ERα, but not ERβ, mediates the expression of sexual behavior in the female rat

Behavioural Brain Research

Volumn 191, Issue 1, 2008, Pages 111-117

  Mazzucco, Christine A ^a,b   Walker, Hope A ^a   Pawluski, Jodi L ^a,b   Lieblich, Stephanie E ^a,b   Galea, Liisa A M ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

ER agonists; ER ; ER ; Estrogen receptors; Female sexual behavior; Lordosis; Proceptivity; Progesterone; Rat; Receptivity; Reproduction

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; DIMETHYL SULFOXIDE; ESTRADIOL; ESTRADIOL BENZOATE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; PROPIONITRILE; SESAME SEED OIL; CONTRACEPTIVE AGENT; DRUG DERIVATIVE; ESTRADIOL 3-BENZOATE; GINSENOSIDE; GINSENOSIDE 20S PROTOPANAXATRIOL; GINSENOSIDE 20S-PROTOPANAXATRIOL; NICOTINAMIDE ADENINE DINUCLEOTIDE; SAPOGENIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; LORDOSIS; MALE; MATING; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR INTRINSIC ACTIVITY; SEXUAL BEHAVIOR; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; DOSE RESPONSE; DRUG COMBINATION; DRUG EFFECT; METABOLISM; PHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CONTRACEPTIVE AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMBINATIONS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; GINSENOSIDES; NAD; OVARIECTOMY; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SAPOGENINS; SEXUAL BEHAVIOR, ANIMAL;

EID: 43249107149     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2008.03.016     Document Type: Article

References (61)

