Benzo[a]pyrene-7,8-diol-9,10-epoxide causes caspase-mediated apoptosis in H460 human lung cancer cell line

Cell Cycle

Volumn 6, Issue 22, 2007, Pages 2826-2834

  Xiao, Hui ^a   Rawal, Malika ^a   Hahm, Eun Ryeong ^a   Singh, Shivendra V ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Apoptosis; Benzo a pyrene; BPDE; Lung cancer

Indexed keywords

7,8 DIHYDROXYBENZO[A]PYRENE 9,10 OXIDE; BENZYLOXYCARBONYLISOLEUCYLGLUTAMYLTHREONYLASPARTYL FLUOROMETHYL KETONE; BENZYLOXYCARBONYLLEUCYLGLUTAMYLHISTIDYLASPARTYL FLUOROMETHYL KETONE; CASPASE 8; CASPASE 8 INHIBITOR; CASPASE 9; CASPASE 9 INHIBITOR; DNA FRAGMENT; HISTONE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRONCHUS MUCOSA; CANCER CELL CULTURE; CELL IMMORTALIZATION; CELL STRUCTURE; CHROMATIN CONDENSATION; CONCENTRATION (PARAMETERS); CYTOSOL; DOWN REGULATION; ELECTRON MICROSCOPY; EMBRYO; ENZYME DEGRADATION; EPITHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; LUNG CANCER; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PROTEIN FAMILY; PROTEIN FUNCTION; UPREGULATION;

MUS;

EID: 37249063031     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.6.22.4891     Document Type: Article

References (44)

