[en] Oestrogens activate nucleus- and membrane-initiated signalling. Nucleus-initiated events control
a wide array of physiological and behavioural responses. These effects generally take place
within relatively long periods of time (several hours to days). By contrast, membrane-initiated
signalling affects a multitude of cellular functions in a much shorter timeframe (seconds to
minutes). However, much less is known about their functional significance. Furthermore, the origin
of the oestrogens able to trigger these acute effects is rarely examined. Finally, these two
distinct types of oestrogenic actions have often been studied independently such that we do
not exactly know how they cooperate to control the same response. The present review presents
a synthesis of recent work carried out in our laboratory that aimed to address these issues in
the context of the study of male sexual behaviour in Japanese quail, which is a considered as a
suitable species for tackling these issues. The first section presents data indicating that 17b-oestradiol,
or its membrane impermeable analogues, acutely enhances measures of male sexual
motivation but does not affect copulatory behaviour. These effects depend on the activation of
membrane-initiated events and local oestrogen production. The second part of this review discusses
the regulation of brain oestrogen synthesis through post-translational modifications of
the enzyme aromatase. Initially discovered in vitro, these rapid and reversible enzymatic modulations
occur in vivo following variations in the social and environment context and therefore
provide a mechanism of acute regulation of local oestrogen provision with a spatial and time
resolution compatible with the rapid effects observed on male sexual behaviour. Finally, we
discuss how these distinct modes of oestrogenic action (membrane- versus nucleus-initiated)
acting in different time frames (short- versus long-term) interact to control different components
(motivation versus performance) of the same behavioural response and improve reproductive
fitness.
Research center :
Giga-Neurosciences - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Seredynski, Aurore ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
de Bournonville, Catherine ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Dickens, Molly
Charlier, Thierry
Ball, Gregory F
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
Rapid control of reproductive behaviour by locally synthesised oestrogens: focus on aromatase.
Publication date :
2013
Journal title :
Journal of Neuroendocrinology
ISSN :
0953-8194
eISSN :
1365-2826
Publisher :
Blackwell Publishing, Oxford, United Kingdom
Volume :
25
Issue :
11
Pages :
1070-8
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NIMH - National Institute of Mental Health [US-MD] [US-MD] FRFC - Fonds de la Recherche Fondamentale Collective [BE] ULg FSR - Université de Liège. Fonds spéciaux pour la recherche [BE] NSF - National Science Foundation [US-VA] [US-VA] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Funding number :
FRFC (Nbr. 2.4537.9); NSF International research Fellowship (IRFP 0910495) to MJD
Etgen AM, Pfaff DW. Molecular mechanisms of hormone action on behavior. Academic Press: San Diego, CA, 2009.
Do Rego JL, Seong JY, Burel D, Leprince J, Luu-The V, Tsutsui K, Tonon MC, Pelletier G, Vaudry H. Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides. Front Neuroendocrinol 2009; 30: 259-301.
Santen RJ, Brodie H, Simpson ER, Siiteri PK, Brodie A. History of aromatase: saga of an important biological mediator and therapeutic target. Endocr Rev 2009; 30: 343-375.
Balthazart J, Baillien M, Cornil CA, Ball GF. Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol Behav 2004; 83: 247-270.
Roselli CE, Liu M, Hurn PD. Brain aromatization: classic roles and new perspectives. Semin Reprod Med 2009; 27: 207-217.
Cornil CA, Charlier TD. Rapid behavioural effects of oestrogens and fast regulation of their local synthesis by brain aromatase. J Neuroendocrinol 2010; 22: 664-673.
Charlier TD, Cornil CA, Ball GF, Balthazart J. Diversity of mechanisms involved in aromatase regulation and estrogen action in the brain. Biochim Biophys Acta 2010; 1800: 1094-1105.
Etgen AM. Estrogen regulation of neurotransmitter and growth factor signaling in the brain. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds. Hormones, Brain and Behavior. San Diego, CA: Academic Press, 2002.
