Gper and ESRs are expressed in rat round spermatids and mediate oestrogen-dependent rapid pathways modulating expression of cyclin B1 and Bax

International Journal of Andrology

Volumn 34, Issue 5 PART 1, 2011, Pages 420-429

  Chimento, A ^a   Sirianni, R ^a   Zolea, F ^a   Bois, C ^b   Delalande, C ^b   Ando S ^a   Maggiolini, M ^a   Aquila, S ^a   Carreau, S ^b   Pezzi, V ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

^b UNIVERSITÉ DE CAEN   (France)

Author keywords

Gper; Oestrogen; Oestrogen receptors; Rat; Round spermatids

Indexed keywords

4,4',4'' (4 PROPYL [1H]PYRAZOLE 1,3,5 TRIYL)TRISPHENOL; CYCLIN B1; DIARYLPROPIONITRILE; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR 30; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN BAX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SPERMATID; SPERMATOZOON MATURATION;

ANIMALS; BASE SEQUENCE; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CYCLIN B1; DNA PRIMERS; ENZYME ACTIVATION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLUORESCENT ANTIBODY TECHNIQUE; MALE; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPERMATIDS;

EID: 80053329514     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2010.01100.x     Document Type: Article

References (75)

1. Almog T & Naor Z. (2008) Mitogen activated protein kinases (MAPKs) as regulators of spermatogenesis and spermatozoa functions. Mol Cell Endocrinol 282, 39-44.
2. Bagowski CP, Xiong W & Ferrell JE Jr. (2001) c-Jun N-terminal kinase activation in Xenopus laevis eggs and embryos. A possible non-genomic role for the JNK signaling pathway. J Biol Chem 276, 1459-1465.
3. Bellve AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM & Dym M. (1977) Spermatogenic cells of the prepuberal mouse: isolation and morphological characterization. J Cell Biol 74, 68-85.
4. Bjornstrom L & Sjoberg M. (2005) Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol 19, 833-842.
5. Blanco-Rodriguez J & Martinez-Garcia C. (1997) Apoptosis pattern elicited by oestradiol treatment of the seminiferous epithelium of the adult rat. Reproduction 110, 61-70.
6. Bourguiba S, Genissel C, Lambard S, BouraÇma H & Carreau S. (2003) Regulation of aromatase gene expression in Leydig cells and germ cells. J Steroid Biochem Mol Biol 86, 335-343.
7. Brailoiu E, Dun SL, Brailoiu GC, Mizuo K, Sklar LA, Oprea TI, Prossnitz ER & Dun NJ. (2007) Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J Endocrinol 193, 311-321.
8. Carreau S & Hess R. (2010) Oestrogens and spermatogenesis. Philos Trans R Soc B 365, 1517-1535.
9. Carreau S, Delalande C, Silandre D, Bourguiba S & Lambard S. (2006) Aromatase and estrogen receptors in male reproduction. Mol Cell Endocrinol 246, 65-68.
10. Chagin AS & Savendahl L. (2007) GPR30 estrogen receptor expression in the growth plate declines as puberty progresses. J Clin Endocrinol Metab 92, 4873-4877.
11. Chapman DL & Wolgemuth DJ. (1993) Isolation of the murine cyclin B2 cDNA and characterization of the lineage and temporal specificity of expression of the B1 and B2 cyclins during oogenesis, spermatogenesis and early embryogenesis. Development 118, 229-240.
12. Chimento A, Sirianni R, Delalande C, Silandre D, Bois C, Andò S, Maggiolini M, Carreau S & Pezzi V. (2010) 17β-estradiol activates rapid signaling pathways involved in rat pachytene spermatocytes apoptosis through GPR30 and ERα. Mol Cell Endocrinol 320, 136-144.
13. D'Souza R, Gill-Sharma MK, Pathak S, Kedia N, Kumar R & Balasinor N. (2005) Effect of high intratesticular estrogen on the seminiferous epithelium in adult male rats. Mol Cell Endocrinol 241, 41-48.
14. Ebling FJP, Brooks AN, Cronin AS, Ford H & Kerr JB. (2000) Estrogenic induction of spermatogenesis in the hypogonadal mouse. Endocrinology 141, 2861-2869.
