Role of estrogens in spermatogenesis

Frontiers in Bioscience - Elite

Volumn 4 E, Issue 1, 2012, Pages 1-11

  Carreau, Serge ^a   Bouraima Lelong, Helene ^a   Delalande, Christelle ^a  

^a UNIVERSITÉ DE CAEN   (France)

Author keywords

Aromatase; Estrogen Receptors; Estrogens; Mammals; Review; Spermatogenesis

Indexed keywords

AROMATASE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA;

APOPTOSIS; ARTICLE; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; GERM CELL; MAMMAL; NONHUMAN; REPRODUCTION; SPERMATOGENESIS; TESTIS;

MAMMALIA; RODENTIA; VERTEBRATA;

EID: 84883770921     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: 10.2741/e356     Document Type: Article

References (120)

1. J.M. Saez: Leydig cells : endocrine, paracrine and autocrine regulation. Endocr Rev 15, 574-626 (1994)
2. S. Carreau, C.Genissel, B.Bilinska and J. Levallet: The oestrogen sources in the testis and the reproductive tract of the male. Inter J Androl 22, 211-223 (1999)
3. S. Carreau and R. Hess: Oestrogens and spermatogenesis. Phil Trans R Soc B 365, 1517-1535 (2010)
4. B. Zondek: Mass excretion of oestrogenic hormone in the urine of the stallion. Nature (London), 193, 209-210 (1934)
5. M.F. Jayle, R. Scholler, A. Sfikalis and M. Héron : Excrétion des phénolstéroïdes et des 17 cétostéroïdes après administration de gonadotrophines chorioniques à des hommes. Clin Chem Acta 7, 212-20 (1962)
6. W.F. Hendry, J.M. Parslow and J. Stedronska: Exploratory scrotomy in 168 azoospermic males. Brit. J Urol 55, 785-791 (1983)
7. R.A. Hess: Estrogen in the adult male reproductive tract: A review. Reprod Biol Endocrinol 9, (1): 52 (2003)
8. L. O'Donnell, K.M. Robertson, M.E. Jones and E.R. Simpson: Estrogen and spermatogenesis. Endocr Rev 22, 289-318 (2001)
9. S. Carreau, S. Bourguiba, C. Delalande, D. Silandre, L. Said, I. Galeraud-Denis and S. Lambard: Estrogens and Male Reproduction. Current Med Chem Immunol Endocrinol Metab Agents 8, 59-65 (2008)
10. D.B. Lubahn, J.S. Moyer, T.S.Golding, J.F. Couse, K.S. Korach and O. Smithies:Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90, 11162-11166 (1993)
11. J.F. Couse and K. Korach: Estrogen receptor null mice : what have we learned and where will they lead us? Endocr Rev 20, 358-417 (1999)
12. C.R. Fisher, K.H. Graves, A.F.Parlow and E.R. Simpson: Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci USA 95, 6965-6970 (1998)
13. M.E.E. Jones, W.C. Boon, K. McInnes, L.Maffei, C. Carani and E.R. Simpson: Recognizing rare disorders: aromatase deficiency. Nature Clin Pract Endocrinol & Metab 3, 414-421 (2007)
14. P.T.K. Saunders, R.M. Sharpe, K. Williams, S. Macpherson, H.Urquart, D.S. Irvine, and M.R. Millar: Differential expression of oestrogen receptor and proteins in the testes and male reproductive system of human and non-human primates. Molec Human Reprod 7, 227-336 (2001)
15. J.E. Sierens, S.F. Sneddon, F. Collins F, M. R. Millar and P. T. K. Saunders: Estrogens in Testis Biology. Ann NY Acad Sci 1061, 65-76 (2005)
16. R.A. Hess and K. Carnes: The role of estrogen in the testis and the male reproductive tract : A review. Anim Reprod 1, 5-30 (2004)
17. E.P. Smith , J. Boyd, G.R. Frank, H; Takahashi, R.M.Cohen, B. Specker, T.C.Williams, D.B.Lubahn and K.S. Korach: Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man.N Engl J Med 331, 1056-1061(1994)
18. V. Rochira, A.R.M. Granata, B. Madeo, L. Zirilli, G. Rossi and C. Carani: Estrogens in males : what we have learned in last 10 years? Asian J Androl 7, 3-20 (2005)
19. S. Sebastian and S.E. Bulun : A highly complex organization of the regulatory region of the human CYP19 (aromatase) gene revealed by the Human genome project. J Clin Endocrinol Metab 86, 4600-4602 (2001).
