Sources of oestrogen in the testis and reproductive tract of the male

International Journal of Andrology

Volumn 22, Issue 4, 1999, Pages 211-223

  Carreau, Serge ^a,c   Genissel, C ^a   Bilinska, B ^b   Levallet, J ^a  

^a Universite   (France)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c UNIVERSITÉ DE CAEN   (France)

Author keywords

Aromatase; Mammals; Oestrogen receptors; Oestrogens; Reproductive tract; Spermatogenesis; Spermiogenesis; Testis

Indexed keywords

ANDROGEN; AROMATASE; CELL NUCLEUS RECEPTOR; CYTOCHROME P450; ESTROGEN; ESTROGEN RECEPTOR; GROWTH FACTOR; MEMBRANE RECEPTOR; SEX HORMONE;

AGING; ANIMAL CELL; BEAR; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME LOCALIZATION; ESTROGEN SYNTHESIS; EXON; FOWL; GENE EXPRESSION REGULATION; GERM CELL; HUMAN; LEYDIG CELL; MALE; MALE GENITAL SYSTEM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAT; REPRODUCTION; REVIEW; SERTOLI CELL; SEXUAL MATURATION; SHEEP; SOMATIC CELL; SPERMATOGENESIS; SWINE; TESTIS;

ANIMALS; AROMATASE; ESTROGENS; GENITALIA, MALE; HUMANS; MALE; TESTIS;

EID: 0032788523     PISSN: 01056263     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2605.1999.00172.x     Document Type: Review

References (135)

1. Almadhidi, J., Séralini, G. E., Fresnel, J., Silberzahn, P. & Gaillard, J. L. (1995) Immunohistochemical localization of cytochrome P450 aromatase in equine gonads. Journal of Histochemistry and Cytochemistry, 43, 571-7.
2. Attal, J. (1969) Levels of testosterone, androstenedione, estrone and oestradiol-17β in the testes of fetal sheep. Endocrinology, 85, 280-9.
3. Baggett, B., Eugel, L. L., Balderas, L., Lamman, G., Savard, K. & Dorfman, R. I. (1959) Conversion of C14-androgens to C14-oestrogenic steroids by endocrine tissues. Endocrinology, 64, 600-8.
4. Beck, K. J., Herschel, S., Hungershöffer, R. & Schwinger, E. (1976) The effect of sex steroid hormones on motility and selective migration of X-and Y-bearing human spermatozoa. Fertility and Sterility, 27, 407-12.
5. Benahmed, M. (1995) Growth factors and cytokines in the testis. In: Male Infertility; (ed. F. H. Comhaire), pp. 55-96. Chapman & Hall Medical.
6. Benahmed, M., Bernier, M., Ducharme, I. R. & Saez, J. M. (1982) Steroidogenesis of cultured purified pig Leydig cells: secretion and effects of oestrogens. Molecular and Cellular Endocrinology, 28, 705-16.
7. Benten, W. P. M., Lieberherr, M., Giese, G. & Wunderlich, F. (1998) Estradiol binding to cell surface raises cytosolic free calcium in T cells. FEBS Letters, 422, 349-53.
8. Betka, M. & Callard, G. V. (1998) Negative feedback control of the spermatogenic progression by testicular oestrogen synthesis: insights from the shark testis model. APMIS, 106, 252-8.
9. Bilinska, B., Lesniak, M. & Schmalz, B. (1997) Are ovine Leydig cells able to aromatize androgens? Reproduction Fertility and Development, 9, 1-7.
10. Boitani, C., Ritzen, E. M. & Parvinen, M. (1981) Inhibition of rat Sertoli cell aromatase by factor (s) secreted specifically at spermatogenic stages VII and VIII. Molecular and Cellular Endocrinology, 23, 11-22.
11. Boujrad, N., Hochereau de Reviers, M. T. & Carreau, S. (1995) Evidence for a germ cell control of Sertoli cell function in three models of germ cell depletion in adult rat. Biology of Reproduction, 53, 1345-52.
12. Bulun, S. E., Noble, L. S., Takayama, K., Michael, M. D., Agarwal, V., Fisher, C., Zhao, Y., Hinshelwood, M. M., Ito, Y. & Simpson, E. R. (1997) Endocrine disorders associated with inappropriately high aromatase expression. Journal of Steroid Biochemistry and Molecular Biology, 61 (3-6), 133-9.
