Differential hormonal regulation of estrogen receptors ERα and ERβ and androgen receptor expression in rat efferent ductules

Reproduction

Volumn 128, Issue 1, 2004, Pages 73-86

  Oliveira, Cleida A ^a,b   Mahecha, Germán A B ^b   Carnes, Kay ^a   Prins, Gail S ^c   Saunders, Philippa T K ^d   França, Luiz R ^b   Hess, Rex A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSITY OF ILLINOIS   (United States)

^d MRC Reproductive Biology Unit   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ANDROSTANOLONE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; STEROID HORMONE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CASTRATION; CONTROLLED STUDY; HORMONAL REGULATION; HORMONE SUBSTITUTION; MALE; MALE GENITAL SYSTEM FUNCTION; MODULATION; MORPHOMETRICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR DOWN REGULATION;

EID: 4043145690     PISSN: 14701626     EISSN: None     Source Type: Journal    
DOI: 10.1530/rep.1.00136     Document Type: Article

References (99)

1. Agarwal VR, Sinton CM, Liang C, Fisher C, German DC & Simpson ER 2000 Upregulation of estrogen receptors in the forebrain of aromatase knockout (ARKO) mice. Molecular and Cellular Endocrinology 162 9-16.
2. Atanassova N, McKinnell C, Williams K, Turner KJ, Fisher JS, Saunders PT, Millar MR & Sharpe RM 2001 Age-, cell- and region-specific immunoexpression of estrogen receptor alpha (but not estrogen receptor beta) during postnatal development of the epididymis and vas deferens of the rat and disruption of this pattern by neonatal treatment with diethylstilbestrol. Endocrinology 142 874-886.
3. Banu SK, Govindarajulu P & Aruldhas MM 2002 Testosterone and estradiol up-regulate androgen and estrogen receptors in immature and adult rat thyroid glands in vivo. Steroids 67 1007-1014.
4. Bao B, Kumar N, Karp RM, Garverick HA & Sundaram K 2000 Estrogen receptor-beta expression in relation to the expression of luteinizing hormone receptor and cytochrome p450 enzymes in rat ovarian follicles. Biology of Reproduction 63 1747-1755.
5. Barton MC & Shapiro DJ 1988 Transient administration of estradiol-17 beta establishes an autoregulatory loop permanently inducing estrogen receptor mRNA. PNAS 85 7119-7123.
6. Branham WS, Fishman R, Streck RD, Medlock KL, De George JJ & Sheehan DM 1996 ICI 182,780 inhibits endogenous estrogen-dependent rat uterine growth and tamoxifen-induced developmental toxicity. Biology of Reproduction 54 160-167.
7. Calandra RS, Blaquier JA, del Castillo EJ & Rivarola MA 1975 Androgen dependency of the androgen receptor in rat epididymis. Biochemical and Biophysical Research Communications 67 97-102.
8. Cho HW, Nie R, Carnes K, Zhou Q, Sharief NA & Hess RA 2003 The antiestrogen ICI 182,780 induces early effects on the adult male mouse reproductive tract and long-term decreased fertility without testicular atrophy. Reproductive Biology and Endocrinology 1 57.
9. Cotroneo MS, Wang J, Eltoum IA & Lamartiniere CA 2001 Sex steroid receptor regulation by genistein in the prepubertal rat uterus. Molecular and Cellular Endocrinology 173 135-145.
10. Couse JF & Korach KS 1998 Exploring the role of sex steroids through studies of receptor deficient mice. Journal of Molecular Medicine 76 497-511.
11. Danzo BJ, Cooper TG & Orgebin-Crist MC 1977 Androgen binding protein (ABP) in fluids collected from the rete testis and cauda epididymidis of sexually mature and immature rabbits and observations on morphological changes in the epididymis following ligation of the ductuli efferentes. Biology of Reproduction 17 64-77.
