. Pau K-YF, Berria M, Hess DL, Spies HG. Preovulatory gonadotropin-releasing hormone surge in ovarian-intact rhesus macaques. Endocrinology 1993; 133: 1650-1656.
7. Evans NP, Dahl GE, Glover BH, Karsch FJ. Central regulation of pulsatile gonadotropin-releasing hormone (GnRH) secretion by estradiol during the period leading up to the preovulatory GnRH surge in the ewe. Endocrinology 1994; 134: 1806-1811.
8. Karsch FJ, Evans NP. Feedback actions of estradiol on GnRH secretion during the follicular phase of the estrous cycle. Acta Neurobiol Exp (Wars) 1996; 56: 715-725.
9. Karsch FJ, Bowen JM, Caraty A, Evans NP, Moenter SM. Gonadotropin-releasing hormone requirements for ovulation. Biol Reprod 1997; 56: 303-309.
10. Evans NP, Dahl GE, Mauger DT, Padmanabhan V, Thrun LA, Karsch FJ. Does estradiol induce the preovulatory gonadotropin-releasing hormone (GnRH) surge in the ewe by inducing a progressive change in the mode of operation of the GnRH neurosecretory system. Endocrinology 1995; 136: 5511-5519.
11. Evans NP, Dahl GE, Mauger D, Karsch FJ. Estradiol induces both qualitative and quantitative changes in the pattern of gonadotropin-releasing hormone secretion during the presurge period in the ewe. Endocrinology 1995; 136: 1603-1609.
12. Christian CA, Mobley JL, Moenter SM. Diurnal and estradiol-dependent changes in gonadotropin-releasing hormone neuron firing activity. Proc Natl Acad Sci USA 2005; 102: 15682-15687.
13. Christian CA, Moenter SM. Estradiol induces diurnal shifts in GABA transmission to gonadotropin-releasing hormone neurons to provide a neural signal for ovulation. J Neurosci 2007; 27: 1913-1921.
14. DeFazio RA, Heger S, Ojeda SR, Moenter SM. Activation of A-type gamma-aminobutyric receptors excites gonadotropin-releasing hormone neurons. Mol Endocrinol 2002; 16: 2872-2891.
15. Legan SJ, Coon GA, Karsch FJ. Role of estrogen as initiator of daily LH surges in the ovariectomized rat. Endocrinology 1975; 96: 50-56.
16. Christian CA, Moenter SM. Vasoactive intestinal polypeptide can excite gonadotropin-releasing hormone neurons in a manner dependent on estradiol and gated by time of day. Endocrinology 2008; 149: 3130-3136.
17. Chappell PE, Goodall CP, Tonsfeldt KJ, White RS, Bredeweg E, Latham KL. Modulation of gonadotropin-releasing hormone (GnRH) secretion by an endogenous circadian clock. J Neuroendocrinol 2009; 21: 339-345.
18. Miller JD, Morin LP, Schwartz WJ, Moore RY. New insights into the mammalian circadian clock. Sleep 1996; 19: 641-667.
19. Van der Beek EM, Horvath TL, Wiegant VM, Van den Hurk RV, Buijs RM. Evidence for a direct neuronal pathway from the suprachiasmatic nucleus to the gonadotropin-releasing hormone system: combined tracing and light and electron microscopic immunocytochemical studies. J Comp Neurol 1997; 384: 569-579.
20. Miller BH, Olson SL, Levine JE, Turek FW, Horton TH, Takahashi JS. Vasopressin regulation of the proestrous luteinizing hormone surge in wild-type and clock mutant mice. Biol Reprod 2006; 75: 778-784.
21. Vida B, Deli L, Hrabovszky E, Kalamatianos T, Caraty A, Coen CW, Liposits Z, Kalló I. Evidence for suprachiasmatic vasopressin neurons innervating kisspeptin neurons in the rostral periventricular area of the mouse brain: regulation by oestrogen. J Neuroendocrinol 2010; 22: 1032-1039.
