[en] Testosterone (T) increases brain aromatase activity (AA) in quail and other avian and mammalian species. It was shown both in quail and in rat that this enzymatic induction results from a synergistic action of androgens and estrogens. These studies provide little information on possible anatomical or cellular specificity of the effect. Using a polyclonal antiserum against human placental aromatase, we have previously identified aromatase-immunoreactive (ARO-ir) neurons in the quail brain and demonstrated that T increases the number of ARO-ir cells in the quail preoptic area (POA) supporting previous evidence that T increases AA in the brain. However, which T metabolites are involved, the actual mechanism of regulation and the possibility of anatomical specificity for these effects are not yet clear. In the present study, we disassociated the effects of androgens and estrogens in aromatase induction by comparing ARO-ir neurons of quail treated with T alone or T in the presence of a potent aromatase inhibitor (R76713), which has been shown to depress AA levels and to suppress T-activated copulatory behavior. T increased the number of ARO-ir cells in POA, bed nucleus striae terminalis (BNST) and tuberal hypothalamus (Tu). The T effect was inhibited by concurrent treatment with aromatase inhibitor in Tu, but not in POA and BNST. This differential effect of the aromatase inhibitor fits in very well with our previous studies of the co-localization of aromatase and estrogen receptors. The T effect was blocked by R76713 in areas where ARO-ir and estrogen receptor-ir are generally co-localized (Tu) and was not affected in areas with mainly ARO-ir positive, estrogen receptor-ir negative cells (POA, BNST). This suggests anatomical differences in the expression or clearance of aromatase which may be differentially sensitive to androgens and estrogens and dependent upon the presence of sex steroid receptors.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Foidart, Agnès ; Université de Liège - ULiège > Services généraux (Faculté de médecine) > Service administratif de la Faculté (Médecine)
Surlemont, C.
Harada, N.
Naftolin, F.
Language :
English
Title :
Neuroanatomical Specificity in the Autoregulation of Aromatase-Immunoreactive Neurons by Androgens and Estrogens: An Immunocytochemical Study
Adkins (1977) Effects of diverse androgens on the sexual behavior and morphology of castrated male quail. Horm. Behav. 8:201-207.
Adkins, Adler (1972) Hormonal control of behavior in the Japanese quail. J. Comp. Physiol. Psychol. 81:27-36.
Adkins, Boop, Koutnik, Morris, Pniewski (1980) Further evidence that androgen aromatization is essential for the activation of copulation in male quail. Physiol. Behav. 24:441-446.
Balthazart (1989) Steroid metabolism and the activation of social behavior. Advances in Comparative and Environmental Physiology , Third Edition, J. Balthazart, Springer, Berlin; 3:105-159.
Balthazart (1989) Correlation between the sexually dimorphic aromatase of the preoptic area and sexual behavior in quail: effects of neonatal manipulations of the hormonal milieu. Arch. Int. Physiol. Biochem. 97:465-481.
Balthazart (1991) Testosterone metabolism in the avian hypothalamus. J. Steroid Biochem. Mol. Biol. 40:557-570.
Balthazart, Evrard, Surlemont (1990) Effects of the non-steroidal aromatase inhibitor, R76713 on testosterone-induced sexual behavior in the Japanese quail (Coturnix coturnix japonica). Horm. Behav. 24:510-531.
Balthazart, Foidart, Harada (1990) Immunocytochemical localization of aromatase in the brain. Brain Research 514:327-333.
Balthazart, Foidart, Hendrick (1990) The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol. Behav. 47:83-94.
Balthazart, Foidart, Surlemont, Harada (1990) Preoptic aromatase in quail: behavioral, biochemical and immunocytochemical studies. Hormones, Brain and Behavior in Vertebrates. 2. Behavioral Activation in Males and Females — Social Interactions and Reproductive Physiology, Comp. Physiol. , Third Edition, J. Balthazart, Karger, Basel; 9:45-62.
Balthazart, Foidart, Surlemont, Harada (1991) Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors. J. Neurobiol. 22:143-157.
Balthazart, Foidart, Surlemont, Vockel, Harada (1990) Distribution of aromatase in the brain of the Japanese quail, ring dove, and zebra finch: an immunocytochemical study. J. Comp. Neurol. 301:276-288.
.
Balthazart, Schumacher, Evrard (1990) Sex differences and steroid control of testosterone-metabolizing enzyme activity in the quail brain. J. Neuroendocrinol. 2:675-683.
