The steroidogenic acute regulatory protein as a target of endocrine disruption in male reproduction

Drug Metabolism Reviews

Volumn 39, Issue 2-3, 2007, Pages 353-370

  Clark, Barbara J ^a   Cochrum, Renate K ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Endocrine disruptor; Leydig cell; StAR; Steroidogenesis

Indexed keywords

CYTOCHROME P450 17; CYTOCHROME P450 17 A 1; STEROID HORMONE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TESTOSTERONE; UNCLASSIFIED DRUG;

BIOSYNTHESIS; ENDOCRINE DISEASE; FETUS DEVELOPMENT; HUMAN; LEYDIG CELL; NONHUMAN; REPRODUCTION; REVIEW; STEROIDOGENESIS;

ANIMALS; ARSENITES; ENDOCRINE GLANDS; ENVIRONMENTAL POLLUTANTS; ESTERS; GENE EXPRESSION REGULATION; HUMANS; MALE; PHOSPHOPROTEINS; PHTHALIC ACIDS; REPRODUCTION; STEROIDS; TERATOGENS;

EID: 34548450153     PISSN: 03602532     EISSN: 10979883     Source Type: Journal    
DOI: 10.1080/03602530701519151     Document Type: Review

References (106)

1. Ahmad, S. A., M. H. Sayed, et al. (2001). Arsenic in drinking water and pregnancy outcomes. Environ. Health Perspect. 109:629-631.
2. Akingbemi, B. T., Ge, R., et al. (2004). Phthalate-induced Leydig cell hyperplasia is associated with multiple endocrine disturbances. Proc. Natl. Acad. Sci. USA 101:775-780.
3. Akingbemi, B. T., Ge, R., et al. (2003). Estrogen receptor-alpha gene deficiency enhances androgen biosynthesis in the mouse Leydig cell. Endocrinology 144:84-93.
4. Akingbemi, B. T., Sottas, C. M., et al. (2004). Inhibition of testicular steroidogenesis by the xenoestrogen bisphenol a is associated with reduced pituitary luteinizing hormone secretion and decreased steroidogenic enzyme gene expression in rat Leydig cells. Endocrinology 145:592-603.
5. Akingbemi, B. T., Youker, R. T., et al. (2001). Modulation of rat Leydig cell steroidogenic function by di(2-ethylhexyl)phthalate. Biol. Reprod. 65:1252-1259.
6. Allen, J. A., Diemer, T., et al. (2004). Bacterial endotoxin lipopolysaccharide and reactive oxygen species inhibit Leydig cell steroidogenesis via perturbation of mitochondria. Endocrine 25:265-276.
7. Aposhian, H. V., Zakharyan, R. A., et al. (2003). Oxidation and detoxification of trivalent arsenic species. Toxicol. Appl. Pharmacol. 193:1-8.
8. Barlow, N. J., McIntyre, B. S., et al. (2004). Male reproductive tract lesions at 6, 12, and 18 months of age following in utero exposure to di(n-butyl) phthalate. Toxicol. Pathol. 32:79-90.
9. Barlow, N. J., Phillips, S. L., et al. (2003). Quantitative changes in gene expression in fetal rat testes following exposure to di(n-butyl) phthalate. Toxicol. Sci. 73:431-441.
10. Bodwell, J. E., Kingsley, L. A., et al. (2004). Arsenic at very low concentrations alters glucocorticoid receptor (GR)-mediated gene activation but not GR-mediated gene repression: complex dose-response effects are closely correlated with levels of activated GR and require a functional GR DNA binding domain. Chem. Res. Toxicol. 17:1064-1076.
11. Bose, H. S., Whittal, R. M., et al. (1999). The active form of the steroidogenic acute regulatory protein, StAR, appears to be a molten globule. Proc. Natl. Acad. Sci. USA 96:7250-7255.
12. Caron, K. M., Ikeda, Y., et al. (1997). Characterization of the promoter region of the mouse gene encoding the steroidogenic acute regulatory protein. Mol. Endocrinol. 11:138-147.
