A new APE1/Ref-1-dependent pathway leading to reduction of NF-κB and AP-1, and activation of their DNA-binding activity

Nucleic Acids Research

Volumn 36, Issue 13, 2008, Pages 4327-4336

  Ando, Kozue ^a   Hirao, Satoshi ^a   Kabe, Yasuaki ^a   Ogura, Yuji ^a   Sato, Iwao ^a   Yamaguchi, Yuki ^a   Wada, Tadashi ^a   Handa, Hiroshi ^a  

^a Tokyo Institute of Technology ^*  (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE 1; GLUTATHIONE; GLUTATHIONE TRANSFERASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; REDOX EFFECTOR FACTOR 1; THIOREDOXIN; TRANSCRIPTION FACTOR AP 1;

ANTIOXIDANT ACTIVITY; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; DNA BINDING; ENZYME ACTIVITY; HUMAN; HUMAN CELL; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SITE DIRECTED MUTAGENESIS;

ANIMALS; CELL LINE; CYSTEINE; DNA; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; GLUTATHIONE; HUMANS; MOLECULAR CHAPERONES; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; OXIDATION-REDUCTION; RATS; THIOREDOXINS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS;

MUS;

EID: 48349107170     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn416     Document Type: Article

References (56)

1. Bader,M., Muse,W., Ballou,D.P., Gassner,C. and Bardwell,J.C. (1999) Oxidative protein folding is driven by the electron transport system. Cell, 98, 217-227.
2. Jakob,U., Muse,W., Eser,M. and Bardwell,J.C. (1999) Chaperone activity with a redox switch. Cell, 96, 341-352.
3. Mannick,J.B., Hausladen,A., Liu,L., Hess,D.T., Zeng,M., Miao,Q.X., Kane,L.S., Gow,A.J. and Stamler,J.S. (1999) Fas-induced caspase denitrosylation. Science, 284, 651-654.
4. Tsai,B., Rodighiero,C., Lencer,W.I. and Rapoport,T.A. (2001) Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell, 104, 937-948.
5. Eu,J.P., Sun,J., Xu,L., Stamler,J.S. and Meissner,G. (2000) The skeletal muscle calcium release channel: Coupled O2 sensor and NO signaling functions. Cell, 102 499-509.
6. Xanthoudakis,S., Miao,G., Wang,F., Pan,Y.C. and Curran,T. (1992) Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J., 11, 3323-3335.
7. Xanthoudakis,S. and Curran,T. (1992) Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity. EMBO J., 11, 653-665.
8. Huang,R.P. and Adamson,E.D. (1993) Characterization of the DNA-binding properties of the early growth response-1 (Egr-1) transcription factor: evidence for modulation by a redox mechanism. DNA Cell Biol., 12, 265-273.
9. Ema,M., Hirota,K., Mimura,J., Abe,H., Yodoi,J., Sogawa,K., Poellinger,L. and Fujii-Kuriyama,Y. (1999) Molecular mechanisms of transcription, activation by HLF and HIFlalpha in response to hypoxia: Their stabilization and redox signal-induced interaction with CBP/p300. EMBO J., 18, 1905-1914.
10. Huang,L.E., Arany,Z., Livingston,D.M. and Bunn,H.F. (1996) Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J. Biol. Chem. 271, 32253-32259.
11. Lando,D., Pongratz,I., Poellinger,L. and Whitelaw,M.L. (2000) A redox mechanism controls differential DNA binding activities of hypoxia-inducible factor (HIF) lalpha and the HIF-tike factor. J. Biol. Chem., 275, 4618-4627.
12. Cao,X., Kambe,F., Ohmori,S. and Seo,H. (2002) Oxidoreductive modification of two cysteine residues in paired domain by Ref-1 regulates DNA-binding activity of Pax-8. Biochem. Biophys. Res. Commun., 297, 288-293.
13. Tell,G., Pellizzari,L., Cimarosti,D., Pucillo,C. and Damante,G. (1998) Ref-1 controls pax-8 DNA-binding activity. Biochem. Biophys. Res. Commun., 252, 178-483.
14. Tell,G., Scaloni,A., Pellizzari,L., Formisano,S., Pucillo,C. and Damante,G. (1998) Redox potential controls the structure and DNA binding activity of the paired domain. J. Biol. Chem., 273, 25062-25072.
15. Tell,G., Zecca,A., Pellizzari,L., Spessotto,P., Colombatti,A., Kelley,M.R., Damante,G. and Pucillo,C. (2000) An 'environment to nucleus' signaling system operates in B lymphocytes: Redox status modulates BSAP/Pax-5 activation through Ref-1 nuclear translocation. Nucleic Acids Res., 28, 1099-1105.
