Minireview: Estrogen receptor-initiated mechanisms causal to mammalian reproductive behaviors

Endocrinology

Volumn 152, Issue 4, 2011, Pages 1209-1217

  Pfaff, Donald ^a   Waters, Elizabeth ^a   Khan, Quaiser ^a   Zhang, Xiaoting ^b   Numan, Michael ^c  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c BOSTON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MESSENGER RNA; OXYTOCIN; OXYTOCIN RECEPTOR;

BRAIN NERVE CELL; COGNITION; GENETIC TRANSCRIPTION; HUMAN; MATERNAL BEHAVIOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SEXUAL BEHAVIOR; SHORT SURVEY;

ANIMALS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; HUMANS; RECEPTORS, ESTROGEN; REPRODUCTIVE BEHAVIOR;

EID: 79953210036     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-1007     Document Type: Short Survey

References (117)

1. Pfaff DW 1999 Drive: neurobiological and molecular mechanisms of sexual motivation. Cambridge: The M.I.T. Press
2. Lee AW, Kow L-M, Devidze N, Ribeiro A, Martin-Alguacil N, Schober J, Pfaff D 2009 Genetic mechanisms in neural and hormonal controls over female reproductive behaviors. Hormones Brain and Behavior 2:1163-1186
3. Sakuma Y 2008 Neural substrates for sexual preference and motivation in the female and male rat. Ann NY Acad Sci 1129:55-60 (Review)
4. Ogawa S, Chan J, Gustafsson JA, Korach KS, Pfaff DW 2003 Estrogen increases locomotor activity in mice through estrogen receptor α: specificity for the type of activity. Endocrinology 144:230-239 (Pubitemid 36082802)
5. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA 1996 Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93:5925-5930 (Pubitemid 26190778)
6. Kelly MJ, Moss RL, Dudley CA 1976 Differential sensitivity of preoptic-septal neurons to microelectrophoresed estrogen during the estrous cycle. Brain Res 114:152-157
7. Simerly RB, Chang C, Muramatsu M, Swanson LW 1990 Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294:76-95 (Pubitemid 20104631)
8. Shughrue PJ, Lane MV, Merchenthaler I 1997 Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J Comp Neurol 388:507-525 (Pubitemid 27481288)
9. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE 2003 Immunolocalization of estrogen receptor β in the mouse brain: comparison with estrogen receptor α. Endocrinology [Erratum (2003) 144:2844] 144:2055-2067 (Pubitemid 36543346)
10. Musatov S, Chen W, Pfaff DW, Kaplitt MG, Ogawa S 2006 RNAi-mediated silencing of estrogen receptor (α) in the ventromedial nucleus of hypothalamus abolishes female sexual behaviors. Proc Natl Acad Sci USA 103:10456-10460 (Pubitemid 44051188)
11. Ogawa S, Choleris E, Pfaff DW 2004 Genetic influences on aggressive behaviors and arousability in animals. Ann NY Acad Sci 1036:257-266 (Review)
12. Tetel MJ, Pfaff DW 2010 Contributions of estrogen receptor-α and estrogen receptor-β to the regulation of behavior. Biochim Biophys Acta 1800:1084-1089
13. Numan M, Fleming AS, Levy F 2006 Maternal behavior. In: Neill JD, ed. Knobil and Neill's physiology of reproduction. New York: Elsevier; 1921-1993
14. Numan M, Insel TR 2003 The neurobiology of parental behavior. New York: Springer
15. Numan M 2006 Hypothalamic neural circuits regulating maternal responsiveness toward infants. Behav Cogn Neurosci Rev 5:163-190 (Pubitemid 44673188)
16. Numan M, Sheehan TP 1997 Neuroanatomical circuitry for mammalian maternal behavior. Ann NY Acad Sci 877:101-125 (Pubitemid 27135488)
17. Bridges RS 1984 A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 114:930-940 (Pubitemid 14166102)