1. Aou S., Oomura Y., and Yoshimatsu H. Neuron activity of the ventromedial hypothalamus and the medial preoptic area of the female monkey during sexual behavior. Brain Res 455 (1988) 65-71
2. Audesirk T., Cabell L., Kern M., and Audesirk G. Beta-estradiol influences differentiation of hippocampal neurons in vitro through an estrogen receptor-mediated process. Neuroscience 121 (2003) 927-934
3. Barkhem T., Carlsson B., Nilsson Y., Enmark E., Gustafsson J., and Nilsson S. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol Pharmacol 54 (1998) 105-112
4. Beach F.A. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm Behav 7 (1976) 105-138
5. Brandling-Bennett E.M., Blasberg M.E., and Clark A.S. Paced mating behavior in female rats in response to different hormone priming regimens. Horm Behav 35 (1999) 144-154
6. Buteau-Lozano H., Ancelin M., Lardeux B., Milanini J., and Perrot-Applanat M. Transcriptional regulation of vascular endothelial growth factor by estradiol and tamoxifen in breast cancer cells: a complex interplay between estrogen receptors alpha and beta. Cancer Res 62 (2002) 4977-4984
7. Choleris E., Ogawa S., Kavaliers M., Gustafsson J.A., Korach K.S., Muglia L.J., et al. Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: a detailed behavioral analysis with knockout female mice. Genes Brain Behav 5 (2006) 528-539
8. Coolen L.M., Peters H.J., and Veening J.G. Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res 738 (1996) 67-82
9. Couse J.F., Dixon D., Yates M., Moore A.B., Ma L., Maas R., et al. Estrogen receptor-alpha knockout mice exhibit resistance to the developmental effects of neonatal diethylstilbestrol exposure on the female reproductive tract. Dev Biol 238 (2001) 224-238
10. Enmark E., Pelto-Huikko M., Grandien K., Lagercrantz S., Lagercrantz J., Fried G., et al. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab 82 (1997) 4258-4265
11. Evans R.M. The steroid and thyroid hormone receptor superfamily. Science 240 (1988) 889-895
12. Frasor J., Barnett D.H., Danes J.M., Hess R., Parlow A.F., and Katzenellenbogen B.S. Response-specific and ligand dose-dependent modulation of estrogen receptor (ER) alpha activity by ERbeta in the uterus. Endocrinology 144 (2003) 3159-3166
13. Fugger H.N., Cunningham S.G., Rissman E.F., and Foster T.C. Sex differences in the activational effect of ERalpha on spatial learning. Horm Behav 34 (1998) 163-170
14. Glaeser M., Niederacher D., Djahansouzi S., Hanstein B., Dittrich R., Beckmann M.W., et al. Effects of the antiestrogens tamoxifen and raloxifene on the estrogen receptor transactivation machinery. Anticancer Res 26 (2006) 735-744
15. Greco B., Blasberg M.E., Kosinski E.C., and Blaustein J.D. Response of ERalpha-IR and ERbeta-IR cells in the forebrain of female rats to mating stimuli. Horm Behav 43 (2003) 444-453
16. Hall J.M., and McDonnell D.P. The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 140 (1999) 5566-5578
17. Hansen S., Harthon C., Wallin E., Lofberg L., and Svensson K. Mesotelencephalic dopamine system and reproductive behavior in the female rat: effects of ventral tegmental 6-hydroxydopamine lesions on maternal and sexual responsiveness. Behav Neurosci 105 (1991) 588-598
18. Hardy D.F., and Debold J.F. Effects of mounts without intromission upon the behavior of female rats during the onset of estrogen-induced heat. Physiol Behav 7 (1971) 643-645
19. Hilton G.D., Ndubuizu A.N., and McCarthy M.M. Neuroprotective effects of estradiol in newborn female rat hippocampus. Brain Res Dev Brain Res 150 (2004) 191-198
20. Hoshina Y., Takeo T., Nakano K., Sato T., and Sakuma Y. Axon-sparing lesion of the preoptic area enhances receptivity and diminishes proceptivity among components of female rat sexual behavior. Behav Brain Res 61 (1994) 197-204
21. Hurst A.G., Goad D.W., Mohan M., and Malayer J.R. Independent downstream gene expression profiles in the presence of estrogen receptor alpha or beta. Biol Reprod 71 (2004) 1252-1261
22. Ikeda Y., Nagai A., Ikeda M.A., and Hayashi S. Sexually dimorphic and estrogen-dependent expression of estrogen receptor beta in the ventromedial hypothalamus during rat postnatal development. Endocrinology 144 (2003) 5098-5104
23. Jordan V.C. Alternate antiestrogens and approaches to the prevention of breast cancer. J Cell Biochem Suppl 22 (1995) 51-57
24. Kato A., and Sakuma Y. Neuronal activity in female rat preoptic area associated with sexually motivated behavior. Brain Res 862 (2000) 90-102
25. Kouki T., Kishitake M., Okamoto M., Oosuka I., Takebe M., and Yamanouchi K. Effects of neonatal treatment with phytoestrogens, genistein and daidzein, on sex difference in female rat brain function: estrous cycle and lordosis. Horm Behav 44 (2003) 140-145
26. Kouki T., Okamoto M., Wada S., Kishitake M., and Yamanouchi K. Suppressive effect of neonatal treatment with a phytoestrogen, coumestrol, on lordosis and estrous cycle in female rats. Brain Res Bull 64 (2005) 449-454
27. Krege J.H., Hodgin J.B., Couse J.F., Enmark E., Warner M., Mahler J.F., et al. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci USA 95 (1998) 15677-15682
28. Kudwa A.E., and Rissman E.F. Double oestrogen receptor alpha and beta knockout mice reveal differences in neural oestrogen-mediated progestin receptor induction and female sexual behavior. J Neuroendocrinol 15 (2003) 978-983
29. Kuiper G.G., Enmark E., Pelto-Huikko M., Nilsson S., and Gustafsson J.A. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93 (1996) 5925-5930
30. Mazzucco C.A., Lieblich S.E., Bingham B.I., Williamson M.A., Viau V., and Galea L.A. Both estrogen receptor alpha and estrogen receptor beta agonists enhance cell proliferation in the dentate gyrus of adult female rats. Neuroscience 141 (2006) 1793-1800
