Effects of apigenin on steroidogenesis and steroidogenic acute regulatory gene expression in mouse Leydig cells

Journal of Nutritional Biochemistry

Volumn 22, Issue 3, 2011, Pages 212-218

  Li, Wei ^a   Pandey, Akhilesh K ^a   Yin, Xiangling ^b   Chen, Jau Jiin ^c   Stocco, Douglas M ^b   Grammas, Paula ^a   Wang, XingJia ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^c LAMAR UNIVERSITY   (United States)

Author keywords

Apigenin; Flavonoid; StAR; Steroidogenesis; Testosterone

Indexed keywords

APIGENIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOOXYGENASE 2; MESSENGER RNA; NUCLEAR RECEPTOR DAX 1; PROTEIN KINASE C; STEROID HORMONE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; THROMBOXANE A2 RECEPTOR; THROMBOXANE SYNTHASE;

ANIMAL CELL; ARTICLE; CELL AGING; GENE EXPRESSION; LEYDIG CELL; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEROIDOGENESIS;

ANIMALS; APIGENIN; CELL LINE, TUMOR; CYCLIC AMP; CYCLOOXYGENASE 2; DAX-1 ORPHAN NUCLEAR RECEPTOR; GENE EXPRESSION REGULATION; HUMANS; LEYDIG CELLS; MALE; MICE; MICE, INBRED C3H; PHOSPHOPROTEINS; PROSTAGLANDIN H2; RECEPTORS, THROMBOXANE A2, PROSTAGLANDIN H2; SIGNAL TRANSDUCTION; STEROIDS; THROMBOXANE-A SYNTHASE;

EID: 79951681219     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2010.01.004     Document Type: Article

References (49)

