Benzotriazole UV-stabilizers and benzotriazole: Antiandrogenic activity in vitro and activation of aryl hydrocarbon receptor pathway in zebrafish eleuthero-embryos

Science of the Total Environment

Volumn 482-483, Issue 1, 2014, Pages 125-136

  Fent, Karl ^a,b   Chew, Geraldine ^a   Li, Jun ^a   Gomez, Elena ^c  

^a UNIVERSITY OF APPLIED SCIENCES AND ARTS NORTHWESTERN SWITZERLAND   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITÉ DE MONTPELLIER   (France)

Author keywords

1H benzotriazole; 2 (2 Hydroxy 5 methylphenyl)benzotriazole (UV P); 2 (3 t Butyl 2 hydroxy 5 methylphenyl) 5 chlorobenzotriazole (UV 326); Benzotriazole UV stabilizers; Transcriptomics; Zebrafish

Indexed keywords

CELL DEATH; GENES; HYDROCARBONS; IRRADIATION; SOAPS (DETERGENTS); TRANSCRIPTION;

1H-BENZOTRIAZOLE; 2-(3-T-BUTYL-2-HYDROXY-5-METHYLPHENYL)-5-CHLOROBENZOTRIAZOLE (UV-326); BENZOTRIAZOLES; TRANSCRIPTOMICS; UV STABILIZER; ZEBRAFISH;

CORROSION INHIBITORS;

2 (2 HYDROXY 5 METHYLPHENYL)BENZOTRIAZOLE; 2 (2H BENZOTRIAZOL 2 YL) 4 (1,1,3,3 TETRAMETHYLBUTYL)PHENOL; 2 (2H BENZOTRIAZOL 2 YL) 4,6 DI TERT PENTYLPHENOL; 2 TERT BUTYL 6 (5 CHLORO 2H BENZOTRIAZOL 2 YL) 4 METHYLPHENOL; 2,4 DI TERT BUTYL 6 (5 CHLORO 2H BENZOTRIAZOL 2 YL)PHENOL; AROMATIC HYDROCARBON RECEPTOR; BENZOTRIAZOLE DERIVATIVE; CHRYSENE DERIVATIVE; STABILIZING AGENT; UNCLASSIFIED DRUG; ANTIANDROGEN; BENZOTRIAZOLE; CYTOCHROME P450 1A1; TRIAZOLE DERIVATIVE;

BIOACCUMULATION; CONCENTRATION (COMPOSITION); ECOTOXICOLOGY; EMBRYO; FISH; HORMONE; INHIBITION; PHYSIOLOGY; ULTRAVIOLET RADIATION;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENVIRONMENTAL MONITORING; ENZYME ACTIVATION; FATTY ACID METABOLISM; GENETIC TRANSCRIPTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HORMONE ACTION; IN VITRO STUDY; LIPID METABOLISM; LIQUID LIQUID EXTRACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; SIGNAL TRANSDUCTION; STEROIDOGENESIS; TRANSCRIPTION REGULATION; ULTRAVIOLET IRRADIATION; ZEBRA FISH; 1H-BENZOTRIAZOLE; 2-(2-HYDROXY-5-METHYLPHENYL)BENZOTRIAZOLE (UV-P); 2-(3-T-BUTYL-2-HYDROXY-5-METHYLPHENYL)-5-CHLOROBENZOTRIAZOLE (UV-326); ANIMAL; ANIMAL EMBRYO; BENZOTRIAZOLE UV STABILIZERS; DRUG EFFECT; METABOLISM; PRENATAL DEVELOPMENT; TRANSCRIPTOMICS; ULTRAVIOLET RADIATION; WATER POLLUTANT;

1H-BENZOTRIAZOLE; 2-(2-HYDROXY-5-METHYLPHENYL)BENZOTRIAZOLE (UV-P); 2-(3-T-BUTYL-2-HYDROXY-5-METHYLPHENYL)-5-CHLOROBENZOTRIAZOLE (UV-326); BENZOTRIAZOLE UV STABILIZERS; TRANSCRIPTOMICS; ZEBRAFISH;