22. Williams WP, III, Jarjisian SG, Mikkelsen JD, Kriegsfeld LJ. Circadian control of kisspeptin and a gated GnRH response mediate the preovulatory luteinizing hormone surge. Endocrinology 2011; 152: 595-606.
23. Robertson JL, Clifton DK, de la Iglesia HO, Steiner RA, Kauffman AS. Circadian regulation of Kiss1 neurons: implications for timing the preovulatory gonadotropin-releasing hormone/luteninizing hormone surge. Neuroendocrinology 2009; 150: 3664-3671.
24. Ducret E, Gaidamaka G, Herbison AE. Electrical and morphological characteristics of anteroventral periventricular nucleus kisspeptin and other neurons in the female mouse. Neuroendocrinology 2010; 151: 2223-2232.
25. Suter KJ, Wuarin JP, Smith BN, Dudek FE, Moenter SM. Whole-cell recordings from preoptic/hypothalamic slices reveal burst firing in gonadotropin-releasing hormone neurons identified with green fluorescent protein in transgenic mice. Endocrinology 2000; 141: 3731-3736.
26. Kuehl-Kovarik MC, Pouliot WA, Halterman GL, Handa RJ, Dudek FE, Partin KM. Episodic bursting activity and response to excitatory amino acids in acutely dissociated gonadotropin-releasing hormone neurons genetically targeted with green fluorescent protein. J Neurosci 2002; 22: 213-222.
27. Kuehl-Kovarik MC, Pouliot WA, Partin KM, Handa RJ, Dudek FE. Spike-dependent depolarizing afterpotentials contribute to endogenous bursting in gonadotropin releasing hormone neurons. Neuroscience 2005; 134: 295-300.
28. Chu Z, Moenter SM. Physiologic regulation of a tetrodotoxin-sensitive sodium influx that mediates a slow afterdepolarization potential in gonadotropin-releasing hormone neurons: possible implications for the central regulation of fertility. J Neurosci 2006; 26: 11961-11973.
29. Kelly MJ, Rønnekleiv OK. Electrophysiological analysis of neuroendocrine neuronal activity in hypothalamic slices. In: Levine JE, ed. Methods in Neurosciences: Pulsatility in Neuroendocrine Systems. San Diego, CA: Academic Press Inc., 1994: 47-67.
30. Kelly MJ, Wagner EJ. GnRH neurons and episodic bursting activity. Trends Endocrinol Metab 2002; 13: 409-410.
31. Lee K, Duan W, Sneyd J, Herbison AE. Two slow calcium-activated afterhyperpolarization currents control burst firing dynamics in gonadotropin-releasing hormone neurons. J Neurosci 2010; 30: 6214-6224.
32. Duan W, Lee K, Herbison AE, Sneyd J. A mathematical model of adult GnRH neurons in mouse brain and its bifurcation analysis. J Theor Biol 2011; 276: 22-34.
33. 2+ channels. Neuron 2001; 31: 35-45.
34. Chemin J, Monteil A, Perez-Reyes E, Bourinet E, Nargeot J, Lory P. Specific contribution of human T-type calcium channel isotypes (alpha(1G), alpha(1H) and alpha(1I)) to neuronal excitability. J Physiol 2002; 540: 3-14.
35. Erickson KR, Rønnekleiv OK, Kelly MJ. Role of a T-type calcium current in supporting a depolarizing potential, damped oscillations, and phasic firing in vasopressinergic guinea pig supraoptic neurons. Neuroendocrinology 1993; 57: 789-800.
36. Loose MD, Rønnekleiv OK, Kelly MJ. Membrane properties and response to opioids of identified dopamine neurons in the guinea pig hypothalamus. J Neurosci 1990; 10: 3627-3634.
37. 2+-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J Neurosci 1992; 12: 3804-3817.
