Light-induced cytotoxicity of 16 polycyclic aromatic hydrocarbons on the US EPA priority pollutant list in human skin HaCaT keratinocytes: Relationship between phototoxicity and excited state properties

Environmental Toxicology

Volumn 22, Issue 3, 2007, Pages 318-327

  Wang, Shuguang ^a   Sheng, Yinghong ^a   Feng, Manliang ^a   Leszczynski, Jerzy ^a   Wang, Lei ^a   Tachikawa, Hiroyasu ^a   Yu, Hongtao ^a  

^a JACKSON STATE UNIVERSITY   (United States)

Author keywords

DFT; Excited state energy; HOMO LUMO gap; Human skin keratinocytes; Light absorption; Phototoxicity; Polycyclic aromatic hydrocarbons (PAHs)

Indexed keywords

CYTOTOXICITY; DENSITY FUNCTIONAL THEORY; ENVIRONMENTAL PROTECTION AGENCY; EXCITED STATES; LIGHT ABSORPTION; ORGANIC POLLUTANTS; SKIN;

EXCITED STATE ENERGY; HOMO-LUMO GAP; HUMAN SKIN KERATINOCYTES; PHOTOTOXICITY;

POLYCYCLIC AROMATIC HYDROCARBONS;

ANTHRACENE; BENZ[A]ANTHRACENE; BENZO[A]PYRENE; BENZO[B]FLUORANTHENE; BENZO[GHI]PERYLENE; CHRYSENE; DIBENZ[A,H]ANTHRACENE; INDENO[1,2,3 CD]PYRENE; NAPHTHALENE; POLYCYCLIC AROMATIC HYDROCARBON DERIVATIVE; PYRENE;

CYTOLOGY; LIGHT EFFECT; PAH; PUBLIC HEALTH; SKIN; TOXICITY;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DENSITY FUNCTIONAL THEORY; HUMAN; HUMAN CELL; KERATINOCYTE; LIGHT; PHOTOTOXICITY; POLLUTANT; PRIORITY JOURNAL; SIMULATOR; SKIN TOXICITY; SUNLIGHT; TOXICITY TESTING; UNITED STATES;

CELL LINE, TRANSFORMED; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; HUMANS; KERATINOCYTES; MOLECULAR STRUCTURE; MUTAGENICITY TESTS; MUTAGENS; POLYCYCLIC HYDROCARBONS, AROMATIC; SKIN; TIME FACTORS; TOXICITY TESTS; ULTRAVIOLET RAYS; UNITED STATES; UNITED STATES ENVIRONMENTAL PROTECTION AGENCY;

EID: 34249666537     PISSN: 15204081     EISSN: 15227278     Source Type: Journal    
DOI: 10.1002/tox.20241     Document Type: Article

References (54)

