APE/Ref-1 and the mammalian response to genotoxic stress

Toxicology

Volumn 193, Issue 1-2, 2003, Pages 67-78

  Fritz, Gerhard ^a   Grösch, Sabine ^a   Tomicic, Maja ^a   Kaina, Bernd ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

APE Ref 1; Genotoxic stress; Tumor

Indexed keywords

DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; GUANOSINE TRIPHOSPHATASE; PROTEIN; REACTIVE OXYGEN METABOLITE; REDOX EFFECTOR FACTOR 1; TUMOR MARKER; UNCLASSIFIED DRUG;

APOPTOSIS; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; DOWN REGULATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENOTOXICITY; HUMAN; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SENSITIZATION; TRANSCRIPTION REGULATION; TUMOR;

ALOCASIA MACRORRHIZOS; MAMMALIA;

EID: 0242299711     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0300-483X(03)00290-7     Document Type: Review

References (66)

1. Adimoolam S., Ford J.M. p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc. Natl. Acad. Sci. U.S.A. 99:2002;12985-12990.
2. Babiychuk E., Kushnir S., Van Montagu M., Inze D. The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun. Proc. Natl. Acad. Sci. U.S.A. 98:1994;3299-3303.
3. Barzilay G., Mol C.D., Robson C.N., Walker L.J., Cunningham R.P., Tainer J.A., Hickson I.D. Identification of critical active-site residues in the multifunctional human DNA repair enzyme HAP1. Nat. Struct. Biol. 2:1995;561-568.
4. Barzilay G., Walker L.J., Robson C.N., Hickson I.D. Site-directed mutagenesis of the human DNA repair enzyme HAP1: identification of residues important for AP endonuclease and RNase H activity. Nucl. Acids Res. 23:1995;1544-1550.
5. Bennett R.A., Wilson D.M. III, Wong D., Demple B. Interaction of human apurinic endonuclease and DNA polymerase β in the base excision repair pathway. Proc. Natl. Acad. Sci. U.S.A. 94:1997;7166-7169.
6. Bobola M.S., Blank A., Berger M.S., Stevens B.A., Silber J.R. Apurinic/apyrimidinic endonuclease activity is elevated in human adult gliomas. Clin. Cancer Res. 7:2001;3510-3518.
7. 6-methylguanine-DNA methyltransferase via protein kinase C-mediated signaling. Cancer Res. 58:1998;3950-3956.
8. Dianova, I.I., Bohr, V. A., Dianov, G. L., 2001. Interaction of human AP endonuclease 1 with flap endonuclease 1 and proliferating cell nuclear antigen involved in long-patch base excision repair, Biochemistry 40, pp. 12639-12644.
9. Evans A.R., Limp-Foster M., Kelley M.R. Going APE over Ref-1. Mut. Res. 461:2000;83-108.
10. Flaherty D.M., Monick M.M., Hunninghake G.W. AP endonuclease and the many functions of Ref-1. Am. J. Respir. Cell Mol. Biol. 25:2001;664-667.
11. Fornace A.J. Jr., Zmudzka B., Hollander C., Wilson S.H. Induction of β-polymerase mRNA by DNA-damaging agents in Chinese hamster ovary cells. Mol. Cell. Biol. 9:1989;851-853.
12. Friedberg, E.C., Walker, G.C., Siede, W., 1995. DNA Repair and Mutagenesis. ASM Press, Washington, DC, USA.
13. Fritz G., Brachetti T., Bahlmann F., Schmidt M., Kaina B. Rho GTPases in human breast tumors: expression and mutation analysis and correlation with clinical parameters. Br. J. Cancer. 87:2002;635-644.
14. Fritz G., Kaina B. Phosphorylation of the DNA repair protein APE/Ref-1 by CKII affects redox regulation of AP-1. Oncogene. 18:1999;1033-1040.
15. 6-methylguanine-DNA methyltransferase in mammalian cells by DNA-damaging treatments. Mol. Cell. Biol. 11:1991;4660-4668.
16. 2 induces translocation of APE/Ref-1 to mitochondria in the Raji B-cell line. J. Cell. Phys. 193:2002;180-186.
