Estrogen action: A historic perspective on the implications of considering alternative approaches

Physiology and Behavior

Volumn 99, Issue 2, 2010, Pages 151-162

  Jensen, Elwood V ^a   Jacobson, Herbert I ^b   Walf, Alicia A ^c   Frye, Cheryl A ^c  

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

^b ALBANY MEDICAL COLLEGE   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

fetoprotein; Breast cancer; Estradiol; Estrogen receptor; Neurosteroid; Trophic

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; ALPHA FETOPROTEIN; AROMATASE INHIBITOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HEXESTROL; HISTONE DEACETYLASE INHIBITOR; MONOCLONAL ANTIBODY; PROGESTERONE; RECOMBINANT HUMAN ALPHA FETOPROTEIN; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; TAMOXIFEN; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ANTINEOPLASTIC ACTIVITY; ARTICLE; BEHAVIOR; BRAIN; BREAST CANCER; CANCER PREVENTION; CANCER REGRESSION; CANCER RISK; CANCER THERAPY; COGNITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ESTROGEN ACTIVITY; ESTROGEN SYNTHESIS; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; NONHUMAN; OXIDATION REDUCTION REACTION; POSTMENOPAUSE; PREGNANCY; PREMENOPAUSE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BLOOD LEVEL; RECEPTOR BINDING; TISSUE DISTRIBUTION; UTERUS GROWTH;

ANIMALS; ESTROGENS; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; RECEPTORS, ESTROGEN;

EID: 72649087326     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2009.08.013     Document Type: Article

References (136)

1. Jensen E.V. High point. Breast Cancer Res Treat 9 (1987) 77-86
2. Jensen E.V., and Jacobson H.I. Fate of steroid estrogens in target tissues. In: Pincus G., and Vollmer E.P. (Eds). Biological activities of steroids in relation to cancer (1960), Academic Press, New York 161-174
3. Jensen E.V., and Jacobson H.I. Basic guides to the mechanism of estrogen action. Recent Prog Horm Res 18 (1962) 387-414
4. Toft D., and Gorski J. A receptor molecule for estrogens: isolation from the rat uterus and preliminary characterization. Proc Natl Acad Sci U S A 55 (1966) 1574-1581
5. Toft D., Shyamala G., and Gorski J. A receptor molecule for estrogens: studies using a cell-free system. Proc Natl Acad Sci U S A 57 (1967) 1740-1743
6. Jensen E.V., Suzuki T., Kawashima T., Stumpf W.E., Jungblut P.W., and DeSombre E.R. A two-step mechanisim for the interaction of estradiol with a rat uterus. Proc Natl Acad Sci U S A 59 (1968) 632-638
7. Jensen E.V., and DeSombre E.R. Estrogen-receptor interaction. Science 182 (1973) 126-134
8. O'Malley B.W., Sherman M.R., and Toft D.O. Progesterone "receptors" in the cytoplasm and nucleus of chick oviduct target tissue. Proc Natl Acad Sci U S A 67 (1970) 501-508
9. MacLeod K.N., and Baxter J.D. DNA binding of thyroid hormone receptors. Biochem Biophys Res Commun 62 (1975) 577-583
10. Greene G.L., Closs L.E., Fleming H., DeSombre E.R., and Jensen E.V. Antibodies to estrogen receptor: immunochemical similarity of estrophilin from various mammalian species. Proc Natl Acad Sci U S A 74 (1977) 3681-3685
11. Greene G.L., Fitch F.W., and Jensen E.V. Monoclonal antibodies to estrophilin: probes for the study of estrogen receptors. Proc Natl Acad Sci U S A 77 (1980) 157-161
12. Greene G.L., Nolan C., Engler J.P., and Jensen E.V. Monoclonal antibodies to human estrogen receptor. Proc Natl Acad Sci U S A 77 (1980) 5115-5119
13. Jordan V.C., Jacobson H.I., and Keenan E.J. Determination of estrogen receptor in breast cancer using monoclonal antibody technology: results of a multicenter study in the United States. Cancer Res 46 (1986) 4237s-4240s
14. Greene G.L., Sobel N.B., King W.J., and Jensen E.V. Immunochemical studies of estrogen receptors. J Steroid Biochem 20 (1984) 51-56
