[en] The importance of estrogens in controlling brain and behavioral sexual differentiation in female rodents is an unresolved issue in the field of behavioral neuroendocrinology. Whereas, the current dogma states that the female brain develops independently of estradiol, many studies have hinted at possible roles of estrogen in female sexual differentiation. Accordingly, it has been proposed that alpha-fetoprotein, a fetal plasma protein that binds estrogens with high affinity, has more than a neuroprotective role and specifically delivers estrogens to target brain cells to ensure female differentiation. Here, we review new results obtained in aromatase and alpha-fetoprotein knockout mice showing that estrogens can have both feminizing and defeminizing effects on the developing neural mechanisms that control sexual behavior. We propose that the defeminizing action of estradiol normally occurs prenatally in males and is avoided in fetal females because of the protective actions of alpha-fetoprotein, whereas the feminizing action of estradiol normally occurs postnatally in genetic females.
Research Center/Unit :
Giga-Neurosciences - ULiège
Disciplines :
Neurology
Author, co-author :
Bakker, Julie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Baum, M. J.
Language :
English
Title :
Role for Estradiol in Female-Typical Brain and Behavioral Sexual Differentiation
Publication date :
January 2008
Journal title :
Frontiers in Neuroendocrinology
ISSN :
0091-3022
eISSN :
1095-6808
Publisher :
Elsevier, Atlanta, United States - Florida
Volume :
29
Issue :
1
Pages :
1-16
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NICHD - National Institutes of Health. Eunice Kennedy Shriver National Institute of Child Health and Human Development
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Abelev G.I., Perova S.D., Khramkova N.I., Postnikova Z.A., and Irlin I.S. Production of embryonal alpha-globulin by transplantable mouse hepatomas. Transplantation 1 (1963) 174-180
Ali M., Mujoo K., and Sahib M.K. Synthesis and secretion of alpha-fetoprotein and albumin by newborn rat brain cells in culture. Brain Res. 282 (1982) 47-55
Andrews G.K., Dziadek M., and Tamaoki T. Expression and methylation of the mouse alpha-fetoprotein gene in embryonic, adult, and neoplastic tissues. J. Biol. Chem. 257 (1982) 5148-5153
Arnon R., Teicher E., Bustin M., and Sela M. Preparation of antisera to alpha-fetoprotein making use of estradiol affinity column. FEBS Lett. 32 (1973) 335-338
Aussel C., and Masseyeff R. Rat alpha-fetoprotein-estrogen interaction. J. Steroid Biochem. 9 (1978) 547-551
Bakker J., De Mees C., Douhard Q., Balthazart J., Gabant P., Szpirer J., and Szpirer C. Alpha-fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens. Nat. Neurosci. 9 (2006) 220-226
Bakker J., De Mees C., Szpirer J., Szpirer C., and Balthazart J. Exposure to oestrogen prenatally does not interfere with the normal female-typical development of odour preferences. J. Neuroendocrinol. 19 (2007) 329-334
Bakker J., Honda S., Harada N., and Balthazart J. The aromatase knock-out mouse provides new evidence that estradiol is required during development in the female for the expression of sociosexual behaviors in adulthood. J. Neurosci. 22 (2002) 9104-9112
Bakker J., Honda S., Harada N., and Balthazart J. Restoration of male sexual behavior by adult exogenous estrogens in male aromatase knockout mice. Horm. Behav. 46 (2004) 1-10
Baum M.J. Differentiation of coital behavior in mammals: a comparative analysis. Neurosci. Biobehav. Rev. 3 (1979) 265-284
Baum M.J., and Keverne E.B. Sex difference in attraction thresholds for volatile odors from male and estrous female mouse urine. Horm. Behav. 41 (2002) 213-219
Baum M.J., and Tobet S.A. Effect of prenatal exposure to aromatase inhibitor, testosterone, or antiandrogen on the development of feminine sexual behavior in ferrets of both sexes. Physiol. Behav. 37 (1986) 111-118
