[en] Traditionally, the production and regulation of steroid hormones has been viewed as a multi-organ process involving the hypothalamic-pituitary-gonadal (HPG) axis for sex steroids and the hypothalamic-pituitary-adrenal (HPA) axis for glucocorticoids. However, active steroids can also be synthesized locally in target tissues, either from circulating inactive precursors or de novo from cholesterol. Here, we review recent work demonstrating local steroid synthesis, with an emphasis on steroids synthesized in the brain (neurosteroids) and steroids synthesized in the immune system (immunosteroids). Furthermore, recent evidence suggests that other components of the HPG axis (luteinizing hormone and gonadotropin-releasing hormone) and HPA axis (adrenocorticotropic hormone and corticotropin-releasing hormone) are expressed locally in target tissues, potentially providing a mechanism for local regulation of neurosteroid and immunosteroid synthesis. The balance between systemic and local steroid signals depends critically on life history stage, species adaptations, and the costs of systemic signals. During particular life history stages, there can be a shift from systemic to local steroid signals. We propose that the shift to local synthesis and regulation of steroids within target tissues represents a "Balkanization" of the endocrine system, whereby individual tissues and organs may become capable of autonomously synthesizing and modulating local steroid signals, perhaps independently of the HPG and HPA axes.
Charlier, Thierry ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Chin, Eunice H
Soma, Kiran K
Language :
English
Title :
Neurosteroids, immunosteroids, and the Balkanization of endocrinology.
Abdou N.I., and Abdou N.L. Bone marrow: the bursa equivalent in man?. Science 175 (1972) 446-448
Aird F., Clevenger C.V., Prystowsky M.B., and Redei E. Corticotropin-releasing factor mRNA in rat thymus and spleen. Proc. Natl. Acad. Sci. USA 90 (1993) 7104-7108
Balthazart J., and Ball G.F. Fast regulation of steroid biosynthesis: a further piece in the neurosteroid puzzle. Trends Neurosci. 23 (2000) 57-58
Balthazart J., and Ball G.F. Is brain estradiol a hormone or a neurotransmitter?. Trends Neurosci. 29 (2006) 241-249
Bentley G.E., Moore I.E., Sower S.A., and Wingfield J.C. Evidence for a novel gonadotropin-releasing hormone in hypothalamic and forebrain areas in songbirds. Brain Behav. Evol. 63 (2004) 34-46
Blalock J.E., and Smith E.M. Human leukocyte interferon: structural and biological relatedness to adrenocorticotrophic hormone and endorphins. Proc. Natl. Acad. Sci. USA 77 (1980) 5972-5974
Borlak J., Schulte I., and Thum T. Androgen metabolism in the thymus of fetal and adult rats. Drug Metab. Dispos. 32 (2004) 675-679
Breuner C.W., and Orchinik M. Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175 (2002) 99-112
Bruscoli S., Di Virgilio R., Donato V., Velardi E., Baldoni M., Marchetti C., Migliorati G., and Riccardi C. Genomic and non-genomic effects of different glucocorticoids on mouse thymocyte apoptosis. Eur. J. Pharmacol. 529 (2006) 63-70
Butte J.C., Kakihana R., Farnham M.L., and Noble E.P. The relationship between brain and plasma corticosterone stress response in developing rats. Endocrinology 92 (1973) 1775-1779
Butte J.C., Kakihana R., and Noble E.P. Rat and mouse brain corticosterone. Endocrinology 90 (1972) 1091-1100
