Benzo(a)pyrene modulates fluoranthene-induced cellular responses in HT-29 colon cells in a dual exposure system

Environmental Toxicology and Pharmacology

Volumn 36, Issue 2, 2013, Pages 358-367

  Harris, Kelly L ^a   Myers, Jeremy N ^a   Ramesh, Aramandla ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

Benzo(a)pyrene; Fluoranthene; Metabolism; Polycyclic aromatic hydrocarbons

Indexed keywords

BENZO[A]PYRENE; CASPASE 3; FLUORANTHENE; PROPIDIUM IODIDE;

APOPTOSIS; ARTICLE; BIOTRANSFORMATION; CELL CULTURE; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL GROWTH; CELL METABOLISM; CONTROLLED STUDY; CYTOTOXICITY; ENVIRONMENTAL EXPOSURE; ENZYME ASSAY; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY;

BENZO(A)PYRENE; FLUORANTHENE; METABOLISM; POLYCYCLIC AROMATIC HYDROCARBONS;

ADENOCARCINOMA; APOPTOSIS; BENZO(A)PYRENE; BIOTRANSFORMATION; CARCINOGENS; CASPASE 3; CELL CYCLE; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLONIC NEOPLASMS; COOKING; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; FLUORENES; HT29 CELLS; HUMANS; MEAT; TIME FACTORS;

EID: 84878974938     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2013.04.017     Document Type: Article

References (62)

