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Aryl Hydrocarbon Receptor and Estrogen Receptor Ligand Activity of Organic Extracts from Road Dust and Diesel Exhaust Particulates

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Abstract

A wide variety of contaminants derived from diesel and gasoline engines, tire, asphalt, and natural organic compounds is found in road dust. Polycyclic aromatic compounds (PACs) are the important toxic targets among various contents in road dust and diesel exhaust particulates (DEPs), and endocrine-disrupting activity of PACs was suggested. In the present study, aryl hydrocarbon receptor (AhR) ligand activity was confirmed in the extract of both road dust and DEPs. In the separation of the extracts for both road dust and DEPs with reversed-phase HPLC, it was found that polar fractions contributed to significant AhR ligand activity in both a mouse hepatoma (H1L1) cell system and a yeast system. Furthermore, the contribution of these polar fractions was higher in DEPs than in road dust, probably because of the greater concentration of oxy-PAHs in DEPs than in road dust. The contribution of contaminants associated with the polar region to AhR ligand activity was also evident following the separation of road dust with normal-phase HPLC. Additionally, remarkable estrogen receptor (ER) ligand activity was detected in the highly polar region separated with normal-phase HPLC. It is suggested that many unknown AhR or ER ligand active compounds are contained in the polar region.

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References

  • Adachi J, Mori Y, Matsui S, Takigami H, Fujino J, Kitagawa H, Miller III CA, Kato T, Saeki K, Matsuda T (2001) Indirubin and indigo are potent aryl hydrocarbon receptor ligands present in human urine. J Biol Chem 276:31475–31478

    Article  CAS  Google Scholar 

  • Alsberg T, Strandell M, Westerholm R, Stenberg U (1985) Fractionation and chemical analysis of gasoline exhaust particulate extracts in connection with biological testing. Environ Int 11:249–257

    Article  CAS  Google Scholar 

  • Binková B, Leníček J, Beneš I, Vindová P, Gajdoš O, Fried M, Šrám RJ (1998) Genotoxicity of coke-oven and urban air particulate matter in in vitro acellular assays coupled with 32P-postlabeling and HPLC analysis of DNA adducts. Mutat Res 414:77–94

    Google Scholar 

  • Bols NC, Schirmer K, Joyce EM, Dixon DG, Greenberg BM, Whyte JJ (1999) Ability of polycyclic hydrocarbons to induce 7-ethoxyresorfin-o-deethylase activity in a trout liver cell line. Ecotoxicol Environ Saf 44:118–128

    Article  CAS  Google Scholar 

  • Burczynski ME, Penning (2000) Genotoxic polycyclic aromatic hydrocarbon ortho-quinones generated by aldo-keto reductases induce CYP1A1 via nuclear translocation of the aryl hydrocarbon receptor. Cancer Res 60:908–915

    CAS  Google Scholar 

  • Casellas M, Fernandez P, Bayona JM, Solanas AM (1995) Bioassay-directed chemical analysis of genotoxic components in urban airborne particulate matter from Barcelona (Spain). Chemosphere 30:725–740

    Article  CAS  Google Scholar 

  • Choi J, Oris JT (2003) Assessment of the toxicity of anthracene photo-modification products using the topminnow (Poeciliopsis lucida) hepatoma cell line (PLHC-1). Aquat Toxicol 65:243–251

    Article  CAS  Google Scholar 

  • Chou P-H, Matsui S, Matsuda T (2006) Detection and identification of dyes showing AhR-binding affinity in treated sewage effluents. Water Sci Technol 53(11):35–42

    Article  CAS  Google Scholar 

  • Chou P-H, Matsui S, Misaki K, Matsuda T (2007) Isolation and identification of xenobiotic aryl hydrocarbon receptor ligands in dyeing wastewater. Environ Sci Technol 41:652–657

