Comparative developmental toxicity of environmentally relevant oxygenated PAHs

Toxicology and Applied Pharmacology

Volumn 271, Issue 2, 2013, Pages 266-275

  Knecht, Andrea L ^a   Goodale, Britton C ^a   Truong, Lisa ^a   Simonich, Michael T ^a   Swanson, Annika J ^a   Matzke, Melissa M ^b   Anderson, Kim A ^a   Waters, Katrina M ^b   Tanguay, Robert L ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

Development; Malformation; Morpholino; Oxygenated; PAH; Zebrafish

Indexed keywords

ANTHRAQUINONE; CYTOCHROME P450 1A; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; MESSENGER RNA; PHENANTHRENEQUINONE; POLYCYCLIC AROMATIC HYDROCARBON; SUPEROXIDE DISMUTASE; XANTHONE DERIVATIVE;

ARTICLE; BIOENERGY; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); DEVELOPMENTAL TOXICITY; DILUTION; EMBRYO; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; OXYGENATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRUCTURE ACTIVITY RELATION; ZEBRA FISH;

DEVELOPMENT; MALFORMATION; MORPHOLINO; OXYGENATED; PAH; ZEBRAFISH;

ABNORMALITIES, DRUG-INDUCED; ANIMALS; BIOLOGICAL MARKERS; EMBRYO, NONMAMMALIAN; ENVIRONMENTAL POLLUTANTS; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; MITOCHONDRIA; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; POLYCYCLIC HYDROCARBONS, AROMATIC; REAL-TIME POLYMERASE CHAIN REACTION; RNA; TERATOGENS; ZEBRAFISH;

EID: 84880637536     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.05.006     Document Type: Article

References (60)

