Multiple mechanisms control brain aromatase activity at the genomic and non-genomic level

Journal of Steroid Biochemistry and Molecular Biology

Volumn 86, Issue 3-5, 2003, Pages 367-379

  Balthazart, Jacques ^a   Baillien, Michelle ^a   Charlier, Thierry D ^a   Cornil, Charlotte A ^a   Ball, Gregory F ^b  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Calcium; Estrogen synthase; Glutamate receptors; Preoptic area; Protein phosphorylations; Sexual behavior

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMINO ACID; ANDROGEN; ANDROGEN RECEPTOR; ARECAIDINE; AROMATASE; CALCIUM; DOPAMINE 1 RECEPTOR BLOCKING AGENT; DOPAMINE 2 RECEPTOR BLOCKING AGENT; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GENISTEIN; KAINIC ACID; MAGNESIUM; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; NEUROTRANSMITTER RECEPTOR; PROTEIN KINASE INHIBITOR; STAUROSPORINE; STEROID; STEROID RECEPTOR COACTIVATOR 1; THAPSIGARGIN;

AMINO ACID SEQUENCE; BEHAVIOR; BIOAVAILABILITY; BRAIN; BRAIN ELECTROPHYSIOLOGY; BRAIN HOMOGENATE; BRAIN LEVEL; CALCIUM CELL LEVEL; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CONFERENCE PAPER; DOWN REGULATION; ENZYME ACTIVITY; ESTROGEN SYNTHESIS; EXPERIMENT; EXPLANT; EXPOSURE; GENOME ANALYSIS; GENOMICS; HYPOTHALAMUS; IMMUNOPRECIPITATION; INHIBITION KINETICS; MEASUREMENT; MOLECULAR CLONING; NEUROPHYSIOLOGY; NONHUMAN; PREOPTIC AREA; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; QUAIL; REGULATORY MECHANISM; RNA ANALYSIS; SEASONAL VARIATION; SEQUENCE ANALYSIS; SEX DIFFERENCE; SEX DIFFERENTIATION; STIMULATION; TIME; WESTERN BLOTTING;

PHASIANIDAE;

EID: 0242659906     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-0760(03)00346-7     Document Type: Conference Paper

References (114)

1. Absil P., Baillien M., Ball G.F., Panzica G., Balthazart J. The control of preoptic aromatase activity by afferent inputs in Japanese quail. Brain Res. Rev. 37:2001;38-58.
2. Adkins E.K. Hormonal basis of sexual differentiation in the Japanese quail. J. Comp. Physiol. Psychol. 89:1975;61-71.
3. Adkins E.K., Boop J.J., Koutnik D.L., Morris J.B., Pniewski E.E. Further evidence that androgen aromatization is essential for the activation of copulation in male quail. Physiol. Behav. 24:1980;441-446.
4. Albert K.A., Helmer-Matyjek E., Nairn A.A., Müller T.H., Haycock J.W., Greene L.A., Goldstein M., Greengard P. Calcium/phospholipid-dependent protein kinase (protein kinase C) phosphorylates and activates tyrosine hydroxylase. Proc. Natl. Acad. Sci. U.S.A. 81:1984;7713-7717.
5. Anzick S.L., Kononen J., Walker R.L., Azorsa D.O., Tanner M.M., Guan X.Y., Sauter G., Kallioniemi O.P., Trent J.M., Meltzer P.S. AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science. 277:1997;965-968.
6. Arai S., Ogawa K., Yamachika S., Nishihara T., Nishikawa J. Cloning and functional characterization of chicken p160 coactivator family members. Biochim. Biophys. Acta. 1518:2001;7-18.
7. Aste N., Balthazart J., Absil P., Grossmann R., Mülhbauer E., Viglietti-Panzica C., Panzica G.C. Anatomical and neurochemical definition of the nucleus of the stria terminalis in Japanese quail (Coturnix japonica). J. Comp. Neurol. 396:1998;141-157.
8. Aste N., Panzica G.C., Viglietti-Panzica C., Harada N., Balthazart J. Distribution and effects of testosterone on aromatase mRNA in the quail forebrain: a non-radioactive in situ hybridization study. J. Chem. Neuroanat. 14:1998;103-115.
9. Auger A.P., Tetel M.J., McCarthy M.M. Steroid receptor coactivator-1 (SRC-1) mediates the development of sex-specific brain morphology and behavior. Proc. Natl. Acad. Sci. U.S.A. 97:2000;7551-7555.
