Identification of a novel potential antitumor activity of gossypol as an APE1/Ref-1 inhibitor

Drug Design, Development and Therapy

Volumn 8, Issue , 2014, Pages 485-496

  Qian, Chengyuan ^a   Li, Mengxia ^a   Sui, Jiangdong ^a   Ren, Tao ^a   Li, Zheng ^a   Zhang, Liang ^a   Zhou, Liwei ^a   Cheng, Yi ^a   Wang, Dong ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

BH3 mimetic; Cancer; Oxidative DNA damage

Indexed keywords

DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; GOSSYPOL; PROTEIN BCL 2; REDOX EFFECTOR FACTOR 1; ANTINEOPLASTIC AGENT; APEX1 PROTEIN, HUMAN; CISPLATIN;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL LINE; CANCER GROWTH; CELL DEATH; CELL VIABILITY; DNA BINDING; DNA REPAIR; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; INTERFEROMETRY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG SCREENING; HELA CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CISPLATIN; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; GOSSYPOL; HELA CELLS; HUMANS; MICE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84900399095     PISSN: 11778881     EISSN: None     Source Type: Journal    
DOI: 10.2147/DDDT.S62963     Document Type: Article

References (52)

1. Xanthoudakis S, Curran T. Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity. EMBO J. 1992;11(2):653-665.
2. Robson CN, Hickson ID. Isolation of cDNA clones encoding a human apurinic/apyrimidinic endonuclease that corrects DNA repair and muta-genesis defects in E. coli xth (exonuclease III) mutants. Nucleic Acids Res. 1991;19(20):5519-5523.
3. Demple B, Herman T, Chen DS. Cloning and expression of APE, the cDNA encoding the major human apurinic endonuclease: defnition of a family of DNA repair enzymes. Proc Natl Acad Sci U S A. 1991;88(24): 11450-11454.
4. Helleday T, Petermann E, Lundin C, Hodgson B, Sharma RA. DNA repair pathways as targets for cancer therapy. Nat Rev Cancer. 2008;8(3): 193-204.
5. Xanthoudakis S, Curran T. Redox regulation of AP-1: a link between transcription factor signaling and DNA repair. Adv Exp Med Biol. 1996;387:69-75.
6. Tell G, Damante G, Caldwell D, Kelley MR. The intracellular localization of APE1/Ref-1: more than a passive phenomenon? Antioxid Redox Signal. 2005;7(3-4):367-384.
7. Li Y, Li S, Wu Z, et al. Polymorphisms in genes of APE1, PARP1, and XRCC1: risk and prognosis of colorectal cancer in a northeast Chinese population. Med Oncol. 2013;30(2):505.
8. Cun Y, Dai N, Xiong C, et al. Silencing of APE1 enhances sensitivity of human hepatocellular carcinoma cells to radiotherapy in vitro and in a xenograft model. PLoS One. 2013;8(2):e55313.
9. Wu HH, Chu YC, Wang L, et al. Cytoplasmic Ape1 expression elevated by p53 aberration may predict survival and relapse in resected non-small cell lung cancer. Ann Surg Oncol. 2013;20 Suppl 3:S336-S347.
10. Sheng Q, Zhang Y, Wang R, et al. Prognostic signifcance of APE1 cytoplasmic localization in human epithelial ovarian cancer. Med Oncol. 2012;29(2):1265-1271.
11. Kim JS, Kim JM, Liang ZL, et al. Prognostic signifcance of human apurinic/apyrimidinic endonuclease (APE/Ref-1) expression in rectal cancer treated with preoperative radiochemotherapy. Int J Radiat Oncol Biol Phys. 2012;82(1):130-137.
12. Qing Y, Yang XQ, Zhong Z Y, et al. Microarray analysis of DNA damage repair gene expression profiles in cervical cancer cells radioresistant to 252Cf neutron and X-rays. BMC Cancer. 2010;10:71.
13. Wang D, Luo M, Kelley MR. Human apurinic endonuclease 1 (APE1) expression and prognostic signifcance in osteosarcoma: enhanced sensitivity of osteosarcoma to DNA damaging agents using silencing RNA APE1 expression inhibition. Mol Cancer Ther. 2004;3(6): 679-686.
