Bidirectional modulatory effect of 17β-estradiol on NMDA receptors via ERα and ERβ in the dentate gyrus of juvenile male rats

Neuropharmacology

Volumn 75, Issue , 2013, Pages 262-273

  Tanaka, Motoki ^a   Sokabe, Masahiro ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

17 Estradiol; Dentate gyrus; Estrogen receptor and ; NMDA receptor; Synaptic plasticity

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; LETROZOLE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; GRANULE CELL; HIPPOCAMPUS; HORMONE RESPONSE; JUVENILE ANIMAL; LONG TERM POTENTIATION; MALE; MEMBRANE POTENTIAL; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SYNAPSE;

17Β-ESTRADIOL; DENTATE GYRUS; ESTROGEN RECEPTOR Α AND Β; NMDA RECEPTOR; SYNAPTIC PLASTICITY;

ANIMALS; DENTATE GYRUS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GINSENOSIDES; MALE; NAD; PHENOLS; PIPERAZINES; PIPERIDINES; QUINOXALINES; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SAPOGENINS;

EID: 84883810962     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.07.029     Document Type: Article

References (60)

1. C. Aguirre, A. Jayaraman, C. Pike, and M. Baudry Progesterone inhibits estrogen-mediated neuroprotection against excitotoxicity by down-regulating estrogen receptor-β J. Neurochem. 115 2010 1277 1287
2. M. Arundine, and M. Tymianski Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity Cell Calcium 34 4-5 2003 325 337 (Pubitemid 37021228)
3. F. Bi, M. Foy, M. Thompson, and M. Baudry 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 (Pubitemid 30183349)
4. E. Brailoiu, S.L. Dun, G.C. Brailoiu, K. Mizuo, L.A. Sklar, T.I. Oprea, E.R. Prossnitz, and N.J. Dun Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system J. Endocrinol. 193 2007 311 321
5. C.K. Barha, G.L. Dalton, and L.A. Galea Low doses of 17alpha-estradiol and 17beta-estradiol facilitate, whereas higher doses of estrone and 17alpha- and 17beta-estradiol impair, contextual fear conditioning in adult female rats Neuropsychopharmacology 35 2010 547 559
6. L. Chen, Y. Miyamoto, K. Furuya, N. Mori, and M. Sokabe PREGS induces LTP in the hippocampal dentate gyrus of adult rats via the tyrosine phosphorylation of NR2B coupled to ERK/CREB signaling J. Neurophysiol. 98 2007 1538 1548 (Pubitemid 47435900)
7. T.C. Foster Role of estrogen receptor alpha and beta expression and signaling on cognitive function during aging Hippocampus 22 2012 656 669
8. M.R. Foy, J. Xu, X. Xie, R.D. Brinton, R.F. Thompson, and T.W. Berger 17ß-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation J. Neurophysiol. 81 1999 925 929 (Pubitemid 29264535)
9. M. Foy, M. Baudry, and R. Thompson Estrogen and hippocampal synaptic plasticity Neuron Glia Biol. 1 2004 327 338
10. S.M. Goebel, R.M. Alvestad, S.J. Coultrap, and M.D. Browning Tyrosine phosphorylation of the N-methyl-d-aspartate receptor is enhanced in synaptic membrane fractions of the adult rat hippocampus Brain Res. Mol. Brain Res. 142 2005 65 79 (Pubitemid 41654385)
11. S. Ge, C.H. Yang, K.S. Hsu, G.L. Ming, and H. Song A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain Neuron 54 2009 559 566 (Pubitemid 46756142)
12. J.M. Hall, and D.P. McDonnell The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens Endocrinology 140 1999 5566 5578 (Pubitemid 30645344)
13. E. Hanse, and B. Gustafsson Postsynaptic, but not presynaptic, activity controls the early time course of LTP in the dentate gyrus J. Neurosci. 12 1992 3226 3240
