3-Nitrobenzanthrone and 3-aminobenzanthrone induce DNA damage and cell signalling in Hepa1c1c7 cells

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 684, Issue 1-2, 2010, Pages 11-23

  Landvik, N E ^a   Arlt, V M ^b   Nagy, E ^b   Solhaug, A ^c   Tekpli, X ^d   Schmeiser, H H ^e   Refsnes, M ^a   Phillips, D H ^b   Lagadic Gossmann, D ^d   Holme, J A ^a  

^a NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c NORWEGIAN VETERINARY INSTITUTE   (Norway)

^d IFR 140   (France)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

3 Aminobenzanthrone; 3 Nitrobenzanthrone; Carcinogenesis; Cell death; Cytokines; DNA damage

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 3 AMINOBENZANTHRONE; 3 NITROBENZANTHRONE; ATM PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CURCUMIN; CYTOKINE; DNA; HISTONE H2AX; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHORUS 32; PIFITHRIN ALPHA; POLYCYCLIC AROMATIC COMPOUND; PROTEIN BAX; PROTEIN P53; SINGLE STRANDED DNA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

AIR POLLUTION; ANIMAL CELL; APOPTOSIS; ARTICLE; CARCINOGENICITY; CELL DEATH; CELL NUCLEUS; CHEMICAL STRUCTURE; COMET ASSAY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DNA ADDUCT; DNA DAMAGE; DNA STRAND BREAKAGE; EXHAUST GAS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HEPATOMA CELL; IMMUNE SYSTEM; MITOCHONDRION; MOUSE; MUTAGENICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BENZ(A)ANTHRACENES; CELL CYCLE; CELL DEATH; CELL LINE, TUMOR; CHEMOKINE CXCL2; DNA DAMAGE; ENVIRONMENTAL POLLUTANTS; INTERLEUKIN-6; LIVER NEOPLASMS, EXPERIMENTAL; MICE; MUTAGENS; RECEPTORS, ARYL HYDROCARBON; SIGNAL TRANSDUCTION;

EID: 73949155760     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2009.11.004     Document Type: Article

References (69)