14. Al-Attar A, Gossage L, Fareed KR, et al. Human apurinic/ apyrimidinic endonuclease (APE1) is a prognostic factor in ovarian, gastro- oesophageal and pancreatico-biliary cancers. Br J Cancer. 2010;102(4): 704-709.
15. Xie J Y, Li MX, Xiang DB, et al. Elevated expression of APE1/Ref-1 and its regulation on IL-6 and IL-8 in bone marrow stromal cells of multiple myeloma. Clin Lymphoma Myeloma Leuk. 2010;10(5):385-393.
16. Kelley MR, Cheng L, Foster R, et al. Elevated and altered expression of the multifunctional DNA base excision repair and redox enzyme Ape1/ref-1 in prostate cancer. Clin Cancer Res. 2001;7(4):824-830.
17. Robertson KA, Bullock HA, Xu Y, et al. Altered expression of Ape1/ref-1 in germ cell tumors and overexpression in NT2 cells confers resistance to bleomycin and radiation. Cancer Res. 2001;61(5):2220-2225.
18. Luo M, He H, Kelley MR, Georgiadis MM. Redox regulation of DNA repair: implications for human health and cancer therapeutic development. Antioxid Redox Signal. 2010;12(11):1247-1269.
19. Luo M, Delaplane S, Jiang A, et al. Role of the multifunctional DNA repair and redox signaling protein Ape1/Ref-1 in cancer and endothelial cells: small-molecule inhibition of the redox function of Ape1. Antioxid Redox Signal. 2008;10(11):1853-1867.
20. Xie K, Wei D, Huang S. Transcriptional anti-angiogenesis therapy of human pancreatic cancer. Cytokine Growth Factor Rev. 2006;17(3): 147-156.
21. Li M, and Wilson DM. Human apurinic/apyrimidinic endonuclease 1. Antioxid Redox Signal. 2014;20(4):678-707.
22. Kelley MR, Georgiadis MM, Fishel ML. 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. 2012;5(1):36-53.
23. Al-Saf RI, Odde S, Shabaik Y, Neamati N. Small-molecule inhibitors of APE1 DNA repair function: an overview. Curr Mol Pharmacol. 2012;5(1):14-35.
24. Yang S, Irani K, Heffron SE, Jurnak F, Meyskens FL. Alterations in the expression of the apurinic/apyrimidinic endonuclease-1/redox factor-1 (APE/Ref-1) in human melanoma and identifcation of the therapeutic potential of resveratrol as an APE/Ref-1 inhibitor. Mol Cancer Ther. 2005;4(12):1923-1935.
25. Shimizu N, Sugimoto K, Tang J, et al. High-performance affnity beads for identifying drug receptors. Nat Biotechnol. 2000;18(8):877-881.
26. Kelley MR, Luo M, Reed A, et al. 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 Signal. 2011;14(8):1387-1401.
27. Nyland RL, Luo M, Kelley MR, Borch RF. 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. 2010;53(3):1200-1210.
28. Lin YC, Chitcharoenthum M, Rikihisa Y. Effect of gossypol on spermatozoal lactate dehydrogenase-X (LDH-X) in male rats. Contraception. 1987;36(5):581-592.
29. Le Blanc M, Russo J, Kudelka A P, Smith JA. An in vitro study of inhibitory activity of gossypol, a cottonseed extract, in human carcinoma cell lines. Pharmacol Res. 2002;46(6):551-555.
30. Band V, Hoffer A P, Band H, et al. Antiproliferative effect of gossypol and its optical isomers on human reproductive cancer cell lines. Gynecol Oncol. 1989;32(3):273-277.
31. Tuszynski G P, Cossu G. Differential cytotoxic effect of gossypol on human melanoma, colon carcinoma, and other tissue culture cell lines. Cancer Res. 1984;44(2):768-771.
32. Dodou K, Anderson RJ, Small DA, Groundwater PW. Investigations on gossypol: past and present developments. Expert Opin Investig Drugs. 2005;14(11):1419-1434.
33. Kitada S, Leone M, Sareth S, Zhai D, Reed JC, Pellecchia M. Discovery, characterization, and structure-activity relationships studies of proapoptotic polyphenols targeting B-cell lymphocyte/leukemia-2 proteins. J Med Chem. 2003;46(20):4259-4264.
34. Zhao J, Gao F, Zhang Y, Wei K, Liu Y, Deng X. Bcl2 inhibits abasic site repair by down-regulating APE1 endonuclease activity. J Biol Chem. 2008;283(15):9925-9932.
