Rapid action of oestrogen in luteinising hormone-releasing hormone neurones: The role of GPR30

Journal of Neuroendocrinology

Volumn 21, Issue 4, 2009, Pages 316-321

  Terasawa, Ei ^a,b   Noel, S D ^a   Keen, K L ^a  

^a UNIVERSITY OF WISCONSIN   (United States)

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

Author keywords

GnRH neurones; GPCR; GPR30; Primates; Rapid action of oestrogen

Indexed keywords

CALCIUM ION; DENDRIMER; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR BETA; FULVESTRANT; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 30; GONADORELIN; PERTUSSIS TOXIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONFERENCE PAPER; GENETIC TRANSFECTION; GONADORELIN RELEASE; HORMONE ACTION; HUMAN; NERVE CELL; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR INTRINSIC ACTIVITY; SIGNAL TRANSDUCTION; SPIKE;

ACTION POTENTIALS; ANIMALS; CALCIUM; CELL MEMBRANE; ESTRADIOL; ESTROGEN RECEPTOR BETA; ESTROGENS; LUTEINIZING HORMONE; NEURONS; PERIODICITY; RECEPTORS, G-PROTEIN-COUPLED; TIME FACTORS;

EID: 63749118192     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2009.01839.x     Document Type: Conference Paper

References (53)