Buttgereit F., and Scheffold A. Rapid glucocorticoid effects on immune cells. Steroids 67 (2002) 529-534
Caldwell J.D., Shapiro R.A., Jirikowski G.F., and Suleman F. Internalization of sex hormone-binding globulin into neurons and brain cells in vitro and in vivo. Neuroendocrinology 86 (2007) 84-93
Campbell R.K., Satoh N., and Degnan M. Piecing together evolution of the vertebrate endocrine system. Trends Genet. 20 (2004) 359-366
Cascio C., Russo D., Drago G., Galizzi G., Passantino R., Guarneri R., and Guarneri P. 17β-Estradiol synthesis in the adult male rat retina. Exp. Eye Res. 85 (2007) 166-172
Casey M.L., and MacDonald P.C. Demonstration of steroid 17α-hydroxylase activity in human fetal kidney, thymus, and spleen. Steroids 40 (1982) 91-97
Casey M.L., Winkel C.A., and MacDonald P.C. Conversion of progesterone to deoxycorticosterone in the human fetus: steroid 21-hydroxylase activity in fetal tissues. J. Steroid Biochem. 18 (1983) 449-452
Celotti F., Melcangi R., and Martini L. The 5alpha-reductase in the brain: molecular aspects and relation to brain function. Front. Neuroendocrinol. 13 (1992) 163-215
Chan S.W., and Phillips J.G. Secretion of 17-deoxycorticosteroids by herring gull (Larus argentatus) adrenals. Gen. Comp. Endocrinol. 20 (1973) 274-282
Chin, E.H., Shah, A.H., Schmidt, K.L., Sheldon, L.D., Love, O.P., Soma, K.K., in press. Sex differences in DHEA and estradiol during development in a wild songbird: jugular versus brachial plasma. Horm. Behav.
Cima I., Corazza N., Dick B., Fuhrer A., Herren S., Jakob S., Ayuni E., Mueller C., and Brunner T. Intestinal epithelial cells synthesize glucocorticoids and regulate T cell activation. J. Exp. Med. 200 (2004) 1635-1646
Compagnone N.A., and Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinol. 21 (2000) 1-56
Cooper M.D., Peterson R.D.A., South M.A., and Good R.A. The functions of the thymus system and the bursa system in the chicken. J. Exp. Med. 176 (1966) 6370-6404
Cornil C.A., Ball G.F., and Balthazart J. Significance of the rapid regulation of brain estrogen action: Where do the estrogens come from?. Brain Res. 1126 (2006) 2-6
Corpechot C., Robel P., Axelson M., Sjovall J., and Baulieu E.E. Characterization and measurement of dehydroepiandrosterone sulfate in the rat brain. Proc. Natl. Acad. Sci. USA 78 (1981) 4704-4707
Demas G.E., Cooper M.A., Albers H.E., and Soma K.K. Novel mechanisms underlying neuroendocrine regulation of aggression: a synthesis of rodent, avian, and primate studies. In: Blaustein J.D. (Ed). Behavioral Neurochemistry and Neuroendocrinology. In: Lathja A. (Ed). Handbook of Neurochemistry and Molecular Neurobiology vol. 21 (2007), Springer, Berlin, Germany 337-372
Fargallo J.A., Martinez-Padilla J., Toledano-Diaz A., Santiago-Moreno J., and Davila J.A. Sex and testosterone effects on growth, immunity and melanin coloration of nestling Eurasian kestrels. J. Anim. Ecol. 76 (2007) 201-209
Glick B., Chang T.S., and Jaap R.G. The bursa of Fabricius and antibody production. Poult. Sci. 35 (1956) 224-234
Goodson J.L., Evans A.K., and Soma K.K. Neural responses to aggressive challenge correlate with behavior in nonbreeding sparrows. Neuroreport 16 (2005) 1719-1723
Goodson J.L., Saldanha C.J., Hahn T.P., and Soma K.K. Recent advances in behavioral neuroendocrinology: insights from studies on birds. Horm. Behav. 48 (2005) 461-473
Groothuis T.G.G., and Ros A.F.H. The hormonal control of begging and early aggressive behavior: experiments in black-headed gull chicks. Horm. Behav. 48 (2005) 207-215