15. Green S., Walter P., Kumar V., Krust A., Bornert J.M., Argos P., et al. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature 320 (1986) 134-139
16. Green S., Kumar V., Krust A., Walter P., and Chambon P. Structural and functional domains of the estrogen receptor. Cold Spring Harb Symp Quant Biol 51 (1986) 751-758
17. Green S., Walter P., Greene G., Krust A., Goffin C., Jensen E., et al. Cloning of the human oestrogen receptor cDNA. J Steroid Biochem 24 (1986) 77-83
18. Krust A., Green S., Argos P., Kumar V., Walter P., Bornert J.M., et al. The chicken oestrogen receptor sequence: homology with v-erbA and the human oestrogen and glucocorticoid receptors. EMBO J 5 (1986) 891-897
19. Beatson G.T. On the treatment of inoperable cases of carcinoma of the mamma: suggestions for a new methods of treatment with illustrative cases. Lancet 2 (1986) 104-107
20. Huggins C., Grand L.C., and Brillantes F.P. Mammary cancer induced by a single feeding of polymucular hydrocarbons, and its suppression. Nature 189 (1961) 204-207
21. Jordan V.C. The development of tamoxifen for breast cancer therapy: a tribute to the late Arthur L. Walpole. Breast Cancer Res Treat 11 (1988) 197-209
22. Jensen E.V., Block G.E., Smith S., Kyser K., and DeSombre E.R. Estrogen receptors and breast cancer response to adrenalectomy. Natl Cancer Inst Monogr 34 (1971) 55-70
23. DeSombre E.R., Greene G.L., and Jensen E.V. Estrophillin and endocrine responsiveness of breast cancer. In: McGuie W.L. (Ed). Progress research and therapy (1978), Raven Press, New York 1-14
24. Jensen E.V., and Jordan V.C. The estrogen receptor: a model for molecular medicine. Clin Cancer Res 9 (2003) 1980-1989
25. Peck J.D., Hulka B.S., Poole C., Savitz D.A., Baird D., and Richardson B.E. Steroid hormone levels during pregnancy and incidence of maternal breast cancer. Cancer Epidemiol Biomarkers Prev 4 (2002) 361-368
26. Swanson S.M., Whitaker L.M., Stockard C.R., Myers R.B., Oelschlager D., Grizzle W.E., et al. Hormone levels and mammary epithelial cell proliferation in rats treated with a regimen of estradiol and progesterone that mimics the preventive effect of pregnancy against mammary cancer. Anticancer Res 17 (1997) 4639-4645
27. Grubbs C.J., Hill D.L., McDonough K.C., and Peckham J.C. N-nitroso-N-methylurea-induced mammary carcinogenesis: effect of pregnancy on preneoplastic cells. J Natl Cancer Inst 71 (1983) 625-628
28. Grubbs C.J., Juliana M.M., Hill D.L., and Whitaker L.M. Suppression by pregnancy of chemically induced preneoplastic cells of the rat mammary gland. Anticancer Res. 6 (1986) 1395-1400
29. Jacobson H.I., Thompson W.D., and Janerich D.T. Multiple births and maternal risk of breast cancer. Am J Epidemiol 129 (1989) 865-873
30. Abelev G.I., Perova S.D., Khramkova N.I., Postinkova Z.A., and Irlin I.S. Production of embryonal α-globulin by transplantable mouse hepatomas. Transplantation 1 (1963) 174-180
31. Bergstrand C.G., and Czar B. Demonstration of a new protein fraction in serum from the human fetus. Scand J Clin Lab Invest 8 (1956) 174
32. Andrews G.K., Dziadek M., and Tamaoki T. Expression and methylation of the mouse α-fetoprotein gene in embryonic, adult, and neoplastic tissues. J Biol Chem 257 (1982) 5148-5153
33. Sell S., and Becker F.F. Alpha-fetoprotein. J Natl Cancer Inst 60 (1978) 19-26
34. Tilghman S.M., and Belayew A. Transcriptional control of the murine albumin/α-fetoprotein locus during development. Proc Natl Acad Sci U S A 79 (1982) 5254-5257
35. Crandall B.F. Alpha-fetoprotein: a review. Crit Rev Clin Lab Sci 15 (1981) 127-185
36. Raynaud J.P. Influence of rat estradiol binding plasma protein (EBP) on uterotrophic activity. Steroids 21 (1978) 249-258
37. Jacobson H.I., and Janerich D.T. Pregnanct altered breast cancer risk; mediated by AFP (1987), CRC Press 39-100