20. M. Demura, S. Reierstad, J.E. Innes and S.E. Bulun. Novel promoter I.8 and promoter usage in the CYP19 (Aromatase) gene. Reprod Sci 15, 1044-1053. (2008)
21. E.R. Simpson,Y. Zhao, V.R.Agarwal, M.D. Michael,S.E. Bulun, M.M.Hinshelwood, S.Graham-Lorence, T. Sun, C.R. Fisher, K.Qin, and C.R. Mendelson: Aromatase expression in health and disease. Recent Progress in Hormone Research 52,185-212 (1997)
22. J.D. Chow, E.R. Simpson and W.C. Boon: Alternative 5'- untranslated first exons of the mouse Cyp19A1 (aromatase) gene. J. Steroid Biochem. Mol. Biol. 115, 115-125 (2009).
23. H. Zhao, J. Innes, D.C. Brooks, S. Reierstad, M.B. Yilmaz, Z. Lin and S.E. Bulun: A novel promoter controls Cyp19a1 gene expression in mouse adipose tissue. Reprod. Biol. Endocrinol. 24, 7:37. (2009).
24. D. Silandre, C. Delalande, P. Durand and S. Carreau: Three promoters PII , PI.f and PI.tr direct the expression of aromatase (cyp19) gene in male rat grem cells. J Molec Endocrinol 39, 169-181 (2007)
25. M. Lanzino, S. Catalano, C. Genissel, S. Ando, S. Carreau, K. Hamra and J. McPhaul : Aromatase messenger RNA is derived from the proximal promoter of the aromatase gene in Leydig, Sertoli, and germ cells of the rat testis. Biol Reprod 64,1439-1443 (2001)
26. N.Yamada-Mouri, S. Hirata and J. Kato: Existence and expression of the untranslated first exon of aromatase mRNA in the rat brain. J Steroid Biochem Molec Biol 58,163-166 (1996)
27. J. Levallet, B. Delarue, H. Mittre and S. Carreau: Alternative splicing events in the coding region of cytochrome P450 aromatase in adult male rat germ cells. J Mol Endocrinol 20, 305-312 (1998)
28. S. Carreau: Leydig cell aromatase : from gene to physiological role. In : The Leydig Cell in Health and Disease. Eds : A.H. Payne & M.P. Hardy. Human Press Inc, Totowa, NJ, USA, 189-195 (2007)
29. E.R. Simpson, M.S. Mahendroo, G.D. Means, M.W. Kilgore, M.M. Hinshelwood, S. Graham-Lorence, B. Amarneh, Y. Ito, C.R. Fisher, M.D. Michael, C.R. Mendelson and S.E. Bulun Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15, 342-355 (1994)
30. V. Papadopoulos, S. Carreau, E. Szerman-Joly, M.A. Drosdowsky, L. Dehennin and R. Scholler: Rat testis 17estradiol : identification by gas-chromatography-mass spectrometry and age-related cellular distribution. J Steroid Biochem 24,1211-1216 (1986)
31. C.Boitani, E.M.Ritzen and M. Parvinen: Inhibition of rat Sertoli cell aromatase by factor(s) secreted specifically at spermatogenic stages VII and VIII. Mol Cell Endocrinol 23,11-22 (1981)
32. H. Bouraïma-Lelong, M Vanneste, C. Delalande, L. Zanatta, S. Woczynski and S. Carreau: Aromatase gene expression in immature rat Sertoli cells: age-related changes in the FSH signalling pathway. Reprod Fert Dev 22, 508-515 (2010)
33. H. Nitta, D. Bunick, R.A. Hess, L. Janulis, S.C. Newton, C.F. Milette, Y. Osawa, Y. Shizuta, K. Toda and J.M. Bahr: Germ cells of the mouse testis express P450 aromatase. Endocrinology 132,1396-401(1993).