12. Derecka K, Zhang FP, Ziecik AJ & Huhtaniemi I 1999 Ontogeny of LH receptor gene expression in the pig reproductive tract. Journal of Reproduction and Fertility 115 365-372.
13. Dohle GR, Smit M & Weber RF 2003 Androgens and male fertility. World Journal of Urology 21 341-345.
14. Dukes M, Waterton JC & Wakeling AE 1993 Antiuterotrophic effects of the pure antioestrogen ICI 182,780 in adult female monkeys (Macaca nemestrina): quantitative magnetic resonance imaging. Journal of Endocrinology 138 203-210.
15. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P & Mark M 2000 Effect of single and compound knockouts of estrogen receptors α (ERα) and β (ERβ) on mouse reproductive phenotypes. Development 127 4277-4291.
16. Ebling FJ, Brooks AN, Cronin AS, Ford H & Kerr JB 2000 Estrogenic induction of spermatogenesis in the hypogonadal mouse. Endocrinology 141 2861-2869.
17. 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.
18. Fan X & Robaire B 1998 Orchidectomy induces a wave of apoptotic cell death in the epididymis. Endocrinology 139 2128-2136.
19. Fawcett DW & Hoffer AP 1979 Failure of exogenous androgen to prevent regression of the initial segments of the rat epididymis after efferent duct ligation or orchidectomy. Biology of Reproduction 20 162-181.
20. Fisher JS, Millar MR, Majdic G, Saunders PT, Fraser HM & Sharpe RM 1997 Immunolocalisation of oestrogen 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.
21. Fisher JS, Turner KJ, Brown D & Sharpe RM 1999 Effect of neonatal exposure to estrogenic compounds on development of the excurrent ducts of the rat testis through puberty to adulthood. Environmental Health Perspectives 107 397-405.
22. Gonzalez-Cadavid N, Vernet D, Fuentes Navarro A, Rodriguez JA, Swerdloff RS & Rajfer J 1993 Up-regulation of the levels of androgen receptor and its mRNA by androgens in smooth-muscle cells from rat penis. Molecular and Cellular Endocrinology 90 219-229.
23. Goyal HO & Hrudka F 1980 The resorptive activity in the bull efferent ductules - a morphological and experimental study. Andrologia 12 401-404.
24. Goyal HO & Williams CS 1988 The ductuli efferentes of the goat: a morphological study. Anatomical Record 220 58-67.
25. Goyal HO, Bartol FF, Wiley AA & Neff CW 1997 Immunolocalization of receptors for androgen and estrogen in male caprine reproductive tissues: unique distribution of estrogen receptors in efferent ductule epithelium. Biology of Reproduction 56 90-101.
26. Goyal HO, Bartol FF, Wiley AA, Khalil MK, Williams CS & Vig MM 1998 Regulation of androgen and estrogen receptors in male excurrent ducts of the goat: an immunohistochemical study. Anatomical Record 250 164-171.
27. Guo H, Cai CQ, Schroeder RA & Kuo PC 2001 Osteopontin is a negative feedback regulator of nitric oxide synthesis in murine macrophages. Journal of Immunology 166 1079-1086.
28. Hansen LA, Clulow J & Jones RC 1997 Perturbation of fluid reabsorption in the ductuli efferentes testis of the rat by testosterone propionate, 17β-oestradiol 3-benzoate, flutamide and tamoxifen. International Journal of Andrology 20 265-273.
29. Hess RA 2002 The efferent ductules: structure and functions. In The Epididymis: From Molecules to Clinical Practice, pp 49-80. Eds B Robaire & B Hinton. New York: Kluwer Academic/Plenum.
30. Hess RA, Bunick D, Lee KH, Bahr J, Taylor JA, Korach KS & Lubahn DB 1997a A role for oestrogens in the male reproductive system. Nature 390 509-512.
31. Hess RA, Gist DH, Bunick D, Lubahn DB, Farrell A, Bahr J, Cooke PS & Greene GL 1997b Estrogen receptor (alpha and beta) expression in the excurrent ducts of the adult male rat reproductive tract. Journal of Andrology 18 602-611.