ANDROGEN ANTAGONISTS; ANIMALS; CYTOCHROME P-450 CYP1A1; EMBRYO, NONMAMMALIAN; RECEPTORS, ARYL HYDROCARBON; TRIAZOLES; ULTRAVIOLET RAYS; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

EID: 84905393259     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2014.02.109     Document Type: Article

References (68)

1. Alsop D., Vijayan M.M. Development of the corticosteroid stress axis and receptor expression in zebrafish. Am J Physiol Regul Integr Comp Physiol 2008, 294(3):R711-R719.
2. Andreasen E.A., Hahn M.E., Heidemann W., Peterson R.E., Tanguay R.L. The zebrafish (Danio rerio) aryl hydrocarbon receptor type 1 is a novel vertebrate receptor. Mol Pharmacol 2002, 62:234-249.
3. Andreasen E.A., Spitsbergen J.M., Tanguay R.L., Stegeman J.J., Heideman W., Peterson R.E. Tissue-specific expression of AHR2, ARNT2, and CYP1A in zebrafish embryos and larvae: effects of developmental stage and 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure. Toxicol Sci 2002, 419:403-419.
4. Arukwe A., Nordtug T., Kortner T.M., Mortensen A.S., Brakstad O.G. Modulation of steroidogenesis and xenobiotic biotransformation responses in zebrafish (Danio rerio) exposed to water-soluble fraction of crude oil. Environ Res 2008, 107:362-370.
5. Asimakopoulos A.G., Wang L., Thomaidis N.S., Kannan K. Benzotriazoles and benzothiazoles in human urine from several countries: a perspective on occurrence, biotransformation and human exposure. Environ Int 2013, 59:274-281.
6. Bachelot M., Li Z., Munaron D., Le Gall P., Casellas C., Fenet H., et al. Organic UV-filter concentrations in marine mussels from French coastal regions. Sci Total Environ 2012, 420:273-279.
7. Billiard S.M., Timme-Laragy A.R., Wassenberg D.M., Cockman C., Di Giulio R.T. The role of the AHR pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol Sci 2006, 92:526-536.
8. Blüthgen N., Zucchi S., Fent K. Effects of the UV-filter benzophenone-3 (oxybenzone) at low concentrations in zebrafish (Danio rerio). Toxicol Appl Pharmacol 2012, 263:184-194.
9. Blüthgen N., Meili N., Chew G., Odermatt A., Fent K. Accumulation and profile of the UV-filter octocrylene in adult and embryonic zebrafish. Sci Total Environ 2014, 476-477:207-217.
10. Breedveld G.D., Roseth R., Sparrevik M., Hartnik T., Hem L.J. Persistence of the de-icing additive benzotriazole at an abandoned airport. Water Air Soil Pollut Focus 2003, 3:91-101.
11. Cawkwell L., Lewis F.A., Quirke I. Frequency of allele loss of DCC, p53, RBI, WTI, NFI, NM23 and APC/MCC in colorectal cancer assayed by fluorescent multiplex polymerase chain reaction. Brit J Cancer 1994, 70:813-818.
12. Choi J.E., Kim S., Ahn J.H., Youn P., Kang J.S., Park K., et al. Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquat Toxicol 2010, 100(2):151-159.
13. Christen V., Fent K. Tissue-, sex- and developmental-specific transcription profiles of eight UDP-glucuronosyltransferase in zebrafish (Danio rerio) and regulation by activator of aryl hydrocarbon receptor. Aquat Toxicol 2014, [in press]. 10.1016/j.aquatox.2014.02.019.
14. Christen V., Zucchi S., Fent K. Effects of the UV-filter 2-ethyl-hexyl-4-trimethoxycinnamate (EHMC) on expression of genes involved in hormonal pathways in fathead minnows (Pimephales promelas) and link to vitellogenin induction and histology. Aquat Toxicol 2011, 102:167-176.
15. Corsi S.R., Zitomer D.H., Field J.A., Cancilla D.A. Nonylphenolethoxylates and other additives in aircraft de-icers, anti-icers, and waters receiving airport runoff. Environ Sci Technol 2003, 37:4031-4037.
