Aromatase gene expression in immature rat Sertoli cells: Age-related changes in the FSH signalling pathway

Reproduction, Fertility and Development

Volumn 22, Issue 3, 2010, Pages 508-515

  Bouraïma Lelong, Hélène ^a,b   Vanneste, Marion ^a,b   Delalande, Christelle ^a,b   Zanatta, Leïla ^a,b,c   Wolczynski, Slawomir ^d   Carreau, Serge ^a,b  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITÉ DE CAEN   (France)

^c FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^d MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

Author keywords

Germ cells; Phosphatidylinositol 3 kinase

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AROMATASE; BUCLADESINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; FOLLITROPIN; FORSKOLIN; PHOSPHATIDYLINOSITOL 3 KINASE;

AGING; ANIMAL CELL; ARTICLE; BLOOD TESTIS BARRIER; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; COCULTURE; CONTROLLED STUDY; GENE EXPRESSION; GERM CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PUERPERIUM; RAT; SERTOLI CELL; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AGE FACTORS; AGING; ANALYSIS OF VARIANCE; ANIMALS; AROMATASE; BLOOD-TESTIS BARRIER; CELLS, CULTURED; CHROMONES; ENZYME INHIBITORS; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; ISOQUINOLINES; MALE; MORPHOLINES; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERTOLI CELLS; SIGNAL TRANSDUCTION; SULFONAMIDES;

RATTUS;

EID: 77649330831     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD09168     Document Type: Article

References (35)