34. S. Carreau, S. Lambard, C. Delalande, I. Galeraud- Denis, B. Bilinska and S. Bourguiba: Aromatase expression and role of estrogens in male gonad : A review. Reprod Biol Endocrinol 1, 35 (2003)
35. S. Carreau, C. Delalande, D. Silandre, S. Bourguiba and S. Lambard: Aromatase and estrogen receptors in male reproduction . Mol Cell Endocrinol 246, 65-68 (2006)
36. S. Carreau, C. Delalande and I. Galeraud-Denis: Mammalian sperm quality and aromatase expression. Microsc Res Tech 72, 552-557 (2009)
37. S. Carreau, V. Papadopoulos and M.A. Drosdowsky : Stimulation of adult rat Leydig cell aromatase activity by a Sertoli cell factor. Endocrinology 122,1103-1109 (1988)
38. J. Levallet, B. Bilinska, H. Mittre, C. Genissel, J. Fresnel and S. Carreau: Expression and immunolocalization of functional cytochrome P450 aromatase in mature rat testicular cells. Biol Reprod 58, 919-926 (1998)
39. J. Levallet and S. Carreau: Aromatase gene expression in rat testicular cells. C R Acad Sc Paris 320,123-129 (1997).
40. H. Nakazumi, H. Sasano, I. Maehara, M.Ozaki, F.Tezukaa and S.Orikasa: Estrogen metabolism and impaired spermatogenesis in germ cell tumors of the testis. J Clin Endocrinol Metab 81, 1289-1295 (1996)
41. C. Roger, S. Lambard, A. Bouskine, B. Mograbi, D. Chevallier, M. Nebout, G. Pointis, S. Carreau and P. Fenichel: Estrogen-induced growth inhibition of human seminoma cells expressing estrogen receptor beta and aromatase. J Mol Endocrinol 35, 191-199 (2005).
42. S. Lambard, I. Galeraud-Denis, H. Bouraima , S. Bourguiba, A. Chocat, S. Carreau: Expression of aromatase in human ejaculated spermatozoa: A putative marker of motility. Mol. Hum. Reprod. 9, 117-24 (2003)
43. L. Janulis, J.M.Bahr, R.A. Hess, S. Janssen, Y. Osawa and D. Bunick: Rat testicular germ cells and epidydimal sperm contain active P450 aromatase.J Androl 19, 65-71 (1998)
44. B. Wiszniewska: Primary culture of rat epididymal epithelial cells as a source of estrogen. Andrologia 34, 1-8 (2002)
45. B. Bilinska, B. Schmalz-Fraczek, M. Kotula and S. Carreau: Photoperiod-dependent capability of androgen aromatization and the role of estrogens in bank vole testis visualized by means of immunohistichemistry. Mol Cell Endocrinol 178, 189-198 (2001)
46. M. Kotula-Balak, M. Slomczynska, B. Fraczek, S. Bourguiba, Z. Tabarowski, S. Carreau and B. Bilinska: Complementary approaches demonstrate that cellular aromatization in the bank vole testis is related to photoperiod. Eur J Histochem 47, 55-62 (2003)
47. J.J. Raeside and R.L. Renaud : Estrogen and andogen production by purified Leydig cells from mature boars. Biol Reprod 28,727-733 (1983)
48. H. Mutembei, S. Pesch, G. Schuler and B. Hoffmann: Expression of oestrogen receptors alpha and beta and of aromatase in the testis of immature and mature Boars. Reprod Domest Anim 40, 228-236 (2005)
49. K.M. Eisenhauer, P.M. McCue, D.K.Nayden, Y. Osawa and J.F. Roser: Localization of aromatase in equine Leydig cells. Domest Anim Endocrino 11, 291-298 (1994)
50. H. Sipahutar, P. Sourdaine, S. Moslemi, B. Plainfossé and G.E. Seralini : Immunolocalization of aromatase in stallion Leydig cells and seminiferous tubules. J Histochem Cytochem 51, 311-318 (2003)
51. A. Hejmej, M. Kotula-Balak, J. Sadowska and B. Bilinska: Expression of connexin 43 protein in testes, epididymides and prostates of stallions. Equine Vet J 39, 122-127 (2007).
