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

Volumn 8, Issue 11, 2009, Pages 1273-1282

  Jiang, Yanlin ^a   Guo, Chunlu ^a   Fishel, Melissa L ^a   Wang, Zheng Yu ^a   Vasko, Michael R ^a   Kelley, Mark R ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

APE1 Ref 1; Base excision repair (BER); Oxidative stress; Post mitotic cells; Small molecule inhibitors

Indexed keywords

3 [5 (2,3 DIMETHOXY 6 METHYL 1,4 BENZOQUINOYL)] 2 NONYL 2 PROPIONIC ACID; ADENOVIRUS VECTOR; ALANINE; CYSTEINE; DNA; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE 1; ENZYME INHIBITOR; HYDROGEN PEROXIDE; HYPOXANTHINE; MENADIONE; MESSENGER RNA; METHOXYAMINE; NEUROMODULIN; OXIDIZING AGENT; RETINOIC ACID; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; XANTHINE OXIDASE;

ADENOVIRUS 5; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL KILLING; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; DRUG CYTOTOXICITY; EXCISION REPAIR; FLOW CYTOMETRY; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; INTERPHASE; MITOSIS; NERVE CELL CULTURE; NEUROBLASTOMA CELL; NEUROBLASTOMA SH SY5Y CELL; NEUROPROTECTION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; HUMANS; HYDROGEN PEROXIDE; HYDROXYLAMINES; NEUROBLASTOMA; OXIDATIVE STRESS;

EID: 70349991252     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.08.003     Document Type: Article

References (56)

