Redox Regulation in the Base Excision Repair Pathway: Old and New Players as Cancer Therapeutic Targets

Aleksandra       Rajapakse; Amila      Suraweera; Didier      Boucher; Ali       Naqi; Kenneth      O'Byrne; Derek    J.   Richard; Laura    V.   Croft
doi:10.2174/0929867326666190430092732
Abstract

Background: Reactive Oxygen Species (ROS) are by-products of normal cellular metabolic processes, such as mitochondrial oxidative phosphorylation. While low levels of ROS are important signalling molecules, high levels of ROS can damage proteins, lipids and DNA. Indeed, oxidative DNA damage is the most frequent type of damage in the mammalian genome and is linked to human pathologies such as cancer and neurodegenerative disorders. Although oxidative DNA damage is cleared predominantly through the Base Excision Repair (BER) pathway, recent evidence suggests that additional pathways such as Nucleotide Excision Repair (NER) and Mismatch Repair (MMR) can also participate in clearance of these lesions. One of the most common forms of oxidative DNA damage is the base damage 8-oxoguanine (8-oxoG), which if left unrepaired may result in G:C to A:T transversions during replication, a common mutagenic feature that can lead to cellular transformation.
Objective: Repair of oxidative DNA damage, including 8-oxoG base damage, involves the functional interplay between a number of proteins in a series of enzymatic reactions. This review describes the role and the redox regulation of key proteins involved in the initial stages of BER of 8-oxoG damage, namely Apurinic/Apyrimidinic Endonuclease 1 (APE1), human 8-oxoguanine DNA glycosylase-1 (hOGG1) and human single-stranded DNA binding protein 1 (hSSB1). Moreover, the therapeutic potential and modalities of targeting these key proteins in cancer are discussed.
Conclusion: It is becoming increasingly apparent that some DNA repair proteins function in multiple repair pathways. Inhibiting these factors would provide attractive strategies for the development of more effective cancer therapies.
Keywords: ROS, BER, APE1, hOGG1, hSSB1/NABP2/OBFC2B, DNA repair, cancer therapeutics.
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[1] 
Finkel, T. Reactive oxygen species and signal transduction. IUBMB Life,  2001, 52(1-2), 3-6.
[http://dx.doi.org/10.1080/15216540252774694] [PMID: 11795590] 
[2] 
Finkel, T. Oxidant signals and oxidative stress. Curr. Opin. Cell Biol.,  2003, 15(2), 247-254.
[http://dx.doi.org/10.1016/S0955-0674(03)00002-4] [PMID: 12648682] 
[3] 
Reczek, C.R.; Chandel, N.S. ROS-dependent signal transduction. Curr. Opin. Cell Biol.,  2015, 33, 8-13.
[http://dx.doi.org/10.1016/j.ceb.2014.09.010] [PMID: 25305438] 
[4] 
David, S.S.; O’Shea, V.L.; Kundu, S. Base-excision repair of oxidative DNA damage. Nature,  2007, 447(7147), 941-950.
[http://dx.doi.org/10.1038/nature05978] [PMID: 17581577] 
[5] 
Mikhed, Y.; Daiber, A.; Steven, S. Mitochondrial Oxidative Stress, Mitochondrial DNA Damage and Their Role in Age-Related Vascular Dysfunction. Int. J. Mol. Sci.,  2015, 16(7), 15918-15953.
[http://dx.doi.org/10.3390/ijms160715918] [PMID: 26184181] 
[6] 
Cadet, J.; Wagner, J.R. DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb. Perspect. Biol.,  2013, 5(2)a012559
[http://dx.doi.org/10.1101/cshperspect.a012559] [PMID: 23378590] 
[7] 
Moloney, J.N.; Cotter, T.G. ROS signalling in the biology of cancer. Semin. Cell Dev. Biol., 2017.
[PMID: 28587975] 
[8] 
Ward, J.P.T. From Physiological Redox Signalling to Oxidant Stress. Adv. Exp. Med. Biol.,  2017, 967, 335-342.
[http://dx.doi.org/10.1007/978-3-319-63245-2_21] [PMID: 29047097] 
[9] 
Gibellini, L.; Pinti, M.; Nasi, M.; De Biasi, S.; Roat, E.; Bertoncelli, L.; Cossarizza, A. Interfering with ROS Metabolism in Cancer Cells: The Potential Role of Quercetin. Cancers (Basel),  2010, 2(2), 1288-1311.
[http://dx.doi.org/10.3390/cancers2021288] [PMID: 24281116] 
[10] 
Phaniendra, A.; Jestadi, D.B.; Periyasamy, L. Free radicals: properties, sources, targets, and their implication in various diseases. Indian J. Clin. Biochem.,  2015, 30(1), 11-26.
[http://dx.doi.org/10.1007/s12291-014-0446-0] [PMID: 25646037] 
[11] 
Dröge, W. Free radicals in the physiological control of cell function. Physiol. Rev.,  2002, 82(1), 47-95.
[http://dx.doi.org/10.1152/physrev.00018.2001] [PMID: 11773609] 
[12] 
Finkel, T. Signal transduction by reactive oxygen species. J. Cell Biol.,  2011, 194(1), 7-15.
[http://dx.doi.org/10.1083/jcb.201102095] [PMID: 21746850] 
[13] 
Giles, G.I. The redox regulation of thiol dependent signaling pathways in cancer. Curr. Pharm. Des.,  2006, 12(34), 4427-4443.
[http://dx.doi.org/10.2174/138161206779010549] [PMID: 17168752] 
[14] 
Nohl, H.; Breuninger, V.; Hegner, D. Influence of mitochondrial radical formation on energy-linked respiration. Eur. J. Biochem.,  1978, 90(2), 385-390.
[http://dx.doi.org/10.1111/j.1432-1033.1978.tb12615.x] [PMID: 710436] 
[15] 
Slupphaug, G.; Kavli, B.; Krokan, H.E. The interacting pathways for prevention and repair of oxidative DNA damage. Mutat. Res.,  2003, 531(1-2), 231-251.
[http://dx.doi.org/10.1016/j.mrfmmm.2003.06.002] [PMID: 14637258] 
[16] 
Storr, S.J.; Woolston, C.M.; Zhang, Y.; Martin, S.G. Redox environment, free radical, and oxidative DNA damage. Antioxid. Redox Signal.,  2013, 18(18), 2399-2408.
[http://dx.doi.org/10.1089/ars.2012.4920] [PMID: 23249296] 
[17] 
Halliwell, B. Oxidants and human disease: some new concepts. FASEB J.,  1987, 1(5), 358-364.
[http://dx.doi.org/10.1096/fasebj.1.5.2824268] [PMID: 2824268] 
[18] 
Keyer, K.; Imlay, J.A. Superoxide accelerates DNA damage by elevating free-iron levels. Proc. Natl. Acad. Sci. USA,  1996, 93(24), 13635-13640.
[http://dx.doi.org/10.1073/pnas.93.24.13635] [PMID: 8942986] 
[19] 
Raftery, M. J.   Determination of oxidative protein modifications
  using mass spectrometry. Redox report : communications
  in free radical research, 2014, 19(4), 140-7.
[20] 
Sun, Q.A.; Wu, Y.; Zappacosta, F.; Jeang, K.T.; Lee, B.J.; Hatfield, D.L.; Gladyshev, V.N. Redox regulation of cell signaling by selenocysteine in mammalian thioredoxin reductases. J. Biol. Chem.,  1999, 274(35), 24522-24530.
[http://dx.doi.org/10.1074/jbc.274.35.24522] [PMID: 10455115] 
[21] 
Herold, S.; Röck, G. Mechanistic studies of S-nitrosothiol formation by NO*/O2 and by NO*/methemoglobin. Arch. Biochem. Biophys.,  2005, 436(2), 386-396.
[http://dx.doi.org/10.1016/j.abb.2005.02.013] [PMID: 15797251] 
[22] 
Yuan, K.; Liu, Y.; Chen, H.N.; Zhang, L.; Lan, J.; Gao, W.; Dou, Q.; Nice, E.C.; Huang, C. Thiol-based redox proteomics in cancer research. Proteomics,  2015, 15(2-3), 287-299.
[http://dx.doi.org/10.1002/pmic.201400164] [PMID: 25251260] 
[23] 
Linke, K.; Jakob, U. Not every disulfide lasts forever: disulfide bond formation as a redox switch. Antioxid. Redox Signal.,  2003, 5(4), 425-434.
[http://dx.doi.org/10.1089/152308603768295168] [PMID: 13678530] 
[24] 
Blokhina, O.; Virolainen, E.; Fagerstedt, K.V. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot.,  2003, 91(2), 179-194.