18. Moltz H, Lubin M, Leon M, Numan M 1970 Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiol Behav 5:1373-1377
19. Numan M, Rosenblatt JS, Komisaruk BR 1977 Medial preoptic area and onset of maternal behavior in the rat. J Comp Physiol Psychol 91:146-164 (Pubitemid 8101304)
20. Fahrbach SE, Pfaff DW 1986 Effect of preoptic region implants of dilute estradiol on the maternal behavior of ovariectomized, nulliparous rats. Horm Behav 20:354-363 (Pubitemid 16026100)
21. Ribeiro AC, Musatov S, Shteyler A, Simanduyev S, Arrieta-Cruz I, Ogawa S, Pfaff D 2009 Estrogen-receptor-α expression in the medial preoptic area is necessary for maternal behavior, sexual behavior and aggression, but not running wheel or home-cage activity in female mice. Soc Neurosci 675.15 (Abstract)
22. Fahrbach SE, Morrell JI, Pfaff DW 1985 Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40:526-532 (Pubitemid 15042694)
23. Sugiyama N, Barros RP, Warner M, Gustafsson JA 2010 ERβ: recent understanding of estrogen signaling. Trends Endocrinol Metab 21:545-552
24. Fan X, Xu H, Warner M, Gustafsson JA 2010 ERβ in CNS: new roles in development and function. Prog Brain Res 181:233-250
25. Pedersen CA, Ascher JA, Monroe YL, Prange Jr AJ 1982 Oxytocin induces maternal behavior in virgin female rats. Science 216:648-650
26. Olazábal DE, Young LJ 2006 Oxytocin receptors in the nucleus accumbens facilitate "spontaneous" maternal behavior in adult female prairie voles. Neuroscience 141:559-568
27. Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA 1994 Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108:1163-1171
28. Numan M, Stolzenberg DS 2009 Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front Neuroendocrinol 30:46-64
29. Amico JA, Mantella RC, Vollmer RR, Li X 2004 Anxiety and stress responses in female oxytocin deficient mice. J Neuroendocrinol 16:319-324 (Pubitemid 38618648)
30. Ring RH, Malberg JE, Potestio L, Ping J, Boikess S, Luo B, Schechter LE, Rizzo S, Rahman Z, Rosenhzweig-Lipson S 2006 Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology 185:218-225 (Pubitemid 43363618)
31. Windle RJ, Shanks N, Lightman SL, Ingram CD 1997 Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 138:2829-2834 (Pubitemid 27258513)
32. Yoshida M, Takayanagi Y, Inoue K, Kimura T, Young LJ, Onaka T, Nishimori K 2009 Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J Neurosci 29:2259-2271
33. McCarthy MM, McDonald CH, Brooks PJ, Goldman D 1996 An anxiolytic action of oxytocin is enhanced by estrogen in the mouse. Physiol Behav 60:1209-1215 (Pubitemid 26389050)
34. Bosch OJ, Neumann ID 2008 Brain vasopressin is an important regulator of maternal behavior independent of dams' trait anxiety. Proc Natl Acad Sci USA 105:17139-17144
35. Amico JA, Thomas A, Hollingshead DJ 1997 The duration of estradiol and progesterone exposure prior to progesterone withdrawal regulates oxytocin mRNA levels in the paraventricular nucleus of the rat. Endocr Res 23:141-156 (Pubitemid 27407117)
36. Patisaul HB, Scordalakes EM, Young LJ, Rissman EF 2003 Oxytocin, but not oxytocin receptor, is regulated by oestrogen receptor β in the female mouse hypothalamus. J Neuroendocrinol 15:787-793 (Pubitemid 36880737)
37. Quiñones-Jenab V, Jenab S, Ogawa S, Adan RA, Burbach JP, Pfaff DW 1997 Effects of estrogen on oxytocin receptor messenger ribonucleic acid expression in the uterus, pituitary and forebrain of the female rat. Neuroendocrinology 65:9-17 (Pubitemid 27042813)
