Benzo(a)pyrene-induced apoptotic death of mouse hepatoma Hepa1c1c7 cells via activation of intrinsic caspase cascade and mitochondrial dysfunction

Toxicology

Volumn 199, Issue 1, 2004, Pages 35-46

  Ko, Chang Bo ^a   Kim, Se Jin ^a   Park, Channy ^a   Kim, Bok Ryang ^b   Shin, Chang Ho ^b   Choi, Sujinna ^c   Chung, Sang Young ^c   Noh, Joon Hwa ^c   Jeun, Jin Ho ^a   Kim, Nam Song ^d   Park, Raekil ^a  

^a Wonkwang University School of Medicine   (South Korea)

^b Wonkwang University   (South Korea)

^c Chonnam National University Medical School   (South Korea)

^d SKY Sports Medicine Lab   (South Korea)

Author keywords

2,3,7,8 Tetrachlorodibenzo p dioxin; 3,12 Dimethylbenzo(a)anthracene; BaP; Benzo(a)pyrene; DMBA; MTT; PAH; PARP; Poly(ADP ribose)polymerase; Polycyclic aromatic hydrocarbon; TCDD; VADC; Voltage dependent anion channel

Indexed keywords

AROMATIC HYDROCARBON; BENZO[A]PYRENE; CARCINOGEN; CASPASE 3; CASPASE 9; CYTOCHROME C; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; SERINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CATALYSIS; CELL ACTIVATION; CELL LINE; CYTOSOL; DOSE RESPONSE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME RELEASE; MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; TIME; TRANSCRIPTION INITIATION;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BENZO(A)PYRENE; CARCINOGENS; CARCINOMA, HEPATOCELLULAR; CASPASES; CELL LINE, TUMOR; ENZYME ACTIVATION; HEPATOCYTES; MEMBRANE POTENTIALS; MICE; MITOCHONDRIA; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 2342522012     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2004.01.039     Document Type: Article

References (41)

