Benzotriazole ultraviolet stabilizers show potent activities as human aryl hydrocarbon receptor ligands

Environmental Science and Technology

Volumn 49, Issue 1, 2015, Pages 578-587

  Nagayoshi, Haruna ^a   Kakimoto, Kensaku ^a   Takagi, Sokichi ^a   Konishi, Yoshimasa ^a   Kajimura, Keiji ^a   Matsuda, Tomonari ^b  

^a OSAKA PREFECTURAL INSTITUTE OF PUBLIC HEALTH   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBONS; CONSUMER PRODUCTS; ENDOCRINOLOGY; HORMONES; HYDROCARBONS; PIGMENTS; POLYCYCLIC AROMATIC HYDROCARBONS;

AGONISTIC ACTIVITY; AQUATIC ENVIRONMENTS; ARYL HYDROCARBON RECEPTOR; EFFECTIVE CONCENTRATION; PHYSIOLOGICAL EFFECTS; SIMULTANEOUS MONITORING; THYROID HORMONE RECEPTOR; ULTRAVIOLET STABILIZERS;

LIGANDS;

AROMATIC HYDROCARBON RECEPTOR; BENZOTRIAZOLE DERIVATIVE; CYTOCHROME P450 1A1; STABILIZING AGENT; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA; AHR PROTEIN, HUMAN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BENZOTRIAZOLE; LIGAND; THYROID HORMONE RECEPTOR; TRIAZOLE DERIVATIVE;

AQUATIC ENVIRONMENT; BIOASSAY; CONCENTRATION (COMPOSITION); ENZYME ACTIVITY; HORMONE; HUMAN ACTIVITY; LIGAND; METABOLISM; YEAST;

AGAR GEL ELECTROPHORESIS; ARTICLE; CARBON SOURCE; CONTROLLED STUDY; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME DEGRADATION; ESCHERICHIA COLI; LIGAND BINDING; LONG TERM EXPOSURE; MARINE SPECIES; NONHUMAN; REPORTER GENE; SACCHAROMYCES CEREVISIAE; TERATOGENESIS; ULTRAVIOLET RADIATION; CHEMISTRY; HUMAN; METABOLISM; REGRESSION ANALYSIS;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CYTOCHROME P-450 CYP1A1; HUMANS; LIGANDS; RECEPTORS, ARYL HYDROCARBON; RECEPTORS, THYROID HORMONE; REGRESSION ANALYSIS; SACCHAROMYCES CEREVISIAE; TRIAZOLES; ULTRAVIOLET RAYS;

EID: 84924993224     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es503926w     Document Type: Article

References (64)