Vasudevan N, Pfaff DW. Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front Neuroendocrinol 2008; 29: 238-257.
Micevych P, Dominguez R. Membrane estradiol signaling in the brain. Front Neuroendocrinol 2009; 30: 315-327.
Cornil CA, Ball GF, Balthazart J. Rapid control of male typical behaviors by brain-derived estrogens. Front Neuroendocrinol 2012; 33: 425-446.
Kelly MJ, Ronnekleiv OK. Membrane-initiated actions of estradiol that regulate reproduction, energy balance and body temperature. Front Neuroendocrinol 2012; 33: 376-387.
Micevych P, Christensen A. Membrane-initiated estradiol actions mediate structural plasticity and reproduction. Front Neuroendocrinol 2012; 33: 331-341.
Luine VN, Frankfurt M. Estrogens facilitate memory processing through membrane mediated mechanisms and alterations in spine density. Front Neuroendocrinol 2012; 33: 388-402.
Gintzler AR, Liu NJ. Importance of sex to pain and its amelioration; relevance of spinal estrogens and its membrane receptors. Front Neuroendocrinol 2012; 33: 412-424.
Terasawa E, Kenealy BP. Neuroestrogen, rapid action of estradiol, and GnRH neurons. Front Neuroendocrinol 2012; 33: 364-375.
Ball GF, Balthazart J. Japanese quail as a model system for studying the neuroendocrine control of reproductive and social behaviors. ILAR J 2010; 51: 310-325.
Cross E, Roselli CE. 17β-estradiol rapidly facilitates chemoinvestigation and mounting in castrated male rats. Am J Physiol 1999; 276: R1346-R1350.
Cornil CA, Dalla C, Papadopoulou-Daifoti Z, Baillien M, Balthazart J. Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain. Behav Brain Res 2006; 66: 110-123.
Cornil CA, Taziaux M, Baillien M, Ball GF, Balthazart J. Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail. Horm Behav 2006; 49: 45-67.
Cornil CA, Stevenson TJ, Ball GF. Are rapid changes in gonadal testosterone release involved in the fast modulation of brain estrogen effects? Gen Comp Endocrinol 2009; 163: 298-305.
Taziaux M, Cornil CA, Balthazart J. Aromatase inhibition blocks the expression of sexually-motivated cloacal gland movements in male quail. Behav Process 2004; 67: 461-469.
Balthazart J, Castagna C, Ball GF. Aromatase inhibition blocks the activation and sexual differentiation of appetitive male sexual behavior in japanese quail. Behav Neurosci 1997; 111: 381-397.
Balthazart J, Evrard L, Surlemont C. Effects of the non-steroidal inhibitor R76713 on testosterone-induced sexual behavior in the japanese quail (Coturnix coturnix japonica). Horm Behav 1990; 24: 510-531.
Seredynski AL, Balthazart J, Christophe VJ, Ball GF, Cornil CA. Neuroestrogens rapidly regulate sexual motivation but not performance. J Neurosci 2013; 33: 164-174.
Vasudevan N, Kow L-M, Pfaff DW. Early membrane estrogenic effects required for full expression of slower genomic actions in a nerve cell line. Proc Natl Acad Sci USA 2001; 98: 12267-12271.
Kow L-M, Pfaff DW. The membrane actions of estrogens can potentiate their lordosis behavior-facilitating genomic actions. Proc Natl Acad Sci USA 2004; 101: 12354-12357.
Cornil CA, Ball GF, Balthazart J. Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res 2006; 1126: 2-26.
Roselli CE. The distribution and regulation of aromatase in the mammalian brain: from mice to monkeys. In: Balthazart J, Ball GF, eds. Brain Aromatase, Estrogens and Behavior. Oxford: Oxford University Press 2012: 43-63.
