Firing pattern and rapid modulation of activity by estrogen in primate luteinizing hormone releasing hormone-1 neurons

Endocrinology

Volumn 146, Issue 10, 2005, Pages 4312-4320

  Abe, Hideki ^a,c   Terasawa, Ei ^a,b  

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; FULVESTRANT; GONADORELIN; GONADORELIN 1; POTASSIUM ION; RECEPTOR BLOCKING AGENT; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ESTROGEN ACTIVITY; HORMONE ACTION; LATENT PERIOD; NERVE CELL; NERVE CONDUCTION; NERVE STIMULATION; NONHUMAN; PATCH CLAMP; PRIMATE; PRIORITY JOURNAL; RECORDING;

ANIMALS; ESTRADIOL; EVOKED POTENTIALS; GONADOTROPIN-RELEASING HORMONE; LUTEINIZING HORMONE; MACACA MULATTA; NEURONS; PYRROLIDONECARBOXYLIC ACID;

EID: 24944439023     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2005-0435     Document Type: Article

References (62)

1. Wilson RC, Kesner JS, Kaufman JM, Uemura T, Akema T, Knobil E 1984 Central electrophysiologic correlates of pulsatile luteinizing hormone secretion in the rhesus monkey. Neuroendocrinology 39:256-260
2. Tanaka T, Ozawa T, Hoshino K, Mori Y 1995 Changes in the gonadotropin-releasing hormone pulse generator activity during the estrous cycle in the goat. Neuroendocrinology 62:553-561
3. Nishihara M, Takeuchi Y, Tanaka T, Mori Y 1999 Electrophysiological correlates of pulsatile and surge gonadotrophin secretion. Rev Reprod 4:110-116
4. Terasawa E 2003 Pulse generation in LHRH neurons. In: Handa R, Hayashi S, Terasawa E, Kawata M, eds. Neuroplasticity, development, and steroid hormone action. Boca Raton, FL: CRC Press; 153-168
5. Terasawa E 2001 Luteinizing hormone-releasing hormone (LHRH) neurons: mechanism of pulsatile LHRH release. Vitam Horm 63:91-129
6. 2+ oscillations in luteinizing hormone-releasing hormone neurons derived from the embryonic olfactory placode of the rhesus monkey. J Neurosci 19:5898-5909
7. Terasawa E, Keen KL, Mogi K, Claude P 1999 Pulsatile release of luteinizing hormone-releasing hormone (LHRH) in cultured LHRH neurons derived from the embryonic olfactory placode of the rhesus monkey. Endocrinology 140:1432-1441
8. Moore Jr JP, Shang E, Wray S 2002 In situ GABAergic modulation of synchronous gonadotropin releasing hormone-1 neuronal activity. J Neurosci 22:8932-8941
9. Parhar IS 2002 Cell migration and evolutionary significance of GnRH subtypes. Prog Brain Res 141:3-17
10. Skynner MJ, Slater R, Sim JA, Allen ND, Herbison AE 1999 Promoter transgenics reveal multiple gonadotropin-releasing hormone-I-expressing cell populations of different embryological origin in mouse brain. J Neurosci 19:5955-5966
11. Spergel DJ, Kruth 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
12. Suter KJ, Song WJ, Sampson TL, Wuarin JP, Saunders JT, Dudek FE, Moenter SM 2000 Genetic targeting of green fluorescent protein to gonadotropinreleasing hormone neurons: characterization of whole-cell electrophysiological properties and morphology. Endocrinology 141:412-419
13. Suter KJ, Wuarin JP, Smith BN, Dudek FE, Moenter SM 2000 Whole-cell recordings from preoptic/hypothalamic slices reveal burst firing in gonadotropin-releasing hormone neurons identified with green fluorescent protein in transgenic mice. Endocrinology 141:3731-3736
14. DeFazio RA, Heger S, Ojeda SR, Moenter SM 2002 Activation of A-type gamma-aminobutyric acid receptors excites gonadotropin-releasing hormone neurons. Mol Endocrinol 16:2872-2891
15. DeFazio RA, Moenter SM 2002 Estradiol feedback alters potassium currents and firing properties of gonadotropin-releasing hormone neurons. Mol Endocrinol 16:2255-2265
16. Moenter SM, DeFazio RA, Pitts GR, Nunemaker CS 2003 Mechanisms underlying episodic gonadotropin-releasing hormone secretion. Front Neuroendocrinol 24:79-93
17. Nunemaker CS, DeFazio RA, Moenter SM 2003 A targeted extracellular approach for recording long-term firing patterns of excitable cells: a practical guide. Biol Proced Online 5:53-62
18. Nunemaker CS, DeFazio RA, Moenter SM 2003 Calcium current subtypes in gonadotropin-releasing hormone neurons. Biol Reprod 69:1914-1922
