Estrogen receptor α and β mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone

Neuroscience

Volumn 134, Issue 3, 2005, Pages 847-856

  Isgor, C ^a   Watson, S J ^b  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Doublecortin; Hippocampus; Ki 67; Neurogenesis

Indexed keywords

DOUBLECORTIN; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; KI 67 ANTIGEN; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENTATE GYRUS; GENE EXPRESSION; IMMUNOREACTIVITY; MALE; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRIFORM CORTEX; RAT; TELENCEPHALON;

ANIMALS; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBRAL VENTRICLES; DENTATE GYRUS; DIAGNOSTIC IMAGING; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KI-67 ANTIGEN; MALE; MICROTUBULE-ASSOCIATED PROTEINS; NEUROPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 23644452513     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2005.05.008     Document Type: Article

References (79)

1. R.A. Adan, J.J. Cox, T.V. Beischlag, J.P. Burbach A composite hormone response element mediates the transactivation of the rat oxytocin gene by different classes of nuclear hormone receptors Mol Endocrinol 7 1993 47 57
2. J. Altman Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain with special reference to persisting neurogenesis in the olfactory bulb J Comp Neurol 137 1969 433 458
3. A.P. Arnold, R.A. Gorski Gonadal steroid induction of structural sex differences in the central nervous system Annu Rev Neurosci 7 1984 413 442
4. I. Azcoitia, A. Sierra, L.M. Garcia-Segura Estradiol prevents kainic acid-induced neuronal loss in the rat dentate gyrus Neuroreport 9 1998 3075 3079
5. I. Azcoitia, A. Sierra, L.M. Garcia-Segura Localization of estrogen receptor β-immunoreactivity in astrocytes of the adult rat brain Glia 26 1999 260 267
6. M. Banasr, M. Hery, J.M. Brezun, A. Daszuta Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus Eur J Neurosci 14 2001 1417 1424
7. C. Beyer Estrogen and the developing mammalian brain Anat Embryol 199 1999 379 390
8. K. Brännvall, L. Korhonen, D. Lindholm Estrogen-receptor-dependent regulation of neural stem cell proliferation and differentiation Mol Cell Neurosci 21 2002 512 520
9. A receptor subunit expression predicts functional changes in hippocampal dentate granule cells during postnatal development J Neurochem 77 2001 1266 1278
10. J.P. Brown, S. Couillard-Després, C.M. Cooper-Kuhn, J. Winkler, L. Aigner, H.G. Kuhn Transient expression of doublecortin during adult neurogenesis J Comp Neurol 467 2003 1 10
11. H.A. Cameron, R.D.G. McKay Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus J Comp Neurol 435 2001 406 415
12. G.P. Cardona-Gomez, L. DonCarlos, M. Garcia-Segura Insulin-like growth factor 1 receptors and estrogen receptors colocalize in female rat brain Neuroscience 99 2000 751 760
13. M.M. Costa, V.I. Reus, O.M. Wolkowitz, F. Manfredi, M. Lieberman Estrogen replacement therapy and cognitive decline in memory-impaired post-menopausal women Biol Psychiatry 46 1999 182 188
14. F. Doetsch The glial identity of neural stem cells Nat Neurosci 6 2003 1127 1134
15. D.B. Dubal, M.L. Kashon, L.C. Pettigrew, J.M. Ren, S.P. Finklestein, S.W. Rau, P.M. Wise Estradiol protects against ischemic injury J Cereb Blood Flow Metab 18 1998 1253 1258
16. D.B. Dubal, H. Zhu, J. Yu, S.W. Rau, P.J. Shughrue, I. Merchenthaler, M.S. Kindy, P.M. Wise Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury Proc Natl Acad Sci U S A 98 2001 1952 1957
17. F. Francis, A. Koulakoff, D. Boucher, P. Chafey, B. Schaar, M.-C. Vinet, G. Friocourt, N. McDonnell, O. Reiner, A. Kahn, S.K. McConnell, Y. Berwald-Netter, P. Denoulet, J. Chelly Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons Neuron 23 1999 247 256
18. R.M.R. Gangemi, M. Perera, G. Corte Regulatory genes controlling cell fate choice in embryonic and adult neural stem cells J Neurochem 89 2004 286 306
19. L.M. Garcia-Segura, I. Azcoitia, L.L. DonCarlos Neuroprotection by estradiol Prog Neurobiol 63 2001 29 60
20. J.G. Gleeson, P.T. Lin, L.A. Flanagan, C.A. Walsh Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons Neuron 23 1999 257 271
21. L. Gollapudi, M.M. Oblinger Stable transfection of PC12 cells with estrogen receptor (ERα) protective effects of estrogen on cell survival after serum deprivation J Neurosci Res 56 1999 99 108
22. B. Greco, E.A. Allegretto, M.J. Tetel, J.D. Blaustein Coexpression of ERβ with ERα and progestin receptor proteins in the female rat forebrain Effects of estradiol treatment Endocrinology 142 2001 5172 5181