32. Hess RA, Bunick D & Bahr J 2001 Oestrogen, its receptors and function in the male reproductive tract - a review. Molecular and Cellular Endocrinology 178 29-38.
33. Hess RA, Zhou Q & Nie R 2002 The role of estrogens in the endocrine and paracrine regulation of the efferent ductules, epididymis and vas deferens. In The Epididymis: From Molecules to Clinical Practice, pp 317-338. Eds B Robaire & B Hinton. New York: Kluwer Academic/Plenum.
34. Hess RA 2003 Estrogen in the adult male reproductive tract. A review. Reproductive Biology and Endocrinology 1 52.
35. Ilio KY & Hess RA 1994 Structure and function of the ductuli efferentes: a review. Microscopic Research and Technology 29 432-467.
36. Jackson GL, Kuehl D & Rhim TJ 1991 Testosterone inhibits gonadotropin-releasing hormone pulse frequency in the male sheep. Biology of Reproduction 45 188-194.
37. Janulis L, Hess RA, Bunick D, Nitta H, Janssen S, Asawa Y & Bahr JM 1996 Mouse epididymal sperm contain active P4 aromatase which decreases as sperm traverse the epididymis. Journal of Andrology 17 111-116.
38. Janulis L, Bahr JM, Hess RA, Janssen S, Osawa Y & Bunick D 1998 Rat testicular germ cells and epididymal sperm contain active P450 aromatase. Journal of Andrology 19 65-71.
39. Jeyaraj DA, Grossman G, Weaver C & Petrusz P 2002 Dynamics of testicular germ cell proliferation in normal mice and transgenic mice overexpressing rat androgen-binding protein: a flow cytometric evaluation. Biology of Reproduction 66 877-885.
40. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA & Smithies O 1998 Generation and reproductive phenotypes of mice lacking estrogen receptor beta. PNAS 95 15677-15682.
41. Lauber AH, Mobbs CV, Muramatsu M & Pfaff DW 1991 Estrogen receptor messenger RNA expression in rat hypothalamus as a function of genetic sex and estrogen dose. Endocrinology 129 3180-3186.
42. Lee KH, Hess RA, Bahr JM, Lubahn DB, Taylor J & Bunick D 2000 Estrogen receptor alpha has a functional role in the mouse rete testis and efferent ductules. Biology of Reproduction 63 1873-1880.
43. Lee KH, Finnigan-Bunick C, Bahr J & Bunick D 2001 Estrogen regulation of ion transporter messenger RNA levels in mouse efferent ductules are mediated differentially through estrogen receptor (ER) alpha and ERbeta. Biology of Reproduction 65 1534-1541.
44. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS & Smithies O 61993 Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. PNAS 90 11162-11166.
45. Lynch CS & Story AJ 2000 Dihydrotestosterone and estrogen regulation of rat brain androgen-receptor immunoreactivity. Physiology and Behavior 69 445-453.
46. McKinnell C, Atanassova N, Williams K, Fisher JS, Walker M, Turner KJ, Saunders TK & Sharpe RM 2001 Suppression of androgen action and the induction of gross abnormalities of the reproductive tract in male rats treated neonatally with diethylstilbestrol. Journal of Andrology 22 323-338.
47. Mansour MM, Machen MR, Tarleton BJ, Wiley AA, Wower J, Bartol FF & Goyal HO 2001 Expression and molecular characterization of estrogen receptor alpha messenger RNA in male reproductive organs of adult goats. Biology of Reproduction 64 1432-1438.
48. al-Matubsi HY, Fairclough RJ & Jenkin G 1998 Oestrogenic effects of ICI 182,780, a putative ant-oestrogen, on the secretion of oxytocin and prostaglandin F2 alpha during oestrous cycle in the intact ewe. Animal Reproduction Science 51 81-96.