1. Fishel M.L., Vasko M.R., and Kelley M.R. DNA repair in neurons: so if they don't divide what's to repair?. Mutat. Res. 614 (2007) 24-36
2. Georgiadis M.M., Luo M., Gaur R.K., Delaplane S., Li X., and Kelley M.R. Evolution of the redox function in mammalian apurinic/apyrimidinic endonuclease. Mutat. Res. 643 (2008) 54-63
3. Luo M., Delaplane S., Jiang A., Reed A., He Y., Fishel M., Nyland Ii R.L., Borch R.F., Qiao X., Georgiadis M.M., and Kelley M.R. 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)
4. Wilson III D.M., and Mattson M.P. Neurodegeneration: nicked to death. Curr. Biol. 17 (2007) R55-58
5. Mura C.V., Delgado R., Aguirre P., Bacigalupo J., and Nunez M.T. Quiescence induced by iron challenge protects neuroblastoma cells from oxidative stress. J. Neurochem. 98 (2006) 11-19
6. Bains J.S., and Shaw C.A. Neurodegenerative disorders in humans: the role of glutathione in oxidative stress-mediated neuronal death. Brain Res. Brain Res. Rev. 25 (1997) 335-358
7. Olivieri G., Baysang G., Meier F., Muller-Spahn F., Stahelin H.B., Brockhaus M., and Brack C. N-acetyl-l-cysteine protects SHSY5Y neuroblastoma cells from oxidative stress and cell cytotoxicity: effects on beta-amyloid secretion and tau phosphorylation. J. Neurochem. 76 (2001) 224-233
8. Jiang Y., Guo C., Vasko M.R., and Kelley M.R. Implications of apurinic/apyrimidinic endonuclease in reactive oxygen signaling response after cisplatin treatment of dorsal root ganglion neurons. Cancer Res. 68 (2008) 6425-6434
9. Vasko M.R., Guo C., and Kelley M.R. The multifunctional DNA repair/redox enzyme Ape1/Ref-1 promotes survival of neurons after oxidative stress. DNA Repair (Amst.) 4 (2005) 367-379
10. Fung H., and Demple B. A vital role for Ape1/Ref1 protein in repairing spontaneous DNA damage in human cells. Mol. Cell 17 (2005) 463-470
11. Jeon B.H., and Irani K. APE1/Ref-1: versatility in progress. Antioxid. Redox Signal. (2008)
12. Sharma M., Sharma P., and Pant H.C. CDK-5-mediated neurofilament phosphorylation in SHSY5Y human neuroblastoma cells. J. Neurochem. 73 (1999) 79-86
13. Pahlman S., Mamaeva S., Meyerson G., Mattsson M.E., Bjelfman C., Ortoft E., and Hammerling U. Human neuroblastoma cells in culture: a model for neuronal cell differentiation and function. Acta Physiol. Scand Suppl. 592 (1990) 25-37
14. Tell G., Quadrifoglio F., Tiribelli C., and Kelley M.R. The many functions of APE1/Ref-1: not only a DNA repair enzyme. Antioxid. Redox Signal. (2008)
15. Izumi T., Schein C.H., Oezguen N., Feng Y., and Braun W. Effects of backbone contacts 3′ to the abasic site on the cleavage and the product binding by human apurinic/apyrimidinic endonuclease (APE1). Biochemistry 43 (2004) 684-689
16. Brewer G.J., Torricelli J.R., Evege E.K., and Price P.J. Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35 (1993) 567-576
17. Fishel M.L., He Y., Smith M.L., and Kelley M.R. Manipulation of base excision repair to sensitize ovarian cancer cells to alkylating agent temozolomide. Clin. Cancer Res. 13 (2007) 260-267
18. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 (2001) 402-408
19. Adem A., Mattsson M.E., Nordberg A., and Pahlman S. Muscarinic receptors in human SH-SY5Y neuroblastoma cell line: regulation by phorbol ester and retinoic acid-induced differentiation. Brain Res. 430 (1987) 235-242
20. Pahlman S., Ruusala A.I., Abrahamsson L., Mattsson M.E., and Esscher T. Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation. Cell Differ. 14 (1984) 135-144
21. Karns L.R., Ng S.C., Freeman J.A., and Fishman M.C. Cloning of complementary DNA for GAP-43, a neuronal growth-related protein. Science 236 (1987) 597-600
22. Bapat A., Fishel M., and Kelley M.R. Going Ape as an approach to cancer therapeutics. Antioxid. Redox Signal. (2008)
23. Liu L., Taverna P., Whitacre C.M., Chatterjee S., and Gerson S.L. Pharmacologic disruption of base excision repair sensitizes mismatch repair-deficient and -proficient colon cancer cells to methylating agents. Clin. Cancer Res. 5 (1999) 2908-2917
24. Fortini P., Calcagnile A., Vrieling H., van Zeeland A.A., Bignami M., and Dogliotti E. Mutagenic processing of ethylation damage in mammalian cells: the use of methoxyamine to study apurinic/apyrimidinic site-induced mutagenesis. Cancer Res. 53 (1993) 1149-1155
25. Shi M.M., Godleski J.J., and Paulauskis J.D. Regulation of macrophage inflammatory protein-1alpha mRNA by oxidative stress. J. Biol. Chem. 271 (1996) 5878-5883
26. Comporti M. Three models of free radical-induced cell injury. Chem. Biol. Interact. 72 (1989) 1-56
27. Kooij A. A re-evaluation of the tissue distribution and physiology of xanthine oxidoreductase. Histochem. J. 26 (1994) 889-915
28. Colpaert E.E., and Lefebvre R.A. Interaction of hypoxanthine/xanthine oxidase with nitrergic relaxation in the porcine gastric fundus. Br. J. Pharmacol. 130 (2000) 359-366
29. Kulkarni A., McNeill D.R., Gleichmann M., Mattson M.P., and Wilson III D.M. XRCC1 protects against the lethality of induced oxidative DNA damage in nondividing neural cells. Nucleic Acids Res. 36 (2008) 5111-5121
30. Fishel M.L., and Kelley M.R. The DNA base excision repair protein Ape1/Ref-1 as a therapeutic and chemopreventive target. Mol. Aspects Med. 28 (2007) 375-395