1. Boxall, A. B.; Rudd, M. A.; Brooks, B. W.; Caldwell, D. J.; Choi, K.; Hickmann, S.; Innes, E.; Ostapyk, K.; Staveley, J. P.; Verslycke, T.; Ankley, G. T.; Beazley, K. F. Review pharmaceuticals and personal care products in the environment: What are the big questions ? Environ. Health Perspect. 2012, 120 (9), 1221-1229 DOI: 10.1289/ ehp.1104477.
2. Brausch, J. M.; Rand, G. M. A review of personal care products in the aquatic environment: Environmental concentrations and toxicity. Chemosphere 2011, 82 (11), 1518-1532 DOI: 10.1016/j.chemosphere. 2010.11.018.
3. Nakata, H.; Murata, S.; Filatreau, J. Occurrence and concentrations of benzotriazole UV stabilizers in marine organisms and sediments from the Ariake Sea, Japan. Environ. Sci. Technol. 2009, 43 (18), 6920-6926 DOI: 10.1021/es900939j.
4. Montesdeoca-Esponda, S.; Sosa-Ferrera, Z.; Santana-Rodríguez, 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 (3), 867-876 DOI: 10.1007/s00216-012-5906-x.
5. Stasinakis, A. S.; Thomaidis, N. S.; Arvaniti, O. S.; Asimakopoulos, A. G.; Samaras, V. G.; Ajibola, A.; Mamais, D.; Lekkas, T. D. Contribution of primary and secondary treatment on the removal of benzothiazoles, benzotriazoles, endocrine disruptors, pharmaceuticals and perfluorinated compounds in a sewage treatment plant. Sci. Total Environ. 2013, 463-464, 1067-1075 DOI: 10.1016/ j.scitotenv.2013.06.087.
6. 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 (9), 3909-3916 DOI: 10.1021/es2004057.
7. Kim, J. W.; Isobe, T.; Malarvannan, G.; Sudaryanto, A.; Chang, K. H.; Prudente, M.; Tanabe, S. Contamination of benzotriazole ultraviolet stabilizers in house dust from the Philippines: Implications on human exposure. Sci. Total Environ. 2012, 424 (1), 174-181 DOI: 10.1016/j.scitotenv.2012.02.040.
8. National Institute of Technology and Evaluation-Japan CHEmicals Collaborative Knowledge database (J-CHECK) Website; http://www. safe.nite.go.jp/jcheck/List6Action?category= 211&request-locale=en.
9. National Institute of Technology and Evaluation Chemical Risk Information Platform (CHIRP) Website; http://www.safe.nite.go.jp/ english/sougou/view/ComprehensiveInfoDisplay-en.faces.
10. Hirata-Koizumi, M.; Ogata, H.; Imai, T.; Hirose, A.; Kamata, E.; Ema, M. A 52-week repeated dose toxicity study of ultraviolet absorber 2-(2′-hydroxy-3′,5′-di-tert-butylphenyl)benzotriazole in rats. Drug Chem. Toxic ol. 2008, 31 (1), 81-96 DOI: 10.1080/ 01480540701688758.
11. Kim, J. W.; Isobe, T.; Ramaswamy, B. R.; Chang, K. H.; Amano, A.; Miller, T. M.; Siringan, F. P.; Tanabe, S. 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 (5), 751-758 DOI: 10.1016/j.chemosphere.2011.06.054.
12. 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 DOI: 10.2131/jts.36.247.
13. Schlumpf, M.; Cotton, B.; Conscience, M.; Haller, V.; Steinmann, B.; Lichtensteiger, W. In vitro and in vivo estrogenicity of UV screens. Environ. Health Perspect. 2001, 109 (3), 239-244.
14. Schlumpf, M.; Kypke, K.; Wittassek, M.; Angerer, J.; Mascher, H.; Mascher, D.; Vökt, C.; Birchler, M.; Lichtensteiger, W. Exposure patterns of UV filters, fragrances, parabens, phthalates, organochlor pesticides, PBDEs, and PCBs in human milk: Correlation of UV filters with use of cosmetics. Chemosphere 2010, 81 (10), 1171-1183 DOI: 10.1016/j.chemosphere.2010.09.079.
15. Tinwell, H.; Lefevre, P. A.; Moffat, G. J.; Burns, A.; Odum, J.; Spurway, T. D.; Orphanides, G.; Ashby, J. Confirmation of uterotrophic activity of 3-(4-methylbenzylidine)camphor in the immature rat. Environ. Health Perspect. 2002, 110 (5), 533-536.
16. Kawamura, Y.; Ogawa, Y.; Nishimura, T.; Kikuchi, Y.; Nishikawa, J. I.; Nishihara, T.; Tanamoto, K. Estrogenic activities of UV stabilizers used in food contact plastics and benzophenone derivatives tested by the yeast two-hybrid assay. J. Health Sci. 2003, 49 (3), 205-212 DOI: 10.1248/jhs.49.205.
