Estrogen synthase; Preoptic area; Sexual Behavior; Protein phosphorylations; Calcium; Glutamate receptors
Abstract :
[en] Evidence has recently accumulated indicating that aromatase activity in the preoptic area is modulated in parallel by both slow (hours to days) genomic and rapid (minutes to hours) non-genomic mechanisms. We review here these two types of control mechanisms and their potential contribution to various aspects of brain physiology in quail. High levels of aromatase mRNA, protein and activity (AA) are present in the preoptic area of this species where the transcription of aromatase is controlled mainly by steroids. Estrogens acting in synergy with androgens play a key role in this control and both androgen and estrogen receptors (ER; alpha and beta subtypes) are present in the preoptic area even if they are not necessarily co-localized in the same cells as aromatase. Steroids have more pronounced effects on aromatase transcription in males than in females and this sex difference could be caused, in part, by a sexually differentiated expression of the steroid receptor coactivator 1 in this area. The changes in aromatase concentration presumably control seasonal variations as well as sex differences in brain estrogen production. Aromatase activity in hypothalamic homogenates is also rapidly (within minutes) down-regulated by exposure to conditions that enhance protein phosphorylation such as the presence of high concentrations of calcium, magnesium and ATP. Similarly, pharmacological manipulations such as treatment with thapsigargin or stimulation of various neurotransmitter receptors (alpha-amino-3-hydroxy-methyl-4-isoxazole propionic acid (AMPA), kainate, and N-methyl-d-aspartate (NMDA)) leading to enhanced intracellular calcium concentrations depress within minutes the aromatase activity measured in quail preoptic explants. The effects of receptor stimulation are presumably direct: electrophysiological data confirm the presence of these receptors in the membrane of aromatase-expressing cells. Inhibitors of protein kinases interfere with these processes andWestern blotting experiments on brain aromatase purified by immunoprecipitation confirm that the phosphorylations regulating aromatase activity directly affect the enzyme rather than another regulatory protein. Accordingly, several phosphorylation consensus sites are present on the deduced amino acid sequence of the recently cloned quail aromatase. Fast changes in the local availability of estrogens in the brain can thus be caused by aromatase phosphorylation so that estrogen could rapidly regulate neuronal physiology and behavior. The rapid as well as slower processes of local estrogen production in the brain thus match well with the genomic and non-genomic actions of steroids in the brain. These two processes potentially provide sufficient temporal variation in the bio-availability of estrogens to support the entire range of established effects for this steroid.
Research Center/Unit :
Centre de Neurobiologie Cellulaire et Moléculaire Departement of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, USA
Disciplines :
Neurosciences & behavior
Author, co-author :
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Baillien, Michelle
Charlier, Thierry ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Ball, Gregory
Language :
English
Title :
Multiple mechanisms control brain aromatase activity at the genomic and non-genomic level
Publication date :
2003
Journal title :
Journal of Steroid Biochemistry and Molecular Biology
ISSN :
0960-0760
eISSN :
1879-1220
Publisher :
Pergamon Press, Oxford, United Kingdom
Volume :
86
Pages :
367-379
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NIH - National Institutes of Health FWB - Fédération Wallonie-Bruxelles ULg FSR - Université de Liège. Fonds spéciaux pour la recherche FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture F.R.S.-FNRS - Fonds de la Recherche Scientifique
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Bibliography
Absil, P., Baillien, M., Ball, G.F., Panzica, G., Balthazart, J., The control of preoptic aromatase activity by afferent inputs in Japanese quail (2001) Brain Res. Rev., 37, pp. 38-58