10. Baillien M., Balthazart J. A direct dopaminergic control of aromatase activity in the quail preoptic area. J. Steroid Biochem. Mol. Biol. 63:1997;99-113.
11. J. Balthazart, Steroid metabolism and the activation of social behavior, in: J. Balthazart (Ed.), Advances in Comparative and Environmental Physiology, vol. 3, Springer-Verlag, Berlin, 1989, pp. 105-159.
12. J. Balthazart, M. Baillien, G.F. Ball, Interactions between aromatase (estrogen synthase) and dopamine in the control of male sexual behavior in quail, Comp. Biochem. Physiol. B 132 (2002) 37-55.
13. Balthazart J., Baillien M., Ball G.F. Phosphorylation processes mediate rapid changes of brain aromatase activity. J. Steroid Biochem. Mol. Biol. 79:2001;261-277.
14. Balthazart J., Baillien M., Ball G.F. Rapid and reversible inhibition of brain aromatase activity. J. Neuroendocrinol. 13:2001;63-73.
15. J. Balthazart, M. Baillien, T.D. Charlier, G.F. Ball, Calcium-dependent phosphorylation processes control brain aromatase in quail, Eur. J. Neurosci. 17 (2003) 1591-1606.
16. Balthazart J., Ball G.F. The Japanese quail as a model system for the investigation of steroid-catecholamine interactions mediating appetitive and consummatory aspects of male sexual behavior. Ann. Rev. Sex Res. 9:1998;96-176.
17. Balthazart J., Ball G.F. New insights into the regulation and function of brain estrogen synthase (aromatase). TINS. 21:1998;243-249.
18. Balthazart J., Ball G.F. Fast regulation of steroid biosynthesis: a further piece in the neurosteroid puzzle. TINS. 23:2000;57-58.
19. J. Balthazart, C. Dejace, G.C. Panzica, G.F. Ball, Rapid effects of estrogens on CREB phosphorylation in the quail brain, Soc. Neurosci. Abstr. Program No. 383.13 (2002). Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. CD-ROM.
20. Balthazart J., Foidart A. Brain aromatase and the control of male sexual behavior. J. Steroid Biochem. Mol. Biol. 44:1993;521-540.
21. Balthazart J., Foidart A., Baillien M., Harada N., Ball G.F. Anatomical relationships between aromatase and tyrosine hydroxylase in the quail brain: double-label immunocytochemical studies. J. Comp. Neurol. 391:1998;214-226.
22. Balthazart J., Foidart A., Harada N. Immunocytochemical localization of aromatase in the brain. Brain Res. 514:1990;327-333.
23. Balthazart J., Foidart A., Hendrick J.C. The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol. Behav. 47:1990;83-94.
24. Balthazart J., Foidart A., Houbart M., Prins G.S., Ball G.F. Distribution of androgen receptor-immunoreactive cells in the quail forebrain and their relationship with aromatase immunoreactivity. J. Neurobiol. 35:1998;323-340.
25. Balthazart J., Foidart A., Surlemont C., Harada N. Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors. J. Neurobiol. 22:1991;143-157.
26. Balthazart J., Schumacher M., Ottinger M.A. Sexual differences in the Japanese quail: behavior, morphology and intracellular metabolism of testosterone. Gen. Comp. Endocrinol. 51:1983;191-207.
27. Balthazart J., Stoop R., Foidart A., Harada N. Synergistic control by androgens and estrogens of aromatase in the quail brain. NeuroReport. 5:1994;1729-1732.
28. Barraclough C.A., Wise P.M. The role of catecholamines in the regulation of pituitary luteinizing hormone and follicle stimulating-hormone secretion. Endo. Rev. 3:1982;91-119.
29. G.V. Callard, Aromatization in brain and pituitary: an evolutionary perspective, in: F. Celotti, F. Naftolin, L. Martini (Eds.), Metabolism of Hormonal Steroids in the Neuroendocrine Structures, Raven Press, New York, 1984, pp. 79-102.
30. Callard G.V., Petro Z., Ryan K.J. Conversion of androgen to estrogen and other steroids in the vertebrate brain. Am. Zool. 18:1978;511-523.
31. Callard G.V., Petro Z., Ryan K.J. Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology. 103:1978;2283-2290.
32. F. Celotti, R. Massa, L. Martini, Metabolism of sex steroids in the central nervous system, in: L.J. DeGroot (Ed.), Endocrinology, Grune & Stratton, New York, 1979, pp. 41-53.
