Upregulation of peripubertal rat leydig cell steroidogenesis following 24 h in vitro and in vivo exposure to atrazine

Toxicological Sciences

Volumn 118, Issue 1, 2010, Pages 52-60

  Pogrmic Majkic, Kristina ^a   Fa, Svetlana ^a   Dakic, Vanja ^a   Kaisarevic, Sonja ^a   Kovacevic, Radmila ^a  

^a UNIVERSITY OF NOVI SAD   (Serbia)

Author keywords

Atrazine; Gene expression; LC steroidogenesis

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ANDROGEN; ATRAZINE; CHORIONIC GONADOTROPIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYTOCHROME P450 17; CYTOCHROME P450 17A1; ENZYME; MESSENGER RNA; REGULATOR PROTEIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN; STEROIDOGENIC FACTOR 1; TESTOSTERONE; UNCLASSIFIED DRUG;

ANDROGEN SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EXPOSURE; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; LEYDIG CELL; MALE; NONHUMAN; PUBERTY; RAT; SIGNAL TRANSDUCTION; STEROIDOGENESIS; TOXICITY TESTING; UPREGULATION;

ANDROGENS; ANIMALS; ATRAZINE; CELL SURVIVAL; CELLS, CULTURED; CYCLIC AMP; GONADAL STEROID HORMONES; HERBICIDES; LEYDIG CELLS; MALE; PHOSPHOPROTEINS; PROGESTERONE; RATS; RATS, WISTAR; SEXUAL MATURATION; STEROID 17-ALPHA-HYDROXYLASE; STEROIDOGENIC FACTOR 1; TESTOSTERONE; TETRAZOLIUM SALTS; THIAZOLES; UP-REGULATION;

RATTUS;

EID: 77958455522     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq227     Document Type: Article

References (45)