[http://dx.doi.org/10.1093/aob/mcf118] [PMID: 12509339] 
[25] 
He, L.; He, T.; Farrar, S.; Ji, L.; Liu, T.; Ma, X.  Antioxidants
 Maintain Cellular Redox Homeostasis by Elimination
 of Reactive Oxygen Species. Cellular physiology and biochemistry
 : int. j. of exper. Cellu. physio., biochemistry, and
pharmacology, 2017, 44(2), 532-553.
[26] 
Papp, L.V.; Holmgren, A.; Khanna, K.K. Selenium and selenoproteins in health and disease. Antioxid. Redox Signal.,  2010, 12(7), 793-795.
[http://dx.doi.org/10.1089/ars.2009.2973] [PMID: 19905883] 
[27] 
Papp, L.V.; Lu, J.; Holmgren, A.; Khanna, K.K. From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid. Redox Signal.,  2007, 9(7), 775-806.
[http://dx.doi.org/10.1089/ars.2007.1528] [PMID: 17508906] 
[28] 
Mariotti, M.; Ridge, P.G.; Zhang, Y.; Lobanov, A.V.; Pringle, T.H.; Guigo, R.; Hatfield, D.L.; Gladyshev, V.N. Composition and evolution of the vertebrate and mammalian selenoproteomes. PLoS One,  2012, 7(3)e33066
[http://dx.doi.org/10.1371/journal.pone.0033066] [PMID: 22479358] 
[29] 
Luo, M.; He, H.; Kelley, M.R.; Georgiadis, M.M. Redox regulation of DNA repair: implications for human health and cancer therapeutic development. Antioxid. Redox Signal.,  2010, 12(11), 1247-1269.
[http://dx.doi.org/10.1089/ars.2009.2698] [PMID: 19764832] 
[30] 
Kalinina, E.V.; Chernov, N.N.; Novichkova, M.D. Role of glutathione, glutathione transferase, and glutaredoxin in regulation of redox-dependent processes. Biochemistry (Mosc.),  2014, 79(13), 1562-1583.
[http://dx.doi.org/10.1134/S0006297914130082] [PMID: 25749165] 
[31] 
Lu, J.; Holmgren, A. The thioredoxin antioxidant system. Free Radic. Biol. Med.,  2014, 66, 75-87.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.07.036] [PMID: 23899494] 
[32] 
Lu, J.; Holmgren, A. The thioredoxin superfamily in oxidative protein folding. Antioxid. Redox Signal.,  2014, 21(3), 457-470.
[http://dx.doi.org/10.1089/ars.2014.5849] [PMID: 24483600] 
[33] 
Ghezzi, P. Regulation of protein function by glutathionylation. Free Radic. Res.,  2005, 39(6), 573-580.
[http://dx.doi.org/10.1080/10715760500072172] [PMID: 16036334] 
[34] 
Poole, L.B. The basics of thiols and cysteines in redox biology and chemistry. Free Radic. Biol. Med.,  2015, 80, 148-157.
[http://dx.doi.org/10.1016/j.freeradbiomed.2014.11.013] [PMID: 25433365] 
[35] 
Davies, M.J. Protein oxidation and peroxidation. Biochem. J.,  2016, 473(7), 805-825.
[http://dx.doi.org/10.1042/BJ20151227] [PMID: 27026395] 
[36] 
Kasamatsu, S.; Nishimura, A.; Morita, M.; Matsunaga, T.; Abdul Hamid, H.; Akaike, T. Redox Signaling Regulated by Cysteine Persulfide and Protein Polysulfidation. Molecules,  2016, 21(12)E1721
[http://dx.doi.org/10.3390/molecules21121721] [PMID: 27983699] 
[37] 
Nkabyo, Y.S.; Ziegler, T.R.; Gu, L.H.; Watson, W.H.; Jones, D.P. Glutathione and thioredoxin redox during differentiation in human colon epithelial (Caco-2) cells. Am. J. Physiol. Gastrointest. Liver Physiol.,  2002, 283(6), G1352-G1359.
[http://dx.doi.org/10.1152/ajpgi.00183.2002] [PMID: 12433666] 
[38] 
Jackson, S.P.; Bartek, J. The DNA-damage response in human biology and disease. Nature,  2009, 461(7267), 1071-1078.
[http://dx.doi.org/10.1038/nature08467] [PMID: 19847258] 
[39] 
Poprac, P.; Jomova, K.; Simunkova, M.; Kollar, V.; Rhodes, C.J.; Valko, M. Targeting Free Radicals in Oxidative Stress-Related Human Diseases. Trends Pharmacol. Sci.,  2017, 38(7), 592-607.
[http://dx.doi.org/10.1016/j.tips.2017.04.005] [PMID: 28551354] 
[40] 
Schieber, M.; Chandel, N.S. ROS function in redox signaling and oxidative stress. Curr. Biol.,  2014, 24(10), R453-R462.
[http://dx.doi.org/10.1016/j.cub.2014.03.034] [PMID: 24845678] 
[41] 
Lindahl, T. Instability and decay of the primary structure of DNA. Nature,  1993, 362(6422), 709-715.
[http://dx.doi.org/10.1038/362709a0] [PMID: 8469282] 
[42] 
Lindahl, T.; Barnes, D.E. Repair of endogenous DNA damage. Cold Spring Harb. Symp. Quant. Biol.,  2000, 65, 127-133.
[http://dx.doi.org/10.1101/sqb.2000.65.127] [PMID: 12760027] 
[43] 
Imlay, J.A.; Chin, S.M.; Linn, S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science,  1988, 240(4852), 640-642.
[http://dx.doi.org/10.1126/science.2834821] [PMID: 2834821] 
[44] 
Imlay, J.A.; Linn, S. DNA damage and oxygen radical toxicity. Science,  1988, 240(4857), 1302-1309.
[http://dx.doi.org/10.1126/science.3287616] [PMID: 3287616] 
[45] 
Cadet, J.; Douki, T.; Ravanat, J.L. Oxidatively generated base damage to cellular DNA. Free Radic. Biol. Med.,  2010, 49(1), 9-21.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.03.025] [PMID: 20363317] 
[46] 
Cooke, M.S.; Evans, M.D.; Dizdaroglu, M.; Lunec, J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J.,  2003, 17(10), 1195-1214.
[http://dx.doi.org/10.1096/fj.02-0752rev] [PMID: 12832285] 
[47] 
Evans, M.D.; Dizdaroglu, M.; Cooke, M.S. Oxidative DNA damage and disease: induction, repair and significance. Mutat. Res.,  2004, 567(1), 1-61.
[http://dx.doi.org/10.1016/j.mrrev.2003.11.001] [PMID: 15341901] 
[48] 
Sedelnikova, O.A.; Redon, C.E.; Dickey, J.S.; Nakamura, A.J.; Georgakilas, A.G.; Bonner, W.M. Role of oxidatively induced DNA lesions in human pathogenesis. Mutat. Res.,  2010, 704(1-3), 152-159.
[http://dx.doi.org/10.1016/j.mrrev.2009.12.005] [PMID: 20060490] 
[49] 
Nie, B.; Gan, W.; Shi, F.; Hu, G.X.; Chen, L.G.; Hayakawa, H.; Sekiguchi, M.; Cai, J.P. Age-dependent accumulation of 8-oxoguanine in the DNA and RNA in various rat tissues. Oxid. Med. Cell. Longev.,  2013, 2013303181
[http://dx.doi.org/10.1155/2013/303181] [PMID: 23738036] 
[50] 
Valavanidis, A.; Vlachogianni, T.; Fiotakis, K.; Loridas, S. Pulmonary oxidative stress, inflammation and cancer: respirable particulate matter, fibrous dusts and ozone as major causes of lung carcinogenesis through reactive oxygen species mechanisms. Int. J. Environ. Res. Public Health,  2013, 10(9), 3886-3907.
[http://dx.doi.org/10.3390/ijerph10093886] [PMID: 23985773] 
[51] 
Grollman, A.P.; Moriya, M. Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet.,  1993, 9(7), 246-249.
[http://dx.doi.org/10.1016/0168-9525(93)90089-Z] [PMID: 8379000] 
[52] 
Kasai, H.; Nishimura, S. Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res.,  1984, 12(4), 2137-2145.
[http://dx.doi.org/10.1093/nar/12.4.2137] [PMID: 6701097] 
[53] 
Kohda, K.; Tada, M.; Hakura, A.; Kasai, H.; Kawazoe, Y. Formation of 8-hydroxyguanine residues in DNA treated with 4-hydroxyaminoquinoline 1-oxide and its related compounds in the presence of seryl-AMP. Biochem. Biophys. Res. Commun.,  1987, 149(3), 1141-1148.