13. Callard, G. V., Petro, Z. & Ryan, K. J. (1978) Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology, 103, 2283-90.
14. Carani, C., Qin, K., Simoni, M., Faustini-Fustini, M., Serpente, S., Bold, J., Korach, K. S. & Simpson, E. R. (1997) Effect of testosterone and oestradiol in a man with aromatase deficiency. The New England Journal of Medicine, 337, 91-95.
15. Carreau, S. (1986) L'Androgen Binding Protein (ABP) chez le rat, le bélier, le taureau et l'homme: Analyse comparée. In: Binding Proteins of Steroid Hormones, Vol. 149 (eds M. G. Forest & M. Pugeat), pp. 293-303. Colloque INSERM, J. Libbey Eurotext Ltd, Montrouge, France.
16. Carreau, S. (1994) Germ cell-Sertoli cells interactions and Leydig cell function. In: Cell and Molecular Biology of the Testis, Frontiers in Endocrinology 5 (eds M. L. Dufau, A. Fabbri, & A. Isidori), pp. 137-148. Serono Symposia Publications, Rome.
17. Carreau, S. (1996) Paracrine control of human Leydig cell and Sertoli cell functions. Folia Histochemica et Cytobiologica, 3, 111-9.
18. Carreau, S. & Levallet, J. (1998a) L'aromatase testiculaire: du gène à la protéine. Andrologie, 8, 191-8.
19. Carreau, S., Bilinska, B. & Levallet, J. (1998b) Les cellules germinales mâles: une nouvelle source d'estrogènes dans le testicule des mammifères. Annales D'endocrinologie, 59, 79-92.
20. Carreau, S., Papadopoulos, V. & Drosdowsky, M. A. (1988) Stimulation of adult rat Leydig cell aromatase activity by a Sertoli cell factor. Endocrinology, 122, 1103-9.
21. Cazorla, O., Seck, M., Pisselet, C., Perreau, C., Saumande, J., Fontaine, J., de Reviers, M. & Hochereau-de Reviers, M. T. (1998) Anti-Müllerian hormone (AMH) secretion in prepubertal and adult rams. Journal of Reproduction and Fertility, 112 (2), 259-66.
22. Cheng, C. Y. & Boettcher, B. (1979) The effects of steroids on the in vitro migration of washed human spermatozoa in modified tyrode's solution or in fasting human blood serum. Fertility and Sterility, 32, 566-70.
23. Conley, A. J., Corbin, C. J., Hinshelwood, M. M., Liu, Z., Simpson, E. R., Ford, J. J. & Harada, N. (1996) Functional aromatase expression in porcine adrenal gland and testis. Biology of Reproduction, 54, 497-505.
24. Cooke, P. S., Young, P., Hess, R. A. & Cunha, G. R. (1991) Estrogen receptor expression in developing epididymis, efferent ductules, and other male reproductive organs. Endocrinology, 128, 2874-9.
25. Danzo, B. J. (1997) Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environmental Health Perspectives, 105, 294-301.
26. Dorrington, J. H. & Armstrong, D. T. (1975) Follicle stimulating hormone stimulates oestradiol-17β synthesis in cultured Sertoli cells. Proceedings of the National Academy of Sciences (USA), 72, 2677-81.
27. Durkee, T. J., Mueller, M. & Zinaman, M. (1998) Identification of oestrogen receptor protein and messenger ribonucleic acid in human spermatozoa. American Journal of Obstetrics and Gynecology, 178, 1288-95.
28. Eddy, E. M., Washburn, T. F., Bunch, D. O., Goulding, E. H., Gladen, B. C., Lubahn, D. B. & Korach, K. S. (1996) Targeted disruption of the oestrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology, 137, 4796-805.
29. Enmark, E., Pelto-Huikko, M., Grandien, K., Lagercrantz, S., Lagercrantz, J., Fried, G., Nordenskjöld, M. & Gustafsson, J. A. (1997) Human oestrogen receptor β-gene structure, chromosomal localization, and expression pattern. Journal of Clinical Endocrinology and Metabolism, 82, 4258-65.
30. Ergün, S., Ungerfroren, H., Holstein, A. F. & Davidoff, M. S. (1997) Estrogen and progesterone receptors and oestrogen receptor-related antigen (ER-D5) in human epididymis. Molecular Reproduction and Development, 47, 448-55.
31. Fisher, C. R., Graves, K, H., Parlow, A. F. & Simpson, E. R. (1998) Characterization of mice deficient in aromatase (ArKo) because of targeted disruption of the cyp 19 gene. Proceedings of the National Academy of Sciences (USA), 95, 6965-70.
