Polycyclic aromatic hydrocarbons and their quinones modulate the metabolic profile and induce DNA damage in human alveolar and bronchiolar cells

International Journal of Hygiene and Environmental Health

Volumn 216, Issue 5, 2013, Pages 553-565

  Gurbani, Deepak ^a,d   Bharti, Santosh Kumar ^c   Kumar, Ashutosh ^a   Pandey, Alok K ^a   Ana, Godson R E E ^b   Verma, Ambrish ^a   Khan, Altaf Husain ^a   Patel, Devendra K ^a   Mudiam, M K R ^a   Jain, Swatantra K ^d   Roy, Raja ^c   Dhawan, Alok ^a,e  

^a CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

^b UNIVERSITY OF IBADAN   (Nigeria)

^c SANJAY GANDHI POSTGRADUATE INSTITUTE OF MEDICAL SCIENCES   (India)

^d HAMDARD UNIVERSITY   (India)

^e AHMEDABAD UNIVERSITY   (India)

Author keywords

Genotoxicity; Human lung cells; Metabolic profiling; Polycyclic aromatic hydrocarbons (PAHs); Quinones

Indexed keywords

CARCINOGEN; POLYCYCLIC AROMATIC HYDROCARBON; QUINONE DERIVATIVE;

AIR POLLUTANT; ARTICLE; BRONCHUS; CELL LINE; CYTOLOGY; DNA DAMAGE; DRUG EFFECT; ENVIRONMENTAL MONITORING; GENETICS; GENOTOXICITY; HUMAN; HUMAN LUNG CELLS; INDIA; LUNG ALVEOLUS; METABOLIC PROFILING; MICRONUCLEUS TEST; MUTAGEN TESTING; PARTICULATE MATTER; POLYCYCLIC AROMATIC HYDROCARBONS (PAHS); SALMONELLA TYPHI; TUMOR CELL LINE;

GENOTOXICITY; HUMAN LUNG CELLS; METABOLIC PROFILING; POLYCYCLIC AROMATIC HYDROCARBONS (PAHS); QUINONES;

AIR POLLUTANTS; BRONCHI; CARCINOGENS; CELL LINE; CELL LINE, TUMOR; DNA DAMAGE; ENVIRONMENTAL MONITORING; HUMANS; INDIA; MICRONUCLEUS TESTS; MUTAGENICITY TESTS; PARTICULATE MATTER; POLYCYCLIC HYDROCARBONS, AROMATIC; PULMONARY ALVEOLI; QUINONES; SALMONELLA TYPHI;

MAMMALIA;

EID: 84880046089     PISSN: 14384639     EISSN: 1618131X     Source Type: Journal    
DOI: 10.1016/j.ijheh.2013.04.001     Document Type: Article

References (60)

