Perfluorododecanoic acid-induced steroidogenic inhibition is associated with steroidogenic acute regulatory protein and reactive oxygen species in cAMP-stimulated leydig cells

Toxicological Sciences

Volumn 114, Issue 2, 2010, Pages 285-294

  Shi, Zhimin ^a   Feng, Yixing ^a   Wang, Jianshe ^a   Zhang, Hongxia ^a   Ding, Lina ^a   Dai, Jiayin ^a  

^a INSTITUTE OF ZOOLOGY   (China)

Author keywords

PFDoA; ROS; StAR; Steroidogenesis

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ADENOSINE TRIPHOSPHATE; BENZODIAZEPINE RECEPTOR; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYCLIC AMP; HYDROGEN PEROXIDE; MESSENGER RNA; PERFLUORODECANOIC ACID; PROGESTERONE; REACTIVE OXYGEN METABOLITE; STEROID; STEROIDOGENIC ACUTE REGULATORY PROTEIN; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ARTICLE; BIOLUMINESCENCE; CELL STIMULATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE EXPRESSION; INHIBITION KINETICS; LEYDIG CELL; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROGESTERONE SYNTHESIS; PROMOTER REGION; RADIOIMMUNOASSAY; RAT; REAL TIME POLYMERASE CHAIN REACTION; STEROIDOGENESIS; WESTERN BLOTTING;

ANIMALS; CELL LINE, TUMOR; CELL SURVIVAL; CYCLIC AMP; GENE EXPRESSION REGULATION; HYDROGEN PEROXIDE; LAURIC ACIDS; LEYDIG CELLS; MALE; MICE; MITOCHONDRIA; PHOSPHOPROTEINS; PROGESTERONE; RATS; REACTIVE OXYGEN SPECIES; SPECIES SPECIFICITY; TESTOSTERONE;

RATTUS;

EID: 77951544400     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq014     Document Type: Article

References (43)

