Age- and cell-related gene expression of aromatase and estrogen receptors in the rat testis

Journal of Molecular Endocrinology

Volumn 45, Issue 3, 2010, Pages 147-159

  Bois, C ^a,b   Delalande, C ^a,b   Nurmio, M ^c   Parvinen, M ^c   Zanatta, L ^a,b,d   Toppari, J ^c   Carreau, S ^a,b  

^a UNIVERSITÉ DE CAEN   (France)

^b CEMAGREF   (France)

^c UNIVERSITY OF TURKU   (Finland)

^d FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MESSENGER RNA;

AGE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL TYPE; CONTROLLED STUDY; DNA MODIFICATION; EXON; GENE DELETION; GENE EXPRESSION; GENE INSERTION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GERM CELL; HAPLOIDY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PACHYTENE; PRIORITY JOURNAL; RAT; SEMINIFEROUS TUBULE EPITHELIUM; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; TESTIS; WILD TYPE;

AGING; ANIMALS; AROMATASE; CELL COMPARTMENTATION; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MALE; ORGAN SPECIFICITY; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ESTROGEN; RNA, MESSENGER; SERTOLI CELLS; TESTIS;

EID: 77957376255     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1677/JME-10-0041     Document Type: Article

References (62)

1. Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ 1990 Basic local alignment search tool. Journal of Molecular Biology 215 403-410. (Pubitemid 20364473)
2. Antal MC, Krust A, Chambon P & Mark M 2008 Sterility and absence of histopathological defects in nonreproductive organs of a mouse ERβ-null mutant. PNAS 105 2433-2438.
3. Aschim EL, Saether T, Wiger R, Grotmol T & Haugen TB 2004 Differential distribution of splice variants of estrogen receptor beta in human testicular cells suggests specific functions in spermatogenesis. Journal of Steroid Biochemistry and Molecular Biology 92 97-106.
4. Bellve AR, Millette CF, Bhatnagar YM & O'Brien DA 1977 Dissociation of the mouse testis and characterization of isolated spermatogenic cells. Journal of Histochemistry and Cytochemistry 25 480-494. (Pubitemid 8185293)
5. Boitani C, Ritzén EM & 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 11-21.
6. Bouraïma-Lelong H, Vanneste M, Delalande C, Zanatta L, Wolczynski S & Carreau S 2010 Aromatase gene expression in immature rat Sertoli cells: age-related changes in the FSH signaling pathway. Reproduction, Fertility, and Development 22 508-515.
7. Bourguiba S, Chater S, Delalande C, Benahmed M & Carreau S 2003a Regulation of aromatase gene expression in purified germ cells of adult male rats: effects of transforming growth factor β, tumor necrosis factor a, and cyclic adenosine 3′,5′-monophosphate. Biology of Reproduction 69 592-601.
8. Bourguiba S, Lambard S & Carreau S 2003b Steroids control the aromatase gene expression in purified germ cells from the adult male rat. Journal of Molecular Endocrinology 31 83-94.
9. Brand H, Kos M, Denger S, Flouriot G, Gromoll J, Gannon F & Reid G 2002 A novel promoter is involved in the expression of estrogen receptor alpha in human testis and epididymis. Endocrinology 143 3397-3404.
10. Bryant WM, Gibson MA & Shupnik MA 2006 Stimulation of the novel estrogen receptor-alpha intronic TERP-1 promoter by estrogens, androgen, pituitary adenylate cyclase-activating peptide, and forsokolin, and autoregulation by TERP-1 protein. Endocrinology 147 543-551.
11. Carpino A, Pezzi V, Rago V, Bilinska B & Ando S 2001 Immunolocalization of cytochrome P450 aromatase in rat testis during postnatal development. Tissue and Cell 33 349-353. (Pubitemid 32755107)
12. Carreau S & Hess R 2010 Oestrogens and spermatogenesis. Philosophical Transactions of the Royal Society of London. Series B 365 1517-1535.
13. Carreau S, Delalande C & Denis-Galeraud I 2009 Mammalian sperm quality and aromatase expression. Microscopy Research and Technique 72 552-557.
14. Chimento A, Sirianni R, Delalande C, Silandre D, Bois C, Andò S, Maggioloni M, Carreau S & Pezzi V 2010 17β-estradiol activates rapid signaling pathways involved in rat pachytene spermatocytes apoptosis through GPR30 and ER alpha. Molecular and Cellular Endocrinology 320 136-144.
15. Dadoune JP 1994 The cellular biology of mammalian spermatids: a review. Bulletin de l'Association des Anatomistes 78 33-40.