13. Chakraborti, D., Mukherjee, S. C., et al. (2003). Arsenic groundwater contamination in Middle Ganga Plain, Bihar, India: a future danger? Environ. Health Perspect. 111:1194-1201.
14. Chang, S. I., Jin, B., et al. (2007). Arsenic-induced toxicity and the protective role of ascorbic acid in mouse testis. Toxicol. Appl. Pharmacol. 218:196-203.
15. Chattopadhyay, S., Ghosh, S., et al. (1999). Effect of sodium arsenite on plasma levels of gonadotrophins and ovarian steroidogenesis in mature albino rats: duration-dependent response. J. Toxicol. Sci. 24:425-431.
16. Chattopadhyay, S., Ghosh, S., et al. (2001). Protection of sodium arsenite-induced ovarian toxicity by coadministration of L-ascorbate (vitamin C) in mature wiStAR strain rat. Arch. Environ. Contam. Toxicol. 41:83-89.
17. Chattopadhyay, S., Ghosh, S., et al. (2003). Effect of dietary co-administration of sodium selenite on sodium arsenite-induced ovarian and uterine disorders in mature albino rats. Toxicol. Sci. 75:412-422.
18. Chen, H., Li, S., et al. (2004). Chronic inorganic arsenic exposure induces hepatic global and individual gene hypomethylation: implications for arsenic hepatocarcinogenesis. Carcinogenesis 25:1779-1786.
19. Christenson, L. K., Johnson, P. F., et al. (1999). CCAAT/enhancer-binding proteins regulate expression of the human steroidogenic acute regulatory protein (StAR) gene. J. Biol. Chem. 274:26591-26598.
20. Christenson, L. K., Osborne, T. F., et al. (2001). Conditional response of the human steroidogenic acute regulatory protein gene promoter to sterol regulatory element binding protein-1a. Endocrinology 142:28-36.
21. Clark, B. J., Combs, R. (1999). Angiotensin II and cyclic adenosine 3′,5′-monophosphate induce human steroidogenic acute regulatory protein transcription through a common steroidogenic factor-1 element. Endocrinology 140:4390-4398.
22. Clark, B. J., Corbitt, C., et al. (2006). Decreased Serum Testosterone Levels in Adult Male Mice Prenatally Exposed to Arsenite. 88th Annual Meeting of the Endocrine Society Boston, MA.
23. Clark, B. J., Ranganathan, V., et al. (2001). Steroidogenic acute regulatory protein expression is dependent upon post-translational effects of cAMP-dependent protein kinase A. Mol. Cell Endocrinol. 173:183-192.
24. Clark, B. J., Wells, J., et al. (1994). 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. 269:28314-28322.
25. Clem, B. F., Clark, B. J. (2006). Association of the mSin3A-histone deacetylase 1/2 corepressor complex with the mouse steroidogenic acute regulatory protein gene. Mol. Endocrinol. 20:100-113.
26. Clem, B. F., Hudson, E. A., et al. (2004). Cyclic adenosine 3′,5′-monophosphate (cAMP) enhances cAMP-responsive element binding (CREB) protein phosphorylation and phospho-CREB interaction with the mouse steroidogenic acute regulatory (StAR) protein gene promoter. Endocrinology. 146:1348-1356.
27. Couse, J. E., Mahato, D., et al. (2001). Molecular mechanism of estrogen action in the male: insights from the estrogen receptor null mice. Reprod. Fertil. Dev. 13:211-219.
28. Delbes, G., Levacher, C., et al. (2005). Endogenous estrogens inhibit mouse fetal Leydig cell development via Estrogen Receptor {alpha}. Endocrinology. 146:2454-2461.
29. Diemer, T., Allen, J. A., et al. (2003). Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (StAR) protein and steroidogenesis. Endocrinology 144:2882-2891.
30. Eddy, E. M., Washburn, T. F., et al. (1996). Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 137:4796-4805.
31. Fielden, M. R., Halgren, R. G., et al. (2002). Gestational and lactational exposure of male mice to diethylstilbestrol causes long-term effects on the testis, sperm fertilizing ability in vitro, and testicular gene expression. Endocrinology 143:3044-3059.