1. Abbas A.O., Brack W. Polycyclic aromatic hydrocarbons in Niger Delta soil: contamination sources and profiles. Int. J. Environ. Sci. Technol. 2006, 2:343-352.
2. Aries E., Andesrson D.R., Fisher R. Exposure assessment of workers to airborne PCDD/Fs, PCBs and PAHs at an electric arc furnace steel-making plant in the UK. Ann Occup Hyg 2008, 52:213-225.
3. Aquilina N.J., Delgado-Saborit J.M., Meddings C., Baker S., Harrison R.M., Jacob P., Wilson M., Yu L., Duan M., Benowitz N.L. Environmental and biological monitoring of exposures to PAHs and ETS in the general population. Environ. Int. 2010, 36:763-771.
4. 2-deoxyguanosine adduct. Carcinogenesis 1986, 7:859-865.
5. Blagosklonny M.V., Pardee A.B. The restriction point of the cell cycle. Cell Cycle 2002, 1:103-110.
6. Buesen R., Mock M., Seidel A., Jacob J., Lampen A. Interaction between metabolism and transport of benzo[a]pyrene and its metabolites in enterocytes. Toxicol. Appl. Pharmacol. 2002, 183:168-178.
7. 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.
8. Culp S.J., Gaylor D.W., Sheldon W.G., Goldstein L.S., Beland F.A. A comparison tar and benzo(a)pyrene in a 2-year bioassay. Carcinogenesis 1998, 19:117-124.
9. Danion M., LeFloch S., Kannan R., Lamour F., Quentel C. Effects of in vivo chronic hydrocarbons pollution on sanitary status and immune system in sea bass (Dicentrachus labrax L.). Aquat. Toxicol. 2011, 105:300-311.
10. de Waard P.W., de Kok T.M., Maas L.M., Peijnenburg A.A., Hoogenboom R.L., Aarts J.M., van Schooten F.J. Influence of TCDD and natural Ah receptor agonists on benzo[a]pyrene-DNA adduct formation in the Caco-2 human colon cell line. Mutagenesis 2008, 2:67-73.
11. Diggs D.L., Huderson A.C., Harris K.L., Myers J.N., Banks L.D., Rekhadevi P.V., Niaz M.S., Ramesh A. Polycyclic aromatic hydrocarbons and digestive tract cancers: a perspective. J. Environ. Sci. Health C: Environ. Carcinog. Ecotoxicol. Rev. 2011, 29:324-357.
12. Min mouse model of colon cancer. Tumour Biol. 2012, 33:1255-1260.
13. Ebert M.N., Klinder A., Peters W.H.M., Schaferhenrich A., Sendt W., Scheele J., Pool-Zobel B.L. Expression of glutathione S-transferases (GSTs) in human colon cells and inducibility of GSTM2 by butyrate. Carcinogenesis 2003, 24:1637-1644.
14. EPA Integrated Risk Information System (IRIS) National Center for Environmental Assessment 2001, Available online at:, (accessed May 2003). http://www.epa.gov/iris/index.html.
15. Grainger J., Huang W., Patterson D.G., Turner W.E., Pirkle J., Caudill S.P., Wang R.Y., Needham L.L., Sampson E.J. Reference range levels of polycyclic aromatic hydrocarbons in the US population by measurement of urinary monohydroxy metabolites. Environ. Res. 2006, 100:394-423.
16. Grimmer G., Naujack K.W., Dettbarn G. Gaschromatographic determination of polycyclic aromatic hydrocarbons, aza-arenes, aromatic amines in the particle and vapor phase of mainstream and sidestream smoke of cigarettes. Toxicol. Lett. 1987, 35:117-124.
17. Hakura A., Seki Y., Sonoda J., Hosokawa S., Aoki T., Suganuma A., Kerna W.D., Tsukidate K. Rapid induction of colonic adenocarcinoma in mice exposed to benzo[a]pyrene and dextran sulfate sodium. Food Chem. Toxicol. 2011, 49:2997-3001.
18. Min mouse exposed to benzo(a)pyrene. Toxicol. Pathol. 2009, 37:938-946.
19. Herbst U., Fuchs J.I., Teubner W., Steinberg P. Malignant transformation of human colon epithelial cells by benzo[c]phenanthrene dihydrodiolepoxides as well as 2-hydroxyamino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Toxicol. Appl. Pharmacol. 2006, 212:136-145.
20. Hinoshita F., Hardin J.A., Sherr D.H. Fluoranthene induces programmed cell death and alters growth of immature B cell populations in bone marrow cultures. Toxicology 1992, 73:203-218.
21. Hsieh T., Halicka D., Lu X., Kunicki J., Guo J., Darzynkiewicz Z., Wu J. Effects of resveratrol on the G(0)-G(1) transition and cell cycle progression of mitogenically stimulated human lymphocytes. Biochem. Biophys. Res. Commun. 2002, 297:1311-1317.
