Chromium-mediated apoptosis: Involvement of DNA-dependent protein kinase (DNA-PK) and differential induction of p53 target genes

DNA Repair

Volumn 7, Issue 9, 2008, Pages 1484-1499

  Hill, Richard ^a   Leidal, Andrew M ^a   Madureira, Patricia A ^b   Gillis, Laura D ^a   Waisman, David M ^b   Chiu, Arthur ^c   Lee, Patrick W K ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

ATM; ATR; DNA damage; DNA PK; p21; p53; PUMA

Indexed keywords

CHROMIUM; DNA DEPENDENT PROTEIN KINASE; P21 ACTIVATED KINASE 1; PROTEIN P53; RNA POLYMERASE II;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; DNA DAMAGE; ENZYME ACTIVATION; ENZYME INHIBITION; GAMMA IRRADIATION; GENE INDUCTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MESSENGER RNA SYNTHESIS; PRIORITY JOURNAL; PROTEIN STABILITY; RNA TRANSLATION;

APOPTOSIS; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CHROMIUM; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; GAMMA RAYS; GENES, P53; HUMANS; MODELS, BIOLOGICAL; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 48149095219     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.05.007     Document Type: Article

References (66)

1. Hollstein M., Sidransky D., Vogelstein B., and Harris C.C. p53 mutations in human cancers. Science 253 (1991) 49-53
2. Vogelstein B., Lane D., and Levine A.J. Surfing the p53 network. Nature 408 (2000) 307-310
3. Vogelstein B., and Kinzler K.W. p53 function and dysfunction. Cell 70 (1992) 523-526
4. Waldman T., Kinzler K.W., and Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res. 55 (1995) 5187-5190
5. Polyak K., Xia Y., Zweier J.L., Kinzler K.W., and Vogelstein B. A model for p53-induced apoptosis. Nature 389 (1997) 300-305
6. Bunz F., Dutriaux A., Lengauer C., Waldman T., Zhou S., Brown J.P., Sedivy J.M., Kinzler K.W., and Vogelstein B. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282 (1998) 1497-1501
7. Gartel A.L., Serfas M.S., and Tyner A.L. p21-negative regulator of the cell cycle. Proc. Soc. Exp. Biol. Med. 213 (1996) 138-149
8. Zhang L., Yu J., Park B.H., Kinzler K.W., and Vogelstein B. Role of BAX in the apoptotic response to anticancer agents. Science 290 (2000) 989-992
9. Chan T.A., Hwang P.M., Hermeking H., Kinzler K.W., and Vogelstein B. Cooperative effects of genes controlling the G (2)/M checkpoint. Genes Dev. 14 (2000) 1584-1588
10. Schuler M., and Green D.R. Mechanisms of p53-dependent apoptosis. Biochem. Soc. Trans. 29 (2001) 684-688
11. Chipuk J.E., Bouchier-Hayes L., Kuwana T., Newmeyer D.D., and Green D.R. PUMA couples the nuclear and cytoplasmic proapoptotic function of p53. Science 309 (2005) 1732-1735
12. Yu J., Wang Z., Kinzler K.W., Vogelstein B., and Zhang L. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 1931-1936
13. Zilfou J.T., Spector M.S., and Lowe S.W. Slugging it out: fine tuning the p53-PUMA death connection. Cell 123 (2005) 545-548
14. Tanaka T., Ohkubo S., Tatsuno I., and Prives C. hCAS/CSE1L associates with chromatin and regulates expression of select p53 target genes. Cell 130 (2007) 638-650
15. Mattia M., Gottifredi V., McKinney K., and Prives C. p53-dependent p21 mRNA elongation is impaired when DNA replication is stalled. Mol. Cell. Biol. (2006) 1309-1320
16. Espinosa J.M., and Emerson B.M. Transcriptional regulation by p53 through intrinsic DNA/chromatin binding and site-directed cofactor recruitment. Mol. Cell 8 (2001) 57-69
17. Espinosa J.M., Verdun R.E., and Emerson B.M. p53 functions through stress- and promoter-specific recruitment of transcription initiation components before and after DNA damage. Mol. Cell 12 (2003) 1015-1027
18. Achanta G., Pelicano H., Feng L., Plunkett W., and Huang P. Interaction of p53 and DNA-PK in response to nucleoside analogues: potential role as a sensor complex for DNA damage. Cancer Res. 61 (2001) 8723-8729
19. Rinaldo C., Prodosmo A., Mancini F., Iacovelli S., Sacchi A., Moretti F., and Soddu S. MDM2-regulated degradation of HIPK2 prevents p53Ser46 phosphorylation and DNA damage-induced apoptosis. Mol. Cell 25 (2007) 739-750
20. Woo R.A., McLure K.G., Lees-Miller S.P., Rancourt D.E., and Lee P.W. DNA-dependent protein kinase acts upstream of p53 in response to DNA damage. Nature 394 (1998) 700-704
21. Bartek J., and Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3 (2003) 421-429