    Article  CAS  Google Scholar 

  • Clemons JH, Allan IM, Marvin CH, Wu Z, McCarry BE, Bryant DW, Zacharewski TR (1998) Evidence of estrogen- and TCDD-like activities in crude and fractionated extracts of PM10 air particulate material using in vitro gene expression assays. Environ Sci Technol 32:1853–1860

    Article  CAS  Google Scholar 

  • Colborn T (2004) Endocrine disruption overview: Are males at risk? Adv Exp Med Biol 545:189–201

    CAS  Google Scholar 

  • Crepineau C, Rychen G, Feidt C, Le Roux Y, Lichtfouse E, Laurent F (2003) Contamination of pastures by polycyclic aromatic hydrocarbons (PAHs) in the vicinity of a highway. J Agr Food Chem 51:4841–4845

    Article  CAS  Google Scholar 

  • Denison M, Brouwer A, Clark G (1998) U.S. patent 5,854,010

  • Denison MS, Pandini A, Nagy SR, Baldwin EP, Bonati L (2002) Ligand binding and activation of the Ah receptor. Chem-Biol Interact 141:3–24

    Article  CAS  Google Scholar 

  • Durant JL, Busby WF Jr, Lafleur AL, Penman BW, Crespi CL (1996) Human cell mutagenicity of oxygenated, nitrated and unsubstituted polycyclic aromatic hydrocarbons associated with urban aerosols. Mutat Res 371:123–157

    Article  CAS  Google Scholar 

  • Fernandez P, Bayona JM (1992) Use of off-line gel permeation chromatography-normal-phase liquid chromatography for the determination of polycyclic aromatic compounds in environmental samples and standard reference materials (air particulate matter and marine sediment). J Chromatogr 625:141–149

    Article  CAS  Google Scholar 

  • Giesy JP, Hilsherova K, Jones PD, Kannan K, Machala M (2002) Cell bioassays for detection of aryl hydrocarbon (AhR) and estrogen receptor (ER) mediated activity in environmental samples. Mar Poll Bull 45:3–16

    Article  CAS  Google Scholar 

  • Hannigan MP, Cass GR, Penman BW, Crespi CL, Lafleur AL, Busby WF Jr, Thilly WG, Simoneit BRT (1998) Bioassay-directed chemical analysis of Los Angeles airborne particulate matter using a human cell mutagenicity assay. Environ Sci Technol 32:3502–3514

    Article  CAS  Google Scholar 

  • Hirose T, Morito K, Kizu R, Toriba A, Hayakawa K, Ogawa S, Inoue S., Muramatsu M, Masamune Y (2001) Estrogenic/antiestrogenic activities of benzo[a]pyrene monohydroxy derivatives. J Health Sci 47:552–558

    Article  CAS  Google Scholar 

  • IARC (1983) Polynuclear aromatic compounds. Part 1. Chemical, environmental and experimental data. IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. Vol. 32. IARC, Lyon, France

    Google Scholar 

  • Iida M, Oguri H (2003) Japan patent 2003180393

  • Jones JM, Anderson JW (1999) Relative potencies of PAHs and PCBs based on the response of human cells. Environ Toxicol Pharmacol 7:19–26

    Article  CAS  Google Scholar 

  • Kamiya M, Toriba A, Onoda Y, Kizu R, Hayakawa K (2005) Evaluation of estrogenic activities of hydroxylated polycyclic aromatic hydrocarbons in cigarette smoke condensate. Food Chem Toxicol 43:1017–1027

    Article  CAS  Google Scholar 

  • Kannan K, Villneuve DL, Yamashita N, Imagawa T, Hashimoto S, Miyazaki A, Giesy JP (2000) Vertical profile of dioxin-like and estrogenic activities associated with a sediment core from Tokyo Bay, Japan. Environ Sci Technol 34:3568–3573

    Article  CAS  Google Scholar 

  • Kawanishi M, Takamura-Enya T, Ermawati R, Shimohara C, Sakamoto M, Matsukawa K, Matsuda T, Murahashi T, Matsui S, Wakabayashi K, Watanabe T, Tashiro Y, Yagi T (2004) Detection of genistein as an estrogenic contaminant of river water in Osaka. Environ Sci Technol 38:6424–6429