1. Andreou G., Rapsomanikis S. Polycyclic aromatic hydrocarbons and their oxygenated derivatives in the urban atmosphere of Athens. J. Hazard. Mater. 2009, 172:363-373.
2. Aubier M. Traffic-related pollutants and their impact on allergic respiratory diseases. Bull. Acad. Natl. Med. 2009, 193:1305-1313. (discussion 1303-1313).
3. Bai Y., Suzuki A.K., Sagai M. The cytotoxic effects of diesel exhaust particles on human pulmonary artery endothelial cells in vitro: role of active oxygen species. Free Radic. Biol. Med 2001, 30:555-562.
4. Baulig A., Sourdeval M., Meyer M., Marano F., Baeza-Squiban A. Biological effects of atmospheric particles on human bronchial epithelial cells, comparison with diesel exhaust particles. Toxicol. In Vitro 2003, 17:567-573.
5. 1H NMR spectroscopy. TrAC-Trend Anal. Chem. 2012, 35:5-26.
6. Boffetta P., Jourenkova N., Gustavsson P. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Cause Control 1997, 8:444-472.
7. 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.
8. Bosetti C., Boffetta P., La Vecchia C. Occupational exposures to polycyclic aromatic hydrocarbons, and respiratory and urinary tract cancers: a quantitative review to 2005. Ann. Oncol. 2007, 18:431-446.
9. Cavallo D., Ursini C.L., Carelli G., Iavicoli I., Ciervo A., Perniconi B., Rondinone B., Gismondi M., Iavicoli S. Occupational exposure in airport personnel: characterization and evaluation of genotoxic and oxidative effects. Toxicology 2006, 223:26-35.
10. Central Pollution Control Board I. National Ambient Air Quality Standards 2009, http://www.cpcb.nic.in/National_Ambient_Air_Quality_Standards.php.
11. Courter L.A., Pereira C., Baird W.M. Diesel exhaust influences carcinogenic PAH-induced genotoxicity and gene expression in human breast epithelial cells in culture. Mutat. Res. 2007, 625:72-82.
12. Courter L.A., Luch A., Musafia-Jeknic T., Arlt V.M., Fischer K., Bildfell R., Pereira C., Phillips D.H., Poirier M.C., Baird W.M. The influence of diesel exhaust on polycyclic aromatic hydrocarbon-induced DNA damage, gene expression, and tumor initiation in Sencar mice in vivo. Cancer Lett. 2008, 265:135-147.
13. Assessment of benzo[a]pyrene atmospheric concentrations in the UK to support the establishment of a national PAH objective 2001, DEFRA, Available at http://uk-air.defra.gov.uk/reports/empire/aeat-env-r-0620.pdf.
14. Don Porto Carero A., Hoet P.H., Verschaeve L., Schoeters G., Nemery B. Genotoxic effects of carbon black particles, diesel exhaust particles, and urban air particulates and their extracts on a human alveolar epithelial cell line (A549) and a human monocytic cell line (THP-1). Environ. Mol. Mutagen 2001, 37:155-163.
15. Franco S.S., Nardocci A.C., Gunther W.M. PAH biomarkers for human health risk assessment: a review of the state-of-the-art. Cad. Saude. Publica 2008, 24(Suppl. 4):s569-s580.
16. Gagne J.P., Hendzel M.J., Droit A., Poirier G.G. The expanding role of poly(ADP-ribose) metabolism: current challenges and new perspectives. Curr. Opin. Cell. Biol. 2006, 18:145-151.
17. Gurbani D., Kukshal V., Laubenthal J., Kumar A., Pandey A., Tripathi S., Arora A., Jain S.K., Ramachandran R., Anderson D., Dhawan A. Mechanism of inhibition of the ATPase domain of human topoisomerase IIalpha by 1,4-benzoquinone, 1,2-naphthoquinone, 1,4-naphthoquinone, and 9,10-phenanthroquinone. Toxicol. Sci. 2012, 126:372-390.
18. Huang W., Smith T.J., Ngo L., Wang T., Chen H., Wu F., Herrick R.F., Christiani D.C., Ding H. Characterizing and biological monitoring of polycyclic aromatic hydrocarbons in exposures to diesel exhaust. Environ. Sci. Technol. 2007, 41:2711-2716.
19. IARC Diesel and gasoline engine exhausts and some nitroarenes. IARC Monogr. Eval. Carcinog. Risks Hum. 2012, 105.
20. Indian Standard Method for measurement of Air Pollution. Respirable Suspended Particulate Matter (PM10). Bureau of Indian Standard 2006, New Delhi Part (23) IS 5182. (IV).
21. Jakober C.A., Riddle S.G., Robert M.A., Destaillats H., Charles M.J., Green P.G., Kleeman M.J. Quinone emissions from gasoline and diesel motor vehicles. Environ. Sci. Technol. 2007, 41:4548-4554.
22. Karaman A., Pirim I. Exposure to bitumen fumes and genotoxic effects on Turkish asphalt workers. Clin. Toxicol. (Phila) 2009, 47:321-326.
23. Ko F.W., Hui D.S. Outdoor air pollution: impact on chronic obstructive pulmonary disease patients. Curr. Opin. Pulm. Med. 2009, 15:150-157.