22. Taylor W.R., and Stark G.R. Regulation of the G2/M transition by p53. Oncogene 20 (2001) 1803-1815
23. Vaziri C., Saxena S., Jeon Y., Lee C., Murata K., Machida Y., Wagle N., Hwang D.S., and Dutta A. A p53-dependent checkpoint pathway prevents rereplication. Mol. Cell 11 (2003) 997-1008
24. Lees-Miller S.P., Chen Y.R., and Anderson C.W. Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol. Cell. Biol. 10 (1990) 6472-6481
25. Hermeking H., and Eick D. Mediation of c-Myc-induced apoptosis by p53. Science 265 (1994) 2091-2093
26. Wu X., and Levine A.J. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 3602-3606
27. Lowe S.W., and Ruley H.E. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev. 7 (1993) 535-545
28. Debbas M., and White E. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7 (1993) 546-554
29. Jack M.T., Woo R.A., Hirao A., Cheung A., Mak T.W., and Lee P.W. Chk2 is dispensable for p53-mediated G1 arrest but is required for a latent p53-mediated apoptotic response. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 9825-9829
30. Jack M.T., Woo R.A., Motoyama N., Takai H., and Lee P.W. DNA-dependent protein kinase and checkpoint kinase 2 synergistically activate a latent population of p53 upon DNA damage. J. Biol. Chem. 279 (2004) 15269-15273
31. Woo R.A., Jack M.T., Xu Y., Burma S., Chen D.J., and Lee P.W. DNA damage-induced apoptosis requires the DNA-dependent protein kinase, and is mediated by the latent population of p53. EMBO J. 21 (2002) 3000-3008
32. Bharti A., Kraeft S.K., Gounder M., Pandey P., Jin S., Yuan Z.M., Lees-Miller S.P., Weichselbaum R., Weaver D., Chen L.B., Kufe D., and Kharbanda S. Inactivation of DNA-dependent protein kinase by protein kinase Cdelta: implications for apoptosis. Mol. Cell. Biol. 18 (1998) 6719-6728
33. Jimenez G.S., Bryntesson F., Torres-Arzayus M.I., Priestley A., Beeche M., Saito S., Sakaguchi K., Appella E., Jeggo P.A., Taccioli G.E., Wahl G.M., and Hubank M. DNA-dependent protein kinase is not required for the p53-dependent response to DNA damage. Nature 400 (1999) 81-83
34. Occupational exposure to hexavalent chromium. Final rule, Fed. Regist. 71 (2006) 10099-10385.
35. O'Brien T.J., Ceryak S., and Patierno S.R. Complexities of chromium carcinogenesis: role of cellular response, repair and recovery mechanisms. Mutat. Res. 533 (2003) 3-36
36. Salnikow K., Zhitkovich A., and Costa M. Analysis of the binding sites of chromium to DNA and protein in vitro and in intact cells. Carcinogenesis 13 (1992) 2341-2346
37. Bose R.N., Fonkeng B.S., Moghaddas S., and Stroup D. Mechanisms of DNA damage by chromium (V) carcinogens. Nucleic Acids Res. 26 (1998) 1588-1596
38. Strauss J.K., and Maher III L.J. DNA bending by asymmetric phosphate neutralization. Science 266 (1994) 1829-1834
39. O'Brien T.J., Fornsaglio J.L., Ceryak S., and Patierno S.R. Effects of hexavalent chromium on the survival and cell cycle distribution of DNA repair-deficient S. cerevisiae. DNA Repair (Amst) 1 (2002) 617-627
40. Manning F.C., Xu J., and Patierno S.R. Transcriptional inhibition by carcinogenic chromate: relationship to DNA damage. Mol. Carcinogen. 6 (1992) 270-279
41. Bridgewater L.C., Manning F.C., Woo E.S., and Patierno S.R. DNA polymerase arrest by adducted trivalent chromium. Mol. Carcinogen. 9 (1994) 122-133
42. Ha L., Ceryak S., and Patierno S.R. Chromium (VI) activates ataxia telangiectasia mutated (ATM) protein. Requirement of ATM for both apoptosis and recovery from terminal growth arrest. J. Biol. Chem. 278 (2003) 17885-17894
43. Ye J., Wang S., Leonard S.S., Sun Y., Butterworth L., Antonini J., Ding M., Rojanasakul Y., Vallyathan V., Castranova V., and Shi X. Role of reactive oxygen species and p53 in chromium (VI)-induced apoptosis. J. Biol. Chem. 274 (1999) 34974-34980
44. Carlisle D.L., Pritchard D.E., Singh J., Owens B.M., Blankenship L.J., Orenstein J.M., and Patierno S.R. Apoptosis and P53 induction in human lung fibroblasts exposed to chromium (VI): effect of ascorbate and tocopherol. Toxicol. Sci. 55 (2000) 60-68
45. Carlisle D.L., Pritchard D.E., Singh J., and Patierno S.R. Chromium (VI) induces p53-dependent apoptosis in diploid human lung and mouse dermal fibroblasts. Mol. Carcinogen. 28 (2000) 111-118