Bennett J.A., DeFreest L., Anaka I., Saadati H., Balulad S., Jacobson H.I., and Andersen T.T. AFPep: an anti-breast cancer peptide that is orally active. Breast Cancer Res. Treat. 98 (2006) 133-141
Bennett J.A., Mesfin F.B., Andersen T.T., Gierthy J.F., and Jacobson H.I. A peptide derived from alpha-fetoprotein prevents the growth of estrogen-dependent human breast cancers sensitive and resistant to tamoxifen. Proc. Natl. Acad. Sci. USA 99 (2002) 2211-2215
Bergstrand C.G., and Czar B. Demonstration of a new protein fraction in serum from the human fetus. Scand. J. Clin. Lab. Invest. 8 (1956) 174
Blizard D., and Denef C. Neonatal androgen effects on open-field activity and sexual behavior in the female rat: the modifying influence of ovarian secretions during development. Physiol. Behav. 11 (1973) 65-69
Bodo C., and Rissman E.F. Androgen receptor is essential for sexual differentiation of responses to olfactory cues in mice. Eur. J. Neurosci. 25 (2007) 2182-2190
Booth J.E. Sexual differentiation of the brain. In: Finn C.A. (Ed). Oxford Reviews of Reproductive vol. I (1979), Clarendon Press, Oxford 58-158 Ref Type: Serial (Book,Monograph)
Brownbill P., Edwards D., Jones C., Mahendran D., Owen D., Sibley C., Johnson R., Swanson P., and Nelson D.M. Mechanisms of alphafetoprotein transfer in the perfused human placental cotyledon from uncomplicated pregnancy. J. Clin. Invest. 96 (1995) 2220-2226
Clark A.S., Pfeifle J.K., and Edwards D.A. Ventromedial hypothalamic damage and sexual proceptivity in female rats. Physiol. Behav. 27 (1981) 597-602
M.A. Crawford, A.J. Sinclair, Nutritional influences in the evolution of the mammalian brain, in: CIBA Foundation Symposium, Churchill London, Malnutrition and the Developing Brain, 1972, pp. 267-287.
Cuckle H.S., Wald N.J., and Lindenbaum R.H. Maternal serum alpha-fetoprotein measurement: a screening test for Down syndrome. Lancet 1 (1984) 926-929
Daniels D., Miselis R.R., and Flanagan-Cato L.M. Central neuronal circuit innervating the lordosis-producing muscles defined by transneuronal transport of pseudorabies virus. J. Neurosci. 19 (1999) 2823-2833
De Mees C., Laes J.F., Bakker J., Smitz J., Hennuy B., Van Vooren P., Gabant P., Szpirer J., and Szpirer C. Alpha-fetoprotein controls female fertility and prenatal development of the gonadotropin-releasing hormone pathway through an antiestrogenic action. Mol. Cell. Biol. 26 (2006) 2012-2018
De Vries G.J., Rissman E.F., Simerly R.B., Yang L.Y., Scordalakes E.M., Auger C.J., Swain A., Lovell-Badge R., Burgoyne P.S., and Arnold A.P. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 22 (2002) 9005-9014
Dohler K.D., Hancke J.L., Srivastava S.S., Hofmann C., Shryne J.E., and Gorski R.A. Participation of estrogens in female sexual differentiation of the brain; neuroanatomical, neuroendocrine and behavioral evidence. In: De Vries G.J., De Bruin J.P.C., Uylings H.B.M., and Corner M.A. (Eds). Progress in Brain Research. Sex differences in the brain, the relation between structure and function 61 (1984), Elsevier, Amsterdam 99-117 Ref Type: Serial (Book,Monograph)
Dorner G. Sexual differentiation of the brain. Vitam. Horm. 38 (1981) 325-381 Ref Type: Serial (Book,Monograph)
Dorries K.M., Adkins-Regan E., and Halpern B.P. Olfactory sensitivity to the pheromone, androstenone, is sexually dimorphic in the pig. Physiol. Behav. 57 (1995) 255-259
Dunlap J.L., Gerall A.A., and McLean L.D. Enhancement of female receptivity in neonatally castrated males by prepuberal ovarian transplants. Physiol. Behav. 10 (1973) 701-705
Edwards D.A., and Burge K.G. Olfactory control of the sexual behavior of male and female mice. Physiol. Behav. 11 (1973) 867-872
Feder H.H., and Whalen R.E. Feminine behavior in neonatally castrated and estrogen-treated male rats. Science 147 (1965) 306-307
