Induction of PUMA-α and down-regulation of PUMA-β expression is associated with benzo(a)pyrene-induced apoptosis in MCF-7 cells

Toxicology Letters

Volumn 188, Issue 3, 2009, Pages 214-222

  Tampio, Marjo ^a   Markkanen, Piia ^b   Puttonen, Katja A ^a   Hagelberg, Eveliina ^a   Heikkinen, Hannu ^a   Huhtinen, Kati ^a   Loikkanen, Jarkko ^a   Hirvonen, Maija Riitta ^a,b   Vähäkangas, Kirsi H ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

Cell viability; Cytochrome c; Flow cytometry; Polycyclic aromatic hydrocarbons; PUMA; ROS

Indexed keywords

APOPTOSOME; BENZO[A]PYRENE; CYTOCHROME C; DNA; PROTEIN P53; PUMA PROTEIN; PUMA PROTEIN ALPHA; PUMA PROTEIN BETA; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL FRACTIONATION; CELL STRAIN MCF 7; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; DNA CONTENT; DOWN REGULATION; EXPOSURE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOBLOTTING; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BENZO(A)PYRENE; CELL LINE, TUMOR; CYTOCHROMES C; CYTOSOL; DOWN-REGULATION; FLOW CYTOMETRY; HUMANS; IMMUNOBLOTTING; MEMBRANE POTENTIALS; MICROSCOPY, CONFOCAL; MITOCHONDRIA; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS; REACTIVE OXYGEN SPECIES; UP-REGULATION;

RODENTIA;

EID: 67349276700     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2009.04.016     Document Type: Article

References (52)