1. International Agency for Research on Cancer, Diesel and gasoline engine exhaust and some nitroarenes. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, No. 46, IARC, Lyon, France, 1989.
2. Arlt V.M. 3-Nitrobenzanthrone, a potential human cancer hazard in diesel exhaust and urban air pollution: a review of the evidence. Mutagenesis 20 (2005) 399-410
3. Boffetta P., Jourenkova N., and Gustavsson P. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Contr. 8 (1997) 444-472
4. Arlt V.M., Stiborova M., Henderson C.J., Osborne M.R., Bieler C.A., Frei E., Martinek V., Sopko B., Wolf C.R., Schmeiser H.H., and Phillips D.H. Environmental pollutant and potent mutagen 3-nitrobenzanthrone forms DNA adducts after reduction by NAD(P)H:quinone oxidoreductase and conjugation by acetyltransferases and sulfotransferases in human hepatic cytosols. Cancer Res. 65 (2005) 2644-2652
5. Arlt V.M., Zhan L., Schmeiser H.H., Honma M., Hayashi M., Phillips D.H., and Suzuki T. DNA adducts and mutagenic specificity of the ubiquitous environmental pollutant 3-nitrobenzanthrone in Muta Mouse. Environ. Mol. Mutagen. 43 (2004) 186-195
6. Arlt V.M., Bieler C.A., Mier W., Wiessler M., and Schmeiser H.H. DNA adduct formation by the ubiquitous environmental contaminant 3-nitrobenzanthrone in rats determined by (32)P-postlabeling. Int. J. Cancer 93 (2001) 450-454
7. Nagy E., Johansson C., Zeisig M., and Moller L. Oxidative stress and DNA damage caused by the urban air pollutant 3-NBA and its isomer 2-NBA in human lung cells analyzed with three independent methods. J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 827 (2005) 94-103
8. Tokiwa H., Sera N., Horikawa K., Nakanishi Y., and Shigematu N. The presence of mutagens/carcinogens in the excised lung and analysis of lung cancer induction. Carcinogenesis 14 (1993) 1933-1938
9. Arlt V.M., Gingerich J., Schmeiser H.H., Phillips D.H., Douglas G.R., and White P.A. Genotoxicity of 3-nitrobenzanthrone and 3-aminobenzanthrone in Muta™Mouse and lung epithelial cells derived from Muta™Mouse. Mutagenesis 23 (2008) 483-490
10. Enya T., Kawanishi M., Suzuki H., Matsui S., and Hisamatsu Y. An unusual DNA adduct derived from the powerfully mutagenic environmental contaminant 3-nitrobenzanthrone. Chem. Res. Toxicol. 11 (1998) 1460-1467
11. Arlt V.M., Glatt H., Muckel E., Pabel U., Sorg B.L., Seidel A., Frank H., Schmeiser H.H., and Phillips D.H. Activation of 3-nitrobenzanthrone and its metabolites by human acetyltransferases, sulfotransferases and cytochrome P450 expressed in Chinese hamster V79 cells. Int. J. Cancer 105 (2003) 583-592
12. Arlt V.M., Glatt H., Muckel E., Pabel U., Sorg B.L., Schmeiser H.H., and Phillips D.H. Metabolic activation of the environmental contaminant 3-nitrobenzanthrone by human acetyltransferases and sulfotransferase. Carcinogenesis 23 (2002) 1937-1945
13. Arlt V.M., Hewer A., Sorg B.L., Schmeiser H.H., Phillips D.H., and Stiborova M. 3-aminobenzanthrone, a human metabolite of the environmental pollutant 3-nitrobenzanthrone, forms DNA adducts after metabolic activation by human and rat liver microsomes: evidence for activation by cytochrome P450 1A1 and P450 1A2. Chem. Res. Toxicol. 17 (2004) 1092-1101
14. Stiborova M., Arlt V.M., Henderson C.J., Wolf C.R., Frei E., Schmeiser H.H., and Phillips D.H. Molecular mechanism of genotoxicity of the environmental pollutant 3-nitrobenzanthrone. Biomed. Pap. Med. Fac. Univ. Palacky. Olomouc. Czech. Rep. 149 (2005) 191-197
