Differential response of Leydig cells in expressing 11β-HSD type I and cytochrome P450 aromatase in male rats subjected to corticosterone deficiency

Molecular and Cellular Endocrinology

Volumn 311, Issue 1-2, 2009, Pages 18-23

  Parthasarathy, Chandrakesan ^a   Yuvaraj, Sambandam ^a   Ilangovan, Ramachandran ^a   Janani, Panneerselvam ^b   Kanagaraj, Palaniyandi ^a   Balaganesh, Muthusamy ^a   Natarajan, Bhaskaran ^a   Sittadjody, Sivanandane ^a   Balasubramanian, Karundevi ^a  

^a UNIVERSITY OF MADRAS   (India)

^b PRESIDENCY COLLEGE   (India)

Author keywords

11 HSD; Aromatase; Corticosterone deficiency; Leydig cell; mRNA expression

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; AROMATASE; CORTICOSTERONE; ESTRADIOL; MESSENGER RNA; METYRAPONE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE DEFICIENCY; ENZYME ACTIVITY; ENZYME ANALYSIS; ESTRADIOL BLOOD LEVEL; GENE EXPRESSION; HORMONE DEFICIENCY; LEYDIG CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEROIDOGENESIS; TESTOSTERONE BLOOD LEVEL;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ANIMALS; AROMATASE; CORTICOSTERONE; ESTRADIOL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LEYDIG CELLS; MALE; METYRAPONE; RATS; RATS, WISTAR; RNA, MESSENGER; TESTOSTERONE;

EID: 69249230874     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.06.014     Document Type: Article

References (58)