33. T.D. Charlier, G.F. Ball, J. Balthazart, Sexually-differentiated expression of the steroid receptor coactivator SRC-1 in the steroid-sensitive areas regulating sexual behavior in the quail brain, Soc. Neurosci. Abstr. (2002); Program No. 383.16. Abstract Viewer/Itinerary Planner, Society for Neuroscience, Washington, DC (CD-ROM).
34. Charlier T.D., Lakaye B., Ball G.F., Balthazart J. The steroid receptor coactivator SRC-1 exhibits a high expression in steroid-sensitive brain areas regulating reproductive behaviors in the quail brain. Neuroendocrinology. 76:2002;297-315.
35. Corbin C.J., Graham-Lorence S., McPhaul M., Mason J.I., Mendelson C.R., Simpson E.R. Isolation of a full-length cDNA insert encoding human aromatase system cytochrome P-450 and its expression in nonsteroidogenic cells. Proc. Natl. Acad. Sci. U.S.A. 85:1988;8948-8952.
36. Cornil C.A., Balthazart J., Seutin V. Electrophysiological and neurochemical characterization of neurons in the Japanese quail preoptic area. Abst. Soc. Neurosci. 27:2001;2277.
37. Cornil C.A., Foidart A., Minet A., Balthazart J. Immunocytochemical localization of ionotropic glutamate receptors subunits in the adult quail forebrain. J. Comp. Neurol. 428:2000;577-608.
38. Cornil C.A., Balthazart J., Motte P., Massotte L., Seutin V. Dopamine activates noradrenergic receptors in the preoptic area. J. Neurosci. 22:2002;9320-9330.
39. Cross E., Roselli C.E. 17beta-estradiol rapidly facilitates chemoinvestigation and mounting in castrated male rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 276:1999;R1346-R1350.
40. Daubner S.C., Lauriano C., Haycock J.W., Fitzpatrick P.F. Site-directed mutagenesis of serine 40 of rat tyrosine hydroxylase. J. Biol. Chem. 267:1992;12639-12646.
41. de Vries G.J. Sex differences in neurotransmitter systems. J. Neuroendocrinol. 2:1990;1-13.
42. Dellovade T.L., Harada N., Rissman E.F. Distribution and steroid dependence of aromatase enzyme immunoreactivity in limbic nuclei of the female musk shrew brain. Brain Res. 634:1994;141-149.
43. Foidart A., Lakaye B., Grisar T., Ball G.F., Balthazart J. Estrogen receptor-beta in quail: cloning. J. Neurobiol. 40:1999;327-342.
44. Foidart A., Reid J., Absil P., Yoshimura N., Harada N., Balthazart J. Critical re-examination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. J. Chem. Neuroanat. 8:1995;267-282.
45. Gu Q., Korach K.S., Moss R.L. Rapid action of 17beta-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors. Endocrinology. 140:1999;660-666.
46. Harada N. Cloning of a complete cDNA encoding human aromatase: immunochemical identification and sequence analysis. Biochem. Biophys. Res. Commun. 156:1988;725-732.
47. Harada N., Abe-Dohmae S., Loeffen R., Foidart A., Balthazart J. Synergism between androgens and estrogens in the induction of aromatase and its messenger RNA in the brain. Brain Res. 622:1993;243-256.
48. Harada N., Yamada K., Foidart A., Balthazart J. Regulation of aromatase cytochrome P-450 (estrogen synthetase) transcripts in the quail brain by testosterone. Mol. Brain Res. 15:1992;19-26.
49. Herbison A.E. Multimodal influence of estrogen upon gonadotropin- releasing hormone neurons. Endocr. Rev. 19:1998;302-330.
50. Hochberg Z., Bick T., Pelman R., Brandes J.M., Barzilai D. The dual effect of calcium on aromatization by cultured human trophoblast. J. Steroid Biochem. 24:1986;1217-1219.
51. Hong H., Kohli K., Garabedian M.J., Stallcup M.R. GRIP1, a transcriptional coactivator for the AF-2 transactivation domain of steroid, thyroid, retinoid, and vitamin D receptors. Mol. Cell. Biol. 17:1997;2735-2744.
52. Hutchison J.B., Steimer T., Hutchison R.E. Formation of behaviorally active estrogen in the dove brain: induction of preoptic aromatase by intracranial testosterone. Neuroendocrinology. 43:1986;416-427.