1. Arfsten DP, Davenport R, Schaeffer DJ. 1994. UV-A coexposure enhances the toxicity of aromatic hydrocarbons, munitions, and metals to photobacterium phosphoreum. Biomed Environ Sci 7: 101-108.
2. Arfsten DP, Schaeffer DJ, Mulveny DC. 1996. The effects of near ultraviolet radiation on the toxic effects of polycyclic aromatic hydrocarbons in animals and plants: A review. Ecotoxicol Environ Saf 33:1-24.
3. Barlow Y, Pye RJ. 1997. Ketratinocyte culture. Methods Mol Biol 75:117-129.
4. Baum E. 1978. Occurrence and surveillance of polycyclic aromatic hydrocarbons. In: Gelboin H, Ts'O T, editors. Polycyclic Hydrocarbons Cancer. New York: Academic Press. pp 45-70.
5. Bauschlicher CW. 1995. A comparison of the accuracy of different functionals. Chem Phys Lett 246:40.
6. Becke AD. 1993. Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 98:5648.
7. Betowski LD, Enlow M, Riddick L. 2002. The phototoxicity of polycyclic aromatic hydrocarbons: a theoretical study of excited states and correlation to experiment. Comput Chem 26:371-377.
8. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761-767.
9. Cances MT, Mennucci V, Tomasi J. 1997. A new integral equation formalism for the polarizable continuum model: Theoretical background and applications to isotropic and anisotropic dielectrics. J Chem Phys 107:3032.
10. Chen JW, Kong LR, Zhu CM, Huang QG, Wang LS. 1996. Correlation between photolysis rate constant of polycyclic aromatic hydrocarbons and frontier molecular orbital energy. Chemosphere 33:1143-1150.
11. Connell DW, Hawker DW, Warne MJ, Vowles PP. 1997. Polycyclic aromatics hydrocarbons (PAHs). In: McCombs K, Stark-weather AW, editors. Introduction into Environmental Chemistry. Boca Raton, FL: CRC Press LLC. pp 205-217.
12. Conney AH. 1982. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons. Cancer Res 42:4875-4917.
13. Dabestani R, Ivanov IN. 1999. Invited Review: A Comparison of Physical, Spectroscopical and Photophysical Properties of Polycyclic Aromatic Hydrocarbons. Photochem Photobiol 70:10-34.
14. de Lima Ribeiro FA, Ferreira MMC. 2005. QSAR model of the phototoxicity of polycyclic aromatic hydrocarbon. Theochem 719:191-200.
15. Dipple A. 1985. Polycyclic aromatic hydrocarbons and carcinogenesis. Washington, DC: Ameraican Chemical Society.
16. Dong S, Fu PP, Shirsat RN, Hwang H-M, Leszczynski J, Yu H. 2002. UVA light-induced DNA cleavage by isomeric methyl-benz[a]anthracenes. Chem Res Toxicol 15:400-409.
17. Dong S, Hwang H-M, Shi X, Holloway L, Yu H. 2000. UVA-induced DNA single strand cleavage by 1-hydroxypyrene and formation of covalent adducts between DNA and 1-hydroxypyrene. Chem Res Toxicol 13:585-593.
18. El-Azhary AA, Suter HU. 1996. Comparison between Optimized geometries and vibrational frequencies calculated by the DFT methods. Phys Chem 100:15056.
19. Foote CS. 1976. Free Radical Biology. New York: Academic Press. pp 85-133.
20. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JJA, Vreven T, Kudin KN, Burant JC, Millam JM, Lyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA. 2004, Gaussian, Wallingford, CT.
21. Gutman I, Milun M, Trinajstic N. 1977a. Graph theory and molecular orbitals, XIX. Non-parametric resonance energies of arbitrary conjugated systems. J Am Chem Soc 99:1692-1704.
22. Gutman I, Milun M, Trinajstic N. 1977b. Topological resonance energies of annlenes. Croat Chem Acta 49:441-452.
23. Huang X-D, Dixon DG, Greenberg BM. 1993. Impact of UV radiation and photomodification on the toxicity of PAHs to the higher plant Lemna gibba (Duckweed). Environ Toxicol Chem 12:1067-1077.
24. Huang X-D, Dixon DG, Greenberg BM. 1995. Increased polycyclic aromatic hydrocarbon toicity following their photomidification in natural sunlight: Impactss on the Duckweed Lemna gibba L. G-3. Ecotoxicol Environ Safety 32:194-200.
25. Kagan J, Kagan E. 1986. The toxicity of benzo[a]pyrene and pyrene in the mosquito Aedes aegypti in the dark and in the presence of ultraviolet light. Chemosphere 15:243-251.
26. Krylov SN, Huang X-D, Zeiler LF, Dixon DG, Greenberg BM. 1997. Mechanistic quantitative structure-activity relationship model for the photoinduced toxicity of polycyclic aromatic hydrocarbons. I. Physical model based on chemical kinetics in a two-compartment system. Environ Toxicol Chem 16:2283-2295.
27. Kubicki JD, Blake GA, Apitz SE. 1999. Molecular models of benzene and selected polycyclic aromatic hydrocarbons in the aqueous and absorbed states. Environ Toxicol Chem 18:1956-1662.
28. Landrum PF, Giesy JP, Oris JT, Alfred PM. 1987. Photoinduced toxicity of polycyclic aromatic hydrocarbons to aquatic organisms. In: Vandermeulen JH, Hrudey SE, editors. Symposium on Oil Pollution of Freshwater. Ann Arbor: Pergamon, pp 304-318.