52. T. Tsubota, L. Howell-Skalla, H. Nitta, Y. Osawa, J.I. Mason, P.G. Meiers, R.A. Nelson, J.M. Bahr: Seasonal changes in spermatogenesis and testicular steroidogenesis in the male black bear Ursus americanus. J. Reprod. Fertil. 109, 21-27 (1997)
53. I. Kopera, M. Szczepanowicz, Z. Gizejewski, J. Sadowska and B. Bilinska: Immunoexpression of aromatase in immature and adult males of the European bison (Bison bonasus, Linnaeus 1758). Reprod Domest Anim doi: 10.1111/j.1439-0531. 2008.01280.x
54. J. Schon and S.Blottner: Estrogens are involved in seasonal regulation of spermatogenesis and sperm maturation in roe deer (Capreolus capreolus). Gen Comp Endocrinol 159, 257-263 (2008).
55. A.C. Pereyra-Martinez, C.E. Roselli, H.L. Stadelman, and J.A. Resko: Cytochrome P450 aromatase in testis and epididymis of male rhesus monkeys. Endocrine 16, 15-19 (2001)
56. A.H. Payne, R.P. Kelch, S.S. Musich and M.E. Halpern: Intratesticular site of aromatization in the human. J Clin Endocrinol Metab 42,1081-1087 (1976)
57. P. Foucault, S. Carreau, W. Kuczynski, J.M.Guillaumin, P. Bardos and M.A. Drosdowsky: The human Sertoli cells in vitro: lactate, estradiol-17ß and transferrin productions. J Androl 13, 361-367 (1992)
58. S. Lambard, I. Galeraud-Denis, P.T. Saunders and S. Carreau: Human immature germ cells and ejaculated spermatozoa contain aromatase and oestrogen receptors. J. Mol. Endocrinol. 32, 279-289 (2004).
59. S. Aquila, D. Sisci, M. Gentile, E. Middea, L. Siciliano and S. Ando: Human ejaculated spermatozoa contain active P450 aromatase. J Clin Endocrinol Metab 87, 3385-3390 (2002)
60. S. Carreau, S. Wolczynski and I. Galeraud-Denis : Aromatase, oestrogens and human male reproduction. Phil Trans R Soc B 365, 1571-1579 (2010)
61. F. Carpino, F. Romeo and F.V. Rago: Aromatase immunolocalization in human ductuli efferentes and proximal ductus epididymis. J Anat 204, 217-220 (2004)
62. J.S. Fisher, M.R. Millar, G. Majdic, P.T. Saunders, H.M. Fraser and R.M. Sharpe: Immunolocalisation of estrogen receptor-alpha within the testis and excurrent ducts of the rat and marmoset monkey from perinatal life to adulthood. J Endocrinol 153, 485-495 (1997)
63. P.T.K. Saunders, J.S. Fisher, R.M. Sharpe and M.R. Millar: Expression of oestrogen receptor beta (ER?) occurs in multiple cell types, including some germ cells, in the rat testis. J Endocrinol 156, R13-R17 (1998)
64. G. Pelletier, C. Labrie and F. Labrie: Localization of oestrogen receptor alpha, oestrogen receptor beta and androgen receptors in the rat reproductive organs. J Endocrinol 165, 359-370 (2000)
65. A.M. van Pelt, D.G. de Rooij, B. van der Burg, P.T. van der Saag, J.A. Gustafsson, and G.G. Kuiper: Ontogeny of estrogen receptor-beta expression in rat testis. Endocrinology 140, 478-483 (1999).