14. K. Hernández-Fonseca, L. Massieu, S. García de la Cadena, C. Guzmán, and I. Camacho-Arroyo Neuroprotective role of estradiol against neuronal death induced by glucose deprivation in cultured rat hippocampal neurons Neuroendocrinology 96 2012 41 50
15. S. Higo, Y. Hojo, H. Ishii, T. Kominami, K. Nakajima, D. Poirier, T. Kimoto, and S. Kawato Comparison of sex-steroid synthesis between neonatal and adult rat hippocampus Biochem. Biophys. Res. Commun. 385 2009 62 66
16. Y. Hojo, T.A. Hattori, T. Enami, A. Furukawa, K. Suzuki, H.T. Ishii, H. Mukai, J.H. Morrison, W.G. Janssen, S. Kominami, N. Harada, T. Kimoto, and S. Kawato Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons Proc. Natl. Acad. Sci. U. S. A. 101 2004 865 870 (Pubitemid 38121049)
17. Y. Hojo, G. Murakami, H. Mukai, S. Higo, Y. Hatanaka, M. Ogiue-Ikeda, H. Ishii, T. Kimoto, and S. Kawato Estrogen synthesis in the brain - role in synaptic plasticity and memory Mol. Cell. Endocrinol. 290 2008 31 43
18. G.Z. Huang, and C.S. Woolley Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism Neuron 74 2012 801 808
19. K. Ito, K.L. Skinkle, and T.P. Hicks Age-dependent, steroid-specific effects of oestrogen on long-term potentiation in rat hippocampal slices J. Physiol. 515 1999 209 220 (Pubitemid 29092633)
20. T. Ivanova, and C. Beyer Ontogenetic expression and sex differences of aromatase and estrogen receptor-alpha/beta mRNA in the mouse hippocampus Cell Tissue Res. 300 2000 231 237 (Pubitemid 30333176)
21. K.B. Jelks, R. Wylie, C.L. Floyd, A.K. McAllister, and P. Wise Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: critical role of estrogen receptor-alpha J. Neurosci. 27 2007 6903 6913 (Pubitemid 47015894)
22. T. Kimoto, T. Tsurugizawa, Y. Ohta, J. Makino, Ho Tamura, Y. Hojo, N. Takata, and S. Kawato Neurosteroid synthesis by cytochrome p450-containing systems localized in the rat brain hippocampal neurons: N-methyl-d-aspartate and calcium-dependent synthesis Endocrinology 142 2001 3578 3589 (Pubitemid 32681768)
23. T. Kimoto, H. Ishii, S. Higo, Y. Hojo, and S. Kawato Semicomprehensive analysis of the postnatal age-related changes in the mRNA expression of sex steroidogenic enzymes and sex steroid receptors in the male rat hippocampus Endocrinology 151 2010 5795 5806
24. G. Köhr, and P.H. Seeburg Subtype-specific regulation of recombinant NMDA receptor-channels by protein tyrosine kinases of the Src family J. Physiol. 492 1996 445 452 (Pubitemid 26137754)
25. G.G. Kuiper, B. Carlsson, K. Grandien, E. Enmark, J. Häggblad, S. Nilsson, and J.A. Gustafsson Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta Endocrinology 138 1997 863 870 (Pubitemid 27089735)
26. G. Lei, S. Xue, N. Chéry, Q. Liu, J. Xu, C.L. Kwan, Y.P. Fu, Y.M. Lu, M. Liu, K.W. Harder, and X.M. Yu Gain control of N-methyl-d-aspartate receptor activity by receptor-like protein tyrosine phosphatase alpha EMBO J. 21 2002 2977 2989 (Pubitemid 34670382)
27. Z. Li, R. Zhou, S. Cui, G. Xie, W. Cai, M. Sokabe, and L. Chen Dehydroepiandrosterone sulfate prevents ischemia-induced impairment of long-term potentiation in rat hippocampal CA1 by up-regulating tyrosine phosphorylation of NMDA receptor Neuropharmacology 51 2006 958 966 (Pubitemid 44528605)
28. M.K. Lindberg, S. Movérare, S. Skrtic, H. Gao, K. Dahlman-Wright, J.A. Gustafsson, and C. Ohlsson Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a "ying yang" relationship between ERalpha and ERbeta in mice Mol. Endocrinol. 17 2003 203 208 (Pubitemid 36187395)