53. Hutchison J.B., Steimer T.H. Formation of behaviorally effective 17beta-estradiol in the dove brain: steroid control of preoptic aromatase. Endocrinology. 118:1986;2180-2187.
54. Jakab R.L., Horvath T.L., Leranth C., Harada N., Naftolin F. Aromatase immunoreactivity in the rat brain: gonadectomy-sensitive hypothalamic neurons and an unresponsive "limbic ring" of the lateral septum-bed nucleus-amygdala complex. J. Steroid Biochem. Mol. Biol. 44:1993;481-498.
55. Jensen E.V., Suzuki T., Kawashima T., Stumpf W.E., Jungblut P.W., DeSombre E.R. A two-step mechanism for the interaction of estradiol with rat uterus. Proc. Natl. Acad. Sci. U.S.A. 59:1968;632-638.
56. Joëls M. Steroid hormones and excitability in the mammalian brain. Front. Neuroendocrinol. 18:1997;2-48.
57. M.J. Kelly, O.K. Ronnekleiv, Rapid membrane effects of estrogen in the central nervous system, in: D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.), Hormones, Brain and Behavior, vol. 3, Academic Press, San Diego, 2002, pp. 361-380.
58. Kuiper G.G.J.M., Enmark E., Pelto-Huikko M., Nilsson S., Gustafsson J.Å. Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. U.S.A. 93:1996;5925-5930.
59. Kuiper G.G.J.M., Shughrue P.J., Merchenthaler I., Gustafsson J.-Å. The estrogen receptor b subtype: a novel mediator of estrogen action in neuroendocrine systems. Front. Neuroendocrinol. 19:1998;253-286.
60. Küppers E., Ivanova T., Karolczak M., Beyer C. Estrogen: a multifunctional messenger to nigrostriatal dopaminergic neurons. J. Neurocytol. 29:2000;375-385.
61. Lauber M.E., Lichtensteiger W. Pre- and postnatal ontogeny of aromatase cytochrome P450 messenger ribonucleic acid expression in the male rat brain studied by in situ hybridization. Endocrinology. 135:1994;1661-1668.
62. Leo C., Chen J.D. The SRC family of nuclear receptor co-activators. Gene. 245:2000;1-11.
63. Lephart E.D. A review of brain aromatase cytochrome P450. Brain Res. Rev. 22:1996;1-26.
64. Li H., Gomes P.J., Chen J.D. RAC3, a steroid/nuclear receptor-associated coactivator that is related to SRC-1 and TIF2. Proc. Natl. Acad. Sci. U.S.A. 94:1997;8479-8484.
65. Matsumine H., Herbst M.A., Ou S.-H.I., Wilson J.D., McPhaul M.J. Aromatase mRNA in the extragonadal tissues of chickens with the henny-feathering trait is derived from a distinctivepromoter structure that contains a segment of a retroviral long terminal repeat. Functional organization of the Sebright, Leghorn, and Campine aromatase genes. J. Biol. Chem. 266:1991;19900-19907.
66. McEwen B.S. Steroid hormone actions on the brain: when is the genome involved? Horm. Behav. 28:1994;396-405.
67. McEwen B.S. The molecular and neuroanatomical basis for estrogen effects in the central nervous system. J. Clin. Endocrinol. Metab. 84:1999;1790-1797.
68. McEwen B.S., Alves S.E. Estrogen actions in the central nervous system. Endocr. Rev. 20:1999;279-307.
69. McKenna N.J., Lanz R.B., O'Malley B.W. Nuclear receptor coregulators: cellular and molecular biology. Endocr. Rev. 20:1999;321-344.
70. McPhaul M.J., Noble J.F., Simpson E.R., Mendelson C.R., Wilson J.D. The expression of a functional cDNA encoding the chicken cytochrome P-450 arom (aromatase) that catalyzes the formation of estrogen from androgen. J. Biol. Chem. 263:1988;16358-16363.
71. Means G.D., Mahendroo M.S., Corbin C.J., Mathis J.M., Powell F.E., Mendelson C.R., Simpson E.R. Structural analysis of the gene encoding human aromatase cytochrome P-450, the enzyme responsible for estrogen biosynthesis. J. Biol. Chem. 264:1989;19385-19391.
72. Mermelstein P.G., Becker J.B., Surmeier D.J. Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor. J. Neurosci. 16:1996;595-604.
