Estrogen and ovariectomy regulate mRNA and protein of glutamic acid decarboxylases and cation-chloride cotransporters in the adult rat hippocampus

Neuroendocrinology

Volumn 80, Issue 5, 2004, Pages 308-323

  Nakamura, Nozomu H ^a   Rosell, Daniel R ^a   Akama, Keith T ^a   McEwen, Bruce S ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Glutamate decarboxylases; Gonadal steroids; Gonadectomy; Hippocampus; Immunocytochemistry; Ion transporters

Indexed keywords

CHLORIDE; COTRANSPORTER; ESTRADIOL; ESTROGEN; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; MESSENGER RNA; PROTEIN; ISOENZYME; POTASSIUM CHLORIDE SYMPORTERS; POTASSIUM-CHLORIDE SYMPORTERS; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1 PROTEIN; SODIUM-POTASSIUM-CHLORIDE COTRANSPORTER 1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; ANIMAL; BLOOD; COMPARATIVE STUDY; DRUG EFFECT; GENETICS; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; ESTRADIOL; FEMALE; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ISOENZYMES; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SYMPORTERS; TIME FACTORS;

EID: 15544364376     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000083657     Document Type: Article

References (89)

1. Woolley CS: Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 1998;34:140-148.
2. Segal M, Murphy D: Estradiol induces formation of dendritic spines in hippocampal neurons: Functional correlates. Horm Behav 2001;40:156-159.
3. Terasawa E, Timiras PS: Electrical activity during the estrous cycle of the rat: Cyclic changes in limbic structures. Endocrinology 1968;83:207-216.
4. Sandstrom NJ, Williams CL: Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 2001;115:384-393.
5. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan LP, Alves SE: Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 2001;429:355-371.
6. McEwen BS, Akama K, Alves S, Brake WG, Bulloch K, Lee S, Li C, Yuen G, Milner TA: Tracking the estrogen receptor in neurons: Implications for estrogen-induced synapse formation. Proc Natl Acad Sci USA 2001;98:7093-7100.
7. McEwen BS: Invited review: Estrogens effects on the brain: Multiple sites and molecular mechanisms. J Appl Physiol 2001;91:2785-2801.
8. Freund TF, Buzsaki G: Interneurons of the hippocampus. Hippocampus 1996;6:347-470.
9. Weiland NG, Orikasa C, Hayashi S, McEwen BS: Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J Comp Neurol 1997;388:603-612.
10. Loy R, Gerlach JL, McEwen BS: Autoradiographic localization of estradiol-binding neurons in the rat hippocampal formation and entorhinal cortex. Brain Res 1988;467:245-251.
11. Shughrue PJ, Merchenthaler I: Evidence for novel estrogen binding sites in the rat hippocampus. Neuroscience 2000;99:605-612.
12. Shughrue PJ, Merchenthaler I: Distribution of estrogen receptor beta immunoreactivity in the rat central nervous system. J Comp Neurol 2001;436:64-81.
13. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE: Immunolocalization of estrogen receptor beta in the mouse brain: Comparison with estrogen receptor alpha. Endocrinology 2003;144:2055-2067.
14. Murphy DD, Cole NB, Greenberger V, Segal M: Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. J Neurosci 1998;18:2550-2559.
15. Rudick CN, Woolley CS: Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat. J Neurosci 2001;21:6532-6543.
16. Paulsen O, Moser EI: A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity. Trends Neurosci 1998;21:273-278.
17. Weiland NG: Glutamic acid decarboxylase messenger ribonucleic acid is regulated by estradiol and progesterone in the hippocampus. Endocrinology 1992;131:2697-2702.
18. A receptors in the dorsal hippocampus by estradiol and progesterone. Brain Res 1989;487:178-83.
19. 3H]muscimol binding in hippocampus, hypothalamus and midbrain in rats. J Neuroendocrinol 1992;4:393-399.
20. Rudick CN, Woolley CS: Selective estrogen receptor modulators regulate phasic activation of hippocampal CAl pyramidal cells by estrogen. Endocrinology 2003;144:179-187.
21. Ben-Ari Y: Excitatory actions of GABA during development: The nature of the nurture. Nat Rev Neurosci 2002;3:728-739.
22. Owens DF, Kriegstein AR: Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 2002;3:715-727.
23. Vardi N, Zhang LL, Payne JA, Sterling P: Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. J Neurosci 2000;20:7657-7663.
24. A receptor-mediated responses in pyramidal cells of rat hippocampus. J Neurophysiol 1993;69:1541-1555.
25. A receptors. Science 1995;269:977-981.
26. + transient. J Neurosci 1997;17:7662-7672.
27. A receptors in rat CA1 pyramidal neurons. J Neurophysiol 1997;77:2213-2218.
28. - accumulation responsible for depolarizing GABAergic responses in mature hippocampal neurons. J Neurophysiol 2003;90:2752-2756.
