Glutamate regulation of GnRH neuron excitability

Brain Research

Volumn 1364, Issue , 2010, Pages 35-43

  Iremonger, Karl J ^a   Constantin, Stephanie ^a   Liu, Xinhuai ^a   Herbison, Allan E ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

AMPA; EPSC; Glutamate; GnRH; Kainate; LHRH; NMDA; Puberty

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; GLUTAMIC ACID; GONADORELIN; KAINIC ACID; KAINIC ACID RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; RECEPTOR SUBUNIT;

CALCIUM CURRENT; ELECTROPHYSIOLOGY; HUMAN; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; REGULATORY MECHANISM; REPRODUCTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; ELECTROPHYSIOLOGICAL PHENOMENA; ESTROUS CYCLE; FEMALE; GLUTAMIC ACID; GONADOTROPIN-RELEASING HORMONE; HUMANS; NEURONAL PLASTICITY; NEURONS; NEUROSECRETORY SYSTEMS; PUBERTY; RECEPTORS, IONOTROPIC GLUTAMATE;

EID: 78649524203     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.08.071     Document Type: Review

References (67)

1. R. Abbud, and M.S. Smith Do GnRH neurons express the gene for the NMDA receptor? Brain Res. 690 1995 117 120
2. M. Arslan, C.R. Pohl, and T.M. Plant dl-2-Amino-5-phosphonopentanoic acid, a specific N-methyl-d-aspartic acid receptor antagonist, suppresses pulsatile LH release in the rat Neuroendocrinology 47 1988 465 468
3. J.D. Bailey, A. Centers, and L. Jennes Expression of AMPA receptor subunits (GluR1-GluR4) in gonadotrophin-releasing hormone neurones of young and middle-aged persistently oestrous rats during the steroid-induced luteinising hormone surge J. Neuroendocrinol. 18 2006 1 12
4. F. Bordi, and A. Ugolini Group I metabotropic glutamate receptors: implications for brain diseases Prog. Neurobiol. 59 1999 55 79 (Pubitemid 29274422)
5. J.P. Bourguignon, A. Gerard, J. Mathieu, A. Mathieu, and P. Franchimont Maturation of the hypothalamic control of pulsatile gonadotropin-releasing hormone secretion at onset of puberty. I. Increased activation of N-methyl-d-aspartate receptors Endocrinology 127 1990 873 881 (Pubitemid 20248134)
6. J.N. Bourne, and K.M. Harris Balancing structure and function at hippocampal dendritic spines Annu. Rev. Neurosci. 31 2008 47 67
7. D.W. Brann, and V.B. Mahesh Endogenous excitatory amino acid involvement in the preovulatory and steroid-induced surge of gonadotropins in the female rat Endocrinology 128 1991 1541 1547
8. D.S. Bredt, and R.A. Nicoll AMPA receptor trafficking at excitatory synapses Neuron 40 2003 361 379 (Pubitemid 37244101)
9. R.E. Campbell, S.K. Han, and A.E. Herbison Biocytin filling of adult gonadotropin-releasing hormone neurons in situ reveals extensive, spiny, dendritic processes Endocrinology 146 2005 1163 1169
10. R.E. Campbell Defining the gonadotrophin-releasing hormone neuronal network: transgenic approaches to understanding neurocircuitry J. Neuroendocrinol. 19 2007 561 573
11. A.G. Carter, and W.G. Regehr Quantal events shape cerebellar interneuron firing Nat. Neurosci. 5 2002 1309 1318
12. W.P. Chen, J.W. Witkin, and A.J. Silverman Sexual dimorphism in the synaptic input to gonadotropin releasing hormone neurons Endocrinology 126 1990 695 702
13. C.A. Christian, and S.M. Moenter Estradiol induces diurnal shifts in GABA transmission to gonadotropin-releasing hormone neurons to provide a neural signal for ovulation J. Neurosci. 27 2007 1913 1921 (Pubitemid 46310307)
14. C.A. Christian, J. Pielecka-Fortuna, and S.M. Moenter Estradiol suppresses glutamatergic transmission to gonadotropin-releasing hormone neurons in a model of negative feedback in mice Biol. Reprod. 80 2009 1128 1135
