Monobutyl Phthalate Inhibits Steroidogenesis by Downregulating Steroidogenic Acute Regulatory Protein Expression in Mouse Leydig Tumor Cells (MLTC-1)

REFERENCES

• Ascoli , M. , Fanelli , F. and Segaloff , D. L. 2002 . The lutropin/choriogonadotropin receptor, A 2002 perspective . Endocr. Rev. , 23 : 141 – 174 .
   PubMed Web of Science ®Google Scholar
• Ascoli , M. and Segaloff , D. L. 1989 . Regulation of the differentiated functions of Leydig tumor cells by epidermal growth factor . Ann. NY Acad. Sci. , 564 : 99 – 115 .
   PubMed Web of Science ®Google Scholar
• Barlow , N. J. , Phillips , S. L. , Wallace , D. G. , Sar , M. , Gaido , K. W. and Foster , P. M. 2003 . Quantitative changes in gene expression in fetal rat testes following exposure to di(n-butyl) phthalate . Toxicol. Sci. , 73 : 431 – 441 .
   PubMed Web of Science ®Google Scholar
• Blount , B. C. , Silva , M. J. , Caudill , S. P. , Needham , L. L. , Pirkle , J. L. , Sampson , E. J. , Lucier , G. W. , Jackson , R. J. and Brock , J. W. 2000 . Levels of seven urinary phthalate metabolites in a human reference population . Environ. Health Perspect. , 108 : 979 – 982 .
   PubMed Web of Science ®Google Scholar
• Boujrad , N. , Vidic , B. , Gazouli , M. , Culty , M. and Papadopoulos , V. 2000 . The peroxisome proliferator perfluorodecanoic acid inhibits the peripheral-type benzodiazepine receptor (PBR) expression and hormone-stimulated mitochondrial cholesterol transport and steroid formation in Leydig cells . Endocrinology , 141 : 3137 – 3148 .
   PubMed Web of Science ®Google Scholar
• Caron , K. M. , Soo , S. C. , Wetsel , W. C. , Stocco , D. M. , Clark , B. J. and Parker , K. L. 1997 . Targeted disruption of the mouse gene encoding steroidogenic acute regulatory protein provides insights into congenital lipoid adrenal hyperplasia . Proc. Natl. Acad. Sci. USA , 94 : 11540 – 11545 .
   PubMed Web of Science ®Google Scholar
• Chen , C. W. 2001 . Assessment of endocrine disruptors: approaches, issues, and uncertainties . Folia Histochem. Cytobiol. , 39 ( suppl. 2 ) : 20 – 23 .
   PubMed Web of Science ®Google Scholar
• Chen , J. , Chen , H. , Liu , R. , Song , L. , Bian , Q. , Xu , L. , Zhou , J. , Xiao , H. , Dai , G. , Chang , H. C. and Wang , X. 2005 . Effects of fenvalerate on progesterone production in cultured rat granulosa cells . Reprod. Toxicol. , 20 : 195 – 202 .
   PubMedGoogle Scholar
• Chiao , Y. C. , Cho , W. L. and Wang , P. S. 2002 . Inhibition of testosterone production by propylthiouracil in rat Leydig cells . Biol. Reprod. , 67 : 416 – 422 .
   PubMed Web of Science ®Google Scholar
• Clark , B. J. , Soo , S. C. , Caron , K. M. , Ikeda , Y. , Parker , K. L. and Stocco , D. M. 1995 . Hormonal and developmental regulation of the steroidogenic acute regulatory (StAR) protein . Mol. Endocrinol. , 9 : 1346 – 1355 .
   PubMed Web of Science ®Google Scholar
• Clark , B. J. , Wells , J. , King , S. R. and Stocco , D. M. 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 .
   PubMed Web of Science ®Google Scholar
• Clem , B. F. , Hudson , E. A. and Clark , B. J. 2005 . Cyclic adenosine 3′,5′-monophosphate (cAMP) enhances cAMP-responsive element binding (CREB) protein phosphorylation and phospho-CREB interaction with the mouse steroidogenic acute regulatory protein gene promoter . Endocrinology , 146 : 1348 – 1356 .