17. Fung H., Bennet R.A., Demple B. Key role of a downstream specificity protein 1 site in cell cycle-regulated transcription of the AP endonuclease gene APE1/APEX in NIH3T3 cells. J. Biol. Chem. 276:2001;42011-42017.
18. Grombacher T., Mitra S., Kaina B. Induction of the alkyltransferase (MGMT) gene by DNA damaging agents and the glucocorticoid dexamethasone and comparison with the response of base excision repair genes. Carcinogenesis. 17:1996;2329-2336.
19. Grosch S., Fritz G., Kaina B. Apurinic endonuclease (Ref-1) is induced in mammalian cells by oxidative stress and involved in clastogenic adaptation. Cancer Res. 58:1998;4410-4416.
20. Habraken Y., Laval F. Increased resistance of the Chinese hamster mutant irs1 cells to monofunctional alkylating agents by transfection of the E. coli or mammalian N3-methyladenine-DNA-glycosylase genes. Mutat. Res. 293:1993;187-195.
21. He Y.-H., Wu M., Kobune M., Xu Y., Kelley M.R., Martin W.J. II Expression of yeast apurinic/apyrimidinic endonuclease (APN1) protects lung epithelial cells from bleomycin toxicity. Am. J. Respir. Cell Mol. Biol. 25:2001;692-698.
22. Herring C.J., Deans B., Elder R.H., Rafferty J.A., MacKinnon J., Barzilay G., Hickson I.D., Hendry J.H., Margison G.P. Expression levels of the DNA repair enzyme HAP1 do not correlate with the radiosensitivities of human or HAP1-transfected rat cell lines. Br. J. Cancer. 80:1999;940-945.
23. Herring C.J., West C.M., Wilks D.P., Davidson S.E., Hunter R.D., Berry P., Forster G., MacKinnon J., Rafferty J.A., Elder R.H.et al. Levels of the DNA repair enzyme human apurinic/apyrimidinic endonuclease (APE1, APEX, Ref-1) are associated with the intrinsic radiosensitivity of cervical cancers. Br. J. Cancer. 78:1998;1128-1133.
24. Hirota K., Matsui M., Iwata S., Nishiyama A., Mori K., Yodoi J. AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc. Natl. Acad. Sci. U.S.A. 94:1997;3633-3638.
25. Ho E., Ames B.N. Low intracellular zinc induces oxidative DNA damage, disrupts p53, NF-κB and AP1 DNA binding and affects DNA repair in rat glioma cell line. Proc. Natl. Acad. Sci. U.S.A. 99:2002;16770-16775.
26. Hsieh M.M., Hegde V., Kelley M.R., Deutsch W.A. Activation of APE/Ref-1 redox activity is mediated by reactive oxygen species and PKC phosphorylation. Nucl. Acids Res. 29:2001;3116-3122.
27. Izumi T., Henner W.D., Mitra S. Negative regulation of the major human AP-endonuclease, a multifunctional protein. Biochemistry. 35:1996;14679-14683.
28. Izumi T., Mitra S. Deletion analysis of human AP-endonuclease: minimum sequence required for the endonuclease activity. Carcinogenesis. 19:1998;525-527.
29. Jayaraman L., Murthy K.G.K., Zhu C., Curran T., Xanthoudiakis S., Prives C. Identification of redox/repair protein Ref-1 as a potent activator of p53. Genes Dev. 11:1997;558-570.
30. Kakolyris S., Giatromanolaki A., Koukourakis M., Kaklamanis L., Kanavaros P., Hickson I.D., Barzilay G., Georgoulias V., Gatter K.C., Harris A.L. Nuclear localization of human AP endonuclease 1 (HAP1/Ref-1) associates with prognosis in early operable non-small cell lung cancer (NSCLC). J. Pathol. 189:1999;351-357.
31. Kakolyris S., Kaklamanis L., Engels K., Fox S.B., Taylor M., Hickson I.D., Gatter K.C., Harris A.L. Human AP endonuclease 1 (HAP1) protein expression in breast cancer correlates with lymph node status and angiogenesis. Br. J. Cancer. 77:1998a;1169-1173.
32. Kakolyris S., Kaklamanis L., Engels K., Turley H., Hickson I.D., Gatter K.C., Harris A.L. Human apurinic endonuclease 1 expression in a colorectal adenoma-carcinoma sequence. Cancer Res. 57:1997;1794-1797.