19. Nunemaker CS, Straume M, DeFazio RA, Moenter SM 2003 Gonadotropin- releasing hormone neurons generate interacting rhythms in multiple time domains. Endocrinology 144:823-831
20. Kato M, Ui-Tei K, Watanabe M, Sakuma Y 2003 Characterization of voltage-gated calcium currents in gonadotropin-releasing hormone neurons tagged with green fluorescent protein in rats. Endocrinology 144:5118-5125
21. Terasawa E, Quanbeck CD, Schulz CA, Burich AJ, Luchansky LL, Claude P 1993 A primary cell culture system of luteinizing hormone releasing hormone neurons derived from embryonic olfactory placode in the rhesus monkey. Endocrinology 133:2379-2390
22. Veldhuis JD, Johnson ML 1986 Cluster analysis: a simple, versatile, and robust algorithm for endocrine pulse detection. Am J Physiol 250:E486-E493
23. 2+ oscillations among primate LHRH neurons and nonneuronal cells in vitro. J Neurophysiol 88:1559-1567
24. Kuehl-Kovarik MC, Pouliot WA, Halterman GL, Handa RJ, Dudek FE, Partin KM 2002 Episodic bursting activity and response to excitatory amino acids in acutely dissociated gonadotropin-releasing hormone neurons genetically targeted with green fluorescent protein. J Neurosci 22:2313-2322
25. Kusano K, Fueshko S, Gainer H, Wray S 1995 Electrical and synaptic properties of embryonic luteinizing hormone-releasing hormone neurons in explant cultures. Proc Natl Acad Sci USA 92:3918-3922
26. Charles AC, Hales TG 1995 Mechanisms of spontaneous calcium oscillations and action potentials in immortalized hypothalamic (GT1-7) neurons. J Neurophysiol 73:56-64
27. Sim JA, Skynner MJ, Herbison AE 2001 Heterogeneity in the basic membrane properties of postnatal gonadotropin-releasing hormone neurons in the mouse. J Neurosci 21:1067-1075
28. Mellon PL, Windle JJ, Goldsmith PC, Padula CA, Roberts JL, Weiner RI 1990 Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 5:1-10
29. Krsmanovic LZ, Stojilkovic SS, Merelli F, Dufour SM, Virmani MA, Catt KJ 1992 Calcium signaling and episodic secretion of gonadotropin-releasing hormone in hypothalamic neurons. Proc Natl Acad Sci USA 89:8462-8466
30. Bosma MM 1993 Ion channel properties and episodic activity in isolated immortalized gonadotropin-releasing hormone (GnRH) neurons. J Membr Biol 136:85-96
31. Nunemaker CS, DeFazio RA, Geusz ME, Herzog ED, Pitts GR, Moenter SM 2001 Long-term recordings of networks of immortalized GnRH neurons reveal episodic patterns of electrical activity. J Neurophysiol 86:86-93
32. Steiner RA, Bremner WJ, Clifton DK 1982 Regulation of luteinizing hormone pulse frequency and amplitude by testosterone in the adult male rat. Endocrinology 111:2055-2061
33. Kokoris GJ, Lam NY, Ferin M, Silverman AJ, Gibson MJ 1988 Transplanted gonadotropin-releasing hormone neurons promote pulsatile luteinizing hormone secretion in congenitally hypogonadal (hpg) male mice. Neuroendocrinology 48:45-52
34. Martinez de la Escalera G, Choi AL, Weiner RI 1992 Generation and synchronization of gonadotropin-releasing hormone (GnRH) pulses: intrinsic properties of the GT1-1 GnRH neuronal cell line. Proc Natl Acad Sci USA 89:1852-1855
35. Wetsel WC, Valenca MM, Merchenthaler I, Liposits Z, Lopez FJ, Weiner RI, Mellon PL, Negro-Vilar A 1992 Intrinsic pulsatile secretory activity of immortalized luteinizing hormone-releasing hormone-secreting neurons. Proc Natl Acad Sci USA 89:4149-4153
36. Bhattacharya AN, Dierschke DJ, Yamaji T, Knobil E 1972 The pharmacologic blockade of the circhoral mode of LH secretion in the ovariectomized rhesus monkey. Endocrinology 90:778-786
37. Gearing M, Terasawa E 1988 Luteinizing hormone releasing hormone (LHRH) neuroterminals mapped using the push-pull perfusion method in the rhesus monkey. Brain Res Bull 21:117-121
38. Funabashi T, Suyama K, Uemura T, Hirose M, Hirahara F, Kimura F 2001 Immortalized gonadotropin-releasing hormone neurons (GT1-7 cells) exhibit synchronous bursts of action potentials. Neuroendocrinology 73:157-165
39. Nunemaker CS, DeFazio RA, Moenter SM 2002 Estradiol-sensitive afferents modulate long-term episodic firing patterns of GnRH neurons. Endocrinology 143:2284-2292