[http://dx.doi.org/10.1016/0006-291X(87)90527-4] [PMID: 3122745] 
[54] 
Mitra, S.; Hazra, T.K.; Roy, R.; Ikeda, S.; Biswas, T.; Lock, J.; Boldogh, I.; Izumi, T. Complexities of DNA base excision repair in mammalian cells. Mol. Cells,  1997, 7(3), 305-312.
[PMID: 9264015] 
[55] 
Wallace, S.S.; Murphy, D.L.; Sweasy, J.B. Base excision repair and cancer. Cancer Lett.,  2012, 327(1-2), 73-89.
[http://dx.doi.org/10.1016/j.canlet.2011.12.038] [PMID: 22252118] 
[56] 
Daviet, S.; Couvé-Privat, S.; Gros, L.; Shinozuka, K.; Ide, H.; Saparbaev, M.; Ishchenko, A.A. Major oxidative products of cytosine are substrates for the nucleotide incision repair pathway. DNA Repair (Amst.),  2007, 6(1), 8-18.
[http://dx.doi.org/10.1016/j.dnarep.2006.08.001] [PMID: 16978929] 
[57] 
Melis, J.P.; van Steeg, H.; Luijten, M. Oxidative DNA damage and nucleotide excision repair. Antioxid. Redox Signal.,  2013, 18(18), 2409-2419.
[http://dx.doi.org/10.1089/ars.2012.5036] [PMID: 23216312] 
[58] 
Shafirovich, V.; Geacintov, N.E. Removal of oxidatively generated DNA damage by overlapping repair pathways. Free Radic. Biol. Med.,  2017, 107, 53-61.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.10.507] [PMID: 27818219] 
[59] 
Van Houten, B.; Santa-Gonzalez, G.A.; Camargo, M. DNA repair after oxidative stress: current challenges. Curr. Opin. Toxicol.,  2018, 7, 9-16.
[http://dx.doi.org/10.1016/j.cotox.2017.10.009] [PMID: 29159324] 
[60] 
Ide, H.; Kotera, M. Human DNA glycosylases involved in the repair of oxidatively damaged DNA. Biol. Pharm. Bull.,  2004, 27(4), 480-485.
[http://dx.doi.org/10.1248/bpb.27.480] [PMID: 15056851] 
[61] 
Sancar, A.; Lindsey-Boltz, L.A.; Unsal-Kaçmaz, K.; Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem.,  2004, 73, 39-85.
[http://dx.doi.org/10.1146/annurev.biochem.73.011303.073723] [PMID: 15189136] 
[62] 
Bessho, T.; Roy, R.; Yamamoto, K.; Kasai, H.; Nishimura, S.; Tano, K.; Mitra, S. Repair of 8-hydroxyguanine in DNA by mammalian N-methylpurine-DNA glycosylase. Proc. Natl. Acad. Sci. USA,  1993, 90(19), 8901-8904.
[http://dx.doi.org/10.1073/pnas.90.19.8901] [PMID: 8415629] 
[63] 
Bjorâs, M.; Luna, L.; Johnsen, B.; Hoff, E.; Haug, T.; Rognes, T.; Seeberg, E. Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites. EMBO J.,  1997, 16(20), 6314-6322.
[http://dx.doi.org/10.1093/emboj/16.20.6314] [PMID: 9321410] 
[64] 
Nghiem, Y.; Cabrera, M.; Cupples, C.G.; Miller, J.H. The mutY gene: a mutator locus in Escherichia coli that generates G.C----T.A transversions. Proc. Natl. Acad. Sci. USA,  1988, 85(8), 2709-2713.
[http://dx.doi.org/10.1073/pnas.85.8.2709] [PMID: 3128795] 
[65] 
Lindahl, T. An N-glycosidase from Escherichia coli that releases free uracil from DNA containing deaminated cytosine residues. Proc. Natl. Acad. Sci. USA,  1974, 71(9), 3649-3653.
[http://dx.doi.org/10.1073/pnas.71.9.3649] [PMID: 4610583] 
[66] 
Parikh, S.S.; Mol, C.D.; Slupphaug, G.; Bharati, S.; Krokan, H.E.; Tainer, J.A. Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J.,  1998, 17(17), 5214-5226.
[http://dx.doi.org/10.1093/emboj/17.17.5214] [PMID: 9724657] 
[67] 
Saito, Y.; Uraki, F.; Nakajima, S.; Asaeda, A.; Ono, K.; Kubo, K.; Yamamoto, K. Characterization of endonuclease III (nth) and endonuclease VIII (nei) mutants of Escherichia coli K-12. J. Bacteriol.,  1997, 179(11), 3783-3785.
[http://dx.doi.org/10.1128/JB.179.11.3783-3785.1997] [PMID: 9171430] 
[68] 
Masaoka, A.; Matsubara, M.; Tanaka, T.; Terato, H.; Ohyama, Y.; Kubo, K.; Ide, H. Repair roles of hSMUG1 assessed by damage specificity and cellular activity. Nucleic acids research. Supplement,  2001, 2003(3), 263-264.
[69] 
Altieri, F.; Grillo, C.; Maceroni, M.; Chichiarelli, S. DNA damage and repair: from molecular mechanisms to health implications. Antioxid. Redox Signal.,  2008, 10(5), 891-937.
[http://dx.doi.org/10.1089/ars.2007.1830] [PMID: 18205545] 
[70] 
Krokan, H.E.; Standal, R.; Slupphaug, G. DNA glycosylases in the base excision repair of DNA. Biochem. J.,  1997, 325(Pt 1), 1-16.
[http://dx.doi.org/10.1042/bj3250001] [PMID: 9224623] 
[71] 
Wiederhold, L.; Leppard, J.B.; Kedar, P.; Karimi-Busheri, F.; Rasouli-Nia, A.; Weinfeld, M.; Tomkinson, A.E.; Izumi, T.; Prasad, R.; Wilson, S.H.; Mitra, S.; Hazra, T.K. AP endonuclease-independent DNA base excision repair in human cells. Mol. Cell,  2004, 15(2), 209-220.
[http://dx.doi.org/10.1016/j.molcel.2004.06.003] [PMID: 15260972] 
[72] 
Chen, D.S.; 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.
[http://dx.doi.org/10.1093/nar/19.21.5907] [PMID: 1719484] 
[73] 
Petermann, E.; Keil, C.; Oei, S.L. Roles of DNA ligase III and XRCC1 in regulating the switch between short patch and long patch BER. DNA Repair (Amst.),  2006, 5(5), 544-555.
[http://dx.doi.org/10.1016/j.dnarep.2005.12.008] [PMID: 16442856] 
[74] 
Fortini, P.; Pascucci, B.; Parlanti, E.; Sobol, R.W.; Wilson, S.H.; Dogliotti, E. Different DNA polymerases are involved in the short- and long-patch base excision repair in mammalian cells. Biochemistry,  1998, 37(11), 3575-3580.
[http://dx.doi.org/10.1021/bi972999h] [PMID: 9530283] 
[75] 
Pascucci, B.; Stucki, M.; Jónsson, Z.O.; Dogliotti, E.; Hübscher, U. Long patch base excision repair with purified human proteins. DNA ligase I as patch size mediator for DNA polymerases delta and epsilon. J. Biol. Chem.,  1999, 274(47), 33696-33702.
[http://dx.doi.org/10.1074/jbc.274.47.33696] [PMID: 10559260] 
[76] 
Lindahl, T.; Gally, J.A.; Edelman, G.M. Deoxyribonuclease IV: a new exonuclease from mammalian tissues. Proc. Natl. Acad. Sci. USA,  1969, 62(2), 597-603.
[http://dx.doi.org/10.1073/pnas.62.2.597] [PMID: 5256235] 
[77] 
Robins, P.; Pappin, D.J.; Wood, R.D.; Lindahl, T. Structural and functional homology between mammalian DNase IV and the 5′-nuclease domain of Escherichia coli DNA polymerase I. J. Biol. Chem.,  1994, 269(46), 28535-28538.
[PMID: 7961795] 
[78] 
Roldán-Arjona, T.; Wei, Y.F.; Carter, K.C.; Klungland, A.; Anselmino, C.; Wang, R.P.; Augustus, M.; Lindahl, T. Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase. Proc. Natl. Acad. Sci. USA,  1997, 94(15), 8016-8020.
[http://dx.doi.org/10.1073/pnas.94.15.8016] [PMID: 9223306] 
[79] 
Schuch, A.P.; Moreno, N.C.; Schuch, N.J.; Menck, C.F.M.; Garcia, C.C.M. Sunlight damage to cellular DNA: Focus on oxidatively generated lesions. Free Radic. Biol. Med.,  2017, 107, 110-124.
[http://dx.doi.org/10.1016/j.freeradbiomed.2017.01.029] [PMID: 28109890] 
[80] 
Sugasawa, K. Molecular mechanisms of DNA damage recognition for mammalian nucleotide excision repair. DNA Repair (Amst.),  2016, 44, 110-117.
