The Aromatase Knockout (ArKO) Mouse Provides New Evidence That Estrogens Are Required for the Development of the Female Brain

Annals of the New York Academy of Sciences

Volumn 1007, Issue , 2003, Pages 251-262

  Bakker, J ^a   Honda, S ^b   Harada, N ^b   Balthazart, J ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b FUJITA HEALTH UNIVERSITY   (Japan)

Author keywords

Aromatase; Estradiol; Female differentiation; Olfaction; Sexual behavior

Indexed keywords

ANDROGEN; AROMATASE; CYTOCHROME P450; ESTROGEN; PROGESTERONE;

ANIMAL BEHAVIOR; AROMATIZATION; BRAIN DEVELOPMENT; CONFERENCE PAPER; DRUG EFFECT; ENZYME ACTIVITY; FEMALE; GENE MUTATION; HORMONE RELEASE; KNOCKOUT MOUSE; NONHUMAN; ODOR; OLFACTORY SYSTEM; SEX DIFFERENTIATION; SMELLING DISORDER;

ANIMALIA;

EID: 1342287977     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1196/annals.1286.024     Document Type: Conference Paper

References (52)

1. PHOENIX, C.H., R.W. GOY, A.A. GERALL & W.C. YOUNG. 1959. Organizational action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65: 369-382.
2. FEDER, H.H. & R.E. WHALEN. 1965. Feminine behavior in neonatally castrated and estrogen-treated male rats. Science 147: 306-307.
3. GRADY, K.L., C.H. PHOENIX & W.C. YOUNG. 1965. Role of the developing rat testis in differentiation of the neural tissues mediating mating behavior. J. Comp. Physiol. Psychol. 59: 176-182.
4. TORAN-ALLERAND, C.D. 1976. Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vivo: implications for sexual differentiation. Brain Res. 106: 407-412.
5. GERALL, A.A., J.L. DUNLAP & S.E. HENDRICKS. 1973. Effect of ovarian secretions on female behavioral potentiality in the rat. J. Comp. Physiol. Psychol. 82: 449-465.
6. DÖHLER, K.D., J.L. HANCKE, S.S. SRIVASTAVA, et al. 1984. Participation of estrogens in female sexual differentiation of the brain: neuroanatomical, neuroendocrine, and behavioral evidence. In Progress in Brain Research. Vol. 61. Sex Differences in the Brain: The Relation between Structure and Function. G.J. de Vries, J.P.C. de Bruin, H.B.M. Uylings & M.A. Corner, Eds.: 99-117. Elsevier Science Publishers. Amsterdam.
7. BAUM, M.J. & S.A. TOBET. 1986. 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: 111-118.
8. MATHEWS, G.A., E.W. BRENOWITZ & A.P. ARNOLD. 1988. Paradoxical hypermasculinization of the zebra finch song system by an antiestrogen. Horm. Behav. 22: 540-551.
9. FISHER, C.R., K.H. GRAVES, A.F. PARLOW & E.R. SIMPSON. 1998. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the Cyp19 gene. Proc. Natl. Acad. Sci. USA 95: 6965-6970.
10. HONDA, S., N. HARADA, S. ITO, et al. 1998. Disruption of sexual behavior in male aromatase-deficient mice lacking exons 1 and 2 of the Cyp19 gene. Biochem. Biophys. Res. Commun. 252: 445-449.
11. TODA, K., T. OKADA, K. TAKEDA, et al. 2001. Oestrogen at the neonatal stage is critical for the reproductive ability of male mice as revealed by supplementation with 17β-oestradiol. J. Endocrinol. 170: 99-111.
12. BAKKER, J., S. HONDA, N. HARADA & J. BALTHAZART. 2002. The aromatase knockout mouse provides new evidence that estradiol is required during development in the female for the expression of socio-sexual behaviors in adulthood. J. Neurosci. 22: 9104-9112.
13. BEACH, F.A. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm. Behav. 7: 105-138.
14. TORAN-ALLERAND, C.D. 1984. On the genesis of sexual differentiation of the central nervous system: morphogenetic consequences of steroidal exposure and possible role of a-fetoprotein. In Progress in Brain Research. Vol. 61. Sex Differences in the Brain: The Relation between Structure and Function. G.J. de Vries, J.P.C. de Bruin, H.B.M. Uylings, M.A. Corner, Eds.: 63-98. Elsevier Science Publishers. Amsterdam.
15. WERSINGER, S.R., K. SANNEN, C. VILLALBA, et al. 1997. Masculine sexual behavior is disrupted in male and female mice lacking a functional estrogen receptor α. Horm. Behav. 32: 176-183.
16. PFAFF, D.W., S. SCHWARTZ-GIBLIN, M.M. MCCARTHY & L.-M. KOW. 1994. Cellular and molecular mechanisms of female reproductive behaviors. In The Physiology of Reproduction. Vol. 2. E. Knobil & J. Neill, Eds.: 107-220. Raven Press. New York.
17. EMERY, D.E. & R.L. MOSS. 1984. Lesions confined to the ventromedial hypothalamus decrease the frequency of coital contacts in female rats. Horm. Behav. 18: 313-329.
18. RUBIN, B.S. & R.J. BARFIELD. 1980. Priming of estrous responsiveness by implants of 17 beta-oestradiol in the ventromedial hypothalamic nucleus of female rats. Endocrinology 106: 504-509.
19. KARLSON, P. & M. LUSCHER. 1959. "Phermones": a new term for a class of biologically active substances. Nature 183: 55-56.