31. Kimura T., Sakaida I., Terai S., Matsumura Y., Uchida K., and Okita K. Inhibition of tumor necrosis factor-alpha production retards liver regeneration after partial hepatectomy in rats. Biochem. Biophys. Res. Commun. 231 (1997) 557-560
32. Nagakawa J., Hishinuma I., Miyamoto K., Hirota K., Abe S., Yamanaka T., Katayama K., and Yamatsu I. Protective effects of (2E)-3-[5-(2,3-dimethoxy-6-methyl-1,4-benzoquinoyl)]-2-nonyl-2-propenoic acid on endotoxin-mediated hepatitis in mice. J. Pharmacol. Exp. Ther. 262 (1992) 145-150
33. O'Hara A.M., Bhattacharyya A., Bai J., Mifflin R.C., Ernst P.B., Mitra S., and Crowe S.E. Tumor necrosis factor (TNF)-alpha-induced IL-8 expression in gastric epithelial cells: role of reactive oxygen species and AP endonuclease-1/redox factor (Ref)-1. Cytokine 46 (2009) 359-369
34. Tangpong J., Cole M.P., Sultana R., Joshi G., Estus S., Vore M., St Clair W., Ratanachaiyavong S., St Clair D.K., and Butterfield D.A. Adriamycin-induced, TNF-alpha-mediated central nervous system toxicity. Neurobiol. Dis. 23 (2006) 127-139
35. LoPresti P., Poluha W., Poluha D.K., Drinkwater E., and Ross A.H. Neuronal differentiation triggered by blocking cell proliferation. Cell Growth Differ. 3 (1992) 627-635
36. Mitra S., Izumi T., Boldogh I., Bhakat K.K., Chattopadhyay R., and Szczesny B. Intracellular trafficking and regulation of mammalian AP-endonuclease 1 (APE1), an essential DNA repair protein. DNA Repair (Amst.) 6 (2007) 461-469
37. Vascotto C., Cesaratto L., Zeef L.A., Deganuto M., D'Ambrosio C., Scaloni A., Romanello M., Damante G., Taglialatela G., Delneri D., Kelley M.R., Mitra S., Quadrifoglio F., and Tell G. Genome-wide analysis and proteomic studies reveal APE1/Ref-1 multifunctional role in mammalian cells. Proteomics 9 (2009) 1058-1074
38. Fishel M.L., He Y., Reed A.M., Chin-Sinex H., Hutchins G.D., Mendonca M.S., and Kelley M.R. Knockdown of the DNA repair and redox signaling protein Ape1/Ref-1 blocks ovarian cancer cell and tumor growth. DNA Repair (Amst.) 7 (2008) 177-186
39. Zou G.M., Luo M.H., Reed A., Kelley M.R., and Yoder M.C. Ape1 regulates hematopoietic differentiation of embryonic stem cells through its redox functional domain. Blood 109 (2007) 1917-1922
40. Laposa R.R., and Cleaver J.E. DNA repair on the brain. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 12860-12862
41. Friedberg E.C., and Meira L.B. Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage. Version 5. DNA Repair (Amst.) 2 (2003) 501-530
42. Kelley M.R., and Fishel M.L. DNA repair proteins as molecular targets for cancer therapeutics. Anticancer Agents Med. Chem. 8 (2008) 417-425
43. Pines A., Perrone L., Bivi N., Romanello M., Damante G., Gulisano M., Kelley M.R., Quadrifoglio F., and Tell G. Activation of APE1/Ref-1 is dependent on reactive oxygen species generated after purinergic receptor stimulation by ATP. Nucleic Acids Res. 33 (2005) 4379-4394
44. Evans A.R., Limp-Foster M., and Kelley M.R. Going APE over ref-1. Mutat. Res. 461 (2000) 83-108
45. Harrison J.F., Rinne M.L., Kelley M.R., Druzhyna N.M., Wilson G.L., and Ledoux S.P. Altering DNA base excision repair: use of nuclear and mitochondrial-targeted N-methylpurine DNA glycosylase to sensitize astroglia to chemotherapeutic agents. Glia 55 (2007) 1416-1425
46. Tell G., Damante G., Caldwell D., and Kelley M.R. The intracellular localization of APE1/Ref-1: more than a passive phenomenon?. Antioxid. Redox Signal. 7 (2005) 367-384
47. + channel in human endothelial cells via suppression of NADPH oxidase. Arch. Pharm. Res. 31 (2008) 1291-1301
48. Sossou M., Flohr-Beckhaus C., Schulz I., Daboussi F., Epe B., and Radicella J.P. APE1 overexpression in XRCC1-deficient cells complements the defective repair of oxidative single strand breaks but increases genomic instability. Nucleic Acids Res. 33 (2005) 298-306
49. Yan L., Bulgar A., Miao Y., Mahajan V., Donze J.R., Gerson S.L., and Liu L. Combined treatment with temozolomide and methoxyamine: blocking apurininc/pyrimidinic site repair coupled with targeting topoisomerase IIalpha. Clin. Cancer Res. 13 (2007) 1532-1539
50. Liu L., and Gerson S.L. Therapeutic impact of methoxyamine: blocking repair of abasic sites in the base excision repair pathway. Curr. Opin. Investig. Drugs 5 (2004) 623-627
51. Liu L., Yan L., Donze J.R., and Gerson S.L. Blockage of abasic site repair enhances antitumor efficacy of 1,3-bis-(2-chloroethyl)-1-nitrosourea in colon tumor xenografts. Mol. Cancer Ther. 2 (2003) 1061-1066
52. 2-induced injury by 2,3-dimethoxy-1,4-naphthoquinone. Free Radic. Biol. Med. 15 (1993) 57-67
53. Chang M., Shi M., and Forman H.J. Exogenous glutathione protects endothelial cells from menadione toxicity. Am. J. Physiol. 262 (1992) L637-643
54. Nagakawa J., Hirota K., Hishinuma I., Miyamoto K., Sonoda J., Yamanaka T., Katayama K., and Yamatsu I. Protective effect of E3330, a novel quinone derivative, in galactosamine-induced hepatitis in rats. J. Pharmacol. Exp. Ther. 264 (1993) 496-500
55. Huang Y., Erdmann N., Peng H., Zhao Y., and Zheng J. The role of TNF related apoptosis-inducing ligand in neurodegenerative diseases. Cell Mol. Immunol. 2 (2005) 113-122
56. Hiramoto M., Shimizu N., Sugimoto K., Tang J., Kawakami Y., Ito M., Aizawa S., Tanaka H., Makino I., and Handa H. Nuclear targeted suppression of NF-kappa B activity by the novel quinone derivative E3330. J. Immunol. 160 (1998) 810-819