24. Kondoh H., Lleonart M.E., Bernard D., Gil J. Protection from oxidative stress by enhanced glycolysis: a possible mechanism of cellular immortalization. Histol. Histopathol. 2007, 22:85-90.
25. Kumar A., Pandey A.K., Singh S.S., Shanker R., Dhawan A. Cellular uptake and mutagenic potential of metal oxide nanoparticles in bacterial cells. Chemosphere 2011, 83:1124-1132.
26. 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.
27. Markley J.L., Anderson M.E., Cui Q., Eghbalnia H.R., Lewis I.A., Hegeman A.D., Li J., Schulte C.F., Sussman M.R., Westler W.M., Ulrich E.L., Zolnai Z. New bioinformatics resources for metabolomics. Pac. Symp. Biocomput. 2007, 12:157-168.
28. Matoba S., Kang J.G., Patino W.D., Wragg A., Boehm M., Gavrilova O., Hurley P.J., Bunz F., Hwang P.M. p53 regulates mitochondrial respiration. Science (New York, N.Y.) 2006, 312:1650-1653.
29. Miranda C.L., Chung W.G., Wang-Buhler J.L., Musafia-Jeknic T., Baird W.M., Buhler D.R. Comparative in vitro metabolism of benzo[a]pyrene by recombinant zebrafish CYP1A and liver microsomes from beta-naphthoflavone-treated rainbow trout. Aquat. Toxicol. (Amsterdam, Netherlands) 2006, 80:101-108.
30. Misaki K., Suzuki M., Nakamura M., Handa H., Iida M., Kato T., Matsui S., Matsuda T. Aryl hydrocarbon receptor and estrogen receptor ligand activity of organic extracts from road dust and diesel exhaust particulates. Arch. Environ. Contam. Toxicol. 2008, 55:199-209.
31. Mortelmans K., Zeiger E. The Ames Salmonella/microsome mutagenicity assay. Mutat. Res. 2000, 455:29-60.
32. Nichols W.K., Terry C.M., Cutler N.S., Appleton M.L., Jesthi P.K., Yost G.S. Oxidation at C-1 controls the cytotoxicity of 1,1-dichloro-2,2-bis(p-chlorophenyl)ethane by rabbit and human lung cells. Drug Metab. Dispos. 1995, 23:595-599.
33. Nusse M., Marx K. Flow cytometric analysis of micronuclei in cell cultures and human lymphocytes: advantages and disadvantages. Mutat. Res. 1997, 392:109-115.
34. OECD Bacterial Reverse Mutation Test. OECD Guideline for Testing of Chemicals 1997, 471.
35. Oh S.M., Chung K.H. Identification of mammalian cell genotoxins in respirable diesel exhaust particles by bioassay-directed chemical analysis. Toxicol. Lett. 2006, 161:226-235.
36. Oh S.M., Kim H.R., Park Y.J., Lee S.Y., Chung K.H. Organic extracts of urban air pollution particulate matter (PM2.5)-induced genotoxicity and oxidative stress in human lung bronchial epithelial cells (BEAS-2B cells). Mutat. Res. 2011, 723:142-151.
37. Pandey A.K., Gurbani D., Bajpayee M., Parmar D., Ajmani S., Dhawan A. In silico studies with human DNA topoisomerase-II alpha to unravel the mechanism of in vitro genotoxicity of benzene and its metabolites. Mutat. Res. 2009, 661:57-70.
38. Park B., Donaldson K., Duffin R., Tran L., Kelly F., Mudway I., Morin J.P., Guest R., Jenkinson P., Samaras Z., Giannouli M., Kouridis H., Martin P. Hazard and risk assessment of a nanoparticulate cerium oxide-based diesel fuel additive - a case study. Inhal. Toxicol. 2008, 20:547-566.
39. Pavlides S., Tsirigos A., Migneco G., Whitaker-Menezes D., Chiavarina B., Flomenberg N., Frank P.G., Casimiro M.C., Wang C., Pestell R.G., Martinez-Outschoorn U.E., Howell A., Sotgia F., Lisanti M.P. The autophagic tumor stroma model of cancer: Role of oxidative stress and ketone production in fueling tumor cell metabolism. Cell Cycle 2010, 9:3485-3505.
40. Pope C.A., Burnett R.T., Thun M.J., Calle E.E., Krewski D., Ito K., Thurston G.D. Lung cancer, cardiopulmonary mortality, and long-term exposure to fine particulate air pollution. JAMA-J. Am. Med. Assoc. 2002, 287:1132-1141.
41. Raulf-Heimsoth M., Angerer J., Pesch B., Marczynski B., Hahn J.U., Spickenheuer A., Preuss R., Ruhl R., Rode P., Bruning T. Biological monitoring as a useful tool for the detection of a coal-tar contamination in bitumen-exposed workers. J. Toxicol. Environ. Health A 2008, 71:746-750.
42. Report on Carcinogens Coal Tars and Coal-Tar Pitches 2011, Available at http://ntp.niehs.nih.gov/INDEXA5E1.HTM. Twelfth ed.
43. Report on Carcinogens Diesel Exhaust Particulates 2011, Available at http://ntp.niehs.nih.gov/ntp/roc/twelfth/profiles/DieselExhaustParticulates.pdf. Twelfth ed.
