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Prenatal Hormones Organize Sex Differences of the Neuroendocrine Reproductive System: Observations on Guinea Pigs and Nonhuman Primates

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REFERENCES

  • Anderson, R. H., Fleming, D. E., Rhees, R. W., and Kinghorn, E. (1986). Relationships between sexual activity, plasma testosterone, and the volume of the sexually dimorphic nucleus of the preoptic area in prenatally stressed and non-stressed rats. Brain Res. 370:1–10.

    Google Scholar 

  • Arendash, G. W., and Gorski, R. A. (1983). Effects of discrete lesions of the sexually dimorphic nucleus of the preoptic area or other medial preoptic regions on the sexual behavior of male rats. Brain Res. Bull. 10:147–154.

    Google Scholar 

  • Black, V. H., and Christensen, A. K. (1969). Differentiation of interstitial cells and sertoli cells in fetal guinea pig testes. Am. J. Anat. 124:211–238.

    Google Scholar 

  • Bleier, R., Byne, W., and Siggelkow, I. (1982). Cytoarchitectonic sexual dimorphisms of the medial preoptic and anterior hypothalamic areas in guinea pig, rat, hamster, and mouse. J. Comp. Neurol. 212:118–130.

    Google Scholar 

  • Brinkmann, A. O. (1977). Testosterone synthesis in vitro by the fetal testis of the guinea pig. Steroids 29:861–873.

    Google Scholar 

  • Brown-Grant, K., and Sherwood, M. R. (1971). The ‘early androgen syndrome’ in the guinea-pig. J. Endocrinol. 49:277–291.

    Google Scholar 

  • Buhl, A. E., Pasztor, L. M., and Resko, J. A. (1979). Sex steroids in guinea pig fetuses after sexual differentiation of the gonads. Biol. Reprod. 21:905–908.

    Google Scholar 

  • Byne, W., and Bleier, R. (1987). Medial preoptic sexual dimorphisms in the guinea pig. I. An investigation of their hormonal dependence. J. Neurosci. 7:2688–2696.

    Google Scholar 

  • Byne, W., Warren, J. T., and Siggelkow, I. (1987). Medial preoptic sexual dimorphisms in the guinea pig. II. An investigation of medial preoptic neurogenesis. J. Neurosci. 7:2697–2702.

    Google Scholar 

  • Cherry, J. A., and Baum, M. J. (1990). Effects of lesions of a sexually dimorphic nucleus in the preoptic/anterior hypothalamic area on the expression of androgen-and estrogen-dependent sexual behaviors in male ferrets. Brain Res. 522:191–203.

    Google Scholar 

  • Choate, J. V. A., and Resko, J. A. (1992). Androgen receptor immunoreactivity in intact and castrate guinea pigs using antipeptide antibodies. Brain Res. 597:51–59.

    Google Scholar 

  • Choate, J. V. A., and Resko, J. A. (1994). Prenatal inhibition of aromatase activity affects luteinizing hormone feedback mechanisms and reproductive behaviors of adult guinea pigs. Biol. Reprod. 51:1273–1278.

    Google Scholar 

  • Connolly, P. B., and Resko, J. A. (1989). Role of steroid 5 alpha-reductase activity in sexual differentiation of the guinea pig. Neuroendocrinology 49:324–330.

    Google Scholar 

  • Connolly, P. B., and Resko, J. A. (1994). Prenatal testosterone differentiates brain regions controlling gonadotropin release in guinea pigs. Biol. Reprod. 51:125–130.

    Google Scholar 

  • Connolly, P. B., Choate, J. V. A., and Resko, J. A. (1994a). Effects of exogenous androgen on brain androgen receptors of the fetal rhesus monkey. Neuroendocrinology 59:271–276.

    Google Scholar 

  • Connolly, P. B., Roselli, C. E., Resko, J. A. (1994b). Aromatase activity in developing guinea pig brain: Ontogeny and effects of exogenous androgens. Biol. Reprod. 50:436–441.

    Google Scholar 

  • Cummins, D., and Yahr, P. (1984). Lesions of the sexually dimorphic area disrupt mating and marking in male gerbils. Brain Res. Bull. 13:185–193.

    Google Scholar 

  • Dantchakoff, V. (1938), Role des hormones dans la manifestation des instincts sexueles. Compt. Rend. 206:945–947.

    Google Scholar 

  • De Jonge, F. H., Lauwerse, A. L., Ooms, M. P., Evers, P., Endert, E., and Van De Poll, N. E. (1989). Lesions of the SDN-POA inhibit sexual behavior of male Wistar rats. Brain Res. Bull. 23:483–492.

    Google Scholar 

  • Goldfoot, D. A., and Van Der Werff Ten Bosch, J. J. (1975). Mounting behavior of female guinea pigs after prenatal and adult administration of the propionates of testosterone, dihydrotestosterone, and androstanediol. Horm. Behav. 6:139–148.

