Benzo(a)pyrene-7,8-diol-9,10-epoxide induced p53-independent necrosis via the mitochondria-associated pathway involving Bax and Bak activation

Human and Experimental Toxicology

Volumn 34, Issue 2, 2015, Pages 179-190

  Zhang, W ^a   Liu, N ^b   Wang, X ^c   Jin, X ^a   Du, H ^a   Peng, G ^a   Xue, J ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b Hainan People's Hospital   (China)

^c XUZHOU CENTRAL HOSPITAL   (China)

Author keywords

Bak; Bax; BMK cells; BPDE; necrosis

Indexed keywords

BENZO (A) PYRENE 7,8 DIOL 9,10 EPOXIDE; BENZO[A]PYRENE DERIVATIVE; CASPASE; CYTOCHROME C; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; UNCLASSIFIED DRUG; BAK1 PROTEIN, MOUSE; BAX PROTEIN, MOUSE; BENZO[A]PYRENE 7,8 DIHYDRODIOL 9,10 OXIDE;

ANIMAL CELL; ARTICLE; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; FLOW CYTOMETRY; MITOCHONDRION; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; CELL LINE; CELL SURVIVAL; CHEMICALLY INDUCED; DRUG EFFECTS; GENETICS; METABOLISM; NECROSIS;

7,8-DIHYDRO-7,8-DIHYDROXYBENZO(A)PYRENE 9,10-OXIDE; ANIMALS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; CELL SURVIVAL; CYTOCHROMES C; MICE; MITOCHONDRIA; NECROSIS; PROTO-ONCOGENE PROTEINS C-BCL-2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84921976044     PISSN: 09603271     EISSN: 14770903     Source Type: Journal    
DOI: 10.1177/0960327114533358     Document Type: Article

References (46)