23. N.B. Hastings, E. Gould Rapid extension of axons into the CA3 region by adult-generated granule cells J Comp Neurol 413 1999 146 154
24. N.B. Hastings, M.I. Seth, P. Tanapat, T.A. Rydel, E. Gould Granule neurons generated during development extend divergent axon collaterals to hippocampal area CA3 J Comp Neurol 452 2002 324 333
25. W. Jiang, J.-C. Wang, Z. Zhang, A.H. Sheerin, X. Zhang Response of seizure-induced newborn neurons in the dentate gyrus of adult rats to second episode of seizures Brain Res 1006 2004 248 252
26. T. Jover, H. Tanaka, A. Calderone, K. Oguro, M.V.L. Bennett, A.M. Etgen, R.S. Zukin Estrogen protects against global ischemia-induced neuronal death and prevents action of apoptotic signaling cascades in the hippocampal CA1 J Neurosci 22 2002 2115 2124
27. G. Kempermann, S. Jessberger, B. Steiner, G. Kronenberg Milestones of neuronal development in the adult hippocampus Trends Neurosci 27 2004 447 452
28. S. Koike, M. Sakai, M. Muramatsu Molecular cloning and characterization of rat estrogen receptor cDNA Nucleic Acids Res 15 1987 2499 2513
29. G. Kronenberg, K. Reuter, B. Steiner, M.D. Brandt, S. Jessberger, M. Yamaguchi, G. Kempermann Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli J Comp Neurol 467 2003 455 463
30. F.P.M. Kruijver, R. Balesar, A.M. Espila, U.A. Unmehopa, D.F. Swaab Estrogen-receptor-β distribution in the human hypothalamus similarities and differences with ERα distribution J Comp Neurol 466 2003 251 277
31. G.G.J.M. Kuiper, E. Enmark, M. Pelto-Huikko, S. Nilsson, J.-A. Gustafsson Cloning of a novel estrogen receptor expressed in rat prostate and ovary Proc Natl Acad Sci U S A 93 1996 5925 5930
32. V.N. Luine, L.F. Jacome, N.J. MacLusky Rapid enhancement of visual and place memory by estrogens in rats Endocrinology 144 2003 2836 2844
33. V.N. Luine, S.T. Richards, V.Y. Wu, K.D. Beck Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters Horm Behav 34 1998 149 162
34. M.B. Luskin Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone Neuron 11 1993 173 189
35. R.H. Lustig In vitro models for the effects of sex hormones on neurons Ann N Y Acad Sci 784 1996 370 380
36. R.H. Lustig Sex hormone modulation of neural development in vitro Horm Behav 28 1994 383 395
37. T.M. Madsen, P.E.G. Kristjansen, T.G. Bolwig, G. Wörtwein Arrested hippocampal neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat Neuroscience 119 2003 635 642
38. E.A. Markakis, F.H. Gage Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles J Comp Neurol 406 1999 449 460
39. A.Y. Maslov, T.A. Barone, R.J. Plunkett, S.C. Pruitt Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice J Neurosci 24 2004 1726 1733
40. B. McEwen Estrogen actions throughout the brain Recent Prog Horm Res 57 2002 357 384
41. B.S. McEwen, S.H. Alves Estrogen actions in the central nervous system Endocr Rev 20 1999 279 307
42. T.A. Milner, B.S. McEwen, S. Hayashi, C.J. Li, L.P. Reagan, S.E. Alves Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites J Comp Neurol 429 2001 355 371
43. R.C. Miranda, C.D. Toran-Allerand Developmental expression of estrogen receptor mRNA in the rat cerebellar cortex a nonisotopic in situ hybridization histochemistry study Cereb Cortex 2 1992 1 15
44. A.K. Murashov, E.S. Pak, W.A. Hendricks, L.M. Tatko 17β-Estradiol enhances neuronal differentiation of mouse embryonic stem cells FEBS Lett 569 2004 165 168
45. J. Nacher, C. Crespo, B. McEwen Doublecortin expression in the adult telencephalon Eur J Neurosci 14 2001 629 644
46. 3H-thymidine incorporation and neurogenesis J Neurosci 13 1993 2930 2938
47. C. Patrone, G. Pollio, E. Vegeto, E. Enmark, I. de Curtis, J.-A. Gustafsson, A. Maggi Estradiol induces differential neuronal phenotypes by activating estrogen receptor alpha or beta Endocrinology 141 2000 1839 1845
48. M. Perez-Martin, I. Azcoitia, J.L. Trejo, A. Sierra, L.M. Garcia-Segura An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin-like growth factor-I in the dentate gyrus of adult female rat Eur J Neurosci 18 2003 923 930
49. K. Pettersson, K. Grandien, G.G. Kuiper, J.A. Gustafsson Mouse estrogen receptor β forms estrogen response element-binding heterodimers with estrogen receptor α Mol Endocrinol 11 1997 1486 1496
50. M.S. Rao, A.K. Shetty Efficacy of doublecortin as a marker to analyze the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus Eur J Neurosci 19 2004 234 246
51. R. Sandyk Estrogens and pathophysiology of Parkinson's disease Int J Neurosci 45 1989 119 122