1. International Agency for Research on Cancer. IARC Monographs on the evaluation of the Carcinogenic risk of Chemicals to Humans. Polynuclear Aromatic Compounds, Part 1. Chemical, Environmental, and Experimental Data, Vol. 32. International Agency for Research on Cancer. Lyon, France. 1983
2. Buening MK, Wislocki PG, Levin W, Yagi H, Thakker DR, Akagi H, Koreeda M, Jerina DM, Conney AH. Tumorigenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides in newborn mice: exceptional activity of (+)-7beta,8alpha-dihydroxy-9alpha,10alpha-epoxy-7,8,9, 10-tetrahydrobenzo[a]pyrene. Proc Natl Acad Sci USA. 1978;75:5358-61.
3. Slaga TJ, Bracken WJ, Gleason G, Levin W, Yagi H, Jerina DM, Conney AH. Marked differences in the skin tumor-initiating activities of the optical enantiomers of the diastereomeric benzo(a)pyrene 7,8-diol-9,10- epoxides. Cancer Res 1979;39:67-71.
4. Hu X, Benson PJ, Srivastava SK, Xia H, Bleicher RJ, Zaren HA, Awasthi S, Awasthi YC, Singh SV. Induction of glutathione S-transferase ? as a bioassay for the evaluation of potency of inhibitors of benzo(a)pyrene-induced cancer in a murine model. Int J Cancer 1997;73:897-902.
5. Gelboin HV. Benzo(a)pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes. Physiol Rev 1980;60:1107-66.
6. Thakker DR, Yagi H, Levin W, Wood AW, Conney AH, Jerina DM. Polycyclic aromatic hydrocarbons: metabolic activation to ultimate carcinogens. In: Anders MW, ed. Bioactivation of Foreign Compounds. New York, NY: Academic Press, 1985:177-242.
7. Dipple A. Polycyclic hydrocarbons and carcinogenesis: an introduction. In: Harvey RG, ed. ACS Symposium Series 283. Washington, DC: American Chemical Society, 1985:1-17.
8. Yang SK, Gelboin HV. Nonenzymatic reduction of benzo(a) pyrene diol epoxides to trihyd roxypentahydrobenzo(a)pyrenes by reduced nicotinamide adenine dinucleotide phosphate. Cancer Res 1976;36:4185-9.
9. Dock L, Waern F, Martinez M, Grover PL, Jernstrom B. Studies on the further activation of benzo[a]pyrene diol epoxides by rat liver microsomes and nuclei. Chem Biol Interact 1986;58:301-18.
10. Thakker DR, Yagi H, Levin W, Lu AYH, Conney AH, Jerina DM. Stereospecificity of microsomal and purified epoxide hydrase from rat liver: hydration of arene oxides of polycyclic hydrocarbons. J Biol Chem 1977;252:6328-34.
11. Robertson IGC, Guthenberg C, Mannervik B, Jernstrom B. Differences in stereoselectivity and catalytic efficiency of three human glutathione transferases in the conjugation of glutathione with 7β,8α-dihydroxy- 9α,10α-oxy-7,8,9,10-tetrahydrobenzo(a)pyrene. Cancer Res 1986;46:2220-4.
12. Hu X, Srivastava SK, Xia H, Awasthi YC, Singh SV. An alpha class mouse glutathione S-transferase with exceptional catalytic efficiency in the conjugation of glutathione with 7ß,8α-dihydroxy-9α,10α- oxy-7,8,9,10-tetrahydrobenzo(a)pyrene. J Biol Chem 1996;271:32684-8.
13. Fields WR, Morrow CS, Doss AJ, Sundberg K, Jernstrom B, Townsend AJ. Overexpression of stably transfected human glutathione-S-transferase P1-1 protects against DNA damage by benzo[a]pyrene diol-epoxide in human T47D cells. Mol Pharmacol 1998;54:298-304.
14. Hu X, Herzog C, Zimniak P, Singh SV. Differential protection against benzo[a]pyrene-7,8-dihydrodiol-9,10-epoxide-induced DNA damage in HepG2 cells stably transfected with allelic variants of ? class human glutathione S-transferase. Cancer Res 1999;59:2358-62.
15. Guo J, Pan SS, Singh SV. Exceptional activity of murine glutathione transferase A1-1 against (7R,8S)-dihydroxy-(9S,10R)-epoxy-7,8,9,10- tetrahydrobenzo[a]pyrene-induced DNA damage in stably transfected cells. Mol Carcinogenesis 2003;36:67-73.
16. Guo N, Faller DV, Vaziri C. Carcinogen-induced S-phase arrest is Chk1 mediated and caffeine sensitive. Cell Growth Diff 2002;13:77-86.
17. Xiao H, Singh SV. p53 regulates cellular responses to environmental carcinogen benzo[a]pyrene-7,8-diol-9,10-epoxide in human lung cancer cells. Cell Cycle 2007;6:1753-61.
18. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. Proapoptotic Bax and Bak: a requisite gateway to mitochondrial dysfunction and death. Science 2001;292:727-30.
