Anatomical relationships between aromatase and tyrosine hydroxylase in the quail brain: Double-label immunocytochemical studies

Journal of Comparative Neurology

Volumn 391, Issue 2, 1998, Pages 214-226

  Balthazart, Jacques ^a   Foidart, Agnes ^a   Baillien, Michelle ^a   Harada, Nobuhiro ^b   Ball, Gregory F ^c  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b FUJITA HEALTH UNIVERSITY   (Japan)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Catecholamines; Dopamine; Japanese quail; Medial preoptic nucleus; Norepinephrine; Sexual behavior

Indexed keywords

ANTIGEN; AROMATASE; CATECHOLAMINE; DOPAMINE; ESTRADIOL; NORADRENALIN; TESTOSTERONE; TYROSINE 3 MONOOXYGENASE;

ANIMAL TISSUE; ARTICLE; BRAIN; ENZYME ACTIVITY; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; MALE; MEDIAL PREOPTIC AREA; NONHUMAN; PREOPTIC NUCLEUS; PRIORITY JOURNAL; QUAIL; RADIOENZYMATIC ASSAY; SEXUAL BEHAVIOR; STRIA TERMINALIS; TELENCEPHALON;

ANIMALS; AROMATASE; BIOLOGICAL MARKERS; BRAIN; COTURNIX; DOPAMINE; IMMUNOHISTOCHEMISTRY; MALE; NERVE FIBERS; NOREPINEPHRINE; TYROSINE 3-MONOOXYGENASE;

EID: 0032498634     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980209)391:2<214::AID-CNE5>3.0.CO;2-5     Document Type: Article

References (86)