32. Fisher, J. S., Millar, M. R., Majdic, G., Saunders, P. T. K., Fraser, H. M. & Sharpe, R. M. (1997) Immunolocalisation of oestrogen receptor-α within the testis and excurrent ducts of the rat and marmoset monkey from perinatal life to adulthood. Journal of Endocrinology, 153, 485-95.
33. Fisher, J. S., Turner, K. J. M. R., Fraser, H. M., Saunders, P. T. K., Brown, D. & Sharpe, R. M. (1998) Immunoexpression of Aquaporin-1 in the efferent ducts of the rat and marmoset monkey during development, its modulation by oestrogens, and its possible role in fluid resorption. Endocrinology, 139, 3935-45.
34. Foucault, P., Drosdowsky, M. A. & Carreau, S. (1994) Germ cell and Sertoli cell interactions in human testis: evidence for stimulatory and inhibitory effects. Human Reproduction, 9, 2062-8.
35. Free, M. J. & Jaffe, R. A. (1979) Collection of rete testis fluid from rats without previous efferent duct ligation. Biology of Reproduction, 20, 269-78.
36. Gill-Sharina, M. K., Gopalkrishnan, K., Balasinor, N., Parte, P., Jayaraman, S. & Juneja, H. S. (1993) Effects of tamoxifen on the fertility of male rats. Journal of Reproduction and Fertility, 99, 395-402.
37. Goldzieher, J. W. & Roberts, I. S. (1952) Identification of oestrogen in the human testis. Journal of Clinical Endocrinology and Metabolism, 12, 143-50.
38. Gunasegaram, R., Chew, P. C. T., Loganath, A., Peh, K. L. & Ratnam, S. S. (1998) A Δ4-3-keto pathway for testosterone synthesis in human spermatozoa. Archives of Andrology, 40, 49-57.
39. Hansen, L. A., Clulow, J. & Jones, R. C. (1997) Perturbation of fluid resorption in the efferent ducts of the rat by testosterone propionate, 17β-oestradiol 3-benzoate, flutamide and tamoxifen. International Journal of Andrology, 20, 265-273.
40. Harris, C. A., Henttu, P., Parker, M. G. & Sumpter, J. P. (1997) The oestrogenic activity of phthalate esters in vitro. Environmental Health Perspectives, 105, 801-11.
41. Hendry, W. F., Parslow, J. M. & Stedronska, J. (1983) Exploratory scrotomy in 168 azoospermic males. British Journal of Urology, 55, 785-91.
42. Hess, R. A., Bunick, D. & Bahr, J. M. (1995) Sperm, a source of oestrogen. Environmental Health Perspectives, 103, 59-62.
43. Hess, R. A., Bunick, D., Lee, K. H., Bahr, J., Taylor, J. A., Korach, K. S. & Lubahn, D. B. (1997b) A role for oestrogens in the male reproductive tract. Nature, 390, 509-12.
44. Hess, R. A., Gist, D. H., Bunick, D., Lubahn, D. B., Farrell, A., Bahr, J., Cooke, P. S. & Greene, G. L. (1997a) Estrogen receptor (α & β) expression in the excurrent ducts of the adult male rat reproductive tract. Journal of Andrology, 18, 602-11.
45. Hickey, G. J., Krasnow, J. S., Beattie, W. G. & Richards, J. S. (1990) Aromatase cytochrome P450 in rat ovarian granulosa cells before and after luteinization: adenosine 3′,5′-monophosphate-dependent and independent regulation. Cloning and sequencing of rat aromatase cDNA and 5′ genomic DNA. Molecular Endocrinology, 4, 1-12.
46. Hiramatsu, M., Maehara, I., Ozaki, M., Harada, N., Orikasa, S. & Sasano, H. (1997) Aromatase in hyperplasia and carcinoma of the human prostate. Prostate, 31, 118-24.
47. Hyder, S. M., Stancel, G. M. & Loose-Mirchell, D. S. (1991) Presence of an oestradiol response region in the mouse c-fos oncogene. Steroids, 56, 498-504.
48. Inkster, S., Yue, W. & Brodie, A. (1995) Human testicular aromatase: immunocytochemical and biochemical studies. Journal of Clinical Edocrinology and Metabolism, 80, 1941-7.