15. Filardo EJ, Quinn JA, Bland KI & Frackelton AR Jr. (2000) Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol 14, 1649-1660.
16. Filardo EJ, Quinn JA, Frackelton AR Jr & Bland KI. (2002) Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol 16, 70-84.
17. Fisher JS, Millar MR, Majdic G, Saunders PT, Fraser HM & Sharpe RM. (1997) Immunolocalization of oestrogen receptor-a within the testis and excurrent ducts of the rat and marmoset monkey from perinatal life to adulthood. J Endocrinol 153, 485-495.
18. Funakoshi T, Yanai A, Shinoda K, Kawano MM & Mizukami Y. (2006) G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun 346, 904-910.
19. Gancarczyk M, Paziewska-Hejmej A, Carreau S, Tabarowski Z & Bilinska B. (2004) Dose- and photoperiod-dependent effects of 17beta-estradiol and the anti-estrogen ICI 182, 780 on testicular structure, acceleration of spermatogenesis, and aromatase immunoexpression in immature bank voles. Acta Histochem 106, 269-278.
20. Godet M, Thomas A, Rudkin BB & Durand P. (2000) Developmental changes in cyclin B1 and cyclin-dependent kinase 1 (CDK1) levels in the different populations of spermatogenic cells of the post-natal rat testis. Eur J Cell Biol 79, 816-823.
21. Godet M, Sabido O, Gilleron J & Durand P. (2008) Meiotic progression of rat spermatocytes requires mitogen-activated protein kinases of Sertoli cells and close contacts between the germ cells and the Sertoli cells. Dev Biol 315, 173-188.
22. Gromoll J, Wessels J, Rosiepen G, Brinkworth MH & Weinbauer GF. (1997) Expression of mitotic cyclin B1 is not confined to proliferating cells in the rat testis. Biol Reprod 57, 1312-1319.
23. Harrington WR, Kim SH, Funk CC, Madak-Erdogan Z, Schiff R, Katzenellenbogen JA & Katzenellenbogen BS. (2006) Estrogen dendrimer conjugates that preferentially activate extranuclear, nongenomic versus genomic pathways of estrogen action. Mol Endocrinol 20, 491-502.
24. Hess RA & Carnes K. (2004) The role of estrogen in testis and the male reproductive tract: a review and species comparison. Anim Reprod 1, 5-30.
25. Hess RA, Gist DH, Bunick D, Lubahn DB, Farrell A, Bahr J, Cooke PS & Greene GL. (1997) Estrogen receptor (alpha and beta) expression in the excurrent ducts of the adult male rat reproductive tract. J Androl 18, 602-611.
26. Hewitt SC, Deroo BJ & Korach KS. (2005a) Signal transduction. A new mediator for an old hormone? Science 307, 1572-1573.
27. Hewitt SC, Harrell JC & Korach KS. (2005b) Lessons in estrogen biology from knockout and transgenic animals. Annu Rev Physiol 67, 285-308.
28. Isensee J, Meoli L, Zazzu V, Nabzdyk C, Witt H, Soewarto D et al. (2009) Expression pattern of G protein-coupled receptor 30 in LacZ reporter mice. Endocrinology 150, 1722-1730.
29. Kaushal N & Bansal MP. (2007) Dietary selenium variation-induced oxidative stress modulates CDC2/cyclin B1 expression and apoptosis of germ cells in mice testis. J Nutr Biochem 18, 553-564.
30. Klinefelter GR, Hall PF & Ewing LL. (1987) Effect of luteinizing hormone deprivation in situ on steroidogenesis of rat Leydig cells purified by a multistep procedure. Biol Reprod 36, 769-783.
31. Lei K, Nimnual A, Zong WX, Kennedy NJ, Flavell RA, Thompson CB, Bar-Sagi D & Davis RJ. (2002) The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH2-terminal kinase. Mol Cell Biol 22, 4929-4942.
32. Levallet J, Bilinska B, Mittre H, Genissel C, Fresnel J & Carreau S. (1998) Expression and immunolocalization of functional cytochrome P450 aromatase in mature rat testicular cells. Biol Reprod 58, 919-926.
33. Levin ER. (2005) Integration of the extranuclear and nuclear actions of estrogen. Mol Endocrinol 19, 1951-1959.
34. Levin ER & Pietras R. (2008) Estrogen receptors outside the nucleus in breast cancer. Breast Cancer Res Treat 108, 351-361.
