Regulatory role of human AP-endonuclease (APE1/Ref-1) in YB-1-mediated activation of the multidrug resistance gene MDR1

Molecular and Cellular Biology

Volumn 28, Issue 23, 2008, Pages 7066-7080

  Chattopadhyay, Ranajoy ^a   Das, Soumita ^a   Maiti, Amit K ^a   Boldogh, Istvan ^a   Xie, Jingwu ^b   Hazra, Tapas K ^a   Kohno, Kimitoshi ^c   Mitra, Sankar ^a   Bhakat, Kishor K ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DOXORUBICIN; MULTIDRUG RESISTANCE PROTEIN 1; Y BOX BINDING PROTEIN 1;

ACETYLATION; ARTICLE; CANCER CELL; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

ACETYLATION; CELL LINE, TUMOR; CISPLATIN; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; DOXORUBICIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; P-GLYCOPROTEIN; UP-REGULATION; Y-BOX-BINDING PROTEIN 1;

EID: 57349170258     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00244-08     Document Type: Article

References (66)

1. Bargou, R. C., K. Jurchott, C. Wagener, S. Bergmann, S. Metzner, K. Bommert, M. Y. Mapara, K. J. Winzer, M. Dietel, B. Dorken, and H. D. Royer. 1997. Nuclear localization and increased levels of transcription factor YB-1 in primary human breast cancers are associated with intrinsic MDR1 gene expression. Nat. Med. 3:447-450.
2. Bhakat, K. K., T. Izumi, S. H. Yang, T. K. Hazra, and S. Mitra. 2003. Role of acetylated human AP-endonuclease (APE1/Ref-1) in regulation of the parathyroid hormone gene. EMBO J. 22:6299-6309.
3. Bhakat, K. K., S. K. Mokkapati, I. Boldogh, T. K. Hazra, and S. Mitra. 2006. Acetylation of human 8-oxoguanine-DNA glycosylase by p300 and its role in 8-oxoguanine repair in vivo. Mol. Cell. Biol. 26:1654-1665.
4. Bobola, M. S., L. S. Finn, R. G. Ellenbogen, J. R. Geyer, M. S. Berger, J. M. Braga, E. H. Meade, M. E. Gross, and J. R. Silber. 2005. Apurinic/apyrimidinic endonuclease activity is associated with response to radiation and chemotherapy in medulloblastoma and primitive neuroectodermal tumors. Clin. Cancer Res. 11:7405-7414.
5. Boeckman, H. J., K. S. Trego, and J. J. Turchi. 2005. Cisplatin sensitizes cancer cells to ionizing radiation via inhibition of nonhomologous end joining. Mol. Cancer Res. 3:277-285.
6. Borst, P., and R. O. Elferink. 2002. Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 71:537-592.
7. Chattopadhyay, R., L. Wiederhold, B. Szczesny, I. Boldogh, T. K. Hazra, T. Izumi, and S. Mitra. 2006. Identification and characterization of mitochondrial abasic (AP)-endonuclease in mammalian cells. Nucleic Acids Res. 34:2067-2076.
8. Chaudhary, P. M., and I. B. Roninson. 1993. Induction of multidrug resistance in human cells by transient exposure to different chemotherapeutic drugs. J. Natl. Cancer Inst. 85:632-639.
9. Clarke, R., S. Currier, O. Kaplan, E. Lovelace, V. Boulay, M. M. Gottesman, and R. B. Dickson. 1992. Effect of P-glycoprotein expression on sensitivity to hormones in MCF-7 human breast cancer cells. J. Natl. Cancer Inst. 84:1506-1512.
10. Damia, G., L. Imperatori, M. Stefanini, and M. D'Incalci. 1996. Sensitivity of CHO mutant cell lines with specific defects in nucleotide excision repair to different anti-cancer agents. Int. J. Cancer 66:779-783.