66. C.N. Mowa and T. Iwagana. Expression of estrogen receptor-alpha and -beta mRNAs in the male reproductive system of the rat as revealed by in situ hybridization. J Mol Endocrinol 26, 165-174 (2001)
67. P.J. Shugrue, M.V. Lane, P.J. Scrimo and I. Merchenthaler: Comparative distribution of estrogen receptor-alpha (ER-alpha) and beta (ER-beta) mRNA in the rat pituitary, gonad, and reproductive tract. Steroids 63, 498-504 (1998)
68. P.T.K. Saunders, S.M. Maguire, J. Gaughan, M.R. Millar: Expression of estrogen receptor beta (ER?) in multiple rat tissues visualized by immunohistochemistry. J Endocrinol 154,R13-R16 (1997)
69. K E. Friend, E.M. Resnick, L.M. Ang and M.A. Shupnik: Specific modulation of estrogen receptor mRNA isoforms in rat pituitary throughout the estrous cycle and in response to steroid hormones. Mol Cell Endocrinol 131, 147-155 (1997)
70. A.Chimento, R. Sirianni, C. Delalande, D. Silandre, C. Bois, S. Ando, M. Maggiolini, S. Carreau and V. Pezzi : 17?-estradiol activates rapid signaling pathways involved in rat pachytene spermatocytes apoptosis through GPR30 and ER?. Mol Cell Endocrinol 320, 136-144 (2010)
71. T.F. Lucas, E.R. Siu, C.A. Esteves, H.P. Monteiro, C.A. Oliveira, C.S. Porto, M.F. Lazari: 17 beta-estradiol induces the translocation of the estrogen receptors ERS1 and ERS2 to the cell membrane, MAPK3/1 phosphorylation and proliferation of cultured immature rat Sertoli cells. Biol Reprod 78,101-114 (2008)
72. O.M. Tirado, D.M. Selva, N. Toran, C.A. Suarez- Quian, M. Jansen, D.P. McDonnell, J. Reventos and F. Munell: Increased expression of estrogen receptor beta in pachytene spermatocytes after short-term methoxyacetic acid administration. J Androl 25, 84-94 2004
73. V. Pentikaïnen, K. Erkkilä, L. Suomalainen, M. Otala, M.O. Pentikaïnen, M. Parvinen, and L. Dunkel: Estradiol acts as a germ cell survival factor in the human testsi in vitro. J Clin Endocrinol Metab 85, 2057-2067 (2000)
74. P.T. Saunders, M.R. Millar, S. Macpherson, D.S. Irvine, N.P. Groome, L.R. Evans R.M., Sharpe and G.A. Scobie: ERbeta1 and the ERbeta2 splice variant (ERbetacx/beta2) are expressed in distinct cell populations in the adult human testis. J. Clin. Endocrinol. Metab. 87, 2706-2715 (2002)
75. E.L. Aschim, T. Saether, R. Wiger, T. Grotmol and T.B. Haugen: Differential distribution of splice variants of estrogen receptor beta in human testicular cells suggests specific functions in spermatogenesis. J. Steroid Biochem. Mol. Biol. 92, 97-106 (2004).
76. S. Aquila, D. Sisci, M. Gentile, E. Middea, S. Catalano, A. Carpino, V. Rago and S. Ando: Estrogen receptor (ER)alpha and ER beta are both expressed in human ejaculated spermatozoa: evidence of their direct interaction with phosphatidylinositol-3-OH kinase/Akt pathway. J. Clin. Endocrinol. Metab. 89, 1443-1451 (2004).