33. Kakolyris S., Kaklamanis L., Giatromanolaki A., Koukourakis M., Hickson I.D., Barzilay G., Turkey H., Leek R.D., Kanavaros P., Georgoulias V.et al. Expression and subcellular localization of human AP endonuclease 1 (HAP1/Ref-1) protein: a basis for its role in human disease. Histopathology. 33:1998b;561-569.
34. Karimpour S., Lou J., Lin L.L., Rene L.M., Lagunas L., Ma X., Karra S., Bradbury C.M., Markovina S., Goswami P.C.et al. Thioredoxin reductase regulates AP-1 activity as well as thioredoxin nuclear localization via active cysteines in response to ionizing radiation. Oncogene. 21:2002;6317-6327.
35. Koukourakis M.I., Giatromanolaki A., Kakolyris S., Sivridis E., Georgoulias V., Funtzilas G., Hickson I.D., Gatter K.C., Harris A.L.et al. Nuclear expression of human apurinic/apyrimidinic endonuclease (HAP1/Ref-1) in head-and-neck cancer is associated with resistance to chemoradiotherapy and poor outcome. Int. J. Rad. Oncol. Biol. Phys. 50:2001;27-36.
36. Lindahl T., Nyberg B. Rate of depurination of native deoxyribonucleic acid. Biochemistry. 11:1972;3610-3618.
37. Loeb L.A., Preston B.D. Mutagenesis by apurinic/apyrimidinic sites. Ann. Rev. Genet. 20:1986;201-230.
38. Meira L.B., Devaraj S., Kisby G.E., Burns D.K., Daniel R.L., Hammer R.E., Grundy S., Jialal I., Friedberg E.C.et al. Heterozygosity for the mouse Apex gene results in phenotypes associated with oxidative stress. Cancer Res. 61:2001;5552-5557.
39. Moore D.H., Michael H., Tritt R., Parsons S.H., Kelley M.R. Alterations in the expression of the DNA repair/redox enzyme APE/Ref-1 in epithelial ovarian cancers. Clin. Cancer Res. 6:2000;602-609.
40. Morgan M.A., Chu C.S., Benjamin I., Randall T.C., Boyd J., Rubin S.C. Alterations in the expression of the DNA repair/redox enzyme APE/Ref-1 in epithelial ovarian cancers. Gyn. Oncol. 72:1999;520.
41. Mullenders L.H. Transcription response and nucleotide excision repair. Mutat. Res. 409:1998;59-64.
42. Ochs K., Sobol R.W., Wilson S.H., Kaina B. Cells deficient in DNA polymerase β are hypersensitive to alkylating agent-induced apoptosis and chromosomal breakage. Cancer Res. 59:1999;1544-1551.
43. Ono Y., Furuta T., Ohmoto T., Akiyama K., Seki S. Stable expression in rat glioma cells of sense and anti-sense nucleic acids to a human multifunctional DNA repair enzyme, APEX nuclease. Mutat. Res. 315:1994;55-63.
44. Ozaki M., Suzuki S., Irani K. Redox factor-1/APE suppresses oxidative stress by inhibiting the rac1 GTPase. FASEB J. 16:2002;889-890.
45. Puglisi F., Aprile G., Minisini A.M., Barbone F., Cataldi P., Tell G., Kelley M.R., Damante G., Beltrami C.A., Di Loreto C. Prognostic significance of APE1/Ref-1 subcellular localization in non-small cell lung carcinomas. Anticancer Res. 21:2001;4041-4049.
46. Puglisi F., Barbone F., Tell G., Aprile G., Pertoldi B., Raiti C., Kelley M.R., Damante G., Sobrero A., Beltrami C.A.et al. Prognostic role of APE/Ref-1 subcellular expression in stage I-III breast carcinomas. Oncol. Rep. 9:2002;11-17.
47. Ramana C.V., Boldogh I., Izumi T., Mitra S. Activation of apurinic/apyrimidinic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotoxicity of free radicals. Proc. Natl. Acad. Sci. U.S.A. 95:1998;5061-5066.
48. Robertson K.A., Bullock H.A., Xu Y., Tritt R., Zimmerman E., Ulbright T.M., Foster R.S., Einhorn L.H., Kelley M.R. Altered expression of APE1/Ref-1 in germ cell tumors and overexpression in NT2 cells confers resistance to bleomycin and radiation. Cancer Res. 61:2001;2220-2225.