11. Daviet, S., S. Couve-Privat, L. Gros, K. Shinozuka, H. Ide, M. Saparbaev, and A. A. Ishchenko. 2007. Major oxidative products of cytosine are substrates for the nucleotide incision repair pathway. DNA Repair (Amsterdam) 6:8-18.
12. Demple, B., and L. Harrison. 1994. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63:915-948.
13. Evans, A. R., M. Limp-Foster, and M. R. Kelley. 2000. Going APE over ref-1. Mutat. Res. 461:83-108.
14. Fantini, D., C. Vascotto, M. Deganuto, N. Bivi, S. Gustincich, G. Marcon, F. Quadrifoglio, G. Damante, K. K. Bhakat, S. Mitra, and G. Tell. 2008. APE1/Ref-1 regulates PTEN expression mediated by Egr-1. Free Radic. Res. 42:20-29.
15. Freitas, S., D. H. Moore, H. Michael, and M. R. Kelley. 2003. Studies of apurinic/apyrimidinic endonuclease/ref-1 expression in epithelial ovarian cancer: correlations with tumor progression and platinum resistance. Clin. Cancer Res. 9:4689-4694.
16. Fritz, G., S. Grosch, M. Tomicic, and B. Kaina. 2003. APE/Ref-1 and the mammalian response to genotoxic stress. Toxicology 193:67-78.
17. Fuchs, S., J. Philippe, P. Corvol, and F. Pinet. 2003. Implication of Ref-1 in the repression of renin gene transcription by intracellular calcium. J. Hypertens. 21:327-335.
18. Fujita, T., K. Ito, H. Izumi, M. Kimura, M. Sano, H. Nakagomi, K. Maeno, Y. Hama, K. Shingu, S. Tsuchiya, K. Kohno, and M. Fujimori. 2005. Increased nuclear localization of transcription factor Y-box binding protein 1 accompanied by up-regulation of P-glycoprotein in breast cancer pretreated with paclitaxel. Clin. Cancer Res. 11:8837-8844.
19. Gao, Z., Z. Gao, J. Z. Fields, and B. M. Boman. 1998. Co-transfection of MDR1 and MRP antisense RNAs abolishes the drug resistance in multidrug-resistant human lung cancer cells. Anticancer Res. 18:3073-3076.
20. Gottesman, M. M., T. Fojo, and S. E. Bates. 2002. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer 2:48-58.
21. Gros, L., A. A. Ishchenko, H. Ide, R. H. Elder, and M. K. Saparbaev. 2004. The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway. Nucleic Acids Res. 32:73-81.
22. Hang, B., A. Chenna, H. Fraenkel-Conrat, and B. Singer. 1996. An unusual mechanism for the major human apurinic/apyrimidinic (AP) endonuclease involving 5′ cleavage of DNA containing a benzene-derived exocyclic adduct in the absence of an AP site. Proc. Natl. Acad. Sci. USA 93:13737-13741.
23. Higashi, K., Y. Inagaki, K. Fujimori, A. Nakao, H. Kaneko, and I. Nakatsuka. 2003. Interferon-gamma interferes with transforming growth factor-beta signaling through direct interaction of YB-1 with Smad3. J. Biol. Chem. 278:43470-43479.
24. Higashi, K., Y. Inagaki, N. Suzuki, S. Mitsui, A. Mauviel, H. Kaneko, and I. Nakatsuka. 2003. Y-box-binding protein YB-1 mediates transcriptional repression of human alpha 2(I) collagen gene expression by interferon-gamma. J. Biol. Chem. 278:5156-5162.
25. Horton, J. K., G. Roy, J. T. Piper, B. Van Houten, Y. C. Awasthi, S. Mitra, M. A. Alaoui-Jamali, I. Boldogh, and S. S. Singhal. 1999. Characterization of a chlorambucil-resistant human ovarian carcinoma cell line overexpressing glutathione S-transferase mu. Biochem. Pharmacol. 58:693-702.