77. S. Solakidi, A.M. Psarra, S. Nikolaropoulos and C.E. Sekeris: Estrogen receptors alpha and beta (ERalpha and ERbeta) and androgen receptor (AR) in human sperm: localization of ERbeta and AR in mitochondria of the midpiece. Hum. Reprod. 20, 3481-3487 (2005)
78. E.R. Prossnitz, J.B. Aterburn, H.O. Smith, T.I.Oprea, L.A. Sklar and H.J. Hathaway : Estrogen signaling through the transmembrane G proteincoupled receptor GPR30. Annu Rev Physiol 70, 165-190 (2008)
79. R. Sirianni, A. Chimento, C. Ruggiero, A. De Luca, R. Lappano, S. Ando, M. Maggiolini, and V. Pezzi: The Novel Estrogen Receptor, G Protein-Coupled Receptor 30, Mediates the Proliferative Effects Induced by 17{beta}- Estradiol on Mouse Spermatogonial GC-1 Cell Line. Endocrinology 149, 5043-5051 (2008)
80. D. Mahato, E.H. Goulding, K.S. Korach, E.M. Eddy: Spermatogenic cells do not require estrogen receptor-? for development or function. Endocrinology 141, 1273-1276 (2000).
81. D. Mahato, E.H. Goulding, K.S. Korach, E.M. Eddy : Estrogen receptor-? is required by the supporting somatic cells for spermatogenesis. Mol. Cell. Endocrinol. 178, 57-63 (2001).
82. A. Joseph, B. D. Shur, C. Ko, P. Chambon, R. A. Hess : Epididymal hypo-osmolality induces abnormal sperm morphology and function in the estrogen receptor alpha knockout mouse. Biol. Reprod., in press (2010).
83. A. Joseph, R. Hess, D.J. Schaeffer, C. Ko, S. Hudgin- Spivey, P. Chambon, B.D. Shur: Absence of estrogen receptor alpha leads to physiological alterations in the mouse epididymis and consequence defects in sperm function. Biol. Reprod. In press, (2010).
84. M. C. Antal, A. Krust, P. Chambon, M. Mark : Sterility and absence of histopathological defects in non reproductive organs of a mouse ER?-null mutant. Proc Natl Acad Sci USA 105, 2433-2438 (2008).
85. K.M. Robertson, L. O'Donnell, M. E. E. Jones, S. J. Meachem, W.C. Boon, C.R. Fisher, K.H. Graves, R.I. McLachlan and E.R. Simpson: Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc Natl Acad Sci USA 96,7986-7991 (1999)
86. K.A. Fowler, K.Gill, N. Kirma, D.L. Dillehay and R.R.Tekmal: Overexpression aromatase leads to development of testicular Leydig cell tumors. Am J Pathol 156, 347-353 (2000).
87. X. Li, E. Nokkala, W. Yan, T. Streng, N. Saarinen, A. Wärri, I. Huhtaniemi I., R. Santti, S. Mäkelä and M. Poutanen,. Altered structure and function of reproductive organs in transgenic male mice overexpressing human aromatase. Endocrinology. 142, 2435-42 (2001)
88. X. Li and N. Rahman: Impact of androgen/estrogen ratio: lessons learned from the aromatase over-expression mice. Gen. Comp. Endocrinol. 159, 1-9 (2008).
89. J. Weiss, M.L. Bernhardt, M.M. Laronda, L.A. Hurley, C. Glidewell-Kenney, S. Pillai, M. Tong, K.S. Korach and J.L. Jameson: Estrogen actions in the male reproductive system involve estrogen response element-independent pathways. Endocrinology 149, 6198-6206 (2008)
90. K.W. Sinkevicius, M. Laine, T.L. Lotan, K.Woloszyn, J.H. Richburg and G.L. Greene: Estrogen dependent and - independent estrogen receptor falpha signaling separately regulate male fertility. Endocrinology 150, 2898-28905 (2009).