1. Bennett M., MacDonald K., Chan S.W., Luzio J.P., Simari R., Weissberg P. Cell surface trafficking of F as: a rapid mechanism of p53-mediated apoptosis. Science. 282:1998;290-293
2. Burchiel S.W., Davis D.A., Ray S.D., Barton S.L. DMBA induces programmed cell death (apoptosis) in the A20.1 murine B cell lymphoma. Fundam. Appl. Toxicol. 21:1993;120-124
3. Chen S., Nguyen N., Tamura K., Karin M., Tukey R.H. The role of the Ah receptor and p38 in benzo(a) pyrene-7, 8-dihydrodiol and benzo(a) pyrene-7, 8-dihydrodiol 9, 10-epoxide-induced apoptosis. J. Biol. Chem. 278:2003;19526-19533
4. Conney A.H. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G.H.A. Clowes memorial lecture. Cancer Res. 42:1982;4875-4917
5. Denissenko M.F., Pao A., Tang M., Pfeifer G.P. Preferential formation of benzo(a)pyrene addicts at lung cancer mutational hotspots in p53. Science. 274:1996;430-432
6. Dipple A. DNA adducts of chemical carcinogens. Carcinogenesis. 16:1995;437-441
7. El-Deiry W.S., Tokino T., Velculescu V.E., Levy D.B., Parsons R., Trent J.M., Lin D., Mercer W.E., Kinzler K.W., Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell. 19:1994;817-825
8. Fernandez-Salguero P., Pineau T., Hilbert D.M., McPhail T., Lee S.S., Kimura S., Nebert D.W., Rudikoff S., Ward J.M., Gonzalez F.J. Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science. 268:1995;722-726
9. Ferreira C.G., Span S.W., Peters G.J., Kruyt F.A., Giaccone G. Chemotherapy triggers apoptosis in a caspase-8-dependent and mitochondria-controlled manner in the non small cell lung cancer cell line NCI-H460. Cancer Res. 60:2000;7133-7141
10. Fritsche M., Haessler C., Brandner G. Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene. 8:1993;307-318
11. Fuchs E.J., Mckenna K.A., Bedi A. p53-dependent DNA damage-induced apoptosis requires Fas/APO-1-independent activation of CPP32beta. Cancer Res. 57:1997;2550-2554
12. Germain M., Affar E.B., Amours D., Dixit V.M., Salvesen G.S., Poirier G. Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. J. Biol. Chem. 274:1999;28379-28384
13. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312
14. Henkels K.M., Turchi J.J. Cisplatin-induced apoptosis proceeds by caspase-3-dependent and -independent pathways in cisplatin-resistant and -sensitive human ovarian cancer cell lines. Cancer Res. 59:1999;3077-3083
15. Hsing A., Faller D.V., Vaziri C. DNA-damaging aryl hydrocarbons induce mdm2 expression via p53-independent post-transcriptional mechanisms. J. Biol. Chem. 275:2000;26024-26031
16. Kamath A.B., Xu H., Nagarkatti P.S., Nagarkatti M. Evidence for the induction of apoptosis in thymocytes by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in vivo. Toxicol. Appl. Pharmacol. 142:1997;367-377
17. Lei W., Yu R., Mandlekar S., Kong A-N.T. Induction of apoptosis and activation of interleukin 1β-converting enzyme/Ced-3 protease (caspase-3) and c-Jun NH2-terminal kinase 1 by benzo(a)pyrene. Cancer Res. 58:1998;2102-2106
18. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:1997;479-489
19. Lowe S.W., Schmitt E.M., Smith S.W., Osborne B.A., Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature. 362:1993;847-849
20. Miller M.L., Andringa A., Cody T., Dixon K., Albert R.E. Cell proliferation and nuclear abnormalities are increased and apoptosis is decreased in the epidermis of the p53 null mouse after topical application of benzo(a)pyrene. Cell Prolif. 29:1996;561-576
21. Miyashita T., Reed J.C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 80:1995;293-299
22. Nebert D.W., Gonzalez F.J. P450 genes: structure, evolution, and regulation. Annu. Rev. Biochem. 56:1987;954-993
23. Pei X., Nakanishi Y., Yakayama K., Bai F., Hara N. Benzo(a)pyrene activates the human p53 gene through induction of nuclear factor kB activity. J. Biol. Chem. 274:1999;35240-35246
24. Phillips D.H. Fifty years of benzo(a)pyrene. Nature. 303:1983;468-472
25. Polyak K., Xia Y., Zweier J.L., Kinzler K.W., Vogelstein B. A model for p53-induced apoptosis. Nature. 389:1997;300-305
26. Reyes H., Reisz-Porszasz S., Hankinson O. Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science. 256:1992;1193-1195
27. Saleh A., Srinivasula S.M., Acharya S., Fishel R., Alnemri E.S. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J. Biol. Chem. 274:1999;17941-17945
28. Schuler M., Bossy-Wetzel E., Goldstein J.C., Fitzgerald P.F., Green D.R. p53 induces apoptosis by caspase activiation through mitochondrial cytochrome c release. J. Biol. Chem. 275:2000;7337-7342
29. Sheikh M.S., Burns T.F., Huang Y., Wu G.S., Amundson S., Brooks K.S., Fornace A.J. Jr., El-Deiry W.S. p53-dependent and -independent regulation of the death receptor KILLER/DR5 gene expression in response to genotoxic stress and tumor necrosis factor alpha. Cancer Res. 58:1998;1593-1598
30. Shimada T., Gillam E.M., Sandhu P., Guo Z., Tukey R.H., Guengerich F.R. Activation of procarcinogens by human cytochrome P450 enzymes expressed in Escherichia coli: simplified bacterial systems for genotoxicity assays. Carcinogenesis. 15:1994;2523-2529
31. Shimada T., Gillam E.M., Oda Y., Tsumura F., Sutter T.R., Guengerich F.P., Inoue K. Metabolism of benzo(a)pyrene to trans-7, 8-dihydroxy-7, 8-dihydrobenzo(a)pyrene by recombinant human cytochrome P450 1B1 and purified liver epoxide hydrolase. Chem. Res. Toxicol. 12:1999;623-629
32. Shimada T., Inoue K., Suzuki Y., Kawai T., Azuma E., Nakajima T., Shindo M., Kurose K., Sugie A., Yamagishi Y. Aryl hydrocarbon receptor-dependent induction of liver and lung cytochromes P450, 1A1, 1A2, and 1B1 by polycyclic aromatic hydrocarbons and polychlorinated biphenyls in genetically-engineered C57BL/6J mice. Carcinogenesis. 23:2003;1199-1207
33. Soengas M.S., Alarcon R.M., Yoshida H., Giaccia A.J., Hakem R., Mak T.W., Lowe S.W. Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition. Science. 84:1999;156-159
34. Tanaka H., Arakawa H., Yamaguchi T., Shiraish K., Fukuda S., Matsui K., Takei Y., Nakamura Y. A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature. 404:2000;42-49
35. Tokiwa H., Sera N., Horikawa K., Nakanishi Y., Shigematu N. The presence of mutagens/carcinogens in the excised lung and analysis of lung cancer induction. Carcinogenesis. 14:1993;1933-1938
36. Vaziri C., Faller D.V. A benzo(a)pyrene-induced cell cycle checkpoint resulting in p53-independent G1 arrest in 3T3 fibroblasts. J. Biol. Chem. 272:1997;2762-2769
37. Venkatachalam S., Denissenko M., Wani A.A. Modulation of (+/-)-anti-BPDE-mediated p53 accumulation by inhibitors of protein kinase C and poly(ADP-ribose) polymerase. Oncogene. 14:1997;801-809
38. Wieder T., AramPorkop F.E., Schmelz K., Schulze-Osthoff K., Beyaert R., Dorken B., Daniel P.T. Activation of caspase-8 in drug-induced apoptosis of B-lymphoid cells is independent of CD95/Fas receptor-ligand interaction and occurs downstream of caspase-3. Blood. 97:2001;1378-1387
39. Wislocki P.G., Wood A.W., Chang R.L., Levin W., Yagi H., Hernandez O., Dansette P.M., Herina D.M., Conney A.H. Mutagenicity and cytotoxicity of benzo(a)pyrene arene oxides, phenols, quinones, and dihydrodiols in bacterial and mammalian cells. Cancer Res. 36:1976;3350-3357
40. Xu Y., Bialik S., Jones B.E., Iimuro Y., Kitsis R.N., Srinivasan A., Brenner D.A., Czaja M.J. NF-kB inactivation converts a hepatocyte cell line TNF-a response from proliferation to apoptosis. Am. J. Physiol. Cell Physiol. 275:1998;C1058-C1066
41. Yu Y., Little J.B. p53 is involved in but not required for ionizing radiation-induced caspase-3 activation and apoptosis in human lymphoblast cell lines. Cancer Res. 5:1998;4277-4281