38. Jacobson H.I., Thompson W.D., and Janerich D.T. Multiple birth and maternal risk of breast cancer. Am J Epidemiol 129 (1989) 865-873
39. Richardson B.E., Hulka B.S., Peck J.L., Hughes C.L., Vandenberg B.J., Christianson R.E., et al. Levels of maternal serum α-fetoprotein (AFP) in pregnant women and subsequent breast cancer risk. Am J Epidemiol 148 (1998) 719-727
40. Sonnenschein C., Ucci A.A., and Soto A.M. Growth inhibition of estrogen-sensitive rat mammary tumors. Effect of an α-fetoprotein-secreting hepatoma. J Natl Cancer Inst 64 (1980) 1147-1152
41. Bennett J.A., Zhu S., Pagano-Mirarchi A., Kellom T.A., and Jacobson H.I. α-fetoprotein derived from a human hepatoma prevents growth of estrogen-dependent human breast cancer xenografts. Clin Cancer Res 4 (1998) 2877-2884
42. Jacobson H.I., Bennett J.A., and Mizejewski G.J. Inhibition of estrogen-dependent breast cancer growth by a reaction product of α-fetoprotein and estradiol. Cancer Res 50 (1990) 415-420
43. Bennett J.A., Semeniuk D.J., Jacobson H.I., and Murgita R.A. Similarity between natural and recombinant human α-fetoprotein as inhibitors of estrogen-dependent breast cancer growth. Breast Cancer Res Treat 45 (1997) 169-179
44. Jacobson H.I., Lemanski N., Narendran A., Agarwal A., Bennett J.A., and Andersen T.T. Hormones of pregnancy, α-feto protein, and reduction of breast cancer risk. Adv Exp Med Biol 617 (2008) 477-484
45. Murgita R.A., and Tomasi Jr. T.B. Suppression of the immune response by α-fetoprotein on the primary and secondary antibody response. J Exp Med 141 (1975) 269-286
46. Bennett J.A., Mesfin F.B., Andersen T.T., Gierthy J.F., and Jacobson H.I. A peptide derived from α-fetoprotein prevents the growth of estrogen-dependent human breast cancers sensitive and resistant to tamoxifen. Proc Natl Acad Sci U S A 99 (2002) 2211-2215
47. Joseph L.C., Bennett J.A., Kirschner K.N., Shields G.C., Hughes J., Lostritto N., et al. Antiestrogenic and anticancer activities of peptides derived from the active site of α-fetoprotein. J Pept Sci 15 (2009) 319-325
48. Mizejewski G.J., Muehlemann M., and Dauphinee M. Update of α fetoprotein growth-inhibitory peptides as biotherapeutic agents for tumor growth and metastasis. Chemotherapy 52 (2006) 83-90
49. Mesfin F.B., Bennett J.A., Jacobson H.I., Zhu S., and Andersen T.T. α-fetoprotein-derived antiestrotrophic octapeptide. Biochim Biophys Acta 1501 (2000) 33-43
50. Mesfin F.B., Andersen T.T., Jacobson H.I., Zhu S., and Bennett J.A. Development of a synthetic cyclized peptide derived from α-fetoprotein that prevents the growth of human breast cancer. J Pept Res 58 (2001) 246-256
51. DeFreest L.A., Mesfin F.B., Joseph L., McLeod D.J., Stallmer A., Reddy S., et al. Synthetic peptide derived from α-fetoprotein inhibits growth of human breast cancer: investigation of the pharmacophore and synthesis optimization. J Pept Res 63 (2004) 409-419
52. Bennett J.A., DeFreest L., Anaka I., Saadati H., Balulad S., Jacobson H.I., et al. AFPep: an anti-breast cancer peptide that is orally active. Breast Cancer Res Treat 98 (2006) 133-141
53. Parikh R.R., Gildener-Leapman N., Narendran A., Lin H.Y., Lemanski N., Bennett J.A., et al. Prevention of N-methyl-N-nitrosourea-induced breast cancer by α-fetoprotein (AFP)-derived peptide, a peptide derived from the active site of AFP. Clin Cancer Res 11 (2005) 8512-8520
54. Kuiper G.G., Enmark E., Pelto-Huikko M., Nilsson S., and Gustafsson J.A. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A 93 (1996) 5925-3
55. Kuiper G.G., and Gustafsson J.A. The novel estrogen receptor-β subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett 410 (1997) 87-90
56. Matthews J., and Gustafsson J.A. Estrogen signaling: a subtle balance between ER α and ER β. Mol Interv 3 (2003) 281-292