    Article  CAS  Google Scholar 

  • Kitamura S, Kato T, Iida M, Jinno N, Suzuki T, Ohta S, Fujimoto N, Hanada H, Kashiwagi K, Kashiwagi A (2005) Anti-thyroid hormonal activity of tetrabromobisphenol A, a flame retardant, and related compounds: affinity to the mammalian thyroid hormone receptor, and effect on tadpole metamorphosis. Life Sci 76:1589–1601

    Article  CAS  Google Scholar 

  • Kizu R, Okamura K, Toriba A, Kakishima H, Mizokami A, Burnstein KL, Hayakawa K (2003) A role of aryl hydrocarbon receptor in the antiandrogenic effects of polycyclic aromatic hydrocarbons in LNCaP human prostate carcinoma cells. Arch Toxicol 77:335–343

    CAS  Google Scholar 

  • Kojima H, Iida M, Katsura E, Kanetoshi A, Hori Y, Kobayashi K (2003) Effects of a diphenyl ether-type herbicide, chlornitrofen, and its amino derivative on androgen and estrogen receptor activities. Environ Health Perspect 111:497–502

    Article  CAS  Google Scholar 

  • Lee B-C, Matsui S, Shimizu Y, Matsuda T (2005a) Characterization of the first flush in storm water runoff from an urban roadway. Environ Technol 26:773–782

    Article  CAS  Google Scholar 

  • Lee B-C, Shimizu Y, Matsuda T, Matsui S (2005b) Characterization of polycyclic aromatic hydrocarbons (PAHs) in different size fractions in deposited road particles (DRPs) from Lake Biwa area, Japan. Environ Sci Technol 39:7402–7409

    Article  CAS  Google Scholar 

  • Lee B-C, Matsui S, Shimizu Y, Matsuda T, Tanaka Y (2005c) A new installation for road runoff: up-flow filtration by porous polypropylene media. Water Sci Technol 52(12):225–232

    CAS  Google Scholar 

  • Letzel T, Pöshl U, Wissiack R, Rosenberg E, Grasserbauer M, Niessner R (2001) Phenyl-modified reversed-phase liquid chromatography coupled ionization mass spectrometry: a universal method for the analysis of partially oxidized aromatic hydrocarbons. Anal Chem 73:1634–1645

    Article  CAS  Google Scholar 

  • Machala M, Vondráček J, Bláha L, Ciganek M, Neča J (2001a) Aryl hydrocarbon receptor-mediated activity of mutagenic polycyclic aromatic hydrocarbons determined using in vitro reporter gene assay. Mutat Res 497:49–62

    CAS  Google Scholar 

  • Machala M, Ciganek M, Bláha L, Minksová K, Vondráčk J (2001b) Aryl hydrocarbon receptor-mediated and estrogenic activities of oxygenated polycyclic aromatic hydrocarbons and azaarenes originally identified in extracts of river sediments. Environ Toxicol Chem 20:2736–2743

    Article  CAS  Google Scholar 

  • Matsumoto H, Kashimoto T (1986) Embryotoxicity of organic extracts from airborne particulates in ambient air in the chicken embryo. Arch Environ Contam Toxicol 15:447–452

    Article  CAS  Google Scholar 

  • Mcdonald JD, Barr EB, White RK, Chow JC, Schauer JJ, Zielinska B, Grosjean E (2004) Generation and characterization of four dilutions of diesel engine exhaust for a subchronic inhalation study. Environ Sci Technol 38:2513–2522

    Article  CAS  Google Scholar 

  • Miller CA III (1999) A human aryl hydrocarbon receptor signaling pathway constructed in yeast displays additive responses to ligand mixtures. Toxicol Appl Pharmacol 160:297–303

