Seredynski, Aurore ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Ball, Gregory F; Johns Hopkins University > Department of Psychology and Brain Sciences
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Charlier, Thierry ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
Specific activation of estrogen recepto alpha and beta enhances male sexual behavior and neuroplasticity in male Japanese quail
Publication date :
2011
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, San Franscisco, United States - California
Ball GF, Balthazart J, (2009) Neuroendocrine Regulation of Reproductive Behavior in Birds. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, Brain and Behavior. 2nd ed San Diego, CA Academic Press pp. 855-895.
Hull EM, Rodriguez-Manzo G, (2009) Male sexual behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, Brain aand Behavior San Diego, CA Academic Press pp. 5-65.
Balthazart J, Schumacher M, Malacarne G, (1985) Interaction of androgens and estrogens in the control of sexual behavior in male Japanese quail. Physiol Behav 35: 157-166.
Adkins EK, Pniewski EE, (1978) Control of reproductive behavior by sex steroids in male quail. J Comp Physiol Psychol 92: 1169-1178.
Schumacher M, Balthazart J, (1983) The effects of testosterone and its metabolites on sexual behavior and morphology in male and female Japanese quail. Physiol Behav 30: 335-339.
Ryan KJ, (1959) Biological aromatization of steroids. J Biol Chem 234: 268-272.
Naftolin F, Ryan KJ, Davies IJ, Petro Z, Kuhn M, (1975) The formation and metabolism of estrogens in brain tissue. Adv Biosci 15: 105-121.
Adkins EK, Boop JJ, Koutnik DL, Morris JB, Pnieswski EE, (1980) Further evidence that androgen aromatization is essential for the activation of copulation in male quail. Physiol Behav 24: 441-446.
Balthazart J, Foidart A, Surlemont C, Vockel A, Harada N, (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.
Schumacher M, Balthazart J, (1987) Neuroanatomical distribution of testosterone-metabolizing enzymes in the Japanese quail. Brain Res 422: 137-148.
Foidart A, Reid J, Absil P, Yoshimura N, Harada N, et al. (1995) 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.
Panzica GC, Viglietti-Panzica C, Balthazart J, (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.
Balthazart J, Ball GF, (2007) Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front Neuroendocrinol 28: 161-178.
Balthazart J, Tlemçani O, Harada N, (1996) Localization of testosterone-sensitive and sexually dimorphic aromatase-immunoreactive cells in the quail preoptic area. J Chem Neuroanat 11: 147-171.
Aste N, Panzica GC, Viglietti-Panzica C, Harada N, Balthazart J, (1998) Distribution and effects of testosterone on aromatase mRNA in the quail forebrain: A non-radioactive in situ hybridization study. J Chem Neuroanat 14: 103-115.
Viglietti-Panzica C, Aste N, Balthazart J, Panzica GC, (1994) Vasotocinergic innervation of sexually dimorphic medial preoptic nucleus of the male Japanese quail: Influence of testosterone. Brain Res 657: 171-184.
Panzica G, Pessatti M, Viglietti-Panzica C, Grossmann R, Balthazart J, (1999) Effects of testosterone on sexually dimorphic parvocellular neurons expressing vasotocin mRNA in the male quail brain. Brain Res 850: 55-62.
Panzica G, Aste N, Castagna C, Viglietti-Panzica C, Balthazart J, (2001) Steroid-induced plasticity in the sexually dimorphic vasotocinergic innervation of the avian brain: behavioral implications. Brain Res Rev 37: 178-200.
Absil P, Baillien M, Ball GF, Panzica G, Balthazart J, (2001) The control of preoptic aromatase activity by afferent inputs in Japanese quail. Brain Res Rev 37: 38-58.
Vasudevan N, Pfaff DW, (2007) Membrane-initiated actions of estrogen in neurobiology: emerging principles. Endocr Rev 28: 1-19.
McEwen BS, Alves SE, (1999) Estrogen actions in the central nervous system. Endocr Rev 20: 279-307.
Klinge CM, (2001) Estrogen receptor interaction with estrogen response elements. Nucleic Acid Res 29: 2905-2919.
Nilsson S, Mäkelä S, Treuter E, Tujague M, Thomsen J, et al. (2001) Mechanisms of estrogen action. Physiol Rev 81: 1535-1565.
Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schütz G, et al. (1995) The nuclear receptor superfamily: the second decade. Cell 83: 835-839.
Mosselman S, Polman J, Gustafsson J-A, (1996) ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett 392: 49-53.
Kuiper GGJM, Gustafsson J-Å, (1997) The novel estrogen receptor-beta subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett 410: 87-90.
Lakaye B, Foidart A, Grisar T, Balthazart J, (1998) Partial cloning and distribution of estrogen receptor beta in the avian brain. Neuroreport 9: 2743-2748.
Foidart A, Lakaye B, Grisar T, Ball GF, Balthazart J, (1999) Estrogen receptor-beta in quail: Cloning, tissue expression and neuroanatomical distribution. J Neurobiol 40: 327-342.
Halldin K, Axelsson J, Holmgren C, Brunstrom B, (2006) Localization of estrogen receptor-alpha and-beta mRNA in brain areas controlling sexual behavior in Japanese quail. J Neurobiol 66: 148-154.
PJ, Lane MV, Merchenthaler I, (1997) Comparative distribution of estrogen receptor alpha and beta mRNA in the rat central nervous system. J Comp Neurol 388: 507-525.
Kuiper GG, Shughrue PJ, Merchenthaler I, Gustafsson JA, (1998) The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol 19: 253-286.
Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, et al. (1998) Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A 95: 15677-15682.
Rissman EF, Wersinger SR, Fugger HN, Foster TC, (1999) Sex with knock-out models: behavioral studies of estrogen receptor alpha. Brain Res 835: 80-90.
Gustafsson JA, (1999) Estrogen receptor beta-a new dimension in estrogen mechanism of action. J Endocrinol 163: 379-383.
Weiser MJ, Foradori CD, Handa RJ, (2008) Estrogen receptor beta in the brain: from form to function. Brain Res Rev 57: 309-320.
Bodo C, Rissman EF, (2006) New roles for estrogen receptor beta in behavior and neuroendocrinology. Front Neuroendocrinol 27: 217-232.
Rissman EF, (2008) Roles of oestrogen receptors alpha and beta in behavioural neuroendocrinology: beyond Yin/Yang. J Neuroendocrinol 20: 873-879.
Dominguez-Salazar E, Bateman HL, Rissman EF, (2004) Background matters: the effects of estrogen receptor a gene disruption on male sexual behavior are modified by background strain. Horm Behav 46: 482-490.
Manas ES, Unwalla RJ, Xu ZB, Malamas MS, Miller CP, et al. (2004) Structure-based design of estrogen receptor-beta selective ligands. J Am Chem Soc 126: 15106-15119.
Malamas MS, Manas ES, McDevitt RE, Gunawan I, Xu ZB, et al. (2004) Design and synthesis of aryl diphenolic azoles as potent and selective estrogen receptor-beta ligands. J Med Chem 47: 5021-5040.
Meyers MJ, Sun J, Carlson KE, Marriner GA, Katzenellenbogen BS, et al. (2001) Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 44: 4230-4251.
Stauffer SR, Coletta CJ, Tedesco R, Nishiguchi G, Carlson K, et al. (2000) Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem 43: 4934-4947.
Mazzucco CA, Walker HA, Pawluski JL, Lieblich SE, Galea LA, (2008) ERalpha, but not ERbeta, mediates the expression of sexual behavior in the female rat. Behav Brain Res 191: 111-117.
Clipperton-Allen AE, Almey A, Melichercik A, Allen CP, Choleris E, (2011) Effects of an estrogen receptor alpha agonist on agonistic behaviour in intact and gonadectomized male and female mice. Psychoneuroendocrinology. In press doi:10.1016/j.psyneuen.2010.12.010.
Hammond R, Mauk R, Ninaci D, Nelson D, Gibbs RB, (2009) Chronic treatment with estrogen receptor agonists restores acquisition of a spatial learning task in young ovariectomized rats. Horm Behav 56: 309-314.
Jacome LF, Gautreaux C, Inagaki T, Mohan G, Alves S, et al. (2010) Estradiol and ERbeta agonists enhance recognition memory, and DPN, an ERbeta agonist, alters brain monoamines. Neurobiol Learn Mem 94: 488-498.
