Effects of atrazine on CYP19 gene expression and aromatase activity in testes and on plasma sex steroid concentrations of male African clawed frogs (Xenopus laevis)

Toxicological Sciences

Volumn 86, Issue 2, 2005, Pages 273-280

  Hecker, Markus ^a   Park, June Woo ^a   Murphy, Margaret B ^a   Jones, Paul D ^a   Solomon, Keith R ^b   Van Der Kraak, Glen ^b   Carr, James A ^c   Smith, Ernest E ^c   du Preez, Louis ^d   Kendall, Ronald J ^c   Giesy, John P ^a,e  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF GUELPH   (Canada)

^c TEXAS TECH UNIVERSITY   (United States)

^d NORTH WEST UNIVERSITY   (South Africa)

^e CITY UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Amphibians; Aromatase; Endocrine modulation; Estrogen synthesis; Gene expression; Q RT PCR

Indexed keywords

AROMATASE; ATRAZINE; ESTRADIOL; SEX HORMONE; TESTOSTERONE;

AFRICA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; ENZYME MECHANISM; FROG; GENE EXPRESSION; GONAD; HORMONE BLOOD LEVEL; LONG TERM EXPOSURE; MALE; NONHUMAN; STATISTICAL SIGNIFICANCE; STEROIDOGENESIS; TESTIS; TESTOSTERONE BLOOD LEVEL; XENOPUS LAEVIS;

ANIMALS; AROMATASE; ATRAZINE; ESTRADIOL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HERBICIDES; MALE; RNA, MESSENGER; TESTIS; TESTOSTERONE; XENOPUS LAEVIS;

AMPHIBIA; ANURA; XENOPUS LAEVIS;

EID: 26444433927     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfi203     Document Type: Article

References (40)