Schlinger BA, Balthazart J. Aromatase and Behavior: concept gained from studies of aromatase in the avian brain. In: Balthazart J, Ball GF, eds. Aromatase, Estrogens and Behavior. Oxford: Oxford University Press, 2012; 169-199.
Balthazart J, Schumacher M, Evrard L. Sex differences and steroid control of testosterone-metabolizing enzyme activity in the quail brain. J Neuroendocrinol 1990; 2: 675-683.
Vockel A, Pröve E, Balthazart J. Effects of castration and testosterone treatment on the activity of testosterone-metabolizing enzymes in the brain of male and female zebra finches. J Neurobiol 1990; 21: 808-825.
Hutchison JB, Steimer TH. Formation of behaviorally effective 17β-estradiol in the dove brain: steroid control of preoptic aromatase. Endocrinology 1986; 118: 2180-2187.
Roselli CE, Horton LE, Resko JA. Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 1985; 117: 2471-2477.
Roselli CE, Stadelman H, Horton LE, Resko JA. Regulation of androgen metabolism and luteinizing hormone-releasing hormone content in discrete hypothalamic and limbic areas of male rhesus macaques. Endocrinology 1987; 120: 97-106.
Resko JA, Pereyra-Martinez AC, Stadelman HL, Roselli CE. Region-specific regulation of cytochrome P450 aromatase messenger ribonucleic acid by androgen in brains of male rhesus monkeys. Biol Reprod 2000; 62: 1818-1822.
Abdelgadir SE, Resko JA, Ojeda SR, Lephart ED, McPhaul MJ, Roselli CE. Androgens regulate aromatase cytochrome P450 messenger ribonucleic acid in rat brain. Endocrinology 1994; 135: 395-401.
Roselli CE, Stormshak F, Resko JA. Distribution and regulation of aromatase activity in the ram hypothalamus and amygdala. Brain Res 1998; 811: 105-110.
Voigt C, Ball GF, Balthazart J. Effects of sex steroids on aromatase mRNA expression in the male and female quail brain. Gen Comp Endocrinol 2011; 170: 180-188.
Schumacher M, Alexandre C, Balthazart J. Interactions des androgènes et des oestrogènes dans le contrôle de la reproduction. CR Acad Sci Paris 1987; 305: 569-574.
Roselli CE. Synergistic induction of aromatase activity in the rat brain by estradiol and 5alpha-dihydrotestosterone. Neuroendocrinology 1991; 53: 79-84.
Harada N, Abe-Dohmae S, Loeffen R, Foidart A, Balthazart J. Synergism between androgens and estrogens in the induction of aromatase and its messenger RNA in the brain. Brain Res 1993; 622: 243-256.
Balthazart J, Baillien M, Ball GF. Rapid and reversible inhibition of brain aromatase activity. J Neuroendocrinol 2001; 13: 63-73.
Balthazart J, Baillien M, Ball GF. Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 2006; 147: 359-366.
Cornil CA, Balthazart J, Motte P, Massotte L, Seutin V. Dopamine activates noradrenergic receptors in the preoptic area. J Neurosci 2002; 22: 9320-9330.
Cornil CA, Seutin V, Motte P, Balthazart J. Electrophysiological and neurochemical characterization of neurons of the medial preoptic area in Japanese quail (Coturnix japonica). Brain Res 2004; 1029: 224-240.
Konkle AT, Balthazart J. Sex differences in the rapid control of aromatase activity in the quail preoptic area. J Neuroendocrinol 2011; 23: 424-434.
Cornil CA, Leung CH, Pletcher ER, Naranjo KC, Blauman SJ, Saldanha CJ. Acute and specific modulation of presynaptic aromatization in the vertebrate brain. Endocrinology 2012; 153: 2562-2567.
Charlier TD, Harada N, Balthazart J, Cornil CA. Human and quail aromatase activity is rapidly and reversibly inhibited by phosphorylating conditions. Endocrinology 2011; 152: 4199-4210.
