P53 activation by Ni(II) is a HIF-1α independent response causing caspases 9/3-mediated apoptosis in human lung cells

Toxicology and Applied Pharmacology

Volumn 269, Issue 3, 2013, Pages 233-239

  Wong, Victor C ^a   Morse, Jessica L ^a   Zhitkovich, Anatoly ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Apoptosis; Cancer; HIF 1; Hypoxia; Nickel; P53

Indexed keywords

CASPASE 3; CASPASE 9; CYCLIN DEPENDENT KINASE INHIBITOR 1A; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NICKEL; NICKEL CHLORIDE; PROTEIN MDM2; PROTEIN MDMX; PROTEIN NOXA; PROTEIN P21; PROTEIN P53; PUMA PROTEIN; SERINE;

APOPTOSIS; ARTICLE; CELL DEATH; CLONOGENESIS; CONTROLLED STUDY; DNA DAMAGE; GENOTOXICITY; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROBLAST; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UPREGULATION;

APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CASPASE 9; CELL LINE; DNA DAMAGE; GENE KNOCKDOWN TECHNIQUES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUNG; NICKEL; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84876962431     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.03.023     Document Type: Article

References (51)

1. An W.G., Kanekal M., Simon M.C., Maltepe E., Blagosklonny M.V., Neckers L.M. Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature 1998, 392:405-408.
2. Beckerman R., Donner A.J., Mattia M., Peart M.J., Manley J.L., Espinosa J.M., Prives C. A role for Chk1 in blocking transcriptional elongation of p21 RNA during the S-phase checkpoint. Genes Dev. 2009, 23:1364-1377.
3. Biedermann K.A., Landolph J.R. Induction of anchorage independence in human diploid foreskin fibroblasts by carcinogenic metal salts. Cancer Res. 1987, 47:3815-3823.
4. Chen D., Li M., Luo J., Gu W. Direct interactions between HIF-1 alpha and Mdm2 modulate p53 function. J. Biol. Chem. 2003, 278:13595-13598.
5. Costa M., Mollenhauer H.H. Carcinogenic activity of particulate nickel compounds is proportional to their cellular uptake. Science 1980, 209:515-517.
6. Costa M., Davidson T.L., Chen H., Ke Q., Zhang P., Yan Y., Huang C., Kluz T. Nickel carcinogenesis: epigenetics and hypoxia signaling. Mutat. Res. 2005, 592:79-88.
7. Davidson T.L., Chen H., Di Toro D.M., D'Angelo G., Costa M. Soluble nickel inhibits HIF-prolyl-hydroxylases creating persistent hypoxic signaling in A549 cells. Mol. Carcinog. 2006, 45:479-489.
8. Ding J., Zhang X., Li J., Song L., Ouyang W., Zhang D., Xue C., Costa M., Meléndez J.A., Huang C. Nickel compounds render anti-apoptotic effect to human bronchial epithelial Beas-2B cells by induction of cyclooxygenase-2 through an IKKbeta/p65-dependent and IKKalpha- and p50-independent pathway. J. Biol. Chem. 2006, 281:39022-39032.
9. Ding J., He G., Gong W., Wen W., Sun W., Ning B., Huang S., Wu K., Huang C., Wu M., Xie W., Wang H. Effects of nickel on cyclin expression, cell cycle progression and cell proliferation in human pulmonary cells. Cancer Epidemiol. Biomarkers Prev. 2009, 18:1720-1729.
10. Gao F., Brant K.A., Ward R.M., Cattley R.T., Barchowsky A., Fabisiak J.P. Multiple protein kinase pathways mediate amplified IL-6 release by human lung fibroblasts co-exposed to nickel and TLR-2 agonist, MALP-2. Toxicol. Appl. Pharmacol. 2010, 247:146-157.
11. Garrison S.P., Phillips D.C., Jeffers J.R., Chipuk J.E., Parsons M.J., Rehg J.E., Opferman J.T., Green D.R., Zambetti G.P. Genetically defining the mechanism of Puma- and Bim-induced apoptosis. Cell Death Differ. 2012, 19:642-649.