1. Andric, N., Kostic, T., Kaisarevic, S., Fa, S., Pogrmic, K., and Kovacevic, R. (2008). In vivo and in vitro effects of PCB126 and PCB153 on rat testicular androgenesis. Environ. Toxicol. Pharmacol. 25, 222-226.
2. Andric, N. L., Kostic, T. S., Zoric, S. N., Stanic, B. D., Andric, S. A., and Kovacevic, R. Z. (2006a). Effect of a PCB-based transformer oil on testicular steroidogenesis and xenobiotic-metabolizing enzymes. Reprod. Toxicol. 22, 102-110.
3. Andric, S. A., Kostic, T. S., and Stojilkovic, S. S. (2006b). Contribution of multidrug resistance protein MRP5 in control of cyclic guanosine 5-monophosphate intracellular signaling in anterior pituitary cells. Endocrinology 147, 3435-3445.
4. Andric, S. A., Kostic, T. S., Stojilkovic, S. S., and Kovacevic, R. Z. (2000). Inhibition of rat testicular androgenesis by polychlorinated biphenyl mixture aroclor 1248. Biol. Reprod. 62, 1882-1888.
5. Azhar, S., and Reaven, E. (2002). Scavenger receptor class BI and selective cholesteryl ester uptake: partners in the regulation of steroidogenesis. Mol. Cell. Endocrinol. 195, 1-26.
6. Barr, D. B., Panuwet, P., Nguyen, J. V., Udunka, S., and Needham, L. L. (2007). Assessing exposure to atrazine and its metabolites using biomonitoring. Environ. Health Perspect. 115, 1474-1478.
7. Birnbaum, L. S., and Fenton, S. E. (2003). Cancer and developmental exposure to endocrine disruptors. Environ. Health Perspect. 111, 389-394.
8. Cooper, R. L., Laws, S. C., Das, P. C., Norotsky, M. G., Goldman, J. M., Tyrey, E. L., and Stoker, T. E. (2007). Atrazine and reproductive function: mode and mechanism of action studies. Birth Defects Res. B. Dev. Reprod. Toxicol. 80, 98-112.
9. Cooper, R. L., Stoker, T. E., Tyrey, L., Goldman, J. M., and McElroy, W. K. (2000). Atrazine disrupts the hypothalamic control of pituitary-ovarian function. Toxicol. Sci. 53, 297-307.
10. Crain, D. A., Guillette, L. J., Jr., Rooney, A. A., and Pickford, D. B. (1997). Alterations in steroidogenesis in alligators (Alligator mississippiensis) exposed naturally and experimentally to environmental contaminants. Environ. Health Perspect. 105, 528-533.
11. Fraites, M. J., Cooper, R. L., Buckalew, A., Jayaraman, S., Mills, L., and Laws, S. C. (2009). Characterization of the hypothalamic-pituitary-adrenal axis response to atrazine and metabolites in the female rat. Toxicol. Sci. 112, 88-99.
12. Friedmann, A. S. (2002). Atrazine inhibition of testosterone production in rat males following peripubertal exposure. Reprod. Toxicol. 16, 275-279.
13. Gasic,S.,Budimir,M.,Brkic,D.,andNeskovic,N.(2002).Residues of atrazine in agricultural areas of Serbia. J. Serb. Chem. Soc. 12, 887-892.
14. Hayes, T., Haston, K., Tsui, M., Hoang, A., Haeffele, C., and Vonk, A. (2003). Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ. Health Perspect. 111, 568-575.
15. Hayes, T. B., Khoury, V., Narayan, A., Nazir, M., Park, A., Brown, T., Adame, L., Chan, E., Buchholz, D., Stueve, T., et al. (2010). Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). Proc. Natl. Acad. Sci. U.S.A. 107, 4612-4617.
16. Heneweer, M., Van der Berg, M., and Sanderson, T. (2004). A comparison of human H295 and rat R2C cell lines as in vitro screening tools for effects on aromatase. Toxicol. Lett. 146, 183-194.
17. Laws, S. C., Ferrell, J. M., Stoker, T. E., and Cooper, R. L. (2003). Pubertal development in female Wistar rats following exposure to propazine and atrazine biotransformation by-products, diamino-S-chlorotriazine and hydroxyatrazine. Toxicol. Sci. 76, 190-200.
18. Laws, S. C., Ferrell, J. M., Stoker, T. E., Schmid, J., and Cooper, R. L. (2000). The effects of atrazine on female Wistar rats: an evaluation of the protocol for assessing pubertal development and thyroid function. Toxicol. Sci. 58, 366-376.
19. Laws, S. C., Hotchkiss, M., Ferrell, J., Jayaraman, S., Mills, L., Modic, W., Tinfo, N., Fraites, M., Stoker, T., and Cooper, R. (2009). Chlorotriazine herbicides and metabolites activate an ACTH-dependent release of corticosterone in male Wistar rats. Toxicol. Sci. 112, 78-87.
20. Leckie, C. M., Welberg, L. A. M., and Seckl, J. R. (1998). 11β-Hydroxysteroid dehydrogenase is a predominant reductase in intact rat Leydig cells. J. Endocrinol. 159, 233-238.
21. Lehmann, T. P., Biernacka-Lukanty, J. M., Saraco, N., Langlois, D., Li, J. Y., and Trzeciak, W. H. (2005). Temporal pattern of the induction of SF-1 gene expression by the signal transduction pathway involving 3',5'-cyclic adenosine monophosphate. Acta. Biochim. Pol. 52, 485-491.
22. Li, D., Urs, A. N., Allegood, J., Leon, A., Merrill, A. H., Jr., and Sewer, M. B. (2007). Cyclic AMP-stimulated interaction between steroidogenic factor 1 and diacylglycerol kinase theta facilitates induction of CYP17. Mol. Cell. Biol. 27, 6669-6685.