49. Janulis, L., Bahr, J. M., Hess, R. A. & Bunick, D. (1996) P450 aromatase messenger ribonucleic acid expression in male rat germ cells: detection by reverse transcription-polymerase chain reaction amplification. Journal of Andrology, 17, 651-8.
50. Janulis, L., Bahr, J. M., Hess, R. A., Jansen, S., Osawa, Y. & Bunick, D. (1998) Rat testicular germ cells and epididymal sperm contain active P450 aromatase. Journal of Andrology, 19, 65-71.
51. Janulis, L., Hess, R. A., Bunick, D., Nitta, H., Janssen, S., Osawa, Y. & Bahr, J. M. (1996) Mouse epididymal sperm contains active P450 aromatase which decreases as sperm traverse the epididymis. Journal of Andrology, 17, 111-6.
52. Jayle, M. F., Baulieu, E. E., Scholler, R., Lisboa, B. P. & Savole, J. C. (1958) Exploration dynamique de la fonction endocrinienne du testicule. Revue Française D'Etudes Clinique et Bíologique, 3, 455-61.
53. Jayle, M. F., Scholler, R., Sfikalis, A. & Héron, M. (1962) Excrétion des phénolstéroïdes et des 17 cétostéroïdes après administration de gonadotropines chorioniques à des hommes. Clinica Chemica Acta, 7, 212-20.
54. de Jong, F. H., Hey, A. H. & van der Molen, H. J. (1973) Effects of gonadotrophins on the secretion of oestradiol-17β and testosterone by the rat testis. Journal of Endocrinology, 57, 277-84.
55. de Jong, F. H., Hey, A. H. & van der Molen, H. J. (1974) Oestradiol-17β and testosterone in rat testis tissue: effect of gonadotrophins, localization and production in vitro. Journal of Endocrinology, 60, 409-19.
56. Kelch, R. P., Jenner, M. A., Weinstein, R., Kaplan, S. L. & Grumbach, M. M. (1972) Estradiol and testosterone secretion by human, simian and canine testes in males with hypogonadism and in male pseudohermaphrodites with the feminizing testes syndrome. Journal of Clinical Investigation, 51, 824-30.
57. Kuiper, G. G. J. M., Carlsson, B., Grandien, K., Enmark, E., Häggbland, J., Nilsson, S. & Gustafsson, J. A. (1997) Comparison of the ligand binding specificity and transcript tissue distribution of oestrogen receptors α and β. Endocrinology, 138, 863-70.
58. Kuiper, G. G. J. M., Enmark, E., Pelto-Huikko, M., Nilsson, S. & Gustafsson, J. A. (1996) Cloning of a novel oestrogen receptor expressed in rat prostate and ovary. Proceedings of the National Academy of Sciences (USA), 93, 5925-30.
59. Kumari, G. L., Allag, I. S., Das, R. P. & Datta, J. K. (1980) Regional differences in steroidogenesis and hormone levels in the epididymis and vas deferons of adult rats. International Journal of Andrology, 3, 267-81.
60. Kurosumi, M., Ishimura, K., Fujita, H. & Osawa, Y. (1985) Immunocytochemical localization of aromatase in rat testis. Histochemistry, 83, 401-4.
61. Kwon, S., Hess, R. A., Bunick, D., Nitta, H., Janulis, L., Osawa, Y. & Bahr, J. M. (1995) Rooster testicular germ cells and epididymal sperm contain P450 aromatase. Biology of Reproduction, 53, 1259-64.
62. Le Magueresse, B. & Jegou, B. (1986) Possible involvement of germ cells in the regulation of ooestradiol-17β and ABP secretion by immature rat Sertoli cells (in vitro studies). Biochemical and Biophysical Research Communications, 141, 861-9.
63. Leach, R. B., Maddock, W. O., Tokuyama, I., Paulsen, C. A. & Nelson, W. O. (1956) Clinical studies of testicular hormone production. Recent Progress in Hormone Research, 12, 377-97.
64. Lejeune, H., Habert, R. & Saez, J. M. (1998a) Origin, proliferation and differentiation of Leydig cells. Journal of Molecular Endocrinology, 20, 1-25.
65. Lejeune, H., Jegou, B., Carreau, S. & Saez, J. M. (1996) Régulation paracrine et autocrine des fonctions testiculaires. In: Endocrinologie Masculine, Vol. 7 (eds J. Belaish, M. A. Drosdowsky, & A. Vermeulen), pp. 77-103. Doin-Paris, Paris.