57. Nishihara E., Nagayama Y., Inoue S., Hiroi H., Muramatsu M., Yamashita S., et al. Ontogenetic changes in the expression of estrogen receptor α and β in rat pituitary gland detected by immunohistochemistry. Endocrinology 141 (2000) 615-620
58. Välimaa H., Savolainen S., Soukka T., Silvoniemi P., Mäkelä S., Kujari H., et al. Estrogen receptor-β is the predominant estrogen receptor subtype in human oral epithelium and salivary glands. J Endocrinol 180 (2004) 55-62
59. Hiroi H., Inoue S., Watanabe T., Goto W., Orimo A., Momoeda M., et al. Differential immunolocalization of estrogen receptor alpha and beta in rat ovary and uterus. J Mol Endocrinol 22 (1999) 37-44
60. Gustafsson J.A. What pharmacologists can learn from recent advances in estrogen signalling. Trends Pharmacol Sci 24 (2003) 479-485
61. Pfaff D.W. Cerebral implantation and autoradiographic studies of sex hormones. In: Money J. (Ed). Sex Research: New Developments (1965), Holt/Rinehart/Winston, New York 219-235
62. Pfaff D.W. Autoradiographic localization of radioactivity in rat brain after injection of tritiated sex hormones. Science 161 848 (1968 Sep 27) 1355-1356
63. Pfaff D.W. Uptake of 3H-estradiol by the female rat brain. An autoradiographic study. Endocrinology 82 (1968) 1149-1155
64. Pfaff D.W. Estrogens and brain function (1980), Springer Verlag, New York
65. Cohen R.S., and Pfaff D.W. Ultrastructure of neurons in the ventromedial nucleus or the hypothalamus in ovariectomized rats with or without estrogen treatment. Cell Tissue Res 217 (1981) 451-470
66. Osterlund M.K., Gustafsson J.A., Keller E., and Hurd Y.L. Estrogen receptor β (ERβ) messenger ribonucleic acid (mRNA) expression within the human forebrain: distinct distribution pattern to ERα mRNA. J Clin Endocrinol Metab 85 (2000) 3840-3846
67. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J Comp Neurol 388 (1997) 507-525
68. Shughrue P.J., and Merchenthaler I. Distribution of estrogen receptor β immunoreactivity in the rat central nervous system. J Comp Neurol 436 (2001) 64-81
69. Choleris E., Ogawa S., Kavaliers M., Gustafsson J.A., Korach K.S., Muglia L.J., et al. Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: a detailed behavioral analysis with knockout female mice. Genes Brain Behav 5 (2006) 528-539
70. Garey J., Goodwillie A., Frohlich J., Morgan M., Gustafsson J.A., Smithies O., et al. Genetic contributions to generalized arousal of brain and behavior. Proc Natl Acad Sci U S A 100 (2003) 11019-11022
71. Musatov S., Chen W., Pfaff D.W., Kaplitt M.G., and Ogawa S. RNAi-mediated silencing of estrogen receptor α in the ventromedial nucleus of hypothalamus abolishes female sexual behaviors. Proc Natl Acad Sci U S A 103 (2006) 10456-10460
72. Ogawa S., Chan J., Gustafsson J.A., Korach K.S., and Pfaff D.W. Estrogen increases locomotor activity in mice through estrogen receptor α: specificity for the type of activity. Endocrinology 144 (2003) 230-239
73. Clemons M., and Goss P. Estrogen and the risk of breast cancer. N Engl J Med 344 (2001) 276-285
74. Toniolo P.G., Levitz M., Zeleniuch-Jacquotte A., Banerjee S., Koenig K.L., Shore R.E., et al. A prospective study of endogenous estrogens and breast cancer in postmenopausal women. J Natl Cancer Inst 87 (1995) 190-197
75. Thomas H.V., Key T.J., Allen D.S., Moore J.W., Dowsett M., Fentiman I.S., et al. A prospective study of endogenous serum hormone concentrations and breast cancer risk in post-menopausal women on the island of Guernsey. Br J Cancer 76 (1997) 401-405
76. Cauley J.A., Lucas F.L., Kuller L.H., Stone K., Browner W., and Cummings S.R. Elevated serum estradiol and testosterone concentrations are associated with a high risk for breast cancer. Study of osteoporotic fractures research group. Ann Intern Med 130 (1999) 270-277