[http://dx.doi.org/10.1016/j.dnarep.2016.05.015] [PMID: 27264556] 
[81] 
Li, J.; Wang, Q.E.; Zhu, Q.; El-Mahdy, M.A.; Wani, G.; Praetorius-Ibba, M.; Wani, A.A. DNA damage binding protein component DDB1 participates in nucleotide excision repair through DDB2 DNA-binding and cullin 4A ubiquitin ligase activity. Cancer Res.,  2006, 66(17), 8590-8597.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-1115] [PMID: 16951172] 
[82] 
Fousteri, M.; Vermeulen, W.; van Zeeland, A.A.; Mullenders, L.H. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell,  2006, 23(4), 471-482.
[http://dx.doi.org/10.1016/j.molcel.2006.06.029] [PMID: 16916636] 
[83] 
Egly, J.M.; Coin, F. A history of TFIIH: two decades of molecular biology on a pivotal transcription/repair factor. DNA Repair (Amst.),  2011, 10(7), 714-721.
[http://dx.doi.org/10.1016/j.dnarep.2011.04.021] [PMID: 21592869] 
[84] 
Compe, E.; Egly, J.M. TFIIH: when transcription met DNA repair. Nat. Rev. Mol. Cell Biol.,  2012, 13(6), 343-354.
[http://dx.doi.org/10.1038/nrm3350] [PMID: 22572993] 
[85] 
Gaillard, P.H.L.; Wood, R.D. Activity of individual ERCC1 and XPF subunits in DNA nucleotide excision repair. Nucleic Acids Res.,  2001, 29(4), 872-879.
[http://dx.doi.org/10.1093/nar/29.4.872] [PMID: 11160918] 
[86] 
Constantinou, A.; Gunz, D.; Evans, E.; Lalle, P.; Bates, P.A.; Wood, R.D.; Clarkson, S.G. Conserved residues of human XPG protein important for nuclease activity and function in nucleotide excision repair. J. Biol. Chem.,  1999, 274(9), 5637-5648.
[http://dx.doi.org/10.1074/jbc.274.9.5637] [PMID: 10026181] 
[87] 
Mocquet, V.; Lainé, J.P.; Riedl, T.; Yajin, Z.; Lee, M.Y.; Egly, J.M. Sequential recruitment of the repair factors during NER: the role of XPG in initiating the resynthesis step. EMBO J.,  2008, 27(1), 155-167.
[http://dx.doi.org/10.1038/sj.emboj.7601948] [PMID: 18079701] 
[88] 
Moser, J.; Kool, H.; Giakzidis, I.; Caldecott, K.; Mullenders, L.H.; Fousteri, M.I. Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III alpha in a cell-cycle-specific manner. Mol. Cell,  2007, 27(2), 311-323.
[http://dx.doi.org/10.1016/j.molcel.2007.06.014] [PMID: 17643379] 
[89] 
Koch, S.C.; Simon, N.; Ebert, C.; Carell, T.   Molecular
 mechanisms of xeroderma pigmentosum (XP) proteins. Q.
 Rev. Biophys., 2016, 49e5.
[90] 
Black, J.O. Xeroderma Pigmentosum. Head Neck Pathol.,  2016, 10(2), 139-144.
[http://dx.doi.org/10.1007/s12105-016-0707-8] [PMID: 26975629] 
[91] 
Natale, V.; Raquer, H. Xeroderma pigmentosum-Cockayne syndrome complex. Orphanet J. Rare Dis.,  2017, 12(1), 65.
[http://dx.doi.org/10.1186/s13023-017-0616-2] [PMID: 28376890] 
[92] 
Kropachev, K.; Ding, S.; Terzidis, M.A.; Masi, A.; Liu, Z.; Cai, Y.; Kolbanovskiy, M.; Chatgilialoglu, C.; Broyde, S.; Geacintov, N.E.; Shafirovich, V. Structural basis for the recognition of diastereomeric 5@′,8-cyclo-2@′-deoxypurine lesions by the human nucleotide excision repair system. Nucleic Acids Res.,  2014, 42(8), 5020-5032.
[http://dx.doi.org/10.1093/nar/gku162] [PMID: 24615810] 
[93] 
Klungland, A.; Höss, M.; Gunz, D.; Constantinou, A.; Clarkson, S.G.; Doetsch, P.W.; Bolton, P.H.; Wood, R.D.; Lindahl, T. Base excision repair of oxidative DNA damage activated by XPG protein. Mol. Cell,  1999, 3(1), 33-42.
[http://dx.doi.org/10.1016/S1097-2765(00)80172-0] [PMID: 10024877] 
[94] 
Rodriguez, G.P.; Song, J.B.; Crouse, G.F. In vivo bypass of 8-oxodG. PLoS Genet.,  2013, 9(8)e1003682
[http://dx.doi.org/10.1371/journal.pgen.1003682] [PMID: 23935538] 
[95] 
Colussi, C.; Parlanti, E.; Degan, P.; Aquilina, G.; Barnes, D.; Macpherson, P.; Karran, P.; Crescenzi, M.; Dogliotti, E.; Bignami, M. The mammalian mismatch repair pathway removes DNA 8-oxodGMP incorporated from the oxidized dNTP pool. Curr. Biol.,  2002, 12(11), 912-918.
[http://dx.doi.org/10.1016/S0960-9822(02)00863-1] [PMID: 12062055] 
[96] 
Russo, M.T.; De Luca, G.; Degan, P.; Bignami, M. Different DNA repair strategies to combat the threat from 8-oxoguanine. Mutat. Res.,  2007, 614(1-2), 69-76.
[http://dx.doi.org/10.1016/j.mrfmmm.2006.03.007] [PMID: 16769088] 
[97] 
Avkin, S.; Livneh, Z. Efficiency, specificity and DNA polymerase-dependence of translesion replication across the oxidative DNA lesion 8-oxoguanine in human cells. Mutat. Res.,  2002, 510(1-2), 81-90.
[http://dx.doi.org/10.1016/S0027-5107(02)00254-3] [PMID: 12459445] 
[98] 
Liu, D.; Keijzers, G.; Rasmussen, L.J. DNA mismatch repair and its many roles in eukaryotic cells. Mutat. Res.,  2017, 773, 174-187.
[http://dx.doi.org/10.1016/j.mrrev.2017.07.001] [PMID: 28927527] 
[99] 
Lamers, M.H.; Perrakis, A.; Enzlin, J.H.; Winterwerp, H.H.; de Wind, N.; Sixma, T.K. The crystal structure of DNA mismatch repair protein MutS binding to a G x T mismatch. Nature,  2000, 407(6805), 711-717.
[http://dx.doi.org/10.1038/35037523] [PMID: 11048711] 
[100] 
Owen, B.A.H.; H Lang, W.; McMurray, C.T. The nucleotide binding dynamics of human MSH2-MSH3 are lesion dependent. Nat. Struct. Mol. Biol.,  2009, 16(5), 550-557.
[http://dx.doi.org/10.1038/nsmb.1596] [PMID: 19377479] 
[101] 
Honda, M.; Okuno, Y.; Hengel, S.R.; Martín-López, J.V.; Cook, C.P.; Amunugama, R.; Soukup, R.J.; Subramanyam, S.; Fishel, R.; Spies, M. Mismatch repair protein hMSH2-hMSH6 recognizes mismatches and forms sliding clamps within a D-loop recombination intermediate. Proc. Natl. Acad. Sci. USA,  2014, 111(3), E316-E325.
[http://dx.doi.org/10.1073/pnas.1312988111] [PMID: 24395779] 
[102] 
Macpherson, P.; Barone, F.; Maga, G.; Mazzei, F.; Karran, P.; Bignami, M. 8-oxoguanine incorporation into DNA repeats in vitro and mismatch recognition by MutSalpha. Nucleic Acids Res.,  2005, 33(16), 5094-5105.
[http://dx.doi.org/10.1093/nar/gki813] [PMID: 16174844] 
[103] 
Kadyrov, F.A.; Dzantiev, L.; Constantin, N.; Modrich, P. Endonucleolytic function of MutLalpha in human mismatch repair. Cell,  2006, 126(2), 297-308.
[http://dx.doi.org/10.1016/j.cell.2006.05.039] [PMID: 16873062] 
[104] 
Zhang, Y.; Yuan, F.; Presnell, S.R.; Tian, K.; Gao, Y.; Tomkinson, A.E.; Gu, L.; Li, G.M. Reconstitution of 5@-directed human mismatch repair in a purified system. Cell,  2005, 122(5), 693-705.