1. Adkins, E.K. (1977) Effects of diverse androgens on the sexual behavior and morphology of castrated male quail. Horm. Behav. 8:201-207.
2. Adkins, E.K., J.J. Boop, D.L. Koutnik, J.B. Morris, and E.E. Pniewski (1980) Further evidence that androgen aromatization is essential for the activation of copulation in male quail. Physiol. Behav. 24:441-446.
3. Adkins, E.K., and E.E. Pniewski (1978) Control of reproductive behavior by sex steroids in male quail. J. Comp. Physiol. Psychol. 92:1169-1178.
4. Armstrong, R.C., and M.R. Montminy (1993) Transsynaptic control of gene expression. Annu. Rev. Neurosci. 16:17-29.
5. Arnold, A.P., F. Nottebohm, and D.W. Pfaff (1976) Hormone concentrating cells in vocal control areas of the brain of the zebra finch (Poephila guttata). J. Comp. Neurol. 165:487-512.
6. Bailhache, T., and J. Balthazart (1993) The catecholaminergic system of the quail brain: Immunocytochemical studies of dopamine β-hydroxylase and tyrosine hydroxylase. J. Comp. Neurol. 329:230-256.
7. Baillien, M., and J. Balthazart (1997) A direct dopaminergic control of aromatase activity in the quail preoptic area. J. Steroid Biochem. Mol. Biol. (in press).
8. Ball, G.F. (1990) Chemical neuroanatomical studies of the steroid-sensitive songbird vocal control system: A comparative approach. In J. Balthazart (ed): Hormones, Brain and Behaviour in Vertebrates. 1. Sexual Differentiation, Neuroanatomical Aspects, Neurotransmitters and Neuropeptides. Basel: Karger, Comp. Physiol, vol. 8, pp. 148-167.
9. Ball, G.F. (1994) Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars. Brain Behav. Evol. 44:234-246.
10. 2-adrenergic receptors in the brain of the Japanese quail as determined by quantitative autoradiography: Implications for the control of sexually dimorphic reproductive processes. Brain Res. 491:68-79.
11. Ball, G.F., J.M. Casto, and J. Balthazart (1995) Autoradiographic localization of D1-like dopamine receptors in the forebrain of male and female Japanese quail and their relationship with immunoreactive tyrosine hydroxylase. J. Chem. Neuroanat. 9:121-133.
12. 2-adrenergic receptor binding, and aromatase activity in the brain of the Japanese quail. Brain Res. 492:163-175.
13. Balthazart, J., and G.F. Ball (1992) Is dopamine interacting with aromatase to control sexual behavior in male quail? Poult. Sci. Rev. 4:217-233.
14. Balthazart, J., and G.F. Ball (1993) Neurochemical differences in two steroid-sensitive areas mediating reproductive behaviors. Adv. Comp. Environ. Physiol. 15:133-161.
15. Balthazart, J., and A. Foidart (1993) Brain aromatase and the control of male sexual behavior. J. Steroid Biochem. Mol. Biol. 44:521-540.
16. Balthazart, J., J.M. Libioulle, and P. Sante (1988) Stimulatory effects of the noradrenergic neurotoxin DSP4 on sexual behavior in male quail. Behav. Proc. 17:27-44.
17. Balthazart, J., M. Gahr, and C. Surlemont (1989) Distribution of estrogen receptors in the brain of the Japanese quail: An immunocytochemical study. Brain Res. 507:205-214.
18. Balthazart, J., A. Foidart, P. Sante, and J.C. Hendrick (1992a) Effects of β-methyl-para-tyrosine on monoamine levels in the Japanese quail: Sex differences and testosterone effects. Brain Res. Bull. 28:275-288.
19. Balthazart, J.,A. Foidart, E.M. Wilson, and G.F. Ball (1992b) Immunocytochemical localization of androgen receptors in the male songbird and quail brain. J. Comp. Neurol. 317:407-420.
20. Balthazart, J., J. Reid, P. Absil, A. Foidart, and G.F. Ball (1995) Appetitive as well as consummatory aspects of male sexual behavior in quail are activated by androgens and estrogens. Behav. Neurosci. 109:485-501.
21. Balthazart, J., P. Absil, A. Foidart, M. Houbart, N. Harada, and G.F. Ball (1996a) Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): Implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J. Neurobiol. 31:129-148.
22. Balthazart, J., A. Foidart, P. Absil, and N. Harada (1996b) Effects of testosterone and its metabolites on aromatase-immunoreactive cells in the quail brain: Relationship with the activation of male reproductive behavior. J. Steroid Biochem. Mol. Biol. 56:185-200.
