Estrogen receptor function as revealed by knockout studies: Neuroendocrine and behavioral aspects

Hormones and Behavior

Volumn 31, Issue 3, 1997, Pages 232-243

  Rissman, Emilie F ^a   Wersinger, Scott R ^a   Taylor, Julia A ^b   Lubahn, Dennis B ^b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; ESTROGEN; ESTROGEN RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; ESTROGEN RELEASE; FEMALE; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MALE; MOLECULAR CLONING; MOUSE; NEUROENDOCRINE SYSTEM; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; SEXUAL BEHAVIOR;

EID: 0031171415     PISSN: 0018506X     EISSN: None     Source Type: Journal    
DOI: 10.1006/hbeh.1997.1390     Document Type: Article

References (77)

1. Aronica, S. M., Kraus, W. L., and Katzenellenbogen, B. S. (1994). Estrogen action via the cAMP signalling pathway: Stimulation of adenylate cyclase and cAMP-regulated gene transcription. Proc. Natl. Acad. Sci. USA 91, 8517-8521.
2. Auchus, R. J., and Fuqua, S. A. W. (1994). The oestrogen receptor. In M. C. Shepperd and P. M. Stewart (Eds.), Balliere's Clinical Endocrinology and Metabolism: Hormones, Enzymes and Receptors, Vol. 8, pp. 433-449. Balliere Tindall, London.
3. Baum, M. J., and Vreeburg, J. T. M. (1973). Copulation in castrated male rats following combined treatment with estradiol and dihydrotestosterone. Science 182, 283-285.
4. Baum, M. J., and Vreeburg, J. T. M. (1976). Differential effects of the anti-estrogen MER-25 and of three 5α-reduced androgens on mounting and lordosis behavior in the rat. Horm. Behav. 7, 87-104.
5. Baum, M. J., Tobet, S. A., Starr, M. S., and Bradshaw, W. G. (1982). Implantation of dihydrotestosterone propionate into the lateral septum or medial amygdala facilitates copulation in castrated male rats given estradiol systemically. Horm. Behav. 16, 208-223.
6. Baum, M. J., Carroll, R. S., Cherry, J. A., and Tobet, S. A. (1990). Steroidal control of behavioral neuroendocrine and brain sexual differentiation: Studies in a carnivore, the ferret. J. Neuroendocrinol. 2, 401-418.
7. Bean, N. J., Nyby, J., Kerchner, M., and Dahinden, Z. (1986). Hormonal regulation of chemosignal-stimulated precopulatory behaviors in male housemice (Mus musculus). Horm. Behav. 20(4), 390-404.
8. Berthois, Y., Pourreau-Schneider, N., Yannariello-Brown, J., Collin, T. J., and Watson, C. S. (1986). Estradiol membrane binding sites on human breast cancer cell lines. J. Steroid Biochem. 25, 96-97.
9. Blaustein, J. D., and Olster, D. H. (1989). Gonadal steroid hormone receptors and social behaviors. In J. Balthazart (Ed.), Advances in Comparative and Environmental Physiology, Vol. III, pp. 31-104. Springer-Verlag, Berlin.
10. Byers, M., Kuiper, G. G. J., J. M., Gustaffson, J. A., and Park-Sarge, O. K. (1997). Estrogen receptor β mRNA expression in rat ovary: down-regulation by gonadotrophins. Mol. Endocrinol. 11, 172-182.
11. Charest, N. J., Zhou, Z.-X., Lubahn, D. B., Olsen, K. L., Wilson, E. M., and French, F. S. (1991). A frameshift mutation destabilizes androgen receptor messenger RNA in the Tfm mouse. Mol. Endocrinol. 5, 573-581.
12. Christensen, L. W., and Clemens, L. G. (1974). Intrahypothalamic implants of testosterone or estradiol and resumption of masculine sexual behavior in long-term castrated male rats. Endocrinology 95(4), 984-990.
13. Christensen, L. W., and Clemens, L. G. (1975). Blockage of testosterone-induced mounting behavior in the male rat with intracranial application of the aromatization inhibitor, androst-1,4,6-triene-3,17-dione. Endocrinology 97, 1545-1551.
14. Couse, J. F., Curtis, S. W., Washburn, T. F., Lindzey, J., Golding, T. S., Lubahn, D. B., Smithies, O., and Korach, K. S. (1995a). Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene. Mol. Endocrinol. 9, 1441-1454.
15. Couse, J. F., Curtis, S. W., Washburn, T. F., Eddy, E. M., Schomberg, D. W., and Korach, K. S. (1995b). Disruption of the mouse oestrogen receptor gene: resulting phenotypes and experimental findings. Biochem. Soc. Trans. 23(4), 929-935.