19. Xiao D, Choi S, Johnson DE, Vogel VG, Johnson CS, Trump DL, Lee YJ, Singh SV. Diallyl trisulfide-induced apoptosis in human prostate cancer cells involves c-Jun N-terminal kinase and extracellular-signal regulated kinase-mediated phosphorylation of Bcl-2. Oncogene 2004;23:5594-606.
20. Kim YA, Xiao D, Xiao H, Powolny AA, Lew KL, Reilly ML, Zeng Y, Wang Z, Singh SV. Mitochondria-mediated apoptosis by diallyl trisulfide in human prostate cancer cells is associated with generation of reactive oxygen species and regulated by Bax/Bak. Mol. Cancer Ther 2007;6:1599-609.
21. Singh SV, Srivastava SK, Choi S, Lew KL, Antosiewicz J, Xiao D, Zeng Y, Watkins SC, Johnson CS, Trump DL, Lee YJ, Xiao H, Herman-Antosiewicz A. Sulforaphane-induced cell death in human prostate cancer cells is initiated by reactive oxygen species. J Biol Chem 2005;280:19911-24.
22. Xiao D, Lew KL, Zeng Y, Xiao H, Marynowski SW, Dhir R, Singh SV. Phenethyl isothiocyanate-induced apoptosis in PC-3 human prostate cancer cells is mediated by reactive oxygen species-dependent disruption of the mitochondrial membrane potential. Carcinogenesis 2006;27:2223-34.
23. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science 1995;267:1456-62.
24. Ferri KF, Kroemer G. Organelle-specific initiation of cell death pathways. Nature Cell Biol 2001;3:E255-E63.
25. Hockenbery D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 1990;348:334-6.
26. Reed JC. Bcl-2 family proteins: regulators of apoptosis and chemoresistance in hematologic malignancies. Semin Hematol 1997;34:9-19.
27. Chao DT, Korsmeyer SJ. Bcl-2 family: regulators of cell death. Annu Rev Immunol 1998;16:395-419.
28. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998;281:1322-6.
29. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007;87:99-163.
30. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998;281:1305-8.
31. Liu X, Kim C, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996;86:147-57.
32. Thornberry N, Lazebnick Y. Caspases: enemies within. Science 1998;281:1312-6.
33. Wolf BB, Green DR. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 1999;274:20049-52.
34. Marshall CJ, Vousden KH, Phillips DH. Activation of c-Ha-ras-1 proto-oncogene by in vitro modification with a chemical carcinogen, benzo[a]pyrene diol-epoxide. Nature 1984;310:586-9.
35. Song S, Lippman SM, Zou Y, Ye X, Ajani JA, Xu X. Induction of cyclooxygenase-2 by benzo[a]pyrene diol epoxide through inhibition of retinoic acid receptor-β2 expression. Oncogene 2005;24:8268-76.
36. Venkatachalam S, Denissenko MF, Alvi N, Wani AA. Rapid activation of apoptosis in human promyelocytic leukemic cells by (±)-anti-benzo[a] pyrene diol epoxide induced DNA damage. Biochem Biophys Res Commun 1993;197:722-9.
37. Jyonouchi H, Sun S, Iijima K, Wang M, Hecht SS. Effects of anti-7,8-dihydroxy-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene on human small airway epithelial cells and the protective effects of myo-inositol. Carcinogenesis. 1999;20:139-45.
38. Kim SJ, Ko CB, Park C, Kim BR, Sung TH, Koh DH, Kim NS, Oh KJ, Chung SY, Park R. p38 MAP kinase regulates benzo(a)pyrene-induced apoptosis through the regulation of p53 activation. Arch Biochem Biophys 2005;444:121-9.
39. Huc L, Rissel M, Solhaug A, Tekpli X, Gorria M, Torriglia A, Holme JA, Dimanche-Boitrel MT, Lagadic-Gossmann D. Multiple apoptotic pathways induced by p53-dependent acidification in benzo[a]pyrene-exposed hepatic F258 cells. J Cell Physiol 2006;208:527-37.
40. + exchanger isoform 1 activation controls hexokinase II expression in benzo(a)pyrene-induced apoptosis. Cancer Res 2007;67:1696-705.
41. Burdick AD, Ivnitski-Steele ID, Lauer FT, Burchiel SW. PYK2 mediates anti-apoptotic AKT signaling in response to benzo[a]pyrene diol epoxide in mammary epithelial cells. Carcinogenesis 2006;27:2331-40.
42. Solhaug A, Ovrebo S, Mollerup S, Lag M, Schwarze PE, Nesnow S, Holme JA. Role of cell signaling in B[a]P-induced apoptosis: characterization of unspecific effects of cell signaling inhibitors and apoptotic effects of B[a]P metabolites. Chem Biol Interact 2005;151:101-19.
43. Chen S, Nguyen N, Tamura K, Karin M, Tukey RH. 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 2003;278:19526-33.
44. Blagosklonny MV. Carcinogenesis, cancer therapy and chemoprevention. Cell Death Differ 2005;12:592-602.