Inhibition of apurinic/apyrimidinic endonuclease I's redox activity revisited

Biochemistry

Volumn 52, Issue 17, 2013, Pages 2955-2966

  Zhang, Jun ^b   Luo, Meihua ^a   Marasco, Daniela ^c   Logsdon, Derek ^a   Lafavers, Kaice A ^a   Chen, Qiujia ^a   Reed, April ^a   Kelley, Mark R ^a   Gross, Michael L ^b   Georgiadis, Millie M ^a,d  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASE EXCISION REPAIRS; CANCER THERAPEUTICS; DIFFERENTIAL SCANNING FLUORIMETRY; ELECTROPHORETIC MOBILITY SHIFT; ENDONUCLEASE ACTIVITIES; HYDROGEN-DEUTERIUM EXCHANGE; NEGATIVELY CHARGED; REDOX REGULATION;

CARBOXYLATION; ELECTROPHORETIC MOBILITY; MASS SPECTROMETRY; MELTING POINT; PROTEINS; REDOX REACTIONS; REPAIR;

AMIDES;

AMIDE; APURINIC APYRIMIDINIC ENDONUCLEASE 1 PROTEIN; CARBOXYLIC ACID; CARBOXYLIC ACID DERIVATIVE; ENDONUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; ENZYME ACTIVITY; ENZYME INHIBITION; FLUOROMETRY; GEL MOBILITY SHIFT ASSAY; IN VITRO STUDY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; TEMPERATURE;

DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLUOROMETRY; MASS SPECTROMETRY; MODELS, MOLECULAR; OXIDATION-REDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84877054603     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400179m     Document Type: Article

References (54)