16. Das, S. K., Taylor, J. A., Korach, K. S., Paria, B. C., Dey, S. K., and Lubahn, D. B. Estrogenic responses in estrogen receptor (ER)-deficient mice reveal a novel non-ER mediated signaling pathway. Submitted for publication.
17. De Vries, G. J. (1990). Sex differences in neurotransmitter systems. J. Neuroendocrinol. 2, 1-13.
18. Donaldson, K. M., Tong, S. Y., Washburn, T., Lubahn, D. B., Eddy, E. M., Hutson, J. M., and Korach, K. S. (1996). Morphometric study of the gubernaculum in male estrogen receptor mutant mice. J. Androl. 17, 91-95.
19. Eddy, E. M., Washburn, T. F., Bunch, D. O., Goulding, E. H., Gladen, B. C., Lubahn, D. B., and Korach, K. S. (1996). Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 137, 4796-4805.
20. Edwards, D. A. (1968). Mice: Fighting by neonatally androgenized females. Science 161, 1027-1028.
21. Edwards, D. A. (1971). Neonatal administration of androstenedione, testosterone or testosterone propionate: Effects on ovulation, sexual receptivity and aggressive behavior in female mice. Physiol. Behav. 6(3), 223-228.
22. Evans, R. M. (1988). The steroid and thyroid receptor superfamily. Science 240, 889-895.
23. Even, M. D., vom Saal, F. S. (1991). Seminal vesicle and preputial gland response to steroids in adult male mice is influenced by prior intrauterine position. Physiol. Behav. 51, 11-16.
24. Farhat, M. Y., Lavigne, M. C., and Ramwell, P. W. (1996). The vascular protective effects of estrogen. FASEB J. 10, 615-624.
25. Frank, G. R. (1995). The role of estrogen in pubertal skeletal physiology: epiphyseal maturation and mineralization of the skeleton. Acta Pediatr. 84, 627-630.
26. Freeman, L. M., Padgett, B. A., Prins, G. S., and Breedlove, S. M. (1995). Distribution of androgen receptor immunoreactivity in the spinal cord of wild-type, androgen-insensitive and gonadectomized male rats. J. Neurobiol. 27, 51-59.
27. Freter, C. E., Lippman, M. E., Cheville, A., Zinn, S., and Gelman, E. P. (1988). Alterations in phosphoinositide metabolism associated with 17β-estradiol and growth factor treatment of MCF-7 breast cancer cells. Mol. Endocrinol. 2, 159-166.
28. Friend, K. E., Ang, L. W., and Shupnik, M. A. (1995). Estrogen regulates the expression of several different estrogen receptor mRNA isoforms in rat pituitary. Proc. Natl. Acad. Sci. USA 92, 4367-4371.
29. Graber, R., Sumida, C., Vallette, G., and Nunez, E. A. (1992). Rapid and long-term effects of 17β-estradiol on PIP2-phospholipase C-specific activity of MCF-7 cells. Cell. Signal. 5, 181-186.
30. Greene, G. L., Sobel, N. B., King, W. J., and Jensen, E. V. (1984). Immunochemical studies of estrogen receptors. J. Steroid Biochem. 20, 51-56.
31. He, W. W., Young, C. Y.-F., and Tindall, D. J. (1990). The molecular basis of the mouse testicular feminization (Tfm) mutation: A frameshift mutation. "72nd Annual Meeting of the Endocrine Soc. Atlanta, GA," p. 240.
32. Heimer, L., and Larsson, K. (1966/1967). Impairment of mating behavior in male rats following lesions in the preoptic-anterior hypothalamic continuum. Brain Res. 3, 248-263.
33. Hou, Q., and Gorski, J. (1993). Estrogen receptor and progesterone receptor genes are expressed differentially in mouse embryos during preimplantation development. Proc. Natl. Acad. Sci. USA 90, 9460-9464.
34. Jordan, V. C., and Dix, C. J. (1979). Effect of estradiol benzoate, tamoxifen and monohydroxytamoxifen on immature rat uterine progesterone receptor synthesis and endometrial cell division. J. Steroid Biochem. 11, 285-291.
35. Karas, R. H., Baur, W. E., van Eickles, M., and Mendelsohn, M. E. (1995). Human vascular smooth cells express an estrogen receptor isoform. FEBS Lett. 377, 103-108.
36. Kimura, T., and Hagiwara, Y. (1985). Regulation of urine marking in male and female mice: Effects of sex steroids. Horm. Behav. 19, 64-70.