    Article  CAS  Google Scholar 

  • Misaki K, Matsui S, Matsuda T (2007a) Metabolic enzyme induction by HepG2 cells exposed to oxygenated and nonoxygenated polycyclic aromatic hydrocarbons. Chem Res Toxicol 20:277–283

    Article  CAS  Google Scholar 

  • Misaki K, Kawami H, Tanaka T, Handa Y, Nakamura M, Matsui S, Matsuda T (2007b) Aryl hydrocarbon receptor ligand activity of polycyclic aromatic ketones and polycyclic aromatic quinones. Environ Toxicol Chem 26:1370–1379

    Article  CAS  Google Scholar 

  • Moore MN, Livingstone DR, Widdows J (1989) Hydrocarbons in marine mollusks: biological effects and ecological consequences. In: Varanasi U (ed) Metabolism of polycyclic aromatic hydrocarbons in the aquatic environment. CRC Press, Boca Raton, FL, pp 291–328

    Google Scholar 

  • Nikolaou K, Masclet P, Mouvier G. (1984) Sources and chemical reactivity of polynuclear aromatic hydrocarbons in the atmosphere—a critical review. Sci Total Environ 32:103–132

    Article  CAS  Google Scholar 

  • Ohtake F, Takeyama K, Matsumoto T, Kitagawa H, Yamamoto Y, Nohara K, Tohyama C, Krust A, Mimura J, Chambon P, Yanagisawa J, Fujii-Kuriyama Y, Kato S (2003) Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 423:545–550

    Article  CAS  Google Scholar 

  • Ohtake F, Baba A, Takada I, Okada M, Iwasaki K, Miki H, Takahashi S, Kouzmenko A, Nohara K, Chiba T, Fujii-Kuriyama Y, Kato S (2007) Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446:562–566

    Article  CAS  Google Scholar 

  • Okamura K, Kizu R, Toriba A, Murahashi T, Mizokami A, Burnstein KL, Klinge CM, Hayakawa K (2004) Antiandrogenic activity of extracts of diesel exhaust particles emmited from diesel-engine truck under different engine loads and speeds. Toxicology 195:243–254

    Article  CAS  Google Scholar 

  • Pedersen DU, Durant JL, Taghizadeh K, Hemond HF, Lafleur AL, Cass GR (2005) Human cell mutagens in respirable airborne particles from the northeastern United States. 2. Quantification of mutagens and other organic compounds. Environ Sci Technol 39:9547–9560

    Article  CAS  Google Scholar 

  • Rogge WF, Hildemann LM, Mazurek MA, Cass GR (1993a) Sources of fine organic aerosol. 2. Noncatalyst and catalyst-equipped automobiles and heavy-duty diesel trucks. Environ Sci Technol 27:636–651

    Article  CAS  Google Scholar 

  • Rogge WF, Hildemann LM, Mazurek MA, Cass GR (1993b) Sources of fine organic aerosol. 3. Road dust, tire debris, and organometallic brakes lining dust: Roads as sources and sinks. Environ Sci Technol 27:1892–1904

    Article  CAS  Google Scholar 

  • Schmidt JV, Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Dev Bioll 12:55–89

    Article  CAS  Google Scholar 

  • Till M, Riebniger D, Schmitz H-J, Schrenk D (1999) Potency of various polycyclic aromatic hydrocarbons as inducers of CYP1A1 in rat hepatocyte cultures. Chem-Biol Interact 117:135–150

    Article  CAS  Google Scholar 

  • Tsukue N, Toda N, Tsubone H, Sagai M, Jin WZ, Watanabe G, Taya K, Birumachi J, Suzuki AK (2001) Diesel exhaust (DE) affects the regulation of testicular function in male fischer 344 rats. J Toxicol Environ Health A 63:115–126

    Article  CAS  Google Scholar 

  • Tsukue N, Yoshida S, Sugawara I, Takeda K (2004) Effect of diesel exhaust on development of fetal reproductive function in ICR female mice. J Health Sci 50:174–180