17. Morohoshi, 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 (4), 457-469 DOI: 10.1016/j.tiv.2005.01.004.
18. Fent, K.; Chew, G.; Li, J.; Gomez, E. Benzotriazole UVstabilizers and benzotriazole: Antiandrogenic activity in vitro and activation of aryl hydrocarbon receptor pathway in zebrafish eleutheroembryos. Sci. Total Environ. 2014, 482-483, 125-136 DOI: 10.1016/ j.scitotenv.2014.02.109.
19. Zhang, S.; Qin, C.; Safe, S. H. Flavonoids as aryl hydrocarbon receptor agonists/antagonists: Effects of structure and cell context. Environ. Health Perspect. 2003, 111 (16), 1877-1882 DOI: 10.1289/ ehp.6322.
20. Denison, M. S.; Nagy, S. R. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol. 2003, 43, 309-334 DOI: 10.1146/ annurev.pharmtox.43.100901.135828.
21. Fernandez-Salguero, P. M.; Hilbert, D. M.; Rudikoff, S.; Ward, J. M.; Gonzalez, F. J. Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol. Appl. Pharmacol. 1996, 140 (1), 173-179 DOI: 10.1006/ taap.1996.0210.
22. Gonzalez, F. J.; Fernandez-Salguero, P. The aryl hydrocarbon receptor: Studies using the AHR-null mice. Drug Metab. Dispos. 1998, 26 (12), 1194-1198.
23. Mimura, J.; Yamashita, K.; Nakamura, K.; Morita, M.; Takagi, T. N.; Nakao, K.; Ema, M.; Sogawa, K.; Yasuda, M.; Katsuki, M.; Fujii-Kuriyama, Y. Loss of teratogenic response to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice lacking the Ah (dioxin) receptor. Genes Cells 2003, 2 (10), 645-654 DOI: 10.1046/j.1365-2443.1997.1490345.x.
24. Evans, R. The steroid and thyroid hormone receptor superfamily. Science 1988, 240 (4854), 889-895 DOI: 10.1126/ science.3283939.
25. Zhang, J.; Lazar, M. A. The mechanism of action of thyroid hormones. Annu. Rev. Physiol. 2000, 62, 439-466 DOI: 10.1146/ annurev.physiol.62.1.439.
26. Mullur, R.; Liu, Y. Y.; Brent, G. A. Thyroid hormone regulation of metabolism. Physiol. Rev. 2014, 94, 355-382 DOI: 10.1152/ physrev.00030.2013.
27. Remaud, S.; Gothié, J. D.; Morvan-Dubois, G.; Demeneix, B. A. Thyroid hormone signaling and adult neurogenesis in mammals. Front. Endocrinol. 2014, 5 (62), 1-7 DOI: 10.3389/fendo.2014.00062.
28. Schroeder, A. C.; Privalsky, M. L. Thyroid hormones, T3 and T4, in the brain. Front. Endocrinol. 2014, 5 (40), 1-6 DOI: 10.3389/ fendo.2014.00040.
29. Lazar, M. A.; Chin, W. W. Nuclear thyroid hormone receptors. J. Clin. Invest. 1990, 86 (6), 1777-1782 DOI: 10.1172/JCI114906.
30. Amano, I.; Miyazaki, W.; Iwasaki, T.; Shimokawa, N.; Koibuchi, N. The effect of hydroxylated polychlorinated biphenyl (OH-PCB) on thyroid hormone receptor (TR)-mediated transcription through native-thyroid hormone response element (TRE). Ind. Health 2010, 48 (1), 115-118 DOI: 10.2486/indhealth.48.115.
31. Cantón, R. F.; Sanderson, J. T.; Nijmeijer, S.; Bergman, A.; Letcher, R. J.; Van Den Berg, M. In vitro effects of brominated flame retardants and metabolites on CYP17 catalytic activity: A novel mechanism of action? Toxicol. Appl. Pharmacol. 2006, 216 (2), 274-281 DOI: 10.1016/j.taap.2006.05.007.
32. Li, F.; Xie, Q.; Li, X.; Li, N.; Chi, P.; Chen, J.; Wang, Z.; Hao, C. Hormone activity of hydroxylated polybrominated diphenyl ethers on human thyroid receptor-beta: In vitro and in silico investigations. Environ. Health Perspect. 2010, 118 (5), 602-606 DOI: 10.1289/ ehp.0901457.
33. Zhou, T.; Taylor, M. M.; Devito, M. J.; Crofton, K. M. Developmental exposure to brominated diphenyl ethers results in thyroid hormone disruption. Toxicol. Sci. 2002, 66 (1), 105-116 DOI: 10.1093/toxsci/66.1.105.
34. Miller, C. A. A human aryl hydrocarbon receptor signaling pathway constructed in yeast displays additive responses to ligand mixtures. Toxicol. Appl. Pharmacol. 1999, 160 (3), 297-303 DOI: 10.1006/taap.1999.8769.