1. Luo, M., He, H., Kelley, M. R., and Georgiadis, M. M. (2010) Redox regulation of DNA repair: Implications for human health and cancer therapeutic development Antioxid. Redox Signaling 12, 1247-1269
2. Tell, G., Quadrifoglio, F., Tiribelli, C., and Kelley, M. R. (2009) The Many Functions of APE1/Ref-1: Not Only a DNA Repair Enzyme Antioxid. Redox Signaling 11, 601-620
3. Koukourakis, M. I., Giatromanolaki, A., Kakolyris, S., Sivridis, E., Georgoulias, V., Funtzilas, G., Hickson, I. D., Gatter, K. C., and Harris, A. L. (2001) 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. Radiat. Oncol., Biol., Phys. 50, 27-36
4. Kakolyris, S., Kaklamanis, L., Engels, K., Fox, S. B., Taylor, M., Hickson, I. D., Gatter, K. C., and Harris, A. L. (1998) Human AP endonuclease 1 (HAP1) protein expression in breast cancer correlates with lymph node status and angiogenesis Br. J. Cancer 77, 1169-1173
5. Robertson, K. A., Bullock, H. A., Xu, Y., Tritt, R., Zimmerman, E., Ulbright, T. M., Foster, R. S., Einhorn, L. H., and Kelley, M. R. (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
6. Fung, H. and Demple, B. (2005) A vital role for Ape1/Ref1 protein in repairing spontaneous DNA damage in human cells Mol. Cell 17, 463-470
7. Tell, G., Crivellato, E., Pines, A., Paron, I., Pucillo, C., Manzini, G., Bandiera, A., Kelley, M. R., Di Loreto, C., and Damante, G. (2001) Mitochondrial localization of APE/Ref-1 in thyroid cells Mutat. Res. 485, 143-152
8. Chattopadhyay, R., Wiederhold, L., Szczesny, B., Boldogh, I., Hazra, T. K., Izumi, T., and Mitra, S. (2006) Identification and characterization of mitochondrial abasic (AP)-endonuclease in mammalian cells Nucleic Acids Res. 34, 2067-2076
9. Tell, G. and Wilson, D. M., III (2010) Targeting DNA repair proteins for cancer treatment Cell. Mol. Life Sci. 67, 3569-3572
10. Kelley, M., Georgiadis, M., and Fishel, M. (2012) APE1/Ref-1 Role in Redox Signaling: Translational Applications of Targeting the Redox Function of the DNA Repair/Redox Protein APE1/Ref-1 Curr. Mol. Pharmacol. 5, 36-53
11. 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. U.S.A. 88, 11450-11454
12. 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
13. Bhakat, K. K., Yang, S. H., and Mitra, S. (2003) Acetylation of human AP-endonuclease 1, a critical enzyme in DNA repair and transcription regulation Methods Enzymol. 371, 292-300
14. 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. (2009) APE1/Ref-1 interacts with NPM1 within nucleoli and plays a role in the rRNA quality control process Mol. Cell. Biol. 29, 1834-1854
15. 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. U.S.A. 94, 3633-3638
16. 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, 6688-6695
17. Ziel, K. A., Campbell, C. C., Wilson, G. L., and Gillespie, M. N. (2004) Ref-1/Ape is critical for formation of the hypoxia-inducible transcriptional complex on the hypoxic resonse element of the rat pulmonary artery endothelial cell VEGF FASEB J. 18, 986-988
18. Gray, M. J., Zhang, J., Ellis, L. M., Semenza, G. L., Evans, D. B., Watowich, S. S., and Gallick, G. E. (2005) HIF-1α, STAT3, CBP/p300 and Ref-1/APE are components of a transcriptional complex that regulates Src-dependent hypoxia-induced expression of VEGF in pancreatic and prostate carcinomas Oncogene 24, 3110-3120
19. Pines, A., Perrone, L., Bivi, N., Romanello, M., Damante, G., Gulisano, M., Kelley, M. R., Quadrifoglio, F., and Tell, G. (2005) Activation of APE1/Ref-1 is dependent on reactive oxygen species generated after purinergic receptor stimulation by ATP Nucleic Acids Res. 33, 4379-4394
20. Pines, A., Bivi, N., Romanello, M., Damante, G., Kelley, M. R., Adamson, E. D., D'Andrea, P., Quadrifoglio, F., Moro, L., and Tell, G. (2005) Cross-regulation between Egr-1 and APE/Ref-1 during early response to oxidative stress in the human osteoblastic HOBIT cell line: Evidence for an autoregulatory loop Free Radical Res. 39, 269-281
21. 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