1. Andò, S., Sirianni, R., Forastieri, P., Casaburi, I., Lanzino, M., Rago, V., Giordano, F., Giordano, C., Carpino, A., and Pezzi,V. (2001). Aromatase expression in prepuberal Sertoli cells: effect of thyroid hormone. Mol. Cell. Endocrinol. 178, 11-21. doi:10.1016/S0303-7207(01)00443-9 (Pubitemid 32515345)
2. Boitani, C., Ritzén, E. M., and Parvinen, M. (1981). Inhibition of rat Sertoli cell aromatase by factor(s) secreted specifically at spermatogenic Stages VII and VIII. Mol. Cell. Endocrinol. 23, 11-22. doi:10.1016/0303-7207(81) 90113-1 (Pubitemid 11065719)
3. Bourguiba, S., Chater, S., Delalande, C., Benahmed, M., and Carreau, S. (2003). Regulation of aromatase gene expression in purified germ cells of adult male rats: effects of transforming growth factor beta, tumor necrosis factor alpha, and cyclic adenosine 3′5′-monosphosphate. Biol. Reprod. 69, 592-601. doi:10.1095/BIOLREPROD.102.013961 (Pubitemid 36885965)
4. Carlone, D. L., and Richards, J. S. (1997). Functional interactions, phosphorylation, and levels of 3′5′-cyclic adenosine monophosphate-regulatory element binding protein and steroidogenic factor-1 mediate hormoneregulated and constitutive expression of aromatase in gonadal cells. Mol. Endocrinol. 11, 292-304. doi:10.1210/ME.11.3.292 (Pubitemid 27106325)
5. Carpino, A., Pezzi, V., Rago, V., Bilinska, B., and Andò, S. (2001). Immunolocalization of cytochrome P450 aromatase in rat testis during postnatal development. Tissue Cell 33, 349-353. doi:10.1054/TICE. 2001.0186 (Pubitemid 32755107)
6. Carreau, S., Delalande, C., Silandre, D., Bourguiba, S., and Lambard, S. (2006). Aromatase and estrogen receptors in male reproduction. Mol. Cell. Endocrinol. 246, 65-68. doi:10.1016/J.MCE.2005.11.021 (Pubitemid 43238398)
7. Crépieux, P., Marion, S., Martinat, N., Fafeur, V., Vern,Y. L., Kerboeuf, D., Guillou, F., and Reiter,E. (2001).The ERK-dependent signalling is stagespecifically modulated by FSH, during primary Sertoli cell maturation. Oncogene 20, 4696-4709. doi:10.1038/SJ.ONC.1204632 (Pubitemid 32762441)
8. Davies, S. P., Reddy, H., Caivano, M., and Cohen, P. (2000). Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105. doi:10.1042/0264-6021:3510095 (Pubitemid 30781561)
9. Fitzpatrick, S. L., and Richards, J. S. (1993). Cis-acting elements of the rat aromatase promoter required for cyclic adenosine 3′5′- monophosphate induction in ovarian granulosa cells and constitutive expression in R2C Leydig cells. Mol. Endocrinol. 7, 341-354. doi:10.1210/ME.7.3.341 (Pubitemid 23104523)
10. Galdieri, M., Ziparo, E., Palombi, F., Russo, M., and Stafanini, M. (1981). Pure Sertoli cell cultures: a new model for the study of somatic-germ cell interactions. J. Androl. 5, 249-254.
11. Genissel, C., Levallet, J., and Carreau, S. (2001). Regulation of cytochrome P450 aromatase gene expression in adult rat Leydig cells: comparison with estradiol production. J. Endocrinol. 168, 95-105. doi:10.1677/ JOE.0.1680095 (Pubitemid 32099357)
12. Kwintkiewicz, J., Cai, Z., and Stocco, C. (2007). Follicle-stimulating hormone-induced activation of Gata4 contributes in the up-regulation of Cyp19 expression in rat granulosa cells. Mol. Endocrinol. 21, 933-947. doi:10.1210/ME.2006-0446 (Pubitemid 46984733)
13. Lanzino, M., Catalano, S., Genissel, C., Ando, S., Carreau, S., Hamra, K., and McPhaul, M. J. (2001). 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. doi:10.1095/ BIOLREPROD64.5.1439
14. Le Magueresse, B., and Jégou, B. (1986). Possible involvement of germcells in the regulation of oestradiol-17 beta and ABP secretion by immature rat Sertoli cells (in vitro studies). Biochem. Biophys. Res. Commun. 141, 861-869. doi:10.1016/S0006-291X(86)80252-2 (Pubitemid 17001936)
15. Levallet, G., Levallet, J., Bouraïma-Lelong, H., and Bonnamy, P. J. (2007). Expression of the cAMP-phosphodiesterase PDE4D isoforms and age-related changes in follicle-stimulating hormone-stimulated PDE4 activities in immature rat sertoli cells. Biol. Reprod. 76, 794-803. doi:10.1095/BIOLREPROD.106.055343 (Pubitemid 46651220)
16. Levallet, J., Bilinska, B., Mittre, H., Genissel, C., Fresnel, J., and Carreau, S. (1998). Expression and immunolocalization of functional cytochrome P450 aromatase in mature rat testicular cells. Biol. Reprod. 58, 919-926. doi:10.1095/BIOLREPROD58.4.919 (Pubitemid 28144979)
17. Li, X., and Rahman, N. (2008). Impact of androgen/estrogen ratio: lessons learned from the aromatase over-expression mice. Gen. Comp. Endocrinol. 159, 1-9. doi:10.1016/J.YGCEN.2008.07.025
18. Lucas,T. F., Siu, E. R., Esteves, C. A., Monteiro, H. P., Oliveira, C. A., Porto, C. S., and Lazari, M. F. (2008). 17?-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. doi:10.1095/BIOLREPROD.107.063909