1. Herbison AE. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr Rev 1998; 19: 302-330.
2. Terasawa E. Luteinizing hormone-releasing hormone (LHRH) neurons: mechanism of pulsatile LHRH release. Vitam Horm 2001; 63: 91-129.
3. Shivers BD, Harlan RE, Morrell JI, Pfaff DW. Absence of oestradiol concentration in cell nuclei of LHRH-immunoreactive neurones. Nature 1983; 304: 345-347.
4. Lehman MN, Karsch FJ. Do gonadotropin-releasing hormone, tyrosine hydroxylase, and beta-endorphin-immunoreactive neurons contain estrogen receptors? A double-label immunocytochemical study in the Suffolk ewe. Endocrinology 1993; 133: 887-895.
5. Herbison AE, Horvath TL, Naftolin F, Leranth C. Distribution of estrogen receptor-immunoreactive cells in monkey hypothalamus: Relationship to neurones containing luteinizing hormone-releasing hormone and tyrosine hydroxylase. Neuroendocrinology 1995; 61: 1-10.
6. Terasawa E, Fernandez DL. Neurobiological mechanisms of the onset of puberty in primates. Endocr Rev 2001; 22: 111-151.
7. Abrahám IM, Han SK, Todman MG, Korach KS, Herbison AE. Estrogen receptor beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo. J Neurosci 2003; 23: 5771-5777.
8. 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.
9. Abe H, Terasawa E. Firing pattern and rapid modulation of activity by estrogen in primate luteinizing hormone releasing hormone-1 neurons. Endocrinology 2005; 146: 4312-4320.
10. Herbison AE, Pape JR. New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front Neuroendocrinol 2002; 22: 292-308.
11. Sharifi N, Reuss AE, Wray S. Prenatal LHRH neurons in nasal explant cultures express estrogen receptor beta transcript. Endocrinology 2002; 143: 2503-2507.
12. Hrabovszky E, KallóI, Szlávik N, Keller E, Merchenthaler I, Liposits Z. Gonadotropin-releasing hormone neurons express estrogen receptor-beta. J Clin Endocrinol Metab 2007; 92: 2827-2830.
13. Skinner DC, Dufourny L. Oestrogen receptor beta-immunoreactive neurones in the ovine hypothalamus: Distribution and colocalization with gonadotropin-releasing hormone. J Neuroendocrinol 2005; 17: 29-39.
14. Hu L, Gustofson RL, Feng H, Leung PK, Mores N, Krsmanovic LZ, Catt KJ. Converse regulatory functions of estrogen receptor-alpha and -beta subtypes expressed in hypothalamic gonadotropin-releasing hormone neurons. Mol Endocrinol 2008; 22: 2250-2259.
15. Butler JA, Sjöberg M, Coen CW. Evidence for oestrogen receptor alpha-immunoreactivity in gonadotrophin-releasing hormone-expressing neurones. J Neuroendocrinol 1999; 11: 331-335.
16. Hrabovszky E, Shughrue PJ, Merchenthaler I, Hajszan T, Carpenter CD, Liposits Z, Petersen SL. Detection of estrogen receptor-beta messenger ribonucleic acid and 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2000; 141: 3506-3509.
17. Hrabovszky E, Steinhauser A, Barabas K, Shughrue PJ, Petersen SL, Merchenthaler I, Liposits Z. Estrogen receptor-beta immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2001; 142: 3261-3264.
18. Micevych PE, Chaban V, Ogi J, Dewing P, Lu JK, Sinchak K. Estradiol stimulates progesterone synthesis in hypothalamic astrocyte cultures. Endocrinology 2007; 148: 782-789.
19. Abe H, Keen KL, Terasawa E. Rapid action of estrogens on intracellular calcium oscillations in primate luteinizing hormone-releasing hormone-1 neurons. Endocrinology 2008; 149: 1155-1162.
20. Terasawa E, Quanbeck CD, Schulz CA, Burich AJ, Luchansky LL, Claude P. A primary cell culture system of luteinizing hormone releasing hormone neurons derived from embryonic olfactory placode in the rhesus monkey. Endocrinology 1993; 133: 2379-2390.
21. Terasawa E, Schanhofer WK, Keen KL, Luchansky L. Intracellular Ca(2+) oscillations in luteinizing hormone-releasing hormone neurons derived from the embryonic olfactory placode of the rhesus monkey. J Neurosci 1999; 19: 5898-5909.
22. Terasawa E, Keen KL, Mogi K, Claude P. Pulsatile release of luteinizing hormone-releasing hormone (LHRH) in cultured LHRH neurons derived from the embryonic olfactory placode of the rhesus monkey. Endocrinology 1999; 140: 1432-1441.
23. Gearing M, Terasawa E. Luteinizing hormone releasing hormone (LHRH) neuroterminals mapped using the push-pull perfusion method in the rhesus monkey. Brain Res Bull 1988; 21: 117-121.
24. 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.
25. Noel SD, Keen KL, Baumann DI, Filardo EJ, Terasawa E. Involvement of G-protein coupled receptor 30 (GPR30) in rapid action of estrogen in primate LHRH neurons. Mol Endocrinol 2009; 23: 349-359.
26. Filardo EJ, Quinn JA, Bland KI, Frackelton AR Jr. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol 2000; 14: 1649-1660.