38. Young LJ, Wang Z, Donaldson R, Rissman EF 1998 Estrogen receptor-β is essential for induction of oxytocin receptor by estrogen. Neuroreport 9:933-936 (Pubitemid 28179303)
39. Champagne F, Diorio J, Sharma S, Meaney MJ 2001 Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci USA 98:12736-12741 (Pubitemid 33020015)
40. Champagne FA, Weaver IC, Diorio J, Sharma S, Meaney MJ 2003 Natural variations in maternal care are associated with estrogen receptor-α expression and estrogen sensitivity in the medial preoptic area. Endocrinology 144:4720-4724 (Pubitemid 37378383)
41. Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf S, Meaney MJ 2006 Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology 147:2909-2915 (Pubitemid 43764626)
42. Choleris E, Gustafsson JA, Korach KS, Muglia LJ, Pfaff DW, Ogawa S 2003 An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-α and -β knockout mice. Proc Natl Acad Sci USA 100:6192-6197 (Pubitemid 36581861)
43. Choleris E, Ogawa S, Kavaliers M, Gustafsson JA, Korach KS, Muglia LJ, Pfaff DW 2006 Involvement of estrogen receptor α, β and oxytocin in social discrimination: A detailed behavioral analysis with knockout female mice. Genes Brain Behav 5:528-539
44. Rønnekleiv OK, Kelly MJ 2005 Diversity of ovarian steroid signaling in the hypothalamus. Front Neuroendocrinol 26:65-84 (Review)
45. Stolzenberg DS, Zhang KY, Luskin K, Ranker L, Balkema J, Bress J, Numan M 2009 A single injection of 17β-estradiol at the time of pup presentation promotes the onset of maternal behavior in pregnancy-terminated rats. Horm Behav 56:121-127
46. Stolzenberg DS, McKenna JB, Keough S, Hancock R, Numan MJ, Numan M 2007 Dopamine D1 receptor stimulation of the nucleus accumbens or the medial preoptic area promotes the onset of maternal behavior in pregnancy-terminated rats. Behav Neurosci 121:907-919 (Pubitemid 350051294)
47. Vasudevan N, Pfaff DW 2007 Membrane initiated actions of estrogens in neuroendocrinology: emerging principles. Endocr Rev 28:1-19 (Pubitemid 46220848)
48. Kow LM, Pfaff DW 2004 The membrane actions of estrogens can potentiate their lordosis behavior-facilitating genomic actions. Proc Natl Acad Sci USA 101:12354-12357 (Pubitemid 39145447)
49. Meaney MJ 2010 Epigenetics and the biological definition of gene x environment interactions. Child Dev 81:41-79
50. Schwarz JM, Nugent BM, McCarthy MM 2010 Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span. Endocrinology 151:4871-4881
51. Gagnidze K, Weil ZM, Pfaff DW 2010 Histone modifications proposed to regulate sexual differentiation of brain and behavior. Bioessays 32:932-939
52. McGraw LA, Young LJ 2010 The prairie vole: an emerging model organism for understanding the social brain. Trends Neurosci 33:103-109
53. Young LJ, Wang Z 2004 The neurobiology of pair bonding. Nature Neurosci 7:1048-1054 (Pubitemid 41184443)
54. Numan N 2011 Neural circuits regulating maternal behavior: implications for understanding the neural basis of social cooperation and competition. In: Brown S, Brown M, Penner L, eds. Self-interest and beyond: toward a new understanding of human caregiving. New York: Oxford University Press; 81-101
55. Guastella AJ, Mitchell PB, Mathews F 2008 Oxytocin enhances the encoding of positive social memories in humans. Biol Psychiatry 64:256-258
56. Rodrigues SM, Saslow LR, Garcia N, John OP, Keltner D 2009 Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proc Natl Acad Sci USA 106:21437-21441