1. Allran, J. W., and Karasov, W. H. (2000). Effects of atrazine and nitrate on northern Leopard frog [i#(Rana pipiens)#1i] larvae exposed in the laboratory from posthatch through metamorphosis. [i#Environ. Toxicol. Chem.#1i] [b#19#1b], 2850-2855.
2. Allran, J. W., and Karasov, W. H. (2001). Effects of atrazine on embryos, larvae, and adults of anuran amphibians. [i#Environ. Toxicol. Chem.#1i] [b#20#1b], 769-775.
3. Bisson, M., and Hontela, A. (2002). Cytotoxic and endocrine-disrupting potential of atrazine, diazone, endosulfan, and mancozeb in adrenocortical steroidogenic cells of rainbow trout exposed [i#in vitro. Toxicol. Appl. Pharmacol.#1i] [b#180#1b], 110-117.
4. Bradford, M. (1976). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. [i#Anal. Biochem.#1i] [b#72#1b], 248-254.
5. Carr, J. A., Gentles, A., Smith, E. E., Goleman, W. L., Urquidi, L. J., Thuett, K., Kendall, R. J., Giesy, J. P., Gross, T. S., Solomon, K. R. [i#et al.#1i] (2003). Response of larval [i#Xenopus laevis#1i] to atrazine: Assessment of growth, metamorphosis, and gonadal and laryngeal morphology. [i#Environ. Toxicol. Chem.#1i] [b#22#1b], 396-405.
6. Chang, L. W., Toth, G. P., Gordon, D. A., Graham, D. W., Meier, J. R., Knapp, C. W., DeNoyelles, F. J., Campbell, S., and Lattier, D. L. (2005). Responses of molecular indicators of exposure in mesocosms: Common carp [i#(Cyprinus carpio)#1i] exposed to the herbicides alachlor and atrazine. [i#Environ. Toxicol. Chem.#1i] [b#24#1b], 190-197.
7. Coady, K. K., Murphy, M. B., Villeneuve, D. L., Hecker, M., Jones, P. D., Carr, J. A., Solomon, K., Smith, E. E., Van Der Kraak, G., Kendall, R. J. [i#et al.#1i] (2004). Effects of atrazine on metamorphosis, growth, and gonadal development in the green frog [i#(Rana clamitans). J. Toxicol. Environ. Health, A#1i] [b#67#1b], 941-957.
8. Coady, K. K., Murphy, M. B., Villeneuve, D. L., Hecker, M., Carr, J. A., Solomon, K. R., Smith, E. E., Van Der Kraak, G., Kendall, R. J., and Giesy, J. P. (2005). Effects of atrazine on metamorphosis, growth, and gonadal and laryngeal development in [i#Xenopus laevis. Exotoxicol. Environ. Safety#1i] in press.
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. [i#Toxicol. Sci.#1i] [b#53#1b], 297-307.
10. Corn, P. S. (2000). Amphibian declines: Review of some current hypothesis. In [i#Ecotoxicology of Amphibians and Reptiles#1i] (D.W. Sparling, G. Linder, and C.A. Bishop, eds.), pp. 663-698. Society of Environmental Toxicology and Chemistry, Pensacola, FL.
11. Crain, D. A., Spiteri, I. D., and Guillette, L. J., Jr. (1999). The functional and structural observations of the neonatal reproductive system of alligators exposed [i#in ovo#1i] to atrazine, 2,4-D, or estradiol. [i#Toxicol. Ind. Health#1i] [b#15#1b], 180-185.
12. Cuisset, B., Pradelles, P., Kime, D. E., Kuehn, E. R., Babin, P., Davail, S., and Le Menn, F. (1994). Enzyme immunoassay for 11-ketotestosterone using acetylcholinesterase as label: Application to the measurement of 11-ketotestosterone in plasma of Siberian sturgeon. [i#Comp. Biochem. Physiol. C#1i] [b#108#1b], 229-241.
13. Girault, I., Lerebours, F., Tozlu, S., Spyratos, F., Tubiana-Hulin, M., Lidereau, R., and Bieche, I. (2002). Real-time reverse transcription PCR assay of CYP19 expression: Application to a well-defined series of post-menopausal breast carcinomas. [i#J. Steroid Biochem. Mol. Biol.#1i] [b#82#1b], 323-332.
14. Gluth, G., and Hanke, W. (1985). A comparison of physiological changes in carp, [i#Cyprinus carpio#1i], induced by several pollutants at sublethal concentrations. I. The dependency on exposure time. [i#Ecotoxicol. Environ. Safety#1i] [b#9#1b], 179-188.
15. Hanioka, N., Jinno, H., Tanaka-Kagawa, T., Nishimura, T., and Ando, M. (1998). Changes in rat liver cytochrome P450 enzymes by atrazine and simazine treatment. [i#Xenobiotica#1i] [b#28#1b], 683-698.
16. Hayes, T. B., Collins, A., Lee, M., Mendoza, M., Noriega, N., Stuart, A. A., and Vonk, A. (2002). Hermaphroditic, demasculinized frogs after exposure to the herbicide, atrazine, at low ecologically relevant doses. [i#Proc. Natl. Acad. Sci. USA#1i] [b#99#1b], 5408-5476.
17. Hecker, M., Giesy, J. P., Jones, P. D., Jooste, A. M., Carr, J. A., Solomon, K. R., Smith, E. E., Van Der Kraak, G., Kendall, R. J., and Du Preez, L. H. (2004). Plasma sex steroid concentrations and gonadal aromatase activities in African clawed frogs [i#(Xenopus laevis)#1i] from the corn-growing region of South Africa. [i#Environ. Toxicol. Chem.#1i] [b#23#1b], 205-216.
18. Hecker, M. (2001). Natural variability of endocrine functions and their modulation by anthropogenic influences: Investigations of the bream [i#(Abramis brama#1i] [L.]) along the Elbe River, and in a reference site. 16, -149. 2001. Hamburg, Germany, University of Hamburg. Reports of the Center for Marine and Athmospheric Science, Series E.
19. Hecker, M., Kim, W. J., Park, J.-W., Murphy, M. B., Villeneuve, D. L., Coady, K. K., Jones, P. D., Solomon, K. R., Van der Kraak, G. J., Carr, J. A. [i#et al.#1i] (2005). Plasma concentrations of estradiol and testosterone, gonadal aromatase activity and ultrastructure of the testis in [i#Xenopus laevis#1i] exposed to estradiol or atrazine. [i#Aq. Toxicol.#1i] [b#72#1b], 383-396.