Guillemin R. Peptides in the brain: the new endocrinology of the neuron. Science 202 (1978) 390-402
Haltmeyer G.C., Denenberg V.H., Thatcher J., and Zarrow M.X. Response of the adrenal cortex of the neonatal rat after subjection to stress. Nature 212 (1966) 1371-1373
Hammond G.L., Smith C.L., Patterson N.A., and Sibbald W.J. A role for corticosteroid-binding globulin in delivery of cortisol to activated neutrophils. J. Clin. Endocrinol. Metab. 71 (1990) 34-39
Hau M. Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays 29 (2007) 133-144
Hau M., Stoddart S.T., and Soma K.K. Territorial aggression and hormones during the non-breeding season in a tropical bird. Horm. Behav. 45 (2004) 40-49
Hayward L.S., and Wingfield J.C. Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen. Comp. Endocrinol. 135 (2004) 365-371
Hennebold J.D., Ryu S.Y., Mu H.H., Galbraith A., and Daynes R.A. 11β-hydroxysteroid dehydrogenase modulation of glucocorticoid activities in lymphoid organs. Am. J. Physiol. Reg. Integ. Comp. Physiol. 270 (1996) 1296-1306
Herold M.J., McPherson K.G., and Reichardt H.M. Glucocorticoids in T cell apoptosis and function. Cell. Mol. Life Sci. 63 (2006) 60-72
Hojo Y., Hattori T.A., Enami T., Furukawa A., Suzuki K., Ishii H.T., Mukai H., Morrison J.H., Janessen W.G., Kominami S., Harada N., Kimoto T., and Kawato S. Adult rat male hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017α and P450 aromatase localized in neurons. Proc. Natl. Acad. Sci. USA 101 (2004) 865-870
Holloway C.C., and Clayton D.F. Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat. Neurosci. 4 (2001) 170-175
Ibanez C., Guennoun R., Liere P., Eychenne B., Pianos A., El-Etr M., Baulieu E.E., and Schumacher M. Developmental expression of genes involved in neurosteroidogenesis: 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase in the rat brain. Endocrinology 144 (2003) 2902-2911
Ito N., Ito T., Kromminga A., Bettermann A., Takigawa M., Kees F., Straub R.H., and Paus R. Human hair follicles display a functional equivalent of the hypothalamic-pituitary-adrenal axis and synthesize cortisol. FASEB J. 19 (2005) 1332-1334
Jirikowski G.F., Pusch L., Mopert B., Herbert Z., and Caldwell J.D. Expression of corticosteroid binding globulin in the rat central nervous system. J. Chem. Neuroanat. 34 (2007) 22-28
Jondal M., Pazirandeh A., and Okret S. Different roles for glucocorticoids in thymocyte homeostasis?. Trends Immunol. 25 (2004) 595-600
Jungmann R.A., Kot E., and Schweppe J.S. In vitro 17β-hydroxysteroid dehydrogenase activity in human thymus. Steroid 10 (1967) 397-409
Katz A., Heiblum R., Meidan R., and Robinzon B. Distinct features of dehydrocorticosterone reduction into corticosterone in the liver and duodenum of the domestic fowl (Gallus gallus domesticus). Gen. Comp. Endocrinol. 154 (2007) 67-74
Kayes-Wandover K.M., and White P.C. Steroidgenic enzyme gene expression in the human heart. J. Clin. Endocrinol. Metab. 85 (2000) 2519-2525
Ketterson E.D., Nolan Jr. V., and Sandell M. Testosterone in females: mediator of adaptivetraits, constraint on sexual dimorphism, or both?. Am. Nat. 166 (2005) S85-S98
Koenig H.L., Schumacher M., Ferzaz B., Thi A.N., Ressouches A., Guennoun R., Jung-Testas I., Robel P., Akwa Y., and Baulieu E.E. Progesterone synthesis and myelin formation by Schwann cells. Science 268 (1995) 1500-1503