66. Lejeune, H., Sanchez, P. & Saez, J. M. (1998b) Enhancement of long-term testosterone secretion and steroidogenic enzyme expression in human Leydig cells by coculture with human Sertoli cell-enriched preparations. International Journal of Andrology, 21, 129-40.
67. Lephart, E. D., Peterson, K. G., Noble, J. F., George, F. W. & McPhaul, M. J. (1990) The structure of cDNA clones encoding the aromatase P-450 isolated from a rat Leydig cell tumor line demonstrates differential processing of aromatase mRNA in rat ovary and neoplastic cell line. Molecular and Cellular Endocrinology, 70, 31-40.
68. Levallet, J. & Carreau, S. (1997) Aromatase gene expression in rat testicular cells in vitro Comptes Rendus Académie Des Sciences (Paris), 320, 123-9.
69. Levallet, J., Bilinska, B., Mittre, H., Genissel, C., Fresnel, J. & Carreau, S. (1998a) Expression and immunolocalization of functional cytochrome P450 aromatase in mature rat testicular cells. Biology of Reproduction, 58, 919-26.
70. Levallet, J., Mittre, H., Delarue, B. & Carreau, S. (1998b) Alternative splicing in the coding region of the cytochrome P450 aromatase gene in male rat germ cells. Journal of Molecular Endocrinology, 20, 305-12.
71. Li, H., Papadopoulos, V., Vidic, B., Dym, M. & Culty, M. (1997) Regulation of rat testis gonocyte proliferation by platelet-derived growth factor and oestradiol: identification of signalling mechanisms involved. Endocrinology, 138, 1289-98.
72. Lubahn, D. B., Moyer, J. S., Golding, T. S., Couse, J. F., Korach, K. S. & Smithies, O. (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse oestrogen receptor gene. Proceedings of the National Academy of Sciences (USA), 90, 11162-6.
73. Luconi, M., Bonaccorsi, L., Maggi, M., Pecchioli, P., Krausz, C., Forti, G. & Baldi, E. (1998) Identification and characterization of functional nongenomic progesterone receptors on human sperm membrane. Journal of Clinical Endocrinology and Metabolism, 83, 877-85.
74. Lyng, F. M., Jones, G. R. & Rommerts, F. F. G. (1998) A new membrane receptor for androgens? Proceedings of the European Testis Workshop (Capri, Italy), E15.
75. MacCalman, C. D., Getsios, S., Farookhi, R. & Blaschuk, O. W. (1997) Estrogens potentiate the stimulatory effects of follicle-stimulating hormone on N-cadherin messenger ribonucleic acid levels in cultured mouse Sertoli cells. Endocrinology, 138, 41-8.
76. Mahendroo, M. S., Means, G. D., Mendelson, C. R. & Simpson, E. R. (1991) Tissue-specific expression of human P-450AROM. The promoter responsible for expression in adipose tissue is different from that utilized in placenta. Journal of Biological Chemistry, 266, 11276-81.
77. Majdic, G., Sharpe, R. M. & Saunders, P. T. K. (1997) Maternal oestrogen/xenoestrogen exposure alters expression of steroidogenic factor-1 (SF-1/Ad4 BP) in the fetal rat testis. Molecular and Cellular Endocrinology, 127, 91-8.
78. Marie, E., Vendrely, E., de Reviers, M. & Carreau, S. (1995) Stéroides plasmatiques et intratesticulaires: existe-t-il des correlations avee la spermatogenèse chez l'homme fertile et infécond. Annales D'endocrinologie, 56 (4), 337.
79. Martel, C., Melner, M. H., Gagné, D., Simard, J. & Labrie, F. (1994) Widespread tissue distribution of steroid sulfatase, 3β-hydroxysteroid dehydrogenase/isomerase (3β-HSD), 17β-HSD, 5α-reductase and aromatase activities in the rhesus monkey. Molecular and Cellular Endocrinology, 104, 103-1.
80. Meistrich, M. L., Hughes, T. J. & Bruce, W. R. (1975) Alteration of epididymal sperm transport and maturation in mice by oestrogen and testosterone. Nature, 258, 145-7.
81. Morishima, A., Grumbach, M. M., Simpson, E. R., Fisher, C. & Qin, K. (1995) Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of oestrogens. Journal of Clinical Endocrinology and Metabolism, 80, 3689-98.
82. Morrish, D. W., Venner, P. M., Siy, O., Barron, G., Bhardwaj, D. & Outhet, D. (1990) Mechanisms of endocrine dysfunction in patients with testicular cancer. Journal of the National Cancer Institute, 82, 412-8.