Neese SL, Korol DL, Katzenellenbogen JA, Schantz SL, (2010) Impact of estrogen receptor alpha and beta agonists on delayed alternation in middle-aged rats. Horm Behav 58: 878-890.
Balthazart J, Absil P, Gérard M, Appeltants D, Ball GF, (1998) Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J Neurosci 18: 6512-6527.
Schumacher M, Balthazart J, (1984) The postnatal demasculinization of sexual behavior in the Japanese quail. Horm Behav 18: 298-312.
Balthazart J, Schumacher M, Ottinger MA, (1983) Sexual differences in the Japanese quail: behavior, morphology and intracellular metabolism of testosterone. Gen Comp Endocrinol 51: 191-207.
Sachs BD, (1967) Photoperiodic control of the cloacal gland of the Japanese quail. Science 157: 201-203.
Delville Y, Hendrick JC, Sulon J, Balthazart J, (1984) Testosterone metabolism and testosterone-dependent characteristics in Japanese quail. Physiol Behav 33: 817-823.
Adkins EK, Adler NT, (1972) Hormonal control of behavior in the Japanese quail. J Comp Physiol Psychol 81: 27-36.
Hutchison RE, (1978) Hormonal differentiation of sexual behavior in Japanese quail. Horm Behav 11: 363-387.
Seiwert CM, Adkins-Regan E, (1998) The foam production system of the male japanese quail: characterization of structure and function. Brain Behav Evol 52: 61-80.
Cornil CA, Holloway KS, Taziaux M, Balthazart J, (2004) The effects of aromatase inhibition on testosterone-dependent conditioned rhythmic cloacal sphincter movement in male Japanese quail. Physiol Behav 83: 99-105.
Carere C, Ball GF, Balthazart J, (2007) Sex differences in projections from preoptic area aromatase cells to the periaqueductal gray in Japanese quail. J Comp Neurol 500: 894-907.
Gray DA, Simon E, (1983) Mammalian and avian antidiuretic hormone: studies related to possible specise variation in osmoregulatory systems. J Comp Physiol 151: 241-246.
Beach FA, (1956) Characteristics of masculine "sex drive". Nebraska Symposium on Motivation 4: 1-32.
Pfaus JG, (1996) Frank A. Beach award. Homologies of animal and human sexual behaviors. Horm Behav 30: 187-200.
Ball GF, Balthazart J, (2008) How useful is the appetitive and consummatory distinction for our understanding of the neuroendocrine control of sexual behavior? Horm Behav 53: 307-311; author reply 315-308.
Balthazart J, Reid J, Absil P, Foidart A, Ball GF, (1995) Appetitive as well as consummatory aspects of male sexual behavior in quail are activated by androgens and estrogens. Behav Neurosci 109: 485-501.
Balthazart J, Ball GF, (1997) Neuroendocrine regulation of appetitive and consummatory aspects of male sexual behavior in Japanese quail. In: Etches R, Harvey S, editors. Perspectives in Avian Endocrinology Bristol, UK Society for Endocrinology pp. 241-255.
Balthazart J, Ball GF, (1998) The Japanese quail as a model system for the investigation of steroid-catecholamine interactions mediating appetitive and consummatory aspects of male sexual behavior. Ann Rev Sex Res 9: 96-176.
Domjan M, (1987) Photoperiodic and endocrine control of social proximity behavior in male Japanese quail (Coturnix coturnix japonica). Behav Neurosci 101: 385-392.
Domjan M, Hall S, (1986) Determinants of social proximity in Japanese quail (Coturnix coturnix japonica): male behavior. J Comp Psychol 100: 59-67.
Thompson RR, Goodson JL, Ruscio MG, Adkins-Regan E, (1998) Role of the archistriatum nucleus taeniae in the sexual behavior of male Japanese quail (Coturnix japonica): a comparison of function with the medial nucleus of the amygdala in mammals. Brain Behav Evol 51: 215-229.
Balthazart J, Castagna C, Ball GF, (1997) Aromatase inhibition blocks the activation and sexual differentiation of appetitive male sexual behavior in Japanese quail. Behav Neurosci 111: 381-397.