29. Gulledge AT, Stuart GJ: Excitatory actions of GABA in the cortex. Neuron 2003;37:299-309.
30. Chavas J, Marty A: Coexistence of excitatory and inhibitory GABA synapses in the cerebellar interneuron network. J Neurosci 2003;23:2019-2031.
31. Stein V, Nicoll RA: GABA generates excitement. Neuron 2003;37:375-378.
32. Payne JA, Rivera C, Voipio J, Kaila K: Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 2003;26:199-206.
33. Nakamura N, Fujita H, Kawata M: Effects of gonadectomy on immunoreactivity for choline acetyltransferase in the cortex, hippocampus, and basal forebrain of adult male rats. Neuroscience 2002;109:473-485.
34. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR: Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 1994;14:1834-1855.
35. Sloviter RS, Dichter MA, Rachinsky TL, Dean E, Goodman JH, Sollas AL, Martin DL: Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J Comp Neurol 1996;373:593-618.
36. Moffatt CA, Rissman EF, Shupnik MA, Blaustein JD: Induction of progestin receptors by estradiol in the forebrain of estrogen receptor-alpha gene-disrupted mice. J Neurosci 1998;18:9556-9563.
37. Schreihofer DA, Resnick EM, Soh AY, Shupnik MA: Transcriptional regulation by a naturally occurring truncated rat estrogen receptor (ER), truncated ER product-1 (TERP-1). Mol Endocrinol 1999;13:320-329.
38. Solum DT, Handa RJ: Localization of estrogen receptor alpha (ER alpha) in pyramidal neurons of the developing rat hippocampus. Dev Brain Res 2001;128:165-175.
39. Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates, ed 4. San Diego, Academic Press, 1998.
40. Guillery RW, Herrup K: Quantification without pontification: Choosing a method for counting objects in sectioned tissues. J Comp Neurol 1997;386:2-7.
41. Mufson EJ, Cai WJ, Jaffar S, Chen E, Stebbins G, Sendera T, Kordower JH: Estrogen receptor immunoreactivity within subregions of the rat forebrain: Neuronal distribution and association with perikarya containing choline acetyltransferase. Brain Res 1999;849:253-274.
42. Woolley CS, Wenzel HJ, Schwartzkroin PA: Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region of the adult female rat. J Comp Neurol 1996;373:108-117.
43. Yankova M, Hart SA, Woolley CS: Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: A serial electron-microscopic study. Proc Natl Acad Sci USA 2001;98:3525-3530
44. Gould E, Woolley CS, Frankfurt M, McEwen BS: Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 1990;10:1286-1291.
45. Woolley CS, McEwen BS: Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 1993;336:293-306.
46. Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA: Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: Correlation with dendritic spine density. J Neurosci 1997;17:1848-1859.
47. Daniel JM, Dohanich GP: Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 2001;21:6949-6956.
48. Rudick CN, Woolley CS: Estradiol induces a phasic Fos response in the hippocampal CA1 and CA3 regions of adult female rats. Hippocampus 2000;10:274-283.
49. Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ: Two genes encode distinct glutamate decarboxylases. Neuron 1991;7:91-100.
50. - cotransporter expression in rat neocortex. Brain Res Dev Brain Res 1998;109:281-292.
51. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999;397:251-255.
52. Reagan LP, McKittrick CR, McEwen BS: Corticosterone and phenytoin reduce neuronal nitric oxide synthase messenger RNA expression in rat hippocampus. Neuroscience 1999;91:211-219.
53. Rosell DR, Nacher J, Akama KT, McEwen BS: Spatiotemporal distribution of gp 130 cytokines and their receptors after status epilepticus: Comparison with neuronal degeneration and microglial activation. Neuroscience 2003;122:329-348.
54. Du F, Eid T, Lothman EW, Kohler C, Schwarcz R: Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J Neurosci 1995;15:6301-6313.
55. Lucas LR, Angulo JA, Le Moal M, McEwen BS, Piazza P: Neurochemical characterization of individual vulnerability to addictive drugs in rats. Eur J Neurosci 1998;10:3153-3163.
56. Feldblum S, Erlander MG, Tobin AJ: Different distributions of GAD65 and GAD67 mRNAs suggest that the two glutamate decarboxylases play distinctive functional roles. J Neurosci Res 1993;34:689-706.
57. Houser CR, Esclapez M: Localization of mRNAs encoding two forms of glutamic acid decarboxylase in the rat hippocampal formation. Hippocampus 1994;4:530-545.
58. Stone DJ, Walsh J, Benes FM: Localization of cells preferentially expressing GAD(67) with negligible GAD(65) transcripts in the rat hippocampus: A double in situ hybridization study. Mol Brain Res 1999;71:201-209.
59. Kanaka C, Ohno K, Okabe A, Kuriyama K, Itoh T, Fukuda A, Sato K: The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1,2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 2001;104:933-946.