Firestein S. How the olfactory system makes sense of scents. Nature 413 (2001) 211-218
Fisher C.R., Graves K.H., Parlow A.F., and Simpson E.R. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc. Natl. Acad. Sci. USA 95 (1998) 6965-6970
Gabant P., Forrester L., Nichols J., Van Reeth T., De Mees C., Pajack B., Watt A., Smitz J., Alexandre H., Szpirer C., and Szpirer J. Alpha-fetoprotein, the major fetal serum protein, is not essential for embryonic development but is required for female fertility. Proc. Natl. Acad. Sci. USA 99 (2002) 12865-12870
Gerall A.A., Dunlap J.L., and Hendricks S.E. Effect of ovarian secretions on female behavioral potentiality in the rat. J. Comp. Physiol. Psychol. 82 (1973) 449-465
Gibori G., and Sridaran R. Sites of androgen and estradiol production in the second half of pregnancy in the rat. Biol. Reprod. 24 (1981) 249-256
Gillespie J.R., and Uversky V.N. Structure and function of alpha-fetoprotein: a biophysical overview. Biochim. Biophys. Acta 1480 (2000) 41-56
Gorski R.A., and Jacobson C.D. Sexual differentiation of the brain. In: Kogan S.E., and Hafez E.S.E. (Eds). Pediatric Andrology (1981), Martinus Nijfhoff, The Hague, The Netherlands 109-134 Ref Type: Serial (Book,Monograph)
Goy R.W., and McEwen B.S. Sexual Differentiation of the Brain (1980), Masachusettes Institute of Technology Press, Cambridge MA, USA Ref Type: Serial (Book,Monograph)
Grady K.L., Phoenix C.H., and Young W.C. Role of the developing rat testis in differentiation of the neural tissues mediating mating behavior. J. Comp. Physiol. Psychol. 59 (1965) 176-182
Greco T.L., and Payne A.H. Ontogeny of expression of the genes for steroidogenic enzymes P450 side-chain cleavage, 3 beta-hydroxysteroid dehydrogenase, P450 17 alpha-hydroxylase/C17-20 lyase, and P450 aromatase in fetal mouse gonads. Endocrinology 135 (1994) 262-268
Haddow J.E., Macri J.N., and Munson M. The amnion regulates movement of fetally derived alpha-fetoprotein into maternal blood. J. Lab. Clin. Med. 94 (1979) 344-347
Han T.M., and De Vries G.J. Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis. J. Neurobiol. 54 (2003) 502-510
Honda S., Harada N., Ito S., Takagi Y., and Maeda S. Disruption of sexual behavior in male aromatase-deficient mice lacking exons 1 and 2 of the cyp19 gene. Biochem. Biophys. Res. Commun. 252 (1998) 445-449
Jost A. Sur le contrôle hormonal de différenciation sexuelle du lapin. Arch. Anat. Microscop. Morphol. Exp. 39 (1950) 577-598
Keller M., Douhard Q., Baum M.J., and Bakker J. Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice. Chem. Senses 31 (2006) 315-323
Keller M., Pierman S., Douhard Q., Baum M.J., and Bakker J. The vomeronasal organ is required for the expression of lordosis behaviour, but not sex discrimination in female mice. Eur. J. Neurosci. 23 (2006) 521-530
Keverne E.B. The vomeronasal organ. Science 286 (1999) 716-720
Kimoto H., Haga S., Sato K., and Touhara K. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437 (2005) 898-901
Koopman P., Munsterberg A., Capel B., Vivian N., and Lovell-Badge R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348 (1990) 450-452
Kudwa A.E., Boon W.C., Simpson E.R., Handa R.J., and Rissman E.F. Dietary phytoestrogens dampen female sexual behavior in mice with a disrupted aromatase enzyme gene. Behav. Neurosci. 121 (2007) 356-361
Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., van der B.B., and Gustafsson J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139 (1998) 4252-4263
Lamprecht S.A., Kohen F., Ausher J., Zor U., and Lindner H.R. Hormonal stimulation of oestradiol-17 beta release from the rat ovary during early postnatal development. J. Endocrinol. 68 (1976) 343-344
Leighton P.C., Kitau M.J., Chard T., Gordon Y.B., and Leek A.E. Levels of alpha-fetoprotein in maternal blood as a screening test for fetal neural-tube defect. Lancet 2 (1975) 1012-1015