35. Liu X, Zhu P, Sham KWY, Yuen JML, Xie C, Zhang Y et al. (2009) Identification of a membrane estrogen receptor in zebrafish with homology to mammalian GPER and its high expression in early germ cells of the testis. Biol Reprod 80, 1253-1261.
36. Lucas TFG, Siu ER, Esteves CA, Monteiro HP, Oliveira CA, Porto CS & Lazari MF. (2008) 17beta-estradiol induces the translocation of the estrogen receptors ESR1 and ESR2 to the cell membrane, MAPK3/1 phosphorylation and proliferation of cultured immature rat Sertoli cells. Biol Reprod 78, 101-114.
37. Maggiolini M & Picard D. (2010) The unfolding stories of GPR30, a new membrane-bound estrogen receptor. J Endocrinol 204, 105-114.
38. Maggiolini M, Vivacqua A, Fasanella G, Recchia AG, Sisci D, Pezzi V, Montanaro D, Musti AM, Picard D & Ando S. (2004) The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17beta-estradiol and phytoestrogens in breast cancer cells. J Biol Chem 279, 27008-27016.
39. Manavathi B & Kumar R. (2006) Steering estrogen signals from the plasma membrane to the nucleus: two sides of the coin. J Cell Physiol 207, 594-604.
40. Matthews J & Gustafsson JA. (2003) Estrogen signaling: a subtle balance between ERa and ERb. Mol Interv 3, 281-292.
41. Matthews J, Wihlen B, Tujague M, Wan J, Strom A & Gustafsson JA. (2006) Estrogen receptor (ER) β modulates ERα-mediated transcriptional activation by altering the recruitment of c-Fos and c-Jun to estrogen-responsive promoters. Mol Endocrinol 20, 534-543.
42. Migliaccio A, Di Domenico M, Castoria G, Nanayakkara M, Lombardi M, de Falco A, Bilancio A, Varricchio L, Ciociola A & Auricchio F. (2005) Steroid receptor regulation of epidermal growth factor signaling through Src in breast and prostate cancer cells: steroid antagonist action. Cancer Res 65, 10585-10593.
43. Mishra DP & Shaha C. (2005) Estrogen-induced spermatogenic cell apoptosis occurs via the mitochondrial pathway: role of superoxide and nitric oxide. J Biol Chem 280, 6181-6196.
44. Mutembei HM, Pesch S, Schuler G & Hoffmann B. (2005) Expression of oestrogen receptors alpha and beta and of aromatase in the testis of immature and mature boars. Reprod Domest Anim 40, 228-236.
45. O'Donnell L, Robertson KM, Jones ME & Simpson ER. (2001) Estrogen and spermatogenesis. Endocr Rev 22, 289-318.
46. Oldereid NB, Angelis PD, Wiger R & Clausen OPF. (2001) Expression of Bcl-2 family proteins and spontaneous apoptosis in normal human testis. Mol Hum Reprod 7, 403-408.
47. Otto C, Fuchs I, Kauselmann G, Kern H, Zevnik B, Andreasen P et al. (2009) GPR30 does not mediate estrogenic responses in reproductive organs in mice. Biol Reprod 80, 34-41.
48. Pedram A, Razandi M & Levin ER. (2006) Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol 20, 1996-2009.
49. Pelletier G, Labrie C & Labrie F. (2000) Localization of oestrogen receptor alpha, oestrogen receptor beta and androgen receptors in the rat reproductive organs. J Endocrinol 165, 359-370.
50. Pentikäinen V, Erkkilä K, Suomalainen L, Parvinen M & Dunkel L. (2000) Estradiol acts as a germ cell survival factor in the human testis in vitro. J Clin Endocrinol Metab 85, 2057-2067.
51. Porter LA, Cukier IH & Lee JM. (2003) Nuclear localization of cyclin B1 regulates DNA damage-induced apoptosis. Blood 101, 1928-1933.
52. Prossnitz ER & Maggiolini M. (2009) Mechanisms of estrogen signaling and gene expression via GPR30. Mol Cell Endocrinol 308, 32-38.
53. Ramesh R, Pearl CA, At-Taras E, Roser JF & Berger T. (2007) Ontogeny of androgen and estrogen receptor expression in porcine testis: effect of reducing testicular estrogen synthesis. Anim Reprod Sci 102, 286-299.
54. Revankar CM, Cimino DF, Sklar LA, Arterburn JB & Prossnitz ER. (2005) A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307, 1625-1630.
55. Robertson KM, O'Donnell L, Jones MEE, Meachem SJ, Boon WC, Fisher CR, Graves KH, McLachlan RI & Simpson ER. (1999) Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. PNAS 96, 7986-7991.