29. Lee C, Yang W, Parr R. 1988. Developemnt of the colle-salvetti correlation energy formula into a functional of the electron density. Phys Rev B 37:785.
30. Leigh IM, Newton Bishop JA, Kripke ML. 1996. Instruction Skin Cancer. Cancer Surv. 26:1-6.
31. Liu Z, Lu Y, Rosenstein B, Lebwohl M, Wei H. 1998. Benzo[a]-pyrene enhances the formation of 8-hydroxy-2′-deoxyguanosine by ultraviolet A radiation in calf thymus DNA and human epidermoid carcinoma. Biochemistry 37:10307-10312.
32. Mekenyan OG, Ankley GT, Veith GD, Call DJ. 1994. QSARs for photoinduced Toxicity. I. Acute lethality of polycyclic aromatic hydrocarbons to Daphnia magna. Chemosphere 28:567-582.
33. Miehlich B, Savin A, Stoll H, Preuss H. 1989. Results obtained with the correlation energy density functionals of Becke and Lee, Yang and Parr. Chem Phys Lett 90:5622.
34. National Toxicology Program, P. H. S. US Department of Health and Human Services. 1998. Integrated Laboratory Systems, Research Triangle Park, NC. pp 178-181.
35. Newsted JL, Giesy JP. 1987. Predictive models for photoinduced acute toxicity of polycyclic aromatic hydrocarbons to Daphnia magna, Strauss (Cladocera, Crustacea). Environ Toxicol Chem 6:445-461.
36. Pelletier MC, Burgess RM, Ho KT, Kuhn A, McKinney RA, Ryba SA. 1997. Phototoxicity of individual polycyclic aromatic hydrocarbons and petroleum to marine invertebrae lavae and juveniles. Environ Toxicol Chem 16:2190-2199.
37. Pitts JN. 1979. Photochemical and biological implications of the atmosphere reactions of amines and benzo[a]pyrene, Philos Trans R Soc (London) A 290:551-576.
38. Rotman B, Papermaster BW. 1966. Membrane properties of living mammalian cells as studied by enzymatic hydrolysis of fluorogenic esters. Proc Nat Acad Sci USA 55:134-141.
39. Schirmer K, Dixon DG, Greenberg BM, Bols NC. 1998. Ability of 16 priority PAHs to be directly cytotoxic to a cell line from the rainbow trout gill. Toxicology 127:129-141.
40. Schirmer K, Herbrick JS, Greenberg BM, Dixon DG, Bols NC. 1998. Use of fish gill cells in culture to evaluate the cytotoxicity and photocytotoxicity of intact and photomodified creasote. Environ Toxicol Chem 18:1277-1288.
41. Schlegel GB. 1982. Optimization of equilibrium geometries and transition struuctures. J Comp Chem 3:214.
42. Sheng Y, Leszczynski J. 2004. Theoretical study of the substituent and solvent effects on the molecular structures, absorption and emission spectra of open-form spiropyrans. Collect Czechoslovak Chem Comm 69:47-62.
43. Sheng Y, Leszczynski J, Garcia AA, Rosario R, Gust D, Springer J. 2004. Comprehensive theoretical study of the conversion reactions of spiropyrans: substituent and solvent effects. J Phys Chem 108:16233.
44. Stephens PJ, Devlin FJ, Chabalowski CF, Frisch MJ. 1994. Ab initio calculation of vibrational absorption and circular dichroism spectra using density functional force fields. Phys Chem 98:11623.
45. Straman RE, Scuseria GE, Frisch MJ. 1998. An efficient implementation of time -dependent density-functional theory for the calculation of excitation energies of large molecules. Chem Phys 109:8218.
46. Swartz RC, Ferraro SP, Lamberson JO, Cole FA, Ozretich RJ, Boese BL, Schults DW, Behrenfeld M, Ankley GT. 1997. Photoactivation and toxicity of mixtures of polycyclic aromatic hydrocarbon compounds in marine sediment. Environ Toxicol Chem 16:2151-2157.
47. USEPA. 1982. Office of the Federal Registration (OFR), Appendix A: Priorty pollutants. Fed Reg 47:52309.
48. Utesch D, Eray K, Diehl E. 1996. Phototoxicity testing of polycyclic aromatic hydrocarbons (PAH) in mammalian cells in vitro. Polycycl Arom Compd 10:117-121.
49. Warshawsky D. 1999. Polycyclic aromatic hydrocarbons in carcinogenesis. Environ Health Perspect 107:317-320.
50. Xu J, Yan J, Wang X, Yu H, Milliken T. 2004. Photochemical reaction of chrysene in acetonitrile/water. Polycycl Arom Compd 24:249-256.
51. Yan J, Wang L, Fu P, Yu H. 2004. Photomutagenicity of 16 polycyclic aromatic hydrocarbons from the US EPA priority pullutant list. Mutat Res 557:99-108.
52. Yan J, Xia Q, Cherng S, Wamer WG, Howard PC, Yu H, Fu PP. 2006. Photoirradiation of representative polycyclic aromatic hydrocarbons and twelve methylbenz[a]anthracenes with UVA Light: Formation of lipid peroxidation. Toxicol Ind Health 22:147-151.
53. Yu H. 2002. Environmental carcinogenic polycyclic aromatic hydrocarbons: Photochemistry and phototoxicity. J Environ Sci Health Part C: Environ Carcinog Ecotoxic Revs 20:149-183.
54. Yu H, Xia Q, Yan J, Herreno-Saenz D, Wu Y-S, Tang I-W, Fu PP. 2006. Photoirradiation of polycyclic aromatic hydrocarbons with UVA light-a pathway leading to generation of reactive oxygen species, lipid peroxidation, and DNA damage. J Environ Res Public Health 3:348-354.