15. Dipple A., Khan Q.A., Page J.E., Ponten I., and Szeliga J. DNA reactions, mutagenic action and stealth properties of polycyclic aromatic hydrocarbon carcinogens. Int. J. Oncol. 14 (1999) 103-111 (Review)
16. Luch A. Cell cycle control and cell division: implications for chemically induced carcinogenesis. Chembiochem 3 (2002) 506-516
17. Paajarvi G., Jernstrom B., Seidel A., and Stenius U. Anti-diol epoxide of benzo[a]pyrene induces transient Mdm2 and p53 Ser15 phosphorylation, while anti-diol epoxide of dibenzo[a,l]pyrene induces a nontransient p53 Ser15 phosphorylation. Mol. Carcinogen. 47 (2008) 301-309
18. Landvik N.E., Gorria M., Arlt V.M., Asare N., Solhaug A., Lagadic-Gossmann D., and Holme J.A. Effects of nitrated-polycyclic aromatic hydrocarbons and diesel exhaust particle extracts on cell signalling related to apoptosis: possible implications for their mutagenic and carcinogenic effects. Toxicology 231 (2007) 159-174
19. Solhaug A., Refsnes M., Lag M., Schwarze P.E., Husoy T., and Holme J.A. Polycyclic aromatic hydrocarbons induce both apoptotic and anti-apoptotic signals in Hepa1c1c7 cells. Carcinogenesis 25 (2004) 809-819
20. Wiger R., Finstad H.S., Hongslo J.K., Haug K., and Holme J.A. Paracetamol inhibits cell cycling and induces apoptosis in HL-60 cells. Pharmacol. Toxicol. 81 (1997) 285-293
21. Gallagher J.E., Shank T., Lewtas J., Lefevre P.A., and Ashby J. Relative sensitivity of 32P-postlabelling of DNA and the autoradiographic UDS assay in the liver of rats exposed to 2-acetylaminofluorene (2AAF). Mutat. Res. 252 (1991) 247-257
22. Arlt V.M., Schmeiser H.H., Osborne M.R., Kawanishi M., Kanno T., Yagi T., Phillips D.H., and Takamura-Enya T. Identification of three major DNA adducts formed by the carcinogenic air pollutant 3-nitrobenzanthrone in rat lung at the C8 and N2 position of guanine and at the N6 position of adenine. Int. J. Cancer 118 (2006) 2139-2146
23. Marx J. Cancer research. Inflammation and cancer: the link grows stronger. Science 306 (2004) 966-968
24. Oesterling E., Toborek M., and Hennig B. Benzo[a]pyrene induces intercellular adhesion molecule-1 through a caveolae and aryl hydrocarbon receptor mediated pathway. Toxicol. Appl. Pharmacol. 232 (2008) 309-316
25. Kundu J.K., and Surh Y.J. Inflammation: gearing the journey to cancer. Mutat. Res. 659 (2008) 15-30
26. Arlt V.M., Sorg B.L., Osborne M., Hewer A., Seidel A., Schmeiser H.H., and Phillips D.H. DNA adduct formation by the ubiquitous environmental pollutant 3-nitrobenzanthrone and its metabolites in rats. Biochem. Biophys. Res. Commun. 300 (2003) 107-114
27. Arlt V.M., Henderson C.J., Wolf C.R., Schmeiser H.H., Phillips D.H., and Stiborova M. Bioactivation of 3-aminobenzanthrone, a human metabolite of the environmental pollutant 3-nitrobenzanthrone: evidence for DNA adduct formation mediated by cytochrome P450 enzymes and peroxidases. Cancer Lett. 234 (2006) 220-231
28. Arlt V.M., Stiborova M., Hewer A., Schmeiser H.H., and Phillips D.H. Human enzymes involved in the metabolic activation of the environmental contaminant 3-nitrobenzanthrone: evidence for reductive activation by human NADPH:cytochrome p450 reductase. Cancer Res. 63 (2003) 2752-2761
29. Albertini R.J., Anderson D., Douglas G.R., Hagmar L., Hemminki K., Merlo F., Natarajan A.T., Norppa H., Shuker D.E., Tice R., Waters M.D., and Aitio A. IPCS guidelines for the monitoring of genotoxic effects of carcinogens in humans. International Programme on Chemical Safety. Mutat. Res. 463 (2000) 111-172
30. Efeyan A.M. Serrano. p53: guardian of the genome and policeman of the oncogenes. Cell Cycle 6 (2007) 1006-1010