Lephart E.D., West T.W., Weber K.S., Rhees R.W., Setchell K.D., Adlercreutz H., and Lund T.D. Neurobehavioral effects of dietary soy phytoestrogens. Neurotoxicol. Teratol. 24 (2002) 5-16
Lisk R.D. Progesterone: biphasic effects on the lordosis response in adult or neonatally gonadectomized rats. Neuroendocrinology 5 (1969) 149-160
Mackiewicz A., and Breborowicz J. The in vitro production of alpha-fetoprotein variants by human fetal organs. Oncodev. Biol. Med. 1 (1980) 251-261
MacLusky N.J., and Naftolin F. Sexual differentiation of the central nervous system. Science 211 (1981) 1294-1302
Malsbury C.W., Kow L.M., and Pfaff D.W. Effects of medial hypothalamic lesions on the lordosis response and other behaviors in female golden hamsters. Physiol. Behav. 19 (1977) 223-237
Mathews D., and Edwards D.A. The ventromedial nucleus of the hypothalamus and the hormonal arousal of sexual behaviors in the female rat. Horm. Behav. 8 (1977) 40-51
Mathews G.A., Brenowitz E.A., and Arnold A.P. Paradoxical hypermasculinization of the zebra finch song system by an antiestrogen. Horm. Behav. 22 (1988) 540-551
McCall A.L., Han S.J., Millington W.R., and Baum M.J. Non-saturable transport of [3H]oestradiol across the blood-brain barrier in female rats is reduced by neonatal serum. J. Reprod. Fertil. 61 (1981) 103-108
McCarthy M.M., and Konkle A.T. When is a sex difference not a sex difference?. Front. Neuroendocrinol. 26 (2005) 85-102
McEwen B.S., Plapinger L., Chaptal C., Gerlach J., and Wallach G. Role of fetoneonatal estrogen binding proteins in the associations of estrogen with neonatal brain cell nuclear receptors. Brain Res. 96 (1975) 400-406
Meijs-Roelofs H.M., Uilenbroek J.T., de Jong F.H., and Welschen R. Plasma oestradiol-17beta and its relationship to serum follicle-stimulating hormone in immature female rats. J. Endocrinol. 59 (1973) 295-304
Mizejewski G.J., Muehlemann M., and Dauphinee M. Update of alpha fetoprotein growth-inhibitory peptides as biotherapeutic agents for tumor growth and metastasis. Chemotherapy 52 (2006) 83-90
Mizejewski G.J., and Vonnegut M. Characteristics of the androgenization produced in mice by neonatal exposure to alpha-fetoprotein antibodies. Teratology 25 (1982) 351-360
Naftolin F., Ryan K.J., Davies I.J., Reddy V.V., Flores F., Petro Z., Kuhn M., White R.J., Takaoka Y., and Wolin L. The formation of estrogens by central neuroendocrine tissues. Recent Prog. Horm. Res. 31 (1975) 295-319
Nagel S.C., vom Saal F.S., and Welshons W.V. Developmental effects of estrogenic chemicals are predicted by an in vitro assay incorporating modification of cell uptake by serum. J. Steroid Biochem. Mol. Biol. 69 (1999) 343-357
Newby D., Dalgliesh G., Lyall F., and Aitken D.A. Alphafetoprotein and alphafetoprotein receptor expression in the normal human placenta at term. Placenta 26 (2005) 190-200
Nunez E.A., Benassayag C., Savu L., Vallette G., and Jayle M.F. Serum binding of some steroid hormones during development in different animal species, discussion of the biological significance of this binding. Ann. Biol. Anim. Biochem. Biophys. 16 (1976) 491-501
Pfaff D.W., and Sakuma Y. Deficit in the lordosis reflex of female rats caused by lesions in the ventromedial nucleus of the hypothalamus. J. Physiol. 288 (1979) 203-210
Pfaff D.W., Schwartz-Giblin S., McCarthy M.M., and Kow L.-M. Cellular and molecular mechanisms of female reproductive behaviors. In: Knobil E., and Neill J. (Eds). The Physiology of Reproduction vol. 2 (1994), Raven Press, New York 107-220 Ref Type: Serial (Book,Monograph)
Pfeiffer C.A. Sexual differences in the hypophyses and their determination by the gonads. Am. J. Anat. 58 (1936) 195-226
Phoenix C.H., Goy R.W., Gerall A.A., and Young W.C. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65 (1959) 369-382
Pierman S., Douhard Q., Balthazart J., Baum M.J., and Bakker J. Attraction thresholds and sex discrimination of urinary odorants in male and female aromatase knockout (ArKO) mice. Horm. Behav. 49 (2006) 96-104