91. H. Sakamoto, K. Matsuda, K. Hosokawa, M. Nishi, J.F. Morris, E.R. Prossnitz and M. Kawata: Expression of G protein-coupled receptor-30, a G protein-coupled membrane estrogen receptor, in oxytocin neurons of the rat paraventricular and supraoptic nuclei. Endocrinology 148, 5842-5850 (2007)
92. J. Isensee, L. Meoli, V. Zazzu, C. Nabzdyk, H. Witt, D. Soewarto, K. Effertz, H. Fuchs, V. Gailus-Durner, D. Busch, T. Adler, M.H. de Angelis, M. Irgang, C. Otto and P.R. Noppinger : Expression pattern of G protein-coupled receptor 30 in LacZ reporter mice. Endocrinology 150, 1722-1730 (2009).
93. C.M. Revankar, D.F. Cimino, L.A. Sklar, J.B. Arterburn, E.R. and Prossnitz: A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307, 1625- 1630 (2005).
94. T. Funakoshi, A. Yanai, K. Shinoda, M.M. Kawano and Y. Mizukami: G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem. Biophys. Res. Commun. 346, 904-910 (2006).
95. M.H Perrard and P. Durand : Redundancy of the effcet of TGFbeta1 and beta-NGF on the second meiotic division of rat spermatocytes. Microsc Res Tech 72, 596-602 (2009)
96. C. Otto, I. Fuchs, G. Kauselmann, H. Kern, B. Zevnik, P. Andreasen, G. Schwarz, H. Altmann, M. Klewer, M. Schoor, R. Vonk and K.H. Fritzemeier: GPR30 does not mediate estrogenic responses in reproductive organs in mice. Biol Reprod. 80, 34-41 (2009).
97. E.R. Levin : G protein-coupled receptor 30 : estrogen recptor or collaborator? Endocrinology 150, 1563-1565 (2009)
98. Y. Wang, R.Thuillier and M. Culty: prenatal estrogen exposure differentially affects estrogen receptor-associated proteins in rat testis gonocytes. Biol Reprod 71, 1652-1664 (2004).
99. K.L. Porter, G. Shetty, G.A. Shuttlesworth, C.C.Y Weng, I.Huhtaniemi, P. Pakarinen and M.L Meistrich: Estrogen enhances recovery from radiation-induced spermatogonial arrest in rat testes. J Androl 30, 440-451 (2009)
100. R. Walczak-Jedrzejowska, J. Slowikowska-Hilczer, K. Marchlewsk, E. Oszukowska and K. Kula: During seminiferous tubule maturation testosterone and synergistic action of FSH with estradiol support germ cell survival while estradiol alone has pro-apoptotic effect. Folia Histochem Cytobiol 45, S 59-64 (2007)
101. M.Gancarczyk, A. Paziewska , S. Carreau and B. Bilinska : Dose and photoperiod- dependent effect of 17?- estradiol or ICI 182,780 administration on testicular structure, acceleration of spermatogenesis and aromatase immunoexpression in immature bank voles. Acta Histochem 106, 269-278 (2004)
102. F.J. Ebling, A.N.Brooks, AA.S.Cronin, H. Ford and J.B. Kerr: Estrogenic induction of spermatogenesis in the hypogonadal mouse. Endocrinology 141, 2861-2869 (2000)
103. T.R. Pak , G.R. Lynch and P.S. Tsai : Estrogen accelerates gonadal recrudescence in photo-regressed male siberian hamsters. Endocrinology 143, 4131-4134 (2002)
104. S. Assinder, R. Davis, M. Fenwick and A. Glover: Adult-only exposure of male rats to a diet of high phytoestrogen content increases apoptosis of meiotic and post-meiotic germ cells. Reproduction 133, 11-19 (2007)
105. G. Delbes, C. Levacher, C. Pairault, C. Racine, C. Duquenne, A. Krust and R. Habert: Estrogen receptor betamediated inhibition of male germ cell line development in mice by endogenous estrogens during perinatal life. Endocrinology 145, 3395-3403 (2004)