    Article  CAS  Google Scholar 

  • van Lipzig MMH, Vermeulen ME, Gusinu R, Legler J, Frank H, Seidel A, Meerman JHN (2005) Formation of estrogenic metabolites of benzo[a]pyrene and chrysene by cytochrome P450 activity and their combined and supra-maximal estrogenic activity. Environ Toxicol Pharmacol 19:41–55

    Article  CAS  Google Scholar 

  • Vos JG, Dybing E, Greim HA, Ladefoged O, Lambre C, Terazona JV, Brandt I, Vethaak AD (2000) Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation. Crit Rev Toxicol 30:71–133

    Article  CAS  Google Scholar 

  • Watanabe N, Oonuki Y (1999) Inhalation of diesel engine exhaust affects spermatogenesis in growing male rats. Environ Health Perspect 107:539–544

    Article  CAS  Google Scholar 

  • Wells PG, Kim PM, Laposa RR, Nicol CJ, Parman T, Winn LM (1997) Oxidative damage in chemical teratogenesis. Mutat Res 396:65–78

    CAS  Google Scholar 

  • Yoshida S, Sagai M, Oshio S, Umeda T, Ihara T, Sugamata M, Sugawara I, Takeda K (1999) Exposure to diesel exhaust affects the male reproductive system of mice. Int J Androl 22:307–315

    Article  CAS  Google Scholar 

  • Ziccardi MH, Gardner IA, Denison MS (2002) Application of the luciferase recombinant cell culture bioassay system for the analysis of polycyclic aromatic hydrocarbons. Environ Toxicol Chem 21:2027–2033

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Charles A. Miller III of the Department of Environmental Health Sciences and the Tulane-Xavier Center for Bioenvironmental Research, Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana, for kindly supplying us with the YCM3 strain. We acknowledge the Shiga National Highway Construction Work Office, Kinki Regional Construction Agency, Ministry of Construction, and Ritto Management Office, Nagoya Management Agency, Japan Highway Public Corp., for their cooperation in collection of road dust; Dr. Yoshihisa Shimizu, Research Center for Environmental Quality Management, Kyoto University, for kindly allowing us to use the ASE instrument; and Dr. Ryoichi Kizu, Faculty of Pharmaceutical Sciences, Doshisha Woman’s College of Liberal Arts, Kyoto, for kindly providing us with diesel particulates. We also thank Hirofumi Kawami and Tota Tanaka, Research Center for Environmental Quality Management, Kyoto University, and Dr. Byung-Cheol Lee, Department of Environment Research, Korea Institute of Construction Technology, for their assistance. This work was supported in part by Grants-in-Aid for Scientific Research (13027245, 16201012) from the Japanese Ministry of Education, Science, Sports and Culture.

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Authors and Affiliations

  1. Department of Environmental Engineering, Graduate School of Engineering, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto, 606-8501, Japan

    Kentaro Misaki & Masato Suzuki

  2. Department of Technology and Ecology, Graduate School of Global Environmental Studies, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto, 606-8501, Japan

    Kentaro Misaki, Saburo Matsui & Tomonari Matsuda

  3. Hiyoshi Corporation, 908 Kitanosho-cho, Omihachiman, Shiga, 523-8555, Japan

    Masafumi Nakamura & Hiroshi Handa

  4. Otsuka Pharmaceutical Company, Ltd, 224-18 Ebisuno Hiraishi, Kawauchi-cho, Tokushima, 771-0195, Japan

    Mitsuru Iida & Teruhisa Kato

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  1. Kentaro Misaki
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Correspondence to Tomonari Matsuda.

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Misaki, K., Suzuki, M., Nakamura, M. et al. Aryl Hydrocarbon Receptor and Estrogen Receptor Ligand Activity of Organic Extracts from Road Dust and Diesel Exhaust Particulates. Arch Environ Contam Toxicol 55, 199–209 (2008). https://doi.org/10.1007/s00244-007-9110-5

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