Rapid estrogen regulation of DHEA metabolism in the male and female songbird brain

Journal of Neurochemistry

Volumn 104, Issue 1, 2008, Pages 244-253

  Pradhan, Devaleena S ^a   Yu, Yan ^a   Soma, Kiran K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

3beta HSD; 5beta reductase; Androstenedione; Aromatase; Bird; Corticosterone; Dehydroepiandrosterone; Estradiol; HPLC; Neurosteroid; Non genomic; Song; Stress; Testosterone; Zebra finch

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ESTRADIOL; ESTROGEN; PRASTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN TISSUE; CELL NUCLEUS; CENTRIFUGATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FINCH; HORMONE METABOLISM; IN VITRO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SEX; SONGBIRD; SUPERNATANT; TAENIOPYGIA GUTTATA; WHOLE CELL;

ANIMALS; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, THIN LAYER; DEHYDROEPIANDROSTERONE; DIHYDROTESTOSTERONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; ESTRADIOL; ESTROGENS; FEMALE; FINCHES; MALE; MULTIENZYME COMPLEXES; PROGESTERONE REDUCTASE; SEX CHARACTERISTICS; STEROID ISOMERASES; TIME FACTORS;

AVES; PASSERI; TAENIOPYGIA GUTTATA;

EID: 37249009695     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04953.x     Document Type: Article

References (66)