19. Lynch, J. P., Lala, D. S., Peluso, J. J., Luo,W., Parker, K. L., and White, B. A. (1993). Steroidogenic factor 1, an orphan nuclear receptor, regulates the expression of the rat aromatase gene in gonadal tissues. Mol. Endocrinol. 7, 776-786. doi:10.1210/ME.7.6.776 (Pubitemid 23207381)
20. Malkov, M., Fisher, Y., and Don, J. (1998). Developmental schedule of the postnatal rat testis determined by flow cytometry. Biol. Reprod. 59, 84-92. doi:10.1095/BIOLREPROD59.1.84 (Pubitemid 28304357)
21. McDonald, C. A., Millena, A. C., Reddy, S., Finlay, S., Vizcarra, J., Khan, S. A., and Davis, J. S. (2006). Follicle-stimulating hormone-induced aromatase in immature rat Sertoli cells requires an active phosphatidylinositol 3-kinase pathway and is inhibited via the mitogen-activated protein kinase signaling pathway. Mol. Endocrinol. 20, 608-618. doi:10.1210/ME.2005-0245 (Pubitemid 43291212)
22. Meroni, S. B., Riera, M. F., Pellizzari, E. H., Galardo, M. N., and Cigorraga, S. B. (2004). FSH activates phosphatidylinositol 3-kinase/protein kinase B signaling pathway in 20-day-old Sertoli cells independently of IGF-I. J. Endocrinol. 180, 257-265. doi:10.1677/JOE.0.1800257 (Pubitemid 38312606)
23. Papadopoulos, V., Carreau, S., Szerman-Joly, E., Drosdowsky, M. A., Dehennin, L., and Scholler, R. (1986). Rat testis 17beta-estradiol: identification by gas chromatography-mass spectrometry and age related cellular distribution. J. Steroid Biochem. 24, 1211-1216. doi: 10.1016/0022-4731(86) 90385-7 (Pubitemid 16056658)
24. Parakh, T. N., Hernandez, J. A., Grammer, J. C., Weck, J., Hunzicker-Dunn, M., Zeleznik, A. J., and Nilson, J. H. (2006). Follicle-stimulating hormone/cAMP regulation of aromatase gene expression requires betacatenin. Proc. Natl Acad. Sci. USA 103, 12 435-12 440. doi:10.1073/ PNAS.0603006103
25. Perrard, M. H., Vigier, M., Chapat, C., Silandre, D., Rudkin, B. B., and Durand, P. (2007). beta-Nerve growth factor participates in an auto/ paracrine pathway of regulation of the meiotic differentiation of rat spermatocytes. J. Cell. Physiol. 210, 51-62. doi:10.1002/JCP.20805 (Pubitemid 44904700)
26. Robertson, K. M., O'Donnell, L., Jones, M. E., Meachem, S. J., Boon,W. C., Fisher, C. R., Graves, K. H., McLachlan, R. I., and Simpson, E. R. (1999). Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc. Natl Acad. Sci. USA 96, 7986-7991. doi:10.1073/PNAS.96.14.7986 (Pubitemid 29328394)
27. Schteingart, H. F., Meroni, S. B., Cánepa, D. F., Pellizzari, E. H., and Cigorraga, S. B. (1999). Effects of basic fibroblast growth factor and nerve growth factor on lactate production, gamma-glutamyl transpeptidase and aromatase activities in cultured Sertoli cells. Eur. J. Endocrinol. 141, 539-545. doi:10.1530/EJE.0.1410539
28. Silandre,D., Delalande, C., Durand, P., and Carreau, S. (2007).Three promoters PII, PI.f, and PI.tr direct the expression of aromatase (cyp19) gene in male rat germ cells. J. Mol. Endocrinol. 39, 169-181. doi:10.1677/JME-07-0046 (Pubitemid 47337875)
29. Simoni, M., Gromoll, J., and Nieschlag, E. (1997). The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 18, 739-773. doi:10.1210/ER.18.6. 739 (Pubitemid 28009566)
30. Steinberger, A., Hintz, M., and Heindel, J. J. (1978). Changes in cyclicAMP responses to FSH in isolated rat Sertoli cells during sexual maturation. Biol. Reprod. 19, 566-572. doi:10.1095/BIOLREPROD19.3.566
31. Tena-Sempere, M., Barreiro, M. L., Gonzales, L. C., Gaytan, F., Zhang, F. P., Carminos, J. E., Pinilla, L., Casanueva, F. F., Dieguez, C., and Aguilar, E. (2002). Novel expression and functional role of ghrelin in rat testis. Endocrinology 143, 717-725. doi:10.1210/EN.143.2.717 (Pubitemid 34107228)
32. Tremblay, J. J., andViger, R. S. (2001). Nuclear receptor Dax-1 represses the transcriptional cooperation between GATA-4 and SF-1 in Sertoli cells. Biol. Reprod. 64, 1191-1199. doi:10.1095/BIOLREPROD64.4.1191
33. Tung, P. S., and Fritz, I. B. (1984). Autoimmune orchitis can be induced by thymic lymphocytes autosensitized against syngeneic sertoli cells in vitro. Biol. Reprod. 30, 979-990. doi:10.1095/BIOLREPROD30.4.979
34. Walker, W. H., and Cheng, J. (2005). FSH and testosterone signaling in Sertoli cells. Reproduction. 130, 15-28. [Review] doi:10.1530/REP.1. 00358 (Pubitemid 41015229)
35. Wang, Z. J., Jeffs, B., Ito, M., Achermann, J. C.,Yu, R. N., Hales, D. B., and Jameson, J. L. (2001). Aromatase (Cyp19) expression is up-regulated by targeted disruption of Dax1. Proc. Natl Acad. Sci. USA 98, 7988-7993. doi:10.1073/PNAS.141543298 (Pubitemid 32642674)