20. Meredith, M. 2001. Human vomeronasal organ function. Chem. Sens. 24: 433-445.
21. THOMPSON, M.L. & D.A. EDWARDS. 1972. Olfactory bulb ablation and hormonally induced mating in spayed female mice. Physiol. Behav. 8: 1141-1146.
22. EDWARDS, D.A. & K.G. BURGE. 1973. Olfactory control of the sexual behavior of male and female mice. Phsyiol. Behav. 11: 867-872.
23. FIRESTEIN, S. 2001. How the olfactory system makes sense of scents. Nature 413: 211-218.
24. SCOTT, J.W. 1986. The olfactory bulb and central pathways. Experientia 42: 223-232.
25. PRICE, J.L. 1987. In Neurobiology of Taste and Smell. T.E. Finger & W.L. Sliver, Eds.: 179-203. Wiley. New York.
26. SHIPLEY, M.T. & M. ENNIS. 1996. Functional organization of the olfactory system. J. Neurobiol. 30: 123-176.
27. KEVERNE, E.B. 1999. The vomeronasal organ. Science 286: 716-720.
28. MEREDITH, M. & R.J. O'CONNELL. 1979. Efferent control of stimulus access to the hamster vomeronasal organ. J. Physiol. (Lond.) 286: 301-316.
29. HALPERN, M., L.S. SHAPIRO & C. JIA. 1995. Differential localisation of G proteins in the opossum vomeronasal system. Brain Res. 677: 157-161.
30. SCALIA, F. & S.S. WINANS. 1975. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161: 31-55.
31. KEVETTER, G.A. & S.S. WINANS. 1981. Connections of the corticomedial amygdala in the golden hamster. I. Efferents of the "vomeronasal amygdala." J. Comp. Neurol. 197: 81-98.
32. LAU, Y.E., J.A. CHERRY, M.J. BAUM & S.K. MANI. 2003. Induction of Fos in the accessory olfactory system by male odors persists in female mice with a null mutation of the aromatase (Cyp19) gene. Brain Res. Bull. 60: 143-150.
33. WENIGER, J.P. 1993. Estrogen production by fetal rat gonads. J. Steroid Biochem. Mol. Biol. 44: 459-462.
34. WENIGER, J.P., A. ZEIS & J. CHOURAQUI. 1993. Estrogen production by fetal and infantile rat ovaries. Reprod. Nutr. Dev. 33: 129-136.
35. RAYNAUD, P. 1971. Influence of rat estradiol binding plasma protein (EBP) on uterotrophic activity. Steroids 21: 249-258.
36. LIEBERBURG, I. & B.S. MCEWEN. 1975. Estradiol-17b: a metabolite of testosterone recovered in cell nuclei from limbic areas of neonatal rat brains. Brain Res. 85: 165-170.
37. MCEWEN, B.S., L. PLAPINGER, C. CHAPTAL, et al. 1975. The role of fetoneonatal estrogen binding proteins in the association of estrogen with neonatal brain cell nuclear receptors. Brain Res. 96: 400-407.
38. BEYER, C., A. WOZNIAK & J.B. HUTCHISON. 1993. Sex-specific aromatization of testosterone in mouse hypothalamic neurons. Neuroendocrinology 58: 673-681.
39. HUTCHISON, J.B., C. BEYER, R.E. HUTCHISON & A. WOZNIAK. 1995. Sexual dimorphism in the developmental regulation of brain aromatase. J. Steroid. Biochem. Mol. Biol. 53: 307-313.
40. POINTIS, G., M.T. LATREILLE & L. CEDARD. 1980. Gonado-pituitary relationships in the fetal mouse at various times during sexual differentiation. J. Endocrinol. 86: 483-488.
41. SCHLINGER, B.A., K.K. SOMA & S.E. LONDON. 2001. Neurosteroids and brain sexual differentiation. TINS 24: 429-431.
42. HOLLOWAY, C.C. & D.E. CLAYTON. 2001. Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat. Neurosci. 4: 170-175.
43. COMPAGNONE, N.A. & S.H. MELLON. 2000. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinol. 21: 1-56.
44. GOY, R.W. 1970. Experimental control of psychosexuality. Philos. Trans. R. Soc. Lond. B Biol. Sci. 259: 149-162.
45. VREEBURG, J.T.M., P.D.M. VAN DER VAART & P. VAN DER SCHOOT. 1977. Prevention of central defeminization but not masculinization in male rats by inhibition of oestrogen biosynthesis. J. Endocrinol. 74: 375-382.
46. BAUM, M.J. 1979. Differentiation of coital behavior in mammals: a comparative analysis. Neurosci. Biobehav. Rev. 3: 265-284.
47. DAVIS, P.G., C.V. CHAPTEL & B.S. MCEWEN. 1979. Independence of differentiation of masculine and feminine sexual behavior in rats. Horm. Behav. 12: 12-19.
48. BAKKER, J., T. BRAND, J. VAN OPHEMERT & A.K. SLOB. 1993. Hormonal regulation of adult partner preference behavior in neonatally ATD-treated male rats. Behav. Neurosci. 107: 480-487.
49. FITCH, R.H., A.S. BERREBI, P.E. COWELL, et al. 1990. Corpus callosum: effects of neonatal hormones on sexual dimorphism in the rat. Brain Res. 515: 111-116.
50. MACK, C.M., R.H. FITCH, P.E. COWELL, et al. 1993. Ovarian estrogen acts to feminize the female rat's corpus callosum. Dev. Brain Res. 71: 115-119.
51. MACK, C.M., R.F. MCGIVERN, L.H. HYDE & V.H. DENENBERG. 1996. Absence of postnatal testosterone fails to demasculinize the male rat's corpus callosum. Dev. Brain Res. 95: 252-255.
52. BIMONTE, H.A., C.M. MACK, A.J. STAVNEZER & V.H. DENENBERG. 2000. Ovarian hormones can organize the rat corpus callosum in adulthood. Dev. Brain Res. 21: 637-645.