83. Morse, W. I., Clark, A. F., MacLeod, S. C., Ernst, W. A. & Grossee, C. L. (1962) Urine oestrogen responses to human chorionic gonadotropin in gonad of old and hypogonadal men. Journal of Clinical Endocrinology and Metabolism, 22, 678-5.
84. Mosselman, S., Polman, J. & Dijkema, R. (1996) ERβ: identification and characterization of a novel oestrogen receptor β. FEBS Letters, 392, 49-53.
85. Nakazumi, H., Sasano, H., Maehara, I., Ozaki, M., Tezuka, F. & Orikasa, S. (1996) Estrogen metabolism and impaired spermatogenesis in germ cell tumors of the testis. Journal of Clinical Endocrinology and Metabolism, 81, 1289-95.
86. Nakhala, A. M., Mather, J. P., Janne, O. A. & Bardin, C. W. (1984) Estrogen and androgen receptors in Sertoli, Leydig, myoid and epithelial cells: effects of time in culture and cell density. Endocrinology, 115, 121-8.
87. Nelson, D. R., Koymans, L., Kamataki, T., Stegeman, J. J., Feyereisen, R., waxman, D. J., Waterman, M. R., Gotoh, O., Coon, M. J., Estabrook, R. W., Gunsalus, I. C. & Nebert, D. W. (1996) P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics, 6, 1-42.
88. Nitta, H., Bunick, D., Hess, R. A., Janulis, L., Newton, S. C., Millette, C. E., Osawa, Y., Shizuta, Y., Toda, K. & Bahr, J. M. (1993) Germ cells of the mouse testis express P450 aromatase. Endocrinology, 132, 1396-401.
89. O'Marcaigh, A. S., Ledger, G. A., Roche, P. C., Parisi, J. E. & Zimmerman, D. (1995) Aromatase expression in human germinomas with possible biological effects. Journal of Clinical Endocrinology and Metabolism, 80, 3763-66.
90. Oh, R. & Tamaoki, B. (1970) Steroidogenesis in equine testis. Acta Endocrinologica (Copenh), 64, 1-16.
91. Papadopoulos, V., Carreau, S., Szerman-Joly, E., Drosdowsky, M. A., Dehennin, L. & Scholler, R. (1986) Rat testis 17β-oestradiol: identification by gas chromatography-mass spectrometry and age related cellular distribution. Journal of Steroid Biochemistry, 24, 1211-6.
92. Papadopoulos, V., Drosdowsky, M. A. & Carreau, S. (1987) On the existence of two Leydig cell populations in aged human testis. Annals of the New York Academy of Sciences, 513, 356-9.
93. Papadopoulos, V., Jia, M. C., Culty, M., Hall, P. F. & Dym, M. (1993) Rat Sertoli cell aromatase cytochrome P450: regulation by cell culture conditions and relationship to the state of cell differentiation. In Vitro Cellular and Development Biology 29A, 943-9.
94. Papadopoulos, V., Kamtchouing, P., Drosdowsky, M. A., Hochereau de Reviers, M. T. & Carreau, S. (1987) Adult rat Sertoli cells secrete a factor or factors which modulate Leydig cell function. Journal of Endocrinology, 114, 459-67.
95. Payne, A. H., Kelch, R. P., Musich, S. S. & Halpern, M. E. (1976) Intratesticular site of aromatization in the human. Journal of Clinical Endocrinology and Metabolism, 42, 1081-7.
96. Phamanthu, N. T., Bonnamy, P. J., Bouakka, M. & Bpequet, J. (1995) Inhibition of proteoglycan synthesis induces an increase in FSH-stimulated oestradiol production by immature rat Sertoli cells. Molecular And Cellular Endocrinology, 109, 37-45.
97. Pomerantz, D. K. (1979) Effects of in vivo gonadotropin treatment on oestrogen levels in the testis of the immature rat. Biology of Reproduction, 21, 1247-55.
98. Pomerantz, D. K. (1980) Developmental changes in the ability of follicle stimulating hormone to stimulate oestrogen synthesis in vivo by the testis of the rat. Biology of Reproduction, 23, 948-54.
99. Pudney, J., Canick, J. A., Clifford, N. M., Knopp, J. B. & Callard, G. V. (1985) Location of enzymes of androgen and oestrogen biosynthesis in the testis of the ground squirrel. Biology of Reproduction, 33, 971-80.
