[en] It is increasingly recognized that estrogens produce rapid and transient effects at many neural sites ultimately impacting physiological and behavioral endpoints. The ability of estrogens to acutely regulate cellular processes implies that their concentration should also be rapidly fine-tuned. Accordingly, rapid changes in the catalytic activity of aromatase, the limiting enzyme for estrogen synthesis, have been identified that could serve as a regulatory mechanism of local estrogen concentrations. However, the precise anatomical localization, time-course, triggering stimuli and functional significance of these enzymatic changes in vivo are not well understood. To address these issues as to where, when and why aromatase activity (AA) rapidly changes after sexual interactions, AA was assayed in six populations of aromatase-expressing cells microdissected from the brain of male quail that experienced varying durations of visual exposure to or copulation with a female. Sexual interactions resulted in a rapid AA inhibition. This inhibition occurred in specific brain regions (including the medial preoptic nucleus), in a context-dependent fashion and time-scale suggestive of post-translational modifications of the enzyme. Interestingly, the enzymatic fluctuations occurring in the preoptic area followed rather than preceded copulation and were tied specifically to the female's presence. This pattern of enzymatic changes suggests that rapid estrogen effects are important during the motivational phase of the behavior to trigger physiological events essential to activate mate search and copulation.
Research center :
Giga-Neurosciences - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
de Bournonville, Catherine ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Dickens, Molly J.
Ball, Gregory F.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
Dynamic changes in brain aromatase activity following sexual interactions in males: Where, when and why?
Publication date :
2013
Journal title :
Psychoneuroendocrinology
ISSN :
0306-4530
eISSN :
1873-3360
Publisher :
Pergamon Press (part of Elsevier Science), Oxford, United Kingdom
Volume :
38
Issue :
6
Pages :
789-99
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
ULg
Funders :
NIH - National Institutes of Health [US-MD] [US-MD] ULiège 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]
Adkins E.K., Adler N.T. Hormonal control of behavior in the Japanese quail. J. Comp. Physiol. Psychol. 1972, 81:27-36.
Baillien M., Balthazart J. A direct dopaminergic control of aromatase activity in the quail preoptic area. J. Steroid Biochem. Mol. Biol. 1997, 63:99-113.
Ball G.F., Balthazart J. Neuroendocrine regulation of reproductive behavior in birds. Hormones, Brain and Behavior 2009, 855-895. Academic Press, San Diego. 2nd ed. W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
Balthazart J., Absil P., Gerard M., Appeltants D., Ball G.F. Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J. Neurosci. 1998, 18:6512-6527.
Balthazart J., Baillien M., Ball G.F. Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 2006, 147:359-366.
Balthazart J., Baillien M., Charlier T.D., Ball G.F. Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur. J. Neurosci. 2003, 17:1591-1606.
Balthazart J., Baillien M., Cornil C.A., Ball G.F. Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol. Behav. 2004, 83:247-270.
Balthazart J., Foidart A., Hendrick J.C. The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol. Behav. 1990, 47:83-94.
Balthazart J., Taziaux M., Holloway K., Ball G.F., Cornil C.A. Behavioral effects of brain-derived estrogens in birds. Ann. N. Y. Acad. Sci. 2009, 1163:31-48.
Bazzett T., Lumley L., Bitran D., Markowski V., Warner R., Hull E. Male rat copulation following 6-OHDA lesions of the medial preoptic area: resistance to repeated administration and rapid behavioral recovery. Brain Res. 1992, 580:164-170.
Charlier T.D., Harada N., Balthazart J., Cornil C.A. Human and quail aromatase activity is rapidly and reversibly inhibited by phosphorylating conditions. Endocrinology 2011, 152:4199-4210.
Cornil C.A., Ball G.F. Effects of social experience on subsequent sexual performance in naive male Japanese quail (Coturnix japonica). Horm. Behav. 2010, 57:515-522.
Cornil C.A., Ball G.F., Balthazart J., Charlier T.D. Organizing effects of sex steroids on brain aromatase activity in quail. PLoS ONE 2011, 6:e19196.
Cornil C.A., Charlier T.D. Rapid behavioural effects of oestrogens and fast regulation of their local synthesis by brain aromatase. J. Neuroendocrinol. 2010, 22:664-673.
Cornil C.A., 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, 166:110-123.
Cornil C.A., Dalla C., Papadopoulou-Daifoti Z., Baillien M., Dejace C., Ball G.F., Balthazart J. Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior. Endocrinology 2005, 146:3809-3820.
Cornil C.A., Leung C.H., Pletcher E.R., Naranjo K.C., Blauman S.J., Saldanha C.J. Acute and specific modulation of presynaptic aromatization in the vertebrate brain. Endocrinology 2012, 153:2562-2567.
Cornil C.A., 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.
Cornil C.A., Taziaux M., Baillien M., Ball G.F., Balthazart J. Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail. Horm. Behav. 2006, 49:45-67.
Cross E., Roselli C.E. 17-Beta-estradiol rapidly facilitates chemoinvestigation and mounting in castrated male rats. Am. J. Physiol. 1999, 276:R1346-R1350.
Dickens M.J., Cornil C.A., Balthazart J. Acute stress differentially affects aromatase activity in specific brain nuclei of adult male and female quail. Endocrinology 2011, 152:4242-4251.