20. Heneweer, M., Van den Berg, M., and Sanderson, J. T. (2004). A comparison of human H295R and rat R2C cell lines as [i#in vitro#1i] screening tools for effects on aromatase. [i#Toxicol. Lett.#1i] [b#146#1b] 183-194.
21. Hopenhayn-Rich, C., Stump, M. L., and Browning, S. R. (2002). Regional assessment of atrazine exposure and incidence of breast and ovarian cancers in Kentucky. [i#Arch. Environ. Contam. Toxicol.#1i] [b#42#1b], 127-136.
22. Kazeto, Y., Place, A. R., and Trant, J. M. (2004). Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish [i#(Danio rerio)#1i] juveniles. [i#Aq. Toxicol.#1i] [b#69#1b], 25-34.
23. Larson, D. L., McDonald, S., Fivizzani, A. J., Newton, W. E., and Hamilton, S. J. (1998). Effects of the herbicide atrazine on [i#Ambystoma tigrinum#1i] metamorphosis: Duration, larval growth, and hormonal response. [i#Physiol. Zool.#1i] [b#71#1b], 671-679.
24. Lephart, E. D., and Simpson, E. R. (1991). Assay for aromatase activity. In [i#Methods of Enzymology#1i] (M. R. Waterman and E. F. Johnson, eds.), pp. 477-483. Academic Press, New York.
25. Liddle, C., Goodwin, B. J., George, J., Tapner, M., and Farrell, G. C. (1998). Separate and interactive regulation of cytochrome P450 3A4 by triiodothyronine, dexamethasone, and growth hormone in cultured hepatocytes. [i#J. Clin. Endocrinol. Metab.#1i] [b#83#1b], 2411-2416.
26. Nash, J. P., Davail-Cuisset, B., Bhattacharyya, S., Suter, H. C., Le Menn, F., and Kime, D. E. (2000). An enzyme linked immunosorbant assay (ELISA) for testosterone, estradiol, and 17,20b-dihydroxy-4-pregnen-3-one using acetylcholinesterase as tracer: Application to measurement of diel patterns in rainbow trout [i#(Oncorhynchus mykiss). Fish Physiol. Biochem.#1i] [b#22#1b], 255-263.
27. Nemoto, N., and Sakurai, J. (1992). Differences in regulation of gene expression between Cyp1a-1 and Cyp1a-2 in adult mouse hepatocytes in primary culture. [i#Carcinogenesis#1i] [b#13#1b], 2249-2254.
28. Oh, S. M., Shim, S. H., and Chung, K. H. (2003). Antiestrogenic action of atrazine and its major metabolites [i#in vitro. J. Health Sci.#1i] [b#49#1b], 65-71.
29. Oulmi, Y., Negele, R. D., and Braunbeck, T. (1995). Segment specificity of the cytological response in rainbow trout [i#(Oncorhynchus mykiss)#1i] renal tubules following prolonged exposure to sublethal concentrations of atrazine. [i#Ecotoxicol. Environ. Safety#1i] [b#32#1b], 39-50.
30. Raaijmakers, M. H., van Ernst, L., De Witte, T., Mensink, E., and Raymakers, R. A. (2002). Quantitative assessment of gene expression in highly purified hematopoietic cells using real-time reverse transcriptase polymerase chain reaction. [i#Exp. Hematol.#1i] [b#30#1b], 481-487.
31. Roberge, M., Hakk, H., and Larsen, G. (2004). Atrazine is a competitive inhibitor of phosphodiesterase but does not affect the estrogen receptor. [i#Toxicol. Lett.#1i] [b#154#1b], 61-68.
32. Sanderson, J. T., Boerma, J., Lansbergen, G., and Van den Berg, M. (2002). Induction and inhibition of aromatase (CYP19) activity by various classes of pesticides in H295R human adrenocortical carcinoma cells. [i#Toxicol. Appl. Pharmacol.#1i] [b#182#1b], 44-54.
33. Sanderson, J. T., Seinen, W., Giesy, J. P., and Van den Berg, M. (2000). 2-chloro-s-triazine herbicides induce aromatase activity in H295R human adrenocortical carcinoma cells. A novel mechanism for estrogenicity. [i#Toxicol. Sci.#1i] [b#54#1b], 127.
34. Solomon, K. R., Baker, D. B., Richards, R. P., Dixon, K. R., Maine, S. J., LaPoint, T. W., Kendall, R. J., Giddings, J. M., Giesy, J. P., Hall, L. W. J. [i#et al.#1i] (1996). Ecological risk assessment of atrazine in North American surface waters. [i#Environ. Toxicol. Chem.#1i] [b#15#1b], 76.
35. Spano, L., Tyler, C. R., Van Aerle, R., Devos, P., Mandiki, S. N. M., Silvestre, F., Thome, J. P., and Kestemont, P. (2004). Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish [i#(Carassius auratus). Aq. Toxicol.#1i] [b#66#1b], 369-379.
36. Stoker, T. E., Parks, L. G., Gray, L, E., and Cooper, R. L. (2000). Endocrine disrupting chemicals: Prepubertal exposures and effects on sexual maturation and thyroid function in the male rat. A focus on the EDSTAC recommendations. [i#Crit. Rev. Toxicol.#1i] [b#30#1b], 197-252.
37. Waxman, D. J. (1988). Interactions of hepatic cytochromes P-450 with steroid hormones - Regioselectivity and stereospecificity of steroid metabolism and hormonal regulation of rat P450 enzyme expression. [i#Biochem. Pharmacol.#1i] [b#37#1b], 71-84.
38. Waxman, D. J., Lapenson, D. P., Aoyama, T., Gelboin, H. V., Gonzalez, F. J., and Korzekwa, K. (1991). Steroid hormone hydroxylase specificities of eleven cDNA-expressed human cytochrome P450s. [i#Arch. Biochem. Biophys.#1i] [b#290#1b], 160-166.
39. Wiechmann, A. F., and Smith, A. R. (2001). Melatonin receptor RNA is expressed in photoreceptors and displays a diurnal rhythm in [i#Xenopus#1i] retina. [i#Brain Res. Mol. Brain Res.#1i] [b#91#1b], 104-111.
40. Zhang, Q. Y., He, W., Dunbar, D., and Kaminsky, L. (1997). Induction of CYP1A1 by beta-naphthoflavone in IEC-18 rat intestinal epithelial cells and potentiation of induction by dibutyryl cAMP. [i#Biochem. Biophys. Res. Commun.#1i] [b#233#1b], 623-626.