1. 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. Off. J. Soc. Toxicol. 2002, 68:403-419.
2. Avellaneda P.M., Englehardt J.D., Olascoaga J., Babcock E.A., Brand L., Lirman D., Rogge W.F., Solo-Gabriele H., Tchobanoglous G. Relative risk assessment of cruise ships biosolids disposal alternatives. Mar. Pollut. Bull. 2011, 62:2157-2169.
3. Billiard S.M., Timme-Laragy A.R., Wassenberg D.M., Cockman C., Di Giulio R.T. The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol. Sci. 2006, 92:526-536.
4. Bolton J.L., Trush M.A., Penning T.M., Dryhurst G., Monks T.J. Role of quinones in toxicology. Chem. Res. Toxicol. 2000, 13:135-160.
5. Cai G., Zhu Junfeng, Shen Chao, Cui Yimin, Du Jiulin, Chen Xiaodong The effects of cobalt on the development, oxidative stress, and apoptosis in zebrafish embryos. Biol. Trace Elem. Res. 2012, 150:200-207.
6. Channell M.M., Paffett M.L., Devlin R.B., Madden M.C., Campen M.J. Circulating factors induce coronary endothelial cell activation following exposure to inhaled diesel exhaust and nitrogen dioxide in humans: evidence from a novel translational in vitro model. Toxicol Sci. 2012, 127:179-186.
7. Chung M.Y., Lazaro R.A., Lim D., Jackson J., Lyon J., Rendulic D., Hasson A.S. Aerosol-borne quinones and reactive oxygen species generation by particulate matter extracts. Environ. Sci. Technol. 2006, 40:4880-4886.
8. Coull B.A., Agresti A. The use of mixed logit models to reflect heterogeneity in capture-recapture studies. Biometrics 1999, 55:294-301.
9. Dejmek J., Selevan S.G., Benes I., Solansky I., Sram R.J. Fetal growth and maternal exposure to particulate matter during pregnancy. Environ Health Perspect. 1999, 107:475-480.
10. Dejmek J., Solansky I., Benes I., Lenicek J., Sram R.J. The impact of polycyclic aromatic hydrocarbons and fine particles on pregnancy outcome. Environ Health Perspect. 2000, 108:1159-1164.
11. Delfino R.J., Staimer N., Tjoa T., Arhami M., Polidori A., Gillen D.L., Kleinman M.T., Schauer J.J., Sioutas C. Association of biomarkers of systemic inflammation with organic components and source tracers in quasi-ultrafine particles. Environ. Heal. Perspect. 2010, 118:756-762.
12. Ding J., Zhong J., Yang Y., Li B., Shen G., Su Y., Wang C., Li W., Shen H., Wang B., Wang R., Huang Y., Zhang Y., Cao H., Zhu Y., Simonich S.L., Tao S. Occurrence and exposure to polycyclic aromatic hydrocarbons and their derivatives in a rural Chinese home through biomass fuelled cooking. Environ Pollut. 2012, 169:160-166.
13. Dranka B.P., Benavides G.A., Diers A.R., Giordano S., Zelickson B.R., Reily C., Zou L., Chatham J.C., Hill B.G., Zhang J., Landar A., Darley-Usmar V.M. Assessing bioenergetic function in response to oxidative stress by metabolic profiling. Free Radic Biol Med. 2011, 51:1621-1635.
14. Freeman M.F., Tukey J.W. Transformations related to the angular and the square root. Ann. Math. Stat. 1950, 21:607-611.
15. Garner L.V., Di Giulio R.T. Glutathione transferase pi class 2 (GSTp2) protects against the cardiac deformities caused by exposure to PAHs but not PCB-126 in zebrafish embryos. Comp. Biochem. Physiol. Toxicol. Pharmacol. 2012, 155:573-579. CBP.
16. Goodale B.C., La Du J.K., Bisson W.H., Janszen D.B., Waters K.M., Tanguay R.L. AHR2 mutant reveals functional diversity of aryl hydrocarbon receptors in zebrafish. PLoS One 2012, 7:e29346.
17. Grant W.B. Air pollution in relation to U.S. cancer mortality rates: an ecological study; likely role of carbonaceous aerosols and polycyclic aromatic hydrocarbons. Anticancer. Res. 2009, 29:3537-3545.
18. Hayes J.D., Pulford D.J. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol. 1995, 30:445-600.
19. Hoshuyama T., Pan G., Tanaka C., Feng Y., Yu L., Liu T., Liu L., Hanaoka T., Takahashi K. Mortality of iron-steel workers in Anshan, China: a retrospective cohort study. Int. J. Occup. Environ. Heal. 2006, 12:193-202.
20. Howsam M., Jones K.C. Sources of PAHs in the environment., anthropogenic compounds. Part I. PAHs and Related Compounds 1998, 137-174. Springer-Verlag, Berlin.
21. Incardona J.P., Day H.L., Collier T.K., Scholz N.L. Developmental toxicity of 4-ring polycyclic aromatic hydrocarbons in zebrafish is differentially dependent on AH receptor isoforms and hepatic cytochrome P4501A metabolism. Toxicol. Appl. Pharmacol. 2006, 217:308-321.