1. Abraham I. M. Herbison A. E. (2005) Major sex differences in non-genomic estrogen actions on intracellular signaling in mouse brain in vivo. J. Neurosci. 131, 945 951.
2. Baillien M., Cornil C. A., Ball G. F. Balthazart J. (2004) Sexual performance and stress rapidly alter the preoptic aromatase activity in quail. Soc. Neurosci. Abstr. San Diego, Program No. 88.4.
3. Balthazart J. Ball G. F. (2006) Is brain estradiol a hormone or a neurotransmitter? TINS 29, 241 249.
4. Balthazart J., Cornil C. A., Taziauz M., Charlier T. D., Baillien M. Ball G. F. (2006) Rapid changes in production and behavioral action of estrogens. Neuroscience 138, 783 791.
5. Baulieu E. E. (1998) Neurosteroids: a novel function of the brain. Psychoneuroendocrinol. 23, 8 963.
6. 2 dopamine receptor binding. Brain Res. 637, 163 172.
7. Blaustein J. D., Lehman M. N., Turcotte J. C. Greene G. (1992) Estrogen receptors in dendrites and axon terminals in the guinea pig hypothalamus. Endocrinology 131, 281 290.
8. Bradford M. M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248 254.
9. Coirini H., Gouézou M., Delespierre B., Liere P., Pianos A., Eychenne B., Schumacher M. Guennoun R. (2003a) Characterization and regulation of the 3β-HSD enzyme in the rat sciatic nerve. J. Neurochem. 84, 119 126.
10. Coirini H., Gouézou M., Delespierre B., Schumacher M. Guennoun R. (2003b) 3β-hydroxysteroid dehydrogenase isomerase (3β-HSD) activity in the rat sciatic nerve: kinetic analysis and regulation by steroids. J. Steroid Biochem. Mol. Biol. 85, 89 94.
11. Cornil C. A., Ball G. F. Balthazart J. (2006) Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res. 1126, 2 26.
12. Demas G. E., Cooper M. A., Albers H. E. Soma K. K. (2007) Novel mechanisms underlying neuroendocrine regulation of aggression: a synthesis of rodent, avian and primate studies. in : Blaustein J. D. (ed Behavioral Neurochemistry and Neuroendocrinology (vol. 21), in Lajtha A (series ed) Handbook of Neurochemistry and Molecular Neurobiology, Springer, Berlin, Germany, pp. 337 372.
13. Driggers P. H. Segars J. H. (2002) Estrogen action and cytoplasmic signaling pathways. Part II: the role of growth factors and phosphorylation. Trends Endocrinol. Metab. 13, 422 427.
14. Freking F., Ramachandran B. Schlinger B. A. (1998) Regulation of aromatase, 5α- and 5β-reductase in primary cell cultures of developing zebra finch telencephalon. J. Neurobiol. 36, 30 40.
15. Goodson J. L., Evans A. K. Soma K. K. (2005a) Neural responses to aggressive challenge correlate with behavior in nonbreeding sparrows. NeuroReport 16, 1719 1723.
16. Goodson J. L., Saldanha C. J., Hahn T. P. Soma K. K. (2005b) Recent advances in behavioral neuroendocrinology: insights from studies on birds. Horm. Behav. 48, 461 473.
17. Gower D. B. Cooke G. M. (1983) Regulation of steroid-transforming enzymes by endogenous steroids. J. Steroid Biochem. 19, 1527 1556.
18. 4- isomerase (3β-HSD), is expressed in rat brain. Mol. Brain. Res. 30, 287 300.
19. Gurney M. E. (1981) Hormonal control of cell form and number in the zebra finch song system. J. Neurosci. 1, 658 673.
20. Hart S. A., Snyder M. A., Smejkalova T. Woolley C. S. (2007) Estrogen mobilizes a subset of estrogen receptor-α-immunoreactive vesicles in inhibitory presynaptic boutons in hippocampal CA1. J. Neurosci. 27, 2102 2111.
21. Hau M., Stoddard S. T. Soma K. K. (2004) Territoral aggression and hormones during the non-breeding season in a tropical bird. Horm. Behav. 45, 40 49.
22. Horvat A., Nikezic G., Petrovic S. Kanazir D. T. (2001) Binding of estradiol to synaptosomal mitochondria: physiological significance. Cell. Mol. Life Sci. 58, 636 644.
23. Hutchison J. B., Wingfield J. C. Hutchison R. E. (1984) Sex differences in plasma concentrations of steroids during the sensitive period for brain differentiation in the zebra finch. J. Endocrinol. 103, 363 369.
24. Kelly M. J., Moss R. L. Dudley C. A. (1976) Differential sensitivity of preoptic-septal neurons to microelectrophoresed estrogen during the estrous cycle. Brain Res. 114, 152 157.
25. Kelly M. J., Qui J., Wagner E. J. Ronnekleiv O. K. (2003) Rapid effects of estrogen on G protein-coupled receptor activation of potassium channels in the central nervous system (CNS). J. Steroid Biochem. Mol. Biol. 83, 187 193.
26. Kimonides V. G., Khatibi N. H., Svendsen C. N., Sofroniew M. V. Herbert J. (1998) Dehydroepiandrosterone (DHEA) and DHEA-sulfate (DHEAS) protect hippocampal neurons against excitatory amino acid-induced neurotoxicity. Proc. Natl. Acad. Sci. 95, 1852 1857.
27. Labrie F., Luu-The V., Belanger A., Lin S.-X., Simard J., Pelletier G. Labrie C. (2005) Is dehydroepiandrosterone a hormone? J. Endocrinol. 187, 169 196.
28. 2 + uptake by estrogen receptor agonists and antagonists. Br. J. Pharmacol. 145, 862 871.
29. London S. E., Monks D. A., Wade J. Schlinger B. A. (2006) Widespread capacity for steroid synthesis in the avian brain and song system. Endocrinology 147, 5975 5987.
30. Mason J. I. (1993) The 3β-hydroxysteroid dehygdrogenase gene family of enzymes. Trends Endocrinol. Metab. 4, 199 203.
31. Matsunaga M., Ukena K. Tsutsui K. (2001) Expression and localization of cytochrome P450 17α-hydroxylase/c17,20-lyase in the avian brain. Brain Res. 899, 112 122.
32. Mensah-Nyagan A. G., Feuilloley M., Dupont E., Do-Rego J.-C., Leboulenger F., Pelletier G. Vaudry H. (1994) Immunocytochemical localization and biological activity of 3beta-hydroxysteroid dehydrogenase in the central nervous system of the frog. J. Neurosci. 14, 7306 7318.
33. Mensah-Nyagan A. G., Saredi S., Schaeffer V., Kibaly C., Meyer L., Melcangi R. C. Patte-Mensah C. (2007) Assessment of neuroactive steroid formation in diabetic rat spinal cord using high-performance liquid chromatography and continuous flow scintillation detection. Neurochem. Int., in press.
