Cadmium and copper inhibit both DNA repair activities of polynucleotide kinase

DNA Repair

Volumn 9, Issue 1, 2010, Pages 83-89

  Whiteside, James R ^a   Box, Clare L ^a   McMillan, Trevor J ^a   Allinson, Sarah L ^a  

^a LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

Cadmium; Copper; Heavy metals; Polynucleotide kinase; Single strand breaks

Indexed keywords

CADMIUM; COBALT; COPPER; LEAD; NICKEL; POLYNUCLEOTIDE 5' HYDROXYL KINASE; ZINC;

ARTICLE; CARCINOGENICITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA REPAIR; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; NEUROTOXICITY; PRIORITY JOURNAL; SINGLE STRANDED DNA BREAK;

CADMIUM; COPPER; DNA REPAIR; DNA, SINGLE-STRANDED; ENZYME INHIBITORS; POLYNUCLEOTIDE 5'-HYDROXYL-KINASE;

EID: 72949103910     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.11.004     Document Type: Article

References (58)

1. Florea A.M., and Busselberg D. Occurrence, use and potential toxic effects of metals and metal compounds. Biometals 19 (2006) 419-427
2. Waalkes M.P. Metal carcinogenesis. In: Sarkar B. (Ed). Heavy Metals in the Environment (2002), CRC Press pp. 121-146
3. Beyersmann D., and Hartwig A. Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch. Toxicol. 82 (2008) 493-512
4. Witkiewicz-Kucharczyk A., and Bal W. Damage of zinc fingers in DNA repair proteins, a novel molecular mechanism in carcinogenesis. Toxicol. Lett. 162 (2006) 29-42
5. Maynard S., Schurman S.H., Harboe C., de Souza-Pinto N.C., and Bohr V.H. Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 30 (2009) 2-10
6. Dianov G.L., and Parsons J.L. Co-ordination of DNA single strand break repair. DNA Rep. (Amst.) 6 (2007) 454-460
7. Fatur T., Lah T.T., and Filipic M. Cadmium inhibits repair of UV-, methyl methanesulfonate- and N-methyl-N-nitrosourea-induced DNA damage in Chinese hamster ovary cells. Mutat. Res. 529 (2003) 109-116
8. Hartmann A., and Speit G. Effect of arsenic and cadmium on the persistence of mutagen-induced DNA lesions in human cells. Environ. Mol. Mutagen. 27 (1996) 98-104
9. Lynn S., Lai H.T., Kao S.M., Lai J., and Jan K.Y. Cadmium inhibits DNA strand break rejoining in methyl methanesulfonate-treated CHO-K1 cells. Toxicol. Appl. Pharmacol. 144 (1997) 171-176
10. De Boeck M., Lison D., and Kirsch-Volders M. Evaluation of the in vitro direct and indirect genotoxic effects of cobalt compounds using the alkaline comet assay. Influence of interdonor and interexperimental variability. Carcinogenesis 19 (1998) 2021-2029
11. Caldecott K.W. Single-strand break repair and genetic disease. Nat. Rev. Genet. 9 (2008) 619-631
12. Karimi-Busheri F., Daly G., Robins P., Canas B., Pappin D.J., Sgouros J., Miller G.G., Fakhrai H., Davis E.M., Le Beau M.M., and Weinfeld M. Molecular characterization of a human DNA kinase. J. Biol. Chem. 274 (1999) 24187-24194
13. Dobson C.J., and Allinson S.L. The phosphatase activity of mammalian polynucleotide kinase takes precedence over its kinase activity in repair of single strand breaks. Nucleic Acids Res. 34 (2006) 2230-2237
14. Karimi-Busheri F., Lee J., Tomkinson A.E., and Weinfeld M. Repair of DNA strand gaps and nicks containing 3′-phosphate and 5′-hydroxyl termini by purified mammalian enzymes. Nucleic Acids Res. 26 (1998) 4395-4400
15. Jilani A., Ramotar D., Slack C., Ong C., Yang X.M., Scherer S.W., and Lasko D.D. Molecular cloning of the human gene, PNKP, encoding a polynucleotide kinase 3′-phosphatase and evidence for its role in repair of DNA strand breaks caused by oxidative damage. J. Biol. Chem. 274 (1999) 24176-24186
16. Habraken Y., and Verly W.G. The DNA 3′-phosphatase and 5′-hydroxyl kinase of rat liver chromatin. FEBS Lett. 160 (1983) 46-50
17. Pheiffer B.H., and Zimmerman S.B. 3′-Phosphatase activity of the DNA kinase from rat liver. Biochem. Biophys. Res. Commun. 109 (1982) 1297-1302