22. Kim K.H., Jahan S.A., Kabir E. A review of diseases associated with household air pollution due to the use of biomass fuels. J. Hazard. Mater. 2011, 192:425-431.
23. Layshock J.A., Wilson G., Anderson K.A. Ketone and quinone-substituted polycyclic aromatic hydrocarbons in mussel tissue, sediment, urban dust, and diesel particulate matrices. Environ. Toxicol. Chem. 2010, 29:2450-2460.
24. Lee M.S., Magari S., Christiani D.C. Cardiac autonomic dysfunction from occupational exposure to polycyclic aromatic hydrocarbons. Occup. Environ. Med. 2011, 68:474-478.
25. Lewtas J. Air pollution combustion emissions: characterization of causative agents and mechanisms associated with cancer, reproductive, and cardiovascular effects. Mutat. Res. 2007, 636:95-133.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
27. Lundstedt S., White P.A., Lemieux C.L., Lynes K.D., Lambert L.B., Oberg L., Haglund P., Tysklind M. Sources, fate, and toxic hazards of oxygenated polycyclic aromatic hydrocarbons (PAHs) at PAH-contaminated sites. Ambio 2007, 36:475-485.
28. Mandrell D., Truong L., Jephson C., Sarker M.R., Moore A., Lang C., Simonich M.T., Tanguay R.L. Automated zebrafish chorion removal and single embryo placement. J. Lab. Autom. 2012, 17:66-74.
29. Mathew L.K., Andreasen E.A., Tanguay R.L. Aryl hydrocarbon receptor activation inhibits regenerative growth. Mol. Pharmacol. 2006, 69:257-265.
30. Mazurek M.A. Molecular identification of organic compounds in atmospheric complex mixtures and relationship to atmospheric chemistry and sources. Environ. Heal. Perspect. 2002, 110(Suppl. 6):995-1003.
31. Medeiros P.M., Simoneit B.R. Source profiles of organic compounds emitted upon combustion of green vegetation from temperate climate forests. Environ. Sci. Technol. 2008, 42:8310-8316.
32. Nebert D.W., Karp C.L. Endogenous functions of the aryl hydrocarbon receptor (AHR): intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. J. Biol. Chem. 2008, 283:36061-36065.
33. 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.
34. Nemmar A., Al-Salam S., Zia S., Marzouqi F., Al-Dhaheri A., Subramaniyan D., Dhanasekaran S., Yasin J., Ali B.H., Kazzam E.E. Contrasting actions of diesel exhaust particles on the pulmonary and cardiovascular systems and the effects of thymoquinone. Br. J. Pharmacol. 2011, 164:1871-1882.
35. Okona-Mensah K.B., Battershill J., Boobis A., Fielder R. An approach to investigating the importance of high potency polycyclic aromatic hydrocarbons (PAHs) in the induction of lung cancer by air pollution. Food Chem. Toxicol. Int. J. Publ. Brit. Ind. Biol. Res.Assoc. 2005, 43:1103-1116.
36. Pedersen D.U., Durant J.L., Penman B.W., Crespi C.L., Hemond H.F., Lafleur A.L., Cass G.R. Human-cell mutagens in respirable airborne particles in the northeastern United States. 1. Mutagenicity of fractionated samples. Environ. Sci. Technol. 2004, 38:682-689.
37. Pedersen D.U., Durant J.L., Taghizadeh K., Hemond H.F., Lafleur A.L., Cass G.R. Human cell mutagens in respirable airborne particles from the northeastern United States. 2. Quantification of mutagens and other organic compounds. Environ. Sci. Technol. 2005, 39:9547-9560.
38. Perera F.P., Whyatt R.M., Jedrychowski W., Rauh V., Manchester D., Santella R.M., Ottman R. Recent developments in molecular epidemiology: A study of the effects of environmental polycyclic aromatic hydrocarbons on birth outcomes in Poland. Am J Epidemiol. 1998, 147:309-314.
39. Perera F.P., Rauh V., Whyatt R.M., Tsai W.Y., Tang D., Diaz D., Hoepner L., Barr D., Tu Y.H., Camann D., Kinney P. Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3years of life among inner-city children. Environ. Heal. Perspect. 2006, 114:1287-1292.
40. Perera F.P., Jedrychowski W., Rauh V., Whyatt R.M. Molecular epidemiologic research on the effects of environmental pollutants on the fetus. Environ Health Perspect. 1999, 107(Suppl 30):451-460.
41. Perera F.P., Li Z., Whyatt R., Hoepner L., Wang S., Camann D., Rauh V. Prenatal airborne polycyclic aromatic hydrocarbon exposure and child IQ at age 5years. Pediatrics 2009, 124:e195-e202.