Labrie F., Luu-The V., Belanger A., Lin S.X., Simard J., Pelletier G., and Labrie C. Is dehydroepiandrosterone a hormone?. J. Endocrinol. 187 (2005) 169-196
Lechner O., Dietrich H., Wiegers G.J., Vacchio M., and Wick G. Glucocorticoid production in the chicken bursa and thymus. Int. Immunol. 13 (2001) 769-776
Lechner O., Wiegers G.J., Oliveira-dos-Santos A.J., Dietrich H., Recheis H., Waterman M., Boyd R., and Wick G. Glucocorticoid production in the murine thymus. Eur. J. Immunol. 30 (2000) 337-346
Lee K.A., Wikelski M., Robinson W.D., Robinson T.R., and Klasing K.C. Constitutive immune defenses correlate with life-history variables in tropical birds. J. Anim. Ecol. 77 (2008) 356-363
Levine S. Regulation of the hypothalamic-pituitary-adrenal axis in the neonatal rat: role of maternal behavior. Neurotox. Res. 4 (2002) 557-564
Liu T., Wimalasena J., Bowen R.L., and Atwood C.S. Luteinizing hormone receptor mediates neuronal pregnenolone production via up-regulation of steroidogenic acute regulatory protein expression. J. Neurochem. 100 (2007) 1329-1339
London S.E., Monks D.A., Wade J., and Schlinger B.A. Widespread capacity for steroid synthesis in the avian brain and song system. Endocrinology 147 (2006) 5975-5987
Losel R., and Wehling M. Nongenomic actions of steroid hormones. Nat. Rev. Mol. Cell Biol. 4 (2003) 46-56
MacKenzie S.M., Clark C.J., Ingram M.C., Lai M., Seckl J., Gomez-Sanchez C.E., Fraser R., Connell J.M., and Davies E. Corticosteroid production by fetal rat hippocampal neurons. Endocr. Res. 26 (2000) 531-535
Matsuzaki J., Tsuji T., Imazeki I., Ikeda H., and Nishimura T. Immunosteroid as a regulator for Th1/Th2 balance: its possible role in autoimmune disease. Autoimmunity 38 (2005) 369-375
McEwen B.S., and Wingfield J.C. The concept of allostasis in biology and biomedicine. Horm. Behav. 43 (2003) 2-15
Mellon S.H. Neurosteroid regulation of central nervous system development. Pharmacol. Ther. 116 (2007) 107-124
Mellon S.H., and Deschepper C.F. Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Res. 629 (1993) 283-292
Mellon S.H., and Vaudry H. Biosynthesis of neurosteroids and regulation of their synthesis. Int. Rev. Neurobiol. 46 (2001) 33-78
Mendel C.M. The free hormone hypothesis: a physiologically based mathematical model. Endocr. Rev. 10 (1989) 232-274
Mensah-Nayagan A.G., Beaujean D., Luu-The V., Pelletier G., and Vaudry H. Anatomical and biochemical evidence for the synthesis of unconjugated and sulfated neurosteroids in amphibians. Brain Res. Brain Res. Rev. 37 (2001) 13-24
Micevych P.E., Soma K.K., and Sinchak K. Neuroprogesterone: key to estrogen positive feedback?. Brain Res. Rev. 57 (2008) 470-480
Naftolin F., Ryan K.J., Davies I.J., Petro Z., and Kuhn M. The formation and metabolism of estrogens in brain tissue. Adv. Biosci. 15 (1975) 105-121
Newman A.E.M., Chin E.H., Schmidt K.L., Bond L., Wynne-Edwards K.E., and Soma K.K. Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoassay. Gen. Comp. Endocrinol. 155 (2008) 503-510
Newman A.E.M., Pradhan D.S., and Soma K.K. DHEA and corticosterone are regulated by season and acute stress in a wild songbird: jugular versus brachial plasma. Endocrinology 149 (2008) 2537-2545
Ng K.-M., Catalano M.G., Pinos T., Selva D.M., Avvakumov G.V., Munell F., and Hammond G.L. Evidence that fibulin family members contribute to the steroid-dependent extravascular sequestration of sex hormone-binding globulin. J. Biol. Chem. 281 (2006) 15853-15861