Taziaux M, Cornil CA, Balthazart J, (2004) Aromatase inhibition blocks the expression of sexually-motivated cloacal gland movements in male quail. Behav Processes 67: 461-469.
Balthazart J, Gahr M, Surlemont C, (1989) Distribution of estrogen receptors in the brain of the Japanese quail: an immunocytochemical study. Brain Res 50: 205-214.
Voigt C, Ball GF, Balthazart J, (2009) Sex differences in the expression of sex steroid receptor mRNA in the quail brain. J Neuroendocrinol 21: 1045-1062.
Balthazart J, Evrard L, Surlemont C, (1990) Effects of the non-steroidal inhibitor R76713 on testosterone-induced sexual behavior in the Japanese quail (Coturnix coturnix japonica). Horm Behav 24: 510-531.
Adkins EK, Nock BL, (1976) The effects of the antiestrogen CI-628 on sexual behavior activated by androgen and estrogen in quail. Horm Behav 7: 417-429.
Alexandre C, Balthazart J, (1986) Effects of metabolism inhibitors, antiestrogens and antiandrogens on the androgen and estrogen induced sexual behavior in Japanese quail. Physiol Behav 38: 581-591.
Harada N, Abe-Dohmae S, Loeffen R, Foidart A, Balthazart J, (1993) Synergism between androgens and estrogens in the induction of aromatase and its messenger RNA in the brain. Brain Res 622: 243-256.
Balthazart J, Stoop R, Foidart A, Harada N, (1994) Synergistic control by androgens and estrogens of aromatase in the quail brain. Neuroreport 5: 1729-1732.
Roselli CE, (1991) Synergistic induction of aromatase activity in the rat brain by estradiol and 5 alpha-dihydrotestosterone. Neuroendocrinology 53: 79-84.
Charlier TD, Ball GF, Balthazart J, (2008) Rapid action on neuroplasticity precedes behavioral activation by testosterone. Horm Behav 54: 488-495.
Balthazart J, Foidart A, Hendrick JC, (1990) The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol Behav 47: 83-94.
Balthazart J, Foidart A, Houbart M, Prins GS, Ball GF, (1998) Distribution of androgen receptor-immunoreactive cells in the quail forebrain and their relationship with aromatase immunoreactivity. J Neurobiol 35: 323-340.
Balthazart J, Foidart A, Surlemont C, Harada N, (1991) Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors. J Neurobiol 22: 143-157.
Absil P, Papello M, Viglietti-Panzica C, Balthazart J, Panzica G, (2002) The medial preoptic nucleus receives vasotocinergic inputs in male quail: a tract-tracing and immunocytochemical study. J Chem Neuroanat 24: 27-39.
Shapiro RA, Xu C, Dorsa DM, (2000) Differential transcriptional regulation of rat vasopressin gene expression by estrogen receptor alpha and beta. Endocrinology 141: 4056-4064.
Axelson JF, Leeuwen FW, (1990) Differential localization of estrogen receptors in various vasopressin synthesizing nuclei of the rat brain. J Neuroendocrinol 2: 209-216.
Hrabovsky E, Kallò I, Hajszan T, Shugrue PJ, Merchenthaler I, et al. (1998) Expression of estrogen receptor-β messenger ribonucleic acid in oxytocin and vasopressin neurons of the rat supraoptic and paraventricular nuclei. Endocrinology 139: 2600-2604.
Alves SE, Lopez V, McEwen BS, Weiland NG, (1998) Differential colocalization of estrogen receptor beta (ERbeta) with oxytocin and vasopressin in the paraventricular and supraoptic nuclei of the female rat brain: an immunocytochemical study. Proc Natl Acad Sci U S A 95: 3281-3286.
Laflamme N, Nappi RE, Drolet G, Labrie C, Rivest S, (1998) Expression and neuropeptidergic characterization of estrogen receptors (ERalpha and ERbeta) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J Neurobiol 36: 357-378.
Panzica GC, Castagna C, Viglietti-Panzica C, Russo C, Tlemçani O, et al. (1998) Organizational effects of estrogens on brain vasotocin and sexual behavior in quail. J Neurobiol 37: 684-699.