22. Madhusudan, S. and Hickson, I. D. (2005) DNA repair inhibition: A selective tumour targeting strategy Trends Mol. Med. 11, 503-511
23. Luo, M., Zhang, J., He, H., Su, D., Chen, Q., Gross, M. L., Kelley, M. R., and Georgiadis, M. M. (2012) Characterization of the redox activity and disulfide bond formation in apurinic/apyrimidinic endonuclease Biochemistry 51, 695-705
24. Kim, Y. J., Kim, D., Illuzzi, J. L., Delaplane, S., Su, D., Bernier, M., Gross, M. L., Georgiadis, M. M., and Wilson, D. M., III (2011) S-Glutathionylation of cysteine 99 in the APE1 protein impairs abasic endonuclease activity J. Mol. Biol. 414, 313-326
25. 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
26. Georgiadis, M., Luo, M., Gaur, R., Delaplane, S., Li, X., and Kelley, M. (2008) Evolution of the redox function in mammalian apurinic/apyrimidinic endonuclease Mutat. Res. 643, 54-63
27. Vascotto, C., Bisetto, E., Li, M., Zeef, L. A., D'Ambrosio, C., Domenis, R., Comelli, M., Delneri, D., Scaloni, A., Altieri, F., Mavelli, I., Quadrifoglio, F., Kelley, M. R., and Tell, G. (2011) Knock-in reconstitution studies reveal an unexpected role of Cys-65 in regulating APE1/Ref-1 subcellular trafficking and function Mol. Biol. Cell 22, 3887-3901
28. Shimizu, N., Sugimoto, K., Tang, J., Nishi, T., Sato, I., Hiramoto, M., Aizawa, S., Hatakeyama, M., Ohba, R., Hatori, H., Yoshikawa, T., Suzuki, F., Oomori, A., Tanaka, H., Kawaguchi, H., Watanabe, H., and Handa, H. (2000) High-performance affinity beads for identifying drug receptors Nat. Biotechnol. 18, 877-881
29. Su, D., Delaplane, S., Luo, M., Rempel, D. L., Vu, B., Kelley, M. R., Gross, M. L., and Georgiadis, M. M. (2011) Interactions of Apurinic/Apyrimidinic Endonuclease with a Redox Inhibitor: Evidence for an Alternate Conformation of the Enzyme Biochemistry 50, 82-92
30. Manvilla, B. A., Wauchope, O., Seley-Radtke, K. L., and Drohat, A. C. (2011) NMR studies reveal an unexpected binding site for a redox inhibitor of AP endonuclease 1 Biochemistry 50, 10540-10549
31. Li, M., Zhong, Z., Zhu, J., Xiang, D., Dai, N., Cao, X., Qing, Y., Yang, Z., Xie, J., Li, Z., Baugh, L., Wang, G., and Wang, D. (2010) Identification and characterization of mitochondrial targeting sequence of human apurinic/apyrimidinic endonuclease 1 J. Biol. Chem. 285, 14871-14881
32. Zhang, J., Chalmers, M. J., Stayrook, K. R., Burris, L. L., Garcia-Ordonez, R. D., Pascal, B. D., Burris, T. P., Dodge, J. A., and Griffin, P. R. (2010) Hydrogen/deuterium exchange reveals distinct agonist/partial agonist receptor dynamics within vitamin D receptor/retinoid X receptor heterodimer Structure 18, 1332-1341
33. Luo, M., Delaplane, S., Jiang, A., Reed, A., He, Y., Fishel, M., Nyland, R. L., II, Borch, R. F., Qiao, X., Georgiadis, M. M., and Kelley, M. R. (2008) Role of the multifunctional DNA repair and redox signaling protein Ape1/Ref-1 in cancer and endothelial cells: Small molecule inhibition of Ape1's redox functio Antioxid. Redox Signaling 10, 1853-1867
34. Wang, D., Luo, M., and Kelley, M. R. (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
35. Kelley, M. R., Luo, M., Reed, A., Su, D., Delaplane, S., Borch, R. F., Nyland, R. L., Gross, M. L., and Georgiadis, M. M. (2011) Functional Analysis of Novel Analogues of E3330 That Block the Redox Signaling Activity of the Multifunctional AP Endonuclease/Redox Signaling Enzyme APE1/Ref-1 Antioxid. Redox Signaling 14, 1387-1401
36. Kreklau, E. L., Limp-Foster, M., Liu, N., Xu, Y., Kelley, M. R., and Erickson, L. C. (2001) A novel fluorometric oligonucleotide assay to measure O(6)-methylguanine DNA methyltransferase, methylpurine DNA glycosylase, 8-oxoguanine DNA glycosylase and abasic endonuclease activities: DNA repair status in human breast carcinoma cells overexpressing methylpurine DNA glycosylase Nucleic Acids Res. 29, 2558-2566
37. Luo, M. and Kelley, M. R. (2004) Inhibition of the human apurinic/apyrimidinic endonuclease (APE1) repair activity and sensitization of breast cancer cells to DNA alkylating agents with lucanthone Anticancer Res. 24, 2127-2134