Balthazart, Schumacher, Ottinger (1983) Sexual differences in the Japanese quail: behavior, morphology and intracellular metabolism of testosterone. Gen. Comp. Endocrinol. 51:191-207.
Balthazart, Surlemont (1990) Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail POA. Brain Res. Bull. 25:7-14.
Balthazart, Surlemont (1990) Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol. Behav. 48:599-609.
Baylé, Ramade, Oliver (1974) Stereotaxic topography of the brain of the quail. J. Physiol. (Paris) 68:219-241.
Callard, Schlinger, Pasmanik, Corina (1990) Aromatization and estrogen action in the brain. Progress in Comparative Endocrinology , A. Epple, C.G. Scanes, M.H. Stetson, Wiley-Liss, New York; 105-111.
Callard, Petro, Ryan (1978) Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology 103:2283-2290.
De Coster, Wouters, Bowden, Vanden Bossche, Bruynseels, Tuman, Van Ginckel, Snoeck, Van Peer, Janssen (1990) New non-steroidal aromatase inhibitors: focus on R76713. J. Steroid Biochem. 37:335-341.
Döhler, Hancke, Srivastava, Hofman, Shryne, Gorski (1984) Participation of estrogens in female sexual differentiation of the brain; neuroanatomical, neuroendocrine and behavioral evidence. Prog. Brain Res. 61:99-117.
Harada (1988) Novel properties of human placental aromatase as cytochrome P-450: purification and characterization of a unique form of aromatase. J. Biochem. 103:106-113.
Hutchison, Joris, Hutchison, Steimer (1989) Steroid control of sexual behavior and brain aromatase in the dove: effects of nonaromatizable androgens, methyltrienolone (R1881), and 5α-dihydrotestosterone. Horm. Behav. 23:542-555.
Hutchison, Schumacher (1986) Development of testosterone-metabolizing pathways in the avian brain: enzyme localization and characteristics. Dev. Brain Res. 25:33-42.
Hutchison, Steimer (1986) Formation of behaviorally effective 17β-estradiol in the dove brain: steroid control of preoptic aromatase. Endocrinology 118:2180-2187.
Hutchison, Steimer, Hutchison (1986) Formation of behaviorally active estrogen in the dove brain: induction of preoptic aromatase by intracranial testosterone. Neuroendocrinology 43:416-427.
Hutchison (1978) Hormonal differentiation of sexual behavior in Japanese quail. Horm. Behav. 11:363-387.
Kuenzel, Masson A Stereotaxic Atlas of the Brain of the Chick (Gallus domesticus) , The Johns Hopkins University Press, Baltimore; 1988, 1-166.
Kuenzel, VanTienhoven (1982) Nomenclature and location of avian hypothalamic nuclei and associated circumventricular organs. J. Comp. Neurol. 206:293-313.
Lephart, Ojeda (1990) Hypothalamic aromatase activity in male and female rats during juvenile peripubertal development. Neuroendocrinology 51:385-393.
MacLusky, Clark, Naftolin, Goldman-Rakic (1987) Estrogen formation in the mammalian brain: possible role of aromatase in sexual differentiation of the hippocampus and neocortex. Steroids 50:459-474.
Naftolin, Garcia-Segura, Keefe, Leranth, MacLusky, Brawer (1990) Estrogen effects on the synaptology and neural membranes of the rat hypothalamic arcuate nucleus. Biol. Reprod. 42:21-28.
Naftolin, MacLusky (1984) Aromatization hypothesis revisited. Sexual Differentiation: Basic and Clinical Aspects , M. Serio, M. Motta, M. Zanisi, L. Martini, Raven, New York; 79-91.
Naftolin, MacLusky, Leranth, Sakamoto, Garcia-Segura (1988) The cellular effects of estrogens on neuroendocrine tissues. J. Steroid Biochem. 30:195-207.
Naftolin, Ryan, Davies, Reddy, Flores, Petro, Kuhn, White, Takaoka, Wolin (1975) The formation of estrogens by central neuroendocrine tissues. Rec. Prog. Horm. Res. 31:295-319.
Naftolin, Ryan, Petro (1972) Aromatization of androstenedione by the anterior hypothalamus of adult male and female rats. Endocrinology 90:295-298.
Palkovits (1973) Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Research 59:449-450.
Palkovits, Brownstein (1983) Microdissection of brain areas by the punch technique. Brain Microdissection Techniques , A.C. Cuello, Wiley, New York; 1-36.