Mattsson A, Mura E, Brunstrom B, Panzica G, Halldin K, (2008) Selective activation of estrogen receptor alpha in Japanese quail embryos affects reproductive organ differentiation but not the male sexual behavior or the parvocellular vasotocin system. Gen Comp Endocrinol 159: 150-157.
Watson JT, Adkins-Regan E, (1989) Neuroanatomical localization of sex steroid-concentrating cells in the japanese quail (Coturnix japonica): autoradiography with [3H]-testosterone, [3H]-estradiol and [3H]-dihydrotestosterone. Neuroendocrinology 49: 51-64.
Absil P, Braquenier JB, Balthazart J, Ball G, (2002) Effects of lesions of nucleus taeniae on appetitive and consummatory aspects of male sexual behavior in japanese quail. Brain Behav Evol 60: 13-35.
Balthazart J, Surlemont C, (1990) Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol Behav 48: 599-609.
Rissman EF, Wersinger SR, Fugger HN, Foster TC, (1999) Sex with knockout models: behavioral studies of estrogen receptor alpha. Brain Res 835: 80-90.
Temple JL, Fugger HN, Li X, Shetty SJ, Gustafsson J, et al. (2001) Estrogen receptor beta regulates sexually dimorphic neural responses to estradiol. Endocrinology 142: 510-513.
Temple JL, Scordalakes EM, Bodo C, Gustafsson JA, Rissman EF, (2003) Lack of functional estrogen receptor beta gene disrupts pubertal male sexual behavior. Horm Behav 44: 427-434.
Rissman EF, Early AH, Taylor JA, Korach KS, Lubahn DB, (1997) Estrogen receptors are essential for female sexual receptivity. Endocrinology 138: 507-510.
Scordalakes EM, Imwalle DB, Rissman EF, (2002) Oestrogen's masculine side: mediation of mating male mice. Reproduction 124: 331-338.
Ogawa S, Washburn TF, Taylor J, Lubahn DB, Korach KS, et al. (1998) Modifications of testosterone-dependent behaviors by estrogen receptor-alpha gene disruption in male mice. Endocrinology 139: 5058-5069.
Nomura M, Andersson S, Korach KS, Gustafsson JA, Pfaff DW, et al. (2006) Estrogen receptor-beta gene disruption potentiates estrogen-inducible aggression but not sexual behaviour in male mice. Eur J Neurosci 23: 1860-1868.
Scordalakes EM, Rissman EF, (2003) Aggression in male mice lacking functional estrogen receptor alpha. Behav Neurosci 117: 38-45.
Choleris E, Gustafsson JA, Korach KS, Muglia LJ, Pfaff DW, et al. (2003) An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-alpha and-beta knockout mice. Proc Natl Acad Sci U S A 100: 6192-6197.
Choleris E, Kavaliers M, Pfaff DW, (2004) Functional genomics of social recognition. J Neuroendocrinol 16: 383-389.
Patisaul HB, Scordalakes EM, Young LJ, Rissman EF, (2003) Oxytocin, but not oxytocin receptor, is regulated by oestrogen receptor beta in the female mouse hypothalamus. J Neuroendocrinol 15: 787-793.
Nomura M, Korach KS, Pfaff DW, Ogawa S, (2003) Estrogen receptor beta (ERbeta) protein levels in neurons depend on estrogen receptor alpha (ERalpha) gene expression and on its ligand in a brain region-specific manner. Brain Res Mol Brain Res 110: 7-14.
Tetel MJ, Pfaff DW, (2010) Contributions of estrogen receptor-alpha and estrogen receptors to the regulation of behavior. Biochim Biophys Acta 1800: 1084-1089.
Rhodes ME, Frye CA, (2006) ERbeta-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiol Learn Mem 85: 183-191.
Walf AA, Frye CA, (2005) ERbeta-selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats. Neuropsychopharmacology 30: 1598-1609.
Grassi D, Amorim MA, Garcia-Segura LM, Panzica G, (2010) Estrogen receptor alpha is involved in the estrogenic regulation of arginine vasopressin immunoreactivity in the supraoptic and paraventricular nuclei of ovariectomized rats. Neurosci Lett 474: 135-139.
Lund TD, Rovis T, Chung WC, Handa RJ, (2005) Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 146: 797-807.