26. Ise, T., G. Nagatani, T. Imamura, K. Kato, H. Takano, M. Nomoto, H. Izumi, H. Ohmori, T. Okamoto, T. Ohga, T. Uchiumi, M. Kuwano, and K. Kohno. 1999. Transcription factor Y-box binding protein 1 binds preferentially to cisplatin-modified DNA and interacts with proliferating cell nuclear antigen. Cancer Res. 59:342-346.
27. Izumi, T., D. B. Brown, C. V. Naidu, K. K. Bhakat, M. A. Macinnes, H. Saito, D. J. Chen, and S. Mitra. 2005. Two essential but distinct functions of the mammalian abasic endonuclease. Proc. Natl. Acad. Sci. USA 102:5739-5743.
28. Izumi, T., and S. Mitra. 1998. Deletion analysis of human AP-endonuclease: minimum sequence required for the endonuclease activity. Carcinogenesis 19:525-527.
29. Izumi, T., L. R. Wiederhold, G. Roy, R. Roy, A. Jaiswal, K. K. Bhakat, S. Mitra, and T. K. Hazra. 2003. Mammalian DNA base excision repair proteins: their interactions and role in repair of oxidative DNA damage. Toxicology 193:43-65.
30. Jayaraman, L., N. C. Moorthy, K. G. Murthy, J. L. Manley, M. Bustin, and C. Prives. 1998. High mobility group protein-1 (HMG-1) is a unique activator of p53. Genes Dev. 12:462-472.
31. Jayaraman, L., K. G. Murthy, C. Zhu, T. Curran, S. Xanthoudakis, and C. Prives. 1997. Identification of redox/repair protein Ref-1 as a potent activator of p53. Genes Dev. 11:558-570.
32. Jiang, Y., C. Guo, M. R. Vasko, and M. R. Kelley. 2008. Implications of apurinic/apyrimidinic endonuclease in reactive oxygen signaling response after cisplatin treatment of dorsal root ganglion neurons. Cancer Res. 68:6425-6434.
33. Jin, S., and K. W. Scotto. 1998. Transcriptional regulation of the MDR1 gene by histone acetyltransferase and deacetylase is mediated by NF-Y. Mol. Cell. Biol. 18:4377-4384.
34. Kelley, M. R., L. Cheng, R. Foster, R. Tritt, J. Jiang, J. Broshears, and M. Koch. 2001. Elevated and altered expression of the multifunctional DNA base excision repair and redox enzyme Ape1/ref-1 in prostate cancer. Clin. Cancer Res. 7:824-830.
35. Kohno, K., H. Izumi, T. Uchiumi, M. Ashizuka, and M. Kuwano. 2003. The pleiotropic functions of the Y-box-binding protein, YB-1. Bioessays 25:691-698.
36. Kohno, K., S. Sato, H. Takano, K. Matsuo, and M. Kuwano. 1989. The direct activation of human multidrug resistance gene (MDR1) by anticancer agents. Biochem. Biophys. Res. Commun. 165:1415-1421.
37. Ludwig, D. L., M. A. MacInnes, Y. Takiguchi, P. E. Purtymun, M. Henrie, M. Flannery, J. Meneses, R. A. Pedersen, and D. J. Chen. 1998. A murine AP-endonuclease gene-targeted deficiency with post-implantation embryonic progression and ionizing radiation sensitivity. Mutat. Res. 409:17-29.
38. Marenstein, D. R., M. T. Ocampo, M. K. Chan, A. Altamirano, A. K. Basu, R. J. Boorstein, R. P. Cunningham, and G. W. Teebor. 2001. Stimulation of human endonuclease III by Y box-binding protein 1 (DNA-binding protein B). Interaction between a base excision repair enzyme and a transcription factor. J. Biol. Chem. 276:21242-21249.
39. Meira, L. B., D. L. Cheo, R. E. Hammer, D. K. Burns, A. Reis, and E. C. Friedberg. 1997. Genetic interaction between HAP1/REF-1 and p53. Nat. Genet. 17:145.