60. Wang C, Shimizu-Okabe C, Watanabe K, Okabe A, Matsuzaki H, Ogawa T, Mori N, Fukuda A, Sato K: Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res Dev Brain Res 2002;139:59-66.
61. Soghomonian JJ, Martin DL: Two isoforms of glutamate decarboxylase: Why? Trends Pharmacol Sci 1998;19:500-505.
62. Martin DL, Tobin AJ: Mechanisms controlling GABA synthesis and degradation in the brain; in Martin DL, Olsen RW (eds): GABA in the Nervous System: The View at Fifty Years. Philadelphia, Lippincott, Williams & Wilkins, 2000, pp 25-41.
63. - regulation. J Neurophysiol 1999;81:1939-1948.
64. Delpire E: Cation-chloride cotransporters in neuronal communication. News Physiol Sci 2000;15:309-312.
65. A receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosci 2000;20:7531-7538.
66. - cotransporter BSC2 in the nervous system. Am J Physiol 1997;272:C173-183.
67. - cotransporter in rat brain during development and its localization in mature astrocytes. Brain Res 2001;911:43-55.
68. - cotransporter expression and inhibitory synaptogenesis in the rat hippocampus: An immunocytochemical analysis. Eur J Neurosci 2002;15:233-245.
69. - in rat hippocampal neurons. Neurosci Lett 1992;143:135-138.
70. Nusser Z, Sieghart W, Benke D, Fritschy JM, Somogyi P: Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA 1996;93:11939-11944.
71. A receptor subunit mRNAsin the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 1992;12:1040-1062.
72. A receptor are regulated by progesterone in subfields of the hippocampus. Mol Brain Res 1995;32:271-278.
73. McCarthy MM, Kaufman LC, Brooks PJ, Pfaff DW, Schwartz-Giblin S: Estrogen modulation of mRNA levels for the two forms of glutamic acid decarboxylase (GAD) in female rat brain. J Comp Neurol 1995;360:685-697.
74. Curran-Rauhut MA, Petersen SL: Regulation of glutamic acid decarboxylase 65 and 67 gene expression by ovarian steroids: Identification of two functionally distinct populations of GABA neurones in the preoptic area. J Neuroendocrinol 2002;14:310-317.
75. Asada H, Kawamura Y, Maruyama K, Kume H, Ding R, Ji FY, Kanbara N, Kuzume H, Sanbo M, Yagi T, Obata K: Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures. Biochem Biophys Res Commun 1996;229:891-895.
76. Asada H, Kawamura Y, Maruyama K, Kume H, Ding RG, Kanbara N, Kuzume H, Sanbo M, Yagi T, Obata K: Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 1997;94:6496-6499.
77. 2) and 2,3,7,8,- tetrachlorodibenzo-p-dioxin (TCDD). Abstr Soc Neurosci 2002;863:3.
78. Russell JM: Sodium-potassium-chloride cotransport. Physiol Rev 2000;80:211-276.
79. Wang H, Yan Y, Kintner DB, Lytle C, Sun D: GABA-mediated trophic effect on oligodendrocytes requires Na-K-2Cl cotransport activity. J Neurophysiol 2003;90:1257-1265.
80. B receptors in the rat central nervous system. J Comp Neurol 1999;405:299-321.
81. 1) receptors in the rat hippocampus by immunocytochemistry and high resolution autoradiography, with specific reference to its localization in identified hippocampal intemeuron subpopulations. Neuropharmacology 1999;38:1707-1721.
82. B inhibition in the dentate gyms of female rats after kainic acid-induced status epilepticus. Epilepsia 2002;43S5:146-151.
83. Mobbs CV, Gee DM, Finch CE: Reproductive senescence in female C57BL/6J mice: Ovarian impairments and neuroendocrine impairments that are partially reversible and delayable by ovariectomy. Endocrinology 1984;115:1653-1662.
84. Adams MM, Oung T, Morrison JH, Gore AC: Length of postovariectomy interval and age. but not estrogen replacement, regulate N-methyl-D-aspartate receptor mRNA levels in the hippocampus of female rats. Exp Neurol 2001;170:345-356.
85. Gee DM, Flurkey K, Mobbs CV, Sinha YN, Finch CE: The regulation of luteinizing hormone and prolactin in C57BL/6J mice: Effects of estradiol implant size, duration of ovariectomy, and aging. Endocrinology 1984;114:685-693.
86. Yuri K, Kawata M: Estrogen receptor-immunoreactive neurons contain calcitonin gene-related peptide, methionine-enkephalin or tyrosine hydroxylase in the female rat preoptic area. Neurosci Res 1994;21:135-141.
87. Funabashi T, Kleopoulos SP, Brooks PJ, Kimura F, Pfaff DW, Shinohara K, Mobbs CV: Changes in estrogenic regulation of estrogen receptor alpha mRNA and progesterone receptor mRNA in the female rat hypothalamus during aging: An in situ hybridization study. Neurosci Res 2000;38:85-92.
88. Caba M, Beyer C, Gonzalez-Mariscal G, Morrell JI: Immunocytochemical detection of estrogen receptor-alpha in the female rabbit forebrain: topography and regulation by estradiol. Neuroendocrinology 2003;77:208-222.
89. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, Milner TA, McEwen BS, Morrison JH: Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci 2002;22:3608-3614.