12. Goodman J.E., Prueitt R.L., Thakali S., Oller A.R. The nickel ion bioavailability model of the carcinogenic potential of nickel-containing substances in the lung. Crit. Rev. Toxicol. 2011, 41:142-174.
13. Gottifredi V., Shieh S., Taya Y., Prives C. p53 accumulates but is functionally impaired when DNA synthesis is blocked. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:1036-1041.
14. Gray D.C., Mahrus S., Wells J.A. Activation of specific apoptotic caspases with an engineered small-molecule-activated protease. Cell 2012, 142:637-646.
15. Green D.R., Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009, 458:1127-1130.
16. Hong J.W., Ryu M.S., Lim I.K. Phosphorylation of serine 147 of tis21/BTG2/pc3 by p-Erk1/2 induces Pin-1 binding in cytoplasm and cell death. J. Biol. Chem. 2005, 280:21256-21263.
17. Huang X., Kitahara J., Zhitkovich A., Dowjat K., Costa M. Heterochromatic proteins specifically enhance nickel-induced 8-oxo-dG formation. Carcinogenesis 1995, 16:1753-1759.
18. Huang C., Li J., Costa M., Zhang Z., Leonard S.S., Castranova V., Vallyathan V., Ju G., Shi X. Hydrogen peroxide mediates activation of nuclear factor of activated T cells (NFAT) by nickel subsulfide. Cancer Res. 2006, 61:8051-8057.
19. Jeffers J.R., Parganas E., Lee Y., Yang C., Wang J., Brennan J., MacLean K.H., Han J., Chittenden T., Ihle J.N., McKinnon P.J., Cleveland J.L., Zambetti G.P. Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 2003, 4:321-328.
20. Ke Q., Davidson T., Kluz T., Oller A., Costa M. Fluorescent tracking of nickel ions in human cultured cells. Toxicol. Appl. Pharmacol. 2007, 219:18-23.
21. Kim H., Tu H.C., Ren D., Takeuchi O., Jeffers J.R., Zambetti G.P., Hsieh J.J., Cheng E.H. Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol. Cell 2009, 36:487-499.
22. Komarov P.G., Komarova E.A., Kondratov R.V., Christov-Tselkov K., Coon J.S., Chernov M.V., Gudkov A.V. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 1999, 285:1733-1737.
23. Kruse J.P., Gu W. Modes of p53 regulation. Cell 2009, 137:609-622.
24. Lee Y.W., Klein C.B., Kargacin B., Salnikow K., Kitahara J., Dowjat K., Zhitkovich A., Christie N.T., Costa M. Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: a new model for epigenetic carcinogens. Mol. Cell. Biol. 1995, 15:2547-2557.
25. 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 1997, 91:479-489.
26. Liu X., Gurel V., Morris D., Murray D., Zhitkovich A., Kane A.B., Hurt R.H. Bioavailability of nickel in single-wall carbon nanotubes. Adv. Mater. 2007, 19:2790-2796.
27. Maehle L., Metcalf R.A., Ryberg D., Bennett W.P., Harris C.C., Haugen A. Altered p53 gene structure and expression in human epithelial cells after exposure to nickel. Cancer Res. 1992, 52:218-221.
28. Mihara M., Erster S., Zaika A., Petrenko O., Chittenden T., Pancoska P., Moll U.M. p53 has a direct apoptogenic role at the mitochondria. Mol. Cell 2003, 11:577-590.
29. Miura T., Patierno S.R., Sakuramoto T., Landolph J.R. Morphological and neoplastic transformation of C3H/10T1/2 Cl 8 mouse embryo cells by insoluble carcinogenic nickel compounds. Environ. Mol. Mutagen. 1989, 14:65-78.
30. Muñoz A., Costa M. Elucidating the mechanisms of nickel compound uptake: a review of particulate and nano-nickel endocytosis and toxicity. Toxicol. Appl. Pharmacol. 2012, 260:1-16.
31. Oda E., Ohki R., Murasawa H., Nemoto J., Shibue T., Yamashita T., Tokino T., Taniguchi T., Tanaka N. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 2000, 288:1053-1058.