35. Li M, Vascotto C, Xu S, et al. Human AP endonuclease/redox factor APE1/ref-1 modulates mitochondrial function after oxidative stress by regulating the transcriptional activity of NRF1. Free Radic Biol Med. 2012;53(2):237-248.
36. Li MX, Wang D, Zhong Z Y, et al. Targeting truncated APE1 in mitochondria enhances cell survival after oxidative stress. Free Radic Biol Med. 2008;45(5):592-601.
37. Wilson DM, Takeshita M, Demple B. A basic site binding by the human apurinic endonuclease, Ape, and determination of the DNA contact sites. Nucleic Acids Res. 1997;25(5):933-939.
38. Swann MJ, Peel LL, Carrington S, Freeman NJ. Dual-polarization interferometry: an analytical technique to measure changes in protein structure in real time, to determine the stoichiometry of binding events, and to differentiate between specifc and nonspecific interactions. Anal Biochem. 2004;329(2):190-198.
39. Karim K, Taylor JD, Cullen DC, Swann MJ, Freeman NJ. Measurement of conformational changes in the structure of transglutaminase on binding calcium ions using optical evanescent dual polarisation interferometry. Anal Chem. 2007;79(8):3023-3031.
40. Chen DS, Herman T, Demple B. Two distinct human DNA diesterases that hydrolyze 3 ′-blocking deoxyribose fragments from oxidized DNA. Nucleic Acids Res. 1991;19(21):5907-5914.
41. Tell G, Quadrifoglio F, Tiribelli C, Kelley MR. The many functions of APE1/Ref-1: not only a DNA repair enzyme. Antioxid Redox Signal. 2009;11(3):601-620.
42. Vascotto C, Bisetto E, Li M, et al. Knock-in reconstitution studies reveal an unexpected role of Cys-65 in regulating APE1/Ref-1 subcellular traffcking and function. Mol Biol Cell. 2011;22(20):3887-3901.
43. Hu F, Mah K, Teramura DJ. Gossypol effects on cultured normal and malignant melanocytes. In Vitro Cell Dev Biol. 1986;22(10):583-588.
44. Yeow WS, Baras A, Chua A, et al. Gossypol, a phytochemical with BH3-mimetic property, sensitizes cultured thoracic cancer cells to Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand. J Thorac Cardiovasc Surg. 2006;132(6):1356-1362.
45. Van Poznak C, Seidman AD, Reidenberg MM, et al. Oral gossypol in the treatment of patients with refractory metastatic breast cancer: a phase I/II clinical trial. Breast Cancer Res Treat. 2001;66(3):239-248.
46. Parsons JL, Dianova II, Dianov GL. APE1 is the major 3 ′-phosphoglycolate activity in human cell extracts. Nucleic Acids Res. 2004;32(12): 3531-3536.
47. Vascotto C, Cesaratto L, Zeef LA, et al. Genome-wide analysis and proteomic studies reveal APE1/Ref-1 multifunctional role in mammalian cells. Proteomics. 2009;9(4):1058-1074.
48. Huang YW, Wang LS, Chang HL, et al. Molecular mechanisms of (-)-gossypol-induced apoptosis in human prostate cancer cells. Anticancer Res. 2006;26(3A):1925-1933.
49. Volate SR, Kawasaki BT, Hurt EM, et al. Gossypol induces apoptosis by activating p53 in prostate cancer cells and prostate tumor-initiating cells. Mol Cancer Ther. 2010;9(2):461-470.
50. Sung B, Ravindran J, Prasad S, Pandey MK, Aggarwal BB. Gossypol induces death receptor-5 through activation of the ROS-ERK-CHOP pathway and sensitizes colon cancer cells to TRAIL. J Biol Chem. 2010; 285(46):35418-35427.
51. Wang Y, Lonard DM, Yu Y, Chow DC, Palzkill TG, O'Malley BW. Small molecule inhibition of the steroid receptor coactivators, SRC-3 and SRC-1. Mol Endocrinol. 2011;25(12):2041-2053.
52. Carrero P, Okamoto K, Coumailleau P, O'Brien S, Tanaka H, Poellinger L. Redox-regulated recruitment of the transcriptional coacti-vators CREB-binding protein and SRC-1 to hypoxia-inducible factor 1 alpha. Mol Cell Biol. 2000;20(1):402-415.