73. Molenda H.A., Griffin A.L., Auger A.P., McCarthy M.M., Tetel M.J. Nuclear receptor co-activators modulate hormone-dependent gene expression in brain and female reproductive behavior in rats. Endocrinology. 143:2002;436-444.
74. Moss R.L., Gu Q., Wong M. Estrogen: nontranscriptional signaling pathway. Rec. Prog. Horm. Res. 52:1997;33-69.
75. F. Naftolin, Metabolism of steroids in the brain, in: V.H.T. James (Ed.), Excerpta Medica International Congress Series, Excerpta Medica, Amsterdam, 1976, pp. 29-33.
76. Naftolin F., Horvath T.L., Balthazart J. Estrogen synthetase (aromatase) immunohistochemistry reveals concordance between avian and rodent limbic systems and hypothalami. Proc. Soc. Exp. Biol. Med. 226:2001;717-725.
77. F. Naftolin, N.J. MacLusky, Aromatization hypothesis revisited, in: M. Serio, M. Motta, M. Zanisi, L. Martini (Eds.), Sexual Differentiation: Basic and Clinical Aspects, Raven Press, New York, 1984, pp. 79-91.
78. Naftolin F., Ryan K.J., Petro Z. Aromatization of androstenedione by the anterior hypothalamus of adult male and female rats. Endocrinology. 90:1972;295-298.
79. Onagbesan O.M., Podie M.J. Calcium-dependent stimulation of estrogen secretion by FSH from theca cells of the domestic hen (Gallus domesticus). Gen. Comp. Endocrinol. 75:1989;177-186.
80. Onate S.A., Tsai S.Y., Tsai M.J., O'Malley B.W. Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science. 270:1995;1354-1357.
81. Panzica G.C., Viglietti-Panzica C., Balthazart J. The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol. 17:1996;51-125.
82. Ramirez V.D., Zheng J.B., Siddique K.M. Membrane receptors for estrogen, progesterone, and testosterone in the rat brain: fantasy or reality. Cell. Mol. Neurobiol. 16:1996;175-198.
83. Resko J.A., Pereyra-Martinez A.C., Stadelman H.L., Roselli C.E. Region-specific regulation of cytochrome P450 aromatase messenger ribonucleic acid by androgen in brains of male rhesus monkeys. Biol. Reprod. 62:2000;1818-1822.
84. Roselli C.E. Sex differences in androgen receptors and aromatase activity in microdissected regions of the rat brain. Endocrinology. 128:1991;1310-1316.
85. Roselli C.E. Synergistic induction of aromatase activity in the rat brain by estradiol and 5alpha-dihydrotestosterone. Neuroendocrinol. 53:1991;79-84.
86. Roselli C.E., Abdelgadir S.E., Resko J.A. Regulation of aromatase gene expression in the adult rat brain. Brain Res. Bull. 44:1997;351-357.
87. Roselli C.E., Abdelgadir S.E., Ronnekleiv O.K., Klosterman S.A. Anatomic distribution and regulation of aromatase gene expression in the rat brain. Biol. Reprod. 58:1998;79-87.
88. Roselli C.E., Ellinwood W.E., Resko J.A. Regulation of brain aromatase activity in rats. Endocrinology. 114:1984;192-200.
89. Roselli C.E., Horton L.E., Resko J.A. Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology. 117:1985;2471-2477.
90. Roselli C.E., Horton L.E., Resko J.A. Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area. Biol. Reprod. 37:1987;628-633.
91. Roselli C.E., Klosterman S.A. Sexual differentiation of aromatase activity in the rat brain: effects of perinatal steroid exposure. Endocrinology. 139:1998;3193-3201.
92. Roselli C.E., Stormshak F., Resko J.A. Distribution of aromatase mRNA in the ram hypothalamus: an in situ hybridization study. J. Neuroendocrinol. 12:2000;656-664.
93. Saldanha C.J., Tuerk M.J., Kim Y.H., Fernandes A.O., Arnold A.P., Schlinger B.A. Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J. Comp. Neurol. 423:2000;619-630.
94. Sanghera M.K., Simpson E.R., McPhaul M.J., Kozlowski G., Conley A.J., Lephart E.D. 5α-and 5 β-reductase Immunocytochemical distribution of aromatase cytochrome P450 in the rat brain using peptide-generated polyclonal antibodies. Endocrinology. 129:1991;2834-2844.