   PubMedGoogle Scholar
• DeRosa , C. , Richter , P. , Pohl , H. and Jones , D. E. 1998 . Environmental exposures that affect the endocrine system: Health implications . J. Toxicol. Environ. Health B , 1 : 3 – 26 .
   PubMed Web of Science ®Google Scholar
• Fisher , J. S. 2004 . Environmental anti-androgens and male reproductive health: Focus on phthalates and testicular dysgenesis syndrome . Reproduction , 127 : 305 – 315 .
   PubMed Web of Science ®Google Scholar
• Foster , P. M. , Mylchreest , E. , Gaido , K. W. and Sar , M. 2001 . Effects of phthalate esters on the developing reproductive tract of male rats . Hum. Reprod. Update , 7 : 231 – 235 .
   PubMed Web of Science ®Google Scholar
• Hedger , M. P. and Culler , M. D. 1997 . Comparison of LHRH-peptidase and plasminogen activator activity in rat testis extracts . Reprod. Fertil. Dev. , 9 : 659 – 664 .
   PubMedGoogle Scholar
• Higuchi , T. T. , Palmer , J. S. , Gray , L. E. and Veeramachaneni , D. N. 2003 . Effects of dibutyl phthalate in male rabbits following in utero, adolescent, or postpubertal exposure . Toxicol. Sci. , 72 : 301 – 313 .
   PubMed Web of Science ®Google Scholar
• Khan , S. A. , Keck , C. , Gudermann , T. and Nieschlag , E. 1990 . Isolation of a protein from human ovarian follicular fluid which exerts major stimulatory effects on in vitro steroid production of testicular, ovarian, and adrenal cells . Endocrinology , 126 : 3043 – 3052 .
   PubMedGoogle Scholar
• Kim , H. S. , Kim , T. S. , Shin , J.-H. , Moon , H. J. , Kang , I. H. , Kim , I. Y. , Oh , J. Y. and Han , S. Y. 2004 . Neonatal exposure to di(n-butyl) phthalate (DBP) alters male reproductive tract development . J. Toxicol. Environ. Health A , 67 : 2045 – 2060 .
   PubMed Web of Science ®Google Scholar
• Kohn , M. C. , Parham , F. , Masten , S. A. , Portier , C. J. , Shelby , M. D. , Broch , J. W. and Needham , L. L. 2000 . Human exposure estimates for phthalates . Environ. Health Perspect. , 108 : A440 – 442 .
   PubMed Web of Science ®Google Scholar
• Koch , H. M. , Rossbach , B. , Drexler , H. and Angerer , J. 2003 . Internal exposure of the general population to DEHP and other phthalates—Determination of secondary and primary phthalate monoester metabolites in urine . Environ. Res. , 93 : 177 – 185 .
   PubMed Web of Science ®Google Scholar
• Koo , H. J. and Lee , B. M. 2004 . Estimated exposure to phthalates in cosmetics and risk assessment . J. Toxicol. Environ. Health A , 67 : 1901 – 1914 .
   PubMed Web of Science ®Google Scholar
• Koo , H. J. and Lee , B. M. 2005 . Human monitoring of phthalates and risk assessment . J. Toxicol. Environ. Health A , 68 : 1379 – 1392 .
   PubMed Web of Science ®Google Scholar
• Kumar , S. , Blumberg , D. L. , Canas , J. A. and Maddaiah , V. T. 1994 . Human chorionic gonadotropin (hCG) increases cytosolic free calcium in adult rat Leydig cells . Cell Calcium , 15 : 349 – 355 .
   PubMedGoogle Scholar
• Lin , D. , Sugawara , T. , Strauss , J. F. III , Clark , B. J. , Stocco , D. M. , Saenger , P. , Rogol , A. and Miller , W. L. 1995 . Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis . Science , 267 : 1828 – 1831 .
   PubMed Web of Science ®Google Scholar
• Lin , T. , Wang , D. , Hu , J. and Stocco , D. M. 1998 . Upregulation of human chorionic gonadotrophin-induced steroidogenic acute regulatory protein by insulin-like growth factor-I in rat Leydig cells . Endocrine , 8 : 73 – 78 .