57. Feldman R, Weller A, Zagoory-Sharon O, Levine A 2007 Postpartum period predict mother-infant bonding. Psychol Sci 18:965-970
58. Feldman R, Gordon I, Schneiderman I, Weisman O, Zagoory-Sharon O 2010 Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35:1133-1141
59. Gordon I, Zagoory-Sharon O, Leckman JF, Feldman R 2010 Oxytocin and the development of parenting in humans. Biol Psychiatry 68:377-382
60. Bakermans-Kranenburg MJ, van Ijzendoorn MH 2008 Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting. SCAN 3:128-134 (Pubitemid 351827056)
61. Strathearn L, Fonagy P, Amico J, Montague PR 2009 Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology 34:2655-2666
62. Fries AB, Ziegler TE, Kurian JR, Jacoris S, Pollak SD 2005 Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior. Proc Natl Acad Sci USA 102:17237-17240 (Pubitemid 41692713)
63. Heim C, Young LJ, Newport DJ, Mletzko T, Miller AH, Nemerorr CB 2009 Lower CSF oxytocin concentrations in women with a history of childhood abuse. Mol Psychiatry 14:954-958
64. Feifel D, MacDonald K 2010 Intranasal oxytocin added adjunct to antipsychotics reduces symptoms in schizophrenia. Biol Psychiatry 67:205
65. Feifel D, Macdonald K, Nguyen A, Cobb P, Warlan H, Galangue B, Minassian A, Becker O, Cooper J, Perry W, Lefebvre M, Gonzales J, Hadley A 2010 Adjunctive intranasal oxytocin reduces symptoms in schizophrenia patients. Biol Psychiatry 68:678-680
66. Feifel D, MacDonald K, Nguyen A, Warlan H, Galangue B, Cobb P, Minassian A, Becker O, Cooper J, Perry W, Lefebvre M, Gonzales J, Hadley A Intranasal oxytocin augmentation of antipsychotic medication in schizophrenia patients. Program of the Annual Meeting of the Society for Neuroscience, Chicago, IL, 2009, No. 644.12
67. Pedersen CA, Penn DL, Rau SW, Salimi K 2010 Oxytocin treatment of social cognitive deficits, paranoia, and other psychotic symptoms in schizophrenia. Biol Psychiatry 67:205
68. Champagne FA 2008 Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29:386-397 (Review)
69. Kumar R, O'Malley B 2008 NR coregulators and human diseases. London: World Scientific Press
70. Hunter RG, McCarthy KJ, Milne TA, Pfaff DW, McEwen BS 2009 Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proc Natl Acad Sci USA 106:20912-20917
71. Gagnidze K, Pfaff DW, Mong JA 2010 Gene expression in neuroendocrine cells during the critical period forsexual differentiation of the brain. Prog Brain Res 186:97-111
72. Soulez M, Parker MG 2001 Identification of novel oestrogen receptor target genes in human ZR75-1 breast cancer cells by expression profiling. J Mol Endocrinol 27:259-274 (Pubitemid 33130125)
73. Frasor J, Danes JM, Komm B, Chang KC, Lyttle CR, Katzenellenbogen BS 2003 Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 144:4562-4574 (Pubitemid 37204856)
74. Kininis M, Chen BS, Diehl AG, Isaacs GD, Zhang T, Siepel AC, Clark AG, Kraus WL 2007 Genomic analyses of transcription factor binding, histone acetylation, and gene expression reveal mechanistically distinct classes of estrogen-regulated promoters. Mol Cell Biol 27:5090-5104 (Pubitemid 47068284)
75. Carroll JS, Brown M 2006 Estrogen receptor target gene: an evolving concept. Mol Endocrinol 20:1707-1714 (Pubitemid 44148078)
76. Cheung E, Kraus WL 2010 Genomic analyses of hormone signaling and gene regulation. Annu Rev Physiol 72:191-218
77. Ambros V 2004 The functions of animal microRNAs. Nature 431:350-355