40. Mitra, S., T. Izumi, I. Boldogh, K. K. Bhakat, J. W. Hill, and T. K. Hazra. 2002. Choreography of oxidative damage repair in mammalian genomes. Free Radic. Biol. Med. 33:15-28.
41. Mol, C. D., T. Izumi, S. Mitra, and J. A. Tainer. 2000. DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination. Nature 403:451-456.
42. Nakshatri, H., P. Bhat-Nakshatri, and R. A. Currie. 1996. Subunit association and DNA binding activity of the heterotrimeric transcription factor NF-Y is regulated by cellular redox. J. Biol. Chem. 271:28784-28791.
43. Oda, Y., A. Sakamoto, N. Shinohara, T. Ohga, T. Uchiumi, K. Kohno, M. Tsuneyoshi, M. Kuwano, and Y. Iwamoto. 1998. Nuclear expression of YB-1 protein correlates with P-glycoprotein expression in human osteosarcoma. Clin. Cancer Res. 4:2273-2277.
44. Ogryzko, V. V., R. L. Schiltz, V. Russanova, B. H. Howard, and Y. Nakatani. 1996. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 87:953-959.
45. Ohga, T., K. Koike, M. Ono, Y. Makino, Y. Itagaki, M. Tanimoto, M. Kuwano, and K. Kohno. 1996. Role of the human Y box-binding protein YB-1 in cellular sensitivity to the DNA-damaging agents cisplatin, mitomycin C, and ultraviolet light. Cancer Res. 56:4224-4228.
46. Ohga, T., T. Uchiumi, Y. Makino, K. Koike, M. Wada, M. Kuwano, and K. Kohno. 1998. Direct involvement of the Y-box binding protein YB-1 in genotoxic stress-induced activation of the human multidrug resistance 1 gene. J. Biol. Chem. 273:5997-6000.
47. Okamoto, T., H. Izumi, T. Imamura, H. Takano, T. Ise, T. Uchiumi, M. Kuwano, and K. Kohno. 2000. Direct interaction of p53 with the Y-box binding protein, YB-1: a mechanism for regulation of human gene expression. Oncogene 19:6194-6202.
48. Okazaki, T., U. Chung, T. Nishishita, S. Ebisu, S. Usuda, S. Mishiro, S. Xanthoudakis, T. Igarashi, and E. Ogata. 1994. A redox factor protein, ref1, is involved in negative gene regulation by extracellular calcium. J. Biol. Chem. 269:27855-27862.
49. Puglisi, F., G. Aprile, A. M. Minisini, F. Barbone, P. Cataldi, G. Tell, M. R. Kelley, G. Damante, C. A. Beltrami, and C. Di Loreto. 2001. Prognostic significance of Ape1/ref-1 subcellular localization in non-small cell lung carcinomas. Anticancer Res. 21:4041-4049.
50. Ramana, C. V., I. Boldogh, T. Izumi, and S. Mitra. 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.
51. Robertson, K. A., H. A. Bullock, Y. Xu, R. Tritt, E. Zimmerman, T. M. Ulbright, R. S. Foster, L. H. Einhorn, and M. R. Kelley. 2001. Altered expression of Ape1/ref-1 in germ cell tumors and overexpression in NT2 cells confers resistance to bleomycin and radiation. Cancer Res. 61:2220-2225.
52. Robertson, K. A., D. P. Hill, Y. Xu, L. Liu, S. Van Epps, D. M. Hockenbery, J. R. Park, T. M. Wilson, and M. R. Kelley. 1997. Down-regulation of apurinic/apyrimidinic endonuclease expression is associated with the induction of apoptosis in differentiating myeloid leukemia cells. Cell Growth Differ. 8:443-449.
53. Roy, S., E. Kenny, S. Kennedy, A. Larkin, J. Ballot, M. Perez De Villarreal, J. Crown, and L. O'Driscoll. 2007. MDR1/P-glycoprotein and MRP-1 mRNA and protein expression in non-small cell lung cancer. Anticancer Res. 27:1325-1330.