   PubMedGoogle Scholar
• Maness , S. C. , McDonnell , D. P. and Gaido , K. W. 1998 . Inhibition of androgen receptor-dependent transcriptional activity by DDT isomers and methoxychlor in HepG12 human hepatoma cells . Toxicol. Appl. Pharmacol , 151 : 135 – 142 .
   PubMed Web of Science ®Google Scholar
• Manna , P. R. , Eubank , D. W. , Lalli , E. , Sassone-Corsi , P. and Stocco , D. M. 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 .
   PubMed Web of Science ®Google Scholar
• Manna , P. R. , Eubank , D. W. and Stocco , D. M. 2004a . Assessment of the role of activator protein-1 on transcription of the mouse steroidogenic acute regulatory protein gene . Mol. Endocrinol. , 18 : 558 – 573 .
   PubMed Web of Science ®Google Scholar
• Manna , P. R. , Huhtaniemi , I. T. and Stocco , D. M. 2004b . Detection of hCG responsive expression of the steroidogenic acute regulatory protein in mouse Leydig cells . Biol. Proc. , 6 : 83 – 93 . Online
   PubMedGoogle Scholar
• Manna , P. R. , Huhtaniemi , I. T. , Wang , X. J. , Eubank , D. W. and Stocco , D. M. 2002 . Mechanisms of epidermal growth factor signaling: Regulation of steroid biosynthesis and the steroidogenic acute regulatory protein in mouse Leydig tumor cells . Biol. Reprod. , 67 : 1393 – 1404 .
   PubMedGoogle Scholar
• Manna , P. R. , Pakarinen , P. , El-Hefnawy , T. and Huhtaniemi , I. T. 1999 . Functional assessment of the calcium messenger system in cultured mouse Leydig tumor cells: Regulation of human chorionic gonadotropin-induced expression of the steroidogenic acute regulatory protein . Endocrinology , 140 : 1739 – 1751 .
   PubMed Web of Science ®Google Scholar
• Manna , P. R. and Stocco , D. M. 2005 . Regulation of the steroidogenic acute regulatory protein expression: Functional and physiological consequences . Curr. Drug Targets Immune Endocr. Metabol. Disord. , 5 : 93 – 108 .
   PubMedGoogle Scholar
• Mylchreest , E. , Cattley , R. C. and Foster , P. M. 1998 . Male reproductive tract malformations in rats following gestational and lactational exposure to di(n-butyl) phthalate: An antiandrogenic mechanism? . Toxicol. Sci. , 43 : 47 – 60 .
   PubMed Web of Science ®Google Scholar
• Mylchreest , E. , Sar , M. , Cattley , R. C. and Foster , P. M. 1999 . Disruption of androgen regulated male reproductive development by di(n-butyl) phthalate during late gestation in rats is different from flutamide . Toxicol. Appl. Pharmacol. , 156 : 81 – 95 .
   PubMed Web of Science ®Google Scholar
• Mylchreest , E. , Sar , M. , Wallace , D. G. and Foster , P. M. 2002 . Fetal testosterone insufficiency and abnormal proliferation of Leydig cells and gonodocytes in rats exposed to di(n-butyl) phthalate . Reprod. Toxicol. , 16 : 19 – 28 .
   PubMed Web of Science ®Google Scholar
• Parks , L. G. , Ostby , J. S. , Lambright , C. R. , Abbott , B. D. , Klinefelter , G. R. , Barlow , N. J. and Gray , L. E. 2000 . The plasticizer diethylhexyl phthalate induces malformations by decreasing fetal testosterone synthesis during sexual differentiation in the male rat . Toxicol. Sci. , 58 : 339 – 349 .
   PubMed Web of Science ®Google Scholar
• Qiu , C. , Shan , L. , Yu , M. and Snyderwine , E. G. 2003 . Deregulation of the cyclin d1/cdk4 retinoblastoma pathway in rat mammary gland carcinomas induced by the food-derived carcinogen 2-amino-1-methyl-6-phenylimidazo [4,5-b] pyridine . Cancer Res. , 63 : 5674 – 5678 .
   PubMedGoogle Scholar
• Richards , J. S. 2001 . New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells . Mol. Endocrinol. , 15 : 209 – 218 .