23. Balthazart, J., O. Tlemcani, and G.F. Ball (1996c) Do sex differences in the brain explain sex differences in the hormonal induction of reproductive behavior? What 25 years of research on the Japanese quail tells us. Horm. Behav. 30:627-661.
24. Balthazart, J., O. Tlemçani, and N. Harada (1996d) Localization of testosterone-sensitive and sexually dimorphic aromatase-immunoreactive cells in the quail preoptic area. J. Chem. Neuroanat. 11:147-171.
25. Balthazart, J., P. Absil, M. Baillien, and G.F. Ball (1997a) Morphological and pharmacological evidence for a dopaminergic regulation of aromatase in the quail preoptic area. Abstr. 1st meeting Soc. Behav. Neuroendocrinol., Baltimore, MD.
26. Balthazart, J., C. Castagna, and G.F. Ball (1997b) Aromatization inhibition blocks the activation and sexual differentiation of appetitive male sexual behavior in Japanese quail. Behav. Neurosci. 111:381-397.
27. Baylé, J.D., F. Ramade, and J. Oliver (1974) Stereotaxic topography of the brain of the quail. J. Physiol. (Paris) 68:219-241.
28. Benzo, C.A. (1986) Nervous system. In P.D. Sturkie (ed): Avian Physiology, 4th edit. New York: Springer-Verlag, pp. 1-36.
29. Bradford, M.M. (1976) A rapid sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
30. Breazile, J.E., and W.J. Kuenzel (1993) Systema nervosum centrale. In J.J. Baumel, A.S. King, J.E. Breazile, H.E. Evans, and J.C. Vanden Berge (eds): Handbook of Avian Anatomy: Nomina Anatomicum Avium. Cambridge, MA: Nuttall Ornithological Club, pp. 493-554.
31. Callard, G.V. (1981) Aromatization is cyclic AMP-dependent in cultured brain cells. Brain Res. 204:461-464.
32. Callard, G.V. (1984) Aromatization in brain and pituitary: An evolutionary perspective. In F. Celotti, F. Naftolin, and L. Martini (eds): Metabolism of Hormonal Steroids in the Neuroendocrine Structures. New York: Raven Press, pp. 79-102.
33. Callard, G.V., Z. Petro, and K.J. Ryan (1978a) Conversion of androgen to estrogen and other steroids in the vertebrate brain. Am. Zool. 18:511-523.
34. Callard, G.V., Z. Petro, and K.J. Ryan (1978b) Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology 103:2283-2290.
35. Callard, G.V., A. Kruger, and M. Betka (1995) The goldfish as a model for studying neuroestrogen synthesis, localization, and action in the brain and visual system. Environ. Health Perspect. 103 Suppl. 7:51-57.
36. Cardinali, D.P., M.N. Ritta, and P.V. Gejman (1982) Norepinephrine stimulates testosterone aromatization and inhibits 5a-reduction via β-adrenoreceptors in the rat pineal gland. Mol. Cell. Endocrinol. 28:199-209.
37. Foidart, A., A. De Clerck, N. Harada, and J. Balthazart (1994a) Aromatase-immunoreactive cells in the quail brain: Effects of testosterone and sex dimorphism. Physiol. Behav. 55:453-464.
38. Foidart, A., N. Harada, and J. Balthazart (1994b) Effects of steroidal and non steroidal aromatase inhibitors on sexual behavior and aromatase-immunoreactive cells and fibers in the quail brain. Brain Res. 657:105-123.
39. Foidart, A., N. Harada, and J. Balthazart (1995a) Aromatase-immunoreactive cells are present in mouse brain areas that are known to express high levels of aromatase activity. Cell Tissue Res. 280:561-574.
40. Foidart, A., J. Reid, P. Absil, N. Yoshimura, N. Harada, and J. Balthazart (1995b) 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. 8:267-282.
41. Freidin, M. , and D.W. Pfaff (1995) Molecular actions of steroid hormones and their possible relations to reproductive behaviors. In P.E. Micevych and R.P. Hammer, Jr. (eds): Neurobiological Effects of Sex Steroid Hormones. Cambridge, UK: Cambridge University Press, pp. 350-362.
42. Gahr, M., H.-R. Güttinger, and D.E. Kroodsma (1993) Estrogen receptors in the avian brain: Survey reveals general distribution and forebrain areas unique to songbirds. J. Comp. Neurol. 327:112-122.
43. Gierschik, P., and K.H. Jakobs (1988) Mechanisms for inhibition of adenylate cyclase by alpha-2 adrenergic receptors. In L.E. Limbird (ed): The Alpha-2 Adrenergic Receptors. Clifton, NJ: Humana Press, pp. 75-113.