16. Gaiddon,C., Moorthy,N.C. and Prives,C. (1999) Ref-1 regulates the transactivation and pro-apoptotic functions of p53 in vivo. EMBO J. 18, 5609-5621.
17. Jayaraman,L., Murthy,K.G., Zhu,C., Curran,T., Xanthoudakis,S. and Prives,C. (1997) Identification of redox/repair protein Ref-1 as a potent activator of p53. Genes Dev., 11, 558-570.
18. Abate,C., Patel,L., Rauscher,F.J. III and Curran,T. (1990) Redox regulation of fos and jun DNA-binding activity in vitro. Science, 249, 1157-1161.
19. Matthews,J.R., Kaszubska,W., Turcatti,G., Wells,T.N. and Hay,R.T. (1993) Role of cysteine62 in DNA recognition by the P50 subunit of NF-kappa B. Nucleic Acids Res., 21, 1727-1734.
20. Mitomo,K., Nakayama,K., Fujimoto,K., Sun,X., Seki,S. and Yamamoto,K. (1994) Two different cellular redox systems regulate the DNA-binding activity of the p50 subunit of NF-kappa B in vitro. Gene, 145 197-203.
21. Toledano,M.B., Ghosh,D., Trinh,F. and Leonard,W.J. (1993) N-terminal DNA-binding domains contribute to differential DNA-binding specificities of NF-kappa B p50 and p65. Mol. Cell Biol., 13, 852-860.
22. Matthews,J.R., Wakasugi,N., Virelizier,J.L., Yodoi,J. and Hay,R.T. (1992) Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res., 20, 3821-3830.
23. Nishi,T., Shimizu,N., Hiramoto,M., Sato,I., Yamaguchi,Y., Hasegawa,M., Aizawa,S., Tanaka,H., Kataoka,K., Watanabe,H. et al. (2002) Spatial redox regulation of a critical cysteine residue of NF-kappa B in vivo. J. Biol. Chem., 277, 44548-44556.
24. Droge,W., Schulze-Osthoff, K., Mihm,S., Galter,D., Schenk,H., Eck,H.P., Roth,S. and Gmunder,H. (1994) Functions of glutathione and glutathione disulfide in immunology and immunopathology. FASEB J., 8, 1131-1138.
25. Thomas,J.A., Poland,B. and Honzatko,R. (1995) Protein sulfhydryls and their role in the antioxidant function of protein S-thiolation. Arch. Biochem. Biophys., 319, 1-9.
26. Dickinson,D.A. and Forman,H.J. (2002) Cellular glutathione and thiols metabolism. Biochem. Pharmacol., 64, 1019-1026.
27. Griffith,O.W. (1999) Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic. Biol. Med., 27, 922-935.
28. Kosower,N.S. and Kosower,E.M. (1978) The glutathione status of cells. Int. Rev. Cytol., 54, 109-160.
29. Meister,A. (1988) Glutathione metabolism and its selective modification. J. Biol. Chem., 263, 17205-17208.
30. Kobayashi-Miura,M., Shioji,K., Hoshino,Y., Masutani,H., Nakamura,H. and Yodoi, J. (2007) Oxygen sensing and redox signaling: The role of thioredoxin in embryonic development and cardiac diseases. Am. J. Physiol. Heart Circ. Physiol., 292, H2040-H2050.
31. Demple,B., Herman,T. and Chen,D.S. (1991) Cloning and expression of APE, the cDNA encoding the major human apurinic endonuclease: Definition of a family of DNA repair enzymes. Proc. Natl Acad. Sci. USA, 88, 11450-11454.
32. Robson,C.N. and Hickson,I.D. (1991) Isolation of cDNA clones encoding a human apurinic/apyrimidinic endonuclease that corrects DNA repair and mutagenesis defects in E. coli xth (exonuclease III) mutants. Nucleic Acids Res., 19 5519-5523.
33. Robson,C.N., Milne,A.M., Pappin,D.J. and Hickson,I.D. (1991) Isolation of cDNA clones encoding an enzyme from bovine cells that repairs oxidative DNA damage in vitro: Homology with bacterial repair enzymes. Nucleic Acids Res., 19, 1087-1092.
34. Shimizu,N., Sugimoto,K., Tang,J., Nishi,T., Sato,I., Hiramoto, M., Aizawa,S., Hatakeyama,M., Ohba,R., Hatori,H. et al. (2000) High-performance affinity beads for identifying drug receptors. Nat. Biotechnol., 18, 877-881.
35. Walker,L.J., Robson,C.N., Black,E., Gillespie,D. and Hickson,I.D. (1993) 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, 5370-5376.
36. Ordway,J.M., Eberhart,D. and Curran,T. (2003) Cysteine 64 of Ref-1 is not essential for redox regulation of AP-1 DNA binding. Mol. Cell Biol., 23, 4257-4266.
37. Gorman,M.A., Morera,S., Rothwell,D.G., de La Fortelle,E., Mol,C.D., Tainer,J.A., Hickson,I.D. and Freemont,P.S. (1997) The crystal structure of the human DNA repair endonuclease HAP1 suggests the recognition of extra-helical deoxyribose at DNA abasic sites. EMBO J., 16, 6548-6558.