15. Z. Chu, and S.M. Moenter Endogenous activation of metabotropic glutamate receptors modulates GABAergic transmission to gonadotropin-releasing hormone neurons and alters their firing rate: a possible local feedback circuit J. Neurosci. 25 2005 5740 5749 (Pubitemid 40847886)
16. J. Clarkson, and A.E. Herbison Development of GABA and glutamate signaling at the GnRH neuron in relation to puberty Mol. Cell. Endocrinol. 254-255 2006 32 38 (Pubitemid 44041748)
17. J. Clarkson, W.C. Boon, E.R. Simpson, and A.E. Herbison Postnatal development of an estradiol-kisspeptin positive feedback mechanism implicated in puberty onset Endocrinology 150 2009 3214 3220
18. J. Clarkson, S.K. Han, X. Liu, K. Lee, and A.E. Herbison Neurobiological mechanisms underlying kisspeptin activation of gonadotropin-releasing hormone (GnRH) neurons at puberty Mol. Cell. Endocrinol. 324 2010 45 50
19. H. Cline, and K. Haas The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis J. Physiol. 586 2008 1509 1517 (Pubitemid 351404956)
20. S. Constantin, C.L. Jasoni, B. Wadas, and A.E. Herbison Gamma-aminobutyric acid and glutamate differentially regulate intracellular calcium concentrations in mouse gonadotropin-releasing hormone neurons Endocrinology 151 2010 262 270
21. E.C. Cottrell, R.E. Campbell, S.K. Han, and A.E. Herbison Postnatal remodeling of dendritic structure and spine density in gonadotropin-releasing hormone neurons Endocrinology 147 2006 3652 3661
22. S.G. Cull-Candy, and D.N. Leszkiewicz Role of distinct NMDA receptor subtypes at central synapses Sci. STKE 255 2004 1 9
23. I. Dumalska, M. Wu, E. Morozova, R. Liu, A. van den Pol, and M. Alreja 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 2008 8003 8013
24. O. Eyigor, and L. Jennes Expression of glutamate receptor subunit mRNAs in gonadotropin-releasing hormone neurons during the sexual maturation of the female rat Neuroendocrinology 66 1997 122 129 (Pubitemid 27309838)
25. O. Eyigor, and L. Jennes Kainate receptor subunit-positive gonadotropin-releasing hormone neurons express c-Fos during the steroid-induced luteinizing hormone surge in the female rat Endocrinology 141 2000 779 786 (Pubitemid 32250503)
26. A.C. Gore, T.J. Wu, J.J. Rosenberg, and J.L. Roberts Gonadotropin- releasing hormone and NMDA receptor gene expression and colocalization change during puberty in female rats J. Neurosci. 16 1996 5281 5289
27. G.B. Gu, and R.B. Simerly Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat J. Comp. Neurol. 384 1997 142 164 (Pubitemid 27280229)
28. S.K. Han, M.L. Gottsch, K.J. Lee, S.M. Popa, J.T. Smith, S.K. Jakawich, D.K. Clifton, R.A. Steiner, and A.E. Herbison Activation of gonadotropin- releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty J. Neurosci. 25 2005 11349 11356
29. A.E. Herbison, Physiology of the GnRH neuronal network 2006 Academic Press San Diego
30. A.E. Herbison 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 2008 277 287
31. E. Hrabovszky, G.F. Turi, I. Kallo, and Z. Liposits Expression of vesicular glutamate transporter-2 in gonadotropin-releasing hormone neurons of the adult male rat Endocrinology 145 2004 4018 4021 (Pubitemid 39120545)
32. E. Hrabovszky, and Z. Liposits Novel aspects of glutamatergic signalling in the neuroendocrine system J. Neuroendocrinol. 20 2008 743 751 (Pubitemid 351858726)
33. D.E. Jane, D. Lodge, and G.L. Collingridge Kainate receptors: pharmacology, function and therapeutic potential Neuropharmacology 56 2009 90 113