1. Abney T.O. The potential roles of estrogens in regulating Leydig cell development and function: a review. Steroids 64 (1999) 610-617
2. Aldred L.F., and Cooke B.A. The effect of cell damage on the density and steroidogenic capacity of rat testis Leydig cells, using an NADH exclusion test for determination of viability. J. Steroid Biochem. 18 (1983) 411-414
3. Annane D., Maxime V., Ibrahim F., Alvarez J.C., Abe E., and Boudou P. Diagnosis of adrenal insufficiency in severe sepsis and septic shock. Am. J. Respir. Crit. Care Med. 174 (2006) 1319-1326
4. Badrinarayanan R., Rengarajan S., Nithya P., and Balasubramanian K. Corticosterone impairs the mRNA expression and activity of 3beta- and 17beta-hydroxysteroid dehydrogenases in adult rat Leydig cells. Biochem. Cell Biol. 84 (2006) 745-754
5. Banhegyi G., Benedetti A., Fulceri R., and Senesi S. Cooperativity between 11beta-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase in the lumen of the endoplasmic reticulum. J. Biol. Chem. 279 (2004) 27017-27021
6. Baram T.Z., and Schultz L. Fetal and maternal levels of corticosterone and ACTH after pharmacological adrenalectomy. Life Sci. 47 (1990) 485-489
7. Berneis K., Staub J.J., Gessler A., Meier C., Girard J., and Muller B. Combined stimulation of adrenocorticotropin and compound-S by single dose metyrapone test as an outpatient procedure to assess hypothalamic-pituitary-adrenal function. J. Clin. Endocrinol. Metab. 87 (2002) 5470-5475
8. Betterle C., Dal Pra C., Mantero F., and Zanchetta R. Autoimmune adrenal insufficiency and autoimmune polyendocrine syndromes: autoantibodies, autoantigens, and their applicability in diagnosis and disease prediction. Endocr. Rev. 23 (2002) 327-364
9. Breen K.M., and Karsch F.J. New insights regarding glucocorticoids, stress and gonadotropin suppression. Front. Neuroendocrinol. 27 (2006) 233-245
10. Bujalska I.J., Draper N., Michailidou Z., Tomlinson J.W., White P.C., Chapman K.E., Walker E.A., and Stewart P.M. Hexose-6-phosphate dehydrogenase confers oxo-reductase activity upon 11 beta-hydroxysteroid dehydrogenase type 1. J. Mol. Endocrinol. 34 (2005) 675-684
11. 450 gene expression in human testicular and ovarian sex cord tumors, as well as in normal fetal and adult gonads. J. Clin. Endocrinol. Metab. 78 (1994) 1616-1621
12. Calis M., Gokce C., Ates F., Ulker S., Izgi H.B., Demir H., Kirnap M., Sofuoglu S., Durak A.C., Tutus A., and Kelestimur F. Investigation of the hypothalamo-pituitary-adrenal axis (HPA) by 1 microg ACTH test and metyrapone test in patients with primary fibromyalgia syndrome. J. Endocrinol. Invest. 27 (2004) 42-46
13. Carreau S., Bilinska B., and Levallet J. Male germ cells. A new source of estrogens in the mammalian testis. Ann. Endocrinol. 59 (1998) 79-92
14. Carreau S., Delalande C., Silandre D., Bourguiba S., and Lambard S. Aromatase and estrogen receptors in male reproduction. Mol. Cell. Endocrinol. 246 (2006) 65-68
15. Carreau S., Lambard S., Delalande C., Denis-Galeraud I., Bilinska B., and Bourguiba S. Aromatase expression and role of estrogens in male gonad: a review. Reprod. Biol. Endocrinol. 1 (2003) 35
16. Etches R.J. A radioimmuno assay for corticosterone and its application to the measurement of stress in poultry. Steroids 28 (1976) 763-774
17. Gao H.B., Ge R.S., Lakshmi V., Marandici A., and Hardy M.P. Hormonal regulation of oxidative and reductive activities of 11b-hydroxysteroid dehydrogenase in rat Leydig cells. Endocrinology 138 (1997) 156-161
18. Gao H.B., Shan L.X., Monder C., and Hardy M.P. Suppression of endogenous corticosterone levels in vivo increases the steroidogenic capacity of purified rat Leydig cells in vitro. Endocrinology 137 (1996) 1714-1718
19. Ge R.S., Dong Q., Niu E.M., Sottas C.M., Hardy D.O., Catterall J.F., Latif S.A., Morris D.J., and Hardy M.P. 11β-Hydroxysteroid dehydrogenase 2 in rat Leydig cells: its role in blunting glucocorticoid action at physiological levels of substrate. Endocrinology 146 (2005) 2657-2664