[http://dx.doi.org/10.1016/j.cell.2005.06.027] [PMID: 16143102] 
[105] 
Longley, M.J.; Pierce, A.J.; Modrich, P. DNA polymerase delta is required for human mismatch repair in vitro. J. Biol. Chem.,  1997, 272(16), 10917-10921.
[http://dx.doi.org/10.1074/jbc.272.16.10917] [PMID: 9099749] 
[106] 
Hoege, C.; Pfander, B.; Moldovan, G.L.; Pyrowolakis, G.; Jentsch, S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature,  2002, 419(6903), 135-141.
[http://dx.doi.org/10.1038/nature00991] [PMID: 12226657] 
[107] 
Bienko, M.; Green, C.M.; Crosetto, N.; Rudolf, F.; Zapart, G.; Coull, B.; Kannouche, P.; Wider, G.; Peter, M.; Lehmann, A.R.; Hofmann, K.; Dikic, I. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science,  2005, 310(5755), 1821-1824.
[http://dx.doi.org/10.1126/science.1120615] [PMID: 16357261] 
[108] 
Friedberg, E.C.; Lehmann, A.R.; Fuchs, R.P. Trading places: how do DNA polymerases switch during translesion DNA synthesis? Mol. Cell,  2005, 18(5), 499-505.
[http://dx.doi.org/10.1016/j.molcel.2005.03.032] [PMID: 15916957] 
[109] 
Vaisman, A.; Woodgate, R. Translesion DNA polymerases in eukaryotes: what makes them tick? Crit. Rev. Biochem. Mol. Biol.,  2017, 52(3), 274-303.
[http://dx.doi.org/10.1080/10409238.2017.1291576] [PMID: 28279077] 
[110] 
van der Kemp, P.A.; de Padula, M.; Burguiere-Slezak, G.; Ulrich, H.D.; Boiteux, S. PCNA monoubiquitylation and DNA polymerase eta ubiquitin-binding domain are required to prevent 8-oxoguanine-induced mutagenesis in Saccharomyces cerevisiae. Nucleic Acids Res.,  2009, 37(8), 2549-2559.
[http://dx.doi.org/10.1093/nar/gkp105] [PMID: 19264809] 
[111] 
Hegde, M.L.; Izumi, T.; Mitra, S. Oxidized base damage and single-strand break repair in mammalian genomes: role of disordered regions and posttranslational modifications in early enzymes. Prog. Mol. Biol. Transl. Sci.,  2012, 110, 123-153.
[http://dx.doi.org/10.1016/B978-0-12-387665-2.00006-7] [PMID: 22749145] 
[112] 
Scott, T.L.; Rangaswamy, S.; Wicker, C.A.; Izumi, T. Repair of oxidative DNA damage and cancer: recent progress in DNA base excision repair. Antioxid. Redox Signal.,  2014, 20(4), 708-726.
[http://dx.doi.org/10.1089/ars.2013.5529] [PMID: 23901781] 
[113] 
Nishimura, S. 8-Hydroxyguanine: a base for discovery. DNA Repair (Amst.),  2011, 10(11), 1078-1083.
[http://dx.doi.org/10.1016/j.dnarep.2011.04.006] [PMID: 22121518] 
[114] 
Nishimura, S. Involvement of mammalian OGG1(MMH) in excision of the 8-hydroxyguanine residue in DNA. Free Radic. Biol. Med.,  2002, 32(9), 813-821.
[http://dx.doi.org/10.1016/S0891-5849(02)00778-5] [PMID: 11978483] 
[115] 
German, P.; Szaniszlo, P.; Hajas, G.; Radak, Z.; Bacsi, A.; Hazra, T.K.; Hegde, M.L.; Ba, X.; Boldogh, I. Activation of cellular signaling by 8-oxoguanine DNA glycosylase-1-initiated DNA base excision repair. DNA Repair (Amst.),  2013, 12(10), 856-863.
[http://dx.doi.org/10.1016/j.dnarep.2013.06.006] [PMID: 23890570] 
[116] 
Rowland, M.M.; Schonhoft, J.D.; McKibbin, P.L.; David, S.S.; Stivers, J.T. Microscopic mechanism of DNA damage searching by hOGG1. Nucleic Acids Res.,  2014, 42(14), 9295-9303.
[http://dx.doi.org/10.1093/nar/gku621] [PMID: 25016526] 
[117] 
Richard, D.J.; Bolderson, E.; Cubeddu, L.; Wadsworth, R.I.; Savage, K.; Sharma, G.G.; Nicolette, M.L.; Tsvetanov, S.; McIlwraith, M.J.; Pandita, R.K.; Takeda, S.; Hay, R.T.; Gautier, J.; West, S.C.; Paull, T.T.; Pandita, T.K.; White, M.F.; Khanna, K.K. Single-stranded DNA-binding protein hSSB1 is critical for genomic stability. Nature,  2008, 453(7195), 677-681.
[http://dx.doi.org/10.1038/nature06883] [PMID: 18449195] 
[118] 
Richard, D.J.; Cubeddu, L.; Urquhart, A.J.; Bain, A.; Bolderson, E.; Menon, D.; White, M.F.; Khanna, K.K. hSSB1 interacts directly with the MRN complex stimulating its recruitment to DNA double-strand breaks and its endo-nuclease activity. Nucleic Acids Res.,  2011, 39(9), 3643-3651.
[http://dx.doi.org/10.1093/nar/gkq1340] [PMID: 21227926] 
[119] 
Richard, D.J.; Savage, K.; Bolderson, E.; Cubeddu, L.; So, S.; Ghita, M.; Chen, D.J.; White, M.F.; Richard, K.; Prise, K.M.; Schettino, G.; Khanna, K.K. hSSB1 rapidly binds at the sites of DNA double-strand breaks and is required for the efficient recruitment of the MRN complex. Nucleic Acids Res.,  2011, 39(5), 1692-1702.
[http://dx.doi.org/10.1093/nar/gkq1098] [PMID: 21051358] 
[120] 
Yang, S.H.; Zhou, R.; Campbell, J.; Chen, J.; Ha, T.; Paull, T.T. The SOSS1 single-stranded DNA binding complex promotes DNA end resection in concert with Exo1. EMBO J.,  2013, 32(1), 126-139.
[http://dx.doi.org/10.1038/emboj.2012.314] [PMID: 23178594] 
[121] 
Bolderson, E.; Petermann, E.; Croft, L.; Suraweera, A.; Pandita, R.K.; Pandita, T.K.; Helleday, T.; Khanna, K.K.; Richard, D.J. Human single-stranded DNA binding protein 1 (hSSB1/NABP2) is required for the stability and repair of stalled replication forks. Nucleic Acids Res.,  2014, 42(10), 6326-6336.
[http://dx.doi.org/10.1093/nar/gku276] [PMID: 24753408] 
[122] 
Paquet, N.; Adams, M.N.; Leong, V.; Ashton, N.W.; Touma, C.; Gamsjaeger, R.; Cubeddu, L.; Beard, S.; Burgess, J.T.; Bolderson, E.; O’Byrne, K.J.; Richard, D.J. hSSB1 (NABP2/ OBFC2B) is required for the repair of 8-oxo-guanine by the hOGG1-mediated base excision repair pathway. Nucleic Acids Res.,  2015, 43(18), 8817-8829.
[http://dx.doi.org/10.1093/nar/gkv790] [PMID: 26261212] 
[123] 
Richard, D.J.; Bolderson, E.; Khanna, K.K. Multiple human single-stranded DNA binding proteins function in genome maintenance: structural, biochemical and functional analysis. Crit. Rev. Biochem. Mol. Biol.,  2009, 44(2-3), 98-116.
[http://dx.doi.org/10.1080/10409230902849180] [PMID: 19367476] 
[124] 
Wu, Y.; Lu, J.; Kang, T. Human single-stranded DNA binding proteins: guardians of genome stability. Acta Biochim. Biophys. Sin. (Shanghai),  2016, 48(7), 671-677.
[http://dx.doi.org/10.1093/abbs/gmw044] [PMID: 27217471] 
[125] 
Ashton, N.W.; Bolderson, E.; Cubeddu, L.; O’Byrne, K.J.; Richard, D.J. Human single-stranded DNA binding proteins are essential for maintaining genomic stability. BMC Mol. Biol.,  2013, 14, 9.
[http://dx.doi.org/10.1186/1471-2199-14-9] [PMID: 23548139] 
[126] 
Wold, M.S.; Kelly, T. Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA. Proc. Natl. Acad. Sci. USA,  1988, 85(8), 2523-2527.
[http://dx.doi.org/10.1073/pnas.85.8.2523] [PMID: 2833742] 
[127] 
Huang, J.; Gong, Z.; Ghosal, G.; Chen, J. SOSS complexes participate in the maintenance of genomic stability. Mol. Cell,  2009, 35(3), 384-393.