34. S.I. Kawakami, K. Hirunagi, M. Ichikawa, H. Tsukamura, and K.I. Maeda Evidence for terminal regulation of GnRH release by excitatory amino acids in the median eminence in female rats: a dual immunoelectron microscopic study Endocrinology 139 1998 1458 1461 (Pubitemid 28510169)
35. J. Kiss, K. Kocsis, A. Csaki, and B. Halasz Evidence for vesicular glutamate transporter synapses onto gonadotropin-releasing hormone and other neurons in the rat medial preoptic area Eur. J. Neurosci. 18 2003 3267 3278 (Pubitemid 38031052)
36. M.C. Kuehl-Kovarik, W.A. Pouliot, G.L. Halterman, R.J. Handa, F.E. Dudek, and K.M. Partin 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 2002 2313 2322
37. K. Lee, R. Porteous, R.E. Campbell, B. Luscher, and A.E. Herbison Knockdown of GABAA receptor signaling in GnRH neurons has minimal effects upon fertility Endocrinology 151 2010 4428 4436
38. C. Leranth, L.M. Segura, M. Palkovits, N.J. MacLusky, M. Shanabrough, and F. Naftolin The LH-RH-containing neuronal network in the preoptic area of the rat: demonstration of LH-RH-containing nerve terminals in synaptic contact with LH-RH neurons Brain Res. 345 1985 332 336 (Pubitemid 16217084)
39. X. Liu, K. Lee, and A.E. Herbison Kisspeptin excites gonadotropin- releasing hormone neurons through a phospholipase C/calcium-dependent pathway regulating multiple ion channels Endocrinology 149 2008 4605 4614
40. F.J. Lopez, A.O. Donoso, and A. Negro-Vilar Endogenous excitatory amino acid neurotransmission regulates the estradiol-induced LH surge in ovariectomized rats Endocrinology 126 1990 1771 1773 (Pubitemid 20095791)
41. R.A. McKinney, M. Capogna, R. Durr, B.H. Gahwiler, and S.M. Thompson Miniature synaptic events maintain dendritic spines via AMPA receptor activation Nat. Neurosci. 2 1999 44 49 (Pubitemid 30488939)
42. B.H. Miller, and A.C. Gore N-methyl-d-aspartate receptor subunit expression in GnRH neurons changes during reproductive senescence in the female rat Endocrinology 143 2002 3568 3574 (Pubitemid 34925733)
43. J.G. Ondo, K.A. Pass, and R. Baldwin The effects of neurally active amino acids on pituitary gonadotropin secretion Neuroendocrinology 21 1976 79 87
44. E.N. Ottem, J.G. Godwin, and S.L. Petersen Glutamatergic signaling through the N-methyl-d-aspartate receptor directly activates medial subpopulations of luteinizing hormone-releasing hormone (LHRH) neurons, but does not appear to mediate the effects of estradiol on LHRH gene expression Endocrinology 143 2002 4837 4845
45. E.N. Ottem, J.G. Godwin, S. Krishnan, and S.L. Petersen Dual-phenotype GABA/glutamate neurons in adult preoptic area: sexual dimorphism and function J. Neurosci. 24 2004 8097 8105 (Pubitemid 39280830)
46. A.S. Parent, V. Matagne, M. Westphal, S. Heger, S. Ojeda, and H. Jung Gene expression profiling of hypothalamic hamartomas: a search for genes associated with central precocious puberty Horm. Res. 69 2008 114 123
47. J. Pielecka-Fortuna, and S.M. Moenter Kisspeptin increases gamma-aminobutyric acidergic and glutamatergic transmission directly to gonadotropin-releasing hormone neurons in an estradiol-dependent manner Endocrinology 151 2010 291 300
48. L. Ping, V.B. Mahesh, G.K. Bhat, and D.W. Brann Regulation of gonadotropin-releasing hormone and luteinizing hormone secretion by AMPA receptors. Evidence for a physiological role of AMPA receptors in the steroid-induced luteinizing hormone surge Neuroendocrinology 66 1997 246 253
49. T.M. Plant, V.L. Gay, G.R. Marshall, and M. Arslan Puberty in monkeys is triggered by chemical stimulation of the hypothalamus Proc. Natl Acad. Sci. USA 86 1989 2506 2510 (Pubitemid 19102537)