18. Chappell C., Hanakahi L.A., Karimi-Busheri F., Weinfeld M., and West S.C. Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining. EMBO J. 21 (2002) 2827-2832
19. Audient M., Sales B., Weinfeld M., and Callous P. Involvement of polynucleotide kinase in a poly(ADP-ribose) polymerase-1-dependent DNA double-strand breaks rejoining pathway. J. Mol. Biol. 356 (2006) 257-265
20. Rasouli-Nia A., Karimi-Busheri F., and Weinfeld M. Stable down-regulation of human polynucleotide kinase enhances spontaneous mutation frequency and sensitizes cells to genotoxic agents. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 6905-6910
21. Jacobs J.P., Jones C.M., and Baille J.P. Characteristics of a human diploid cell designated MRC-5. Nature 227 (1970) 168-170
22. McNeill D.R., Narayana A., Wong H.K., and Wilson D.M. Inhibition of Ape1 nuclease activity by lead, iron, and cadmium. Environ. Health Perspect. 112 (2004) 799-804
23. Mani R.S., Fanta M., Karimi-Busheri F., Silver E., Virgen C.A., Caldecott K.W., Cass C.E., and Weinfeld M. XRCC1 stimulates polynucleotide kinase by enhancing its damage discrimination and displacement from DNA repair intermediates. J. Biol. Chem. 282 (2007) 28004-28013
24. Whitehouse C.J., Taylor R.M., Thistlethwaite A., Zhang H., Karimi-Busheri F., Lasko D.D., Weinfeld M., and Caldecott K.W. XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 104 (2001) 107-117
25. Takahashi T., Tada M., Igarashi S., Koyama A., Date H., Yokoseki A., Shiga A., Yoshida Y., Tsuji S., Nishizawa M., and Onodera O. Aprataxin, causative gene product for EAOH/AOA1, repairs DNA single-strand breaks with damaged 3′-phosphate and 3′-phosphoglycolate ends. Nucleic Acids Res. 35 (2007) 3797-3809
26. Barzilay G., and Hickson I.D. Structure and function of apurinic/apyrimidinic endonucleases. Bioessays 17 (1995) 713-719
27. Banerjee S., and Flores-Rozas H. Cadmium inhibits mismatch repair by blocking the ATPase activity of the MSH2-MSH6 complex. Nucleic Acids Res. 33 (2005) 1410-1419
28. Zharkov D.O., and Rosenquist T.A. Inactivation of mammalian 8-oxoguanine-DNA glycosylase by cadmium(II): implications for cadmium genotoxicity. DNA Rep. (Amst.) 1 (2002) 661-670
29. Bravard A., Vacher M., Gouget B., Coutant A., Hillairet de Boisferon F., Marsin S., Chevillard S., and Radicella J.P. Redox regulation of human OGG1 activity in response to cellular oxidative stress. Mol. Cell Biol. 26 (2006) 7430-7436
30. Anderegg G., Hubmann E., Podder N.G., and Wenk F. Pyridinderivate als Komplexbildner. XI. Die Thermodynamik der Metallkomplexbildung mit Bis-, Tris und Tetrakis[2-(pyridyl)methyl]-aminen. Helv. Chem. Acta 60 (1977) 123-140
31. Bertin G., and Averbeck D. Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88 (2006) 1549-1559
32. Giaginis C., Gatzidou E., and Theocharis S. DNA repair systems as targets of cadmium toxicity. Toxicol. Appl. Pharmacol. 213 (2006) 282-290
33. Kasten U., Mullenders L.H., and Hartwig A. Cobalt(II) inhibits the incision and the polymerization step of nucleotide excision repair in human fibroblasts. Mutat. Res. 383 (1997) 81-89
34. Potts R.J., Bespalov I.A., Wallace S.S., Melamede R.J., and Hart B.A. Inhibition of oxidative DNA repair in cadmium-adapted alveolar epithelial cells and the potential involvement of metallothionein. Toxicology 161 (2001) 25-38
35. Potts R.J., Watkin R.D., and Hart B.A. Cadmium exposure down-regulates 8-oxoguanine DNA glycosylase expression in rat lung and alveolar epithelial cells. Toxicology 184 (2003) 189-202
36. Youn C.K., Kim S.H., Lee D.Y., Song S.H., Chang I.Y., Hyun J.W., Chung M.H., and You H.J. Cadmium down-regulates human OGG1 through suppression of Sp1 activity. J. Biol. Chem. 280 (2005) 25185-25195