1. Arteel, G. E., Guo, L., Schlierf, T., Beier, J. I., Kaiser, J. P., Chen, T. S., Liu, M., Conklin, D. J., Miller, H. L., von Montfort, C., et al. (2008). Subhepatotoxic exposure to arsenic enhances lipopolysaccharide-induced liver injury in mice. Toxicol. Appl. Pharmacol. 226, 128-139.
2. 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.
3. Biegel, L. B., Hurtt, M. E., Frame, S. R., O'Connor, J. C., and Cook, J. C. (2001). Mechanisms of extrahepatic tumor induction by peroxisome proliferators in male CD rats. Toxicol. Sci. 60, 44-55.
4. Biegel, L. B., Liu, R. C., Hurtt, M. E., and Cook, J. C. (1995). Effects of ammonium perfluorooctanoate on Leydig cell function: In vitro, in vivo, and ex vivo studies. Toxicol. Appl. Pharmacol. 134, 18-25.
5. Bookstaff, R. C., Moore, R. W., Ingall, G. B., and Peterson, R. E. (1990). Androgenic deficiency in male rats treated with perfluorodecanoic acid. Toxicol. Appl. Pharmacol. 104, 322-333.
6. Boujrad, N., Vidic, B., Gazouli, M., Culty, M., and Papadopoulos, V. (2000). The peroxisome proliferator perfluorodecanoic acid inhibits the peripheraltype benzodiazepine receptor (PBR) expression and hormone-stimulated mitochondrial cholesterol transport and steroid formation in Leydig cells. Endocrinology 141, 3137-3148.
7. Castedo, M., Ferri, K., Roumier, T., Metivier, D., Zamzami, N., and Kroemer, G. (2002). Quantitation of mitochondrial alterations associated with apoptosis. J. Immunol. Methods 265, 39-47.
8. Chandel, N. S., and Schumacker, P. T. (1999). Cells depleted of mitochondrial DNA (rho0) yield insight into physiological mechanisms. FEBS Lett. 454, 173-176.
9. Comelli, M., Metelli, G., and Mavelli, I. (2007). Downmodulation of mitochondrial F0F1 ATP synthase by diazoxide in cardiac myoblasts: a dual effect of the drug. Am. J. Physiol. Heart Circ. Physiol. 292, H820-H829.
10. Diemer, T., Allen, J. A., Hales, K. H., and Hales, D. B. (2003). Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (StAR) protein and steroidogenesis. Endocrinology 144, 2882-2891.
11. Guruge, K. S., Taniyasu, S., Yamashita, N., Wijeratna, S., Mohotti, K. M., Seneviratne, H. R., Kannan, K., Yamanaka, N., and Miyazaki, S. (2005). Perfluorinated organic compounds in human blood serum and seminal plasma: a study of urban and rural tea worker populations in Sri Lanka. J. Environ. Monit. 7, 371-377.
12. Kleszczynski, K., Gardzielewski, P., Mulkiewicz, E., Stepnowski, P., and Skladanowski, A. C. (2007). Analysis of structure-cytotoxicity in vitro relationship (SAR) for perfluorinated carboxylic acids. Toxicol. In Vitro 21, 1206-1211.
13. Klinefelter, G. R., Hall, P. F., and Ewing, L. L. (1987). Effect of luteinizing hormone deprivation in situ on steroidogenesis of rat Leydig cells purified by a multistep procedure. Biol. Reprod. 36, 769-783.
14. 2 generation is decreased by calcium in isolated brain mitochondria. Biochim. Biophys. Acta 1777, 800-807.
15. Kudo, N., and Kawashima, Y. (2003a). Induction of triglyceride accumulation in the liver of rats by perfluorinated fatty acids with different carbon chain lengths: comparison with induction of peroxisomal beta-oxidation. Biol. Pharm. Bull. 26, 47-51.
16. Kudo, N., and Kawashima, Y. (2003b). Toxicity and toxicokinetics of perfluorooctanoic acid in humans and animals. J. Toxicol. Sci. 28, 49-57.
17. Lau, C., Anitole, K., Hodes, C., Lai, D., Pfahles-Hutchens, A., and Seed, J. (2007). Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol. Sci. 99, 366-394.
18. Lau, C., Butenhoff, J. L., and Rogers, J. M. (2004). The developmental toxicity of perfluoroalkyl acids and their derivatives. Toxicol. Appl. Pharmacol. 198, 231-241.
19. Manna, P. R., Chandrala, S. P., King, S. R., Jo, Y., Counis, R., Huhtaniemi, I. T., and Stocco, D. M. (2006). Molecular mechanisms of insulin-like growth factor-I mediated regulation of the steroidogenic acute regulatory protein in mouse Leydig cells. Mol. Endocrinol. 20, 362-378.
20. Manna, P. R., Dyson, M. T., Eubank, D. W., Clark, B. J., Lalli, E., Sassone-Corsi, P., Zeleznik, A. J., and Stocco, D. M. (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.