20. Ge R.S., Gao H.B., Nacharaju V.L., Gunsalus G.L., and Hardy M.P. Identification of a kinetically distinct activity of 11beta-hydroxysteroid dehydrogenase in rat Leydig cells. Endocrinology 138 (1997) 2435-2442
21. Genissel C., and Carreau S. Regulation of the aromatase gene expression in mature rat Leydig cells. Mol. Cell. Endocrinol. 178 (2001) 141-146
22. Genti-Raimondi S., Alvarez C.I., Patrito L.C., and Flury A. Low aromatase activity in microsomes from complete hydatidiform mole. J. Clin. Endocrinol. Metab. 76 (1993) 108-111
23. Hardy M.P., and Ganjam V.K. Stress, 11b-HSD, and Leydig cell function. J. Androl. 18 (1997) 475-479
24. Hardy M.P., Gao H.B., Dong Q., Ge R., Wang Q., Chai W.R., Feng X., and Sottas C. Stress hormone and male reproductive function. Cell Tissue Res. 322 (2005) 147-153
25. Hardy M.P., Sottas C.M., Ge R., McKittrick C.R., Tamashino K.L., McEwen B.S., Haider S.G., Markham C.M., Blanchard R.J., Blanchard D.C., and Sakai R.R. Trends or reproductive hormones in male rats during psychosocial stress; role of glucocorticoid metabolism in behavioral dominance. Biol. Reprod. 67 (2002) 1750-1755
26. Hess R.A. Estrogen in the adult male reproductive tract: a review. Reprod. Biol. Endocrinol. 1 (2003) 52
27. Hewitt K.N., Walker E.A., and Stewart P.M. Minireview: hexose-6-phosphate dehydrogenase and redox control of 11{beta}-hydroxysteroid dehydrogenase type 1 activity. Endocrinology 146 (2005) 2539-2543
28. Lambard S., Silandre D., Delalande C., Denis-Galeraud I., Bourguiba S., and Carreau S. Aromatase in testis: expression and role in male reproduction. J. Steroid Biochem. Mol. Biol. 95 (2005) 63-69
29. Lescoat G., Lescoay D., and Garnier D.H. Influence of adrenalectomy on maturation of gonadotropin function in the male rat. J. Endocrinol. 95 (1982) 1-6
30. Levallet J., and Carreau S. In vitro gene expression of aromatase in rat testicular cells C. R. Acad. Sci. III 320 (1997) 123-129
31. McKnight S.L., Lane M.D., and Gluecksohn-Waelsch S. Is CCAAT/enhancer-binding protein a central regulator of energy metabolism?. Genes Dev. 3 (1989) 2021-2024
32. Moisan M.P., Edwards C.R., and Seckl J.R. Differential promoter usage by the rat 11 beta-hydroxysteroid dehydrogenase gene. Mol. Endocrinol. 6 (1992) 1082-1087
33. Monder C., and Lakshmi V. Corticosteroid 11 beta-dehydrogenase of rat tissues: immunological studies. Endocrinology 126 (1990) 2435-2443
34. Monder C., Miroff Y., Marandici A., and Hardy M.P. 11β-Hydroxysteroid dehydrogenase alleviates glucocorticoid-mediated inhibition of steroidogenesis in rat Leydig cells. Endocrinology 134 (1994) 1199-1204
35. Monder C., and White P.C. 11 beta-hydroxysteroid dehydrogenase. Vitam. Horm. 47 (1993) 187-271
36. Nair N., and Bedwal R.S. Metallothionein in male reproductive organs of adrenalectomized and hydrocortisone-treated Wistar rats. Indian J. Exp. Biol. 42 (2004) 288-291
37. New K.H., Norhazlina A.W., Hamid A., Morat P.B., and Khalid B.A. In vivo effects of stress. ACTH and corticosterone on testicular 11beta-hydroxysteroid dehydrogenase oxidative activity in rats and the possible mechanism of actions. Exp. Clin. Endocrinol. Diabetes 108 (2000) 369-377
38. Oaks M.K., and Raff H. Differentiation of the expression of aldosterone synthase and 11β-hydroxylase mRNA in the rat adrenal cortex by reverse transcriptase-polymerase chain reaction. J. Steroid Biochem. Mol. Biol. 54 (1995) 193-199
39. O'Donnell L., Robertson K.M., Jones M.E., and Simpson E.R. Estrogen and spermatogenesis. Endocr. Rev. 22 (2001) 289-318
40. Parthasarathy C., and Balasubramanian K. Assessment of in vitro effects of metyrapone on Leydig cell steroidogenesis. Steroids 73 (2008) 328-338
41. Parthasarathy C., and Balasubramanian K. Differential effect of corticosterone deficiency on the expression of LH, prolactin and insulin receptors on rat Leydig cells. Mol. Cell. Endocrinol. 285 (2008) 34-42
