Effects of 17β-estradiol on glutamate synaptic transmission and neuronal excitability in the rat medial vestibular nuclei

Neuroscience

Volumn 165, Issue 4, 2010, Pages 1100-1114

  Grassi, S ^a   Frondaroli, A ^a   Scarduzio, M ^a   Dutia, M B ^b   Dieni, C ^a   Pettorossi, V E ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b Centre for Integrative Physiology   (United Kingdom)

Author keywords

estrogenic steroids; glutamate release; neuron excitability; NMDA receptors; synaptic potentiation; vestibular neurons

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR; ESTRADIOL; GLUTAMATE RECEPTOR; GLUTAMIC ACID; GLYCINE RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; ESTROGEN; METABOTROPIC GLUTAMATE RECEPTOR TYPE 1;

ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN SLICE; BRAIN STEM; CONTROLLED STUDY; EVOKED BRAIN STEM RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; HORMONE ACTION; ION CONDUCTANCE; MALE; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL NOISE RATIO; SYNAPTIC TRANSMISSION; VESTIBULAR FUNCTION; VESTIBULAR NERVE; VESTIBULAR NUCLEUS; ACTION POTENTIAL; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; EVOKED RESPONSE; IN VITRO STUDY; METABOLISM; NERVE CELL; PHYSIOLOGY; SYNAPSE; WISTAR RAT;

ACTION POTENTIALS; ANIMALS; ESTRADIOL; ESTROGENS; EVOKED POTENTIALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; MALE; NEURONS; RATS; RATS, WISTAR; RECEPTORS, AMPA; RECEPTORS, GABA; RECEPTORS, GLUTAMATE; RECEPTORS, GLYCINE; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION; VESTIBULAR NERVE; VESTIBULAR NUCLEI;

EID: 74149085506     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.11.039     Document Type: Article

References (64)