Nolten W.E., Holt L.H., and Rueckert P.A. Desoxycorticosterone in normal pregnancy. III. Evidence of a fetal source of desoxycorticosterone. Am. J. Obstet. Gynecol. 139 (1981) 477-482
Norris D.O. Vertebrate Endocrinology. fourth ed. (2007), Elsevier, Burlington, MA
Owen-Ashley N.T., Hasselquist D., and Wingfield J.C. Androgens and the immunocompetence handicap hypothesis. Unraveling direct and indirect pathways of immunosuppression in song sparrows. Am. Nat. 164 (2004) 490-505
Ottaviani E., Franchini A., and Franceschi C. Presence of immunoreactive corticotropin-releasing hormone and cortisol molecules in invertebrate haemocytes and lower and higher vertebrate thymus. Histochem. J. 30 (1998) 61-67
Paus R. Frontiers in the (neuro-)endocrine controls of hair growth. J. Investig. Dermatol. Symp. Proc. 12 (2007) 20-22
Pazirandeh A., Jondal M., and Okret S. Conditional expression of a glucocorticoid receptor transgene in thymocytes reveals a role for thymic-derived glucocorticoids in thymopoiesis in vivo. Endocrinology 146 (2005) 2501-2507
Pazirandeh A., Xue Y., Rafter I., Sjovall J., Jondal M., and Okret S. Paracrine glucocorticoid activity produced by mouse thymic epithelial cells. FASEB J. 13 (1999) 893-901
Pradhan D.S., Yu Y., and Soma K.K. Rapid estrogen regulation of DHEA metabolism in the male and female songbird brain. J. Neurochem. 104 (2008) 244-253
Prange-Kiel J., Jarry H., Schoen M., Kohlmann P., Lohse C., Zhou L., and Rune G.M. Gonadotropin-releasing hormone regulates spine density via its regulatory role in hippocampal estrogen synthesis. J. Cell. Biol. 180 (2008) 417-426
Provost P.R., and Tremblay Y. Genes involved in the adrenal pathway of glucocorticoid synthesis are transiently expressed in the developing lung. Endocrinology 146 (2005) 2239-2245
Reventos J., Sullivan P.M., Joseph D.R., and Gordon J.W. Tissue-specific expression of the rat androgen-binding protein/sex hormone-binding globulin gene in transgenic mice. Mol. Cell. Endocrinol. 96 (1993) 69-73
Rohmann K.N., Schlinger B.A., and Saldanha S.J. Subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain. J. Neurobiol. 67 (2006) 1-9
Romero L.M., Strochlic D., and Wingfield J.C. Corticosterone inhibits feather growth: potential mechanism explaining seasonal down regulation of corticosterone during molt. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 142 (2005) 65-73
Rubolini D., Romano M., Boncoraglio G., Ferraru R.P., Martinelli R., Galeotti P., Fasola M., and Saino N. Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks. Horm. Behav. 47 (2005) 592-605
Rune G.M., and Frotscher M. Neurosteroid synthesis in the hippocampus: role in synaptic plasticity. Neuroscience 136 (2005) 833-842
Sapolsky R.M., and Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 396 (1986) 64-76
Sapolsky R.M., Romero L.M., and Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21 (2000) 55-89
Schlinger B.A., and Callard G.V. Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. Neuroendocrinology 49 (1989) 434-441
Schlinger B.A., Pradhan D.S., and Soma K.K. 3β-HSD activates DHEA in the songbird brain. Neurochem. Int. 52 (2008) 611-620
Schlinger B.A., Soma K.K., and London S.E. Neurosteroids and brain sexual differentiation. Trends Neurosci. 24 (2001) 429-431
Schmidt, K.L., Soma, K.K., in press. Cortisol and corticosterone in the songbird immune and nervous systems: local versus systemic levels during development. Am. J. Physiol. Reg. Integ. Comp. Physiol.