Panzica, Viglietti-Panzica, Calcagni, Anselmetti, Schumacher, Balthazart (1987) Sexual differentiation and hormonal control of the sexually dimorphic preoptic median nucleus in quail. Brain Research 416:59-68.
Panzica, Viglietti-Panzica, Sanchez, Sante, Balthazart (1991) Effects of testosterone on a selected neuronal population within the preoptic sexually dimorphic nucleus of Japanese quail. J. Comp. Neurol. 303:443-456.
Roselli (1991) Synergistic induction of aromatase activity in the rat brain by estradiol and 5α-dihydrotestosterone. Neuroendocrinology 53:79-84.
Roselli, Horton, Resko (1985) Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 117:2471-2477.
Roselli, Horton, Resko (1987) Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area. Biol. Reprod. 37:628-633.
Roselli, Resko (1984) Androgens regulate brain aromatase activity in adult male rats through a receptor mechanism. Endocrinology 114:2183-2189.
Roselli, Resko (1989) Testosterone regulates aromatase activity in discrete brain areas of male rhesus macaques. Biol. Reprod. 40:929-934.
Sar, Lubahn, French, Wilson (1990) Immunohistochemical localization of the androgen receptor in rat and human tissues. Endocrinology 127:3180-3186.
Schlinger, Callard (1987) A comparison of aromatase, 5α- and 5β-reductase activities in the brain and pituitary of male and female quail (Coturnix C. Japonica). J. Exp. Zool. 242:171-180.
Schlinger, Callard (1989) Aromatase activity in quail brain: correlation with aggressiveness. Endocrinology 124:437-443.
Schlinger, Callard (1990) Aromatization mediates aggressive behavior in quail. Gen. Comp. Endocrinol. 79:39-53.
Schlinger, Fivizzani, Callard (1989) Aromatase, 5α- and 5β-reductase in brain, pituitary and skin of the sex-role reversed Wilson's phalarope. J. Endocrinol. 122:573-581.
Schumacher, Alexandre, Balthazart (1987) Interactions des androgènes et des oestrogènes dans le controˆle de la reproduction. C.R. Acad. Sci. Paris, Ser. III 305:569-574.
Schumacher, 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.
Schumacher, Balthazart (1984) The postnatal demasculinization of sexual behavior in the Japanese quail. Horm. Behav. 18:298-312.
Schumacher, Balthazart (1986) Testosterone-induced brain aromatase is sexually dimorphic. Brain Research 370:285-293.
Schumacher, Balthazart (1987) Neuroanatomical distribution of testosterone metabolizing enzymes in the Japanese quail. Brain Research 422:137-148.
Schumacher, Hutchison (1986) Testosterone induces hypothalamic aromatase during early development in quail. Brain Research 377:63-72.
Steimer, Hutchison (1981) Androgen increases formation of behaviourally effective oestrogen in dove brain. Nature 292:345-347.
Steimer, Hutchison (1989) Is the androgen-dependent increase in preoptic estradiol-17β formation due to aromatase induction. Brain Research 480:335-339.
Steimer (1990) Is lateral asymmetry in androgen-dependent aromatase activity sexually differentiated in the rat preoptic area (POA)?. Neuroendocrinology , (Abstract); 52/S1:50.
Steimer, Hutchison (1980) Aromatization of testosterone within a discrete hypothalamic area associated with the behavioral action of androgen in the male dove. Brain Research 192:586-591.
Viglietti-Panzica, Panzica, Fiori, Calcagni, Anselmetti, Balthazart (1986) A sexually dimorphic nucleus in the quail preoptic area. Neurosci. Lett. 64:129-134.
Vockel, Pröve, Balthazart (1990) Sex- and age-related differences in the activity of testosterone-metabolizing enzymes in microdissected nuclei of the zebra finch brain. Brain Research 511:291-302.
Vockel, Pröve, Balthazart (1990) 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.
Watson, Adkins-Regan (1989) Testosterone implanted in the preoptic area of male Japanese quail must be aromatized to activate copulation. Horm. Behav. 23:432-447.
Watson, Adkins-Regan (1989) Activation of sexual behavior by implantation of testosterone propionate and estradiol benzoate into the preoptic area of the male Japanese quail (Coturnix japonica). Horm. Behav. 23:251-268.
Wouters, De Coster, Krekels, Van Dun, Beerens, Haelterman, Raeymaekers, Freyne, Van Gelder, Venet, Janssen (1989) R 76713, a new specific non-steroidal aromatase inhibitor. J. Steroid Biochem. 32:781-788.