35. Kawanishi, M.; Ohnisi, K.; Takigami, H.; Yagi, T. Simple and rapid yeast reporter bioassay for dioxin screening: Evaluation of the dioxin-like compounds in industrial and municipal waste incineration plants. Environ. Sci. Pollut. Res. Int. 2013, 20 (5), 2993-3002 DOI: 10.1007/s11356-012-1214-4.
36. Shiizaki, K.; Asai, S.; Ebata, S.; Kawanishi, M.; Yagi, T. Establishment of yeast reporter assay systems to detect ligands of thyroid hormone receptors alpha and beta. Toxicol. In Vitro 2010, 24 (2), 638-644 DOI: 10.1016/j.tiv.2009.10.001.
37. Miller, C. A. Assessment of aryl hydrocarbon receptor complex interactions using pBEVY plasmids: Expressionvectors with bidirectional promoters for use in Saccharomyces cerevisiae. Nucleic Acids Res. 1998, 26 (15), 3577-3583 DOI: 10.1093/nar/26.15.3577.
38. Adachi, J.; Mori, Y.; Matsui, S.; Takigami, H.; Fujino, J.; Kitagawa, H.; Miller, C. A.; Kato, T.; Saeki, K.; Matsuda, T. Indirubin and indigo are potent aryl hydrocarbon receptor ligands present in human urine. J. Biol. Chem. 2001, 276 (34), 31475-31478 DOI: 10.1074/jbc.C100238200.
39. Gietz, R. D.; Woods, R. A. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 2002, 350, 87-96 DOI: 10.1016/S0076-6879(02) 50957-5.
40. Nthangeni, M. B.; Urban, P.; Pompon, D.; Smit, M. S.; Nicaud, J. M. The use of Yarrowia lipolytica for the expression of human cytochrome P450 CYP1A1. Yeast 2004, 21 (7), 583-592 DOI: 10.1002/yea.1127.
41. Hanioka, N.; Tatarazako, N.; Jinno, H.; Arizono, K.; Ando, M. Determination of cytochrome P450 1A activities in mammalian liver microsomes by high-performance liquid chromatography with fluorescence detection. J. Chromatogr. B. Biomed. Sci. Appl. 2000, 744 (2), 399-406 DOI: 10.1016/S0378-4347(00)00278-4.
42. Chemical Information Review Document for Phenolic Benzotriazole. Supporting Nomination for Toxicological Evaluation by the National Toxicology Program; United States National Toxicology Program: Research Triangle Park, NC, 2011; http://ntp.niehs.nih.gov/ntp/ noms/support-docs/phenolicbenzotriazoles-cird-oct2011-508.pdf.
43. Screening of Benzothiazoles, Benzenediamines, Dicyclohexylamine and Benzotriazoles 2009; Report Number B2023; IVL Swedish Environmental Research Institute Ltd.: Stockholm, 2011; http:// www.ivl.se/download/18.3175b46c133e617730d80009737/ 1350484316250/B2023.pdf.
44. Kameda, Y.; Kimura, K.; Miyazaki, M. Occurrence and profiles of organic sun-blocking agents in surface waters and sediments in Japanese rivers and lakes. Environ. pollut. 2011, 159, 1570-1576 DOI: 10.1016/j.envpol.2011.02.055.
45. Kim, J. W.; Ramaswamy, B. R.; Chang, K. H.; Isobe, T.; Tanabe, S. Multiresidue analytical method for the determination of antimicrobials, preservatives, benzotriazole UV stabilizers, flame retardants and plasticizers in fish using ultra high performance liquid chromatography coupled with tandem mass spectrometry. J. Chromatogr. A 2011, 1218 (22), 3511-3520 DOI: 10.1016/ j.chroma.2011.04.006.
46. Carpinteiro, I.; Abuín, B.; Rodríguez, I.; Ramil, M.; Cela, R. Pressurized solvent extraction followed by gas chromatography tandem mass spectrometry for the determination of benzotriazole light stabilizers in indoor dust. J. Chromatogr. A 2010, 1217, 3729-3735 DOI: 10.1016/j.chroma.2010.04.022.
47. Oberg, M.; Bergander, L.; Håkansson, H.; Rannug, U.; Rannug, A. Identification of the tryptophan photoproduct 6-formylindolo[3,2-b]carbazole, in cell culture medium, as a factor that controls the background aryl hydrocarbon receptor activity. Toxicol. Sci. 2005, 85 (2), 935-943 DOI: 10.1093/toxsci/kfi154.