38. Perez-Reyes E, Cribbs LL, Daud A, Lacerda AE, Barclay J, Williamson MP, Margaret F, Rees M, Lee J-H. Molecular characterization of a neuronal low-voltage-activated T-type calcium channel. Nature 1998; 391: 896-900.
39. Lee J-H, Daud AN, Cribbs LL, Lacerda AE, Pereverzev A, Klockner U, Schneider T, Perez-Reyes E. Cloning and expression of a novel member of the low voltage-activated T-type calcium channel family. J Neurosci 1999; 19: 1912-1921.
40. Qiu J, Bosch MA, Jamali K, Xue C, Kelly MJ, Rønnekleiv OK. Estrogen upregulates T-type calcium channels in the hypothalamus and pituitary. J Neurosci 2006; 26: 11072-11082.
41. Roepke TA, Xue C, Bosch MA, Scanlan TS, Kelly MJ, Rønnekleiv OK. Genes associated with membrane-initiated signaling of estrogen and energy homeostasis. Endocrinology 2008; 149: 6113-6124.
42. Lee AW, Kyrozis A, Chevaleyre V, Kow L-M, Zhou J, Devidze N, Zhang Q, Etgen AM, Pfaff DW. Voltage-dependent calcium channels in ventromedial hypothalamic neurones of postnatal rats: modulation by oestradiol and phenylephrine. J Neuroendocrinol 2008; 20: 188-198.
43. Huguenard JR, McCormick DA. Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J Neurophysiol 1992; 68: 1373-1383.
44. Bosch MA, Hou J, Fang Y, Kelly MJ, Rønnekleiv OK. 17β-estradiol regulation of the mRNA expression of T-type calcium channel subunits: role of estrogen receptor α and estrogen receptor β. J Comp Neurol 2009; 512: 347-358.
45. Qiu J, Bosch MA, Tobias SC, Grandy DK, Scanlan TS, Rønnekleiv OK, Kelly MJ. Rapid signaling of estrogen in hypothalamic neurons involves a novel G protein-coupled estrogen receptor that activates protein kinase C. J Neurosci 2003; 23: 9529-9540.
46. Qiu J, Bosch MA, Tobias SC, Krust A, Graham S, Murphy S, Korach KS, Chambon P, Scanlan TS, Rønnekleiv OK, Kelly MJ. A G protein-coupled estrogen receptor is involved in hypothalamic control of energy homeostasis. J Neurosci 2006; 26: 5649-5655.
47. Zhang C, Bosch MA, Rick EA, Kelly MJ, Rønnekleiv OK. 17β-estradiol regulation of T-type calcium channels in gonadotropin-releasing hormone neurons. J Neurosci 2009; 29: 10552-10562.
48. 2+ currents in rat gonadotropin-releasing hormone neurons. J Physiol Sci 2010; 60: 195-204.
49. Kato M, Ui-Tei K, Watanabe M, Sakuma Y. Characterization of voltage-gated calcium currents in gonadotropin-releasing hormone neurons tagged with green fluorescent protein in rats. Endocrinology 2003; 144: 5118-5125.
50. 2+ channels, SK2 channels and sercas gate sleep-related oscillations in thalamic dendrites. Nat Neurosci 2008; 11: 683-692.
51. Liu S, Shipley MT. Multiple conductances cooperatively regulate spontaneous bursting in mouse olfactory bulb external tufted cells. J Neurosci 2008; 28: 1625-1639.
52. Sun J, Chu Z, Moenter SM. Diurnal in vivo and rapid in vitro effects of estadiol on voltage-gated calcium channels in gonadotropin-releasing hormone neurons. J Neurosci 2010; 30: 3912-3923.
53. Nunemaker CS, DeFazio RA, Moenter SM. Calcium current subtypes in GnRH neurons. Biol Reprod 2003; 69: 1914-1922.
54. Spergel DJ. Calcium and small-conductance calcium-activated potassium channels in gonadotropin-releasing hormone neurons before, during, and after puberty. Endocrinology 2007; 148: 2383-2390.