37. Hartwig A., Asmuss M., Blessing H., Hoffmann S., Jahnke G., Khandelwal S., Pelzer A., and Burkle A. Interference by toxic metal ions with zinc-dependent proteins involved in maintaining genomic stability. Food Chem. Toxicol. 40 (2002) 1179-1184
38. Schwerdtle T., Hamann I., Jahnke G., Walter I., Richter C., Parsons J.L., Dianov G.L., and Hartwig A. Impact of copper on the induction and repair of oxidative DNA damage, poly(ADP-ribosyl)ation and PARP-1 activity. Mol. Nutr. Food Res. 51 (2007) 201-210
39. Taylor R.M., Whitehouse J., Cappelli E., Frosina G., and Caldecott K.W. Role of the DNA ligase III zinc finger in polynucleotide binding and ligation. Nucleic Acids Res. 26 (1998) 4804-4810
40. Wieland M., Levin M.K., Hingorani K.S., Biro F.N., and Hingorani M.M. Mechanism of cadmium-mediated inhibition of Msh2-Msh6 function in DNA mismatch repair. Biochemistry 48 (2009) 9492-9502
41. Clark A.B., and Kunkel T.A. Cadmium inhibits the functions of eukaryotic MutS complexes. J. Biol. Chem. 279 (2004) 53903-53906
42. Jin Y.H., Clark A.B., Slebos R.J., Al-Refai H., Taylor J.A., Kunkel T.A., Resnick M.A., and Gordenin D.A. Cadmium is a mutagen that acts by inhibiting mismatch repair. Nat. Genet. 34 (2003) 326-329
43. Viau M., Gastaldo J., Bencokova Z., Joubert A., and Foray N. Cadmium inhibits non-homologous end-joining and over-activates the MRE11-dependent repair pathway. Mutat. Res. 654 (2008) 13-21
44. Wang P., Guliaev A.B., and Hang B. Metal inhibition of human N-methylpurine-DNA glycosylase activity in base excision repair. Toxicol. Lett. 166 (2006) 237-247
45. Huff J., Lunn R.M., Waalkes M.P., Tomatis L., and Infante P.F. Cadmium-induced cancers in animals and in humans. Int. J. Occup. Environ. Health 13 (2007) 202-212
46. Asmuss M., Mullenders L.H., Eker A., and Hartwig A. Differential effects of toxic metal compounds on the activities of Fpg and XPA, two zinc finger proteins involved in DNA repair. Carcinogenesis 21 (2000) 2097-2104
47. Joseph P. Mechanisms of cadmium carcinogenesis. Toxicol. Appl. Pharmacol. (2009) 272-279
48. Ochi T., and Ohsawa M. Participation of active oxygen species in the induction of chromosomal aberrations by cadmium chloride in cultured Chinese hamster cells. Mutat. Res. 143 (1985) 137-142
49. Filipic M., and Hei T.K. Mutagenicity of cadmium in mammalian cells: implication of oxidative DNA damage. Mutat. Res. 546 (2004) 81-91
50. Llanos R.M., and Mercer J.F. The molecular basis of copper homeostasis copper-related disorders. DNA Cell. Biol. 21 (2002) 259-270
51. Grillo C.A., Reigosa M.A., and Lorenzo de Mele M.F. Effects of copper ions released from metallic copper on CHO-K1 cells. Mutat. Res. 672 (2009) 45-50
52. Guecheva T., Henriques J.A., and Erdtmann B. Genotoxic effects of copper sulphate in freshwater planarian in vivo, studied with the single-cell gel test (comet assay). Mutat. Res. 497 (2001) 19-27
53. Hayashi M., Fuse S., Endoh D., Horiguchi N., Nakayama K., Kon Y., and Okui T. Accumulation of copper induces DNA strand breaks in brain cells of Long-Evans Cinnamon (LEC) rats, an animal model for human Wilson Disease. Exp. Anim. 55 (2006) 419-426
54. Pra D., Franke S.I., Giulian R., Yoneama M.L., Dias J.F., Erdtmann B., and Henriques J.A. Genotoxicity and mutagenicity of iron and copper in mice. Biometals 21 (2008) 289-297
55. Shubber E., Amin N.S., and El-Adhami B.H. Cytogenetic effects of copper-containing intrauterine contraceptive device (IUCD) on blood lymphocytes. Mutat. Res. 417 (1998) 57-63
56. Snyder R.D., and Lachmann P.J. Thiol involvement in the inhibition of DNA repair by metals in mammalian cells. Mol. Toxicol. 2 (1989) 117-128
57. Cai L., Li X.K., Song Y., and Cherian M.G. Essentiality, toxicology and chelation therapy of zinc and copper. Curr. Med. Chem. 12 (2005) 2753-2763
58. Mendez-Armenta M., and Rios C. Cadmium neurotoxicity. Environ. Toxicol. Pharmacol. 23 (2007) 350-358