22. Huang M.C., Chen F.Y., Chou M.T., Su G. Fluoranthene enhances p53 expression and decreases mutagenesis induced by benzo(a)pyrene. Toxicol. Lett. 2012, 13:214-224.
23. Huderson A.C., Harris D.L., Niaz M.S., Ramesh A. Effect of benzo(a)-pyrene exposure on fluoranthene metabolism by mouse adipose tissue microsomes. Toxicol. Mech. Methods 2010, 20:53-58.
24. Hughes N.C., Phillips D.H. Covalent binding of dibenzpyrenes and benzo[a]-pyrene to DNA: evidence for synergistic and inhibitory interactions when applied in combination to mouse skin. Carcinogenesis 1990, 11:1611-1619.
25. Hutchins D.A., Skipper P.L., Naylor S., Tannenbaum S.R. Isolation and characterization of the major fluoranthene-hemoglobin adducts formed in vivo in the rat. Cancer Res. 1988, 48:4756-4761.
26. IPCS. Environmental Health Criteria 202: Selected non-heterocyclic polycyclic aromatic hydrocarbons. International Programme on Chemical Safety, World Health Organization, Lyon, France: 1998.
27. Iwanari M., Nakajima M., Kizu R., Hayakawa K., Yokoi T. Induction of CYP1A1, CYP1A2, and CYP1B1 mRNAs by nitropolycyclic aromatic hydrocarbons in various human tissue-derived cells: chemical-, cytochrome P450 isoform-, and cell-specific differences. Arch. Toxicol. 2002, 76:287-298.
28. Jeffy B.D., Chen E.J., Gudas J.M., Romagnolo D.F. Disruption of cell cycle kinetics by benzo[a]pyrene: inverse expression patterns of BRCA-1 and p53 in MCF-7 cells arrested in S and G2. Neoplasia 2000, 2:460-470.
29. Khalil A., Villard P.H., Dao M.A., Burcelin R., Champion S., Fouchier F., Savouret J.F., Barra Y., Seree E. Polycyclic aromatic hydrocarbons potentiate high-fat diet effects on intestinal inflammation. Toxicol. Lett. 2010, 196:161-167.
30. Kim J.H., Yamaguchi K., Lee S.H., Tithof P.K., Sayler G.S., Yoon J.H., Baek S.J. Evaluation of polycyclic aromatic hydrocarbons in the activation of early growth response-1 and peroxisome proliferator activated receptors. Toxicol. Sci. 2005, 85:585-593.
31. Ko C.B., Kim S.J., Park C., Kim B.R., Shin C.H., Choi S., Chung S.Y., Noh J.H., Jeun J.H., Kim N.S., Park R. Benzo(a)pyrene-induced apoptotic death of mouse hepatoma Hepa1c1c7 cells via activation of intrinsic caspase cascade and mitochondrial dysfunction. Toxicology 2004, 199:35-46.
32. Knuckles M.E., Inyang F., Ramesh A. Acute and subchronic oral toxicity of benzo(a)pyrene in F-344 rats. Toxicol. Sci. 2001, 61:382-388.
33. Knuckles M.E., Inyang F., Ramesh A. Acute and subchronic oral toxicity of fluoranthene in F-344 rats. Ecotoxicol. Environ. Saf. 2004, 59:102-108.
34. Le Hégarat L., Huet S., Fessard V. A co-culture system of human intestinal Caco-2 cells and lymphoblastoid TK6 cells for investigating the genotoxicity of oral compounds. Mutagenesis 2012, 27:631-636.
35. Maga J.A. Polycyclic aromatic hydrocarbon (PAH) composition of mesquite (Prosopis fuliflora) smoke and grilled beef. J. Agric. Food Chem. 1986, 34:249-251.
36. Martí-Cid R., Llobet J.M., Castell V., Domingo J.L. Evolution of the dietary exposure to polycyclic aromatic hydrocarbons in Catalonia, Spain. Food Chem. Toxicol. 2008, 46:3163-3171.
37. Mitchell D.M., Ball J.M. Characterization of a spontaneously polarizing HT-29 cell line, HT-29/c/f8. In Vitro Cell Dev. Biol. Animal 2004, 40:297-302.
38. Myers J.N., Rekhadevi P.V., Ramesh A. Comparative evaluation of different cell lysis and extraction methods for studying benzo(a)pyrene metabolism in HT-29 colon cancer cell cultures. Cell Physiol. Biochem. 2011, 28:209-218.
39. Norbury C.J. The cancer cell cycle. Introduction to the Cellular and Molecular Biology of Cancer 2005, 156-157. Oxford University Press, Oxford, UK. 4th ed. M.A. Knowles, P.J. Selby (Eds.).
40. Ogba N., Wang C., Raychoudhury S. Differential effects of fluoranthene and benzo[a]pyrene in MCF-7 cells. J. Environ. Sci. Health A: Toxicol. Hazard Subst. Environ. Eng. 2005, 40:927-936.
41. Pan C.H., Chan C.C., Wu K.Y. Effects on Chinese restaurant workers of exposure to cooking oil fumes: a cautionary note on urinary 8-hydroxy-2'-deoxyguanosine. Cancer Epidemiol Biomarkers Prev 2008, 17:3351-3357.