40. Costantin JL, Charles AC 1999 Spontaneous action potentials initiate rhythmic intercellular calcium waves in immortalized hypothalamic (GT1-1) neurons. J Neurophysiol 82:429-435
41. Andrew RD, Dudek FE 1984 Analysis of intracellularly recorded phasic bursting by mammalian neuroendocrine cells. J Neurophysiol 51:552-566
42. Andrew RD, Dudek FE 1983 Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism. Science 221:1050-1052
43. Dudek FE, Tasker JG, Wuarin JP 1989 Intrinsic and synaptic mechanisms of hypothalamic neurons studied with slice and explant preparations. J Neurosci Methods 28:59-69
44. Cazalis M, Dayanithi G, Nordmann JJ 1985 The role of patterned burst and interburst interval on the excitation-coupling mechanism in the isolated rat neural lobe. J Physiol 369:45-60
45. Leng G, Brown CH, Russell JA 1999 Physiological pathways regulating the activity of magnocellular neurosecretory cells. Prog Neurobiol 57:625-655
46. Lewis TJ, Rinzel J 2000 Self-organized synchronous oscillations in a network of excitable cells coupled by gap junctions. Network 11:299-320
47. Abe H, Keen KL, Terasawa E Estrogen stimulates intracellular calcium oscillations and synchronization in LHRH neurons derived from monkey olfactory placodes. Proceedings of the 33th Annual Meeting of The Society for Neuroscience, New Orleans, LA, 2003 (Abstract 15.2)
48. Abe H, Keen KL, Frost SI, Terasawa E Estrogen causes rapid stimulatory action through membrane receptors in primate LHRH neurons. Proceedings of the 87th Annual Meeting of The Endocrine Society, San Diego, CA, 2005, p 71 (Abstract OR1-1)
49. Temple JL, Laing E, Sunder A, Wray S 2004 Direct action of estradiol on gonadotropin-releasing hormone-1 neuronal activity via a transcription-dependent mechanism. J Neurosci 24:6326-6333
50. 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 141:3506-3509
51. Hrabovszky E, Steinhauser A, Barabas K, Shughrue PJ, Petersen SL, Merchenthaler I, Liposits Z 2001 Estrogen receptor-β immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 142:3261-3264
52. Herbison AE, Pape JR 2001 New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front Neuroendocrinol 22:292-308
53. Sharifi N, Reuss AE, Wray S 2002 Prenatal LHRH neurons in nasal explant cultures express estrogen receptor beta transcript. Endocrinology 143:2503-2507
54. Skinner DC, Dufourny L 2005 Oestrogen receptor beta-immunoreactive neurones in the ovine hypothalamus: distribution and colocalization with gonadotropin-releasing hormone. J Neuroendocrinol 17:29-39
55. Roy D, Angelini NL, Belsham DD 1999 Estrogen directly represses gonadotropin-releasing hormone (GnRH) gene expression in estrogen receptor-α (ERα)- and ERβ-expressing GT1-7 GnRH neurons. Endocrinology 140:5045-5053
56. Navarro CE, Saeed SA, Murdock C, Martinez-Fuentes AJ, Arora KK, Krsmanovic LZ, Catt KJ 2003 Regulation of cyclic adenosine 3′,5′- monophosphate signaling and pulsatile neurosecretion by Gi-coupled plasma membrane estrogen receptors in immortalized gonadotropin-releasing hormone neurons. Mol Endocrinol 17:1792-1804
57. Norfleet AM, Clarke CH, Gametchu B, Watson CS 2000 Antibodies to the estrogen receptor-α modulate rapid prolactin release from rat pituitary tumor cells through plasma membrane estrogen receptors. FASEB J 14:157-165
58. Marquez DC, Pietras RJ 2001 Membrane-associated binding sites for estrogen contribute to growth regulation of human breast cancer cells. Oncogene 20:5420-5430
59. Razandi M, Pedram A, Greene GL, Levin ER 1999 Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERα and ERβ expressed in Chinese hamster ovary cells. Mol Endocrinol 13:307-319
60. Abraham IM, Todman MG, Korach KS, Herbison AE 2005 Critical in vivo roles for classical estrogen receptors in rapid estrogen actions on intracellular signaling in mouse brain. Endocrinology 145:3055-3061
61. Qiu J, Bosch MA, Tobias SC, Grandy DK, Scanlan TS, Ronnekleiv OK, Kelly MJ 2003 Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J Neurosci 23:9529-9540
62. Knobil E 1981 Patterns of hypophysiotropic signals and gonadotropin secretion in the rhesus monkey. Biol Reprod 24:44-49