49. Migliaccio A, Castoria G, Di Domenico M, de Falco A, Bilancio A, Lombardi M, Barone MV, Ametrano D, Zannini MS, Abbondanza C & Auricchio F 2000 Steroid-induced androgen receptor-oestradiol receptor beta-src complex triggers prostate cancer cell proliferation. EMBO Journal 19 5406-5417.
50. Miller BG, Wild J & Stone GM 1979 Effects of progesterone on the oestrogen-stimulated uterus: a comparative study of the mouse, guinea pig, rabbit and sheep. Australian Journal of Biological Sciences 32 549-560.
51. Morishima A, Grumbach MM, Simpson ER, Fisher C & Qin K 1995 Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. Journal of Clinical Endocrinology and Metabolism 80 3689-3698.
52. Munell F, Suarez-Quian CA, Selva DM, Tirado OM & Reventos J 2002 Androgen-binding protein and reproduction: where do we stand? Journal of Andrology 23 598-609.
53. Nie R, Zhou Q, Jassim E, Saunders PT & Hess RA 2002 Differential expression of estrogen receptors alpha and beta in the reproductive tracts of adult male dogs and cats. Biology of Reproduction 66 1161-1168.
54. Nielsen M, Bogh IB, Schmidt M & Greve T 2001 Immunohistochemical localization of estrogen receptor-alpha in sex ducts and gonads of newborn piglets. Histochemistry and Cell Biology 115 521-526.
55. Ochiai I, Matsuda KI, Nishi M, Ozawa H & Kawata M 2004 Imaging analysis of subcellular correlation of androgen receptor and estrogen receptor alpha in single living cells using GFP color variants. Molecular Endocrinology 18 26-42.
56. Oliveira CA, Carnes K, Franca LR & Hess RA 2001 Infertility and testicular atrophy in the antiestrogen-treated adult male rat. Biology of Reproduction 65 913-920.
57. Oliveira CA, Zhou Q, Carnes K, Nie R, Kuehl DE, Jackson GL, Franca LR, Nakai M & Hess RA 2002 ER function in the adult male rat: short- and long-term effects of the antiestrogen ICI 182,780 on the testis and efferent ductules, without changes in testosterone. Endocrinology 143 2399-2409.
58. Oliveira C, Nie R, Carnes K, Franca LR, Prins GS, Saunders PTK & Hess RA 2003 The antiestrogen ICI 182,780 decreases the expression of estrogen receptor-alpha but has no effect on estrogen receptor-beta and androgen receptor in rat efferent ductules Reproductive Biology and Endocrinology 1 75.
59. Panet-Raymond V, Gottlieb B, Beitel LK, Pinsky L & Trifiro MA 2000 Interactions between androgen and estrogen receptors and the effects on their transactivational properties. Molecular and Cellular Endocrinology 167 139-150.
60. Podesta EJ, Calandra RS, Rivarola MA & Blaquier JA 1975 The effect of castration and testosterone replacement on specific proteins and androgen levels of the rat epididymis. Endocrinology 97 399-405.
61. Preisler-Mashek MT, Solodin N, Stark BL, Tyriver MK & Alarid ET 2002 Ligand-specific regulation of proteasome-mediated proteolysis of estrogen receptor-alpha. American Journal of Physiology, Endocrinology and Metabolism 282 E891-E898.
62. Prins GS 1992 Neonatal estrogen exposure induces lobe-specific alterations in adult rat prostate androgen receptor expression. Endocrinology 130 3703-3714.
63. Prins GS & Birch L 1997 Neonatal estrogen exposure up-regulates estrogen receptor expression in the developing and adult rat prostate lobes. Endocrinology 138 1801-1809.
64. Prins G, Birch L & Greene G 1991 Androgen receptor localization in different cell types of the adult rat proslate. Endocrinology 129 3187-3199.