42. Patten Hitt E., DeLong M.J., Merrill A.H. Benzo(a)pyrene activates extracellular signal-related and p38 mitogen-activated protein kinases in HT29 colon adenocarcinoma cells: involvement in NAD(P)H:quinone reductase activity and cell proliferation. Toxicol. Appl. Pharmacol. 2002, 183:160-167.
43. Phillips D.H., Grover P.L. Polycyclic hydrocarbon activation: bay regions and beyond. Drug Metab. Rev. 1994, 26:443-467.
44. Ramesh A., Walker S.A., Hood D.B., Guillen M.D., Schneider H., Weyand E.H. Bioavailability and risk assessment of orally ingested polycyclic aromatic hydrocarbons. Int. J. Toxicol. 2004, 2:301-333.
45. Ramesh A., Archibong A.E., Hood D.B., Guo Z., Loganathan B.G. Global environmental distribution and human health effects of polycyclic aromatic hydrocarbons. Global Contamination Trends of Persistent Organic Chemicals 2011, 95-124. CRC Press, Boca Raton, FL. B.G. Loganathan, P.K.-S. Lam (Eds.).
46. Ramesh A., Archibong A.E., Huderson A.C., Diggs D.L., Myers J.N., Hood D.B., Rekhadevi P.V., Niaz M.S. Polycyclic aromatic hydrocarbons. Veterinary Toxicology 2012, 797-809. Elsevier, New York. R. Gupta (Ed.).
47. Raychoudhury S.S., Kubinski D. Polycyclic aromatic hydrocarbon-induced cytotoxicity in cultured rat Sertoli cells involves differential apoptotic response. Environ. Health Perspect. 2003, 111:33-38.
48. Rubin H. Synergistic mechanisms in carcinogenesis by polycyclic aromatic hydrocarbons and by tobacco smoke: a bio-historical perspective with updates. Carcinogenesis 2001, 22:1903-1930.
49. Sambruy Y., Ferruzza S., Ranaldi G., DeAngelis I. Intestinal cell culture models. Appl. Toxicol. Pharmacol. Cell Biol. Toxicol. 2001, 17:301-317.
50. Schirmer K., Chan A.G., Greenberg B.M., Dixon D.G., Bols N.C. Ability of 16 priority PAHs to be photocytotoxic to a cell line from the rainbow trout gill. Toxicology 1998, 127:1431-1455.
51. Sjogren M., Ehrenberg L., Rannug U. Relevance of different biological assays in assessing initiating and promoting properties of polycyclic aromatic hydrocarbons with respect to carcinogenic potency. Mutat. Res. 1996, 358:97-112.
52. Tarantini A., Maître A., Lefèbvre E., Marques M., Rajhi A., Douki T. Polycylic aromatic hydrocarbons in binary mixtures modulate the efficiency of benzo[a]pyrene to form DNA adducts in human cells. Toxicology 2011, 279:36-44.
53. Uno S., Makishima M. Benzo(a)pyrene toxicity and inflammatory disease. Curr. Rheumatol. Rev. 2009, 5:266-271.
54. Vaca C., Tornquist M., Rannug U., Lindahl-Kiessling K., Ahrlstrom G., Ehrenberg L. On the bioactivation and genotoxic action of fluoranthene. Arch. Toxicol. 1992, 66:538-545.
55. Walker S.A., Whitten L.B., Seals G.B., Lee W.E., Archibong A.E., Ramesh A. Interspecies comparison of liver and small intestinal microsomal metabolism of fluoranthene. Food Chem. Toxicol. 2006, 44:380-387.
56. Warshawsky D., Barkley W., Bingham E. Factors affecting carcinogenic potential of mixtures. Fundam. Appl. Toxicol. 1993, 20:376-382.
57. Wei W., Li X.F., Li X.N., Chen X.M., Liu A.L., Lu W.Q. Oxidative stress and cell-cycle change induced by coexposed PCB126 and benzo(a) pyrene to human hepatoma (HepG2) cells. Environ. Toxicol. 2010, 27:316-320.
58. Weiss R.S., Leder P., Vaziri C. Critical role for mouse Hus1 in an S-phase DNA damage cell cycle checkpoint. Mol. Cell Biol. 2003, 23:791-803.
59. Wessel N., Ménard D., Pichavant-Rafini K., Olivier H., LeGoff J., Burgeot T., Akcha F. Genotoxic and enzymatic effects of fluoranthene in microsomes and freshly isolated hepatocytes from sole (Solea solea). Aquat. Toxicol. 2012, 108:33-41.
60. Wester P.W., Muller J.J., Slob W., Mohn G.R., Dortant P.M., Kroese E.D. Carcinogenic activity of benzo[a]pyrene in a 2 year oral study in Wistar rats. Food Chem. Toxicol. 2012, 50:927-935.
61. WHO Selected non-heterocyclic polycyclic aromatic hydrocarbons. Environmental Health Criteria 202 1998, World Health Organization, Geneva, 883 pp.
62. Yamaguchi K., Near R., Shneider A., Cui H., Ju S.T., Sherr D.H. Fluoranthene-induced apoptosis in murine T cell hybridomas is independent of the aromatic hydrocarbon receptor. Toxicol. Appl. Pharmacol. 1996, 139:144-152.