23. Manna, P. R., Chandrala, S. P., Jo, Y., and Stocco, D. M. (2006). cAMP-independent signaling regulates steroidogenesis in mouse Leydig cells in the absence of StAR phosphorylation. J. Mol. Endocrinol. 37, 81-95.
24. Manna, P. R., Jo, Y., and Stocco, D. M. (2007). Regulation of Leydig cell steroidogenesis by extracellular signal-regulated kinase 1/2: role of protein kinase A and protein kinase C signaling. J. Endocrinol. 193, 53-63.
25. Morinaga, H., Yanase, T., Noura, M., Okabe, T., Goto, K., and Harada, N. (2004). A benzimidazole fungicide, benomyl, and its metabolite, carbendazim, induce aromatase activity in human ovarian granulose-like tumor cell line (KGN). Endocrinology 145, 1860-1869.
26. Ochoa-Acuña, H., Frankenberger, J., Hahn, L., and Carbajo, C. (2009). Drinking-water herbicide exposure in Indiana and prevalence of small-forgestational-age and preterm delivery. Environ. Health Perspect. 117, 1619-1624.
27. Papadopoulos, V., Liu, J., and Martine, C. (2007). Is there a mitochondrial signaling complex facilitating cholesterol import. Mol. Cell. Endocrinol. 265-266, 59-64.
28. Payne, A. H. (2007). Steroidogenic enzymes in Leydig cells. In The Leydig Cell in Health and Disease. (A. H. Payne and M. P. Hardy, Eds.), pp. 157-171. Humana Press, Totowa, NJ.
29. Payne, A. H., Downing, J., and Wongi, K. L. (1980). Luteinizing hormone receptors and testosterone synthesis in two distinct population of Leydig cells. Endocrinology 106, 1424-1429.
30. Payne, A. H., and Youngblood, G. L. (1995). Regulation of expression of steroidogenic enzymes in Leydig cells. Biol. Reprod. 52, 217-225.
31. Pogrmic, K., Fa, S., Dakic, V., Kaisarevic, S., and Kovacevic, R. (2009). Atrazine oral exposure of peripubertal male rats down-regulates steroidogenesis gene expression in Leydig cells. Toxicol. Sci. 111, 189-197.
32. Rao, R. M., Jo, Y., Leers-Sucheta, S., Bose, H. S., Miller, W. L., and Azhar, S. (2003). 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. 68, 114-121.
33. Roberge, M., Hakk, H., and Larsen, G. (2004). Atrazine is a competitive inhibitor of phosphodiesterase but does not affect the estrogen receptor. Toxicol. Lett. 154, 61-68.
34. Roberge, M. T., Hakk, H., and Larsen, G. (2006). Cytosolic and localized inhibition of phosphodiesterase by atrazine in swine tissue homogenates. Food Chem. Toxicol. 44, 885-890.
35. Sanderson, J. T., Boerma, J., Lansbergen, G. W. A., and Berg, M. (2002). Induction and inhibition of aromatase CYP19 activity by various classes of pesticides in H295R human adrenocortical carcinoma cells. Toxicol. Appl. Pharmacol. 182, 44-54.
36. Sanderson, J. T., Letcher, R. J., Heneweer, M., Giesy, J. P., and Van der Berg, M. (2001). Effects of chloro-S-triazines and metabolites on aromatase activity in various cell lines and on vitellogin production in male carp hepatocytes. Environ. Health Perspect. 109, 1027-1031.
37. Sanderson, J. T., Seinen, W., Giesy, J. P., and Van der Berg, M. (2000). 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicol. Sci. 54, 121-127.
38. Sewer, M. B., and Jagarlapudi, S. (2009). Complex assembly on the human CYP17 promoter. Mol. Cell. Endocrinol. 300, 109-114.
39. Spano, L., Tyler, C. R., van Aerle, R., Devos, P., and Mandiki, S. N. (2004). Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish (Carassius auratus). Aquat. Toxicol. 66, 369-379.
40. Stocco, D. M., Wang, X., Jo, Y., and Manna, P. R. (2005). Multiple signaling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression: more complicated than we thought. Mol. Endocrinol. 19, 2647-2659.
41. Stoker, T. E., Laws, S. C., Guidici, D. L., and Cooper, R. L. (2000a). The effects of atrazine on puberty in male Wistar rats: an evaluation in the protocol for the assessment of pubertal development and thyroid function. Toxicol. Sci. 58, 50-59.
42. Stoker, T. E., Parks, L. G., Gray, L. E., and Cooper, R. L. (2000b). Endocrinedisrupting chemicals: prepubertal exposures and effects on sexual maturation and thyroid function in the male rat. A focus on the EDSTAC recommendations. Crit. Rev. Toxicol. 30, 197-252.
43. Suzawa, M., and Ingraham, H. A. (2008). The herbicide atrazine activates endocrine gene networks via non-steroidal NR5A nuclear receptors in fish and mammalian cells. PLoS One 3, e2117.
44. Trentacoste, S. V., Friedmann, A. S., Youker, R. T., Breckenridge, C. B., and Zirkin, B. R. (2001). Atrazine effects on testosterone levels and androgen-dependent reproductive organs in peripubertal male rats. J. Androl. 22, 142-148.
45. Urs, A. N., Dammer, E., Kelly, S., Wang, E., Merrill, A. H., Jr., and Sewer, M. B. (2007). Steroidogenic factor-1 is a sphingolipid binding protein. Mol. Cell. Endocrinol. 265-266, 174-178.