[http://dx.doi.org/10.1016/j.molcel.2009.06.011] [PMID: 19683501] 
[128] 
Li, Y.; Bolderson, E.; Kumar, R.; Muniandy, P.A.; Xue, Y.; Richard, D.J.; Seidman, M.; Pandita, T.K.; Khanna, K.K.; Wang, W. HSSB1 and hSSB2 form similar multiprotein complexes that participate in DNA damage response. J. Biol. Chem.,  2009, 284(35), 23525-23531.
[http://dx.doi.org/10.1074/jbc.C109.039586] [PMID: 19605351] 
[129] 
Skaar, J.R.; Ferris, A.L.; Wu, X.; Saraf, A.; Khanna, K.K.; Florens, L.; Washburn, M.P.; Hughes, S.H.; Pagano, M. The Integrator complex controls the termination of transcription at diverse classes of gene targets. Cell Res.,  2015, 25(3), 288-305.
[http://dx.doi.org/10.1038/cr.2015.19] [PMID: 25675981] 
[130] 
Skaar, J.R.; Richard, D.J.; Saraf, A.; Toschi, A.; Bolderson, E.; Florens, L.; Washburn, M.P.; Khanna, K.K.; Pagano, M. INTS3 controls the hSSB1-mediated DNA damage response. J. Cell Biol.,  2009, 187(1), 25-32.
[http://dx.doi.org/10.1083/jcb.200907026] [PMID: 19786574] 
[131] 
Xu, S.; Feng, Z.; Zhang, M.; Wu, Y.; Sang, Y.; Xu, H.; Lv, X.; Hu, K.; Cao, J.; Zhang, R.; Chen, L.; Liu, M.; Yun, J.P.; Zeng, Y.X.; Kang, T. hSSB1 binds and protects p21 from ubiquitin-mediated degradation and positively correlates with p21 in human hepatocellular carcinomas. Oncogene,  2011, 30(19), 2219-2229.
[http://dx.doi.org/10.1038/onc.2010.596] [PMID: 21242961] 
[132] 
Xu, S.; Wu, Y.; Chen, Q.; Cao, J.; Hu, K.; Tang, J.; Sang, Y.; Lai, F.; Wang, L.; Zhang, R.; Li, S.P.; Zeng, Y.X.; Yin, Y.; Kang, T. hSSB1 regulates both the stability and the transcriptional activity of p53. Cell Res.,  2013, 23(3), 423-435.
[http://dx.doi.org/10.1038/cr.2012.162] [PMID: 23184057] 
[133] 
Zhang, F.; Ma, T.; Yu, X. A core hSSB1-INTS complex participates in the DNA damage response. J. Cell Sci.,  2013, 126(Pt 21), 4850-4855.
[http://dx.doi.org/10.1242/jcs.132514] [PMID: 23986477] 
[134] 
Paquet, N.; Adams, M.N.; Ashton, N.W.; Touma, C.; Gamsjaeger, R.; Cubeddu, L.; Leong, V.; Beard, S.; Bolderson, E.; Botting, C.H.; O’Byrne, K.J.; Richard, D.J. hSSB1 (NABP2/OBFC2B) is regulated by oxidative stress. Sci. Rep.,  2016, 6, 27446.
[http://dx.doi.org/10.1038/srep27446] [PMID: 27273218] 
[135] 
Ba, X.; Boldogh, I. 8-Oxoguanine DNA glycosylase 1: Beyond repair of the oxidatively modified base lesions. Redox Biol.,  2018, 14, 669-678.
[http://dx.doi.org/10.1016/j.redox.2017.11.008] [PMID: 29175754] 
[136] 
Bruner, S.D.; Norman, D.P.; Verdine, G.L. Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature,  2000, 403(6772), 859-866.
[http://dx.doi.org/10.1038/35002510] [PMID: 10706276] 
[137] 
Bravard, A.; Vacher, M.; Gouget, B.; Coutant, A.; de Boisferon, F.H.; Marsin, S.; Chevillard, S.; Radicella, J.P. Redox regulation of human OGG1 activity in response to cellular oxidative stress. Mol. Cell. Biol.,  2006, 26(20), 7430-7436.
[http://dx.doi.org/10.1128/MCB.00624-06] [PMID: 16923968] 
[138] 
Bravard, A.; Campalans, A.; Vacher, M.; Gouget, B.; Levalois, C.; Chevillard, S.; Radicella, J.P. Inactivation by oxidation and recruitment into stress granules of hOGG1 but not APE1 in human cells exposed to sub-lethal concentrations of cadmium. Mutat. Res.,  2010, 685(1-2), 61-69.
[http://dx.doi.org/10.1016/j.mrfmmm.2009.09.013] [PMID: 19800894] 
[139] 
Campalans, A.; Amouroux, R.; Bravard, A.; Epe, B.; Radicella, J.P. UVA irradiation induces relocalisation of the DNA repair protein hOGG1 to nuclear speckles. J. Cell Sci.,  2007, 120(Pt 1), 23-32.
[http://dx.doi.org/10.1242/jcs.03312] [PMID: 17148573] 
[140] 
Kohno, T.; Shinmura, K.; Tosaka, M.; Tani, M.; Kim, S.R.; Sugimura, H.; Nohmi, T.; Kasai, H.; Yokota, J. Genetic polymorphisms and alternative splicing of the hOGG1 gene, that is involved in the repair of 8-hydroxyguanine in damaged DNA. Oncogene,  1998, 16(25), 3219-3225.
[http://dx.doi.org/10.1038/sj.onc.1201872] [PMID: 9681819] 
[141] 
Lee, A.J.; Hodges, N.J.; Chipman, J.K. Interindividual variability in response to sodium dichromate-induced oxidative DNA damage: role of the Ser326Cys polymorphism in the DNA-repair protein of 8-oxo-7,8-dihydro-2@′-deoxyguanosine DNA glycosylase 1. Cancer Epidemiol. Biomarkers Prev.,  2005, 14(2), 497-505.
[http://dx.doi.org/10.1158/1055-9965.EPI-04-0295] [PMID: 15734978] 
[142] 
Hill, J.W.; Evans, M.K. Dimerization and opposite base-dependent catalytic impairment of polymorphic S326C OGG1 glycosylase. Nucleic Acids Res.,  2006, 34(5), 1620-1632.
[http://dx.doi.org/10.1093/nar/gkl060] [PMID: 16549874] 
[143] 
Kaur, M.P.; Guggenheim, E.J.; Pulisciano, C.; Akbar, S.; Kershaw, R.M.; Hodges, N.J. Cellular accumulation of Cys326-OGG1 protein complexes under conditions of oxidative stress. Biochem. Biophys. Res. Commun.,  2014, 447(1), 12-18.
[http://dx.doi.org/10.1016/j.bbrc.2014.03.044] [PMID: 24680828] 
[144] 
Thakur, S.; Sarkar, B.; Cholia, R.P.; Gautam, N.; Dhiman, M.; Mantha, A.K.  APE1/Ref-1 as an emerging therapeutic
  target for various human diseases: phytochemical modulation
  of its functions. Exp. Mol. Med., 2014, 46e106. 
[145] 
Mol, C.D.; Izumi, T.; Mitra, S.; Tainer, J.A. DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination [corrected]. Nature,  2000, 403(6768), 451-456.
[http://dx.doi.org/10.1038/35000249] [PMID: 10667800] 
[146] 
Sung, J.S.; Demple, B. Roles of base excision repair subpathways in correcting oxidized abasic sites in DNA. FEBS J.,  2006, 273(8), 1620-1629.
[http://dx.doi.org/10.1111/j.1742-4658.2006.05192.x] [PMID: 16623699] 
[147] 
Dyrkheeva, N.S.; Lebedeva, N.A.; Lavrik, O.I. AP Endonuclease 1 as a Key Enzyme in Repair of Apurinic/Apyrimidinic Sites. Biochemistry (Mosc.),  2016, 81(9), 951-967.
[http://dx.doi.org/10.1134/S0006297916090042] [PMID: 27682167] 
[148] 
Chohan, M.; Mackedenski, S.; Li, W.M.; Lee, C.H. Human apurinic/apyrimidinic endonuclease 1 (APE1) has 3@ RNA phosphatase and 3@ exoribonuclease activities. J. Mol. Biol.,  2015, 427(2), 298-311.
[http://dx.doi.org/10.1016/j.jmb.2014.12.001] [PMID: 25498387] 
[149] 
Bhakat, K.K.; Mantha, A.K.; Mitra, S. Transcriptional regulatory functions of mammalian AP-endonuclease (APE1/Ref-1), an essential multifunctional protein. Antioxid. Redox Signal.,  2009, 11(3), 621-638.