77. Hankinson S.E., Willet W.C., Manson J.E., Colditz G.A., Hunter D.J., Spiegelman D., et al. Plasma sex steroid hormone levels and risk of breast cancer in postmenopausal women. J Natl Cancer Inst 90 (1998) 1292-1299
78. Magnusson C., Baron J.A., Correia N., Bergstrom R., Adami H.O., and Persson I. Breast-cancer risk following long-term oestrogen- and oestrogen-progestin-replacement therapy. Int J Cancer 81 (1999) 339-344
79. Colditz G.A., Hankinson S.E., Hunter D.J., Willett W.C., Manson J.E., Stampfer M.J., et al. The use of estrogens and progestins and the risk of breast cancer in postmenopausal women. N Engl J Med 332 (1995) 1589-9
80. Walf A.A., and Frye C.A. Estradiol enhances sociosexual behavior and augments carcinogen-induced tumorigenesis in ovariectomized rats. AGE 31 (2009) 221-229
81. Walf A.A., and Frye C.A. Effects of two estradiol regimens on anxiety and depressive behaviors and trophic effects in peripheral tissues in a rodent model. Gend Med 6 (2009) 300-311
82. Sugiura H., Toyama T., Hara Y., Zhang Z., Kobayashi S., Fujii Y., et al. Expression of estrogen receptor β wild-type and its variant ERβcs/β2 is correlated with better prognosis in breast cancer. Jpn J Clin Oncol 37 (2007) 820-828
83. Frye C.A., Bayon L.E., Pursnani N.K., and Purdy R.H. The neurosteroids, progesterone and 3α, 5α-THP, enhance sexual motivation, receptivity, and proceptivity in female rats. Brain Res 808 (1998) 72-83
84. Walf A.A., and Frye C.A. A review and update of: mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior. Neuropsychopharmacology 31 (2006) 1097-1111
85. Walf A.A., and Frye C.A. ERβ-selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats. Neuropsychopharmacology 30 (2005) 1598-1609
86. Walf A.A., and Frye C.A. Rapid and estrogen receptor β mediated actions in the hippocampus mediate some functional effects of estrogen. Steroids 73 (2008) 997-1007
87. Frye C.A. The role of neurosteroids and non-genomic effects of progestins and androgens in mediating sexual receptivity of rodents. Brain Res Rev 37 (2001) 201-222
88. Frye C.A., Paris J.J., and Rhodes M.E. Engaging in paced mating, but neither exploratory, anti-anxiety, nor social behavior, increases 5α-reduced progestin concentrations in midbrain, hippocampus, striatum, and cortex. Reproduction 133 (2007) 663-674
89. Frye C.A., and Rhodes M.E. Progestin concentrations are increased following paced mating in midbrain, hippocampus, diencephalon, and cortex of rats in behavioral estrus, but only in midbrain of diestrous rats. Neuroendocrinology 83 (2006) 336-347
90. Genazzani A.R., Petraglia F., Bernardi F., Casarosa E., Salvestroni C., Tonetti A., et al. Circulating levels of allopregnanolone in humans: gender, age, and endocrine influences. J Clin Endocrinol Metab 83 (1998) 2099-2103
91. Purdy R.H., Moore Jr. P.H., Rao P.N., Hagino N., Yamaguchi T., Schmidt P., et al. Radioimmunoassay of 3α-hydroxy-5α-pregnan-20-one in rat and human plasma. Steroids 55 (1990) 290-296
92. Sundström I., and Bäckström T. Patients with premenstrual syndrome have decreased saccadic eye velocity compared to control subjects. Biol Psychiatry 44 (1998) 755-764
93. Sundström I., and Bäckström T. Citalopram increases pregnanolone sensitivity in patients with premenstrual syndrome: an open trial. Psychoneuroendocrinology 23 (1998) 73-88
94. Wangs M., Seippel L., Purdy R.H., and Bãckström T. Relationship between symptom severity and steroid variation in women with premenstrual syndrome: study on serum pregnenolone, pregnenolone sulfate, 5α-pregnane-3, 20-dione and 3α-hydroxy-5α-pregnan-20-one. J Clin Endocrinol Metab 81 (1996) 1076-1082
95. Bixo M., Andersson A., Winblad B., Purdy R.H., and Bäckström T. Progesterone, 5α-pregnane-3, 20-dione and 3α-hydroxy-5α-pregnane-20-one in specific regions of the human female brain in different endocrine states. Brain Res 764 (1997) 173-178