52. R. Saunders-Pullman, J. Gordon-Elliott, M. Parides, S. Fahn, H.R. Saunders, S. Bressman The effect of estrogen replacement on early Parkinson's disease Neurology 52 1999 1417 1421
53. R. Schmidt, F. Fazekas, B. Reinhart, P. Kapeller, G. Fazekas, H. Offenbacher, B. Eber, M. Schumacher, W. Freidl Estrogen replacement therapy in older women a neuropsychological and brain MRI study J Am Geriatr Soc 44 1996 1307 1313
54. C. Schmidt-Hieber, P. Jonas, J. Bischofberger Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus Nature 429 2004 184 187
55. T. Scholzen, J. Gerdes The Ki-67 protein from the known and the unknown J Cell Physiol 182 2000 311 322
56. T.J. Shors, G. Miesegaes, A. Beylin, M. Zhao, T. Rydel, E. Gould Neurogenesis in the adult is involved in the formation of new memories Nature 410 2001 372 376
57. T.J. Shors, D.A. Townsend, M. Zhao, Y. Kozorovitskiy, E. Gould Neurogenesis may relate to some but not all types of hippocampal-dependent learning Hippocampus 12 2002 578 584
58. P.J. Shughrue, M.V. Lane, I. Merchenthaler Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system J Comp Neurol 388 1997 507 525
59. P.J. Shughrue, I. Merchenthaler Evidence for novel estrogen binding sites in the rat hippocampus Neuroscience 99 2000 605 612
60. P.J. Shughrue, P.J. Scrimo, I. Merchenthaler Evidence for the colocalization of estrogen receptor-β mRNA and estrogen receptor-α immunoreactivity in neurons of the rat forebrain Endocrinology 139 1998 5267 5270
61. R.B. Simerly, C. Chang, M. Muramatsu, L.W. Swanson Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain an in situ hybridization study J Comp Neurol 294 1990 76 95
62. M.T. Smith, V. Pencea, Z. Wang, M.B. Luskin, T.R. Insel Increased number of BrdU-labeled neurons in the rostral migratory stream of the estrous prairie vole Horm Behav 39 2001 11 21
63. J.S. Snyder, N. Kee, J.M. Wojtowicz Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus J Neurophysiol 85 2001 2423 2431
64. F. Sohrabji, R.C. Miranda, C.D. Toran-Allerand Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor Proc Natl Acad Sci U S A 92 1995 11110 11114
65. D.T. Solum, R.J. Handa Localization of estrogen receptor alpha (ERα) in pyramidal neurons of the developing rat hippocampus Dev Brain Res 128 2001 165 175
66. D.T. Solum, R.J. Handa Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus J Neurosci 22 2002 2650 2659
67. B.B. Stanfield, J.E. Trice Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections Exp Brain Res 72 1988 399 406
68. D.J. Stone, Y. Song, C.P. Anderson, K.K. Krohn, C.E. Finch, I. Rozovsky Bidirectional transcription regulation of glial fibrillary acidic protein by estradiol in vivo and in vitro Endocrinology 139 1998 3202 3209
69. P. Tanapat, N.B. Hastings, A.J. Reeves, E. Gould Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat J Neurosci 19 1999 5792 5901
70. T.J. Toung, R.J. Traystman, P.D. Hurn Estrogen-mediated neuroprotection after experimental stroke in male rats Stroke 29 1998 1666 1670
71. T.K. Toung, P.D. Hurn, R.J. Traystman, F.E. Sieber Estrogen decreases infarct size after temporary focal ischemia in a genetic model of type 1 diabetes mellitus Stroke 31 2000 2701 2706
72. H. van Praag, B.R. Christie, T.J. Sejnowski, F.H. Gage Running enhances neurogenesis, learning and long-term potentiation in mice Proc Natl Acad Sci U S A 96 1999 13427 13431
73. H. van Praag, A.F. Schinder, B.R. Christie, N. Toni, T.D. Palmer, F.H. Gage Functional neurogenesis in the adult hippocampus Nature 415 2002 1030 1034
74. L. Wang, S. Andersson, M. Warner, J.A. Gustafsson Estrogen receptor (ER) β knockout mice reveal a role for ERβ in migration of cortical neurons in the developing brain Proc Natl Acad Sci U S A 100 2003 703 708
75. S. Wang, B.W. Scott, J.M. Wojtowicz Heterogeneous properties of dentate granule neurons in the adult rat J Neurobiol 42 2000 248 257
76. N.G. Weiland, C. Orikasa, S. Hayashi, B.S. McEwen Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats J Comp Neurol 388 1997 603 612
77. C. Woolley, B.S. McEwen Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat J Neurosci 12 1992 2549 2554
78. Y. Xu, M. Berelowitz, J.F. Bruno Characterization of the promoter region of the human somatostatin receptor subtype 2 gene and localization of sequences required for estrogen-responsiveness Mol Cell Endocrinol 139 1998 71 77
79. Y.S. Zhu, D.W. Pfaff DNA binding of hypothalamic nuclear proteins on estrogen response element and preproenkephalin promoter modification by estrogen Neuroendocrinology 62 1995 454 464