21. Manna, P. R., El-Hefnawy, T., Kero, J., and Huhtaniemi, I. T. (2001). Biphasic action of prolactin in the regulation of murine Leydig tumor cell functions. Endocrinology 142, 308-318.
22. Mondillo, C., Pagotto, R. M., Piotrkowski, B., Reche, C. G., Patrignani, Z. J., Cymeryng, C. B., and Pignataro, O. P. (2009). Involvement of nitric oxide synthase in the mechanism of histamine-induced inhibition of Leydig cell steroidogenesis via histamine receptor subtypes in Sprague-Dawley rats. Biol. Reprod. 80, 144-152.
23. Monroe, R. K., and Halvorsen, S. W. (2009). Environmental toxicants inhibit neuronal Jak tyrosine kinase by mitochondrial disruption. Neurotoxicology 30, 589-598.
24. Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
25. Ohmori, K., Kudo, N., Katayama, K., and Kawashima, Y. (2003). Comparison of the toxicokinetics between perfluorocarboxylic acids with different carbon chain length. Toxicology 184, 135-140.
26. Olson, C. T., and Andersen, M. E. (1983). The acute toxicity of perfluorooctanoic and perfluorodecanoic acids in male rats and effects on tissue fatty acids. Toxicol. Appl. Pharmacol. 70, 362-372.
27. Panesar, N. S., Chan, K. W., and Ho, C. S. (2003). Mouse Leydig tumor cells produce C-19 steroids, including testosterone. Steroids 68, 245-251.
28. Pastoor, T. P., Lee, K. P., Perri, M. A., and Gillies, P. J. (1987). Biochemical and morphological studies of ammonium perfluorooctanoate-induced hepatomegaly and peroxisome proliferation. Exp. Mol. Pathol. 47, 98-109.
29. Payne, A. H., and Hales, D. B. (2004). Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr. Rev. 25, 947-970.
30. Renner, R. (2001). Growing concern over perfluorinated chemicals. Environ. Sci. Technol. 35, 154A-160A.
31. Renner, R. (2003). Concerns over common perfluorinated surfactant. Environ. Sci. Technol. 37, 201A-202A.
32. Rooney, J. P. (2007). The role of thiols, dithiols, nutritional factors and interacting ligands in the toxicology of mercury. Toxicology 234, 145-156.
33. Senthilkumar, K., Ohi, E., Sajwan, K., Takasuga, T., and Kannan, K. (2007). Perfluorinated compounds in river water, river sediment, market fish, and wildlife samples from Japan. Bull. Environ. Contam. Toxicol. 79, 427-431.
34. Shi, Z., Ding, L., Zhang, H., Feng, Y., Xu, M., and Dai, J. (2009). Chronic exposure to perfluorododecanoic acid disrupts testicular steroidogenesis and the expression of related genes in male rats. Toxicol. Lett. 188, 192-200.
35. Shi, Z., Zhang, H., Liu, Y., Xu, M., and Dai, J. (2007). Alterations in gene expression and testosterone synthesis in the testes of male rats exposed to perfluorododecanoic acid. Toxicol. Sci. 98, 206-215.
36. Stocco, D. M., and Clark, B. J. (1996). Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem. Pharmacol. 51, 197-205.
37. Tao, L., Kannan, K., Wong, C. M., Arcaro, K. F., and Butenhoff, J. L. (2008). Perfluorinated compounds in human milk from Massachusetts, U.S.A. Environ. Sci. Technol. 42, 3096-3101.
38. Tsai, S. C., Lu, C. C., Lin, C. S., and Wang, P. S. (2003). Antisteroidogenic actions of hydrogen peroxide on rat Leydig cells. J. Cell Biochem. 90, 1276-1286.
39. Turner, T. T., Tung, K. S., Tomomasa, H., and Wilson, L. W. (1997). Acute testicular ischemia results in germ cell-specific apoptosis in the rat. Biol. Reprod. 57, 1267-1274.
40. Van de Vijver, K. I., Holsbeek, L., Das, K., Blust, R., Joiris, C., and De, C. W. (2007). Occurrence of perfluorooctane sulfonate and other perfluorinated alkylated substances in harbor porpoises from the Black Sea. Environ. Sci. Technol. 41, 315-320.
41. Vanden Heuvel, J. P., Kuskikis, B. I., Van Rafelghem, M. J., and Peterson, R. E. (1991). Tissue distribution, metabolism, and elimination of perfluorooctanoic acid in male and female rats. J. Biochem. Toxicol. 6, 83-92.
42. 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.
43. Zini, A., and Schlegel, P. N. (1997). Cu/Zn superoxide dismutase, catalase and glutathione peroxidase mRNA expression in the rat testis after surgical cryptorchidism and efferent duct ligation. J. Urol. 158, 659-663.