1. Feldman H.A., Longcope C., Derby C.A., Johannes C.B., Araujo A.B., Coviello A.D., et al. Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts male aging study. J Clin Endocrinol Metab 2002, 87:589-598.
2. Harman S.M., Metter E.J., Tobin J.D., Pearson J., Blackman M.R. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore longitudinal study of aging. J Clin Endocrinol Metab 2001, 86:724-731.
3. Kaufman J.M., Vermeulen A. The decline of androgen levels in elderly men and its clinical and therapeutic implications. Endocr Rev 2005, 26:833-876.
4. Matsumoto A.M. Andropause: clinical implications of the decline in serum testosterone levels with aging in men. J Gerontol A Biol Sci Med Sci 2002, 57:M76-M99.
5. Vermeulen A. Andropause. Maturitas 2000, 34:5-15.
6. Hogervorst E., Williams J., Budge M., Barnetson L., Combrinck M., Smith A.D. Serum total testosterone is lower in men with Alzheimer's disease. Neuro Endocrinol Lett 2001, 22:163-168.
7. Moffat S.D., Zonderman A.B., Metter E.J., Kawas C., Blackman M.R., Harman S.M., et al. Free testosterone and risk for Alzheimer disease in older men. Neurology 2004, 62:188-193.
8. Ramsden M., Nyborg A.C., Murphy M.P., Chang L., Stanczyk F.Z., Golde T.E., et al. Androgens modulate beta-amyloid levels in male rat brain. J Neurochem 2003, 87:1052-1055.
9. Gouras G.K., Xu H., Gross R.S., Greenfield J.P., Hai B., Wang R., et al. Testosterone reduces neuronal secretion of Alzheimer's beta-amyloid peptides. Proc Natl Acad Sci U S A 2000, 97:1202-1205.
10. Papasozomenos S., Shanavas A. Testosterone prevents the heat shock-induced overactivation of glycogen synthase kinase-3 beta but not of cyclin-dependent kinase 5 and c-jun nh2-terminal kinase and concomitantly abolishes hyperphosphorylation of tau: implications for Alzheimer's disease. Proc Natl Acad Sci U S A 2002, 99:1140-1145.
11. Rosario E.R., Pike C.J. Androgen regulation of beta-amyloid protein and the risk of Alzheimer's disease. Brain Res Rev 2008, 57:444-453.
12. Miller W.L. Molecular biology of steroid hormone synthesis. Endocr Rev 1988, 9:295-318.
13. Wang X., Stocco D.M. The decline in testosterone biosynthesis during male aging: a consequence of multiple alterations. Mol Cell Endocrinol 2005, 238:1-7.
14. Chen H., Hardy M.P., Huhtaniemi I., Zirkin B.R. Age-related decreased Leydig cell testosterone production in the brown Norway rat. J Androl 1994, 15:551-557.
15. Stocco D.M., Clark B.J. Regulation of the acute production of steroids in steroidogenic cells. Endocr Rev 1996, 17:221-244.
16. Clark B.J., Wells J., King S.R., Stocco D.M. The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in ma-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (star). J Biol Chem 1994, 269:28314-28322.
17. Lin D., Sugawara T., Strauss J.F., Clark B.J., Stocco D.M., Saenger P., et al. Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 1995, 267:1828-1831.
18. Wang X.J., Liu Z., Eimerl S., Timberg R., Weiss A.M., Orly J., et al. Effect of truncated forms of the steroidogenic acute regulatory protein on intramitochondrial cholesterol transfer. Endocrinology 1998, 139:3903-3912.
19. Stocco D.M. Star protein and the regulation of steroid hormone biosynthesis. Annu Rev Physiol 2001, 63:193-213.
20. Leers-Sucheta S., Stocco D.M., Azhar S. Down-regulation of steroidogenic acute regulatory (star) protein in rat Leydig cells: implications for regulation of testosterone production during aging. Mech Ageing Dev 1999, 107:197-203.
21. Luo L., Chen H., Zirkin B.R. Leydig cell aging: steroidogenic acute regulatory protein (star) and cholesterol side-chain cleavage enzyme. J Androl 2001, 22:149-156.
22. Culty M., Luo L., Yao Z.X., Chen H., Papadopoulos V., Zirkin B.R. Cholesterol transport, peripheral benzodiazepine receptor, and steroidogenesis in aging Leydig cells. J Androl 2002, 23:439-447.
23. Wang X.J., Dyson M.T., Jo Y., Stocco D.M. Inhibition of cyclooxygenase-2 activity enhances steroidogenesis and steroidogenic acute regulatory gene expression in ma-10 mouse Leydig cells. Endocrinology 2003, 144:3368-3375.
24. Wang X., Shen C.L., Dyson M.T., Eimerl S., Orly J., Hutson J.C., et al. Cyclooxygenase-2 regulation of the age-related decline in testosterone biosynthesis. Endocrinology 2005, 146:4202-4208.
25. Pandey A.K., Yin X., Schiffer R.B., Hutson J.C., Stocco D.M., Grammas P., et al. Involvement of the thromboxane a2 receptor in the regulation of steroidogenic acute regulatory gene expression in murine Leydig cells. Endocrinology 2009, 150:3267-3273.
26. Wang X., Yin X., Schiffer R.B., King S.R., Stocco D.M., Grammas P. Inhibition of thromboxane a synthase activity enhances steroidogenesis and steroidogenic acute regulatory gene expression in ma-10 mouse Leydig cells. Endocrinology 2008, 149:851-857.