29. Y.B. Liu, P.A. Lio, J.F. Pasternak, and B.L. Trommer Developmental changes in membrane properties and postsynaptic currents of granule cells in rat J. Neurophysiol. 76 1996 1074 1088 (Pubitemid 26284590)
30. F. Liu, M. Day, L.C. Muñiz, D. Bitran, R. Arias, R. Revilla-Sanchez, S. Grauer, G. Zhang, C. Kelley, V. Pulito, A. Sung, R.F. Mervis, R. Navarra, W.D. Hirst, P.H. Reinhart, K.L. Marquis, S.J. Moss, M.N. Pangalos, and N.J. Brandon Activation of estrogen receptor-β regulates hippocampal synaptic plasticity and improves memory Nat. Neurosci. 11 2008 334 343 (Pubitemid 351311804)
31. N.R. Miller, T. Jover, H.W. Cohen, R.S. Zukin, and A.M. Etgen Estrogen can act via estrogen receptor alpha and beta to protect hippocampal neurons against global ischemia-induced cell death Endocrinology 146 2005 3070 3079 (Pubitemid 41002816)
32. T.A. Milner, K. Ayoola, C.T. Drake, S.P. Herrick, N.E. Tabori, B.S. McEwen, S. Warrier, and S.E. Alves Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation J. Comp. Neurol. 491 2005 81 95 (Pubitemid 41263413)
33. A. Miñano, X. Xifró, V. Pérez, B. Barneda-Zahonero, C.A. Saura, and J. Rodríguez-Alvarez Estradiol facilitates neurite maintenance by a Src/Ras/ERK signalling pathway Mol. Cell. Neurosci. 39 2008 143 151
34. M. Morissette, M. Le Saux, and T. Di Paolo Effect of oestrogen receptor alpha and beta agonists on brain N-methyl-d-aspartate receptors J. Neuroendocrinol. 20 2008 1006 1014
35. H. Mukai, T. Tsurugizawa, G. Murakami, S. Kominami, H. Ishii, M. Ogiue-Ikeda, N. Takata, N. Tanabe, A. Furukawa, Y. Hojo, Y. Ooishi, J.H. Morrison, W.G. Janssen, J.A. Rose, P. Chambon, S. Kato, S. Izumi, T. Yamazaki, T. Kimoto, and S. Kawato Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons J. Neurochem. 100 2007 950 967 (Pubitemid 46213921)
36. D.D. Murphy, N.B. Cole, V. Greenberger, and M. Segal Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons J. Neurosci. 18 1998 2550 2559 (Pubitemid 28141802)
37. J. Nilsen, S. Chen, and R.D. Brinton Dual action of estrogen on glutamate-induced calcium signaling: mechanisms requiring interaction between estrogen receptors and Src/mitogen activated protein kinase pathway Brain Res. 930 2002 216 234 (Pubitemid 34195646)
38. C.M. Norris, E.M. Blalock, O. Thibault, L.D. Brewer, G.V. Clodfelter, N.M. Porter, and P.W. Landfield Electrophysiological mechanisms of delayed excitotoxicity: positive feedback loop between NMDA receptor current and depolarization-mediated glutamate release J. Neurophysiol. 96 2006 2488 2500 (Pubitemid 44785900)
39. Y. Ooishi, H. Mukai, Y. Hojo, G. Murakami, Y. Hasegawa, T. Shindo, J.H. Morrison, T. Kimoto, and S. Kawato Estradiol rapidly rescues synaptic transmission from corticosterone-induced suppression via synaptic/extranuclear steroid receptors in the hippocampus Cereb. Cortex 22 2012 926 936
40. 2+ transients in spines of CA1 pyramidal neurons from hippocampal slices J. Neurophysiol. 81 1999 1404 1411 (Pubitemid 29272456)
41. J. Prange-Kiel, L. Fester, L. Zhou, H. Lauke, J. Carrétero, and G.M. Rune Inhibition of hippocampal estrogen synthesis causes region-specific downregulation of synaptic protein expression in hippocampal neurons Hippocampus 16 2006 464 471 (Pubitemid 44712070)
42. M. Razandi, A. Pedram, G.L. Greene, and E.R. Levin Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells Mol. Endocrinol. 13 1999 307 319 (Pubitemid 29068005)