32. Ge, R.-S., Chen, G.-R., et al. (2007). Biphasic effects of postnatal exposures to diethylhexylphthalate on the timing of puberty in male rats. J. Androl. 10.2164/jandrol.106.001909.
33. Ge, R.-S., Chen, G.-R., et al. (2007). Phthalate ester toxicity in Leydig cells: Developmental timing and dosage considerations. Reproduct. Toxicol. 23:366-373.
34. Ge, R. S., Dong, Q., et al. (2005). Gene expression in rat Leydig cells during development from the progenitor to adult stage: a cluster analysis. Biol. Reprod. 72:1405-1415.
35. Ge, R. S., Dong, Q., et al. (2006). In search of rat stem Leydig cells: identification, isolation, and lineage-specific development. Proc Natl Acad Sci. USA 103:2719-2724.
36. Guyot, R., Odet, F., et al. (2004). Diethylstilbestrol inhibits the expression of the steroidogenic acute regulatory protein in mouse fetal testis. Mol. Cell Endocrinol. 220:67-75.
37. Hauet, T., Liu, J., et al. (2002). PBR, StAR, and PKA: partners in cholesterol transport in steroidogenic cells. Endocr. Res. 28:395-401.
38. Hauser, R., Williams, P., et al. (2005). Evidence of interaction between polychlorinated biphenyls and phthalates in relation to human sperm motility. Environ. Health Perspect. 113:425-430.
39. Hei, T. K., Filipic, M. (2004). Role of oxidative damage in the genotoxicity of arsenic. Free Radic. Biol. Med. 37:574-581.
40. Hiroi, H., Christenson, L. K., et al. (2004). Temporal and spatial changes in transcription factor binding and histone modifications at the steroidogenic acute regulatory protein (StAR) locus associated with StAR transcription. Mol. Endocrinol. 18:791-806.
41. Hiroi, H., Christenson, L. K., et al. (2004). Regulation of transcription of the steroidogenic acute regulatory protein (StAR) gene: temporal and spatial changes in transcription factor binding and histone modification. Mol. Cell Endocrinol. 215:119-126.
42. Hopenhayn, C., Ferreccio, C., et al. (2003). Arsenic exposure from drinking water and birth weight. Epidemiology 14:593-602.
43. Jana, K., Jana, S., et al. (2006). Effects of chronic exposure to sodium arsenite on hypothalamo-pituitary-testicular activities in adult rats: possible an estrogenic mode of action. Reprod. Biol. Endocrinol. 4:9.
44. Kaltreider, R. C., Davis, A. M., et al. (2001). Arsenic alters the function of the glucocorticoid receptor as a transcription factor. Environ. Health Perspect. 109:245-251.
45. King, S. R., Liu, Z., et al. (1999). Effects of disruption of the mitochondrial electrochemical gradient on steroidogenesis and the Steroidogenic Acute Regulatory (StAR) protein. J. Steroid Biochem. Mol. Biol. 69:143-154.
46. Kumagai, Y., Pi, J. (2004). Molecular basis for arsenic-induced alteration in nitric oxide production and oxidative stress: implication of endothelial dysfunction. Toxicol. Appl. Pharmacol. 198:450-457.
47. Laskey, J. W., Phelps, P. V. (1991). Effect of cadmium and other metal cations on in vitro Leydig cell testosterone production. Toxicol. Appl. Pharmacol. 108:296-306.
48. Lei, Z. M., Mishra, S., et al. (2004). Testicular phenotype in luteinizing hormone receptor knockout animals and the effect of testosterone replacement therapy. Biol Reprod 71:1605-1613.
49. Lei, Z. M., Mishra, S., et al. (2001). Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene. Mol. Endocrinol. 15:184-200.
50. Liu, J., Rone, M. B., et al. (2006). Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J. Biol. Chem. 281:38879-38893.
51. Liu, J., Xie, Y., et al. (2007). Transplacental exposure to inorganic arsenic at a hepatocarcinogenic dose induces fetal gene expression changes in mice indicative of aberrant estrogen signaling and disrupted steroid metabolism. Toxicol. Appl. Pharmacol. 220:284-291.