31. Dent P., Yacoub A., Fisher P.B., Hagan M.P., and Grant S. MAPK pathways in radiation responses. Oncogene 22 (2003) 5885-5896
32. Sengul S., Zwizinski C., and Batuman V. Role of MAPK pathways in light chain-induced cytokine production in human proximal tubule cells. Am. J. Physiol. Renal Physiol. 284 (2003) F1245-F1254
33. Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr. Opin. Cell Biol. 10 (1998) 262-267
34. de Martin R., Schmid J.A., and Hofer-Warbinek R. The NF-kappaB/Rel family of transcription factors in oncogenic transformation and apoptosis. Mutat. Res. 437 (1999) 231-243
35. Nagy E., Zeisig M., Kawamura K., Hisamatsu Y., Sugeta A., Adachi S., and Moller L. DNA adduct and tumor formations in rats after intratracheal administration of the urban air pollutant 3-nitrobenzanthrone. Carcinogenesis 26 (2005) 1821-1828
36. Enya T., Suzuki H., Watanabe T., Hirayama T., and Hisamatsu Y. 3-Nitrobenzanthrone, a powerful bacterial mutagen and suspected human carcinogen found in diesel exhaust and airborne particulates. Environ. Sci. Technol. 31 (1997) 2772-2776
37. Borlak J., Hansen T., Yuan-Zhi X., Sikka H.C., Kumar S., Schmidbauer S., Frank H., Jacob J., and Seidel A. Metabolism and DNA-binding of 3-nitrobenzanthrone in primary rat alveolar type ii cells, in human fetal bronchial, rat epithelial and mesenchymal cell lines. Polycycl. Aromat. Compd. 21 (2002) 73-86
38. Seidel A., Dahmann D., Krekeler H., and Jacob J. Biomonitoring of polycyclic aromatic compounds in the urine of mining workers occupationally exposed to diesel exhaust. Int. J. Hyg. Environ. Health 204 (2002) 333-338
39. Hansen T., Seidel A., and Borlak J. The environmental carcinogen 3-nitrobenzanthrone and its main metabolite 3-aminobenzanthrone enhance formation of reactive oxygen intermediates in human A549 lung epithelial cells. Toxicol. Appl. Pharmacol. 221 (2007) 222-234
40. Holme J.A., Gorria M., Arlt V.M., Ovrebo S., Solhaug A., Tekpli X., Landvik N.E., Huc L., Fardel O., and Lagadic-Gossmann D. Different mechanisms involved in apoptosis following exposure to benzo[a]pyrene in F258 and Hepa1c1c7 cells. Chem. Biol. Interact. 167 (2007) 41-55
41. Nagy E., Adachi S., Takamura-Enya T., Zeisig M., and Moller L. DNA damage and acute toxicity caused by the urban air pollutant 3-nitrobenzanthrone in rats: characterization of DNA adducts in eight different tissues and organs with synthesized standards. Environ. Mol. Mutagen. 47 (2006) 541-552
42. Ford J.M. Regulation of DNA damage recognition and nucleotide excision repair: another role for p53. Mutat. Res. 577 (2005) 195-202
43. Niida H., and Nakanishi M. DNA damage checkpoints in mammals. Mutagenesis 21 (2006) 3-9
44. Hussain S.P., and Harris C.C. Inflammation and cancer: an ancient link with novel potentials. Int. J. Cancer 121 (2007) 2373-2380
45. vom B.J., Krais A., Whibley C., Hollstein M.C., and Schmeiser H.H. The carcinogenic air pollutant 3-nitrobenzanthrone induces GC to TA transversion mutations in human p53 sequences. Mutagenesis 24 (2009) 17-23
46. Zgheib O., Huyen Y., DiTullio Jr. R.A., Snyder A., Venere M., Stavridi E.S., and Halazonetis T.D. ATM signaling and 53BP1. Radiother. Oncol. 76 (2005) 119-122
47. Vousden K.H., and Lu X. Live or let die: the cell's response to p53. Nat. Rev. Cancer 2 (2002) 594-604
48. Bratton S.B., and Cohen G.M. Apoptotic death sensor: an organelle's alter ego?. Trends Pharmacol. Sci. 22 (2001) 306-315