[http://dx.doi.org/10.1089/ars.2008.2198] [PMID: 18715144] 
[150] 
Luo, M.; Delaplane, S.; Jiang, A.; Reed, A.; He, Y.; Fishel, M.; Nyland, R.L., II; Borch, R.F.; Qiao, X.; Georgiadis, M.M.; 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, 10(11), 1853-1867.
[http://dx.doi.org/10.1089/ars.2008.2120] [PMID: 18627350] 
[151] 
Xanthoudakis, S.; Miao, G.G.; Curran, T. The redox and DNA-repair activities of Ref-1 are encoded by nonoverlapping domains. Proc. Natl. Acad. Sci. USA,  1994, 91(1), 23-27.
[http://dx.doi.org/10.1073/pnas.91.1.23] [PMID: 7506414] 
[152] 
Demple, B.; Herman, T.; Chen, D.S. 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,  1991, 88(24), 11450-11454.
[http://dx.doi.org/10.1073/pnas.88.24.11450] [PMID: 1722334] 
[153] 
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.
[http://dx.doi.org/10.1002/j.1460-2075.1992.tb05097.x] [PMID: 1537340] 
[154] 
Nishi, T.; Shimizu, N.; Hiramoto, M.; Sato, I.; Yamaguchi, Y.; Hasegawa, M.; Aizawa, S.; Tanaka, H.; Kataoka, K.; Watanabe, H.; Handa, H. Spatial redox regulation of a critical cysteine residue of NF-kappa B in vivo. J. Biol. Chem.,  2002, 277(46), 44548-44556.
[http://dx.doi.org/10.1074/jbc.M202970200] [PMID: 12213807] 
[155] 
Ema, M.; Hirota, K.; Mimura, J.; Abe, H.; Yodoi, J.; Sogawa, K.; Poellinger, L.; Fujii-Kuriyama, Y. Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J.,  1999, 18(7), 1905-1914.
[http://dx.doi.org/10.1093/emboj/18.7.1905] [PMID: 10202154] 
[156] 
Tell, G.; Zecca, A.; Pellizzari, L.; Spessotto, P.; Colombatti, A.; Kelley, M.R.; Damante, G.; Pucillo, C. 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.,  2000, 28(5), 1099-1105.
[http://dx.doi.org/10.1093/nar/28.5.1099] [PMID: 10666449] 
[157] 
Huang, R.P.; Adamson, E.D. 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.,  1993, 12(3), 265-273.
[http://dx.doi.org/10.1089/dna.1993.12.265] [PMID: 8466649] 
[158] 
Ueno, M.; Masutani, H.; Arai, R.J.; Yamauchi, A.; Hirota, K.; Sakai, T.; Inamoto, T.; Yamaoka, Y.; Yodoi, J.; Nikaido, T. Thioredoxin-dependent redox regulation of p53-mediated p21 activation. J. Biol. Chem.,  1999, 274(50), 35809-35815.
[http://dx.doi.org/10.1074/jbc.274.50.35809] [PMID: 10585464] 
[159] 
Xanthoudakis, S.; Miao, G.; Wang, F.; Pan, Y.C.; Curran, T. Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J.,  1992, 11(9), 3323-3335.
[http://dx.doi.org/10.1002/j.1460-2075.1992.tb05411.x] [PMID: 1380454] 
[160] 
Ando, K.; Hirao, S.; Kabe, Y.; Ogura, Y.; Sato, I.; Yamaguchi, Y.; Wada, T.; Handa, H. A new APE1/Ref-1-dependent pathway leading to reduction of NF-kappaB and AP-1, and activation of their DNA-binding activity. Nucleic Acids Res.,  2008, 36(13), 4327-4336.
[http://dx.doi.org/10.1093/nar/gkn416] [PMID: 18586825] 
[161] 
Luo, M.; Zhang, J.; He, H.; Su, D.; Chen, Q.; Gross, M.L.; Kelley, M.R.; Georgiadis, M.M. Characterization of the redox activity and disulfide bond formation in apurinic/apyrimidinic endonuclease. Biochemistry,  2012, 51(2), 695-705.
[http://dx.doi.org/10.1021/bi201034z] [PMID: 22148505] 
[162] 
Walker, L.J.; Robson, C.N.; Black, E.; Gillespie, D.; Hickson, I.D. 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.,  1993, 13(9), 5370-5376.
[http://dx.doi.org/10.1128/MCB.13.9.5370] [PMID: 8355688] 
[163] 
Kim, Y.J.; Kim, D.; Illuzzi, J.L.; Delaplane, S.; Su, D.; Bernier, M.; Gross, M.L.; Georgiadis, M.M.; Wilson, D.M., III S-glutathionylation of cysteine 99 in the APE1 protein impairs abasic endonuclease activity. J. Mol. Biol.,  2011, 414(3), 313-326.
[http://dx.doi.org/10.1016/j.jmb.2011.10.023] [PMID: 22024594] 
[164] 
Sweasy, J.B.; Lang, T.; DiMaio, D. Is base excision repair a tumor suppressor mechanism? Cell Cycle,  2006, 5(3), 250-259.
[http://dx.doi.org/10.4161/cc.5.3.2414] [PMID: 16418580] 
[165] 
Curtin, N.J. DNA repair dysregulation from cancer driver to therapeutic target. Nat. Rev. Cancer,  2012, 12(12), 801-817.
[http://dx.doi.org/10.1038/nrc3399] [PMID: 23175119] 
[166] 
Xu, Z.; Yu, L.; Zhang, X. Association between the hOGG1 Ser326Cys polymorphism and lung cancer susceptibility: a meta-analysis based on 22,475 subjects. Diagn. Pathol.,  2013, 8, 144.
[http://dx.doi.org/10.1186/1746-1596-8-144] [PMID: 23971971] 
[167] 
Bapat, A.; Fishel, M.L.; Kelley, M.R. Going ape as an approach to cancer therapeutics. Antioxid. Redox Signal.,  2009, 11(3), 651-668.
[http://dx.doi.org/10.1089/ars.2008.2218] [PMID: 18715143] 
[168] 
Fishel, M.L.; Kelley, M.R. The DNA base excision repair protein Ape1/Ref-1 as a therapeutic and chemopreventive target. Mol. Aspects Med.,  2007, 28(3-4), 375-395.
[http://dx.doi.org/10.1016/j.mam.2007.04.005] [PMID: 17560642] 
[169] 
Raffoul, J.J.; Heydari, A.R.; Hillman, G.G. DNA Repair and Cancer Therapy: Targeting APE1/Ref-1 Using Dietary Agents. J. Oncol.,  2012, 2012370481
[http://dx.doi.org/10.1155/2012/370481] [PMID: 22997517] 
[170] 
Evans, A.R.; Limp-Foster, M.; Kelley, M.R. Going APE over ref-1. Mutat. Res.,  2000, 461(2), 83-108.
[http://dx.doi.org/10.1016/S0921-8777(00)00046-X] [PMID: 11018583] 
[171] 
Zou, G.M.; Karikari, C.; Kabe, Y.; Handa, H.; Anders, R.A.; Maitra, A. The Ape-1/Ref-1 redox antagonist E3330 inhibits the growth of tumor endothelium and endothelial progenitor cells: therapeutic implications in tumor angiogenesis. J. Cell. Physiol.,  2009, 219(1), 209-218.
[http://dx.doi.org/10.1002/jcp.21666] [PMID: 19097035] 
[172] 
Kelley, M.R.; Luo, M.; Reed, A.; Su, D.; Delaplane, S.; Borch, R.F.; Nyland, R.L., II; Gross, M.L.; Georgiadis, M.M. 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.
[http://dx.doi.org/10.1089/ars.2010.3410] [PMID: 20874257] 
[173] 
Bennett, S.E.; Kitner, J. Characterization of the aldehyde reactive probe reaction with AP-sites in DNA: influence of AP-lyase on adduct stability. Nucleosides Nucleotides Nucleic Acids,  2006, 25(7), 823-842.
[http://dx.doi.org/10.1080/15257770600726133] [PMID: 16898421] 
[174] 
Lau, J.P.; Weatherdon, K.L.; Skalski, V.; Hedley, D.W. Effects of gemcitabine on APE/ref-1 endonuclease activity in pancreatic cancer cells, and the therapeutic potential of antisense oligonucleotides. Br. J. Cancer,  2004, 91(6), 1166-1173.
[http://dx.doi.org/10.1038/sj.bjc.6602080] [PMID: 15316562] 
[175] 
Mendez, F.; Goldman, J.D.; Bases, R.E. Abasic sites in DNA of HeLa cells induced by lucanthone. Cancer Invest.,  2002, 20(7-8), 983-991.