46. Ceryak S., Zingariello C., O'Brien T., and Patierno S.R. Induction of pro-apoptotic and cell cycle-inhibiting genes in chromium (VI)-treated human lung fibroblasts: lack of effect of ERK. Mol. Cell. Biochem. 255 (2004) 139-149
47. Donehower L.A., Harvey M., Slagle B.L., McArthur M.J., Montgomery Jr. C.A., Butel J.S., and Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356 (1992) 215-221
48. Araki R., Fukumura R., Fujimori A., Taya Y., Shiloh Y., Kurimasa A., Burma S., Li G.C., Chen D.J., Sato K., Hoki Y., Tatsumi K., and Abe M. Enhanced phosphorylation of p53 serine 18 following DNA damage in DNA-dependent protein kinase catalytic subunit-deficient cells. Cancer Res. 59 (1999) 3543-3546
49. Elson A., Wang Y., Daugherty C.J., Morton C.C., Zhou F., Campos-Torres J., and Leder P. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 13084-13089
50. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) method. Methods 25 (2001) 402-408
51. Kaeser M.D., and Iggo R.D. Chromatin immunoprecipitation analysis fails to support the latency model for regulation of p53 DNA binding activity in vivo. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 95-100
52. Komiyama S., Taniguchi S., Matsumoto Y., Tsunoda E., Ohto T., Suzuki Y., Yin H.L., Tomita M., Enomoto A., Morita A., Suzuki T., Ohtomo K., Hosoi Y., and Suzuki N. Potentiality of DNA-dependent protein kinase to phosphorylate Ser46 of human p53. Biochem. Biophys. Res. Commun. 323 (2004) 816-822
53. Tomita Y., Marchenko N., Erster S., Nemajerova A., Dehner A., Klein C., Pan H., Kessler H., Pancoska P., and Moll U.M. WTp53 but not tumor-derived mutants bind to BCL2 via the DNA binding domain and induce mitochondrial permeabilization. J. Biol. Chem. (2006) 8600-8606
54. Sobell H.M. Actinomycin and DNA transcription. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 5328-5331
55. Hill R., Leidal A.M., Madureira P.A., Gillis L.D., Cochrane H.K., Waisman D.M., Chiu A., and Lee P.W. Hypersensitivity to chromium-induced DNA damage correlates with constitutive deregulation of upstream p53 kinases in p21-/- HCT116 colon cancer cells. DNA Repair (Amst) 7 (2008) 239-252
56. Emerson B.M. Specificity of gene regulation. Cell 109 (2002) 267-270
57. Leveillard T., Andera L., Bissonnette N., Schaeffer L., Bracco L., Egly J.M., and Wasylyk B. Functional interactions between p53 and the TFIIH complex are affected by tumour-associated mutations. EMBO J. 15 (1996) 1615-1624
58. Ko L.J., Shieh S.Y., Chen X., Jayaraman L., Tamai K., Taya Y., Prives C., and Pan Z.Q. p53 is phosphorylated by CDK7-cyclin H in a p36MAT1-dependent manner. Mol. Cell. Biol. 17 (1997) 7220-7229
59. Dvir A., Conaway R.C., and Conaway J.W. A role for TFIIH in controlling the activity of early RNA polymerase II elongation complexes. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 9006-9010
60. Dvir A., Tan S., Conaway J.W., and Conaway R.C. Promoter escape by RNA polymerase II. Formation of an escape-competent transcriptional intermediate is a prerequisite for exit of polymerase from the promoter. J. Biol. Chem. 272 (1997) 28175-28178
61. Shinobu N., Maeda T., Aso T., Ito T., Kondo T., Koike K., and Hatakeyama M. Physical interaction and functional antagonism between the RNA polymerase II elongation factor ELL and p53. J. Biol. Chem. 274 (1999) 17003-17010
62. Arakawa H., Wu F., Costa M., Rom W., and Tang M.S. Sequence specificity of Cr (III)-DNA adduct formation in the p53 gene: NGG sequences are preferential adduct-forming sites. Carcinogenesis 27 (2006) 639-645
63. Peterson-Roth E., Reynolds M., Quievryn G., and Zhitkovich A. Mismatch repair proteins are activators of toxic responses to chromium-DNA damage. Mol. Cell. Biol. 25 (2005) 3596-3607
64. Hayashi Y., Kondo T., Zhao Q.L., Ogawa R., Cui Z.G., Feril Jr. L.B., Teranishi H., and Kasuya M. Signal transduction of p53-independent apoptotic pathway induced by hexavalent chromium in U937 cells. Toxicol. Appl. Pharmacol. 197 (2004) 96-106
65. Wakeman T.P., and Xu B. ATR regulates hexavalent chromium-induced S-phase checkpoint through phosphorylation of SMC1. Mutat. Res. 610 (2006) 14-20
66. Pritchard D.E., Ceryak S., Ramsey K.E., O'Brien T.J., Ha L., Fornsaglio J.L., Stephan D.A., and Patierno S.R. Resistance to apoptosis, increased growth potential, and altered gene expression in cells that survived genotoxic hexavalent chromium [Cr (VI)] exposure. Mol. Cell. Biochem. 279 (2005) 169-181