1. Andrescu C.E., Milojkovic B.A., Haasdijk E.D., Kramer P., De Jong F.H., Krust A., De Zeeuw C.I., and De Jeu M.T. Estradiol improves cerebellar memory formation by activating estrogen receptor β. J Neurosci 27 (2007) 10832-10839
2. Babalian A., Vibert N., Assie G., Serafin M., Mühlethaler M., and Vidal P.P. Central vestibular networks in the guinea-pig: functional characterization in the isolated whole brain in vitro. Neuroscience 81 (1997) 405-426
3. Bagnall M.W., Stevens R.J., and du Lac S. Transgenic mouse lines subdivide medial vestibular nucleus neurons into discrete, neurochemically distinct populations. J Neurosci 27 (2007) 2318-2330
4. Balthazart J., and Ball G.F. Is brain estradiol a hormone or a neurotransmitter?. Trends Neurosci 29 (2006) 241-249
5. Bender V.A., Bender K.J., Brasier D.J., and Feldman D.E. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J Neurosci 26 (2006) 4166-4177
6. Bi R., Broutman G., Foy M.R., Thompson R.F., and Baudry M. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc Natl Acad Sci U S A 97 (2000) 3602-3607
7. Bi R., Foy M.R., Thompson R.F., and Baudry M. Effects of estrogen, age, and calpain on MAP kinase and NMDA receptors in female rat brain. Neurobiol Aging 24 (2003) 977-983
8. Brinton R.D., Proffitt P., Tran J., and Kahil M. 17β-estradiol increases the growth and survival of cultured cortical neurons. Neurochem Res 22 (1997) 1339-1351
9. + current in hippocampal pyramidal neurons. J Neurosci 23 (2003) 6338-6344
10. Capocchi G., Della Torre G., Grassi S., Pettorossi V.E., and Zampolini M. NMDA-mediated long term modulation of electrically evoked field potentials in the rat medial vestibular nuclei. Exp Brain Res 90 (1992) 546-550
11. Cordoba Montoya D.A., and Carrer H.F. Estrogen facilitates induction of long-term potentiation in the hippocampus of awake rats. Brain Res 778 (1997) 430-438
12. Corlew R., Wang Y., Ghermazien H., Erisir A., and Philpot B.D. Developmental switch in the contribution of presynaptic and postsynaptic NMDA receptors to long-term depression. J Neurosci 27 (2007) 9832-9845
13. Dominiquez R., Liu R., and Baudry M. 17-β-estradiol-mediated activation of extracellular-signal regulated kinase, phosphatidylinositol 3-kinase/protein kinase B-Akt and N-methyl-d-aspartate receptor phosphorylation in cortical synaptoneurosomes. J Neurochem 101 (2007) 232-240
14. Dutia M.B., Johnston A.R., and Mcqueen D.S. Tonic activity of rat medial vestibular nucleus neurones in vitro and its inhibition by GABA. Exp Brain Res 88 (1992) 466-472
15. Evrard H.C., Harada N., and Balthazart J. Immunocytochemical localization of aromatase in sensory and integrating nuclei of the hindbrain in Japanese quail (Coturnix japonica). J Comp Neurol 473 (2004) 194-212
16. Foy M.R., Xu J., Xie X., Brinton R.D., Thompson R.F., and Berger T.W. 17β-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol 81 (1999) 925-929
17. Foy M.R. 17β-estradiol: effects on CA1 hippocampal synaptic plasticity. Neurobiol Learn Mem 76 (2001) 239-252
18. Gallagher J.P., Phelan K.D., and Shinnick-Gallagher P. Modulation of excitatory transmission at the rat medila vestibular nucleus synapse. Ann N Y Acad Sci 656 (1992) 630-644
19. Gould E., Woolley C.S., Frankfurt M., and McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10 (1990) 1286-1291
20. Grassi S., Della Torre G., Capocchi G., Zampolini M., and Pettorossi V.E. The role of Gaba in NMDA-dependent long term depression (LTD) of rat medial vestibular nuclei. Brain Res 699 (1995) 183-191
21. Grassi S., Pettorossi V.E., and Zampolini M. Low frequency stimulation cancels the high frequency-induced long lasting effects in the rat medial vestibular nuclei. J Neurosci 16 (1996) 3373-3380
22. Grassi S., Francescangeli E., Goracci G., and Pettorossi V.E. Role of platelet-activating factor in long term potentiation of the rat medial vestibular nuclei. J Neurophysiol 79 (1998) 3266-3271
23. Grassi S., Francescangeli E., Goracci G., and Pettorossi V.E. Platelet-activating factor and group I metabotropic glutamate receptors interact for full development and maintenance of long-term potentiation in the rat medial vestibular nuclei. Neuroscience 94 (1999) 549-559
24. Grassi S., and Pettorossi V.E. Role of nitric oxide in long-term potentiation of the rat medial vestibular nuclei. Neuroscience 101 (2000) 157-164
25. Grassi S., and Pettorossi V.E. Synaptic plasticity in the medial vestibular nuclei: role of glutamate receptors and retrograde messengers in rat brainstem slices. Prog Neurobiol 64 (2001) 527-553
26. Grassi S., Frondaroli A., Dieni C., Dutia M.B., and Pettorossi V.E. Neurosteroid modulation of neuronal excitability and synaptic transmission in the rat medial vestibular nuclei. Eur J Neurosci 26 (2007) 23-32
27. Grassi S., Frondaroli A., Dieni C., and Scarduzio M. Effects of 17β-estradiol on synaptic plasticity in the rat medial vestibular nuclei. Acta Otolaryngol 129 (2009) 390-394
28. Grassi S., Frondaroli A., Dieni C., Scarduzio M., and Pettorossi V.E. Long-term potentiation in the rat medial vestibular nuclei depends on locally synthesised 17β-estradiol. J Neurosci 29 (2009) 10779-10783
29. Hojo Y., Hattori T.A., Enami T., Furukawa A., Suzuki K., Ishii H.T., Mukai H., Morrison J.H., Janssen W.G., Kominami S., Harada N., Kimoto T., and Kawato S. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P450 17alpha and P450 aromatase localized in neurons. Proc Natl Acad Sci U S A 101 (2004) 865-870
30. Hojo Y., Murakami G., Mukai H., Higo S., Hatanaka Y., Ikeda M.O., Ishii H., Kimoto T., and Kawato S. Estrogen synthesis in the brain. Role on synaptic plasticity and memory. Mol Cell Endocrinol 290 (2008) 31-43