38. Schreiber,E. and Schaffner,W. (1989) Long-range activation of transcription by SV40 enhancer is affected by 'inhibitory' or 'permissive' DNA sequences between enhancer and promoter. Somat. Cell Mol. Genet., 15, 591-603.
39. Hiramoto,M., Shimizu,N., Sugimoto,K., Tang,J., Kawakami,Y., Ito,M., Aizawa,S., Tanaka,H., Makino,I. and Handa,H. (1998) Nuclear targeted suppression of NF-kappa B activity by the novel quinone derivative E3330. J. Immunol., 160, 810-819.
40. Kataoka,K., Yoshitomo-Nakagawa,K., Shioda,S. and Nishizawa,M. (2001) A set of Hox proteins interact with the Maf oncoprotein to inhibit its DNA binding, transactivation, and transforming activities. J. Biol. Chem. 276, 819-826.
41. Liu,Y., Prasad,R., Beard,W.A., Kedar,P.S., Hou,E.W., Shock,D.D. and Wilson,S.H. (2007) Coordination of steps in single-nucleotide base excision repair mediated by apurinic/apyrimidinic endonuclease 1 and DNA polymerase beta. J. Biol. Chem., 282, 13532-13541.
42. Guan,Z., Basi,D., Li,Q., Mariash,A., Yia,Y.F., Geng,J.G., Kao,E. and Hall,J.L. (2005) Loss of redox factor 1 decreases NF-kappaB activity and increases susceptibility of endothelial cells to apoptosis. Arterioscler. Thromb. Vasc. Biol., 25, 96-101.
43. Hall,J.L., Wang,X., Van,A., Zhao,Y. and Gibbons,G.H. (2001) Overexpression of Ref-1 inhibits hypoxia and tumor necrosis factor-induced endothelial cell apoptosis through nuclear factor-kappab-independent and -dependent pathways. Circ. Res., 88, 1247-1253.
44. Watson,W.H., Yang,X., Choi,Y.E., Jones,D.P. and Kehrer,J.P. (2004) Thioredoxin and its role in toxicology. Toxicol. Sci., 78, 3-14.
45. Hirota,K., Matsui,M., Iwata,S., Nishiyama,A., Mori,K. and Yodoi,J. (1997) AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc. Natl Acad. Sci. USA 94, 3633-3638.
46. Qin,J., Clore,G.M., Kennedy,W.P., Kuszewski,J. and Gronenborn,A.M. (1996) The solution structure of human thioredoxin complexed with its target from Ref-1 reveals peptide chain reversal. Structure, 4 613-620.
47. Wei,S.J., Botero,A., Hirota,K., Bradbury,C.M., Markovina,S., Laszlo,A., Spitz,D.R., Goswami,P.C., Yodoi,J. and Gius,D. (2000) Thioredoxin nuclear translocation and interaction with redox factor-1 activates the activator protein-1 transcription factor in response to ionizing radiation. Cancer Res., 60, 6689-6695.
48. Xanthoudakis,S., Miao,G.G. and Curran,T. (1994) The redox and DNA-repair activities of Ref-1 are encoded by nonoverlapping domains. Proc. Natl Acad. Sci. USA, 91, 23-27.
49. Mantha,A.K., Oezguen,N., Bhakat,K.K., Izumi,T., Braun,W. and Mitra,S. (2008) Unusual role of a cysteine residue in substrate binding and activity of human AP-endonuclease 1. J. Mol. Biol., 379, 28-37.
50. Xanthoudakis,S., Smeyne,R.J., Wallace,J.D. and Curran,T. (1996) The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc. Natl Acad Sci. USA, 93, 8919-8923.
51. Daily,D., Vlamis-Gardikas,A., Offen,D., Mittelman,L., Melamed,E., Holmgren,A. and Barzilai,A. (2001) Glutaredoxin protects cerebellar granule neurons from dopamine-induced apoptosis by activating NF-kappa B via Ref-1. J. Biol. Chem., 276, 1335-1344.
52. Fung,H. and Demple,B. (2005) A vital role for Apel/Ref1 protein in repairing spontaneous DNA damage in human cells. Mol. Cell., 17 463-470.
53. Ramana,C.V., Boldogh,I., Izami,T. and Mitra,S. (1998) 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. USA, 95, 5061-5066.
54. Yang,S., Misner,B., Chiu,R. and Meyskens,F.L. Jr. (2007) Redox effector factor-1, combined with reactive oxygen species, plays an important role in the transformation of JB6 cells. Carcinogenesis, 28, 2382-2390.
55. Yao,K.S., Xanthoudakis,S., Curran,T. and O'Dwyer,P.J. (1994) Activation of AP-1 and of a nuclear redox factor, Ref-1, in the response of HT29 colon cancer cells to hypoxia. Mol. Cell Biol., 14, 5997-6003.
56. Flaherty,D.M., Monick,M.M., Carter,A.B., Peterson,M.W. and Hunninghake,G.W. (2002) Oxidant-mediated increases in redox factor-1 nuclear protein and activator protein-1 DNA binding in asbestos-treated macrophages. J. Immunol., 168, 5675-5681.