1. Achanta G., and Huang P. Role of p53 in sensing oxidative DNA damage in response to reactive oxygen species-generating agents. Cancer Res. 64 (2004) 6233-6239
2. Andrysík Z., Machala M., Chramostová K., Hofmanová J., Kozubík A., and Vondráček J. Activation of ERK1/2 and p38 kinases by polycyclic aromatic hydrocarbons in rat liver epithelial cells is associated with induction of apoptosis. Toxicol. Appl. Pharmacol. 211 (2006) 198-208
3. Antonsson B., Montessuit S., Sanchez B., and Martinou J.C. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J. Biol. Chem. 276 (2001) 11615-11623
4. Bjelogrlic N.M., Mäkinen M., Stenbäck F., and Vähäkangas K. Benzo(a)pyrene-7,8-diol-9,10-epoxide-DNA adducts and increased p53 protein in mouse skin. Carcinogenesis 15 (1994) 771-774
5. de Bruin E.C., and Medema J.P. Apoptosis and non-apoptotic deaths in cancer development and treatment response. Cancer Treat. Rev. 34 (2008) 737-749
6. Burdick A.D., Davis II J.W., Liu K.J., Hudson L.G., Shi H., Monske M.L., and Burchiel S.W. Benzo(a)pyrene quinones increase cell proliferation, generate reactive oxygen species, and transactivate the epidermal growth factor receptor in breast epithelial cells. Cancer Res. 63 (2003) 7825-7833
7. Burdick A.D., Ivnitski-Steele I.D., Lauer F.T., and Burchiel S.W. Pyk2 mediates anti-apoptotic Akt signaling in response to benzo[a]pyrene diol epoxide (BPDE) in mammary epithelial cells. Carcinogenesis 27 (2006) 2331-2340
8. Caino M.C., et al. BP-7,8-dihydrodiol promotes checkpoint activation and G2/M arrest in human bronchoalveolar carcinoma H358 cells. Mol. Pharmacol. 71 (2007) 744-750
9. Chandel N.S., Vander Heiden M.G., Thompson C.B., and Schumacker P.T. Redox regulation of p53 during hypoxia. Oncogene 10 (2000) 3840-3848
10. Chandra J., Samali A., and Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic. Biol. Med. 29 (2000) 323-333
11. Chipuk J.E., and Green D.R. How do Bcl-2 proteins induce mitochondrial outer membrane permeabilization?. Trends Cell Biol. 18 (2008) 157-164
12. Darzynkiewicz Z., Bruno S., Del Bino G., Gorczyca W., Hotz M.A., Lassota P., and Traganos F. Features of apoptotic cells measured by flow cytometry. Cytometry 13 (1992) 795-808
13. Flowers L., Tsuyoshi S., and Penning T.M. DNA strand scission by polycyclic aromatic hydrocarbon o-quinones: role of reactive oxygen species, Cu(II)/Cu(I) redox cycling, and o-semiquinone anion radicals. Biochemistry 36 (1997) 8640-8648
14. Gao A., Liu B., Shi X., Jia X., Ye M., Jiao S., You B., and Huang C. Phosphatidylinositol-3 kinase/Akt/p70S6K/AP-1 signaling pathway mediated benzo(a)pyrene-induced cell cycle alternation via cell cycle regulatory proteins in human embryo lung fibroblasts. Toxicol. Lett. 170 (2007) 30-41
15. Hainaut P., and Vähäkangas K. p53 as a sensor of carcinogenic exposures: Mechanisms of p53 protein induction and lessons from p53 gene mutations. Pathol. Biol. 45 (1997) 833-844
16. Hietakangas V., Poukkula M., Heiskanen K.M., Karvinen J.T., Sistonen L., and Eriksson J.E. Erythroid differentiation sensitizes K562 leukemia cells to TRAIL-induced apoptosis by downregulation of c-FLIP. Mol. Cell. Biol. 23 (2003) 1278-1291
17. Hockley S.L., Arlt V.M., Brewer D., te Poele R., Workman P., Giddings I., and Phillips D.H. AHR-and DNA-damage-mediated gene expression responses induced by benzo(a)pyrene in human cell lines. Chem. Res. Toxicol. 20 (2007) 1797-1810
18. Holme J., Gorria M., Arlt V.M., Øvrebø S., Solhaug A., Tekpli X., Landvik N.E., Huc L., Fardel O., and Lagalic-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
19. Hussain S.P., Amstad P., He P., Robles A., Lupold S., Kaneko I., Ichimiya M., Sengupta S., Mechanic L., Okamura S., Hofseth L.J., Moake M., Nagashima M., Forrester K.S., and Harris C.C. p53-induced up-regulation of MnSOD and GPx but not catalase increases oxidative stress and apoptosis. Cancer Res. 64 (2004) 2350-2356
20. Jänicke R.U., Sprengart M.L., Wati M.R., and Porter A.G. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273 (1998) 9357-9360
21. Jiang M., Wei Q., Wang J., Du Q., Yu J., Zhang L., and Dong Z. Regulation of PUMA-α by p53 in cisplatin-induced renal cell apoptosis. Oncogene 25 (2006) 4056-4066
22. Kim H., Rafiuddin-Shah M., Tu H.-C., Jeffers J.R., Zambetti G.B., Hsieh J.J., and Cheng E.H. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat. Cell Biol. 8 (2006) 1348-1358
23. 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., and Park R. Benzo(a)pyrene-induced apoptotic death of mouse hepatoma Hepa1c1c7 cells via activation of intrinsic caspase cascade and mitochondrial dysfunction. Toxicology 199 (2004) 35-46
24. Levine A.J., Hu W., and Feng Z. The p53 pathway: what questions remain to be explored?. Cell Death Differ. 13 (2006) 1027-1036
25. Loikkanen J., Chvalova K., Naarala J., Vähäkangas K.H., and Savolainen K.M. Pb2+ induced toxicity is associated with p53-independent apoptosis and enhanced by glutamate in GT1-7 neurons. Toxicol. Lett. 144 (2003) 235-246
26. Middelburg R., de Haas R.R., Dekker H., Kerkhoven R.M., Pohlmann P.R., Fuentes-Alburo A., Mohar A., Pinedo H.M., and Lankelma J. Induction of p53-upregulated modulator of apoptosis messenger RNA by chemotherapeutic treatment of locally advanced breast cancer. Clin. Cancer Res. 11 (2005) 1863-1869
27. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983) 55-63
28. Myllynen P., Kurttila T., Vaskivuo L., and Vähäkangas K. DNA damage caused by benzo(a)pyrene in MCF-7 cells is increased by verapamil, probenecid and PSC833. Toxicol. Lett. 28 (2007) 3-12
29. Nakano K., and Vousden K.H. Puma, a novel proapoptotic gene, is induced by p53. Mol. Cell 7 (2001) 683-694
30. Oda K., Arakawa H., Tanaka T., Matsuda K., Tanikawa C., Mori T., Nishimori H., Tamai K., Tokino T., Nakamura Y., and Taya Y. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46 phosphorylated p53. Cell 102 (2000) 849-862
31. Penttinen P., Pelkonen J., Huttunen K., and Hirvonen M.-R. Co-cultivation of Streptomyces californicus and Stachybotrys chartarum stimulates the production of cytostatic compound(s) with immunotoxic properties. Toxicol. Appl. Pharmacol. 217 (2006) 342-351
32. Penttinen P., Tampio M., Mäki-Paakkanen J., Vähäkangas K., Pelkonen J., and Hirvonen M.-R. DNA damage and p53 in RAW264.7 cells induced by the spores of co-cultivated Streptomyces californicus and Stachybotrys chartarum. Toxicology 235 (2007) 92-102
33. Plíšková M., Vondráček J., Vojtěšek B., Kozubík A., and Machala M. Deregulation of cell proliferation by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells reflects both genotoxic and nongenotoxic events. Toxicol. Sci. 83 (2005) 246-256
34. Rämet M., Castrén K., Järvinen K., Pekkala K., Turpeenniemi-Hujanen T., Soini Y., Pääkkö P., and Vähäkangas K. p53 protein expression is correlated with benzo(a)pyrene-DNA adducts in carcinoma cell lines. Carcinogenesis 16 (1995) 2117-2124
35. Sadikovic B., and Rodenhiser D.I. Benzopyrene exposure disrupts DNA methylation and growth dynamics in breast cancer cells. Toxicol. Appl. Pharmacol. 216 (2006) 458-468
36. +-treated SH-SY5Y human dopaminergic cells. J. Neurochem. 105 (2008) 2404-2417
37. Sengupta S., and Harris C.C. p53: traffic cop at the crossroads of DNA repair and recombination. Nat. Rev. Mol. Cell. Biol. 6 (2005) 44-55
38. Solé M., Hernandez-Guillamon M., Boada M., and Unzeta M. p53 phosphorylation is involved in vascular cell death induced by the catalytic activity of membrane-bound SSAO/VAP-1. Biochim. Biophys. Acta 1783 (2008) 1085-1094
39. Solhaug A., Refsnes M., and Holme J.A. Role of cell signalling involved in induction of apoptosis by benzo(a)pyrene and cyclopenta[c,d]pyrene in Hepa1c1c7 cells. J. Cell Biochem. 93 (2004) 1143-1154
40. Solhaug A., Ovrebo S., Mollerup S., Låg M., Schwarze P.E., Nesnow S., and Holme J.A. Role of cell signaling in B[a]P-induced apoptosis: characterization of unspecific effect of cell signaling inhibitors and apoptotic effects of B[a]P metabolites. Chem. Biol. Interact. 151 (2005) 101-119
41. Tampio M., Loikkanen J., Myllynen P., Mertanen A., and Vähäkangas K.H. Benzo(a)pyrene increases phosphorylation of p53 at serine 392 in relation to p53 induction and cell death in MCF-7 cells. Toxicol. Lett. 178 (2008) 152-159
42. Tapiainen T., Järvinen K., Pääkkö P., Bjelogrlic N., and Vähäkangas K. TPA decreases the p53 response to benzo(a)pyrene-DNA adducts in vivo in mouse skin. Carcinogenesis 17 (1996) pp. 1377-1370
43. Topinka J., Marvanová S., Vondráček J., Sevastyanova O., Nováková Z., Krčmář P., Pěnčíková K., and Machala M. DNA adducts formation and induction of apoptosis in rat liver epithelial "stem-like" cells exposed to carcinogenic polycyclic aromatic hydrocarbons. Mutat. Res. 638 (2008) 122-132
44. Vousden K.H. p53 and PUMA: a deadly duo. Science 309 (2005) 1685-1686
45. Wang A., Gu J., Judson-Kremer K., Powell K.L., Mistry H., Simhambhatla P., Aldaz C.M., Gaddis S., and MacLeod M.C. Response of human mammary epithelial cells to DNA damage induced by BPDE: involvement of novel regulatory pathways. Carcinogenesis 24 (2003) 225-234
46. Wang P., Yu J., and Zhang L. The nuclear function of p53 is required for PUMA-mediated apoptosis induced by DNA damage. Proc. Natl. Acad. Sci. 104 (2007) 4054-4059
47. Wolterbeek A.P., Roggeband R., Baan R.A., Feron V.J., and Rutten A.A. Relation between benzo(a)pyrene-DNA-adducts, cell proliferation and p53 expression in tracheal epithelium of hamsters fed a high beta-carotene diet. Carcinogenesis 7 (1995) 1617-1622
48. Xiao H., and Singh S.V. p53 regulates cellular responses to environmental carcinogen benzo(a)pyrene-7,8-diol-9,10-epoxide in human lung cancer cells. Cell Cycle 14 (2007) 1753-1761
49. Xue W., and Warshawsky D. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: A review. Toxicol. Appl. Pharmacol. 206 (2005) 73-93
50. Yee K.S., and Vousden K.H. Contribution of membrane localization to the apoptotic activity of PUMA. Apoptosis 13 (2008) 87-95
51. Yu J., Zhang L., Hwang P.M., Kinzler K.W., and Vogelstein B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell 7 (2001) 673-682
52. Yoshida K., Liu H., and Miki Y. Protein kinase C δ regulates Ser46 phosphorylation of p53 tumor suppressor in the apoptotic response to DNA damage. J. Biol. Chem. 281 (2006) 5734-5740