78. Meister G, Tuschl T 2004 Mechanisms of gene silencing by doublestranded RNA. Nature 431:343-349 (Pubitemid 39265674)
79. Bartel DP 2009 MicroRNAs: target recognition and regulatory functions. Cell 136:215-233
80. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR, Fox EA, Silver PA, Brown M 2005 Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122:33-43 (Pubitemid 40977938)
81. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, Wang Q, Bekiranov S, Sementchenko V, Fox EA, Silver PA, Gingeras TR, Liu XS, Brown M 2006 Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38:1289-1297 (Pubitemid 44646291)
82. Welboren WJ, van Driel MA, Janssen-Megens EM, van Heeringen SJ, Sweep FC, Span PN, Stunnenberg HG 2009 ChIP-Seq of ERα and RNA polymerase II defines genes differentially responding to ligands. EMBO J 28:1418-1428
83. Laganière J, Deblois G, Lefebvre C, Bataille AR, Robert F, Giguère V 2005 From the cover: location analysis of estrogen receptor α target promoters reveals that FOXA1 defines a domain of the estrogen response. Proc Natl Acad Sci USA 102:11651-11656
84. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, Carroll JS, Liu XS, Brown M 2008 FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132:958-970 (Pubitemid 351391952)
85. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schütz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM 1995 The nuclear receptor superfamily: the second decade. Cell 83:835-839
86. Glass CK, Rosenfeld MG 2000 The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev 14:121-141 (Pubitemid 30070977)
87. McKenna NJ, O'Malley BW 2002 Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108:465-474 (Pubitemid 34260872)
88. Roeder RG 2003 Lasker Basic Medical Research Award. The eukaryotic transcriptional machinery: complexities and mechanisms unforeseen. Nat Med 9:1239-1244
89. Hall JM, McDonnell DP 2005 Coregulators in nuclear estrogen receptor action: from concept to therapeutic targeting. Mol Interv 5:343-357 (Pubitemid 43060715)
90. Xu J, Li Q 2003 Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol Endocrinol 17:1681-1692 (Pubitemid 37072287)
91. Malik S, Roeder RG 2005 Dynamic regulation of pol II transcription by the mammalian Mediator complex. Trends Biochem Sci 30:256-263 (Pubitemid 40693869)
92. Kornberg RD 2005 Mediator and the mechanism of transcriptional activation. Trends Biochem Sci 30:235-239 (Pubitemid 40693865)
93. Wang GG, Allis CD, Chi P 2007 Chromatin remodeling and cancer, Part II: ATP-dependent chromatin remodeling. Trends Mol Med 13:373-380
94. Wang GG, Allis CD, Chi P 2007 Chromatin remodeling and cancer, Part I: Covalent histone modifications. Trends Mol Med 13:363-372
95. Zhang X, Krutchinsky A, Fukuda A, Chen W, Yamamura S, Chait BT, Roeder RG 2005 MED1/TRAP220 exists predominantly in a TRAP/ Mediator subpopulation enriched in RNA polymerase II and is required for ER-mediated transcription. Mol Cell 19:89-100 (Pubitemid 40884660)
96. Xu J, Wu RC, O'Malley BW 2009 Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat Rev Cancer 9:615-630
97. Jiang P, Hu Q, Ito M, Meyer S, Waltz S, Khan S, Roeder RG, Zhang X 2010 Key roles for MED1 LxxLL motifs in pubertal mammary gland development and luminal-cell differentiation. Proc Natl Acad Sci USA 107:6765-6770
98. Chen W, Zhang X, Birsoy K, Roeder RG 2010 A muscle-specific knockout implicates nuclear receptor coactivator MED1 in the regulation of glucose and energy metabolism. Proc Natl Acad Sci USA 107:10196-10201