96. Frye C.A., and Bayon L.E. Mating stimuli influence endogenous variations in the neurosteroids 3α, 5α-THP and 3α-Diol. J Neuroendocrinol 11 (1999) 839-847
97. Frye C.A., Paris J.J., and Rhodes M.E. Engaging in paced mating, but neither exploratory, anti-anxiety, nor social behavior, increases 5α-reduced progestin concentrations in midbrain, hippocampus, striatum, and cortex. Reproduction 133 (2007) 663-674
98. Frye C.A., and Vongher J.M. Progesterone and 3α, 5α-THP enhance sexual receptivity in mice. Behav Neurosci 115 (2001) 1118-1128
99. Holzbauer M. Physiological variations in the ovarian production of 5α-pregnane derivatives with sedative properties in the rat. J Steroid Biochem 6 (1975) 1307-1310
100. Holzbauer M. Physiological aspects of steroids with anaesthetic properties. Med Biol 54 (1976) 227-242
101. Holzbauer M., Racké K., and Sharman D.F. Release of endogenous 5-hydroxytryptamine from the neural and the intermediate lobe of the rat pituitary gland evoked by electrical stimulation of the pituitary stalk. Neuroscience 15 (1985) 723-728
102. Kelsey J.L., and Gammon M.D. The epidemiology of breast cancer. CA Cancer J Clin 41 (2001) 146-165
103. Medina D. Breast cancer: the protective effect of pregnancy. Clin Cancer Res 10 (2004) 380S-384S
104. Clarke C.L., and Sutherland R.L. Progestin regulation of cellular proliferation. Endocr Rev 11 (1990) 266-301
105. Frye C.A. Progestins influence motivation, reward, conditioning, stress, and/or response to drugs of abuse. Pharmacol Biochem Behav 86 (2007) 209-219
106. Frye C.A. Neurosteroids - from basic research to clinical perspectives. In: Rubin R.T., and Pfaff D.W. (Eds). Hormones/behavior relations of clinical importance (2009), Academic Press, San Diego 395-416
107. Cheng Y.J., and Karavolas H.J. Conversion of progesterone to 5α-pregnane-3, 20-dione and 3α-hydroxy-5α-pregnan-20-one by rat medical basal hypothalami and the effects of estradiol and stage of estrous cycle on the conversion. Endocrinology 93 (1973) 1157-1162
108. Frye C.A., and Rhodes M.E. Estrogen-priming can enhance progesterone's anti-seizure effects in part by increasing hippocampal levels of allopregnanolone. Pharmacol Biochem Behav 81 (2005) 907-916
109. Vongher J.M., and Frye C.A. Progesterone in conjunction with estradiol has neuroprotective effects in an animal model of neurodegeneration. Pharmacol Biochem Behav 64 (1999) 777-785
110. Walf A.A., Rhodes M.E., and Frye C.A. Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats. Neurobiol Learn Mem 86 (2006) 35-46
111. Walf A.A., Koonce C.J., and Frye C.A. Estradiol or diarylpropionitrile decrease anxiety-like behavior of wildtype, but not estrogen receptor β knockout, mice. Behav Neurosci 122 (2008) 974-981
112. Walf A.A., Koonce C., Manley K., and Frye C.A. Proestrous compared to diestrous wildtype, but not estrogen receptor β knockout, mice have better performance in the spontaneous alternation and object recognition tasks and reduced anxiety-like behavior in the elevated plus and mirror maze. Behav Brain Res 196 (2009) 254-260
113. Walf A., Koonce C., and Frye C. Adult female wildtype, but not oestrogen receptor β knockout, mice have decreased depression-like behaviour during pro-oestrus and following administration of oestradiol or diarylpropionitrile. J Psychopharmacol 23 (2009) 442-450
114. Janowsky J.S. The role of androgens in cognition and brain aging in men. Neuroscience 138 (2006) 1015-1020
115. Janowsky J.S., Oviatt S.K., and Orwoll E.S. Testosterone influences spatial cognition in older men. Behav Neurosci 108 (1994) 325-332
116. Li J.Y., Zhu J.C., Dou J.T., Bai W.J., Deng S.M., and Li M. Effects of androgen supplementation therapy on partial androgen deficiency in the aging male: a preliminary study. Aging Male 5 (2002) 47-51