65. Prins GS, Marmer M, Woodham C, Chang W, Kuiper G, Gustafsson JA & Birch L 1998 Estrogen receptor-beta messenger ribonucleic acid ontogeny in the prostate of normal and neonatally estrogenized rats. Endocrinology 139 874-883.
66. Prins GS, Birch L, Couse JF, Choi I, Katzenellenbogen B & Korach KS 2001 Estrogen imprinting of the developing prostate gland is mediated through stromal estrogen receptor alpha: studies with alphaERKO and betaERKO mice. Cancer Research 61 6089-6097.
67. Quarmby VE, Yarbrough WG, Lubahn DB, French FS & Wilson EM 1990 Autologous down-regulation of androgen receptor messenger ribonucleic acid. Molecular Endocrinology 4 22-28.
68. Rivas A, Fisher JS, Mckinnell C, Atanassova N & Sharpe RM 2002 Induction of reproductive tract developmental abnormalities in the male rat by lowering androgen production or action in combination with a low dose of diethylstilbestrol: evidence for importance of the androgen-estrogen balance. Endocrinology 143 4797-4808.
69. Rivas A, Mckinnell C, Fisher JS, Atanassova N, Williams K & Sharpe RM 2003 Neonatal co-administration of testosterone with diethylstilbestrol prevents diethylstilbestrol induction of most reproductive tract abnormalities in male rats. Journal of Andrology 24 557-567.
70. Robaire B & Viger RS 1995 Regulation of epididymal epithelial cell functions. Biology of Reproduction 52 226-236.
71. 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 (cyp 19) gene. PNAS 96 7986-7991.
72. Roselli CE & Resko JA 1984 Androgens regulate brain aromatase activity in adult male rats through a receptor mechanism. Endocrinology 114 2183-2189.
73. Roselli CE, West NB & Brenner RM 1991 Androgen receptor and 5 alpha-reductase activity in the ductull efferentes and epididymis of adult rhesus macaques. Biology of Reproduction 44 739-745.
74. Rosenfeld CS, Ganjam VK, Taylor JA, Yuan X, Stiehr JR, Hardy MP & Lubahn DB 1998 Transcription and translation of estrogen receptor-beta in the male reproductive tract of estrogen receptor-alpha knock-out and wild-type mice. Endocrinology 139 2982-2987.
75. Rosner W, Hryb DJ, Khan MS, Nakhla AM & Romas NA 1998 Androgens, estrogens, and second messengers. Steroids 63 278-281.
76. Sar M, Lubahn DB, French FS & Wilson EM 1990 Immunohistochemical localization of the androgen receptor in rat and human tissues. Endocrinology 127 3180-3186.
77. Saunders PT, Millar MR, Williams K, Macpherson S, Harkiss D, Anderson RA, Orr B, Groome NP, Scobie G & Fraser HM 2000 Differential expression of estrogen receptor-alpha and -beta and androgen receptor in the ovaries of marmosets and humans. Biology of Reproduction 63 1098-1105.
78. Saunders PT, Sharpe RM, Williams K, Macpherson S, Urquart H, Irvine DS & Millar MR 2001 Differential expression of oestrogen receptor alpha and beta proteins in the testes and male reproductive system of human and non-human primates. Molecular Human Reproduction 7 227-236.
79. Schleicher G, Drews U, Stumpf WE & Sar M 1984 Differential distribution of dihydrotestosterone and estradiol binding sites in the epididymis of the mouse. An autoradiographic study. Histochemistry 81 139-147.
80. Shughrue 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.
81. Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB & Korach KS 1994 Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. New England Journal of Medicine 331 1056-1061.
82. Stone GM, McCaffery C & Miller BG 1982 Effects of progesterone on nuclear and cytosol steroid receptor levels in the oestrogen-stimulated uterus: comparison of the sheep and mouse. Australian Journal of Biological Sciences 35 403-415.
83. Tarleton BJ, Wiley AA & Bartol FF 1999 Endometrial development and adenogenesis in the neonatal pig: effects of estradiol valerate and the antiestrogen ICI 182,780. Biology of Reproduction 61 253-263.