95. Schlinger B.A., Callard G.V. A comparison of aromatase (Coturnix c. japonica). J. Exp. Zool. 242:1987;171-180.
96. Schumacher M., Alexandre C., Balthazart J. Interactions des androgènes et des oestrogènes dans le contrôle de la reproduction. C. R. Acad. Sci. Paris, Ser. III. 305:1987;569-574.
97. Schumacher M., Balthazart J. Testosterone-induced brain aromatase is sexually dimorphic. Brain Res. 370:1986;285-293.
98. Schumacher M., Balthazart J. Neuroanatomical distribution of testosterone metabolizing enzymes in the Japanese quail. Brain Res. 422:1987;137-148.
99. Shen P., Campagnoni C.W., Kampf K., Schlinger B.A., Arnold A.P., Campagnoni A.T. Isolation and characterization of a zebra finch aromatase cDNA: in situ hybridization reveals high aromatase expression in brain. Mol. Brain Res. 24:1994;227-237.
100. Shen P., Schlinger B.A., Campagnoni A.T., Arnold A.P. An atlas of aromatase mRNA expression in the zebra finch brain. J. Comp. Neurol. 360:1995;172-184.
101. Simpson E.R., Mahendroo M.S., Means G.D., Kilgore M.W., Hinshelwood M.M., Graham-Lorence S., Amarneh B., Ito Y., Fisher C.R., Michael M.D., Mendelson C.R., Bulun S.E. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr. Rev. 15:1994;342-355.
102. Steimer T., Hutchison J.B. Androgen increases formation of behaviourally effective oestrogen in dove brain. Nature. 292:1981;345-347.
103. T. Steimer, J.B. Hutchison, Micromethods for the in vitro study of steroid metabolism in the brain using radiolabelled tracers, in: B. Greenstein (Ed.), Neuroendocrine Research Methods, vol. 2, Harwood, Chur, Switzerland, 1991, pp. 875-919.
104. Takeshita A., Cardona G.R., Koibuchi N., Suen C.S., Chin W.W. TRAM-1, A novel 160-kDa thyroid hormone receptor activator molecule, exhibits distinct properties from steroid receptor coactivator-1. J. Biol. Chem. 272:1997;27629-27634.
105. Terashima M., Toda K., Kawamoto T., Kuribayashi I., Ogawa Y., Maeda T., Shizuta Y. Isolation of a full-length cDNA encoding mouse aromatase P450. Arch. Biochem. Biophys. 285:1991;231-237.
106. Tsuruo Y., Ishimura K., Hayashi S., Osawa Y. Immunohistochemical localization of estrogen receptors within aromatase-immunoreactive neurons in the fetal and neonatal rat brain. Anat. Embryol. (Berl.). 193:1996;115-121.
107. Tsuruo Y., Ishimura K., Osawa Y. Presence of estrogen receptors in aromatase-immunoreactive neurons in the mouse brain. Neurosci. Lett. 195:1995;49-52.
108. Vockel A., Pröve E., Balthazart J. Effects of castration and testosterone treatment on the activity of testosterone-metabolizing enzymes in the brain of male and female zebra finches. J. Neurobiol. 21:1990;808-825.
109. Voegel J.J., Heine M.J., Zechel C., Chambon P., Gronemeyer H. TIF2, a 160. kDa transcriptional mediator for the ligand-dependent activation function AF-2 of nuclear receptors Embo. J. 15:1996;3667-3675.
110. C.K. Wagner, J.I. Morrell, The distribution and steroid hormone regulation of aromatase mRNA expression in the brains of adult male and female rats: a cellular level analysis using in situ hybridization, J. Comp. Neurol. 370 (1996) 71-84.
111. Walters M.R. Steroid hormone receptors and the nucleus. Endocr. Rev. 6:1985;512-543.
112. R.I. Weiner, P.R. Findell, C. Kordon, Role of classic and peptide neuromediators in the neuroendocrine regulation of LH and prolactin, in: E. Knobil, J. Neill, et al. (Eds.), The Physiology of Reproduction, Raven Press, New York, 1988, pp. 1235-1281.
113. Xu J., Liao L., Ning G., Yoshida-Komiya H., Deng C., O'Malley B.W. The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/TRAM-1) is required for normal growth, puberty, female reproductive function, and mammary gland development. Proc. Natl. Acad. Sci. U.S.A. 97:2000;6379-6384.
114. Zhou Y., Watters J.J., Dorsa D.M. Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain. Endocrinology. 137:1996;2163-2166.