49. Szakmary A., Huang S.M., Chang D.T., Beachy P.A., Sander M. Overexpression of a Rrp1 transgene reduces the somatic mutation and recombination frequency induced by oxidative DNA damage in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 93:1996;1607-1612.
50. Tan Z., Sun N., Schreiber S.S. Immunohistochemical localization of redox factor-1 (Ref-1) in Alzheimer's hippocampus. Neuroreport. 9:1998;2749-2752.
51. Tanner, B., Grimme, S., Schiffer, I., Heimerdinger, C., Pilch, H., Schmidt, M., Dutkowski, P., Neubert, S., Oesch, F., Fritz, G., Kaina, B., Hengstler, J., 2003. Nuclear expression of apurinic/apyrimidinic endonuclease (APE) increases with progression of ovarian carcinomas, submitted for publication.
52. Thomson B., Tritt R., Davis M., Kelley M.R. Histology-specific expression of a DNA repair protein in pediatric rhabdo-myosarcomas. J. Pediatr. Hematol. Oncol. 23:2001;234-239.
53. Tomicic M., Eschbach E., Kaina B. Expression of yeast but not human apurinic/apyrimidinic endonuclease renders Chinese hamster cells more resistant to DNA damaging agents. Mutat. Res. 383:1997;155-165.
54. van Steeg H., Mullenders L.H., Vijg J. Mutagenesis and carcinogenesis in nucleotide excision repair-deficient XPA knock out mice. Mutat. Res. 450:2000;167-180.
55. Walker L.J., Craig R.B., Harris A.L., Hickson I.D. A role for the human DNA repair enzyme HAP1 in cellular protection against DNA damaging agents and hypoxic stress. Nucl. Acids Res. 22:1994;4884-4889.
56. Walker L.J., Robson C.N., Black E., Gillespie D., Hickson I.D. Identification of residues in the human DNA repair enzyme HAP1 (Ref-1) that are essential for redox regulation of jun DNA binding. Mol. Cell. Biol. 13:1993;5370-5376.
57. Wang C.Y., Mayo M.W., Baldwin A.S. Jr. TNF and cancer therapy-induced apoptosis: potentiation by inhibition of NF-κB. Science. 274:1996;784-786.
58. Wei S.J., Botero H., Hirota K., Bradbury C.M., Markovina S., Lazlo A., Spitz D.R., Goswami P.C., Yodoi J., Gius D. Thioredoxin nuclear translocation and interaction with redox factor-1 activates the activator protein-1 transcription factor in response to ionizing radiation. Cancer Res. 60:2000;6688-6695.
59. Wilson D.M., Bennett R.A., Marquis J.C., Ansari P., Demple B. Trans-complementation by human apurinic endonuclease (APE) of hypersensitivity to DNA damage and spontaneous mutator phenotype in apn1-yeast. Nucl. Acids Res. 23:1995;5027-5033.
60. Wood R.D. Nucleotide excision repair in mammalian cells. J. Biol. Chem. 272:1997;23465-23468.
61. Xanthoudakis S., Curran T. Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA binding activity. EMBO J. 11:1992;653-665.
62. Xanthoudakis S., Miao G., Wang F., Pan Y.C., Curran T. Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J. 11:1992;3323-3335.
63. Xanthoudakis S., Miao G.G., Curran T. The redox and DNA-repair activities of Ref-1 are encoded by non-overlapping domains. Proc. Natl. Acad. Sci. U.S.A. 91:1994;23-27.
64. Xu Y., Moore D.H., Broshears J., Liu L., Wilson T.M., Kelley M.R. The apurinic/apyrimidinic endonuclease (APE/Ref-1) DNA repair enzyme is elevated in pre-malignant and malignant cervical cancer. Anticancer Res. 17:1997;3713-3719.
65. Xu Y., Parsons S., Hansen W.K., Williams D.A., Kelley M.R. Use of DNA base-excision repair (BER) genes to protect cells: retroviral expression of the yeast AP endonuclease (APN1) enhances the level of protection of mammalian cells agains DNA oxidative and alkylating agents. Environ. Mol. Mutagen. 33:1999;69.
66. Yacoub A., Kelley M.R., Deutsch W.A. The DNA repair activity of human redox/repair protein APE/Ref-1 is inactivated by phosphorylation. Cancer Res. 57:1997;5457-5459.