27. Hales K.H., Diemer T., Ginde S., Shankar B.K., Roberts M., Bosmann H.B., et al. Diametric effects of bacterial endotoxin lipopolysaccharide on adrenal and Leydig cell steroidogenic acute regulatory protein. Endocrinology 2000, 141:4000-4012.
28. Ascoli M. Characterization of several clonal lines of cultured Leydig tumor cells: gonadotropin receptors and steroidogenic responses. Endocrinology 1981, 108:88-95.
29. Resko J.A., Norman R.L., Niswender G.D., Spies H.G. The relationship between progestins and gonadotropins during the late luteal phase of the menstrual cycle in rhesus monkeys. Endocrinology 1974, 94:128-135.
30. Hutson J.C., Garner C.W., Doris P.A. Purification and characterization of a lipophilic factor from testicular macrophages that stimulates testosterone production by Leydig cells. J Androl 1996, 17:502-508.
31. Townson D.H., Wang X.J., Keyes P.L., Kostyo J.L., Stocco D.M. Expression of the steroidogenic acute regulatory protein in the corpus luteum of the rabbit: dependence upon the luteotropic hormone, estradiol-17 beta. Biol Reprod 1996, 55:868-874.
32. Caron K.M., Ikeda Y., Soo S.C., Stocco D.M., Parker K.L., Clark B.J. Characterization of the promoter region of the mouse gene encoding the steroidogenic acute regulatory protein. Mol Endocrinol 1997, 11:138-147.
33. Rao R.M., Jo Y., Leers-Sucheta S., Bose H.S., Miller W.L., Azhar S., et al. Differential regulation of steroid hormone biosynthesis in R2C and MA-10 Leydig tumor cells: role of sr-b1-mediated selective cholesteryl ester transport. Biol Reprod 2003, 68:114-121.
34. Beecher G.R. Overview of dietary flavonoids: nomenclature, occurrence and intake. J Nutr 2003, 133:3248S-3254S.
35. Chen Y.T., Zheng R.L., Jia Z.J., Ju Y. Flavonoids as superoxide scavengers and antioxidants. Free Radic Biol Med 1990, 9:19-21.
36. Lapidot T., Walker M.D., Kanner J. Antioxidant and prooxidant effects of phenolics on pancreatic beta-cells in vitro. J Agric Food Chem 2002, 50:7220-7225.
37. Cardenas M., Marder M., Blank V.C., Roguin L.P. Antitumor activity of some natural flavonoids and synthetic derivatives on various human and murine cancer cell lines. Bioorg Med Chem 2006, 14:2966-2971.
38. Menon L.G., Kuttan R., Kuttan G. Inhibition of lung metastasis in mice induced by b16f10 melanoma cells by polyphenolic compounds. Cancer Lett 1995, 95:221-225.
39. Cho H., Yun C.W., Park W.K., Kong J.Y., Kim K.S., Park Y., et al. Modulation of the activity of pro-inflammatory enzymes, cox-2 and inos, by chrysin derivatives. Pharmacol Res 2004, 49:37-43.
40. Ferrandiz M.L., Alcaraz M.J. Anti-inflammatory activity and inhibition of arachidonic acid metabolism by flavonoids. Agents Actions 1991, 32:283-288.
41. Guerrero J.A., Navarro-Nunez L., Lozano M.L., Martinez C., Vicente V., Gibbins J.M., et al. Flavonoids inhibit the platelet txa(2) signalling pathway and antagonize txa(2) receptors (tp) in platelets and smooth muscle cells. Br J Clin Pharmacol 2007, 64:133-144.
42. Jana K., Yin X., Schiffer R.B., Chen J.J., Pandey A.K., Stocco D.M., et al. Chrysin, a natural flavonoid enhances steroidogenesis and steroidogenic acute regulatory protein gene expression in mouse Leydig cells. J Endocrinol 2008, 197:315-323.
43. Woo K.J., Jeong Y.J., Inoue H., Park J.W., Kwon T.K. Chrysin suppresses lipopolysaccharide-induced cyclooxygenase-2 expression through the inhibition of nuclear factor for il-6 (nf-il6) DNA-binding activity. FEBS Lett 2005, 579:705-711.
44. Zazopoulos E., Lalli E., Stocco D.M., Sassone-Corsi P. DNA binding and transcriptional repression by DAX-1 blocks steroidogenesis. Nature 1997, 390:311-315.
45. Dhawan K., Kumar S., Sharma A. Beneficial effects of chrysin and benzoflavone on virility in 2-year-old male rats. J Med Food 2002, 5:43-48.
46. Brown G.A., Vukovich M.D., Martini E.R., Kohut M.L., Franke W.D., Jackson D.A., et al. Endocrine and lipid responses to chronic androstenediol-herbal supplementation in 30 to 58 year old men. J Am Coll Nutr 2001, 20:520-528.
47. Gambelunghe C., Rossi R., Sommavilla M., Ferranti C., Rossi R., Ciculi C., et al. Effects of chrysin on urinary testosterone levels in human males. J Med Food 2003, 6:387-390.
48. Setchell K.D., Brown N.M., Desai P., Zimmer-Nechemias L., Wolfe B.E., Brashear W.T., et al. Bioavailability of pure isoflavones in healthy humans and analysis of commercial soy isoflavone supplements. J Nutr 2001, 131:1362S-1375S.
49. Setchell K.D., Brown N.M., Zimmer-Nechemias L., Brashear W.T., Wolfe B.E., Kirschner A.S., et al. Evidence for lack of absorption of soy isoflavone glycosides in humans, supporting the crucial role of intestinal metabolism for bioavailability. Am J Clin Nutr 2002, 76:447-453.