Benomyl induction of brain aromatase and toxic effects in the zebrafish embryo

Journal of Applied Toxicology

Volumn 29, Issue 4, 2009, Pages 289-294

  Kim, Dong Jae ^a   Seok, Seung Hyeok ^a   Baek, Min Won ^a   Lee, Hui Young ^a   Na, Yi Rang ^a   Park, Sung Hoon ^a   Lee, Hyun Kyoung ^a   Dutta, Noton Kumar ^a   Kawakami, Koichi ^b,c   Park, Jae Hak ^a  

^a Seoul National University   (South Korea)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

Benomyl; Brain aromatase; EGFP; Toxicity; Zebrafish embryo

Indexed keywords

AROMATASE; BENOMYL;

ANIMAL EXPERIMENT; ARTICLE; CONCENTRATION (PARAMETERS); CONGENITAL MALFORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ESTROGEN ACTIVITY; HATCHING; HEART EDEMA; HEART RATE; INCIDENCE; LORDOSIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; SURVIVAL; TERATOGENICITY; VALIDATION PROCESS; ZEBRA FISH;

ANIMALS; AROMATASE; BENOMYL; BRAIN; EMBRYO, NONMAMMALIAN; FUNGICIDES, INDUSTRIAL; GREEN FLUORESCENT PROTEINS; HEART RATE; MICROINJECTIONS; PLASMIDS; SURVIVAL ANALYSIS; TERATOGENS; TRANSPOSASES; ZEBRAFISH;

DANIO RERIO; RODENTIA;

EID: 65649101931     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1405     Document Type: Article

References (39)