38. Bapat, A., Glass, L. S., Luo, M., Fishel, M. L., Long, E. C., Georgiadis, M. M., and Kelley, M. R. (2010) Novel small molecule inhibitor of Ape1 endonuclease blocks proliferation and reduces viability of glioblastoma cells J. Pharmacol. Exp. Ther. 334, 988-998
39. Gorman, M. A., Morera, S., Rothwell, D. G., 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
40. Beernink, P. T., Segelke, B. W., Hadi, M. Z., Erzberger, J. P., Wilson, D. M., III, and Rupp, B. (2001) Two divalent metal ions in the active site of a new crystal form of human apurinic/apyrimidinic endonuclease, Ape1: Implications for the catalytic mechanism J. Mol. Biol. 307, 1023-1034
41. Niesen, F. H., Berglund, H., and Vedadi, M. (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability Nat. Protoc. 2, 2212-2221
42. Nyland, R. L., Luo, M., Kelley, M. R., and Borch, R. F. (2010) Design and synthesis of novel quinone inhibitors targeted to the redox function of apurinic/apyrimidinic endonuclease 1/redox enhancing factor-1 (Ape1/ref-1) J. Med. Chem. 53, 1200-1210
43. Jiang, A., Gao, H., Kelley, M. R., and Qiao, X. (2011) Inhibition of APE1/Ref-1 Redox Activity with APX3330 Blocks Retinal Angiogenesis in vitro and in vivo Vision Res. 51, 93-100
44. Jedinak, A., Dudhgaonkar, S., Kelley, M. R., and Sliva, D. (2011) Apurinic/Apyrimidinic endonuclease 1 regulates inflammatory response in macrophages Anticancer Res. 31, 379-385
45. Jiang, Y., Zhou, S., Sandusky, G. E., Kelley, M. R., and Fishel, M. L. (2010) Reduced expression of DNA repair and redox signaling protein APE1/Ref-1 impairs human pancreatic cancer cell survival, proliferation, and cell cycle progression Cancer Invest. 28, 885-895
46. Fishel, M. L., Colvin, E. S., Luo, M., Kelley, M. R., and Robertson, K. A. (2010) Inhibition of the redox function of APE1/Ref-1 in myeloid leukemia cell lines results in a hypersensitive response to retinoic acid-induced differentiation and apoptosis Exp. Hematol. 38, 1178-1188
47. Jiang, Y., Guo, C., Fishel, M. L., Wang, Z.-Y., Vasko, M. R., and Kelley, M. R. (2009) Role of APE1 in differentiated neuroblastoma SH-SY5Y cells in response to oxidative stress: Use of APE1 small molecule inhibitors to delineate APE1 functions DNA Repair 8, 1273-1282
48. Jiang, Y., Guo, C., Vasko, M. R., and Kelley, M. R. (2008) Implications of Apurinic/Apyrimidinic Endonuclease in Reactive Oxygen Signaling Response after Cisplatin Treatment of Dorsal Root Ganglion Neurons Cancer Res. 68, 6425-6434
49. Fishel, M. L., He, Y., Reed, A. M., Chin-Sinex, H., Hutchins, G. D., Mendonca, M. S., and Kelley, M. R. (2008) Knockdown of the DNA repair and redox signaling protein Ape1/Ref-1 blocks ovarian cancer cell and tumor growth DNA Repair 7, 177-186
50. Zou, G. M., Luo, M. H., Reed, A., Kelley, M. R., and Yoder, M. C. (2007) Ape1 regulates hematopoietic differentiation of embryonic stem cells through its redox functional domain Blood 109, 1917-1922
51. Madhusudan, S., Smart, F., Shrimpton, P., Parsons, J. L., Gardiner, L., Houlbrook, S., Talbot, D. C., Hammonds, T., Freemont, P. A., Sternberg, M. J., Dianov, G. L., and Hickson, I. D. (2005) Isolation of a small molecule inhibitor of DNA base excision repair Nucleic Acids Res. 33, 4711-4724
52. Seiple, L. A., Cardellina, J. H., II, Akee, R., and Stivers, J. T. (2008) Potent inhibition of human apurinic/apyrimidinic endonuclease 1 by arylstibonic acids Mol. Pharmacol. 73, 669-677
53. Zawahir, Z., Dayam, R., Deng, J., Pereira, C., and Neamati, N. (2009) Pharmacophore guided discovery of small-molecule human apurinic/apyrimidinic endonuclease 1 inhibitors J. Med. Chem. 52, 20-32
54. Simeonov, A., Kulkarni, A., Dorjsuren, D., Jadhav, A., Shen, M., McNeill, D. R., Austin, C. P., and Wilson, D. M., III (2009) Identification and characterization of inhibitors of human apurinic/apyrimidinic endonuclease APE1 PLoS One 4, e5740