31. McDonnell D.P., Connor C.E., Wijayaratne A., Chang C.Y., and Norris J.D. Definition of the molecular and cellular mechanisms underlying the tissue-selective agonist/antagonist activities of selective estrogen receptor modulators. Recent Prog Horm Res 57 (2002) 295-316
32. McInerney E.M., and Katzenellenbogen B.S. Different regions in activation function-1 of the human estrogen receptor required for antiestrogen- and estradiol-dependent transcription activation. J Biol Chem 271 (1996) 24172-24178
33. Meisel R.L., Dohanich G.P., McEwen B.S., and Pfaff D.W. Antagonism of sexual behavior in female rats by ventromedial hypothalamic implants of antiestrogen. Neuroendocrinology 45 (1987) 201-207
34. Meyers M.J., Sun J., Carlson K.E., Marriner G.A., Katzenellenbogen B.S., and Katzenellenbogen J.A. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 44 (2001) 4230-4251
35. Miller N.R., Jover T., Cohen H.W., Zukin R.S., and Etgen A.M. Estrogen can act via estrogen receptor alpha and beta to protect hippocampal neurons against global ischemia-induced cell death. Endocrinology 146 (2005) 3070-3079
36. Moon L.Y., Wakley G.K., and Turner R.T. Dose-dependent effects of tamoxifen on long bones in growing rats: influence of ovarian status. Endocrinology 129 (1991) 1568-1574
37. Mosselman S., Polman J., and Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett 392 (1996) 49-53
38. Nomura M., Andersson S., Korach K.S., Gustafsson J.A., Pfaff D.W., and Ogawa S. Estrogen receptor-beta gene disruption potentiates estrogen-inducible aggression but not sexual behaviour in male mice. Eur J Neurosci 23 (2006) 1860-1868
39. Nomura M., Durbak L., Chan J., Smithies O., Gustafsson J.A., Korach K.S., et al. Genotype/age interactions on aggressive behavior in gonadally intact estrogen receptor beta knockout (betaERKO) male mice. Horm Behav 41 (2002) 288-296
40. Ogawa S., Chan J., Chester A.E., Gustafsson J.A., Korach K.S., and Pfaff D.W. Survival of reproductive behaviors in estrogen receptor beta gene-deficient (betaERKO) male and female mice. Proc Natl Acad Sci USA 96 (1999) 12887-12892
41. Ogawa S., Eng V., Taylor J., Lubahn D.B., Korach K.S., and Pfaff D.W. Roles of estrogen receptor-alpha gene expression in reproduction-related behaviors in female mice. Endocrinology 139 (1998) 5070-5081
42. Paredes R.G., and Vazquez B. What do female rats like about sex? Paced mating. Behav Brain Res 105 (1999) 117-127
43. Pettersson K., Delaunay F., and Gustafsson J.A. Estrogen receptor beta acts as a dominant regulator of estrogen signaling. Oncogene 19 (2000) 4970-4978
44. Pettersson K., and Gustafsson J.A. Role of estrogen receptor beta in estrogen action. Annu Rev Physiol 63 (2001) 165-192
45. Pfaff D.W., Vasudevan N., Kia H.K., Zhu Y.S., Chan J., Garey J., et al. Estrogens, brain and behavior: studies in fundamental neurobiology and observations related to women's health. J Steroid Biochem Mol Biol 74 (2000) 365-373
46. Pfaus J.G., Smith W.J., and Coopersmith C.B. Appetitive and consummatory sexual behaviors of female rats in bilevel chambers. I. A correlational and factor analysis and the effects of ovarian hormones. Horm Behav 35 (1999) 224-240
47. Rhodes M.E., and Frye C.A. ERbeta-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiol Learn Mem 85 (2006) 183-191
48. Rissman E.F., Heck A.L., Leonard J.E., Shupnik M.A., and Gustafsson J.A. Disruption of estrogen receptor beta gene impairs spatial learning in female mice. Proc Natl Acad Sci USA 99 (2002) 3996-4001
49. Rissman E.F., Wersinger S.R., Fugger H.N., and Foster T.C. Sex with knockout models: behavioral studies of estrogen receptor alpha. Brain Res 835 (1999) 80-90
50. 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
51. Shima N., Yamaguchi Y., and Yuri K. Distribution of estrogen receptor beta mRNA-containing cells in ovariectomized and estrogen-treated female rat brain. Anat Sci Int 78 (2003) 85-97
52. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388 (1997) 507-525
53. Shughrue P.J., and Merchenthaler I. Distribution of estrogen receptor beta immunoreactivity in the rat central nervous system. J Comp Neurol 436 (2001) 64-81
54. Simon N.G., Kaplan J.R., Hu S., Register T.C., and Adams M.R. Increased aggressive behavior and decreased affiliative behavior in adult male monkeys after long-term consumption of diets rich in soy protein and isoflavones. Horm Behav 45 (2004) 278-284
55. Stauffer S.R., Coletta C.J., Tedesco R., Nishiguchi G., Carlson K., Sun J., et al. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem 43 (2000) 4934-4947
56. Tremblay G.B., Tremblay A., Copeland N.G., Gilbert D.J., Jenkins N.A., Labrie F., et al. Cloning, chromosomal localization, and functional analysis of the murine estrogen receptor beta. Mol Endocrinol 11 (1997) 353-365
57. Turner R.T., Wakley G.K., Hannon K.S., and Bell N.H. Tamoxifen prevents the skeletal effects of ovarian hormone deficiency in rats. J Bone Miner Res 2 (1987) 449-456
58. Vanderhorst V.G., Gustafsson J.A., and Ulfhake B. Estrogen receptor-alpha and -beta immunoreactive neurons in the brainstem and spinal cord of male and female mice: relationships to monoaminergic, cholinergic, and spinal projection systems. J Comp Neurol 488 (2005) 152-179
59. Walf A.A., Ciriza I., Garcia-Segura L.M., and Frye C.A. Antisense oligodeoxynucleotides for estrogen receptor-beta and alpha attenuate Estradiol's modulation of affective and sexual behavior, respectively. Neuropsychopharmacology 33 (2008) 431-440
60. Walf A.A., and Frye C.A. ERbeta-selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats. Neuropsychopharmacology 30 (2005) 1598-1609
61. Zou A., Marschke K.B., Arnold K.E., Berger E.M., Fitzgerald P., Mais D.E., et al. Estrogen receptor beta activates the human retinoic acid receptor alpha-1 promoter in response to tamoxifen and other estrogen receptor antagonists, but not in response to estrogen. Mol Endocrinol 13 (1999) 418-430