99. Eeckhoute J, Carroll JS, Geistlinger TR, Torres-Arzayus MI, Brown M 2006 A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes Dev 20:2513-2526 (Pubitemid 44396837)
100. Auger AP, Tetel MJ, McCarthy MM 2000 Steroid receptor coactivator-1 (SRC-1) mediates the development of sex specific brain morphology and behavior. Proc Natl Acad Sci USA 97:7551-7555 (Pubitemid 30431501)
101. Molenda HA, Griffin AL, Auger AP, McCarthy MM, Tetel MJ 2002 Nuclear receptor coactivators modulate hormone-dependent gene expression in brain and female reproductive behavior in rats. Endocrinology 143:436-444 (Pubitemid 34107196)
102. Weil ZM, Hunter RG, McEwen BS, Allis CD, Pfaff DW 2009 Estrogenic regulation of histone acetylation in ventromedial hypothalamic neurons. Society for Neuroscience 273.9/DD5
103. Gagnidze K, Weil ZM, Khattak M, Pfaff DW 2010 Estrogen-induced chromatin remodeling and gene transcription in the ventromedial hypothalamus. Society for Neuroscience 495.11/HHH31 (Poster)
104. Romano GJ, Krust A, Pfaff DW 1989 Expression and estrogen regulation of progesterone receptor mRNA in neurons of the mediobasal hypothalamus: an in situ hybridization study. Mol Endocrinol 3:1295-1300 (Pubitemid 19210441)
105. Blaustein JD 2003 Progestin receptors: neuronal integrators of hormonal and environmental stimulation. Ann NY Acad Sci 1007:238-250 (Review)
106. Katzenellenbogen BS, Katzenellenbogen JA 2000 Estrogen receptor transcription and transactivation: Estrogen receptor α and estrogen receptor β: regulation by selective estrogen receptor modulators and importance in breast cancer. Breast Cancer Res 2:335-344 (Review)
107. Garcia-Segura LM, McCarthy MM 2004 Minireview: Role of glia in neuroendocrine function. Endocrinology 145:1082-1086 (Review)
108. Mong JA, Blutstein T 2006 Estradiol modulation of astrocytic form and function: implications for hormonal control of synaptic communication. Neuroscience 138:967-975 (Review)
109. Amateau SK, McCarthy MM 2002 Sexual differentiation of astrocyte morphology in the developing rat preoptic area. J Neuroendocrinol 14:904-910 (Pubitemid 35378708)
110. Woolley CS 2007 Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 47:657-680 (Review)
111. Hart SA, Snyder MA, Smejkalova T, Woolley CS 2007 Estrogen mobilizes a subset of estrogen receptor-alpha-immunoreactive vesicles in inhibitory presynaptic boutons in hippocampal CA1. J Neurosci 27:2102-2111
112. Gould E, Tanapat P, Rydel T, Hastings N 2000 Regulation of hippocampal neurogenesis in adulthood. Biol Psychiatry 48:715-720
113. Suzuki S, Gerhold LM, Böttner M, Rau SW, Dela Cruz C, Yang E, Zhu H, Yu J, Cashion AB, Kindy MS, Merchenthaler I, Gage FH, Wise PM 2007 Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J Comp Neurol 500:1064-1075 (Pubitemid 46110642)
114. Hammond R, Mauk R, Ninaci D, Nelson D, Gibbs RB 2009 Chronic treatment with estrogen receptor agonists restores acquisition of a spatial learning task in young ovariectomized rats. Horm Behav 56:309-314
115. Gibbs RB 2010 Estrogen therapy and cognition: a review of the cholinergic hypothesis. Endocr Rev 31:224-253 (Review)
116. Dubal DB, Zhu H, Yu J, Rau SW, Shughrue PJ, Merchenthaler I, Kindy MS, Wise PM 2001 Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci USA 98:1952-1957 (Pubitemid 32165604)
117. Brown CM, Mulcahey TA, Filipek NC, Wise PM 2010 Production of proinflammatory cytokines and chemokines during neuroinflammation: novel roles for estrogen receptors alpha and beta. Endocrinology 151:4916-4925