Adkins, E.K., Hormonal basis of sexual differentiation in the Japanese quail (1975) J. Comp. Physiol. Psychol., 89, pp. 61-71
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 (1980) Physiol. Behav., 24, pp. 441-446
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 (1984) Proc. Natl. Acad. Sci. U.S.A., 81, pp. 7713-7717
Anzick, S.L., Kononen, J., Walker, R.L., Azorsa, D.O., Tanner, M.M., Guan, X.Y., Sauter, G., Meltzer, P.S., AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer (1997) Science, 277, pp. 965-968
Arai, S., Ogawa, K., Yamachika, S., Nishihara, T., Nishikawa, J., Cloning and functional characterization of chicken p160 coactivator family members (2001) Biochim. Biophys. Acta, 1518, pp. 7-18
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) (1998) J. Comp. Neurol., 396, pp. 141-157
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 (1998) J. Chem. Neuroanat., 14, pp. 103-115
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 (2000) Proc. Natl. Acad. Sci. U.S.A., 97, pp. 7551-7555
Baillien, M., Balthazart, J., A direct dopaminergic control of aromatase activity in the quail preoptic area (1997) J. Steroid Biochem. Mol. Biol., 63, pp. 99-113
Balthazart, J., Steroid metabolism and the activation of social behavior (1989) Advances in Comparative and Environmental Physiology, 3, pp. 105-159. , J. Balthazart (Ed.), Springer-Verlag, Berlin
Balthazart, J., Baillien, M., Ball, G.F., Interactions between aromatase (estrogen synthase) and dopamine in the control of male sexual behavior in quail (2002) Comp. Biochem. Physiol. B, 132, pp. 37-55
Balthazart, J., Baillien, M., Ball, G.F., Phosphorylation processes mediate rapid changes of brain aromatase activity (2001) J. Steroid Biochem. Mol. Biol., 79, pp. 261-277
Balthazart, J., Baillien, M., Ball, G.F., Rapid and reversible inhibition of brain aromatase activity (2001) J. Neuroendocrinol., 13, pp. 63-73
Balthazart, J., Baillien, M., Charlier, T.D., Ball, G.F., Calcium-dependent phosphorylation processes control brain aromatase in quail (2003) Eur. J. Neurosci., 17, pp. 1591-1606
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 (1998) Ann. Rev. Sex Res., 9, pp. 96-176
Balthazart, J., Ball, G.F., New insights into the regulation and function of brain estrogen synthase (aromatase) (1998) TINS, 21, pp. 243-249
Balthazart, J., Ball, G.F., Fast regulation of steroid biosynthesis: A further piece in the neurosteroid puzzle (2000) TINS, 23, pp. 57-58
Balthazart, J., Dejace, C., Panzica, G.C., Ball, G.F., Rapid effects of estrogens on CREB phosphorylation in the quail brain (2002) Soc. Neurosci. Abstr. Program No. 383.13, , Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. CD-ROM
Balthazart, J., Foidart, A., Brain aromatase and the control of male sexual behavior (1993) J. Steroid Biochem. Mol. Biol., 44, pp. 521-540
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 (1998) J. Comp. Neurol., 391, pp. 214-226
Balthazart, J., Foidart, A., Harada, N., Immunocytochemical localization of aromatase in the brain (1990) Brain Res., 514, pp. 327-333
Balthazart, J., Foidart, A., Hendrick, J.C., The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior (1990) Physiol. Behav., 47, pp. 83-94
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 (1998) J. Neurobiol., 35, pp. 323-340
Balthazart, J., Foidart, A., Surlemont, C., Harada, N., Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors (1991) J. Neurobiol., 22, pp. 143-157
Balthazart, J., Schumacher, M., Ottinger, M.A., Sexual differences in the Japanese quail: Behavior, morphology and intracellular metabolism of testosterone (1983) Gen. Comp. Endocrinol., 51, pp. 191-207
Balthazart, J., Stoop, R., Foidart, A., Harada, N., Synergistic control by androgens and estrogens of aromatase in the quail brain (1994) NeuroReport, 5, pp. 1729-1732
Barraclough, C.A., Wise, P.M., The role of catecholamines in the regulation of pituitary luteinizing hormone and follicle stimulating-hormone secretion (1982) Endo. Rev., 3, pp. 91-119