55. Hille B. Potassium channels and chloride channels. In: Hille B, ed. Ion Channels of Excitable Membranes. Sunderland, MA: Sinaur, 2001: 131-165.
56. ATP channels that are regulated by estrogen and responsive to glucose and metabolic inhibition. J Neurosci 2007; 27: 10153-10164.
57. B receptor mediated inhibition of GnRH neurons is suppressed by kisspeptin-GPR54 signaling. Endocrinology 2009; 150: 2388-2394.
58. Lagrange AH, Rønnekleiv OK, Kelly MJ. Estradiol-17β and μ-opioid peptides rapidly hyperpolarize GnRH neurons: a cellular mechanism of negative feedback? Endocrinology 1995; 136: 2341-2344.
59. Xu J, Kirigiti MA, Cowley MA, Grove KL, Smith MS. Suppression of basal spontaneous gonadotropin-releasing hormone neuronal activity during lactation: role of inhibitory effects of neuropeptide Y. Endocrinology 2009; 150: 333-340.
60. Wu M, Dumalska I, Morozova E, Van den Pol AN, Alreja M. Melanin-concentrating hormone directly inhibits GnRH neurons and blocks kisspeptin activation, linking energy balance to reproduction. Proc Natl Acad Sci USA 2009; 106: 17217-17222.
61. Chu Z, Takagi H, Moenter SM. Hyperpolarization-activated currents in gonadotropin-releasing hormones (GnRH) neurons contribute to intrinsic excitability and are regulated by gonadal steroid feedback. J Neurosci 2010; 30: 13373-13383.
62. + channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci 2004; 24: 5301-5306.
63. + channel (SK3) mRNA in the guinea pig brain. Endocrinology 2002; 143: 1097-1107.
64. Kato M, Tanaka N, Usui S, Sakuma Y. SK channel blocker apamin inhibits slow afterhyperpolarization currents in rat gonadotropin-releasing hormone neurones. J Physiol 2006; 2: 431-442.
65. Liu X, Herbison AE. Small-conductance calcium-activated potassium channels control excitability and firing dynamics in gonadotropin-releasing hormone (GnRH) neurons. Endocrinology 2008; 149: 3598-3604.
66. Kelly MJ, Condon TP, Levine JE, Rønnekleiv OK. Combined electrophysiological, immunocytochemical and peptide release measurements in the hypothalamic slice. Brain Res 1985; 345: 264-270.
67. Krsmanovic LZ, Stojikovic SS, Merelli F, Dufour SM, Virmani MA, Catt KJ. Calcium signaling and episodic secretion of gonadotropin-releasing hormone in hypothalamic neurons. Proc Natl Acad Sci USA 1992; 89: 8462-8466.
68. Temple JL, Laing E, Sunder A, Wray S. Direct action of estradiol on gonadotropin-releasing hormone-1 neuronal activity via a transcription-dependent mechanism. J Neurosci 2004; 24: 6326-6333.
69. Temple JL, Wray S. BSA-estrogen compounds differentially alter gonadotropin-releasing hormone-1 neuronal activity. Endocrinology 2005; 146: 558-563.
70. Abe H, Keen KL, Terasawa E. Rapid action of estrogens on intracellular calcium oscillations in primate LHRH-1neurons. Endocrinology 2008; 149: 1155-1162.
71. Harrington WR, Kim SH, Funk CC, Madak-Erdogan Z, Schiff R, Katzenellenbogen JA, Katzenellenbogen BS. Estrogen dendrimer conjugates that preferentially activate extranuclear, nongenomic versus genomic pathways of estrogen action. Mol Endocrinol 2006; 20: 491-502.
72. Noel SD, Keen KL, Baumann DI, Filardo EJ, Terasawa E. Involvement of G-protein couple receptor 30 (GPR30) in rapid action of estrogen in primate LHRH neurons. Mol Endocrinol 2009; 3: 349-359.