16. Deng J., Yu L., Liu C., Yu K., Shi X., Yeung L.W.Y., et al. Hexabromocyclododecane-induced developmental toxicity and apoptosis in zebrafish embryos. Aquat Toxicol 2009, 93(1):29-36.
17. Díaz-Cruz M.S., Gago-Ferrero P., Llorca M., Barceló D. Analysis of UV-filters in tap water and other clean waters in Spain. Anal Bioanal Chem 2012, 402:2325-2333.
18. Evans B.R., Karchner S.I., Franks D.G., Hahn M.E. Duplicate aryl hydrocarbon receptor repressor genes (ahrr1 and ahrr2) in the zebrafish Danio rerio: structure, function, evolution, and AHR-dependent regulation in vivo. Arch Biochem Biophys 2005, 441:151-167.
19. Fent K., Kunz P.Y., Gomez E. UV filters in the aquatic environment induce hormonal effects and affect fertility and reproduction in fish. Chimia 2008, 62:368-375.
20. Fent K., Zenker A., Rapp M. Widespread occurrence of estrogenic UV-filters in aquatic ecosystems in Switzerland. Environ Pollut 2010, 158:1817-1824.
21. Fuzzen M.L.M., Bernier N.J., Van Der Kraak G. Differential effects of 17β-estradiol and 11-ketotestosterone on the endocrine stress response in zebrafish (Danio rerio). Gen Comp Endocrinol 2011, 170:365-373.
22. Gerhard G.S., Kauffman E.J., Grundy M.A. Molecular cloning and sequence analysis of the Danio rerio catalase gene. Comp Biochem Physiol 2000, 127:447-457.
23. Giger W., Schaffner C., Kohler H.E. Benzotriazole and tolyltriazole as aquatic contaminants. 1. Input and occurrence in rivers and lakes. Environ Sci Technol 2006, 40:7186-7192.
24. Gomez E., Pillon A., Fenet H., Rosain D., Duchesne M.J., Nicolas J.C., et al. Estrogenic activity of cosmetic components in reporter cell lines: parabens, UV screens, and musks. J Toxicol Environ Health A 2005, 68:239-251.
25. Harris C.A., Routledge E.J., Schaffner C., Brian J.V., Giger W., Sumpter J.P. Benzotriazole is antiestrogenic in vitro but not in vivo. Environ Toxicol Chem 2007, 26:2367-2372.
26. Hart D.S., Davis L.C., Erickson L.E., Callender T.M. Sorption and partitioning parameters of benzotriazole compounds. Microchem J 2004, 77:9e17.
27. He T., Liang B., Liu W., Shin P.K.S., Wu R.S.S. Estrogenic potential of benzotriazole on marine medaka (Oryzias melastigma). Ecotoxicol Environ Saf 2012, 80:327-332.
28. Hirata-Koizumi M., Watari N., Mukai D., Imai T., Hirose A., Kamata E., et al. A 28-day repeated dose toxicity study of ultraviolet absorber 2-(2'-hydroxy-3',5'-di-tert-butylphenyl) benzotriazole in rats. Drug Chem Toxicol 2007, 30:327-341.
29. Hoffmann J.L., Torontali S.P., Thomason R.G., Lee D.M., Brill J.L., Price B.B., et al. Hepatic gene expression profiling using genechips in zebrafish exposed to 17alpha-ethynylestradiol. Aquat Toxicol 2006, 79:233-246.
30. Hoffmann J.L., Thomason R.G., Lee D.M., Brill J.L., Price B.B., Carr G.J., et al. Hepatic gene expression profiling using GeneChips in zebrafish exposed to 17α-methyldihydrotestosterone. Aquat Toxicol 2008, 87:69-80.
31. Hossain M.S., Larsson A., Scherbak N., Olsson P.E., Orban L. Zebrafish androgen receptor: isolation, molecular, and biochemical characterization. Biol Reprod 2008, 78(2):361-369.
32. Janna H., Scrimshaw M.D., Williams R.J., Chrchley J., Sumpter J.P. From dishwasher to tap? Xenobiotic substances bentotriazole and tolyltriazole in the environment. Environ Sci Technol 2011, 45:3858-3864.
33. Kim J.W., Isobe T., Ramaswamy B.R., Chang K.H., Amano A., Miller T.M., et al. Contamination and bioaccumulation of benzotriazole ultraviolet stabilizers in fish from Manila Bay, the Philippines using an ultra-fast liquid chromatography-tandem mass spectrometry. Chemosphere 2011, 85:751-758.