54. Shibahara, K., T. Uchiumi, T. Fukuda, S. Kura, Y. Tominaga, Y. Maehara, K. Kohno, Y. Nakabeppu, T. Tsuzuki, and M. Kuwano. 2004. Targeted disruption of one allele of the Y-box binding protein-1 (YB-1) gene in mouse embryonic stem cells and increased sensitivity to cisplatin and mitomycin C. Cancer Sci. 95:348-353.
55. Shimizu, N., K. Sugimoto, J. Tang, T. Nishi, I. Sato, M. Hiramoto, S. Aizawa, M. Hatakeyama, R. Ohba, H. Hatori, T. Yoshikawa, F. Suzuki, A. Oomori, H. Tanaka, H. Kawaguchi, H. Watanabe, and H. Handa. 2000. High-performance affinity beads for identifying drug receptors. Nat. Biotechnol. 18:877-881.
56. Szczesny, B., K. K. Bhakat, S. Mitra, and I. Boldogh. 2004. Age-dependent modulation of DNA repair enzymes by covalent modification and subcellular distribution. Mech. Ageing Dev. 125:755-765.
57. Uchiumi, T., K. Kohno, H. Tanimura, K. Matsuo, S. Sato, Y. Uchida, and M. Kuwano. 1993. Enhanced expression of the human multidrug resistance 1 gene in response to UV light irradiation. Cell Growth Differ. 4:147-157.
58. Volm, M., R. Koomagi, J. Mattern, and T. Efferth. 2002. Protein expression profiles indicative for drug resistance of non-small cell lung cancer. Br. J. Cancer 87:251-257.
59. Walker, L. J., C. N. Robson, E. Black, D. Gillespie, and I. D. Hickson. 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.
60. Wang, D., M. Luo, and M. R. Kelley. 2004. Human apurinic endonuclease 1 (APE1) expression and prognostic significance in osteosarcoma: enhanced sensitivity of osteosarcoma to DNA damaging agents using silencing RNA APE1 expression inhibition. Mol. Cancer Ther. 3:679-686.
61. Wiederhold, L., J. B. Leppard, P. Kedar, F. Karimi-Busheri, A. Rasouli-Nia, M. Weinfeld, A. E. Tomkinson, T. Izumi, R. Prasad, S. H. Wilson, S. Mitra, and T. K. Hazra. 2004. AP endonuclease-independent DNA base excision repair in human cells. Mol. Cell 15:209-220.
62. Xanthoudakis, S., G. Miao, F. Wang, Y. C. Pan, and T. Curran. 1992. Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J. 11:3323-3335.
63. Xanthoudakis, S., R. J. Smeyne, J. D. Wallace, and T. Curran. 1996. The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc. Natl. Acad. Sci. USA 93:8919-8923.
64. Xu, Y., D. H. Moore, J. Broshears, L. Liu, T. M. Wilson, and M. R. Kelley. 1997. The apurinic/apyrimidinic endonuclease (APE/ref-1) DNA repair enzyme is elevated in premalignant and malignant cervical cancer. Anticancer Res. 17:3713-3719.
65. Yoo, D. G., Y. J. Song, E. J. Cho, S. K. Lee, J. B. Park, J. H. Yu, S. P. Lim, J. M. Kim, and B. H. Jeon. 2008. Alteration of APE1/ref-1 expression in non-small cell lung cancer: the implications of impaired extracellular superoxide dismutase and catalase antioxidant systems. Lung Cancer 60:277-284.
66. Zaky, A., C. Busso, T. Izumi, R. Chattopadhyay, A. Bassiouny, S. Mitra, and K. K. Bhakat. 2008. Regulation of the human AP-endonuclease (APE1/Ref-1) expression by the tumor suppressor p53 in response to DNA damage. Nucleic Acids Res. 36:1555-1566.