Pineiro A., Olivito A.M., and Uriel J. Fixation of polyunsaturated fatty acids by alpha fetoprotein and serum albumin in rats. Comparison with the accumulation of these acids in developing rat brain. C. R. Seances Acad. Sci. D 289 (1979) 1053-1056
Plapinger L., and McEwen B.S. Ontogeny of estradiol-binding sites in rat brain. I. Appearance of presumptive adult receptors in cytosol and nuclei. Endocrinology 93 (1973) 1119-1128
Plumari L., Viglietti-Panzica C., Allieri F., Honda S., Harada N., Absil P., Balthazart J., and Panzica G.C. Changes in the arginine-vasopressin immunoreactive systems in male mice lacking a functional aromatase gene. J. Neuroendocrinol. 14 (2002) 971-978
Quadros P.S., Goldstein A.Y., De Vries G.J., and Wagner C.K. Regulation of sex differences in progesterone receptor expression in the medial preoptic nucleus of postnatal rats. J. Neuroendocrinol. 14 (2002) 761-767
Quadros P.S., Lopez V., De Vries G.J., Chung W.C., and Wagner C.K. Progesterone receptors and the sexual differentiation of the medial preoptic nucleus. J. Neurobiol. 51 (2002) 24-32
Quadros P.S., Pfau J.L., Goldstein A.Y., De Vries G.J., and Wagner C.K. Sex differences in progesterone receptor expression: a potential mechanism for estradiol-mediated sexual differentiation. Endocrinology 143 (2002) 3727-3739
Raynaud J.P. Influence of rat estradiol binding plasma protein (EBP) on uterotrophic activity. Steroids 21 (1973) 249-258
Rubin B.S., and Barfield R.J. Priming of estrous responsiveness by implants of 17 beta-estradiol in the ventromedial hypothalamic nucleus of female rats. Endocrinology 106 (1980) 504-509
Rubin B.S., Lenkowski J.R., Schaeberle C.M., Vandenberg L.N., Ronsheim P.M., and Soto A.M. Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol A. Endocrinology 147 (2006) 3681-3691
Sato T., Matsumoto T., Kawano H., Watanabe T., Uematsu Y., Sekine K., Fukuda T., Aihara K., Krust A., Yamada T., Nakamichi Y., Yamamoto Y., Nakamura T., Yoshimura K., Yoshizawa T., Metzger D., Chambon P., and Kato S. Brain masculinization requires androgen receptor function. Proc. Natl. Acad. Sci. USA 101 (2004) 1673-1678
Savu L., Benassayag C., Vallette G., Christeff N., and Nunez E. Mouse alpha 1-fetoprotein and albumin. A comparison of their binding properties with estrogen and fatty acid ligands. J. Biol. Chem. 256 (1981) 9414-9418
Schachter B.S., and Toran-Allerand C.D. Intraneuronal alpha-fetoprotein and albumin are not synthesized locally in developing brain. Brain Res. 281 (1982) 93-98
Schaefer M.L., Young D.A., and Restrepo D. Olfactory fingerprints for major histocompatibility complex-determined body odors. J. Neurosci. 21 (2001) 2481-2487
Sell S., and Becker F.F. Alpha-fetoprotein. J. Natl. Cancer Inst. 60 (1978) 19-26
Simerly R.B., Swanson L.W., Handa R.J., and Gorski R.A. Influence of perinatal androgen on the sexually dimorphic distribution of tyrosine hydroxylase-immunoreactive cells and fibers in the anteroventral periventricular nucleus of the rat. Neuroendocrinology 40 (1985) 501-510
Simerly R.B., Zee M.C., Pendleton J.W., Lubahn D.B., and Korach K.S. Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc. Natl. Acad. Sci. USA 94 (1997) 14077-14082
Steward J., and Cygan D. Ovarian hormones act early in development to feminize adult open-field behavior in the rat. Horm. Behav. 14 (1980) 20-32
Tilghman S.M., and Belayew A. Transcriptional control of the murine albumin/alpha-fetoprotein locus during development. Proc. Natl. Acad. Sci. USA 79 (1982) 5254-5257
Tobet S.A., and Baum M.J. Role for prenatal estrogen in the development of masculine sexual behavior in the male ferret. Horm. Behav. 21 (1987) 419-429
Tobet S.A., and Hanna I.K. Ontogeny of sex differences in the mammalian hypothalamus and preoptic area. Cell. Mol. Neurobiol. 17 (1997) 565-601