34. Kim J.W., Chang K.H., Isobe T., Tanabe S. Acute toxicity of benzotriazole ultraviolet stabilizers on freshwater crustacean (Daphnia pulex). J Toxicol Sci 2011, 36:247-251.
35. Kunz P.Y., Fent K. Multiple hormonal activities of UV-filters and comparison of in vivo and in vitro estrogenic activity of ethyl-4-aminobenzoate in fish. Aquat Toxicol 2006, 79:305-324.
36. Liu T.A., Bhuiyan S., Snow R., Yasuda S., Yasuda T., Yang Y.S., et al. Identification and characterization of two novel cytosolic sulfotransferases, SULT1 ST7 and SULT1 ST8, from zebrafish. Aquat Toxicol 2008, 89(2):94-102.
37. Liu C., Wang Q., Liang K., Liu J., Zhou B., Zhang X., et al. Effects of tris(1,3-dichloro-2-propyl) phosphate and triphenyl phosphate on receptor-associated mRNA expression in zebrafish embryos/larvae. Aquat Toxicol 2013, 128-129:147-157.
38. Liu R., Ruan T., Wang T., Song S., Guo F., Jiang G. Determination of nine benzotriazole UV stabilizers in environmental water samples by automated on-line solid phase extraction coupled with high-performance liquid chromatography-tandem mass spectrometry. Talanta 2014, 120:158-166.
39. -δδCtmethod. Methods 2001, 25:402-408.
40. Loos R., Gawlik B.M., Locoro G., Rimaviciute E., Contini S., Bidoglio G. EU-wide survey of polar organic persistent pollutants in European river waters. Environ Pollut 2009, 157:561-568.
41. Loos R., Locoro G., et al. Pan-European survey on the occurrence of selected polar organic persistent pollutants in ground water. Water Res 2010, 44:4115-4126.
42. Martyniuk C.J., Gerrie E.R., Popesku J.T., Ekker M., Trudeau V.L. Microarray analysis in the zebrafish (Danio rerio) liver and telencephalon after exposure to low concentration of 17alpha-ethinylestradiol. Aquat Toxicol 2007, 84:38-49.
43. Montesdeoca-Esponda S., Sosa-Ferrera Z., Santana-Rodriguez J.J. On-line solid phase extraction coupled to ultra-performance liquid chromatography with tandem mass spectrometry detection for the determination of benzotriazole UV stabilizers in coastal marine and wastewater samples. Anal Bioanal Chem 2012, 403:867-876.
44. Moroshi K., Yamamoto H., Kamata R., Shiraishi F., Koda T., Morita M. Estrogenic activity of 37 components of commercial sunscreen lotions evaluated by in vitro assays. Toxicol in Vitro 2005, 19:457-469.
45. Nakata H., Murata S., Filatreau J. Occurrence and concentrations of benzotrizole UV stabilizers in marine organisms and sediments from the Ariake Sea, Japan. Environ Sci Technol 2009, 43:6920-6926.
46. Nakata H., Shinohara R., Murata S., Watanabe M. Detection of benzotriazole UV stabilizers in the blubber of marine mammals by gas chromatography-high resolution mass spectrometry (GC-HRMS). J Environ Monit 2010, 12:2088-2092.
47. Nakata H., Shinohara R.I., Nakazawa Y., Isobe T., Sudarynto A., Subramanian A., et al. Asia-Pacific mussel watch for emerging pollutants: distribution of synthetic musk and benzotriazole UV stabilizers in Asian and US coastal waters. Mar Pollut Bull 2012, 64:2211-2218.
48. Parks N. UV stabilizing chemicals contaminating Japans marine environment. Environ Sci Technol 2009, 43:6896-6897.
49. Pillard D.A., Cornell J.S., Dufresne D.L., Hernandez M.T. Toxicity of benzotriazole and benzotriazole derivatives to three aquatic species. Water Res 2001, 35:557-560.
50. Prasch A.L., Teraoka H., Carney S.A., Dong W., Hiraga T., Stegeman J.J., et al. Aryl hydrocarbon receptor 2 mediates 2,3,7,8-tetrachlorodibenzo-p-dioxin developmental toxicity in zebrafish. Toxicol Sci 2003, 76:138-150.