84. Tena-Sempere M, Navarro J, Pinilla L, Gonzalez LC, Huhtaniemi I & Aguilar E 2000 Neonatal exposure to estrogen differentially alters estrogen receptor alpha and beta mRNA expression in rat testis during postnatal development. Journal of Endocrinology 165 345-357.
85. Thomas EJ, Walton PL, Thomas NM & Dowsett M 1994 The effects of ICI 182,780, a pure anti-oestrogen, on the hypothalamic-pituitary-gonadal axis and on endometrial proliferation in pre-menopausal women. Human Reproduction 9 1991-1996.
86. 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.
87. Turner KJ, Morley M, Atanassova N, Swanston ID & Sharpe RM 2000 Effect of chronic administration of an aromatase inhibitor to adult male rats on pituitary and testicular function and fertility. Journal of Endocrinology 164 225-238.
88. Turner KJ, Morley M, MacPherson S, Millar MR, Wilson JA, Sharpe RM & Saunders PT 2001 Modulation of gene expression by androgen and oestrogens in the testis and prostate of the adult rat following androgen withdrawal. Molecular and Cellular Endocrinology 178 73-87.
89. Vreeburg JTM 1975 Distribution of testosterone and 5α-dihydrotestosterone in rat epididymis and their concentrations in efferent duct fluid. Journal of Endocrinology 67 203-210.
90. Wakeling AE, Bowler J, Wakeling AE, Dukes M & Bowler J 1991 Development of novel oestrogen-receptor antagonists. A potent, specific, pure antiestrogen with clinical potential. Biochemical Society Transactions 19 899-901.
91. Wiszniewska B 2002 Primary culture of the rat epididymal epithelial cells as a source of oestrogen. Andrologia 34 180-187.
92. Woodham C, Birch L & Prins GS 2003 Neonatal estrogen down-regulates prostatic androgen receptor through a proteosome-mediated protein degradation pathway. Endocrinology 144 4841-4850.
93. Yeap BB, Krueger RG & Leedman PJ 1999 Differential posttranscriptional regulation of androgen receptor gene expression by androgen in prostate and breast cancer cells. Endocrinology 140 3282-3291.
94. Yeh S, Miyamoto H, Shima H & Chang C 1998 From estrogen to androgen receptor: a new pathway for sex hormones in prostate. PNAS 95 5527-5532.
95. Zhou Q, Clarke L, Nie R, Carnes K, Lai LW, Lien YH, Verkman A, Lubahn D, Fisher JS, Katzenellenbogen BS & Hess RA 2001 a Estrogen action and male fertility: roles of the sodium/hydrogen exchanger-3 and fluid reabsorption in reproductive tract function. PNAS 98 14132-14137.
96. Zhou S, Zilberman Y, Wassermann K, Bain SD, Sadovsky Y & Gazit D 2001b Estrogen modulates estrogen receptor alpha and beta expression, osteogenic activity, and apoptosis in mesenchymal stem cells (MSCS) of osteoporotic mice. Journal of Cellular Biochemistry. Supplement 36 144-155.
97. Zhou Q, Nie R, Prins GS, Saunders PT, Katzenellenbogen BS & Hess RA 2002 Localization of androgen and estrogen receptors in adult male mouse reproductive tract. Journal of Andrology 23 870-881.
98. Zhu LJ, Hardy MP, Inigo IV, Huhtaniemi I, Bardin CW & Moo-Young AJ 2000 Effects of androgen on androgen receptor expression in rat testicular and epididymal cells: a quantitative immunohistochemical study. Biology of Reproduction 63 368-376.
99. Zou K & Ing NH 1998 Oestradiol up-regulates oestrogen receptor, cyclophilin, and glyceraldehyde phosphate dehydrogenase mRNA concentrations in endometrium, but down-regulates them in liver. Journal of Steroid Biochemistry and Molecular Biology 64 231-237.