44. Gingrich, J.A., and M.G. Caron (1993) Recent advances in the molecular biology of dopamine receptors. Annu. Rev. Neurosci. 16:299-321.
45. Goodman, R.H. (1990) Regulation of neuropeptide gene expression. Annu. Rev. Neurosci. 13:111-127.
46. Harada, N., S. Abe-Dohmae, R. Loeffen, A. Foidart, and J. Balthazart (1993) Synergism between androgens and estrogens in the induction of aromatase and its messenger RNA in the brain. Brain Res. 622:243-256.
47. Horn, G. (1985) Memory, imprinting, and the brain. Oxford: Clarendon Press.
48. Horvath, T.L., L. Roa-Pena, and F. Naftolin (1996) Aromatase in the developing sensory system of the rat. Abstr. 4th Aromatase Conference, Tahoe City, CA, pp. 19.
49. Kelley, D. (1988) Sexually dimorphic behaviors. Annu. Rev. Neurosci. 11:225-251.
50. Kuenzel, W.J., and A. VanTienhoven (1982) Nomenclature and location of avian hypothalamic nuclei and associated circumventricular organs. J. Comp. Neurol. 206:293-313.
51. Kuenzel, W.J., and M. Masson (1988) A stereotaxic atlas of the brain of the chick (Gallus domesticus). Baltimore: The Johns Hopkins University Press.
52. Lauber, M.E., and W. Lichtensteiger (1994) Pre-and postnatal ontogeny of aromatase cytochrome P450 messenger ribonucleic acid expression in the male rat brain studied by in situ hybridization. Endocrinology 135:1661-1668.
53. MacLusky, N.J., A. Philip, C. Hurlburt , and F. Naftolin (1984) Estrogen metabolism in neuroendocrine structures. In F. Celotti, F. Naftolin, and L. Martini (eds): Metabolism of Hormonal Steroids in the Neuroendocrine Structures. New York: Raven Press, pp. 103-116.
54. MacLusky, N.J., F. Naftolin, and P.S. Goldman-Rakic (1986) Estrogen formation and binding in the cerebral cortex of the developing rhesus monkey. Proc. Natl. Acad. Sci. USA 83.513-516.
55. MacLusky, N.J., A.S. Clark, F. Naftolin, and P.S. Goldman-Raldc (1987) Estrogen formation in the mammalian brain: Possible role of aromatase in sexual differentiation of the hippocampus and neocortex. Steroids 50:459-474.
56. McEwen, B.S. (1994a) How do sex and stress hormones affect nerve cells? Ann. NY Acad. Sci. 743:1-18.
57. McEwen, B.S. (1994b) Steroid hormone actions on the brain: When is the genome involved? Horm. Behav. 28:396-405.
58. McEwen, B.S. , and L.C. Krey (1984) Properties of estrogen-sensitive neurons: Aromatization, progestin receptor induction and neuroendocrine effects. In F. Celotti, F. Naftolin, and L. Martini (eds): Metabolism of Hormonal Steroids in the Neuroendocrine Structures. New York: Raven Press, pp. 117-128.
59. Mendelson, C.R., M.E. Smith, W.H. Cleland, and E.R. Simpson (1984) Regulation of aromatase activity of cultured adipose stromal cells by catecholamines and adrenocorticotropin. Mol. Cell. Endocrinol. 37: 61-72.
60. Nestler, E.J., and P. Greengard (1989) Protein phosphorylation and the regulation of neuronal function. In G.J. Siegel. B.W. Agranoff, R.W. Albers, and P.B. Molinoff (eds): Basic Neurochemistry. New York: Raven Press, pp. 373-398.
61. Osawa, Y., T. Higashiyama, Y. Shimizu, and C. Yarborough (1993) Multiple functions of aromatase and the active site structure; Aromatase is the placental estrogen 2-hydroxylase. J. Steroid Biochem. Mol. Biol. 44:469-480.
62. Osawa, Y., T. Higashiyama, and C. Yarborough (1994) Diverse functions of aromatase cyt P-450: Catecholestrogen synthesis, cocaine N-demethyl-ation, and other selective drug metabolisms. Abstr. 8th Int. Conf. on Cytochrome P450, 893-896.
63. Panzica, G.C, C. Viglietti-Panzica, F. Sanchez, P. Sante, and J. Balthazart (1991) Effects of testosterone on a selected neuronal population within the preoptic sexually dimorphic nucleus of the Japanese quail. J. Comp. Neurol. 303:443-456.
64. Panzica, G.C., C. Viglietti-Panzica, and J. Balthazart (1996) The sexually dimorphic medial preoptic nucleus of quail: A key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol. 17:51-125.
65. Pasqualini, C., V. Olivier, B. Guibert, O. Frain, and V. Leviel (1995) Acute stimulatory effect of estradiol on striatal dopamine synthesis. J. Neurochem. 65:1651-1657.