Toda K., Takeda K., Okada T., Akira S., Saibara T., Kaname T., Yamamura K., Onishi S., and Shizuta Y. Targeted disruption of the aromatase P450 gene (Cyp19) in mice and their ovarian and uterine responses to 17beta-oestradiol. J. Endocrinol. 170 (2001) 99-111
Toran-Allerand C.D. Regional differences in intraneuronal localization of alpha-fetoprotein in developing mouse brain. Brain Res. 281 (1982) 213-217
Toran-Allerand C.D. On the genesis of sexual differentiation of the central nervous system: morphogenetic consequences of steroidal exposure and possible role of alpha-fetoprotein. In: De Vries G.J., De Bruin J.P.C., Uylings H.B.M., and Corner M.A. (Eds). Progress in Brain Research. Sex differences in the brain, the relation between structure and function 61 (1984), Elsevier, Amsterdam 63-98 Ref Type: Serial (Book,Monograph)
Toran-Allerand C.D. Neuronal uptake of alpha-fetoprotein (AFP) synthesized and secreted by hepatocytes in liver/brain co-cultures. Neurosci. Lett. 83 (1987) 35-40
Uriel J., de Nechaud B., and Dupiers M. Estrogen-binding properties of rat, mouse and man fetospecific serum proteins. Demonstration by immuno-autoradiographic methods. Biochem. Biophys. Res. Commun. 46 (1972) 1175-1180
Vakharia D., and Mizejewski G.J. Human alpha-fetoprotein peptides bind estrogen receptor and estradiol, and suppress breast cancer. Breast Cancer Res. Treat. 63 (2000) 41-52
Vallette G., Benassayag C., Savu L., Delorme J., Nunez E.A., Doumas J., Maume G., and Maume B.F. The serum competitor of oestrogen-rat alpha 1-foetoprotein interactions. Identification as a mixture of non-esterified fatty acids. Biochem. J. 187 (1980) 851-856
vom Saal F.S., Grant W.M., McMullen C.W., and Laves K.S. High fetal estrogen concentrations: correlation with increased adult sexual activity and decreased aggression in male mice. Science 220 (1983) 1306-1309
Wagner C.K., Pfau J.L., De Vries G.J., and Merchenthaler I.J. Sex differences in progesterone receptor immunoreactivity in neonatal mouse brain depend on estrogen receptor alpha expression. J. Neurobiol. 47 (2001) 176-182
Wagner C.K., Xu J., Pfau J.L., Quadros P.S., De Vries G.J., and Arnold A.P. Neonatal mice possessing an Sry transgene show a masculinized pattern of progesterone receptor expression in the brain independent of sex chromosome status. Endocrinology 145 (2004) 1046-1049
Wallen K. Hormonal influences on sexually differentiated behavior in nonhuman primates. Front. Neuroendocrinol. 26 (2005) 7-26
Weniger J.P. Estrogen production by fetal rat gonads. J. Steroid Biochem. Mol. Biol. 44 (1993) 459-462
Weniger J.P., Zeis A., and Chouraqui J. Estrogen production by fetal and infantile rat ovaries. Reprod. Nutr. Dev. 33 (1993) 129-136
Wersinger S.R., Haisenleder D.J., Lubahn D.B., and Rissman E.F. Steroid feedback on gonadotropin release and pituitary gonadotropin subunit mRNA in mice lacking a functional estrogen receptor alpha. Endocrine 11 (1999) 137-143
Wersinger S.R., Sannen K., Villalba C., Lubahn D.B., Rissman E.F., and De Vries G.J. Masculine sexual behavior is disrupted in male and female mice lacking a functional estrogen receptor alpha gene. Horm. Behav. 32 (1997) 176-183
Wesson D.W., Keller M., Douhard Q., Baum M.J., and Bakker J. Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice. Horm. Behav. 49 (2006) 580-586
Whalen R.E., and Edwards D.A. Hormonal determinants of the development of masculine and feminine behavior in male and female rats. Anat. Rec. 157 (1967) 173-180
Whitten P.L., Patisaul H.B., and Young L.J. Neurobehavioral actions of coumestrol and related isoflavonoids in rodents. Neurotoxicol. Teratol. 24 (2002) 47-54
Wiegand S.J., and Terasawa E. Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology 34 (1982) 395-404
Witcher J.A., and Clemens L.G. A prenatal source for defeminization of female rats is the maternal ovary. Horm. Behav. 21 (1987) 36-43
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.