1. Barnes TB, Verlangieri AJ, Wilson MC. 1983. Reproductive toxicity of methyl-1-(butylcarbamoyl)-2-benzimidazole carbamate (benomyl) in male Wistar rats. Toxicology 28: 103-115.
2. Carter SD, Laskey JW. 1982. Effect of benomyl on reproduction in the male rat. Toxicol. Lett. 11: 87-94.
3. Colborn T, vom Saal FS, Soto AM. 1993. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health. Perspect. 101: 378-384.
4. Daniel TV, Martin PA, Struger J, Sherry J, Marvin CH, McMaster ME, Clarence S, Tetreault G. 2008. Potential endocrine disruption of sexual development in free ranging male northern leopard frogs (Rana pipiens) and green frogs (Rana clamitans) from areas of intensive row crop agriculture. Aquat. Toxicol. 88: 230-242.
5. Davidse LC. 1986. Benzimidazole fungicides: mechanism of action and biological impact. Annu. Rev. Phytopathol. 24: 43-65.
6. Davidse LC, Flach W. 1977. Differential binding of methyl benzimidazol-2-yl carbamate to fungal tubulin as a mechanism of resistance to this antimitotic agent in mutant strains of Aspergillus nidulans. J. Cell Biol. 72: 174-193. (Pubitemid 8007657)
7. DeRosa C, Richter P, Pohl H, Jones DE. 1998. Environmental exposures that affect the endocrine system: public health implications. J. Toxicol. Environ. Health. B Crit. Rev. 1: 3-26.
8. Ellis WG, Semple JL, Hoogenboom ER, Kavlock RJ, Zeman FJ. 1987. Benomyl-induced craniocerebral anomalies in fetuses of adequately nourished and protein-deprived rats. Teratog. Carcinog. Mutagen. 7: 357-375. (Pubitemid 17131324)
9. Gaido KW, Maness SC, McDonnell DP, Dehal SS, Kupfer D, Safe S. 2000. Interaction of methoxychlor and related compounds with estrogen receptor alpha and beta, and androgen receptor: structure-activity studies. Mol. Pharmacol. 58: 852-858.
10. Gardiner JA, Kirkland JJ, Klopping HL, Sherman H. 1974. Fate of benomyl in animals. J. Agric. Food Chem. 22: 419-427.
11. Gray LE Jr, Ostby J, Cooper RL, Kelce WR. 1999. The estrogenic and antiandrogenic pesticide methoxychlor alters the reproductive tract and behavior without affecting pituitary size or LH and prolactin secretion in male rats. Toxicol. Ind. Health 15: 37-47. (Pubitemid 30484116)
12. Guillette LJ Jr, Gross TS, Masson GR, Matter JM, Percival HF, Woodward AR. 1994. Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ. Health Perspect. 102: 680-688. (Pubitemid 24276619)
13. Haeba MH, Hilscherová K, Mazurová E, Bláha L. 2008. Selected endocrine disrupting compounds (vinclozolin, flutamide, ketoconazole and dicofol): effects on survival, occurrence of males, growth, molting and reproduction of Daphnia magna. Environ. Sci. Pollut. Res. Int. 15: 222-227.
14. Hess RA, Linder RE, Strader LF, Perreault SD. 1988. Acute effects and long-term sequelae of 1,3-dinitrobenzene on male reproduction in the rat. II. Quantitative and qualitative histopathology of the testis. J. Androl. 9: 327-342. (Pubitemid 18262990)
15. Hewitt MJ, Mutch P, Pratten MK. 2005. Potential teratogenic effects of benomyl in rat embryos cultured in vitro. Reprod. Toxicol. 20: 271-280. (Pubitemid 40725079)
16. Hoogenboom ER, Ransdell JF, Ellis WG, Kavlock RJ, Zeman FJ. 1991. Effects on the fetal rat eye of maternal benomyl exposure and protein malnutrition. Curr. Eye Res. 10: 601-612.
17. Kavlock RJ, Chernoff N, Gray LE Jr, Gray JA, Whitehouse D. 1982. Teratogenic effects of benomyl in the Wistar rat and CD-1 mouse, with emphasis on the route of administration. Toxicol. Appl. Pharmacol. 62: 44-54. (Pubitemid 12219108)
18. Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, Mishina M. 2004. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Devl. Cell 7: 133-144. (Pubitemid 39172695)
19. Kazeto Y, Place AR, Trant JM. 2004. Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish (Danio rerio) juveniles. Aquat. Toxicol. 69: 25-34. (Pubitemid 38798008)
20. Kishida M, Callard GV. 2001. Distinct cytochrome P450 aromatase isoforms in zebrafish (Danio rerio) brain and ovary are differentially programmed and estrogen regulated during early development. Endocrinology 142: 740-750. (Pubitemid 32222424)
21. Klotz DM, Beckman BS, Hill SM, McLachlan JA, Walters MR, Arnold SF. 1996. Identification of environmental chemicals with estrogenic activity using a combination of in vitro assays. Environ. Health Perspect. 104: 1084-1089. (Pubitemid 26395154)
22. Lim J, Miller MG. 1997a. The role of the benomyl metabolite carbendazim in benomyl-induced testicular toxicity. Toxicol. Appl. Pharmacol. 142: 401-410. (Pubitemid 28381031)
23. Lim J, Miller MG. 1997b. Role of testis exposure levels in the insensitivity of prepubertal rats to carbendazim-induced testicular toxicity. Fundam. Appl. Toxicol. 37: 158-167. (Pubitemid 27316669)
24. Linder RE, Rehnberg GL, Strader LF, Diggs JP. 1988. Evaluation of reproductive parameters in adult male Wistar rats after subchronic exposure (gavage) to benomyl. J. Toxicol. Environ. Health 25: 285-298. (Pubitemid 18272605)
25. Menuet A, Pellegrini E, Brion F, Gueguen MM, Anglade I, Pakdel F, Kah O. 2005. Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene. J. Comp. Neurol. 16: 304-320. (Pubitemid 40471294)
26. Morinaga H, Yanase T, Nomura M, Okabe T, Goto K, Harada N, Nawata H. 2004. A benzimidazole fungicide, benomyl, and its metabolite, carbendazim, induce aromatase activity in a human ovarian granulose-like tumor cell line (KGN). Endocrinology 145: 1860-1869. (Pubitemid 38402395)
27. Ohno K, Araki N, Yanase T, Nawata H, Iida M. 2004. A novel nonradioactive method for measuring aromatase activity using a human ovarian granulosa-like tumor cell line and an estrone ELISA. Toxicol. Sci. 82: 443-450. (Pubitemid 39600071)
28. Sanderson JT, Seinen W, Giesy JP, van den 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. (Pubitemid 30152463)
29. Sawyer SJ, Gerstner KA, Callard GV. 2006. Real-time PCR analysis of cytochrome P450 aromatase expression in zebrafish: gene specific tissue distribution, sex differences, developmental programming, and estrogen regulation. Gen. Comp. Endocrinol. 147: 108-117. (Pubitemid 43674476)
30. Scippo ML, Argiris C, Van De Weerdt C, Muller M, Willemsen P, Martial J, Maghuin-Rogister G. 2004. Recombinant human estrogen, androgen and progesterone receptors for detection of potential endocrine disruptors. Anal. Bioanal. Chem. 378: 664-669.
31. Shtenberg AI, Torchinskii AM. 1972. Relation of the general toxic, embryotoxic and teratogenic action of exogenous chemical substances and possibility of prognosticating their effect in the antenatal period of ontogenesis. Vestn. Akad. Med. Nauk SSSR 3: 39-46.
32. Tchoudakova A, Kishida M, Wood E, Callard GV. 2001. Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. J. Steroid Biochem. Mol. Biol. 78: 427-439. (Pubitemid 34014825)
33. Wang WD, Wang Y, Wen HJ, Buhler DR, Hu CH. 2004. Phenylthiourea as a weak activator of aryl hydrocarbon receptor inhibiting 2,3,7,8-tetrachlorodibenzo-p- dioxin-induced CYP1A1 transcription in zebrafish embryo. Biochem. Pharmacol. 68: 63-71. (Pubitemid 38746542)
34. Westerfield, M. 1995. The Zebrafish Book. University of Oregon Press: Eugene, OR.
35. Who. 1993. Environmental Health Criteria 148: Benomyl. Geneva: World Health Organization.
36. Wise LA, Palmer JR, Hatch EE, Troisi R, Titus-Ernstoff L, Herbst AL, Kaufman R, Noller KL, Hoover RN. 2007. Secondary sex ratio among women exposed to diethylstilbestrol in utero. Environ. Health. Perspect. 115: 1314-1319. (Pubitemid 47471255)
37. Yamada T, Sumida K, Saito K, Ueda S, Yabushita S, Sukata T, Kawamura S, Okuno Y, Seki T. 2005. Functional genomics may allow accurate categorization of the benzimidazole fungicide benomyl: lack of ability to act via steroid-receptor-mediated mechanisms. Toxicol. Appl. Pharmacol. 205: 11-30. (Pubitemid 40693266)
38. Yoon CS, Jin JH, Park JH, Youn HJ, Cheong SW. 2003. The fungicide benomyl inhibits differentiation of neural tissue in the Xenopus embryo and animal cap explants. Environ. Toxicol. 18: 327-337. (Pubitemid 37258745)
39. Zbozinek JV. 1984. Environmental transformations of DPA, SOPP, benomyl, and TBZ. Residue Rev. 92: 113-155. (Pubitemid 14048044)