73. Romanò N, Lee K, Ábrahám IM, Jasoni CL, Herbison AE. Non-classical estrogen modulation of presynaptic GABA terminals modulates calcium dynamics in gonadotropin-releasing hormone (GnRH) neurons. Endocrinology 2008; 149: 5335-5344.
74. Jasoni CL, Todman MG, Strumia MM, Herbison AE. Cell type-specific expression of a genetically encoded calcium indicator reveals intinsic calcium oscillations in adult gonadotropin-releasing hormone neurons. J Neurosci 2007; 27: 860-867.
75. Zhang C, Roepke TA, Kelly MJ, Rønnekleiv OK. Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 2008; 28: 4423-4434.
76. Liu X, Lee K, Herbison AE. Kisspeptin excites gonadotropin-releasing hormone (GnRH) neurons through a phosphilipase C/calcium-dependent pathway regulating multiple ion channels. Endocrinology 2008; 149: 4605-4614.
77. Pielecka-Fortuna J, Chu Z, Moenter SM. Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol. Endocrinology 2008; 149: 1979-1986.
78. Constantin S, Caligioni CS, Stojilkovic S, Wray S. Kisspeptin-10 facilitates a plasma membrane-driven calcium oscillator in gonadotropin-releasing hormone-1 neurons. Endocrinology 2009; 150: 1400-1412.
79. Spergel DJ, Kruth U, Hanley DF, Sprengel R, Seeburg PH. GABA-and glutamate activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J Neurosci 1999; 19: 2037-2050.
80. DeFazio RA, Moenter SM. Estradiol feedback alters potassium currents and firing properties of gonadotropin-releasing hormone neurons. Mol Endocrinol 2002; 16: 2255-2265.
81. Han SK, Abraham IM, Herbison AE. Effect of GABA on GnRH neurons switches from depolarization to hyperpolarization at puberty in the female mouse. Endocrinology 2002; 143: 1459-1466.
82. Herbison AE. Physiology of the gonadotropin-releasing hormone neuronal network. In: Neill JD, ed. Knobil and Neill's Physiology of Reproduction, 3rd edn. Boston, MA: Elsevier, 2006: 1415-1482.
83. Suter KJ. Control of firing by small (S)-α-amino-3-hydroxy-5methyl-isoxazolepropionic acid-like inputs in hypothalamic gonadotropin releasing-hormone (GnRH) neurons. Neuroscience 2004; 128: 443-450.
84. Kroll H, Bolsover S, Hsu J, Kim S-H, Bouloux P-M. Kisspeptin-evoked calcium signals in isolated primary rat gonadotropin-releasing hormone neurones. Neuroendocrinology 2011; 93: 114-120.
85. Clapham DE. TRP channels as cellular sensors. Nature 2003; 426: 517-524.
86. 2+ concentrations. Annu Rev Pharmacol Toxicol 2009; 49: 395-426.
87. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005; 146: 3686-3692.
88. Simerly RB. Hormonal control of the development and regulation of tyrosine hydroxylase expression within a sexually dimorphic population of dopaminergic cells in the hypothalamus. Brain Res Mol Brain Res 1989; 6: 297-310.
89. Ottem EN, Godwin JG, Krishnan S, Petersen SL. Dual-phenotype GABA/glutamate neurons in adult preoptic area: sexual dimorphism and function. J Neurosci 2004; 24: 8097-8105.
90. Liu X, Porteous R, d'Anglemont de Tassigny X, Colledge WH, Millar R, Petersen SL, Herbison AE. Frequency-dependent recruitment of fast amino acid and slow neuropeptide neurotransmitter release controls gonadotropin-releasing hormone neuron excitability. J Neurosci 2011; 31: 2421-2430.
91. Wang Y, Deshpande M, Payne R. 2-Aminoethoxydiphenyl borate inhibits phototransduction and blocks voltage-gated potassium channels in limulus ventral photoreceptors. Cell Calcium 2002; 32: 209-216.