42. Reimers M.J., La Du J.K., Periera C.B., Giovanini J., Tanguay R.L. Ethanol-dependent toxicity in zebrafish is partially attenuated by antioxidants. Neurotoxicol. Teratol. 2006, 28:497-508.
43. Rogge W.F., Hildemann L.M., Mazurek M.A., Cass G.R., Simoneit B.R. Sources of fine organic aerosol. 2. Noncatalyst and catalyst-equipped automobiles and heavy-duty diesel trucks. Environ. Sci. Technol. 1993, 27:636-651.
44. Rogge W.F., Hildemann L.M., Mazurek M.A., Cass G.R., Simoneit B.R. Sources of fine organic aerosol. 8. Boilers burning no. 2 distillate fuel oil. Environ. Sci. Technol. 1997, 31:2731-3737.
45. Senft A.P., Dalton T.P., Nebert D.W., Genter M.B., Puga A., Hutchinson R.J., Kerzee J.K., Uno S., Shertzer H.G. Mitochondrial reactive oxygen production is dependent on the aromatic hydrocarbon receptor. Free Radic. Biol. Med. 2002, 33:1268-1278.
46. Shen G., Tao S., Wang W., Yang Y., Ding J., Xue M., Min Y., Zhu C., Shen H., Li W., Wang B., Wang R., Wang X., Russell A.G. Emission of oxygenated polycyclic aromatic hydrocarbons from indoor solid fuel combustion. Environ. Sci. Technol. 2011, 45:3459-3465.
47. Shen G., Wang W., Yang Y., Ding J., Xue M., Min Y., Zhu C., Shen H., Li W., Wang B., Wang R., Wang X., Tao S., Russell A.G. Emissions of PAHs from indoor crop residue burning in a typical rural stove: emission factors, size distributions, and gas-particle partitioning. Environ. Sci. Technol. 2011, 45:1206-1212.
48. Shertzer H.G., Genter M.B., Shen D., Nebert D.W., Chen Y., Dalton T.P. TCDD decreases ATP levels and increases reactive oxygen production through changes in mitochondrial F0F1-ATP synthase and ubiquinone. Toxicol. Appl. Pharmacol. 2006, 217:363-374.
49. Simoneit B.R., Bi X., Oros D.R., Medeiros P.M., Sheng G., Fu J. Phenols and hydroxy-PAHs (arylphenols) as tracers for coal smoke particulate matter: source tests and ambient aerosol assessments. Environ. Sci. Technol. 2007, 41:7294-7302.
50. Sklorz M., Briede J.J., Schnelle-Kreis J., Liu Y., Cyrys J., de Kok T.M., Zimmermann R. Concentration of oxygenated polycyclic aromatic hydrocarbons and oxygen free radical formation from urban particulate matter. J. Toxic. Environ. Health A 2007, 70:1866-1869.
51. Tian Y. Ah receptor and NF-κB interplay on the stage of epigenome. Biochem. Pharmacol. 2009, 77:670-680.
52. Timme-Laragy A.R., Van Tiem L.A., Linney E.A., Di Giulio R.T. Antioxidant responses and NRF2 in synergistic developmental toxicity of PAHs in zebrafish. Toxicol Sci. 2009, 109:217-227.
53. Van Tiem L.A., Di Giulio R.T. AHR2 knockdown prevents PAH-mediated cardiac toxicity and XRE- and ARE-associated gene induction in zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 2011, 254:280-287.
54. Vione D., Barra S., De Gennaro G., De Rienzo M., Gilardoni S., Perrone M.G., Pozzoli L. Polycyclic aromatic hydrocarbons in the atmosphere: monitoring, sources, sinks and fate. II: sinks and fate. Ann. Chim. 2004, 94:257-268.
55. Wang L., Atkinson R., Arey J. Formation of 9,10-phenanthrenequinone by atmospheric gas-phase reactions of phenanthrene. Atmos. Environ. 2007, 41:2025-2035.
56. Wang W., Jariyasopit N., Schrlau J., Jia Y., Tao S., Yu T.W., Dashwood R.H., Zhang W., Wang X., Simonich S.L. Concentration and photochemistry of PAHs, NPAHs, and OPAHs and toxicity of PM2.5 during the Beijing Olympic Games. Environ. Sci. Technol. 2011, 45:6887-6895.
57. Wu J., Hou H., Ritz B., Chen Y. Exposure to polycyclic aromatic hydrocarbons and missed abortion in early pregnancy in a Chinese population. Sci Total Environ. 2010, 408:2312-2318.
58. Yeager R.L., Reisman S.A., Aleksunes L.M., Klaassen C.D. Introducing the "TCDD-inducible AhR-Nrf2 gene battery". Toxicol. Sci. 2009, 111:238-246.
59. Yu H. Environmental carcinogenic polycyclic aromatic hydrocarbons: photochemistry and phototoxicity. J. Environ. Sci. Health C Reviews Environ. Carcinog. Ecotoxicol. Rev. 2002, 20:149-183.
60. Zielinska B., Sagebiel J., McDonald J.D., Whitney K., Lawson D.R. Emission rates and comparative chemical composition from selected in-use diesel and gasoline-fueled vehicles. J. Air Waste Manag. Assoc. 2004, 54:1138-1150.