37. Kuiper, G. G., J. M., Enmark, E., Pelto-Huikko, M., Nilsson, S., and Gustafsson, J. A. (1996). Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA 93, 5925-5930.
38. Kuiper, G. G., J. M., Carlsson, B., Grandien, K., Enmark, E., Haggblad, J., Nilsson, S., and Gustafsson, J. A. (1997). Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors a and β. Endocrinology 138, 863-870.
39. Lubahn, D. B., Moyer, J. S., Golding, T. S., Couse, J. F., Korach, K. S., and Smithies, O. (1993). Alteration of reproductive function but not prenatal sexual development after insertational disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. USA 90, 11162-11166.
40. Luttge, W. G., and Hall, N. R. (1973). Differential effectiveness of testosterone and its metabolites in the induction of male sexual behavior in two strains of albino mice. Horm. Behav. 4, 31-43.
41. McEwen, B. S. (1991). Non-genomic and genomic effects of steroids on neural activity. Trends Pharmacol. Sci. 12, 141-147.
42. Meisel, R. L., and Sachs, B. D. (1994). The physiology of male sexual behavior. In E. Knobil and J. D. Neill (Eds.), The Physiology of Reproduction, Vol. II, pp. 3-106. Raven Press, New York.
43. Merchenthaler, I., Shughrue, P. J., Lubahn, D. B., Negro-Vilar, A., and Korach, K. S. (1996). Estrogen responses in estrogen receptor-disrupted mice: An in vivo autoradiographic and in situ hybridization study. Int. Congr. Endocrinol. 10(2), 744.
44. Mosselman, S., Polman, J., and Dijkema, R. (1996). ERβ: identification and characterization of a novel human estrogen receptor. FEBS Lett. 92, 49-53.
45. Motelica-Heino, I., Castanier, M., Corbier, P., Edwards, D. A., and Roffi, J. (1988). Testosterone levels in plasma and testes of neonatal mice. J. Steroid Biochem. 31(3), 283-286.
46. Motelica-Heino, I., Edwards, D. A., and Roffi, J. (1993). Intermale aggression in mice: Does hour of castration after birth influence adult behavior? Physiol. Behav. 53, 1017-1019.
47. Nunez, A. A., Nyby, J., and Whitney, G.(1978). The effects of testosterone, estradiol, and dihydrotestosterone on male mouse (Mus musculus) ultrasonic vocalizations. Horm. Behav. 11, 264-272.
48. Nyby, J., Dizinno, G., and Whitney, G. (1977). Sexual dimorphism in ultrasonic vocalizations of mice (Mus musculus): gonadal hormone regulation. J. Comp. Physiol Psychol 91, 1424-1431.
49. Nyby, J., Matochik, J. A., and Barfield, R. J. (1992). Intracranial androgenic and estrogenic stimulation of male-typical behaviors in house mice (Mus domesticus). Horm. Behav. 26, 24-45.
50. Nyby, J. G., and Simon, N. G. (1987). Nonaromatizable androgens may stimulate a male mouse reproductive behavior by binding estrogen receptors. Physiol. Behav. 39, 147-151.
51. Ogawa, S., Lubahn, D. B., Korach, K. S., and Pfaff, D. W. (1995). Behavioral characteristics of transgenic estrogen receptor knockout male mice: Sexual, aggressive and open-field behaviors. Endocrin. Soc. Abstr. 77, 133.
52. Ogawa, S., Gordon, J. D., Taylor, J., Lubahn, D., Korach, K., and Pfaff, D. W. (1996b). Reproductive functions illustrating direct and indirect effects of genes on behavior. Horm. Behav. 30, 487-494.
53. Ogawa, S., Taylor, J., Lubahn, D., Korach, K., and Pfaff, D. W. (1996a). Reversal of sex roles in genetic female mice by disruption of estrogen receptor gene. Neuroendocrinology 64, 467-470.
54. Olsen, K. L. (1992). Genetic influences on sexual behavior differentiation. In Handbook of Behavioral Neurobiology, Vol. 11, pp. 1-40.
55. Pappas, T. C., Gametchu, B., and Watson, C. S. (1994). Membrane estrogen receptors identified by multiple antibody labeling and impeded-ligand binding. FASEB J. 9, 404-410.
56. Pfaff, D. W., Schwartz-Giblin, S., McCarthy, M. M., and Kow, L. M. (1994). Cellular and molecular mechanisms of female reproductive behaviors. In E. Knobil and J. D. Neill (Eds.), The Physiology of Reproduction, Vol. II, pp. 107-220. Raven Press, New York.