31. Horvath T.L., and Wikler K.C. Aromatase in developing sensory system in the rat brain. J Neuroendocrinol 11 (1999) 77-84
32. Kelly M.J., Qiu J., Wagner E.J., and Rønnekleiv O.K. Rapid effects of estrogen on G protein-coupled receptor activation of potassium channels in the central nervous system (CNS). J Steroid Biochem Mol Biol 83 (2002) 187-193
33. Kimoto T., Tsurugizawa T., Ohta Y., Makino J., Tamura H., Hojo Y., Takata N., and Kawato S. Neurosteroid synthesis by citochrome p450-containing systems localized in the rat brain. Endocrinology 142 (2001) 3578-3589
34. Kinney G.A., Peterson B.W., and Slater N.T. The synaptic activation of N-methyl-D-aspartate receptors in the rat medial vestibular nucleus. J Neurophysiol 72 (1994) 1588-1595
35. Johnston A.R., MacLeod N.K., and Dutia M.B. Ionic conductances contributing to spike repolarization and after-potentials in rat medial vestibular nucleus neurones. J Physiol 481 (1994) 61-77
36. Li Z., and Hay M.J. 17-beta-estradiol modulation of area postrema potassium currents. J Neurophysiol 84 (2000) 1385-1391
37. Lin Y., and Carpenter D.O. Medial vestibular neurons are endogenous pacemakers whose discharge is modulated by neurotransmitters. Cell Mol Neurobiol 13 (1993) 601-613
38. McEwen B.S. Estrogen actions throughout the brain. Recent Prog Horm Res 57 (2002) 357-384
39. McEwen B.S., and Alves S.E. Estrogens action in the central nervous system. Endocr Rev 20 (1999) 279-307
40. Mermelstein P.G., Becker J.B., and Surmeier D.J. Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor. J Neurosci 16 (1996) 595-604
41. Mukai H., Takata N., Ishii H.T., Tanabe N., Hojo J., Furukawa A., Kimoto T., and Kawato S. Hippocampal synthesis of estrogens and androgens which are paracrine modulators of synaptic plasticity: synaptocrinology. Neuroscience 138 (2006) 757-764
42. Murphy D.D., and Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroidal hormones. J Neurosci 16 (1996) 4059-4068
43. Naftolin F., Ryan K.J., Davies I.J., Petro Z., and Kuhn M. The formation and metabolism of estrogens in brain tissues. Adv Biosci 15 (1975) 105-121
44. Neuhauser H.K. Epidemiology of vertigo. Curr Opin Neurol 20 (2007) 40-46
45. Nishimura I., Ui-Tei K., Saigo K., Ishii H., Sakuma Y., and Kato M. 17beta-estradiol at physiological concentrations augments Ca(2+) -activated K+ currents via estrogen receptor beta in the gonadotropin-releasing hormone neuronal cell line GT1-7. Endocrinology 149 (2008) 774-782
46. O'Brian C.A., Ioannides C.G., Ward N.E., and Liskamp R.M. Inhibition of protein kinase C and calmodulin by the geometric isomers cis- and trans-tamoxifen. Biopolymers 29 (1990) 97-104
47. Okada M., Ishihara K., Sasa M., Izumi R., Yajin K., and Harada Y. Enhancement of GABA-mediated inhibition of rat medial vestibular nucleus neurons by the neurosteroid 20-hydroxyecdysone. Acta Otolaryngol 118 (1998) 11-16
48. Pedram A., Razandi M., and Levi A.R. Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol 20 (2006) 1996-2009
49. Raz L., Khan M.M., Mahesh V.B., Vadlamudi R.K., and Brann D.W. Rapid estrogen signalling in the brain. Neurosignals 16 (2008) 140-153
50. Rudick C.N., and Wooley C.S. Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat. J Neurosci 21 (2001) 6532-6543
51. Rybak L.P. Metabolic disorders of the vestibular system. Otolaryngol Head Neck Surg 112 (1995) 128-132
52. Serafin M., de Waele C., Khateb A., Vidal P.P., and Mühlethaler M. Medial vestibular nucleus in the guinea-pig. I. Intrinsic membrane properties in brainstem slices. Exp Brain Res 84 (1991) 417-425
53. Serafin M., de Waele C., Khateb A., Vidal P.P., and Mühlethaler M. Medial vestibular nucleus in the guinea-pig. II. Ionic basis of the intrinsic membrane properties in brainstem slices. Exp Brain Res 84 (1991) 426-433
54. Simpson E.R., Mahendroo M.S., Means G.D., Kilgore M.W., Hinshelwood M.M., Graham-Lorence S., Amarneh B., Ito Y., Fisher C.R., and Michael M.D. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15 (1994) 342-355
55. Smith C.C., and McMahon L.L. Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio of NMDA transmission to AMPA transmission is increased. J Neurosci 25 (2005) 7780-7791
56. Smith C.C., and McMahon L.L. Estrogen-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci 26 (2006) 8517-8522
57. Smith M.R., Nelson A.B., and Du Lac S. Regulation of firing response gain by calcium-dependent mechanisms in vestibular nucleus neurons. J Neurophysiol 87 (2002) 2031-2042
58. Straka H., Vibert N., Vidal P.P., Moore L.E., and Dutia M.B. Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity. Prog Neurobiol 76 (2005) 349-392
59. Takazawa T., Saito Y., Tsuzuki K., and Ozawa S. Membrane and firing properties of glutamatergic and GABAergic neurons in the rat medial vestibular nucleus. J Neurophysiol 92 (2004) 3106-3120
60. Wong M., and Moss R.L. Electrophysiological evidence for a rapid membrane action of the gonadal steroid 17 beta-estradiol, on CA1 pyramidal neurons of the rat hippocampus. Brain Res 543 (1991) 148-152
61. Wong M., and Moss R.L. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J Neurosci 12 (1992) 3217-3225
62. Wong M., Thompson T.L., and Moss R.L. Nongenomic actions of estrogen in the brain: physiological significance and cellular mechanisms. Crit Rev Neurosci 10 (1996) 189-203
63. Yamamoto T., Yamanaka T., and Matsunga T. Effects of the neurosteroid dehydropiandrosterone sulphate on medial vestibular nucleus neurons. Acta Otolaryngol 118 (1998) 185-191
64. Yamamoto T., Yamanaka T., Miyahara H., and Matsunga T. The neurosteroid pregnenolone sulphate excites medial vestibular nucleus neurons. Acta Otolaryngol 533 Suppl (1998) 22-25