Callard, G.V., Aromatization in brain and pituitary: An evolutionary perspective (1984) Metabolism of Hormonal Steroids in the Neuroendocrine Structures, pp. 79-102. , F. Celotti, F. Naftolin, L. Martini (Eds.), Raven Press, New York
Callard, G.V., Petro, Z., Ryan, K.J., Conversion of androgen to estrogen and other steroids in the vertebrate brain (1978) Am. Zool., 18, pp. 511-523
Callard, G.V., Petro, Z., Ryan, K.J., Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system (1978) Endocrinology, 103, pp. 2283-2290
Celotti, F., Massa, R., Martini, L., Metabolism of sex steroids in the central nervous system (1979) Endocrinology, pp. 41-53. , L.J. DeGroot (Ed.), Grune & Stratton, New York
Charlier, T.D., Ball, G.F., Balthazart, J., Sexually-differentiated expression of the steroid receptor coactivator SRC-1 in the steroid-sensitive areas regulating sexual behavior in the quail brain (2002) Soc. Neurosci. Abstr., , Program No. 383.16. Abstract Viewer/Itinerary Planner, Society for Neuroscience, Washington, DC (CD-ROM)
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 (2002) Neuroendocrinology, 76, pp. 297-315
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 (1988) Proc. Natl. Acad. Sci. U.S.A., 85, pp. 8948-8952
Cornil, C.A., Balthazart, J., Seutin, V., Electrophysiological and neurochemical characterization of neurons in the Japanese quail preoptic area (2001) Abst. Soc. Neurosci., 27, p. 2277
Cornil, C.A., Foidart, A., Minet, A., Balthazart, J., Immunocytochemical localization of ionotropic glutamate receptors subunits in the adult quail forebrain (2000) J. Comp. Neurol., 428, pp. 577-608
Cornil, C.A., Balthazart, J., Motte, P., Massotte, L., Seutin, V., Dopamine activates noradrenergic receptors in the preoptic area (2002) J. Neurosci., 22, pp. 9320-9330
Cross, E., Roselli, C.E., 17beta-estradiol rapidly facilitates chemoinvestigation and mounting in castrated male rats (1999) Am. J. Physiol. Regul. Integr. Comp. Physiol., 276, pp. 1346-R1350
Daubner, S.C., Lauriano, C., Haycock, J.W., Fitzpatrick, P.F., Site-directed mutagenesis of serine 40 of rat tyrosine hydroxylase (1992) J. Biol. Chem., 267, pp. 12639-12646
De Vries, G.J., Sex differences in neurotransmitter systems (1990) J. Neuroendocrinol., 2, pp. 1-13
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 (1994) Brain Res., 634, pp. 141-149
Foidart, A., Lakaye, B., Grisar, T., Ball, G.F., Balthazart, J., Estrogen receptor-beta in quail: Cloning (1999) J. Neurobiol., 40, pp. 327-342
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 (1995) J. Chem. Neuroanat., 8, pp. 267-282
Gu, Q., Korach, K.S., Moss, R.L., Rapid action of 17beta-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors (1999) Endocrinology, 140, pp. 660-666
Harada, N., Cloning of a complete cDNA encoding human aromatase: Immunochemical identification and sequence analysis (1988) Biochem. Biophys. Res. Commun., 156, pp. 725-732
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 (1993) Brain Res., 622, pp. 243-256
Harada, N., Yamada, K., Foidart, A., Balthazart, J., Regulation of aromatase cytochrome P-450 (estrogen synthetase) transcripts in the quail brain by testosterone (1992) Mol. Brain Res., 15, pp. 19-26
Herbison, A.E., Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons (1998) Endocr. Rev., 19, pp. 302-330
Hochberg, Z., Bick, T., Pelman, R., Brandes, J.M., Barzilai, D., The dual effect of calcium on aromatization by cultured human trophoblast (1986) J. Steroid Biochem., 24, pp. 1217-1219
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 (1997) Mol. Cell. Biol., 17, pp. 2735-2744
Hutchison, J.B., Steimer, T., Hutchison, R.E., Formation of behaviorally active estrogen in the dove brain: Induction of preoptic aromatase by intracranial testosterone (1986) Neuroendocrinology, 43, pp. 416-427
Hutchison, J.B., Steimer, T.H., Formation of behaviorally effective 17beta-estradiol in the dove brain: Steroid control of preoptic aromatase (1986) Endocrinology, 118, pp. 2180-2187
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 (1993) J. Steroid Biochem. Mol. Biol., 44, pp. 481-498
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 (1968) Proc. Natl. Acad. Sci. U.S.A., 59, pp. 632-638