1. Stahl T, Heudorf U, Moriske HJ, et al. Polycyclic aromatic hydrocarbons (PAH) in an indoor environment. Sources, exposure and risk evaluation. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2004 ; 47 (9). 868-81
2. Darwish W, Ikenaka Y, Eldaly E, et al. Mutagenic activation and detoxification of benzo[a]pyrene in vitro by hepatic cytochrome P450 1A1 and phase II enzymes in three meat-producing animals. Food Chem Toxicol. 2011 ; 48 (8-9). 2526-2531
3. Montero R, Serrano L, Davila VM, et al. Infection of rats with Taenia taeniformis metacestodes increases hepatic CYP450, induces the activity of CYP1A1, CYP2B1 and COH isoforms and increases the genotoxicity of the procarcinogens benzo[a]pyrene, cyclophosphamide and aflatoxin B(1). Mutagenesis. 2003 ; 18 (2). 211-216
4. Said B, Ross MK, Salib T, et al. Modulation of DNA adduct formation by successive exposures of DNA to small and bulky chemical carcinogens. Carcinogenesis. 1995 ; 16 (12). 3057-3062
5. Pliskova M, Vondracek J, Vojtesek B, et al. Deregulation of cell proliferation by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells reflects both genotoxic and nongenotoxic events. Toxicol Sci. 2005 ; 83 (2). 246-256
6. Lin T, Yang MS. Benzo[a]pyrene-induced necrosis in the HepG(2) cells via PARP-1 activation and NAD(+) depletion. Toxicology. 2008 ; 245 (1-2). 147-153
7. Burke KE, Wei H. Synergistic damage by UVA radiation and pollutants. Toxicol Ind Health. 2009 ; 25 (4-5). 219-224
8. Jiang Y, Zhou X, Chen X, et al. Benzo(a)pyrene-induced mitochondrial dysfunction and cell death in p53-null Hep3B cells. Mutat Res. 2012 ; 726 (1). 75-83
9. Houghton JA. Apoptosis and drug response. Curr Opin Oncol. 1999 ; 11 (6). 475-481
10. Vaithinathan S, Saradha B, Mathur PP. Methoxychlor induces apoptosis via mitochondria- and FasL-mediated pathways in adult rat testis. Chem Biol Interact. 2012 ; 185 (2). 110-118
11. Yaoxian W, Hui Y, Yunyan Z, et al. Emodin induces apoptosis of human cervical cancer hela cells via intrinsic mitochondrial and extrinsic death receptor pathway. Canc Cell Int. 2013 ; 13 (1). 71
12. Darzynkiewicz Z, Zhao H, Halicka HD, et al. DNA damage signaling assessed in individual cells in relation to the cell cycle phase and induction of apoptosis. Crit Rev Clin Lab Sci. 2012 ; 49 (5-6). 199-217
13. Messner B, Frotschnig S, Steinacher-Nigisch A, et al. Apoptosis and necrosis: two different outcomes of cigarette smoke condensate-induced endothelial cell death. Cell Death Dis. 2012 ; 3: e424
14. Wochna A, Niemczyk E, Kurono C, et al. A possible role of oxidative stress in the switch mechanism of the cell death mode from apoptosis to necrosis - studies on rho0 cells. Mitochondrion. 2007 ; 7 (1-2). 119-124
15. Karch J, Kwong JQ, Burr AR, et al. Bax and Bak function as the outer membrane component of the mitochondrial permeability pore in regulating necrotic cell death in mice. Elife. 2012 ; 2: e00772
16. Gao L, Yu S, Wu Y, et al. Effect of spider venom on cell apoptosis and necrosis rates in MCF-7 cells. DNA Cell Biol. 2007 ; 26 (7). 485-489
17. Leung AM, Redlak MJ, Miller TA. Oxygen radical induced gastric mucosal cell death: apoptosis or necrosis'. Dig Dis Sci. 2008 ; 53 (9). 2429-2435
18. Callen E, Jankovic M, Wong N, et al. Essential role for DNA-PKcs in DNA double-strand break repair and apoptosis in ATM-deficient lymphocytes. Mol Cell. 2009 ; 34 (3). 285-297
19. Elias J, Dimitrio L, Clairambault J, et al. The p53 protein and its molecular network: modelling a missing link between DNA damage and cell fate. Biochim Biophys Acta. 2014 ; 1844: 232-247
20. Biton S, Gropp M, Itsykson P, et al. ATM-mediated response to DNA double strand breaks in human neurons derived from stem cells. DNA Repair (Amst). 2007 ; 6 (1). 128-134
21. Galluzzi L, Morselli E, Kepp O, et al. Targeting p53 to mitochondria for cancer therapy. Cell Cycle. 2008 ; 7 (13). 1949-1955
22. Ding WX, Ni HM, Chen X, et al. A coordinated action of Bax, PUMA, and p53 promotes MG132-induced mitochondria activation and apoptosis in colon cancer cells. Mol Canc Ther. 2007 ; 6 (3). 1062-1069