106. M. Culty: Gonocytes, the forgotten cells of the germ cell lineage. Birth Defects Res 87, 1-26 (2009)
107. R. D'Souza, M.K. Gill-Sharma, S. Pathak, N. Kedia, R. Kumar and N. Balasinor : Effect of high intratesticular estrogen on the seminiferous epithelium in adult male rats. Mol Cell Endocrinol 241, 41-48 (2005)
108. G. Shetty, H. Krishnamurthy, H.N. Krishnamurthy, A.S. Bhatnagar and N.R. Moudgal : Effect of long-term treatment with aromatase inhibitor on testicular function of adult male bonnet monkeys (M. radiata). Steroids 63 : 414-420 (1998)
109. E.D. Albrecht, M.V. Lane, G.R. Marshall, I. Merchenthaler, D.R. Simorangkir, C. R Pohl, T.M. Plant and G.P. Pepe: Estrogen promotes germ cell and seminiferous tubule development in the baboon fetal testis. Biol Reprod 81, 406-414 (2009)
110. K. Hamden, D. Silandre,C. Delalande, A. El Feki and S. Carreau: Protective effects of estrogens and caloric restriction during aging on various rat testis parameters. Asian J Androl 10, 837-845 (2008)
111. K.J. Beck, S. Herscel, R. Hungershofer and E. Schwinger:The effect of steroid hormones on motility and selective migration of X-and Y-bearing human spermatozoa. Fertil Steril 27,407-412 (1976)
112. M. Idaomar, J.F. Guerin, J. Lornage and J.C. Czyba : Stimulation of motility and energy metabolism of spermatozoa from asthenospermic patients by 17?-estradiol. Arch Androl 22,197-202 (1989)
113. N Berensztein, E.B.,Baquedano,M. S.,Gonzalez,C.R., Saraco,. I., Rodriguez, J., R. Ponzio, , M. A. Rivarola, and A. Belgorosky: Expression of aromatase, estrogen receptor a and b, androgen receptor, and cytochrome P-450 scc in the human early prepubertal testis. Pediatr.Res. 60, 740-744 (2006).
114. L Maffei, V.Rochira, L.Zirilli, P. Antunez, C. Aranda, B. Fabre, M.L. Simone, E. Pignatti, E.R. Simpson, C.D. Clyne and C.Carani : A novel compound heterozygous mutation of the aromatase gene in an adult man: reinforced evidence on the relationship between congenital oestrogen deficiency, adiposity and the metabolicsyndrome. Clin Endocrinol 67, 218-224 (2007)
115. V. Rochira and C. Carani : Aromatase deficiency in men: A clinical perspective. Nat Rev Endocrinol 5, 559-568 (2009)
116. I. Czajka-Oraniec and E.R. Simpson: Aromatase research and clinical significance. Polish J Endocrinol 61, in press (2010)
117. A. Bouskine, M. Nebout, B.Mograbi, F. Brucker-Davis, C. Roger and P. Fenichel: Estrogens promote human testicular germ cell cancer through a membranemediated activation of extracellular regulated kinase and protein kinase A. Endocrinology 149, 565-573 (2008)
118. J. Toppari, J.C. Larsen, P. Christiansen, A. Giwercman, P. Grandjean, L.J. Guillette Jr, B. Jegou, T.K. Jensen, P. Jouannet, N. Keiding, H. Leffers, J.A. McLachlan, O. Meyer, J. Muller, E. Rajpert-De Meyts , T. Scheike, R.M. Sharpe , J. Sumpter and N.E.Skakkebaek: Male reproductive health and environmental xenoestrogens. Environ Health Perspect 104, 741-803 (1996)
119. N.E. Skakkebaek: Testicular dysgenesis syndrome: new epidemiological evidence. Int J. Androl 27, 189-201 (2004)
120. M. Maggiolini and D.Picard: The unfolding stories of GPR30, a new membrane-bound estrogen receptor. J Endocrinol 204, 105-114 (2010)