51. Reddy C.M. Comment on "Occurrence and concentrations of benzotrizole UV stablilizers in marine organisms and sediments from the Ariake Sea, Japan". Environ Sci Technol 2009, 43:7998.
52. Reddy C.M., Quinn J.G., King J.K. Free and bound benzotriazoles in marine and freshwater sediments. Environ Sci Technol 2000, 34:973-979.
53. Reemtsma T., Weiss S., Mueller J., Petrovic M., Gonzalez S., Barcelo D., et al. Polar pollutants entry into the water cycle by municipal wastewater: a European perspective. Environ Sci Technol 2006, 40:5451-5458.
54. Routledge E.J., Sumpter J.P. Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen. Environ Toxicol Chem 1996, 15:241-248.
55. Ruan T., Liu R., Fu Q., Wang T., et al. Concentrations and composition profiles of benzotriazole UV stabilizers in municipal sewage sludge in China. Environ Sci Technol 2012, 46:2071-2079.
56. Safe S., Lee S.O., Jin U.H. Role of the aryl hydrocarbon receptor in carcinogenesis and potential as a drug target. Toxicol Sci 2013, 135:1-16.
57. Seeland A., Oetken M., Kiss A., Fries E., Oehlmann J. Acute and chronic toxicity of benzotriazoles to aquatic organisms. Environ Sci Pollut Res 2012, 19:1781-1790.
58. Sohoni P., Sumpter J.P. Several environmental oestrogens are also anti-androgens. J Endocrinol 1998, 158:327-339.
59. Suzuki T., Takagi Y., Osanai H., Li L., Takeuchi M., Katoh Y., et al. Pi class glutathione S-transferase genes are regulated by Nrf2 through an evolutionarily conserved regulatory element in zebrafish. Biochem J 2005, 73:65-73.
60. Tanguay R.L., Abnet C.C., Heideman W., Peterson R.E. Cloning and characterization of the zebrafish (Danio rerio) aryl hydrocarbon receptor 1. Biochim Biophys Acta 1999, 1444:35-48.
61. Van Leerdam J.A., Hogenboom A.C., van der Kooi M.M.E., de Voogt P. Determination of polar 1H-benzotriazoles and benzothiazoles in water by solid-phase extraction and liquid chromatography LTQ FT Orbitrap mass spectrometry. Int J Mass Spectr 2009, 282:99-107.
62. Voutsa D., Hartmann P., Schaffner C., Giger W. Benzotriazoles, alkylphenols, and bisphenol A in municipal wastewaters and in the Glatt River, Switzerland. Environ Sci Pollut Res Int 2006, 13:333-341.
63. Wang L., Asimakopoulos A.G., Moon H.B., Nakata H., Kannan K. Benzotriazole, benzothiazole, and benzophenone compounds in indoor dust from the United States and East Asian countries. Environ Sci Technol 2013, 47:4752-4759.
64. Weisbrod C.J., Kunz P.Y., Zenker A.K., Fent K. Effects of the UV-filter benzophenone-2 on reproduction in fish. Toxicol Appl Pharmacol 2007, 225:255-266.
65. Weiss S., Reemtsma T. Determination of benzotriazole corrosion inhibitors from aqueous environmental samples by liquid chromatography-electrospray ionization-tandem mass spectrometry. Anal Chem 2005, 77:7415-7420.
66. Zhao X., Xu B., Wu F., Zhao, Liao H. Benzotriazole removal from water by Zn-Al-O binary metal oxide adsorbent: behavior, kinetics and mechanism. J Hazard Mater 2010, 184:147-155.
67. Zhang Z., Ren N., Li Y.F., Kunisue T., Gao D., Kannan K. Determination of benzotriazole and benzophenone UV filters in sediment and sewage sludge. Environ Sci Technol 2011, 45:3909-3916.
68. Zucchi S., Blüthgen N., Ieronimo A., Fent K. The UV-absorber benzophenone-4 alters transcripts of genes involved in hormonal pathways in zebrafish (Danio rerio) eleuthero-embryos and adult males. Toxicol Appl Pharmacol 2011, 250:137-146.