52. Liu, J., Xie, Y., et al. (2006). Transplacental arsenic plus postnatal 12-O-teradecanoyl phorbol-13-acetate exposures associated with hepatocarcinogenesis induce similar aberrant gene expression patterns in male and female mouse liver. Toxicol. Appl. Pharmacol. 213:216-223.
53. Liu, K., Lehmann, K. P., et al. (2005). Gene expression profiling following in utero exposure to phthalate esters reveals new gene targets in the etiology of testicular dysgenesis. Biol. Reprod. 73:180-192.
54. Lo, K. C., Lei, Z., et al. (2004). De novo testosterone production in luteinizing hormone receptor knockout mice after transplantation of leydig stem cells. Endocrinology 145:4011-4015.
55. Majdic, G., Sharpe, R. M., et al. (1996). Expression of cytochrome P450 17alpha-hydroxylase/C17-20 lyase in the fetal rat testis is reduced by maternal exposure to exogenous estrogens. Endocrinology 137:1063-1070.
56. Majdic, G., Sharpe, R. M., et al. (1997). Maternal oestrogen/xenoestrogen exposure alters expression of steroidogenic factor-1 (SF-1/Ad4BP) in the fetal rat testis. Mol. Cell. Endocrinol. 127:91-98.
57. Manna, P. R., Dyson, M. T., et al. (2002). Regulation of steroidogenesis and the steroidogenic acute regulatory protein by a member of the cAMP response-element binding protein family. Mol. Endocrinol. 16:184-199.
58. Manna, P. R., Eubank, D. W., et al. (2003). Transcriptional regulation of the mouse steroidogenic acute regulatory protein gene by the cAMP response-element binding protein and steroidogenic factor 1. J. Mol. Endocrinol. 30:381-397.
59. Manna, P. R., Eubank, D. W., et al. (2004). Assessment of the role of activator protein-1 on transcription of the mouse steroidogenic acute regulatory protein gene. Mol. Endocrinol. 18: 558-573.
60. Manna, P. R., Wang, X. J., et al. (2003). Involvement of multiple transcription factors in the regulation of steroidogenic acute regulatory protein gene expression. Steroids 68:1125-1134.
61. Mikkila, T. F., Toppari, J., et al. (2006). Effects of neonatal exposure to 4-tert-octylphenol, diethylstilbestrol, and flutamide on steroidogenesis in infantile rat testis. Toxicol. Sci. 91:456-466.
62. Miller, W. L. (2007). StAR Search - What we know about how the steroidogenic acute regulatory protein mediates mitochondrial cholesterol import. 10.1210/me.2006-0303. Mol. Endocrinol. 21:589-601.
63. Mylchreest, E., Sar, M., et al. (2002). Fetal testosterone insufficiency and abnormal proliferation of Leydig cells and gonocytes in rats exposed to di(n-butyl) phthalate. Reproduct. Toxicol. 16:19-28.
64. Mylchreest, E., Wallace, D. G., et al. (2000). Dose-dependent alterations in androgen-regulated male reproductive development in rats exposed to di(n-butyl) phthalate during late gestation. Toxicol. Sci. 55:143-151.
65. Nackley, A. C., Shea-Eaton, W., et al. (2002). Repression of the steroidogenic acute regulatory gene by the multifunctional transcription factor Yin Yang 1. Endocrinology 143:1085-1096.
66. Navarro Silvera, S. A., Rohan, T. E. (2007). Trace elements and cancer risk: a review of the epidemiologic evidence. Cancer Causes Control 18:7-27.
67. O'Shaughnessy, P. J., Willerton, L., et al. (2002). Changes in Leydig cell gene expression during development in the mouse. Biol. Reprod. 66:966-75.
68. Pant, N., Murthy, R. C., et al. (2004). Male reproductive toxicity of sodium arsenite in mice. Hum Exp Toxicol 23:399-403.
69. Papadopoulos, V., Liu, J., et al. (2007). Is there a mitochondrial signaling complex facilitating cholesterol import? Mol. Cell. Endocrinol. 265-266:59-64.