48. Adachi, J.; Mori, Y.; Matsui, S.; Matsuda, T. Comparison of gene expression patterns between 2,3,7,8-tetrachlorodibenzo-p-dioxin and a natural arylhydrocarbon receptor ligand, indirubin. Toxicol. Sci. 2004, 80 (1), 161-169 DOI: 10.1093/toxsci/kfh129.
49. Wei, Y. D.; Helleberg, H.; Rannug, U.; Rannug, A. Rapid and transient induction of CYP1A1 gene expression in human cells by the tryptophan photoproduct 6-formylindolo[3,2-b]carbazole. Chem. Biol. Interact. 1998, 110 (1-2), 39-55 DOI: 10.1016/S0009-2797(97) 00111-7.
50. Nebert, D. W.; Dalton, T. P.; Okey, A. B.; Gonzalez, F. J. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 2004, 279, 23847-23850 DOI: 10.1074/jbc.R400004200.
51. Mimura, J.; Fujii-Kuriyama, Y. Functional role of AhR in the expression of toxic effects by TCDD. Biochem. Biophys. Acta 2003, 1619 (3), 263-268 DOI: 10.1016/S0304-4165(02)00485-3.
52. Nebert, D. W.; Roe, A. L.; Dieter, M. Z.; Solis, W. A.; Yang, Y.; Dalton, T. P. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 2000, 59 (1), 65-85 DOI: 10.1016/ S0006-2952(99)00310-X.
53. Puga, A.; Xia, Y.; Elferink, C. Role of the aryl hydrocarbon receptor in cell cycle regulation. Chem. Biol. Interact. 2002, 141 (1-2), 117-130 DOI: 10.1016/S0009-2797(02)00069-8.
54. Schrenk, D. Impact of dioxin-type induction of drugmetabolizing enzymes on the metabolism of endo-And xenobiotics. Biochem. Pharmacol. 1998, 55 (8), 1155-1162 DOI: 10.1016/S0006-2952(97)00591-1.
55. Chiba, T.; Chihara, J.; Furue, M. Role of the arylhydrocarbon receptor (AhR) in the Pathology of Asthma and COPD. J. Allergy 2012, 2012 (2012), 372384 DOI: 10.1155/2012/372384.
56. Esser, C.; Rannug, A.; Stockinger, B. The aryl hydrocarbon receptor in immunity. Trends Immunol. 2009, 30 (9), 447-454 DOI: 10.1016/j.it.2009.06.005.
57. Stevens, E. A.; Mezrich, J. D.; Bradfield, C. A. The aryl hydrocarbon receptor: A perspective on potential roles in the immune system. Immunology 2009, 127 (3), 299-311 DOI: 10.1111/j.1365-2567.2009.03054.x.
58. Benson, J. M.; Shepherd, D. M. Dietary ligands of the aryl hydrocarbon receptor induce anti-inflammatory and immunoregulatory effects on murine dendritic cells. Toxicol. Sci. 2011, 124 (2), 327-338 DOI: 10.1093/toxsci/kfr249.
59. Duarte, J. H.; Di Meglio, P.; Hirota, K.; Ahlfors, H.; Stockinger, B. Differential influences of the aryl hydrocarbon receptor on Th17 mediated responses in vitro and in vivo. PloS one 2013, 8 (11), e79819 DOI: 10.1371/journal.pone.0079819.
60. Platzer, B.; Richter, S.; Kneidinger, D.; Waltenberger, D.; Woisetschläger, M.; Strobl, H. Aryl hydrocarbon receptor activation inhibits in vitro differentiation of human monocytes and Langerhans dendritic cells. J. Immunol. 2009, 183 (1), 66-74 DOI: 10.4049/ jimmunol.0802997.
61. Punj, S.; Kopparapu, P.; Jang, H. S.; Phillips, J. L.; Pennington, J.; Rohlman, D.; O'donnell, E.; Iversen, P. L.; Kolluri, S. K.; Kerkvliet, N. I. Benzimidazoisoquinolines: A new class of rapidly metabolized aryl hydrocarbon receptor (AhR) ligands that induce AhR-dependent Tregs and prevent murine graft-versus-host disease. PloS one 2014, 9 (2), e88726 DOI: 10.1371/journal.pone.0088726.
62. Wheeler, J. L.; Martin, K. C.; Resseguie, E.; Lawrence, B. P. Differential consequences of two distinct AhR ligands on innate and adaptive immune responses to influenza A virus. Toxicol. Sci. 2014, 137 (2), 324-334 DOI: 10.1093/toxsci/kft255.
63. Nguyen, N. T.; Hanieh, H.; Nakahama, T.; Kishimoto, T. The roles of aryl hydrocarbon receptor in immune responses. Int. Immunol. 2013, 25 (6), 335-343 DOI: 10.1093/intimm/dxt011.
64. Quintana, F. J.; Basso, A. S.; Iglesias, A. H.; Korn, T.; Farez, M. F.; Bettelli, E.; Caccamo, M.; Oukka, M.; Weiner, H. L. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 2008, 453, 65-71 DOI: 10.1038/nature06880.