   PubMedGoogle Scholar
• Shono , T. and Suita , S. 2003 . Dose-dependent effect of phthalate ester on testicular descent in pre- and post natal rats . Urol. Res. , 31 : 293 – 296 .
   PubMed Web of Science ®Google Scholar
• Shultz , V. D. , Phillips , S. , Sar , M. , Foster , P. M. and Gaido , K. W. 2001 . Altered gene profiles in fetal rat testes after in utero exposure to di(n-butyl) phthalate . Toxicol. Sci. , 64 : 233 – 242 .
   PubMed Web of Science ®Google Scholar
• Silva , M. J. , Barr , D. B. , Reidy , J. A. , Malek , N. A. , Hodge , C. C. , Caudill , S. P. , Brock , J. W. , Needham , L. L. and Calafat , A. M. 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 .
   PubMed Web of Science ®Google Scholar
• Stocco , D. M. 2000 . Intramitochondrial cholesterol transfer . Biochim. Biophys. Acta , 1486 : 184 – 197 .
   PubMedGoogle Scholar
• Stocco , D. M. 2002 . Clinical disorders associated with abnormal cholesterol transport: Mutations in the steroidogenic acute regulatory protein . Mol. Cell Endocrinol. , 191 : 19 – 25 .
   PubMedGoogle Scholar
• Stocco , D. M. and Clark , B. J. 1993 . The requirement of phosphorylation on a threonine residue in the acute regulation of steroidogenesis in MA-10 mouse Leydig cells . J. Steroid Biochem. Mol. Biol. , 46 : 337 – 347 .
   PubMed Web of Science ®Google Scholar
• Stocco , D. M. and Clark , B. J. 1996 . Regulation of the acute production of steroids in steroidogenic cells . Endocr. Rev. , 17 : 221 – 244 .
   PubMed Web of Science ®Google Scholar
• Stocco , D. M. and Khan , S. A. 1992 . Effects of steroidogenesis inducing protein (SIP) on steroid production in MA-10 mouse Leydig tumor cells: Utilization of a non-cAMP second messenger pathway . Mol. Cell Endocrinol. , 84 : 185 – 194 .
   PubMedGoogle Scholar
• Thompson , C. J. , Ross , S. M. and Gaido , K. W. 2004 . Di(n-butyl) phthalate impairs cholesterol transport and steroidogenesis in the fetal rat testis through a rapid and reversible mechanism . Endocrinology , 145 : 1227 – 1237 .
   PubMed Web of Science ®Google Scholar
• Verhoeven , G. , Cailleau , J. , Van , D. J. and Billiau , A. 1988 . Interleukin-1 stimulates steroidogenesis in cultured rat Leydig cells . Mol. Cell Endocrinol. , 57 : 51 – 60 .
   PubMed Web of Science ®Google Scholar
• Walsh , L. P. , McCormick , C. , Martin , C. and Stocco , D. M. 2000a . Roundup inhibits steroidogenesis by disrupting steroidogenic acute regulatory (StAR) protein expression . Environ. Health Perspect. , 108 : 769 – 776 .
   PubMed Web of Science ®Google Scholar
• Walsh , L. P. and Stocco , D. M. 2000 . Effects of lindane on steroidogenesis and steroidogenic acute regulatory protein expression . Biol. Reprod. , 63 : 1024 – 1033 .
   PubMedGoogle Scholar
• Walsh , L. P. , Webster , D. R. and Stocco , D. M. 2000b . Dimethoate inhibits steroidogenesis by disrupting transcription of the steroidogenic acute regulatory (StAR) gene . J. Endocrinol. , 167 : 253 – 263 .
   PubMed Web of Science ®Google Scholar
• Wooton-Kee , C. R. and 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 .
   PubMed Web of Science ®Google Scholar
• Wu , C. S. , Leu , S. F. , Yang , H. Y. and Huang , B. M. 2001 . Melatonin inhibits the expression of steroidogenic acute regulatory protein and steroidogenesis in MA-10 cells . J. Androl. , 22 : 245 – 254 .
   PubMedGoogle Scholar
• Zirkin , B. R. and Chen , H. 2000 . Regulation of Leydig cell steroidogenic function during aging . Biol. Reprod. , 63 : 977 – 981 .
   PubMed Web of Science ®Google Scholar