32. Patel E., Lynch C., Ruff V., Reynolds M. Co-exposure to nickel and cobalt chloride enhances cytotoxicity and oxidative stress in human lung epithelial cells. Toxicol. Appl. Pharmacol. 2012, 258:367-375.
33. Pfeifer G.P., Besaratinia A. Mutational spectra of human cancer. Hum. Genet. 2009, 125:493-506.
34. Pietruska J.R., Liu X., Smith A., McNeil K., Weston P., Zhitkovich A., Hurt R., Kane A.B. Bioavailability, intracellular mobilization of nickel, and HIF-1α activation in human lung epithelial cells exposed to metallic nickel and nickel oxide nanoparticles. Toxicol. Sci. 2011, 124:138-148.
35. Qu W., Kasprzak K.S., Kadiiska M., Liu J., Chen H., Maciag A., Mason R.P., Waalkes M.P. Mechanisms of arsenic-induced cross-tolerance to nickel cytotoxicity, genotoxicity, and apoptosis in rat liver epithelial cells. Toxicol. Sci. 2001, 63:189-195.
36. Ren D., Tu H.C., Kim H., Wang G.X., Bean G.R., Takeuchi O., Jeffers J.R., Zambetti G.P., Hsieh J.J., Cheng E.H. BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science 2010, 330:1390-3139.
37. Reynolds M., Zhitkovich A. Cellular vitamin C increases chromate toxicity via a death program requiring mismatch repair but not p53. Carcinogenesis 2007, 28:1613-1620.
38. Reynolds M., Peterson E., Quievryn G., Zhitkovich A. Human nucleotide excision repair efficiently removes DNA phosphate-chromium adducts and protects cells against chromate toxicity. J. Biol. Chem. 2004, 279:30419-30424.
39. Salnikow K., Zhitkovich A. Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: nickel, arsenic and chromium. Chem. Res. Toxicol. 2008, 21:28-44.
40. Salnikow K., Wang S., Costa M. Induction of activating transcription factor 1 by nickel and its role as a negative regulator of thrombospondin I gene expression. Cancer Res. 1997, 57:5060-5066.
41. Salnikow K., An W.G., Melillo G., Blagosklonny M.V., Costa M. Nickel-induced transformation shifts the balance between HIF-1 and p53 transcription factors. Carcinogenesis 1999, 20:1819-1823.
42. Salnikow K., Blagosklonny M.V., Ryan H., Johnson R., Costa M. Carcinogenic nickel induces genes involved with hypoxic stress. Cancer Res. 2000, 60:38-41.
43. Salnikow K., Davidson T., Zhang Q., Chen L.C., Su W., Costa M. The involvement of hypoxia-inducible transcription factor-1-dependent pathway in nickel carcinogenesis. Cancer Res. 2003, 63:3524-3530.
44. Salnikow K., Donald S.P., Bruick R.K., Zhitkovich A., Phang J.M., Kasprzak K.S. Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J. Biol. Chem. 2004, 279:40337-40344.
45. Toledo F., Wahl G.M. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat. Rev. Cancer 2006, 6:909-923.
46. Vaseva A.V., Marchenko N.D., Ji K., Tsirka S.E., Holzmann S., Moll U.M. p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 2012, 149:1536-1548.
47. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730.
48. Wong V.C., Cash H.L., Morse J.L., Lu S., Zhitkovich A. S-phase sensing of DNA-protein crosslinks triggers TopBp1-independent ATR activation and p53-mediated cell death by formaldehyde. Cell Cycle 2012, 11:2526-2537.
49. Wu H.C., Yang C.Y., Hung D.Z., Su C.C., Chen K.L., Yen C.C., Ho T.J., Su Y.C., Huang C.F., Chen C.H., Tsai L.M., Chen Y.W. Nickel(II) induced JNK activation-regulated mitochondria-dependent apoptotic pathway leading to cultured rat pancreatic β-cell death. Toxicology 2011, 289:103-111.
50. Zhang D., Zaugg K., Mak T.W., Elledge S.J. A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell 2006, 126:529-542.
51. Zou H., Li Y., Liu X., Wang X. An APAF-1·cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 1999, 274:11549-11556.