Joëls, M., Steroid hormones and excitability in the mammalian brain (1997) Front. Neuroendocrinol., 18, pp. 2-48
Kelly, M.J., Ronnekleiv, O.K., Rapid membrane effects of estrogen in the central nervous system (2002) Hormones, Brain and Behavior, 3, pp. 361-380. , D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.), Academic Press, San Diego
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 (1996) Proc. Natl. Acad. Sci. U.S.A., 93, pp. 5925-5930
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 (1998) Front. Neuroendocrinol., 19, pp. 253-286
Küppers, E., Ivanova, T., Karolczak, M., Beyer, C., Estrogen: A multifunctional messenger to nigrostriatal dopaminergic neurons (2000) J. Neurocytol., 29, pp. 375-385
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 (1994) Endocrinology, 135, pp. 1661-1668
Leo, C., Chen, J.D., The SRC family of nuclear receptor co-activators (2000) Gene, 245, pp. 1-11
Lephart, E.D., A review of brain aromatase cytochrome P450 (1996) Brain Res. Rev., 22, pp. 1-26
Li, H., Gomes, P.J., Chen, J.D., RAC3, a steroid/nuclear receptor-associated coactivator that is related to SRC-1 and TIF2 (1997) Proc. Natl. Acad. Sci. U.S.A., 94, pp. 8479-8484
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 (1991) J. Biol. Chem., 266, pp. 19900-19907
Mcewen, B.S., Steroid hormone actions on the brain: When is the genome involved? (1994) Horm. Behav., 28, pp. 396-405
Mcewen, B.S., The molecular and neuroanatomical basis for estrogen effects in the central nervous system (1999) J. Clin. Endocrinol. Metab., 84, pp. 1790-1797
Mcewen, B.S., Alves, S.E., Estrogen actions in the central nervous system (1999) Endocr. Rev., 20, pp. 279-307
Mckenna, N.J., Lanz, R.B., O'malley, B.W., Nuclear receptor coregulators: Cellular and molecular biology (1999) Endocr. Rev., 20, pp. 321-344
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 (1988) J. Biol. Chem., 263, pp. 16358-16363
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 (1989) J. Biol. Chem., 264, pp. 19385-19391
Mermelstein, P.G., Becker, J.B., Surmeier, D.J., Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor (1996) J. Neurosci., 16, pp. 595-604
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 (2002) Endocrinology, 143, pp. 436-444
Moss, R.L., Gu, Q., Wong, M., Estrogen: Nontranscriptional signaling pathway (1997) Rec. Prog. Horm. Res., 52, pp. 33-69
Naftolin, F., Metabolism of steroids in the brain (1976) Excerpta Medica International Congress Series, pp. 29-33. , V.H.T. James (Ed.), Excerpta Medica, Amsterdam
Naftolin, F., Horvath, T.L., Balthazart, J., Estrogen synthetase (aromatase) immunohistochemistry reveals concordance between avian and rodent limbic systems and hypothalami (2001) Proc. Soc. Exp. Biol. Med., 226, pp. 717-725
Naftolin, F., MacLusky, N.J., Aromatization hypothesis revisited (1984) Sexual Differentiation: Basic and Clinical Aspects, pp. 79-91. , M. Serio, M. Motta, M. Zanisi, L. Martini (Eds.), Raven Press, New York, 1984, pp. 79-91
Naftolin, F., Ryan, K.J., Petro, Z., Aromatization of androstenedione by the anterior hypothalamus of adult male and female rats (1972) Endocrinology, 90, pp. 295-298
Onagbesan, O.M., Podie, M.J., Calcium-dependent stimulation of estrogen secretion by FSH from theca cells of the domestic hen (Gallus domesticus) (1989) Gen. Comp. Endocrinol., 75, pp. 177-186
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 (1995) Science, 270, pp. 1354-1357
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 (1996) Front. Neuroendocrinol., 17, pp. 51-125
Ramirez, V.D., Zheng, J.B., Siddique, K.M., Membrane receptors for estrogen, progesterone, and testosterone in the rat brain: Fantasy or reality (1996) Cell. Mol. Neurobiol., 16, pp. 175-198
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 (2000) Biol. Reprod., 62, pp. 1818-1822
Roselli, C.E., Sex differences in androgen receptors and aromatase activity in microdissected regions of the rat brain (1991) Endocrinology, 128, pp. 1310-1316
Roselli, C.E., Synergistic induction of aromatase activity in the rat brain by estradiol and 5alpha-dihydrotestosterone (1991) Neuroendocrinol., 53, pp. 79-84