43. M.E. Rhodes, and C.A. Frye ERbeta-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks Neurobiol. Learn Mem. 85 2006 183 191 (Pubitemid 43247844)
44. G.M. Rune, U. Wehrenberg, J. Prange-Kiel, L. Zhou, G. Adelmann, and M. Frotscher Estrogen up-regulates estrogen receptor alpha and synaptophysin in slice cultures of rat hippocampus Neuroscience 113 2002 167 175 (Pubitemid 34786022)
45. E. Salińska, W. Danysz, and J.W. Łazarewicz The role of excitotoxicity in neurodegeneration Folia Neuropathol. 43 2005 322 339 (Pubitemid 43109290)
46. M.W. Salter, and L.V. Kalia Src kinases: a hub for NMDA receptor regulation Nat. Rev. Neurosci. 5 2004 317 328 (Pubitemid 38478658)
47. C.C. Smith, and L.L. McMahon Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors J. Neurosci. 26 2006 8517 8522 (Pubitemid 44316180)
48. R.X. Song, Z. Zhang, and R.J. Santen Estrogen rapid action via protein complex formation involving ERalpha and Src Trends Endocrinol. Metab. 16 2005 347 353 (Pubitemid 41338739)
49. I. Spigelman, L. Zhang, and P.L. Carlen Patch-clamp study of postnatal development of CA1 neurons in rat hippocampal slices: membrane J. Neurophysiol. 68 1992 55 69
50. S. Szymczak, K. Kalita, J. Jaworski, B. Mioduszewska, A. Savonenko, A. Markowska, I. Merchenthaler, and L. Kaczmarek Increased estrogen receptor beta expression correlates with decreased spine formation in the rat hippocampus Hippocampus 16 2006 453 463 (Pubitemid 44712069)
51. X.J. Tan, Y.B. Dai, W.F. Wu, H.J. Kim, R.P. Barros, T.I. Richardson, B.C. Yaden, M. Warner, D.L. McKinzie, V. Krishnan, and J.Å. Gustafsson Reduction of dendritic spines and elevation of GABAergic signaling in the brains of mice treated with an estrogen receptor β ligand Proc. Natl. Acad. Sci. U. S. A. 109 2012 1708 1712
52. M. Tanaka, and M. Sokabe Continuous de novo synthesis of neurosteroids is required for normal synaptic transmission and plasticity in the dentate gyrus of the rat hippocampus Neuropharmacology 62 2012 2373 2387
53. C.D. Toran-Allerand, X. Guan, N.J. MacLusky, T.L. Horvath, S. Diano, M. Singh, E.S. Connolly Jr., I.S. Nethrapalli, and A.A. Tinnikov ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury J. Neurosci. 22 2002 8391 8401 (Pubitemid 35387579)
54. L.C. Vedder, C.C. Smith, A.E. Flannigan, and L.L. McMahon Estradiol-induced increase in novel object recognition requires hippocampal NR2B-containing NMDA receptors Hippocampus 23 2013 108 115
55. B. Vissel, J.J. Krupp, S.F. Heinemann, and G.L. Westbrook A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux Nat. Neurosci. 4 2001 587 596 (Pubitemid 32507372)
56. Y.T. Wang, and M.W. Salter Regulation of NMDA receptors by tyrosine kinases and phosphatases Nature 369 1994 233 235 (Pubitemid 24154800)
57. J.K. Wide, K. Hanratty, J. Ting, and L.A. Galea High level estradiol impairs and low level estradiol facilitates non-spatial working memory Behav. Brain Res. 155 2004 45 53 (Pubitemid 39119965)
58. C.S. Woolley Acute effects of estrogen on neuronal physiology Annu. Rev. Pharmacol. Toxicol. 47 2007 657 680
59. X.M. Yu, R. Askalan, G.J. Keil 2nd, and M.W. Salter NMDA channel regulation by channel-associated protein tyrosine kinase Src Science 275 1997 674 678 (Pubitemid 27061336)
60. F. Zheng, M.B. Gingrich, S.F. Traynelis, and P.J. Conn Tyrosine kinase potentiates NMDA receptor currents by reducing tonic zinc inhibition Nat. Neurosci. 1 1998 185 191