70. Park, S. Y., Jameson, J. L. (2005). Minireview: transcriptional regulation of gonadal development and differentiation. Endocrinology 146:1035-1042.
71. Parker, K. L., Rice, D. A., et al. (2002). Steroidogenic Factor 1: an essential mediator of endocrine development. Recent Prog. Horm. Res. 57:19-36.
72. Pisarska, M. D., Bae, J., et al. (2004). Forkhead L2 is expressed in the ovary and represses the promoter activity of the steroidogenic acute regulatory gene. Endocrinology 145:3424-3433.
73. Rahman, M. M., Sengupta, M. K., et al. (2005). The magnitude of arsenic contamination in groundwater and its health effects to the inhabitants of the Jalangi - one of the 85 arsenic affected blocks in West Bengal, India. Sci. Total Environ. 338:189-200.
74. Reinhart, A. J., Williams, S. C., et al. (1999). SF-1 (steroidogenic factor-1) and C/EBP beta (CCAAT/enhancer binding protein-beta) cooperate to regulate the murine StAR (steroidogenic acute regulatory) promoter. Mol. Endocrinol. 13:729-741.
75. Samuel, S., Kathirvel, R., et al. (2005). Protein oxidative damage in arsenic induced rat brain: influence of DL-alpha-lipoic acid. Toxicol. Lett. 155:27-34.
76. Sandhoff, T. W., Hales, D. B., et al. (1998). Transcriptional regulation of the rat steroidogenic acute regulatory protein gene by steroidogenic factor 1. Endocrinology 139:4820-4831.
77. Sarkar, M., Chaudhuri, G. R., et al. (2003). Effect of sodium arsenite on spermatogenesis, plasma gonadotrophins and testosterone in rats. Asian J. Androl. 5:27-31.
78. Sen Gupta, R., Kim, J., et al. (2004a). Effect of ascorbic acid supplementation on testicular steroidogenesis and germ cell death in cadmium-treated male rats. Mol. Cell Endocrinol. 221:57-66.
79. Sen Gupta, R., Sen Gupta, E., et al. (2004b). Vitamin C and vitamin E protect the rat testes from cadmium-induced reactive oxygen species. Mol. Cells 17:132-139.
80. Shea-Eaton, W., Sandhoff, T. W., et al. (2002). Transcriptional repression of the rat steroidogenic acute regulatory (StAR) protein gene by the AP-1 family member c-Fos. Mol. Cell Endocrinol. 188:161-170.
81. Shultz, V. D., Phillips, S., et al. (2001). Altered gene profiles in fetal rat testes after in utero exposure to di(n-butyl) phthalate. Toxicol. Sci. 64:233-242.
82. Silva, M. J., Barr, D. B., et al. (2004). Urinary levels of seven phthalate metabolites in the U.S. population from the National Health and Nutrition Examination Survey (NHANES) 1999-2000. Environ. Health Perspect. 112:331-338.
83. Silverman, E., Eimerl, S., et al. (1999). CCAAT enhancer-binding protein beta and GATA-4 binding regions within the promoter of the steroidogenic acute regulatory protein (StAR) gene are required for transcription in rat ovarian cells. J. Biol. Chem. 274:17987-17996.
84. Silverman, E., Yivgi-Ohana, N., et al. (2006). Transcriptional activation of the steroidogenic acute regulatory protein (StAR) gene: GATA-4 and CCAAT/enhancer-binding protein beta confer synergistic responsiveness in hormone-treated rat granulosa and HEK293 cell models. Mol. Cell Endocrinol. 252:92-101.
85. Smith, A. H., Hopenhayn-Rich, C., et al. (1992). Cancer risks from arsenic in drinking water. Environ. Health Perspect. 97:259-267.
86. Stocco, D. M. (2001). StAR protein and the regulation of steroid hormone biosynthesis. Annu. Rev. Physiol. 63:193-213.
87. Stocco, D. M., Clark, B. J. (1996). Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev. 17:221-244.
88. Stocco, D. M., Wells, J., et al. (1993). The effects of hydrogen peroxide on steroidogenesis in mouse Leydig tumor cells. Endocrinology 133:2827-2832.