56. Robertson KM, O'Donnell L, Simpson ER & Jones MEE. (2002) The phenotype of the aromatase knockout mouse reveals dietary phytoestrogens impact significantly on testis function. Endocrinology 143, 2913-2921.
57. Sakamoto H, Matsuda KI, Hosokawa K, Nishi M, Morris JF, Prossnitz ER & Kawata M. (2007) Expression of GPR30, a G protein-coupled membrane estrogen receptor, in oxytocin neurons of the rat paraventricular and supraoptic nuclei. Endocrinology 148, 5842-5850.
58. Saunders PT, Fisher JS, Sharpe RM & Millar MR. (1998) Expression of oestrogen receptor beta (ER beta) occurs in multiple cell types, including some germ cells, in the rat testis. J Endocrinol 156, R13-R17.
59. Sierens JE, Sneddon SF, Collins F, Millar MR & Saunders PTK. (2005) Estrogens in testis biology. Ann NY Acad Sci 1061, 65-76.
60. Sinha Hikim AP & Swerdloff RS. (1999) Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod 4, 38-47.
61. Sinkevicius KW, Laine M, Lotan TL, Woloszyn K, Richburg JH & Greene GL. (2009) Estrogen-dependent and -independent estrogen receptor-α signaling separately regulate male fertility. Endocrinology 150, 2898-2905.
62. Sirianni R, Chimento A, Malivindi R, Mazzitelli I, Andò S & Pezzi V. (2007) Insulin-like growth factor-I, regulating aromatase expression through steroidogenic factor 1, supports estrogen-dependent tumor Leydig cell proliferation. Cancer Res 67, 8368-8377.
63. Sirianni R, Chimento A, Ruggiero C, De Luca A, Lappano R, Andò S, Maggiolini M & Pezzi V. (2008) The novel estrogen receptor, G protein-coupled receptor 30, mediates the proliferative effects induced by 17β-estradiol on mouse spermatogonial GC-1 cell line. Endocrinology 149, 5043-5051.
64. Sofikitis N, Giotitsas N, Tsounapi P, Baltogiannis D, Giannakis D & Pardalidis N. (2008) Hormonal regulation of spermatogenesis and spermiogenesis. J Steroid Biochem Mol Biol 109, 323-330.
65. Song RXD & Santen RJ. (2006) Membrane initiated estrogen signaling in breast cancer. Biol Reprod 75, 9-16.
66. Song RXD, Zhang Z & Santen RJ. (2005) Estrogen rapid action via protein complex formation involving ERα and Src. Trends Endocrinol Metab 16, 347-353.
67. Subramanian M & Shaha C. (2007) Up-regulation of Bcl-2 through ERK phosphorylation is associated with human macrophage survival in an estrogen microenvironment. J Immunol 179, 2330-2338.
68. Trembley JH, Chen Z, Rodrigues CMP, Kren BT & Steer CJ. (2000) Genomic organization and promoter characterization of the rat cyclin B1 gene. Gene 255, 93-104.
69. Walczak-Jedrzejowska R, Slowikowska-Hilczer J, Marchlewsk K, Oszukowska E & Kula K. (2007) 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 41, S59-S64.
70. Wang C, Prossnitz ER & Roy SK. (2007) Expression of G protein-coupled receptor 30 in the hamster ovary: differential regulation by gonadotropins and steroid hormones. Endocrinology 148, 4853-4864.
71. Weiss J, Bernhardt ML, Laronda MM, Hurley LA, Glidewell-Kenney C, Pillai S, Tong M, Korach KS & Jameson JL. (2008) Estrogen actions in the male reproductive system involve estrogen response element-independent pathways. Endocrinology 149, 6198-6206.
72. Wong CH & Yan Cheng C. (2005) Mitogen-activated protein kinases, adherens junction dynamics, and spermatogenesis: a review of recent data. Dev Biol 286, 1-15.
73. Yamashita S. (2004) Localization of estrogen and androgen receptors in male reproductive tissues of mice and rats. Anat Rec A Discov Mol Cell Evol Biol 279, 768-778.
74. Yu Q & Wu J. (2008) Involvement of cyclins in mammalian spermatogenesis. Mol Cell Biochem 315, 17-24.
75. Zhou Q, Nie R, Prins GS, Saunders PTK, Katzenellenbogen BS & Hess RA. (2002) Localization of androgen and estrogen receptors in adult male mouse reproductive tract. J Androl 23, 870-881.