117. Alexander G.M., Swerdloff R.S., Wang C., Davidson T., McDonald V., Steiner B., et al. Androgen-behavior correlations in hypogonadal men and eugonadal men. II. Cognitive abilities. Horm Behav 33 (1998) 85-94
118. Delhez M., Hansenne M., and Legros J.J. Andropause and psychopathology: minor symptoms rather than pathological ones. Psychoneuroendocrinology 28 (2003) 863-874
119. Edinger K.L., and Frye C.A. Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5alpha-reduced metabolites in the hippocampus. Behav Neurosci 118 (2004) 1352-1364
120. Cohen M.B., and Rokhlin O.W. Mechanisms of prostate cancer cell survival after inhibition of AR expression. J Cell Biochem 106 (2009) 363-371
121. Krege J.H. Generation and reproductive phenotypes of mice lacking estrogen receptor β effects in an animal model of neurodegeneration. Pharmacol Biochem Behav 64 (1996) 777-785
122. Brown T.J., Adler G.H., Sharma M., Hochberg R.B., and MacLusky N.J. Androgen treatment decreases estrogen receptor binding in the ventromedial nucleus of the rat brain a quantitative in vitro autoradiographic analysis. Mol Cell Neurosci 5 (1994) 549-555
123. Luttge W.G. Endocrine control of mammalian male sexual behavior: an analysis of the potential role of testosterone metabolites. In: Beyer C. (Ed). Comprehensive Endocrinology. Endocrine Control of Sexual Behavior (1979), Raven Press, New York 341-364
124. Edinger K.L., and Frye C.A. Androgens effects to enhance learning and memory maybe mediated in part by actions at estrogen receptor-β in the hippocampus. Neurobiol Learn Mem 87 (2007) 78-85
125. Gee K.W. Steroid modulation of the GABA/benzodiazepine receptor-linked chloride ionophore. Mol Neurobiol 2 (1988) 291-317
126. Handa R.J., Pak T.R., Kudwa A.E., Lund T.D., and Hinds L. An alternate pathway for androgen regulation of brain function: activation of estrogen receptor β by the metabolite of dihydrotestosterone, 5α-androstane-3β, 17β-diol. Horm Behav 53 (2008) 741-752
127. Pak T.R., Chung W.C., Lund T.D., Hinds L.R., Clay C.M., and Handa R.J. The androgen metabolite, 5α-androstane-3β, 17β-diol, is a potent modulator of estrogen receptor-β1-mediated gene transcription in neuronal cells. Endocrinology 146 (2005) 147-155
128. Frye C.A., Koonce C.J., Edinger K.L., Osborne D.M., and Walf A.A. Androgens with activity at estrogen receptor β have anxiolytic and cognitive-enhancing effects in male rats and mice. Horm Behav 54 (2008) 726-734
129. Walf, A.A. Some of oestrogens' actions in the brain for affective behaviour, but not peripheral trophic effects, involve oestrogen receptor β. J Neuroendo; in revision.
130. Waters E.M., Mitterling K., Spencer J.L., Mazid S., McEwen B.S., and Milner T.A. Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus. Brain Res 1290 (2009) 1-11
131. Lee S.J., and McEwen B.S. Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications. Annu Rev Pharmacol Toxicol 41 (2001) 569-591
132. Morissette G., Couture J.P., Désormeaux A., Adam A., and Marceau F. Lack of direct interaction between enalaprilat and the kinin B1 receptors. Peptides 29 (2008) 606-612
133. Mhrye A.J., and Dorsa D.M. Estrogen acitvates rapid signalingin the brain: role of estrogen receptor α and estrogen receptor β in neurons and glia. Neuroscience 138 (2006) 851-858
134. Rønnekleiv O.K., Malyala A., and Kelly M.J. Membrane initiated signaling of estrogen in the brain. Semin Reprod Med 25 (2007) 165-177
135. Sheldahl L.C., Marriott L.K., Bryant D.M., Shapiro R.A., and Dorsa D.M. Neuroprotective efffects of estrogen and selective estrogen receptor modulators begin at the plasma membrane. Minerva Endocrinol 32 (2007) 87-94
136. Vasudevan N., and Pfaff D.W. Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front Neuroendocrinol 29 (2008) 238-257