    Google Scholar 

  • Gorski, R. A. (1985). Sexual differentiation of the brain: possible mechanisms and implications. Can. J. Physiol. Pharm. 63:577–594.

    Google Scholar 

  • Goy, R. W., and Resko, J. A. (1972). Gonadal hormones and behavior of normal and pseudoher-maphroditic nonhuman female primates. Recent Prog. Horm. Res. 28:707–733.

    Google Scholar 

  • Handa, R. J., Connolly, P. B., and Resko, J. A. (1988). Ontogeny of cytosolic androgen receptors in the brain of the fetal rhesus monkey. Endocrinology 122:1890–1896.

    Google Scholar 

  • Haqq, C. M., King, C., Ukiyama, E., Falsafi, S., Haqq, T. N., Donahoe, P. K., and Weiss, M. A. (1994). Molecular basis of mammalian sexual determination: activation of mullerian inhibiting substance gene expression by SRY. Science 266:494–500.

    Google Scholar 

  • Hines, M., Davis, F. C., Coquelin, A., Goy, R. W., and Gorski, R. A. (1985). Sexually dimorphic regions in the medial preoptic area and the bed nucleus of the stria terminalis of the guinea pig brain. A description and an investigation of their relationship to gonadal steroids in adulthood. J. Neurosci. 5:40–47.

    Google Scholar 

  • Hines, M., Alsum, P., Roy, M., Gorski, R. A., and Goy, R. W. (1987). Estrogenic contributions to sexual differentiation in the female guinea pig: influences of diethystibestrol, and tamoxifen on neural, behavioral, and ovarian development. Horm. Behav. 21:402–417.

    Google Scholar 

  • Houtsmuller, E. J., Brand, T., de Jong, F. H., Joosten, R. N., Van De Poll, N. E., and Slob, A. (1994). SDN-POA volume, sexual behavior and partner preference in male rats affected by perinatal treatment with ATD. Physiol. Behav. 56:535–541.

    Google Scholar 

  • Karsch, F. J., and Foster, D. L. (1975). Sexual differentiation of the mechanism controlling the preovulatory discharge of luteinizing hormone in sheep. Endocrinology 97:373–379.

    Google Scholar 

  • Karsch, F. J., Dierschke, D. J., and Knobil, E. (1973). Sexual differentiation of pituitary function: apparent difference between primates and rodents. Science 179:484–486.

    Google Scholar 

  • MacLusky, N. J., and Naftolin, F. (1981). Sexual differentiation of the central nervous system. Science 211:1294–1302.

    Google Scholar 

  • Neill, J. D. (1972). Sexual differences in the hypothalamic regulation of prolactin secretion. Endocrinology 90:1154–1159.

    Google Scholar 

  • Norman, R. L., and Spies, H. G. (1986). Cyclic ovarian function in a male macaque: Additional evidence for a lack of sexual differentiation in the physiological mechanisms that regulate the cyclic release of gonadotropins in primates. Endocrinology 118:2608–2610.

    Google Scholar 

  • Ortiz, E., Price, D., and Zaaijer, J. P. (1966). Organ culture studies of hormone secretion in endocrine glands of fetal guinea pigs. II. Secretion of androgenic hormone in adrenals and testes during early stages of development. Proc. Natl. Acad. Sci. U.S.A. 69:400–408.

    Google Scholar 

  • Page, D. C., Mosher, R., Simpson, E. M., Fisher, M. C., Mardon, G., Pollack, J., McGillivary, B., and de la Chapelle, A. (1987). The sex-determining region of the human Y chromosome encodes a zinc finger protein. Cell 51:1091–1104.

    Google Scholar 

  • Paredes, R. G., and Baum, M. J. (1995). Altered sexual partner preference in male ferrets given exitotoxic lesions of the preoptic area anterior hypothalamus. J. Neurosci. 15:6619–6630.

    Google Scholar 

  • Pasqualini, J. R., Kincl, F. A., and Sumida, C. (1991). Sexual Differentiation and Fetal Endocrinology. Hormones and the Fetus. Pergamon Press, New York, pp. 265–356.

    Google Scholar 

  • Phoenix, C. H. (1978). Sexual behavior of laboratory-and wild-born male rhesus monkeys. Horm. Behav. 10:178–192.

    Google Scholar 

  • Phoenix, C. H., Goy, R. W., Gerall, A. A., and Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissue mediating mating behavior in the female guinea pig. Endocrinology 65:369–382.

    Google Scholar 

  • Phoenix, C. H., Goy, R. W., and Resko, J. A. (1968). Psychosexual differentiation as a function of androgenic stimulation. In Diamond, M. (ed.), Perspectives in Reproduction and Sexual Behavior, Indiana University Press, Bloomington and London, pp. 33–49.