49. Moll U.M., Wolff S., Speidel D., and Deppert W. Transcription-independent pro-apoptotic functions of p53. Curr. Opin. Cell Biol. 17 (2005) 631-636
50. Komarov P.G., Komarova E.A., Kondratov R.V., Christov-Tselkov K., Coon J.S., Chernov M.V., and Gudkov A.V. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285 (1999) 1733-1737
51. Whiteside T.L. The tumor microenvironment and its role in promoting tumor growth. Oncogene 27 (2008) 5904-5912
52. Roberts P.J., and Der C.J. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 26 (2007) 3291-3310
53. Campbell K.J., Rocha S., and Perkins N.D. Active repression of antiapoptotic gene expression by RelA(p65) NF-kappa B. Mol. Cell 13 (2004) 853-865
54. Persons D.L., Yazlovitskaya E.M., and Pelling J.C. Effect of extracellular signal-regulated kinase on p53 accumulation in response to cisplatin. J. Biol. Chem. 275 (2000) 35778-35785
55. Wang S., and Shi X. Mechanisms of Cr(VI)-induced p53 activation: the role of phosphorylation, mdm2 and ERK. Carcinogenesis 22 (2001) 757-762
56. She Q.B., Chen N., and Dong Z. ERKs and p38 kinase phosphorylate p53 protein at serine 15 in response to UV radiation. J. Biol. Chem. 275 (2000) 20444-20449
57. Janssens S., and Tschopp J. Signals from within: the DNA-damage-induced NF-kappaB response. Cell Death. Differ. 13 (2006) 773-784
58. Coussens L.M., and Werb Z. Inflammation and cancer. Nature 420 (2002) 860-867
59. Pei X.H., Nakanishi Y., Inoue H., Takayama K., Bai F., and Hara N. Polycyclic aromatic hydrocarbons induce IL-8 expression through nuclear factor kappaB activation in A549 cell line. Cytokine 19 (2002) 236-241
60. Aggarwal B.B., Shishodia S., Sandur S.K., Pandey M.K., and Sethi G. Inflammation and cancer: how hot is the link?. Biochem. Pharmacol. 72 (2006) 1605-1621
61. Vogel C.F., and Matsumura F. A new cross-talk between the aryl hydrocarbon receptor and RelB, a member of the NF-kappaB family. Biochem. Pharmacol. 77 (2009) 734-745
62. Hollingshead B.D., Beischlag T.V., Dinatale B.C., Ramadoss P., and Perdew G.H. Inflammatory signaling and aryl hydrocarbon receptor mediate synergistic induction of interleukin 6 in MCF-7 cells. Cancer Res. 68 (2008) 3609-3617
63. Stiborova M., Dracinska H., Hajkova J., Kaderabkova P., Frei E., Schmeiser H.H., Soucek P., Phillips D.H., and Arlt V.M. The environmental pollutant and carcinogen 3-nitrobenzanthrone and its human metabolite 3-aminobenzanthrone are potent inducers of rat hepatic cytochromes P450 1A1 and -1A2 and NAD(P)H:quinone oxidoreductase. Drug Metab. Dispos. 34 (2006) 1398-1405
64. Van Laere S.J., Van A.d., Van den Eynden I.G.G., van D.P., Van Marck E.A., Vermeulen P.B., and Dirix L.Y. NF-kappaB activation in inflammatory breast cancer is associated with oestrogen receptor downregulation, secondary to EGFR and/or ErbB2 overexpression and MAPK hyperactivation. Br. J. Cancer 97 (2007) 659-669
65. Vogel C.F., and Matsumura F. A new cross-talk between the aryl hydrocarbon receptor and RelB, a member of the NF-kappaB family. Biochem. Pharmacol. (2008)
66. Ryan K.M., Ernst M.K., Rice N.R., and Vousden K.H. Role of NF-kappaB in p53-mediated programmed cell death. Nature 404 (2000) 892-897
67. Beinke S., and Ley S.C. Functions of NF-kappaB1 and NF-kappaB2 in immune cell biology. Biochem. J. 382 (2004) 393-409
68. Lee Z.H., and Kim H.H. Signal transduction by receptor activator of nuclear factor kappa B in osteoclasts. Biochem. Biophys. Res. Commun. 305 (2003) 211-214
69. Chiarugi P. PTPs versus PTKs: the redox side of the coin. Free Radic. Res. 39 (2005) 353-364