42. Parthasarathy C., and Balasubramanian K. Effect of corticosterone deficiency and its replacement on Leydig cell steroidogenesis. J. Cell. Biochem. 104 (2008) 1671-1683
43. Parthasarathy C., Yuvaraj S., Sivakumar R., Sankar B.R., and Balasubramanian K. Metyrapone-induced corticosterone deficiency impairs glucose oxidation and steroidogenesis in Leydig cells of adult albino rats. Endocr. J. 49 (2002) 405-412
44. Ramos R.A., Nishio Y., Maiyar A.C., Simon K.E., Ridder C.C., Ge Y., and Firestone G.L. Glucocorticoid-stimulated CCAAT/enhancer-binding protein alpha expression is required for steroid-induced G1 cell cycle arrest of minimal-deviation rat hepatoma cells. Mol. Cell. Biol. 16 (1996) 5288-5301
45. Rengarajan S., and Balasubramanian K. Corticosterone has direct inhibitory effect on the expression of peptide hormone receptors, 11 beta-HSD and glucose oxidation in cultured adult rat Leydig cells. Mol. Cell. Endocrinol. 279 (2007) 52-62
46. Rengarajan S., and Balasubramanian K. Corticosterone induces steroidogenic lesion in cultured adult rat Leydig cells by reducing the expression of star protein and steroidogenic enzymes. J. Cell. Biochem. 103 (2008) 1472-1487
47. Rigaudiere N., Loubassou S., Grizard G., and Boucher D. Characterization of insulin binding and comparative action of insulin and insulin-like growth factor-I on purified Leydig cells from the adult rat. Int. J. Androl. 11 (1988) 165-178
48. Sankar B.R., Maran R.R., Sivakumar R., Govindarajulu P., and Balasubramanian K. Chronic administration of corticosterone impairs LH signal transduction and steroidogenesis in rat Leydig cells. J. Steroid Biochem. Mol. Biol. 72 (2000) 155-162
49. Seminara S.B., Achermann J.C., Genel M., Jameson J.L., and Crowley W.F. X-linked adrenal hypoplasia congenita: a mutation in DAX1 expands the phenotypic spectrum in males and females. J. Clin. Endocrinol. Metab. 84 (1999) 4501-4509
50. Shan L.X., Zhu L.J., Bardin W., and Hardy M.P. Quantitative analysis of androgen receptor messenger ribonucleic acid in developing Leydig cells and Sertoli cells by in situ hybridization. Endocrinology 136 (1995) 3856-3862
51. Sierens J.E., Sneddon S.F., Collins F., Millar M.R., and Saunders P.T. Estrogens in testis biology. Ann. N.Y. Acad. Sci. 1061 (2005) 65-76
52. Sugino Y., Usui T., Okubo K., Nagahama K., Takahashi T., Okuno H., Hatayama H., Ogawa O., Shimatsu A., and Nishiyama H. Genotyping of congenital adrenal hyperplasia due to 21-hydroxylase deficiency presenting as male infertility: case report and literature review. J. Assist. Reprod. Genet. 23 (2006) 377-380
53. Tomlinson J.W., Walker E.A., Bujalska I.J., Draper N., Lavery G.G., Cooper M.S., Hewison M., and Stewart P.M. 11beta-hydroxysteroid dehydrogenase type 1: a tissue-specific regulator of glucocorticoid response. Endocr. Rev. 25 (2004) 831-866
54. Valli G., Sudha S., Ravi Sankar B., Govindarajulu P., and Srinivasan N. Altered corticosterone status impairs steroidogenesis in the granulosa and thecal cells of Wistar rats. J. Steroid Biochem. Mol. Biol. 73 (2000) 153-158
55. Vierhapper H., Nowotay P., and Waldhause W. Production rates of testosterone in patients with Cushing's syndrome. Metabolism 49 (2000) 229-231
56. Walker V.R., and Korach K.S. Estrogen receptor knockout mice as a model for endocrine research. ILAR J. 45 (2004) 455-461
57. Williams L.J., Lyons V., MacLeod I., Rajan V., Darlington G.J., Poli V., Seckl J.R., and Chapman K.E. C/EBP regulates hepatic transcription of 11beta-hydroxysteroid dehydrogenase type 1. A novel mechanism for cross-talk between the C/EBP and glucocorticoid signaling pathways. J. Biol. Chem. 275 (2000) 30232-30239
58. Zirilli L., Rochira V., Diazzi C., Caffagni G., and Carani C. Human models of aromatase deficiency. J. Steroid Biochem. Mol. Biol. 109 (2008) 212-218