44. Ryno M., Rantanen L., Papaioannou E., Konstandopoulos A.G., Koskentalo T., Savela K. Comparison of pressurized fluid extraction, Soxhlet extraction and sonication for the determination of polycyclic aromatic hydrocarbons in urban air and diesel exhaust particulate matter. J. Environ. Monit. 2006, 8:488-493.
45. See S.W., Balasubramanian R., Yang T.S., Karthikeyan S. Assessing exposure to diesel exhaust particles: a case study. J. Toxicol. Environ. Health A 2006, 69:1909-1925.
46. Shinyashiki M., Eiguren-Fernandez A., Schmitz D.A., Di Stefano E., Li N., Linak W.P., Cho S.H., Froines J.R., Cho A.K. Electrophilic and redox properties of diesel exhaust particles. Environ. Res. 2009, 109:239-244.
47. Shultz C.A., Quinn A.M., Park J.H., Harvey R.G., Bolton J.L., Maser E., Penning T.M. Specificity of human aldo-keto reductases, NAD(P)H:quinone oxidoreductase, and carbonyl reductases to redox-cycle polycyclic aromatic hydrocarbon diones and 4-hydroxyequilenin-o-quinone. Chem. Research. Toxicol. 2011, 24:2153-2166.
48. Solomon P.A., Sioutas C. Continuous and semicontinuous monitoring techniques for particulate matter mass and chemical components: a synthesis of findings from EPA's Particulate Matter Supersites Program and related studies. J. Air Waste Manage (1995) 2008, 58:164-195.
49. Spencer W.A., Lehmler H.J., Robertson L.W., Gupta R.C. Oxidative DNA adducts after Cu(2+)-mediated activation of dihydroxy PCBs: role of reactive oxygen species. Free Radical Bio. Med. 2009, 46:1346-1352.
50. Sumi D., Kumagai Y. Chemical biology of 1,2-naphthoquinone, a novel air pollutant that affects signal transduction pathways. Yakugaku Zasshi. 2007, 127:1949-1956.
51. Suresh R., Shally A., Mahdi A.A., Patel D.K., Singh V.K., Rita M. Assessment of association of exposure to polycyclic aromatic hydrocarbons with bronchial asthma and oxidative stress in children: a case control study. Indian J. Occup. Environ. Med. 2009, 13:33-37.
52. Taguchi K., Fujii S., Yamano S., Cho A.K., Kamisuki S., Nakai Y., Sugawara F., Froines J.R., Kumagai Y. An approach to evaluate two-electron reduction of 9,10-phenanthraquinone and redox activity of the hydroquinone associated with oxidative stress. Free Radical Biol. Med. 2007, 43:789-799.
53. Tredaniel J., Aarab-Terrisse S., Teixeira L., Savinelli F., Fraboulet S., Gossot D., Hennequin C. Atmospheric air pollution and lung cancer: epidemiologic data. Rev. Mal. Respir. 2009, 26:437-445. (quiz 481, 484).
54. USEPA Revised Particulate Matter Standards 2005, Available at http://www.epa.gov/region4/airqualitytoolkit/5_airpollutioncontrol/airqualitystandards.pdf.
55. Valavanidis A., Fiotakis K., Vlachogianni T. Airborne particulate matter and human health: toxicological assessment and importance of size and composition of particles for oxidative damage and carcinogenic mechanisms. J. Environ. Sci. Health. C. Environ. Carcinog. Ecotoxicol. Rev. 2008, 26:339-362.
56. van Agen B., Maas L.M., Zwingmann I.H., Van Schooten F.J., Kleinjans J.C. B[a]P-DNA adduct formation and induction of human epithelial lung cell transformation. Environ. Mol. Mutagen. 1997, 30:287-292.
57. Wishart D.S., Knox C., Guo A.C., Eisner R., Young N., Gautam B., Hau D.D., Psychogios N., Dong E., Bouatra S., Mandal R., Sinelnikov I., Xia J., Jia L., Cruz J.A., Lim E., Sobsey C.A., Shrivastava S., Huang P., Liu P., Fang L., Peng J., Fradette R., Cheng D., Tzur D., Clements M., Lewis A., De Souza A., Zuniga A., Dawe M., Xiong Y., Clive D., Greiner R., Nazyrova A., Shaykhutdinov R., Li L., Vogel H.J., Forsythe I. HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res. 2009, 37:D603-D610.
58. Zhang L., Jin Y., Huang M., Penning T.M. The role of human aldo-keto reductases in the metabolic activation and detoxication of polycyclic aromatic hydrocarbons: interconversion of PAH catechols and PAH o-quinones. Front. Pharmacol. 2012, 3:193.
59. Zhao H., Ma J.K., Barger M.W., Mercer R.R., Millecchia L., Schwegler-Berry D., Castranova V., Ma J.Y. Reactive oxygen species- and nitric oxide-mediated lung inflammation and mitochondrial dysfunction in wild-type and iNOS-deficient mice exposed to diesel exhaust particles. J. Toxicol. Environ. Health A 2009, 72:560-570.
60. Zidzik J., Kalina I., Salagovic J., Sram R.J., Rossner P., Popov T., Farmer P.B. Influence of PAHs in ambient air on chromosomal aberrations in exposed subjects: international study - EXPAH. Mutat. Res. 2007, 620:41-48.