Dominguez J.M., Gil M., Hull E.M. Preoptic glutamate facilitates male sexual behavior. J. Neurosci. 2006, 26:1699-1703.
Evrard H.C., Balthazart J. Aromatization of androgens into estrogens reduces response latency to a noxious thermal stimulus in male quail. Horm. Behav. 2004, 45:181-189.
Foidart A., Reid J., Absil P., Yoshimura N., Harada N., Balthazart J. 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. 1995, 8:267-282.
Garcia-Segura L.M. Aromatase in the brain: not just for reproduction anymore. J. Neuroendocrinol. 2008, 20:705-712.
Hull E.M., Dominguez J.M. Getting his act together: roles of glutamate, nitric oxide, and dopamine in the medial preoptic area. Brain Res. 2006, 1126:66-75.
Hull E.M., Du J., Lorrain D.S., Matuszewich L. Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J. Neurosci. 1995, 15:7465-7471.
Hull E.M., Eaton R.C., Markowski V.P., Moses J., Lumley L.A., Loucks J.A. Opposite influence of medial preoptic D1 and D2 receptors on genital reflexes: implications for copulation. Life Sci. 1992, 51:1705-1713.
Hull E.M., Rodriguez-Manzo G. Male sexual behavior. Hormones, Brain and Behavior 2009, 5-65. Academic Press, San Diego. D. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
Hutchison R.E. Hormonal differentiation of sexual behavior in Japanese quail. Horm. Behav. 1978, 11:363-387.
Karlsson U., Sundgren A.K., Nasstrom J., Johansson S. Glutamate-evoked currents in acutely dissociated neurons from the rat medial preoptic nucleus. Brain Res. 1997, 759:270-276.
Kleitz-Nelson H.K., Cornil C.A., Balthazart J., Ball G.F. Differential effects of central injections of D1 and D2 receptor agonists and antagonists on male sexual behavior in Japanese quail. Eur. J. Neurosci. 2010, 32:118-129.
Kleitz-Nelson H.K., Dominguez J.M., Cornil C.A., Ball G.F. Is sexual motivational state linked to dopamine release in the medial preoptic area?. Behav. Neurosci. 2010, 124:300-304.
Maggi A., Ciana P., Belcredito S., Vegeto E. Estrogens in the nervous system: mechanisms and nonreproductive functions. Annu. Rev. Physiol. 2004, 66:291-313.
Palkovits M. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res. 1973, 59:449-450.
Putnam S.K., Sato S., Hull E.M. Effects of testosterone metabolites on copulation and medial preoptic dopamine release in castrated male rats. Horm. Behav. 2003, 44:419-426.
Remage-Healey L., Dong S., Maidment N.T., Schlinger B.A. Presynaptic control of rapid estrogen fluctuations in the songbird auditory forebrain. J. Neurosci. 2011, 31:10034-10038.
Remage-Healey L., Maidment N.T., Schlinger B.A. Forebrain steroid levels fluctuate rapidly during social interactions. Nat. Neurosci. 2008, 11:1327-1334.
Remage-Healey L., Oyama R.K., Schlinger B.A. Elevated aromatase activity in forebrain synaptic terminals during song. J. Neuroendocrinol. 2009, 21:191-199.
Roepke T.A., Ronnekleiv O.K., Kelly M.J. Physiological consequences of membrane-initiated estrogen signaling in the brain. Front. Biosci. 2011, 16:1560-1573.
Roselli C.E., Resko J.A. In vitro assay of aromatase activity in the central nervous system. Neuroendocrin Research Methods 1991, 937-954. Hardwood Academic Publishers, Chur, Switzerland. B. Greenstein (Ed.).
Seiwert C.M., Adkins-Regan E. The foam production system of the male Japanese quail: characterization of structure and function. Brain Behav. Evol. 1998, 52:61-80.
Seredynski A.L., Balthazart J., Ball G.F., Cornil C.A. Brain-derived estrogens acutely affect male sexual motivation but not performance in Japanese quail. Soc. Neurosci. 2012, 2012:482.11. (abstracts).
Taziaux M., Cornil C.A., Balthazart J. Aromatase inhibition blocks the expression of sexually-motivated cloacal gland movements in male quail. Behav. Proc. 2004, 67:461-469.
Taziaux M., Keller M., Bakker J., Balthazart J. Sexual behavior activity tracks rapid changes in brain estrogen concentrations. J. Neurosci. 2007, 27:6563-6572.
Trainor B.C., Kyomen H.H., Marler C.A. Estrogenic encounters: how interactions between aromatase and the environment modulate aggression. Front. Neuroendocrinol. 2006, 27:170-179.
Tsai M.J., O'Malley B.W. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 1994, 63:451-486.
Vasudevan N., Pfaff D.W. Membrane-initiated actions of estrogens in neuroendocrinology: emerging principles. Endocr. Rev. 2007, 28:1-19.
Wersinger S.R., Rissman E.F. Dopamine activates masculine sexual behavior independent of the estrogen receptor alpha. J. Neurosci. 2000, 20:4248-4254.
Xie J., Kuenzel W.J., Sharp P.J., Jurkevich A. Appetitive and consummatory sexual and agonistic behaviour elicits FOS expression in aromatase and vasotocin neurones within the preoptic area and bed nucleus of the stria terminalis of male domestic chickens. J. Neuroendocrinol. 2011, 23:232-243.