100. Raeside, J. J. (1960) The isolation of estrone sulphate and oestradiol-17β sulphate from stallion testis. Canadian Journal of Biochemistry, 47, 811-5.
101. Raeside, J. J. & Renaud, R. L. (1983) Estrogen and androgen production by purified Leydig cells of mature boars. Biology of Reproduction, 28, 727-33.
102. Revelli, A., Massobrio, M. & Tesarik, J. (1998) Nongenomic actions of steroid hormones in reproductive tissues. Endocrine Reviews, 19, 3-17.
103. Rommerts, F. F. G., de Jong, F. H., Brinkmann, A. O. & van der Molen, H. J. (1982) Development and cellular localization of rat testicular aromatase activity. Journal of Reproduction and Fertility, 65, 281-8.
104. Rosner, W., Hryb, D. J., Khan, M. S., Nakhala, A. M. & Romas, N. A. (1998) Androgens, oestrogens, and second messengers. Steroids, 63, 278-81.
105. Saez, J. M. (1994) Leydig cells: endocrine, paracrine and autocrine regulation. Endocrine Reviews, 15, 574-626.
106. Saez. J. M., Sanchez, P., Berthelon, M. C. & Avallet, O. (1989) Regulation of pig Leydig cell aromatase activity by gonadotropins and Sertoli cells. Biology of Reproduction, 41, 813-20.
107. Sanger, F., Nicklen, S. & Coulson, A. R. (1977) DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences (USA), 74, 5463-7.
108. Saunders, P. T. K., Fisher, J. S., Sharpe, R. M. & Millar, M. R. (1998) Expression of oestrogen receptor beta (ERβ) occurs in multiple cell types, including some germ cells, in the rat testis. Journal of Endocrinology, 156, R13-R17.
109. 3H] testosterone in oestrogen receptor containing cells of the epididymis. Journal of Steroid Biochemistry, 32, 299-302.
110. Sharpe, R. M. (1993) Experimental evidence for Sertoli-germ cell and Sertoli-Leydig cell interactions. In: The Sertoli Cell (eds L. D. Russell & M. D. Griswold), pp. 391-438. Cache River Press, Clearwater FL.
111. Sharpe, R. M. (1998) The roles of oestrogen in the male. Trends in Endocrinology and Metabolism, 9, 371-7.
112. Sharpe, R. M., Atanassova, N., McKinnel, C., Parte, P., Turner, K. J., Fisher, J. S., Kerr, J. B., Gromme, N. P., Macpherson, S., Millar, M. R. & Saunders, P. T. K. (1998) Abnormalities in functional development of the Sertoli cells in rats treated neonatally with diethylstilbestrol: a possible role for oestrogen in Sertoli cell development. Biology of Reproduction, 59, 1084-94.
113. Sharpe, R. M. & Skakkebaek, N. E. (1993) Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet, 341, 1392-5.
114. Shetty, G., Krishnamurthy, H., Krishnamurthy, H. N., Bhatnagar, S. & Moudgal, R. N. (1997) Effect of oestrogen deprivation on the male reproductive physiology of male and female primates. Journal of Steroid Biochemistry and Molecular Biology, 61 (3-6), 157-66.
115. Shozu, M., Zhao, Y., Bulun, S. E. & Simpson, E. R. (1998) Multiple splicing events involved in regulation of human aromatase expression by a novel promoter, I.6. Endocrinology, 139, 1610-7.
116. Shughure, P. J., Lane, M. V., Scrimo, P. J. & Merchenthaler, I. (1998) Comparative distribution of oestrogen receptor-alpha (ER-alpha) and beta (ER-beta) in the rat pituitary, gonad and reproductive tract. Steroids, 63 (10), 498-504.
117. Simpson, E. R., Mahendroo, M. S., Means, G. D., Kilgore, M. W., Hinshelwood, M. M., Graham-Lorence, S., Amarneh, B., It, Y., Fisher, C. R., Dodson, M. M., Mendelson, C. R. & Bulun, S. E. (1994) Aromatase cytochrome P450, the enzyme responsible for oestrogen biosynthesis. Endocrine Reviews, 15, 342-55.
118. Simpson, E. R., Michael, M. D., Agarwal, V. R., Hinshelwood, M. M., Bulun, S. E. & Zhao, Y. (1997a) Expression of the CYP 19 (aromatase) gene: an unusual case of alternative promoter usage. FASEB Journal, 11, 29-36.