Roselli, C.E., Abdelgadir, S.E., Resko, J.A., Regulation of aromatase gene expression in the adult rat brain (1997) Brain Res. Bull., 44, pp. 351-357
Roselli, C.E., Abdelgadir, S.E., Ronnekleiv, O.K., Klosterman, S.A., Anatomic distribution and regulation of aromatase gene expression in the rat brain (1998) Biol. Reprod., 58, pp. 79-87
Roselli, C.E., Ellinwood, W.E., Resko, J.A., Regulation of brain aromatase activity in rats (1984) Endocrinology, 114, pp. 192-200
Roselli, C.E., Horton, L.E., Resko, J.A., Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system (1985) Endocrinology, 117, pp. 2471-2477
Roselli, C.E., Horton, L.E., Resko, J.A., Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area (1987) Biol. Reprod., 37, pp. 628-633
Roselli, C.E., Klosterman, S.A., Sexual differentiation of aromatase activity in the rat brain: Effects of perinatal steroid exposure (1998) Endocrinology, 139, pp. 3193-3201
Roselli, C.E., Stormshak, F., Resko, J.A., Distribution of aromatase mRNA in the ram hypothalamus: An in situ hybridization study (2000) J. Neuroendocrinol., 12, pp. 656-664
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 (2000) J. Comp. Neurol., 423, pp. 619-630
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 (1991) Endocrinology, 129, pp. 2834-2844
Schlinger, B.A., Callard, G.V., A comparison of aromatase (Coturnix c. japonica) (1987) J. Exp. Zool., 242, pp. 171-180
Schumacher, M., Alexandre, C., Balthazart, J., Interactions des androgènes et des oestrogènes dans le contrôle de la reproduction (1987) C. R. Acad. Sci. Paris, Ser. III, 305, pp. 569-574
Schumacher, M., Balthazart, J., Testosterone-induced brain aromatase is sexually dimorphic (1986) Brain Res., 370, pp. 285-293
Schumacher, M., Balthazart, J., Neuroanatomical distribution of testosterone metabolizing enzymes in the Japanese quail (1987) Brain Res., 422, pp. 137-148
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 (1994) Mol. Brain Res., 24, pp. 227-237
Shen, P., Schlinger, B.A., Campagnoni, A.T., Arnold, A.P., An atlas of aromatase mRNA expression in the zebra finch brain (1995) J. Comp. Neurol., 360, pp. 172-184
Steimer, T., Hutchison, J.B., Androgen increases formation of behaviourally effective oestrogen in dove brain (1981) Nature, 292, pp. 345-347
Steimer, T., Hutchison, J.B., Micromethods for the in vitro study of steroid metabolism in the brain using radiolabelled tracers (1991) Neuroendocrine Research Methods, 2, pp. 875-919. , B. Greenstein (Ed.), Harwood, Chur, Switzerland
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 (1997) J. Biol. Chem., 272, pp. 27629-27634
Terashima, M., Toda, K., Kawamoto, T., Kuribayashi, I., Ogawa, Y., Maeda, T., Shizuta, Y., Isolation of a full-length cDNA encoding mouse aromatase P450 (1991) Arch. Biochem. Biophys., 285, pp. 231-237
Tsuruo, Y., Ishimura, K., Hayashi, S., Osawa, Y., Immunohistochemical localization of estrogen receptors within aromatase-immunoreactive neurons in the fetal and neonatal rat brain (1996) Anat. Embryol. (Berl.), 193, pp. 115-121
Tsuruo, Y., Ishimura, K., Osawa, Y., Presence of estrogen receptors in aromatase-immunoreactive neurons in the mouse brain (1995) Neurosci. Lett., 195, pp. 49-52
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 (1990) J. Neurobiol., 21, pp. 808-825
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 (1996) Embo. J., 15, pp. 3667-3675
Wagner, C.K., Morrell, J.I., 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 (1996) J. Comp. Neurol., 370, pp. 71-84
Walters, M.R., Steroid hormone receptors and the nucleus (1985) Endocr. Rev., 6, pp. 512-543
Weiner, R.I., Findell, P.R., Kordon, C., Role of classic and peptide neuromediators in the neuroendocrine regulation of LH and prolactin (1988) The Physiology of Reproduction, pp. 1235-1281. , E. Knobil, J. Neill, et al. (Eds.), Raven Press, New York
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 (2000) Proc. Natl. Acad. Sci. U.S.A., 97, pp. 6379-6384
Zhou, Y., Watters, J.J., Dorsa, D.M., Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain (1996) Endocrinology, 137, pp. 2163-2166
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