Balthazart J, Baillien M, Charlier TD, Ball GF. Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur J Neurosci 2003; 17: 1591-1606.
Remage-Healey L, Dong S, Maidment NT, Schlinger BA. Presynaptic control of rapid estrogen fluctuations in the songbird auditory forebrain. J Neurosci 2011; 31: 10034-10038.
Balthazart J, Baillien M, Ball GF. Interactions between kinases and phosphatases in the rapid control of brain aromatase. J Neuroendocrinol 2005; 17: 553-559.
Palkovits M. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 1973; 59: 449-450.
Schumacher M, Balthazart J. Neuroanatomical distribution of testosterone metabolizing enzymes in the Japanese quail. Brain Res 1987; 422: 137-148.
Cornil CA, Ball GF, Balthazart J, Charlier TD. Organizing effects of sex steroids on brain aromatase activity in quail. PLoS ONE 2011; 6: e19196.
de Bournonville C., Dickens MJ, Ball GF, Balthazart J, Cornil CA. Dynamic changes in brain aromatase activity following sexual interactions in males: where, when and why? Psychoneuroendocrinology 2013; 38: 789-799.
Dominguez JM, Gil M, Hull EM. Preoptic glutamate facilitates male sexual behavior. J Neurosci 2006; 26: 1699-1703.
Karlsson U, Sundgren AK, Näsström J, Johansson S. Glutamate-evoked currents in acutely dissociated neurons from the rat medial preoptic nucleus. Brain Res 1997; 759: 270-276.
Kleitz-Nelson HK, Dominguez JM, Ball GF. Dopamine release in the medial preoptic area is related to hormonal action and sexual motivation. Behav Neurosci 2010; 124: 773-779.
Kleitz-Nelson HK, Dominguez JM, Cornil CA, Ball GF. Is sexual motivational state linked to dopamine release in the medial preoptic area? Behav Neurosci 2010; 124: 300-304.
Dominguez JM, Hull EM. Stimulation of the medial amygdala enhances medial preoptic dopamine release: implications for male sexual behavior. Brain Res 2001; 917: 225-229.
Wingfield JC, Sapolsky RM. Reproduction and resistance to stress: when and how. J Neuroendocrinol 2003; 15: 711-724.
Balthazart J, Cornil CA, Charlier TD, Taziaux M, Ball GF. Estradiol, a key endocrine signal in the sexual differentiation and activation of reproductive behavior in quail. J Exp Zool A Ecol Genet Physiol 2009; 311: 323-345.
Dickens MJ, Cornil CA, Balthazart J. Acute stress differentially affects aromatase activity in specific brain nuclei of adult male and female quail. Endocrinology 2011; 152: 4242-4251.
Dickens MJ, Balthazart J, Cornil CA. Brain aromatase and circulating corticosterone are rapidly regulated by combined acute stress and sexual interaction in a sex-specific manner. J Neuroendocrinol 2012; 24: 1322-1334.
Dickens MJ, Cornil CA, Balthazart J. Neurochemical control of rapid stress-induced changes in brain aromatase activity. J Neuroendocrinol 2013; 25: 329-339.
Remage-Healey L, Oyama RK, Schlinger BA. Elevated aromatase activity in forebrain synaptic terminals during song. J Neuroendocrinol 2009; 21: 191-199.
Remage-Healey L, Maidment NT, Schlinger BA. Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 2008; 11: 1327-1334.
Charlier TD, Po KW, Newman AE, Shah AH, Saldanha CJ, Soma KK. 17beta-Estradiol levels in male zebra finch brain: combining Palkovits punch and an ultrasensitive radioimmunoassay. Gen Comp Endocrinol 2011; 167: 18-26.
Cornil CA. Rapid regulation of brain oestrogen synthesis: the behavioural roles of oestrogens and their fates. J Neuroendocrinol 2009; 21: 217-226.