16. Dorrington JH, Roller NF & Fritz IB 1975 Effects of follicle-stimulating hormone in cultures of Sertoli cells preparations. Molecular and Cellular Endocrinology 3 57-70.
17. Eddy EM 2002 Male germ cell expression. Recent Progress in Hormone Research 57 103-128.
18. Eddy EM, Washburn TF, Bunch DO, Goulding EH, Gladen BC, Lubahn DB & Korach KS 1996 Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 137 4796-4805.
19. Fisher JS, Millar MR, Majdic G, Saunders PT, Fraser HM & Sharpe RM 1997 Immunolocalisation of estrogen receptor-alpha within the testis and excurrent ducts of the rat and marmoset monkey from perinatal life to adulthood. Journal of Endocrinology 153 485-495.
20. Franca LR, Ogawa T, Avarbock MR, Brinster RL & Russell LD 1998 Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biology of Reproduction 59 1371-1377.
21. Friend KE, Resnick EM, Ang LW & Shupnik MA 1997 Specific modulation of estrogen receptor mRNA isoforms in rat pituitary throughout the estrous cycle and in response to steroid hormones. Molecular and Cellular Endocrinology 131 147-155.
22. Geffroy-Roisne S, Duval J & Thieulant ML 1992 Multiple forms of affinity-labeled estrogen receptors in rat distinct pituitary cells. Endocrinology 131 1503-1510.
23. Gnessi L, Fabbri A & Spera G 1997 Gonadal peptides as mediators of development and functional control of the testis: an integrated system with hormones and local environment. Endocrine Reviews 18 541-609. (Pubitemid 27349556)
24. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Strom A, Treuter E, Warner M et al. 2007 Estrogen receptors: how do they signal and what are their targets. Physiological Reviews 87 905-913.
25. Janulis L, Bahr JM, Hess RA & 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 17 651-658.
26. Johnston DS, Wright WW, DiCandeloro P, Wilson E, Kopf GS & Jelinsky Scott A 2008 Stage-specific gene expression is a fundamental characteristic of rat spermatogenic cells and Sertoli cells. PNAS 105 8315-8320.
27. Jones ME, Boon WC, Poietto J & Simpson ER 2006 Of mice and men: the evolving phenotype of aromatase deficiency. Trends in Endocrinology and Metabolism 17 55-64.
28. Joseph A, Shur BD, Ko CM, Chambon P & Hess RA 2010 Epididymal hypo-osmolality induces abnormal spermmorphology and function in the estrogen receptor alpha knockout mouse. Biology of Reproduction 82 958-967.
29. Kimmins S, Kotaja N, Davidson I & Sassone-Corsi P 2004 Testis-specific transcription mechanisms promoting germ-cell differentiation. Reproduction 128 5-12.
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. Biology of Reproduction 36 769-783.
31. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA & Smithies O 1998 Generation and reproduction phenotype of mice lacking estrogen receptor beta. PNAS 95 15677-15682.
32. Leblond CP & Clermont Y 1952 Definition of the stages of the cycle of the seminiferous epithelium in the rat. Annals of the New York Academy of Sciences 55 548-573.
33. Levallet J & Carreau S 1997 In vitro gene expression of aromatase in rat testicular cells. Comptes Rendus de l'Académie des Sciences III 320 123-129.
34. 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 58 919-926.
35. Levallet J, Mittre H, Delarue B & Carreau S 1998b Alternative splicing events in the coding region of the cytochrome P450 aromatase gene in male rat germ cells. Journal of Molecular Endocrinology 20 305-312.
36. Li X & Rahman N 2008 Impact of androgen/estrogen ratio: lessons from the aromatase over-expression mice. General and Comparative Endocrinology 159 1-9.
37. Lucas TF, 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. Biology of Reproduction 78 101-114.
38. Maruyama K, Endoh H, Sasaki-Iwaoka H, Kanou H, Shimaya E, Hashimoto S, Kato S & Kawashima H 1998 A novel isoform of rat estrogen receptor beta with 18 amino acid insertion in the ligand binding domain as a putative dominant negative regulator of estrogen action. Biochemical and Biophysical Research Communications 246 142-147.
39. McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, de Kretser DM, Pratis K & Robertson DM 2002 Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Progress in Hormone Research 57 149-179.
40. Mowa CN & Iwagana T 2001 Expression of estrogen receptor-alpha and -beta mRNAs in the male reproductive system of the rat as revealed by in situ hybridization. Journal of Molecular Endocrinology 26 165-174.
