Inactivation by oxidation and recruitment into stress granules of hOGG1 but not APE1 in human cells exposed to sub-lethal concentrations of cadmium

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 685, Issue 1-2, 2010, Pages 61-69

  Bravard, Anne ^a   Campalans, Anna ^a   Vacher, Monique ^a   Gouget, Barbara ^b   Levalois, Céline ^a   Chevillard, Sylvie ^a   Radicella, J Pablo ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b CNRS   (France)

Author keywords

APE1; Cadmium; OGG1; Protein oxidation; Stress granules

Indexed keywords

8 OXOGUANINE GLYCOSYLASE; CADMIUM; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA GLYCOSYLTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; BIOACCUMULATION; CELL FRACTIONATION; CELL GRANULE; CELL PROLIFERATION; CELL STRUCTURE; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME METABOLISM; EXCISION REPAIR; FEMALE; GENE TRANSLOCATION; HUMAN; HUMAN CELL; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

CADMIUM; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASMIC GRANULES; DNA GLYCOSYLASES; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; DOWN-REGULATION; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; RNA PROCESSING, POST-TRANSCRIPTIONAL;

MAMMALIA;

EID: 75749105357     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2009.09.013     Document Type: Article

References (48)

1. IARC (1993) 58.
2. 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
3. Joseph P. Mechanisms of cadmium carcinogenesis. Toxicol. Appl. Pharmacol. 238 (2009) 272-279
4. Waisberg M., Joseph P., Hale B., and Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192 (2003) 95-117
5. Fotakis G., Cemeli E., Anderson D., and Timbrell J.A. Cadmium chloride-induced DNA and lysosomal damage in a hepatoma cell line. Toxicol. In Vitro 19 (2005) 481-489
6. Liu J., Qu W., and Kadiiska M.B. Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol. Appl. Pharmacol. 238 (2009) 209-214
7. Pourahmad J., O'Brien P.J., Jokar F., and Daraei B. Carcinogenic metal induced sites of reactive oxygen species formation in hepatocytes. Toxicol. In Vitro 17 (2003) 803-810
8. Grollman A.P., and Moriya M. Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet. 9 (1993) 246-249
9. Michaels M.L., and Miller J.H. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J. Bacteriol. 174 (1992) 6321-6325
10. Ates I., Suzen H.S., Aydin A., and Karakaya A. The oxidative DNA base damage in testes of rats after intraperitoneal cadmium injection. Biometals 17 (2004) 371-377
11. Filipic M., and Hei T.K. Mutagenicity of cadmium in mammalian cells: implication of oxidative DNA damage. Mutat. Res. 546 (2004) 81-91
12. Rosenquist T.A., Zharkov D.O., and Grollman A.P. Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 7429-7434
13. Arai K., Morishita K., Shinmura K., Kohno T., Kim S.R., Nohmi T., Taniwaki M., Ohwada S., and Yokota J. Cloning of a human homolog of the yeast OGG1 gene that is involved in the repair of oxidative DNA damage. Oncogene 14 (1997) 2857-2861
14. Bjoras M., Luna L., Johnsen B., Hoff E., Haug T., Rognes T., and Seeberg E. Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites. EMBO J. 16 (1997) 6314-6322
15. Radicella J.P., Dherin C., Desmaze C., Fox M.S., and Boiteux S. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 8010-8015
16. Roldan-Arjona T., Wei Y.F., Carter K.C., Klungland A., Anselmino C., Wang R.P., Augustus M., and Lindahl T. Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 8016-8020
17. Arai T., Kelly V.P., Minowa O., Noda T., and Nishimura S. High accumulation of oxidative DNA damage, 8-hydroxyguanine, in Mmh/Ogg1 deficient mice by chronic oxidative stress. Carcinogenesis 23 (2002) 2005-2010
18. Klungland A., Rosewell I., Hollenbach S., Larsen E., Daly G., Epe B., Seeberg E., Lindahl T., and Barnes D.E. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13300-13305
19. Minowa O., Arai T., Hirano M., Monden Y., Nakai S., Fukuda M., Itoh M., Takano H., Hippou Y., Aburatani H., Masumura K., Nohmi T., Nishimura S., and Noda T. Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 4156-4161
20. Wilson D.M.R., and Barsky D. The major human abasic endonuclease: formation, consequences and repair of abasic lesions in DNA. Mutat. Res. 485 (2001) 283-307
21. Demple B., and Harrison L. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63 (1994) 915-948
22. Ludwig D.L., MacInnes M.A., Takiguchi Y., Purtymun P.E., Henrie M., Flannery M., Meneses J., Pedersen R.A., and Chen D.J. A murine AP-endonuclease gene-targeted deficiency with post-implantation embryonic progression and ionizing radiation sensitivity. Mutat. Res. 409 (1998) 17-29