Schumacher M., Guennoun R., Stein D.G., and De Nicola A.F. Progesterone: therapeutic opportunities for neuroprotection and myelin repair. Pharmacol. Ther. 116 (2007) 77-106
Seckl J.R., and Walker B.R. Minireview: 11β-hydroxysteroid dehydrogenase type 1- a tissue specific amplifier of glucocorticoid action. Endocrinology 142 (2001) 1371-1376
Shally A.V. Aspects of hypothalamic regulation of the pituitary gland. Science 202 (1978) 43-53
Siiteri P.K., Murai J.T., Hammond G.L., Nisker J.A., Raymoure W.J., and Kuhn R.W. The serum transport of steroid hormones. Recent Prog. Horm. Res. 38 (1982) 457-510
Sims C.G., and Holberton R.C. Development of the corticosterone stress response in young northern mockingbirds (Mimus polyglottos). Gen. Comp. Endocrinol. 119 (2000) 193-201
Sippell W.G., Becker H., Versmold H.T., Bidlingmaier F., and Knorr D. Longitudinal studies of plasma aldosterone, corticosterone, deoxycorticosterone, progesterone, 17-hydroxyprogesterone, cortisol, and cortisone determined simultaneously in mother and child at birth and during the early neonatal period. I. Spontaneous delivery. J. Clin. Endocrinol. Metab. 46 (1978) 971-985
Slominski A., Wortsman J., Tuckey R.C., and Paus R. Differential expression of HPA axis homolog in skin. Mol. Cell. Endocrinol. (2007) 143-149
Smith E.M., Meyer W.J., and Blalock J.E. Virus-induced corticosterone in hypophysectomized mice: a possible lymphoid adrenal axis. Science 24 (1982) 1311-1312
Soma K.K. Testosterone and aggression: Berthold, birds, and beyond. J. Neuroendocrinol. 18 (2006) 543-551
Soma K.K., Alday N.A., Hau M., and Schlinger B.A. Dehydroepiandrosterone metabolism by 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase in adult zebra finch brain: sex difference and rapid effect of stress. Endocrinology 145 (2004) 1668-1677
Soma, K.K., Scotti, M.A.L., Newman, A.E.M., Charlier, T.D., Demas, G.E., in press. Novel mechanisms for neuroendocrine regulation of aggression. Front. Neuroendocrinol.
Soma K.K., Schlinger B.A., Wingfield J.C., and Saldanha C.J. Brain aromatase, 5α-reductase and 5β-reductase change seasonally in wild male song sparrows. Relationship to sexual and aggressive behaviors. J. Neurobiol. 56 (2003) 209-221
Soma K.K., Sullivan K.K., Tramontin A.D., Saldanha C.J., Schlinger B.A., and Wingfield J.C. Acute and chronic effects of an aromatase inhibitor on territorial aggression in breeding and nonbreeding male song sparrows. J. Comp. Physiol. [A] 186 (2000) 759-769
Soma K.K., Sullivan K., and Wingfield J.C. Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season. Gen. Comp. Endocrinol. 115 (1999) 442-453
Soma K.K., Tramontin A.D., Featherstone J., and Brenowitz E.A. Estrogen contributes to seasonal plasticity of the adult avian song system. J. Neurobiol. 58 (2004) 413-422
Soma K.K., Tramontin A.D., and Wingfield J.C. Oestrogen regulates male aggression in the non-breeding season. Proc. Biol. Sci. 267 (2000) 1089-1096
Soma, K.K., Wingfield, J.C., 1999. Endocrinology of aggression in the non-breeding season. In: Adams, N., Slotow, R. (Eds.), Proceedings of the 22nd International Ornithological Congress, Durban. Birdlife of South Africa, Johannesburg, pp. 1606-1620.