23. Sadikovic B, Rodenhiser DI. Benzopyrene exposure disrupts DNA methylation and growth dynamics in breast cancer cells. Toxicol Appl Pharmacol. 2006 ; 216 (3). 458-468
24. Jiang Y, Rao K, Yang G, et al. Benzo(a)pyrene induces p73 mRNA expression and necrosis in human lung adenocarcinoma H1299 cells. Environ Toxicol. 2011 ; 27 (4). 202-210
25. Ruley HE. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature. 1983 ; 304 (5927). 602-606
26. Guo BC, Xu YH. Bcl-2 over-expression and activation of protein kinase C suppress the TRAIL-induced apoptosis in Jurkat T cells. Cell Res. 2001 ; 11 (2). 101-106
27. Lin T, Mak NK, Yang MS. MAPK regulate p53-dependent cell death induced by benzo[a]pyrene: involvement of p53 phosphorylation and acetylation. Toxicology. 2008 ; 247 (2-3). 145-153
28. Meek DW, Anderson CW. Posttranslational modification of p53: cooperative integrators of function. Cold Spring Harb Perspect Biol. 2009 ; 1 (6). A000950
29. Efeyan A, Serrano M. P53: guardian of the genome and policeman of the oncogenes. Cell Cycle. 2007 ; 6 (9). 1006-1010
30. Yu Z, Wang H, Zhang L, et al. Both p53-PUMA/NOXA-Bax-mitochondrion and p53-p21cip1 pathways are involved in the CDglyTK-mediated tumor cell suppression. Biochem Biophys Res Commun. 2009 ; 386 (4). 607-611
31. Lee DH, Kim C, Zhang L, et al. Role of p53, PUMA, and Bax in wogonin-induced apoptosis in human cancer cells. Biochem Pharmacol. 2008 ; 75 (10). 2020-2033
32. Gallenne T, Gautier F, Oliver L, et al. Bax activation by the BH3-only protein Puma promotes cell dependence on antiapoptotic Bcl-2 family members. J Cell Biol. 2009 ; 185 (2). 279-290
33. Fletcher JI, Meusburger S, Hawkins CJ, et al. Apoptosis is triggered when prosurvival Bcl-2 proteins cannot restrain Bax. Proc Natl Acad Sci USA. 2008 ; 105 (47). 18081-18087
34. Bossowski A, et al. Analysis of intracellular proapoptotic (Bax, Bak) and antiapoptotic (Bcl-2, Bcl-XL) proteins expression in thyrocytes from young patients with immune and non-immune thyroid disorders. Pediatr Endocrinol Diabetes Metab. 2007 ; 13 (2). 63-70
35. Nicotera P, Melino G. Regulation of the apoptosis-necrosis switch. Oncogene. 2004 ; 23 (16). 2757-2765
36. Ramadan S, Terrinoni A, Catani MV, et al. P73 induces apoptosis by different mechanisms. Biochem Biophys Res Commun. 2005 ; 331 (3). 713-717
37. Bae IH, Kang SW, Yoon SH, et al. Cellular components involved in the cell death induced by cisplatin in the absence of p53 activation. Oncol Rep. 2006 ; 15 (5). 1175-1180
38. Lasfer M, et al. Protein kinase PKC delta and c-Abl are required for mitochondrial apoptosis induction by genotoxic stress in the absence of p53, p73 and Fas receptor. FEBS Lett. 2006 ; 580 (11). 2547-2552
39. Park MS, De Leon M, Devarajan P. Cisplatin induces apoptosis in LLC-PK1 cells via activation of mitochondrial pathways. J Am Soc Nephrol. 2002 ; 13 (4). 858-865
40. Mikhailov V, Mikhailov M, Degenhardt K, et al. Association of Bax and Bak homo-oligomers in mitochondria. Bax requirement for Bak reorganization and cytochrome c release. J Biol Chem. 2003 ; 278 (7). 5367-5376
41. Upreti M, Chu R, Galitovskaya E, et al. Key role for Bak activation and Bak-Bax interaction in the apoptotic response to vinblastine. Mol Cancer Ther. 2008 ; 7 (7). 2224-2232
42. Sundararajan R, Cuconati A, Nelson D, et al. Tumor necrosis factor-alpha induces Bax-Bak interaction and apoptosis, which is inhibited by adenovirus E1B 19K. J Biol Chem. 2001 ; 276 (48). 45120-45127
43. Martinou JC, Desagher S, Antonsson B. Cytochrome c release from mitochondria: all or nothing. Nat Cell Biol. 2000 ; 2 (3). E41 - E43
44. Wilson CA, Browning JL. Death of HT29 adenocarcinoma cells induced by TNF family receptor activation is caspase-independent and displays features of both apoptosis and necrosis. Cell Death Differ. 2002 ; 9 (12). 1321-1333
45. Iwasaki R, Ito K, Ishida T, et al. Catechin, green tea component, causes caspase-independent necrosis-like cell death in chronic myelogenous leukemia. Canc Sci. 2009 ; 100 (2). 349-356
46. Artus C, Boujrad H, Bouharrour A, et al. AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX. Embo J. 2012 ; 29 (9). 1585-1599