41. O'Donnell L, Robertson KM, Jones ME & Simpson ER 2001 Estrogen and spermatogenesis. Endocrine Reviews 22 289-318.
42. Papadopoulos V, Carreau S & Drosdowsky MA 1985 Effect of phorbol ester and phospholipase C on LH-stimulated steroidogenesis in purified rat Leydig cells. FEBS Letters 188 312-316. (Pubitemid 16249750)
43. Parvinen M 1982 Regulation of the seminiferous epithelium. Endocrine Reviews 3 404-417.
44. Pelletier G, Labrie C & Labrie F 2000 Localization of oestrogen receptor alpha, oestrogen receptor beta and androgen receptors in the rat reproductive organs. Journal of Endocrinology 165 359-370.
45. van Pelt AM, de Rooij DG, van der Burg B, van der Saag PT, Gustafsson JA & Kuiper GG 1999 Ontogeny of estrogen receptor-beta expression in rat testis. Endocrinology 140 478-483. (Pubitemid 29011194)
46. Petersen DN, Tkalcevic GT, Koza-Taylor PH, Turi TG & Brown TA 1998 Identification of estrogen receptor b2, a functional variant of estrogen receptor b expressed in normal rat tissues. Endocrinology 139 1082-1092.
47. Price RH Jr, Lorenzon N & Handa RJ 2000 Differential expression of estrogen receptor beta splice variants in rat brain: identification and characterization of a novel variant missing exon 4. Molecular Brain Research 80 260-268.
48. Prossnitz ER, Arterburn JB & Sklar LA 2007 GPR30: a G protein-coupled receptor for estrogens. Molecular and Cellular Endocrinology 265-266 138-142.
49. Robertson KM, O'Donnell L, Jones ME, Meachem SJ, Boon WC, Fisher CR, Graves KH, McLachlan RI & Simpson ER 1999 Impairment of spermatogenesis in mice lacking a functional aromatase (cyp19) gene. PNAS 96 7986-7991.
50. Saunders PTK, Maguire SM, Gaughan J & Millar MR 1997 Expression of estrogen receptor beta (ERβ) in multiple rat tissues visualized by immunohistochemistry. Journal of Endocrinology 154 R13-R16.
51. Saunders PTK, Fisher JS, Sharpe RM & Millar MR 1998 Expression of estrogen receptor beta (ER beta) occurs in multiple cell types, including some germ cells, in the rat testis. Journal of Endocrinology 156 13-17.
52. Schaussi D, Tiffoche C & Thieulant ML 2003 Regulation of the intronic promoter of rat estrogen receptor alpha gene, responsible for truncated estrogen receptor product-1 expression. Endocrinology 144 2845-2855. (Pubitemid 36819886)
53. Sethumadhavan K, Bellino FL & Thotakura NR 1991 Estrogen synthetase (aromatase). The cytochrome P-450 component of the human placental enzyme is a glycoprotein. Molecular and Cellular Endocrinology 78 25-32.
54. Shugrue PJ, Lane MV, Scrimo PJ & Merchenthaler I 1998 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.
55. Shupnik MA 2002 Oestrogen receptors, receptor variants and oestrogen actions in the hypothalamic-pituitary axis. Journal of Neuroendocrinology 14 85-94.
56. Silandre D, Delalande C, Durand P & Carreau S 2007 Three promoters PII, PI.f and PI.tr direct the expression of aromatase (cyp19) gene in male rat germ cells. Journal of Molecular Endocrinology 39 169-181.
57. Sirianni R, Chimento A, Ruggiero C, De Luca A, Lappano R, Ando S, Maggiolini M & Pezzi V 2008 The novel estrogen receptor, G protein-coupled receptor 30, mediates the proliferative effects induced by 17beta-estradiol on mouse spermatogonial GC-1 cell line. Endocrinology 149 5043-5051.
58. Skipper JK, Young LJ, Bergeron JM, Telzlaff MT, Osborn CT & Crews D 1993 Identification of an isoform of the estrogen receptor messenger RNA lacking exon four and present in the brain. PNAS 90 7172-7175.
59. Tena-Sempere M, Barreiro ML, Gonzalez LC, Gaytan F, Zhang FP, Caminos JE, Pinilla L, Casanueva FF, Dieguez C & Aguilar E 2002 Novel expression and functional role of ghrelin in rat testis. Endocrinology 143 717-725. (Pubitemid 34107228)
60. Tirado OM, Selva DM, Toran N, Suarez-Quian CA, Jansen M, McDonnell DP, Reventos J & Munell F 2004 Increased expression of estrogen receptor beta in pachytene spermatocytes after short-term methoxyacetic acid administration. Journal of Andrology 25 84-94.
61. Toppari J & Parvinen M 1985 In vitro differentiation of rat seminiferous tubular segments from defined stages of the epithelial cycle morphologic and immunolocalization analysis. Journal of Andrology 6 334-343.
62. Wing TY & Christensen AK 1982 Morphometric studies on rat seminiferous tubules. American Journal of Anatomy 65 13-25. (Pubitemid 12009521)