89. Stoica, A., Katzenellenbogen, B. S., et al. (2000). Activation of estrogen receptor-alpha by the heavy metal cadmium. Mol. Endocrinol. 14:545-553.
90. Styblo, M., Drobna, Z., et al. (2002). The role of biomethylation in toxicity and carcinogenicity of arsenic: a research update. Environ. Health Perspect. 110 Suppl 5:767-71.
91. Sugawara, T., Holt, J. A., et al. (1996). Steroidogenic factor 1-dependent promoter activity of the human steroidogenic acute regulatory protein (StAR) gene. Biochemistry 35:9052-9059.
92. Sugawara, T., Kiriakidou, M., et al. (1997). Multiple steroidogenic factor 1 binding elements in the human steroidogenic acute regulatory protein gene 5′-flanking region are required for maximal promoter activity and cyclic AMP responsiveness. Biochemistry 36:7249-7255.
93. Swan, S. H., Main, K. M., et al. (2005). Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ. Health Perspect. 113:1056-1061.
94. Tremblay, J. J., Hamel, F., et al. (2002). Protein kinase A-dependent cooperation between GATA and CCAAT/enhancer-binding protein transcription factors regulates steroidogenic acute regulatory protein promoter activity. Endocrinology 143:3935-3945.
95. Tremblay, J. J., Viger, R. S. (2001). GATA factors differentially activate multiple gonadal promoters through conserved GATA regulatory elements. Endocrinology 142:977-986.
96. Tremblay, J. J., Viger, R. S. (2003). Transcription factor GATA-4 is activated by phosphorylation of serine 261 via the cAMP/protein kinase a signaling pathway in gonadal cells. J. Biol. Chem. 278:22128-35.
97. Tuckey, R. C., Headlam, M. J., et al. (2002). Transfer of cholesterol between phospholipid vesicles mediated by the steroidogenic acute regulatory protein (StAR). J. Biol. Chem. 277:47123-47128.
98. Waalkes, M. P., Liu, J., et al. (2004). Estrogen signaling in livers of male mice with hepatocellular carcinoma induced by exposure to arsenic in utero. J. Natl. Cancer Inst. 96:466-474.
99. Waalkes, M. P., Liu, J., et al. (2006). Enhanced urinary bladder and liver carcinogenesis in male CD1 mice exposed to transplacental inorganic arsenic and postnatal diethylstilbestrol or tamoxifen. Toxicol. Appl. Pharmacol. 215:295-305.
100. Waalkes, M. P., Ward, J. M., et al. (2004). Induction of tumors of the liver, lung, ovary and adrenal in adult mice after brief maternal gestational exposure to inorganic arsenic: promotional effects of postnatal phorbol ester exposure on hepatic and pulmonary, but not dermal cancers. Carcinogenesis 25:133-41.
101. Waalkes, M. P., Ward, J. M., et al. (2003). Transplacental carcinogenicity of inorganic arsenic in the drinking water: induction of hepatic, ovarian, pulmonary, and adrenal tumors in mice. Toxicol. Appl. Pharmacol. 186:7-17.
102. Wooton-Kee, C. R., Clark, B. J. (2000). Steroidogenic factor-1 influences protein-deoxyribonucleic acid interactions within the cyclic adenosine 3,5-monophosphate-responsive regions of the murine steroidogenic acute regulatory protein gene. Endocrinology 141:1345-1355.
103. Yaworsky, D. C., Baker, B. Y., et al. (2005). pH-dependent Interactions of the carboxyl-terminal helix of steroidogenic acute regulatory protein with synthetic membranes. J. Biol. Chem. 280:2045-2054.
104. Zazopoulos, E., Lalli, E., et al. (1997). DNA binding and transcriptional repression by DAX-1 blocks steroidogenesis. Nature 390:311-315.
105. Zhang, F.-P., Pakarainen, T., et al. (2004). Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology 145:1453-1463.
106. Zhao, D., Xue, H., et al. (2005). Novel signaling stimulated by arsenite increases cholesterol metabolism through increases in unphosphorylated steroidogenic acute regulatory (StAR) protein. Mol. Cell. Endocrinol. 231:95-107.