57. Pietras, R. J., and Szego, C. M. (1980). Partial purification and characterization of oestrogen receptors in subfractions of hepatocyte plasma membranes. Biochem. J. 191, 743-760.
58. Ramirez, V. D. (1992). Characterization of membrane action of steroids. Neuroprotein 1, 35-41.
59. Resko, J. A., and Roselli, C. E. (1992). Brain steroids synthesis and metabolism. Neuroprotein 1, 27-34.
60. Rissman, E. F., Early, A. H., Taylor, J. A., Korach, K. S., and Lubahn, D. B. (1997). Estrogen receptors are essential for female sexual receptivity. Endocrinology 138, 507-510.
61. Roselli, C. E. (1991). Sex differences in androgen receptor and aromatase activity in the rat hypothalamus and limbic system. Endocrinology 117, 2471-2477.
62. Shughrue, P. J., Komm, B., and Merchenthaler, I. (1996). The distribution of estrogen receptor β mRNA in the rat hypothalamus. Steroids 61, 678-681.
63. Shupnik, M. A., Gordon, M. S., and Chin, W. W. (1989). Tissue-specific regulation of rat estrogen receptor mRNAs. Mol. Endocrinol. 3, 660-665.
64. Simerly, R. B. (1990). Hormonal control of neuropeptide gene expression in sexually dimorphic olfactory pathways. Trends Neurosci. 13, 104-110.
65. Simerly, R. B., Korach, K. S., Lubahn, D. B., and Zee, M. (1996). Disruption of the estrogen receptor gene interferes with sexual differentiation of dopamine neurons in the preoptic region of the mouse. Soc. Neurosci. Abstr. 22(1), 561.
66. Skipper, J. K., Young, L. J., Bergeron, J. M., Tetzlaff, M. T., Osborn, C. T., and Crews, D. (1993). Identification of an isoform of the estrogen receptor messenger RNA lacking exon four and present in the brain. Proc. Natl. Acad. Sci. USA 90, 7172-7175.
67. Smith, E. P., Boyd, J., Frank, G. R., Takahashi, H., Cohen, R. M., Specker, B., Williams, T. C., Lubahn, D. B., and Korach, K. S. (1994). Estrogen resistance caused by a mutation in the estrogen receptor gene in a man. N. Engl. J. Med. 331, 1056-1061.
68. Szego, C. M., and Davis, J. S. (1967). Adenosine 3′,5′-monophosphate in rat uterus: Acute elevation by estrogen. Proc. Natl. Acad. Sci. USA 58, 1711-1718.
69. Tobet, S. A., and Fox, T. O. (1992). Sex differences in neuronal morphology influenced hormonally throughout life. In A. A. Gerall, H. Moltz, and I. L. Ward (Eds.), Sexual Differentiation: Handbook of Behavioral Neurobiology, Vol. 11, pp. 41-83. Plenum, New York.
70. vom Saal, F. S., and Bronson, F. H. (1980). Sexual characteristics of adult female mice are correlated with their blood testosterone levels during prenatal development. Science 208, 597-599.
71. vom Saal, F. S., Grant, W., McMullin, C., and Laves, K. (1983). High fetal estrogen concentrations: Correlation with increased adult sexual performance and decreased aggression in male mice. Science 220, 1306-1309.
72. Watson, J. T., and Adkins-Regan, E. (1989). Activation of sexual behavior by implantation of testosterone propionate and estradiol benzoate into the preoptic area of the male Japanese quail. Horm. Behav. 23, 251-268.
73. Wee, B. E., Weaver, D. R., and Clemens, L. G. (1988). Hormonal restoration of masculine sexual behavior in long-term castrated B6D2F1 mice. Physiol. Behav. 42, 77-82.
74. Wersinger, S. R., Sannen, K., Villalba, C., Lubahn, D. B., Rissman, E. F., and De Vries, G. J. Estrogen receptor-α gene is required for masculine sexual behavior. Submitted for publication.
75. Wu, T. C., Wang, L., and Wan, Y. J. (1992). Expression of estrogen receptor gene in mouse oocyte and during embryogenesis. Mol. Reprod. Dev. 33, 407-412.
76. Wu, T. C., Wang, L., and Wan, Y. J. (1993). Detection of estrogen receptor messenger ribonucleic acid in human oocyte and cumulusoocyte complexes using reverse transcriptase-polymerase chain reaction. Fert. Steril. 59, 54-59.
77. Zyzek, E., Dufy-Barbe, L., Dufy, B., and Vincent, J. D. (1981). Short-term effect of estrogen on release of prolactin by pituitary cells in culture. Biochem. Biophys. Res. Commun. 102, 1151-1157.