34. Micevych P. E., Chaban V., Ogi J., Dewing P., Lu J. K. H. Sinchak K. (2007) Estradiol stimulates progesterone synthesis in hypothalamic cultures. Endocrinology 148, 782 789.
35. Milner T. A., McEwen B. S., Hayashi S., Li C. J., Reagan L. P. Alves S. E. (2001) Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J. Comp. Neurol. 429, 355 371.
36. Milner T. A., Ayoola K., Drake C. T., Herrick S. P., Tabori N. E., McEwen B. S., Warrier S. Alves S. E. (2005) Ultrastructural localization of estrogen receptor β immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 491, 81 95.
37. Newman A. E. M., Chin E. H., Schmidt K. L., Bond L., Whynne-Edwards K. E. Soma K. K. (2007) Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoassay. Gen. Comp. Endocrinol., in press.
38. Nottebohm F. Arnold A. P. (1976) Sexual dimorphism in vocal control areas of the songbird brain. Science 194, 211 213.
39. Pelletier G., Luu-The V., Tremblay Y., Belanger A. Labrie F. (2001) Immunoelectron microscopic localization of three key steroidogenic enzymes (cytochrome P450(scc), 3beta-hydroxysteroid dehydrogenase and cytochrome P450(c17)) in rat adrenal cortex and gonads. J. Endocrinol. 171, 373 383.
40. Peterson R. S., Yarram L., Schlinger B. A. Saldanha C. J. (2005) Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proc. Biol. Sci. 272, 2089 2096.
41. Potts G. O., Creange J. E., Harding H. R. Schane H. P. (1978) Trilostane, an orally active inhibitor of steroid biosynthesis. Steroids 32, 257 267.
42. Reiner A., Perkel D. J., Bruce L. et al. (2004) Songbirds and the revised avian brain nomenclature. J. Comp. Neurol. 473, 377 414.
43. Remage-Healey L. Bass A. H. (2007) Plasticity in brain sexuality is revealed by the rapid actions of steroid hormones. J. Neurosci. 27, 1114 1122.
44. Revankar C. M., Cimino D. F., Sklar L. A., Arterburn J. B. Prossnitz E. R. (2005) A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307, 1625 1630.
45. Rohmann K. N., Schlinger B. A. Saldanha C. J. (2007) Subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain. Dev. Neurobiol. 67, 1 9.
46. Romeo R. D., McCarthy J. B., Wang A., Milner T. A. McEwen B. S. (2005) Sex differences in hippocampal estradiol-induced N-M-D-Aspartic acid binding and ultrastructural localization of estrogen receptors. Neuroendocrinology 81, 391 399.
47. Saldanha C. J., Tuerk M. J., Kim Y.-H., Fernandes A. O., Arnold A. P. Schlinger B. A. (2000) Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J. Comp. Neurol. 423, 619 630.
48. Schlinger B. A. Callard G. V. (1989) Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. Neuroendocrinology 49, 434 441.
49. Schlinger B. A., Pradhan D. S. Soma K. K. (2007) 3β-HSD activates DHEA in the songbird brain. Neurochem. Int., in press.
50. Shors T. J., Pickett J., Wood G. E. Paczynski M. (1999) Acute stress enhances estrogen levels in the female rat. Stress 3, 163 171.
51. Sinchak K., Mills R. H., Tao L., LaPolt P., Lu J. K. Micevych P. (2003) Estrogen induces de novo progesterone synthesis in astrocytes. Dev. Neurosci. 25, 343 348.
52. Soma K. K. (2006) Testosterone and aggression: Berthold, birds and beyond. J. Neuroendocrinol. 18, 543 551.
53. Soma K. K. Wingfield J. C. (2001) Dehydroepiandrosterone (DHEA) in songbird plasma: seasonal regulation and relationship to territorial aggression. Gen. Comp. Endocrinol. 123, 144 155.
54. Soma K. K., Tramontin A. D. Wingfield J. C. (2000) Oestrogen regulates male aggression in the non-breeding season. Proc. R. Soc. Lond. B. 267, 1089 1096.
55. Soma K. K., Wissman A. M., Brenowitz E. A. Wingfield J. C. (2002) Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird. Horm. Behav. 41, 203 212.
56. Soma K. K., Alday N. A., Hau M. Schlinger B. A. (2004a) Dehydroepiandrosterone metabolism by 3β-hydroxysteroid dehydrogenase/ Δ5-Δ4 isomerase in adult zebra finch brain: sex difference and rapid effect of stress. Endocrinology 145, 1668 1677.
57. Soma K. K., Tramontin A. D., Featherstone J. Brenowitz E. A. (2004b) Estrogen contributes to seasonal plasticity of the adult avian song control system. J. Neurobiol. 58, 413 422.
58. Soma K. K., Sinchak K., Lakhter A., Schlinger B. A. Micevych P. E. (2005) Neurosteroids and female reproduction: estrogen increases 3β-HSD mRNA and activity in rat hypothalamus. Endocrinology 146, 4386 4390.
59. Tam H. Schlinger B. A. (2007) Activities of 3β-HSD and aromatase in slices of developing and adult zebra finch brain. Gen. Comp. Endocrinol. 150, 26 33.
60. Taziaux M., Keller M., Bakker J. Balthazart J. (2007) Sexual behavior activity tracks rapid changes in brain estrogen concentrations. J. Neurosci. 27, 6563 6572.
61. Thomas P., Pang Y., Filardo E. J. Dong J. (2005) Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146, 624 632.
62. Toran-Allerand C. D., Guan C., MacLusky N. J. et al. (2002) ER-X: a novel, plasma- membrane associated, putative estrogen receptor that is regulated during development and following ischemic brain injury. J. Neurosci. 22, 8391 8401.
63. Vanson A., Arnold A. P. Schlinger B. A. (1996) 3β-hydroxysteroid dehydrogenase/isomerase and aromatase activity in primary cultures of developing zebra finch telencephalon: dehydroepiandrosterone as substrate for synthesis of androstenedione and estrogens. Gen. Comp. Endocrinol. 102, 342 350.
64. Wolf O. T. Kirschbaum C. (1999) Actions of dehydroepiandrosterone and its sulfate in the central nervous system: effects on cognition and emotion in animals and humans. Brain Res. Rev. 30, 264 288.
65. Woolley C. S. (2007) Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 47, 657 680.
66. Yang S.-H., Liu R., Perez E. J. et al. (2004) Mitochondrial localization of estrogen receptor β. Proc. Natl. Acad. Sci. 101, 4130 4135.