119. Simpson, E. R., Zhao, Y., Agarwal, V. R., Michael, M. D., Bulun, S. E., Hinshelwood, M. M., Graham-Lorence, S., Sun, T., Fisher, C. R., Qin, K. & Mendelson, C. R. (1997b) Aromatase expression in health and disease. Recent Progress in Hormone Research, 52, 185-212.
120. Smith, C. L. (1998) Cross-talk between peptide growth factor and oestrogen receptor signaling pathways. Biology of Reproduction, 58, 627-32.
121. Smith, E. P., Boyd, J., Frank, G. R., Takahashi, H., Cohen, R. M., Specker, B., Williams, T. C., Lubahn, D. B. & Korach, K. S. (1994) Estrogen resistance caused by amutation in the oestrogen-receptor gene in a man. The New England Journal of Medicine, 331, 1056-61.
122. Sohoni, P. & Sumpter, J. P. (1998) Several environmental oestrogens are also anti-androgens. Journal of Endocrinology, 158, 327-39.
123. Song, W. C., Qian, Y., Sun, X. & Negishi, M. (1997) Cellular localization and regulation of expression of testicular oestrogen sulfotransferase. Endocrinology, 138, 5006-12.
124. Tea, N. T., Castanier, M., Grenier, J. & Scholler, R. (1972) Taux des oestrogènes dans le plasma séminal. Annales D'Endocrinologie, 33, 297-8.
125. Toppari, J., Larsen, J. C., Christiansen, P., Giwercman, A., Grandjean, P., Guillette, L. J., Jegou, B., Jensen, T. K., Jouannet, P., Keiding, N., Leffers, H., McLachlan, J. A., Meyer, O., Müller, J., Rajpert-de Meyts, E., Scheike, T., Sharpe, R. M., Sumpter, J. S. & Skakkebaek, N. E. (1996) Male reproductive health and environmental xenooestrogens. Environmental Health Perspectives, Suppl. 104, 741-803.
126. Tsai-Morris, C. H., Aquilano, D. R. & Dufau, M. L. (1985) Cellular localization of rat testicular aromatase activity during development. Endocrinology, 116, 38-46.
127. Tsubota, T., Howell-Skalla, L., Nitta, H., Osawa, Y., Mason, J. I., Meiers, P. G., Nelson, R. A. & Bahr, J. M. (1997) Seasonal changes in spermatogenesis and testicular steroidogenesis in the male black bear Ursus Americanus. Journal of Reproduction and Fertility, 109, 21-7.
128. Tsubota, T., Nitta, H., Osawa, Y., Ian Mason, J., Kita, I., Tiba, T. & Bahr, J. M. (1993) Immunolocalization of steroidogenic enzymes, P450scc, 3β-HSD, P450c17, and P450arom in the Hokkaido brown bear (Ursus arctos yesoensis) testis. General and Comparative Endocrinology, 92, 439-4.
129. Tsutsumi, I., Fugimori, K., Nakamura, R. M., Mather, J. P., Ono, T. & diZerega, G. S. (1987) Disruption of seminiferous epithelial function in the rat by ovarian protein. Biology of Reproduction, 36, 451-61.
130. Verhoeven, G. & Cailleau, J. (1988) Testicular peritubular cells secrete a protein under androgen control that inhibits induction of aromatase activity in sertoli cells. Endocrinology, 123, 2100-10.
131. Walzack, R., Rahman, N. A., Oszukowska, S. & Kula, K. (1997) Administration of oestradiol facilitates a stimulatory effect of FSH on first spermatogenesis and testicular growth. VIth International Congress of Andrology, (Salzburg, Austria), A260.
132. Yeh, S., Miyamoto, H., Shima, H. & Chang, C. (1998) From oestrogen to androgen receptor: a new pathway for sex hormones in prostate. Proceedings of the National Academy of Sciences (USA), 95, 5527-32.
133. Young, J., Bulun, S. E., Agarwal, V., Couzinet, B., Mendelson, C. R., Simpson, E. R. & Schaison, G. (1996) Aromatase expression in a feminizing adrenocortical tumor. Journal of Clinical Endocrinology and Metabolism, 81, 3173-6.
134. Young, M. & McPhaul, M. J. (1997) Definition of the elements required for the activity of the rat aromatase promoter in steroidogenic cell lines. Journal of Steroid Biochemistry and Molecular Biology, 61, 341-8.
135. Zondek, B. (1934) Mass excretion of oestrogenic hormone in the urine of the stallion. Nature, 193, 209-10.