Soma K.K., and Wingfield J.C. Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression. Gen. Comp. Endocrinol. 123 (2001) 144-155
Soma K.K., Wissman A.M., Brenowitz E.A., and Wingfield J.C. Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird. Horm. Behav 41 (2002) 203-212
Spencer J.L., Waters E.M., Romeo R.D., Wood G.E., Milner T.A., and McEwen B.S. Uncovering the mechanisms of estrogen effects on hippocampal function. Front. Neuroendocrinol. 29 (2008) 219-237
Sullivan D.A., and Wira C.R. Sex hormone and glucocorticoid receptors in the bursa of Fabricius of immature chicks. J. Immunol. 122 (1979) 2617-2623
Toran-Allerand C.D., Tinnikov A.A., Singh R.J., and Nethrapalli I.S. 17α-Estradiol: a brain active estrogen?. Endocrinology 146 (2005) 3843-3850
Trainor B.C., Lin S., Finy M.S., Rowland M.R., and Nelson R.J. Photoperiod reverses the effects of estrogens on male aggression via genomic and nongenomic pathways. Proc. Natl. Acad. Sci. USA 104 (2007) 9840-9845
Trainor B.C., Finy M.S., and Nelson R.J. Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice. Horm. Behav. 53 (2008) 192-199
Tsutsui K., Matsunaga M., Miyabara H., and Ukena K. Neurosteroid biosynthesis in the quail brain: a review. J. Exp. Zool. 305A (2006) 733-742
Vacchio M.S., Papadopoulos V., and Ashwell J.D. Steroid production in the thymus: implications for thymocyte selection. J. Exp. Med. 179 (1994) 1835-1846
Wada H., Hahn T.P., and Breuner C.W. Development of stress reactivity in white-crowned sparrow nestlings: total corticosterone response increases with age, while free corticosterone response remains low. Gen. Comp. Endocrinol. 150 (2007) 405-413
Wang Y.M., Bayliss D.A., Millhorn D.E., Petruszm P., and Joseph D.R. The androgen-binding protein gene is expressed in male and female rat brain. Endocrinology 127 (1990) 3124-3130
Westphal U. Steroid-Protein Interaction: Monographs on Endocrinology (1971), Springer-Verlag, Berlin
Westphal U. Steroid-protein interaction: from past to present. J. Steroid. Biochem. 19 (1983) 1-15
Widstrom R.L., and Dillon J.S. Is there a receptor for dehydroepiandrosterone or dehydroepiandrosterone sulfate?. Semin. Reprod. Med. 22 (2004) 289-298
Wingfield J.C. Regulation of territorial behavior in the sedentary song sparrow, Melospiza melodia morphna. Horm. Behav. 28 (1994) 1-15
Wingfield J.C., and Hahn T.P. Testosterone and territorial behavior in sedentary and migratory sparrows. Anim. Behav. 47 (1994) 77-89
Wingfield J.C., Hegner R.E., Dufty Jr. A.M., and Ball G.F. The "Challenge Hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136 (1990) 829-846
Wingfield J.C., Lynn S.E., and Soma K.K. Avoiding the 'costs' of testosterone: ecological bases of hormone-behavior interactions. Brain Behav. Evol 57 (2001) 239-251
Wingfield J.C., Matt K.S., and Farner D.S. Physiologic properties of steroid-hormone binding proteins in avian blood. Gen. Comp. Endocrinol. 53 (1984) 281-292
Wingfield J.C., Smith J.P., and Farner D.S. Endocrine responses of white-crowned sparrows to environmental stress. The Condor 84 (1982) 399-409
Wingfield J.C., and Soma K.K. Spring and autumn territorial behavior in song sparrows: same behavior, different mechanisms?. Integr. Comp. Biol. 42 (2002) 11-20
Woolley C.S. Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 47 (2007) 657-680
Yang E.-J., Nasipak B.T., and Kelley D.B. Direct action of gonadotropin in brain integrates behavioral and reproductive functions. Proc. Natl. Acad. Sci. USA 104 (2007) 2477-2482
Zhang T.Y., Ding X., and Daynes R.A. The expression of 11β-hydroxysteroid dehydrogenase type 1 by lymphocytes provides a novel means for intracrine regulation of glucocorticoid activities. J. Immunol. 174 (2005) 879-889
Zmijewski M.A., Sharma R.K., and Slominski A.T. Expression of molecular equivalent of hypothalamic-pituitary-adrenal axis in adult retinal pigment epithelium. J. Endocrinol. 193 (2007) 157-169
Zwain I.H., and Yen S.S. Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140 (1999) 3843-3852