[http://dx.doi.org/10.1081/CNV-120005914] [PMID: 12449731] 
[176] 
Turner, S.; Bases, R.; Pearlman, A.; Nobler, M.; Kabakow, B. The adjuvant effect of lucanthone (miracil D) in clinical radiation therapy. Radiology,  1975, 114(3), 729-731.
[http://dx.doi.org/10.1148/114.3.729] [PMID: 1118579] 
[177] 
Truong, M.T. Current role of radiation therapy in the management of malignant brain tumors. Hematol. Oncol. Clin. North Am.,  2006, 20(2), 431-453.
[http://dx.doi.org/10.1016/j.hoc.2006.01.022] [PMID: 16730301] 
[178] 
Herring, C.J.; West, C.M.; Wilks, D.P.; Davidson, S.E.; Hunter, R.D.; Berry, P.; Forster, G.; MacKinnon, J.; Rafferty, J.A.; Elder, R.H.; Hendry, J.H.; Margison, G.P. Levels of the DNA repair enzyme human apurinic/apyrimidinic endonuclease (APE1, APEX, Ref-1) are associated with the intrinsic radiosensitivity of cervical cancers. Br. J. Cancer,  1998, 78(9), 1128-1133.
[http://dx.doi.org/10.1038/bjc.1998.641] [PMID: 9820167] 
[179] 
Koukourakis, M.I.; Giatromanolaki, A.; Kakolyris, S.; Sivridis, E.; Georgoulias, V.; Funtzilas, G.; Hickson, I.D.; Gatter, K.C.; Harris, A.L. 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.,  2001, 50(1), 27-36.
[http://dx.doi.org/10.1016/S0360-3016(00)01561-3] [PMID: 11316543] 
[180] 
Herring, C.J.; Deans, B.; Elder, R.H.; Rafferty, J.A.; MacKinnon, J.; Barzilay, G.; Hickson, I.D.; Hendry, J.H.; Margison, G.P. Expression levels of the DNA repair enzyme HAP1 do not correlate with the radiosensitivities of human or HAP1-transfected rat cell lines. Br. J. Cancer,  1999, 80(7), 940-945.
[http://dx.doi.org/10.1038/sj.bjc.6690447] [PMID: 10362100] 
[181] 
Naidu, M.D.; Mason, J.M.; Pica, R.V.; Fung, H.; Peña, L.A. Radiation resistance in glioma cells determined by DNA damage repair activity of Ape1/Ref-1. J. Radiat. Res. (Tokyo),  2010, 51(4), 393-404.
[http://dx.doi.org/10.1269/jrr.09077] [PMID: 20679741] 
[182] 
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.; Hickson, I.D. Isolation of a small molecule inhibitor of DNA base excision repair. Nucleic Acids Res.,  2005, 33(15), 4711-4724.
[http://dx.doi.org/10.1093/nar/gki781] [PMID: 16113242] 
[183] 
Earle, J.D.; Foley, J.F.; Wieand, H.S.; Kvols, L.K.; McKenna, P.J.; Krook, J.E.; Tschetter, L.K.; Schutt, A.J.; Twito, D.I. Evaluation of external-beam radiation therapy plus 5-fluorouracil (5-FU) versus external-beam radiation therapy plus hycanthone (HYC) in confined, unresectable pancreatic cancer. Int. J. Radiat. Oncol. Biol. Phys.,  1994, 28(1), 207-211.
[http://dx.doi.org/10.1016/0360-3016(94)90159-7] [PMID: 8270443] 
[184] 
Wilson, D.M., III; Simeonov, A. Small molecule inhibitors of DNA repair nuclease activities of APE1. Cell. Mol. Life Sci.,  2010, 67(21), 3621-3631.
[http://dx.doi.org/10.1007/s00018-010-0488-2] [PMID: 20809131] 
[185] 
Gullett, N.P.; Ruhul Amin, A.R.; Bayraktar, S.; Pezzuto, J.M.; Shin, D.M.; Khuri, F.R.; Aggarwal, B.B.; Surh, Y.J.; Kucuk, O. Cancer prevention with natural compounds. Semin. Oncol.,  2010, 37(3), 258-281.
[http://dx.doi.org/10.1053/j.seminoncol.2010.06.014] [PMID: 20709209] 
[186] 
Yang, S.; Irani, K.; Heffron, S.E.; Jurnak, F.; Meyskens, F.L., Jr Alterations in the expression of the apurinic/apyrimidinic endonuclease-1/redox factor-1 (APE/Ref-1) in human melanoma and identification of the therapeutic potential of resveratrol as an APE/Ref-1 inhibitor. Mol. Cancer Ther.,  2005, 4(12), 1923-1935.
[http://dx.doi.org/10.1158/1535-7163.MCT-05-0229] [PMID: 16373707] 
[187] 
Raffoul, J.J.; Banerjee, S.; Singh-Gupta, V.; Knoll, Z.E.; Fite, A.; Zhang, H.; Abrams, J.; Sarkar, F.H.; Hillman, G.G. Down-regulation of apurinic/apyrimidinic endonuclease 1/redox factor-1 expression by soy isoflavones enhances prostate cancer radiotherapy in vitro and in vivo. Cancer Res.,  2007, 67(5), 2141-2149.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-2147] [PMID: 17332344] 
[188] 
Singh-Gupta, V.; Joiner, M. C.; Runyan, L.; Yunker, C. K.; Sarkar, F. H.; Miller, S.; Gadgeel, S. M.; Konski, A. A.; Hillman, G. G.   Soy isoflavones augment radiation effect by
    inhibiting APE1/Ref-1 DNA repair activity in non-small
    cell lung cancer. Journal of thoracic oncology : official
    publication of the International Association for the Study of
    Lung Cancer, 2011, 6(4), 688-98
[189] 
NIH Clinical Trial Database. www.clinicaltrials.gov
[190] 
Atkins, R. J.; Ng, W.; Stylli, S. S.; Hovens, C. M.; Kaye, A. H. Repair mechanisms help glioblastoma resist treatment.
    Journal of clinical neuroscience : official journal of the
    Neurosurgical Society of Australasia, 2015, 22(1), 14-20. 
[191] 
Montaldi, A.P.; Godoy, P.R.; Sakamoto-Hojo, E.T. APE1/REF-1 down-regulation enhances the cytotoxic effects of temozolomide in a resistant glioblastoma cell line. Mutat. Res. Genet. Toxicol. Environ. Mutagen.,  2015, 793, 19-29.
[http://dx.doi.org/10.1016/j.mrgentox.2015.06.001] [PMID: 26520369] 
[192] 
Gewirtz, D.A. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem. Pharmacol.,  1999, 57(7), 727-741.
[http://dx.doi.org/10.1016/S0006-2952(98)00307-4] [PMID: 10075079] 
[193] 
Chen, S.; Xiong, G.; Wu, S.; Mo, J. Downregulation of apurinic/apyrimidinic endonuclease 1/redox factor-1 enhances the sensitivity of human pancreatic cancer cells to radiotherapy in vitro. Cancer Biother. Radiopharm.,  2013, 28(2), 169-176.
[http://dx.doi.org/10.1089/cbr.2012.1266] [PMID: 23268706] 
[194] 
Gavrilov, K.; Saltzman, W.M. Therapeutic siRNA: principles, challenges, and strategies. Yale J. Biol. Med.,  2012, 85(2), 187-200.
[PMID: 22737048] 
[195] 
Haller, D.G. Chemotherapy for advanced pancreatic cancer. Int. J. Radiat. Oncol. Biol. Phys.,  2003, 56(4)(Suppl.), 16-23.
[http://dx.doi.org/10.1016/S0360-3016(03)00448-6] [PMID: 12826247] 
[196] 
Donley, N.; Jaruga, P.; Coskun, E.; Dizdaroglu, M.; McCullough, A.K.; Lloyd, R.S. Small Molecule Inhibitors of 8-Oxoguanine DNA Glycosylase-1 (OGG1). ACS Chem. Biol.,  2015, 10(10), 2334-2343.
[http://dx.doi.org/10.1021/acschembio.5b00452] [PMID: 26218629] 
[197] 
Tahara, Y.K.; Auld, D.; Ji, D.; Beharry, A.A.; Kietrys, A.M.; Wilson, D.L.; Jimenez, M.; King, D.; Nguyen, Z.; Kool, E.T. Potent and Selective Inhibitors of 8-Oxoguanine DNA Glycosylase. J. Am. Chem. Soc.,  2018, 140(6), 2105-2114.
[http://dx.doi.org/10.1021/jacs.7b09316] [PMID: 29376367] 
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DOI https://dx.doi.org/10.2174/0929867326666190430092732	Print ISSN 0929-8673
Publisher Name Bentham Science Publisher	Online ISSN 1875-533X
Current Medicinal Chemistry

Redox Regulation in the Base Excision Repair Pathway: Old and New Players as Cancer Therapeutic Targets

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