23. Xanthoudakis S., Smeyne R.J., Wallace J.D., and Curran T. The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 8919-8923
24. Meira L.B., Reis A.M., Cheo D.L., Nahari D., Burns D.K., and Friedberg E.C. Cancer predisposition in mutant mice defective in multiple genetic pathways: uncovering important genetic interactions. Mutat. Res. 477 (2001) 51-58
25. Unnikrishnan A., Raffoul J.J., Patel H.V., Prychitko T.M., Anyangwe N., Meira L.B., Friedberg E.C., Cabelof D.C., and Heydari A.R. Oxidative stress alters base excision repair pathway and increases apoptotic response in apurinic/apyrimidinic endonuclease 1/redox factor-1 haploinsufficient mice. Free Radic. Biol. Med. 46 (2009) 1488-1499
26. McNeill D.R., Narayana A., Wong H.K., and Wilson D.M.R. Inhibition of Ape1 nuclease activity by lead, iron, and cadmium. Environ. Health Perspect. 112 (2004) 799-804
27. Zharkov D.O., and Rosenquist T.A. Inactivation of mammalian 8-oxoguanine-DNA glycosylase by cadmium(II): implications for cadmium genotoxicity. DNA Repair (Amst) 1 (2002) 661-670
28. 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
29. Singh K.P., Kumari R., Pevey C., Jackson D., and DuMond J.W. Long duration exposure to cadmium leads to increased cell survival, decreased DNA repair capacity, and genomic instability in mouse testicular Leydig cells. Cancer Lett. 279 (2009) 84-92
30. Youn C.K., Kim S.H., Lee do 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
31. Bravard A., Vacher M., Gouget B., Coutant A., de Boisferon F.H., 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
32. Campalans A., Amouroux R., Bravard A., Epe B., and Radicella J.P. UVA irradiation induces relocalisation of the DNA repair protein hOGG1 to nuclear speckles. J. Cell Sci. 120 (2007) 23-32
33. Sleeman J.E., Ajuh P., and Lamond A.I. snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J. Cell Sci. 114 (2001) 4407-4419
34. Bravard A., Vacher M., Moritz E., Vaslin L., Hall J., Epe B., and Radicella J.P. Oxidation status of human OGG1-S326C polymorphic variant determines cellular DNA repair capacity. Cancer Res. 69 (2009) 3642-3649
35. Bishay K., Ory K., Olivier M.F., Lebeau J., Levalois C., and Chevillard S. DNA damage-related RNA expression to assess individual sensitivity to ionizing radiation. Carcinogenesis 22 (2001) 1179-1183
36. Oudard S., Levalois C., Andrieu J.M., Bougaran J., Validire P., Thiounn N., Poupon M.F., Fourme E., and Chevillard S. Expression of genes involved in chemoresistance, proliferation and apoptosis in clinical samples of renal cell carcinoma and correlation with clinical outcome. Anticancer Res. 22 (2002) 121-128
37. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., and Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3 (2002) (RESEARCH0034)
38. Hua Y., and Zhou J. Survival motor neuron protein facilitates assembly of stress granules. FEBS Lett. 572 (2004) 69-74
39. 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
40. Sens D.A., Park S., Gurel V., Sens M.A., Garrett S.H., and Somji S. Inorganic cadmium- and arsenite-induced malignant transformation of human bladder urothelial cells. Toxicol. Sci. 79 (2004) 56-63
41. Waalkes M.P. Cadmium carcinogenesis in review. J. Inorg. Biochem. 79 (2000) 241-244
42. Mikhailova M.V., Littlefield N.A., Hass B.S., Poirier L.A., and Chou M.W. Cadmium-induced 8-hydroxydeoxyguanosine formation, DNA strand breaks and antioxidant enzyme activities in lymphoblastoid cells. Cancer Lett. 115 (1997) 141-148
43. Banfalvi G., Littlefield N., Hass B., Mikhailova M., Csuka I., Szepessy E., and Chou M.W. Effect of cadmium on the relationship between replicative and repair DNA synthesis in synchronized CHO cells. Eur. J. Biochem. 267 (2000) 6580-6585
44. Anderson P., and Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33 (2008) 141-150
45. Hegde V., Wang M., and Deutsch W.A. Human ribosomal protein S3 interacts with DNA base excision repair proteins hAPE/Ref-1 and hOGG1. Biochemistry 43 (2004) 14211-14217
46. Yacoub A., Augeri L., Kelley M.R., Doetsch P.W., and Deutsch W.A. A Drosophila ribosomal protein contains 8-oxoguanine and abasic site DNA repair activities. EMBO J. 15 (1996) 2306-2312
47. Scadden A.D. Inosine-containing dsRNA binds a stress-granule-like complex and downregulates gene expression in trans. Mol. Cell 28 (2007) 491-500
48. Vascotto C., Fantini D., Romanello M., Cesaratto L., Deganuto M., Leonardi A., Radicella J.P., Kelley M.R., D'Ambrosio C., Scaloni A., Quadrifoglio F., and Tell G. APE1/Ref-1 interacts with NPM1 within nucleoli and plays a role in the rRNA quality control process. Mol. Cell. Biol. 29 (2009) 1834-1854