    Google Scholar 

  • Pomerantz, S. M., Goy, R. W., and Roy, M. M. (1986). Expression of male typical behavior in adult female pseudohermaphroditic rhesus: comparisons with normal males and neonatally gonadectomized males and females. Horm. Behav. 20:483–500.

    Google Scholar 

  • Resko, J. A., Ellinwood, W. E., Pasztor, L. M., and Buhl, A. E. (1980). Sex steroids in the umbilical circulation of fetal rhesus monkeys from the time of gonadal differentiation. J. Clin. Endocrinol. Metab. 50:900–905.

    Google Scholar 

  • Resko, J. A., Buhl, A. E., and Phoenix, C. H. (1987). Treatment of pregnant rhesus macaques with testosterone propionate: observations on its fate in the fetus. Biol. Reprod. 37:1185–1191.

    Google Scholar 

  • Rigaudière, N., Wolff, M. É. (1977) Endocrinologie-Évolution des teneurs en testostérone et dihydrotestostérone dans le plasma, le testicule et l'ovaire chez le cobaye au cours de la vie foetale. C.R. Acad. Sci. Paris 285:989–992.

    Google Scholar 

  • Sachs, B. D., and Meisel, R. L. (1988). The physiology of male sexual behavior. In Knobil, E., and Neill, J. D., (eds.), The Physiology of Reproduction, Raven Press. New York, pp. 1393–1485.

    Google Scholar 

  • Sholl, S. A., and Goy, R. W. (1978). Androgen and estrogen synthesis in the fetal guinea pig gonad. Biol. Reprod. 18:160–169.

    Google Scholar 

  • Short, R. V. (1974). The sexual endocrinology of the perinatal period. In Forest, M. G., and Bertrand, J., (eds.), Colloque International Lyon, France, INSERM, p. 121.

  • Simerly, R. B., and Swanson, L. W. (1988). Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterior grade tract-tracing study in the rat. J. Comp. Neurol. 270:209–242.

    Google Scholar 

  • Steiner, R. A., Clifton, D. K., Spies, H. G., and Resko, J. A. (1976). Sexual differentiation and feedback control of luteinizing hormone secretion in the rhesus monkey. Biol. Reprod. 15:206–212.

    Google Scholar 

  • Terasawa, E., Rodriguez, J. S., Bridson, W. E., and Wiegand, J. (1979). Factors influencing the positive feedback action of estrogen upon the luteinizing hormone surge in the ovariectomized guinea pig. Endocrinology 104:680–686.

    Google Scholar 

  • Toyooka, K. T., Connolly, P. B., Handa, R. J., and Resko, J. A. (1989). Ontogeny of androgen receptors in fetal guinea pig brain. Biol. Reprod. 41:204–212.

    Google Scholar 

  • Toyooka, K. T., Connolly, P. B., and Resko, J. A. (1991). Effects of exogenous steroids on androgen receptors in fetal guinea pig brain. Biol. Reprod. 44:1051–1062.

    Google Scholar 

  • van Wagenen, G. and Simpson, M. E. (1965). Embryology of the Ovary and Testes. Homo sapiens and Macaca mulatta. Yale University Press, New Haven, CT, 1965, p. 59

    Google Scholar 

  • Warembourg, M., Jolivet, A., Milgrom, E. (1989), Immunohisochemical evidence of the presence of estrogen and progesterone receptors in the same neurons of the guinea pig hypothalamus and preoptic area. Brain Res. 480:1–15.

    Google Scholar 

  • Wells, L. J., and van Wagenen, G. (1954). Androgen-induced female pseudohermaphroditism in the monkey (Macaca mulatta): Anatomy of the reproductive organs. Contrib. Embryol. 35:93–106.

    Google Scholar 

  • Westfahl, P. K., Stadelman, H. L., Horton, L. E., and Resko, J. A. (1984). Experimental induction of estradiol positive feedback in intact male monkeys: Absence of inhibition by physiologic concentrations of testosterone. Biol. Reprod. 31:856–862.

    Google Scholar 

  • Wiegand, S. J., Terasawa, E., and Bridson, W. E. (1978). Persistent estrus and blockade of progesterone-induced LH release follows lesions which do not damage the suprachiasmatic nucleus. Endocrinology 102:1645–1648.

    Google Scholar 

  • Yamaji, T., Dierschke, D. J., Hotchkiss, J., Bhattacharya, A. N., Surve, A. H., and Knobil, E. (1971). Estrogen induction of LH release in the rhesus monkey. Endocrinology 89:1034–1041.

    Google Scholar 

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Resko, J.A., Roselli, C.E. Prenatal Hormones Organize Sex Differences of the Neuroendocrine Reproductive System: Observations on Guinea Pigs and Nonhuman Primates. Cell Mol Neurobiol 17, 627–648 (1997). https://doi.org/10.1023/A:1022534019718

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