50. M.T. Price, J.W. Olney, and T.J. Cicero Acute elevations of serum luteinizing hormone induced by kainic acid, N-methyl aspartic acid or homocysteic acid Neuroendocrinology 26 1978 352 358
51. C.B. Roberts, P. Hemond, and K.J. Suter Synaptic integration in hypothalamic gonadotropin releasing hormone (GnRH) neurons Neuroscience 154 2008 1337 1351
52. D.D. Schoepp Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system J. Pharmacol. Exp. Ther. 299 2001 12 20 (Pubitemid 32905113)
53. A. Sergeeva, and H.T. Jansen Neuroanatomical plasticity in the gonadotropin-releasing hormone system of the ewe: seasonal variation in glutamatergic and gamma-aminobutyric acidergic afferents J. Comp. Neurol. 515 2009 615 628
54. D.R. Shimshek, T. Bus, V. Grinevich, F.N. Single, V. Mack, R. Sprengel, D.J. Spergel, and P.H. Seeburg Impaired reproductive behavior by lack of GluR-B containing AMPA receptors but not of NMDA receptors in hypothalamic and septal neurons Mol. Endocrinol. 20 2006 219 231 (Pubitemid 43011683)
55. A. Silverman, I. Livne, J.W. Witkin, The gonadotrophin-releasing hormone (GnRH), neuronal systems: immunocytochemistry and in situ hybridization 1994 Raven New York
56. S.X. Simonian, D.P. Spratt, and A.E. Herbison Identification and characterization of estrogen receptor alpha-containing neurons projecting to the vicinity of the gonadotropin-releasing hormone perikarya in the rostral preoptic area of the rat J. Comp. Neurol. 411 1999 346 358
57. S.X. Simonian, and A.E. Herbison Differing, spatially restricted roles of ionotropic glutamate receptors in regulating the migration of gnrh neurons during embryogenesis J. Neurosci. 21 2001 934 943
58. C. Smyth, and M. Wilkinson A critical period for glutamate receptor-mediated induction of precocious puberty in female rats J. Neuroendocrinol. 6 1994 275 284 (Pubitemid 24189865)
59. D.J. Spergel, U. Kruth, D.F. Hanley, R. Sprengel, and P.H. Seeburg GABA- and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice J. Neurosci. 19 1999 2037 2050 (Pubitemid 29133382)
60. N. Spruston, P. Jonas, and B. Sakmann Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons J. Physiol. 482 Pt 2 1995 325 352
61. K.J. Suter Control of firing by small (S)-alpha-amino-3-hydroxy-5-methyl- isoxazolepropionic acid-like inputs in hypothalamic gonadotropin releasing-hormone (GnRH) neurons Neuroscience 128 2004 443 450
62. M.A. Sutton, H.T. Ito, P. Cressy, C. Kempf, J.C. Woo, and E.M. Schuman Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis Cell 125 2006 785 799
63. H.F. Urbanski, and S.R. Ojeda A role for N-methyl-d-aspartate (NMDA) receptors in the control of LH secretion and initiation of female puberty Endocrinology 126 1990 1774 1776
64. A.N. van den Pol, J.P. Wuarin, and F.E. Dudek Glutamate, the dominant excitatory transmitter in neuroendocrine regulation Science 250 1990 1276 1278
65. T.M. Wintermantel, R.E. Campbell, R. Porteous, D. Bock, H.J. Grone, M.G. Todman, K.S. Korach, E. Greiner, C.A. Perez, G. Schutz, and A.E. Herbison Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility Neuron 52 2006 271 280 (Pubitemid 44548337)
66. S. Wray, and G. Hoffman Postnatal morphological changes in rat LHRH neurons correlated with sexual maturation Neuroendocrinology 43 1986 93 97 (Pubitemid 16073635)
67. W. Yin, J.M. Mendenhall, S.B. Bratton, T. Oung, W.G. Janssen, J.H. Morrison, and A.C. Gore Novel localization of NMDA receptors within neuroendocrine gonadotropin-releasing hormone terminals Exp. Biol. Med. (Maywood) 232 2007 662 673 (Pubitemid 46683392)