27. Carmeci C, Thompson DA, Ring HZ, Francke U, Weigel RJ. Identification of a gene (GPR30) with homology to the G-protein-coupled receptor superfamily associated with estrogen receptor expression in breast cancer. Genomics 1997; 45: 607-617.
28. Filardo EJ, Quinn JA, Frackelton AR Jr, Bland KI. Estrogen action via the G protein-coupled receptor, GPR30: Stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol 2002; 16: 70-84.
29. Maggiolini M, Vivacqua A, Fasanella G, Recchia AG, Sisci D, Pezzi V, Montanaro D, Musti AM, Picard D, Andò S. The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17beta-estradiol and phytoestrogens in breast cancer cells. J Biol Chem 2004; 279: 27008-27016.
30. Bologa CG, Revankar CM, Young SM, Edwards BS, Arterburn JB, Kiselyov AS, Parker MA, Tkachenko SE, Savchuck NP, Sklar LA, Oprea TI, Prossnitz ER. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat Chem Biol 2006; 2: 207-212.
31. RomanòN, Lee K, Abrahám 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.
32. Toran-Allerand CD, Guan X, MacLusky NJ, Horvath TL, Diano S, Singh M, Connolly ES Jr, Nethrapalli IS, Tinnikov AA. ER-X: A novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J Neurosci 2002; 22: 8391-8401.
33. Boulware MI, Weick JP, Becklund BR, Kuo SP, Groth RD, Mermelstein PG. Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J Neurosci 2005; 25: 5066-5078.
34. Boulware MI, Kordasiewicz H, Mermelstein PG. Caveolin proteins are essential for distinct effects of membrane estrogen receptors in neurons. J Neurosci 2007; 27: 9941-9950.
35. Luoma JI, Boulware MI, Mermelstein PG. Caveolin proteins and estrogen signaling in the brain. Mol Cell Endocrinol 2008; 290: 8-13.
36. Dewing P, Boulware MI, Sinchak K, Christensen A, Mermelstein PG, Micevych P. Membrane estrogen receptor-alpha interactions with metabotropic glutamate receptor 1a modulate female sexual receptivity in rats. J Neurosci 2007; 27: 9294-9300.
37. Kelly MJ, Rønnekleiv OK. Membrane-initiated estrogen signaling in hypothalamic neurons. Mol Cell Endocrinol 2008; 290: 14-23.
38. Qiu J, Bosch MA, Tobias SC, Grandy DK, Scanlan TS, Ronnekleiv 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.
39. Qiu J, Bosch MA, Tobias SC, Krust A, Graham SM, Murphy SJ, 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.
40. 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.
41. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 2005; 307: 1625-1630.
42. Filardo E, Quinn J, Pang Y, Graeber C, Shaw S, Dong J, Thomas P. Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane. Endocrinology 2007; 148: 3236-3245.
43. Claing A, Laporte SA, Caron MG, Lefkowitz RJ. Endocytosis of G protein-coupled receptors: Roles of G protein-coupled receptor kinases and beta-arrestin proteins. Prog Neurobiol 2002; 66: 61-79.
44. Funakoshi T, Yanai A, Shinoda K, Kawano MM, Mizukami Y. G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun 2006; 346: 904-910.
45. Brailoiu E, Dun SL, Brailoiu GC, Mizuo K, Sklar LA, Oprea TI, Prossnitz ER, Dun NJ. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J Endocrinol 2007; 193: 311-321.
46. Matsuda K, Sakamoto H, Mori H, Hosokawa K, Kawamura A, Itose M, Nishi M, Prossnitz ER, Kawata M. Expression and intracellular distribution of the G protein-coupled receptor 30 in rat hippocampal formation. Neurosci Lett 2008; 441: 94-99.
47. Chongthammakun S, Terasawa E. Negative feedback effects of estrogen on luteinizing hormone-releasing hormone release occur in pubertal, but not prepubertal, ovariectomized female rhesus monkeys. Endocrinology 1993; 132: 735-743.
48. Mizuno M, Terasawa E. Search for neural substrates mediating inhibitory effects of oestrogen on pulsatile luteinising hormone-releasing hormone release in vivo in ovariectomized female rhesus monkeys (Macaca mulatta). J Neuroendocrinol 2005; 17: 238-245.
49. Knobil E. The neuroendocrine control of the menstrual cycle. Recent Prog Horm Res 1980; 36: 53-88.
50. Herbison AE. Physiology of the GnRH neuronal network. In: Neill JD, ed. Knobil and Neill's Physiology of Reproduction. San Diego, CA: Academic Press/Elsevier, 2006: 1415-1482.
51. 2+ oscillations among primate LHRH neurons and nonneuronal cells in vitro. J Neurophysiol 2002; 88: 1559-1567.
52. Wintermantel TM, Campbell RE, Porteous R, Bock D, Gröne HJ, Todman MG, Korach KS, Greiner E, Pérez CA, Schütz G, Herbison AE. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 2006; 52: 271-280.
53. Glidewell-Kenney C, Hurley LA, Pfaff L, Weiss J, Levine JE, Jameson JL. Nonclassical estrogen receptor alpha signaling mediates negative feedback in the female mouse reproductive axis. Proc Natl Acad Sci USA 2007; 104: 8173-8177.