66. Reiner, A., E.J. Karle, K.D. Anderson , and L. Medina (1994) Catecholaminergic perikarya and fibers in the avian nervous system. In W.J.A.J. Smeets and A. Reiner (eds): Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates. Cambridge, UK: Cambridge University Press, pp. 135-181.
67. Roselli, C.E. , and J.A. Resko (1991) In vitro assay of aromatase activity in the central nervous system. In B. Greenstein (ed): Neuroendocrine Research Methods, Vol. 2. Chur, Switzerland: Harwood Academic-Publishers, pp. 937-951.
68. Saldanha, C.J., V.T. Cam, and B.A. Schlinger (1996) The songbird hippocampus is a site of high aromatase activity. Soc. Neurosci. Abstr. 22:691.
69. Schlinger, B.A., and A.P. Arnold (1991) Brain is the major site of estrogen synthesis in a male songbird. Proc. Natl. Acad. Sci. USA 88:4191-4194.
70. Schlinger, B.A., and G.V. Callard (1987) A comparison of aromatase, 5α-and 5β-reductase activities in the brain and pituitary of male and female quail (Coturnix c. Juponica ). J. Exp. Zool. 242:171-180.
71. Schumacher, M., and J. Balthazart (1983) The effects of testosterone and its metabolites on sexual behavior and morphology in male and female Japanese quail. Physiol. Behav. 30:335-339.
72. Schumacher, M., and J. Balthazart (1986) Testosterone-induced brain aromatase is sexually dimorphic. Brain Res. 370:285-293.
73. Schumacher, M., and J. Balthazart (1987) Neuroanatomical distribution of testosterone metabolizing enzymes in the Japanese quail. Brain Res. 422:137-148.
74. Shen, P., C.W. Campagnoni, K. Kampf, B.A. Schlinger, A.P. Arnold, and A.T. Campagnoni (1994) Isolation and characterization of a zebra finch aromatase cDNA: In situ hybridization reveals high aromatase expression in brain. Mol. Brain Res. 24:227-237.
75. Shen, P., B.A. Schlinger, A.T. Campagnoni, and A.P. Arnold (1995) An atlas of aromatase mRNA expression in the zebra finch brain. J. Comp. Neurol. 360:172-184.
76. Shimizu, Y., C. Yarborough, and Y. Osawa (1993) Competitive product inhibition of aromatase by natural estrogens. J. Steroid Biochem. Mol. Biol. 44:651-656.
77. Simerly, R.B. (1989) Hormonal control of the development and regulation of tyrosine hydroxylase expression within a sexually dimorphic population of dopaminergic cells in the hypothalamus. Mol. Brain Res. 6:297-310.
78. Simerly, R.B., and L.W. Swanson (1987) The distribution of neurotransmitter-specific cells and fibers in the anteroventral periventricular nucleus: Implications for the control of gonadotropin secretion in the rat. Brain Res. 400:11-34.
79. Simerly, R.B., L.W. Swanson, and R.A. Gorski (1985) The distribution of monoaminergic cells and fibers in a periventricular preoptic nucleus involved in the control of gonadotropin release: Immunohistochemical evidence for a dopaminergic sexual dimorphism. Brain Res. 330: 55-64.
80. Timmers, R.J.M., and J.G.D. Lambert (1988) Kinetic studies of the catechol-o-methyltransferase from the brain of the african catfish, Clarias gariepinus. Comp. Biochem. Physiol 91C:399-402.
81. Timmers, R.J.M., and J.G.D. Lambert (1989) Catechol-o-methyltransferase in the brain of the male african catfish, Clarias gariepinus: Distribution and significance for the metabolism of catecholestrogens and dopamine. Fish Physiol. Biochem. 7:201-210.
82. Verhoeven, G. (1980) Effect of neurotransmitters and follicle-stimulating hormone on the aromatization of androgens and the production of 3′,5′-monophosphate by cultured testicular cells. J. Steroid Biochem. 12:315-322.
83. Vockel, A., E. Pröve, and J. Balthazart (1990a) Sex-and age-related differences in the activity of testosterone-metabolizing enzymes in micrudissected nuclei of the zebra finch brain. Brain Res. 511:291-302.
84. Vockel, A., E. Pröve, and J. Balthazart (1990b) Effects of castration and testosterone treatment on the activity of testosterone-metabolizing enzymes in the brain of male and female zebra finches. J. Neurobiol. 21:808-825.
85. Wagner, C.K., and J.I. Morrell (1996) Distribution and steroid hormone regulation of aromatase mRNA expression in the forebrain of adult male and female rats: A cellular-level analysis using in situ hybridization. J. Comp. Neurol. 370:71-84.
86. 3H]-dihydrotestosterone. Neuroendocrinology 49:51-64.