Ligands for Abasic Site-containing DNA and their Use as Fluorescent
Probes

Julika      Schlosser; Heiko      Ihmels
doi:10.2174/1570179419666220216091422
Abstract

Apurinic and apyrimidinic sites, also referred to as abasic or AP sites, are residues of duplex DNA in which one DNA base is removed from a Watson-Crick base pair. They are formed during the enzymatic repair of DNA and offer binding sites for a variety of guest molecules. Specifically, the AP site may bind an appropriate ligand as a substitute for the missing nucleic base, thus stabilizing the abasic site-containing DNA (AP-DNA). Notably, ligands that bind selectively to abasic sites may be employed for analytical and therapeutical purposes. As a result, there is a search for structural features that establish a strong and selective association of a given ligand with the abasic position in DNA. Against this background, this review provides an overview of the different classes of ligands for abasic site-containing DNA (AP-DNA). This review covers covalently binding substrates, namely amine and oxyamine derivatives, as well as ligands that bind to AP-DNA by noncovalent association, as represented by small heterocyclic aromatic compounds, metal-organic complexes, macrocyclic cyclophanes, and intercalator-nucleobase conjugates. As the systematic development of fluorescent probes for AP-DNA has been somewhat neglected so far, this review article contains a survey of the available reports on the fluorimetric response of the ligand upon binding to the AP-DNA. Based on these data, this compilation shall present a perspective for future developments of fluorescent probes for AP-DNA.
Keywords: Nucleic acids, DNA recognition, heterocyclic arenes, metal-organic compounds, fluorescence, cancer.
« Previous Next »
Graphical Abstract

[1]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN Estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin.,  2021, 71(3), 209-249.
 [http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]

[2]
DeVita, V.T., Jr; Chu, E. A history of cancer chemotherapy. Cancer Res.,  2008, 68(21), 8643-8653.
 [http://dx.doi.org/10.1158/0008-5472.CAN-07-6611] [PMID: 18974103]

[3]
Mukherjee, A.; Sasikala, W.D. Drug-DNA intercalation: From discovery to the molecular mechanism. Adv. Protein Chem. Struct. Biol.,  2013, 92, 1-62.
 [http://dx.doi.org/10.1016/B978-0-12-411636-8.00001-8] [PMID: 23954098]

[4]
Neidle, S.; Thurston, D.E. Chemical approaches to the discovery and development of cancer therapies. Nat. Rev. Cancer,  2005, 5(4), 285-296.
 [http://dx.doi.org/10.1038/nrc1587] [PMID: 15803155]

[5]
Rahman, A.; O’Sullivan, P.; Rozas, I. Recent developments in compounds acting in the DNA minor groove. MedChemComm,  2018, 10(1), 26-40.
 [http://dx.doi.org/10.1039/C8MD00425K] [PMID: 30774852]

[6]
Bhaduri, S.; Ranjan, N.; Arya, D.P. An overview of recent advances in duplex DNA recognition by small molecules. Beilstein J. Org. Chem.,  2018, 14, 1051-1086.
 [http://dx.doi.org/10.3762/bjoc.14.93] [PMID: 29977379]

[7]
Rescifina, A.; Zagni, C.; Varrica, M.G.; Pistarà, V.; Corsaro, A. Recent advances in small organic molecules as DNA intercalating agents: Synthesis, activity, and modeling. Eur. J. Med. Chem.,  2014, 74, 95-115.
 [http://dx.doi.org/10.1016/j.ejmech.2013.11.029] [PMID: 24448420]

[8]
Boga, S.; Bouzada, D.; García Peña, D.; Vázquez López, M.; Vázquez, M.E. Sequence-specific DNA recognition with designed peptides. Eur. J. Org. Chem.,  2018, 2018(3), 249-261.
 [http://dx.doi.org/10.1002/ejoc.201700988]

[9]
Wang, M.; Yu, Y.; Liang, C.; Lu, A.; Zhang, G. Recent advances in developing small molecules targeting nucleic acid. Int. J. Mol. Sci.,  2016, 17(6), 779-803.
 [http://dx.doi.org/10.3390/ijms17060779] [PMID: 27248995]

[10]
Banerjee, S.; Veale, E.B.; Phelan, C.M.; Murphy, S.A.; Tocci, G.M.; Gillespie, L.J.; Frimannsson, D.O.; Kelly, J.M.; Gunnlaugsson, T. Recent advances in the development of 1,8-naphthalimide based DNA targeting binders, anticancer and fluorescent cellular imaging agents. Chem. Soc. Rev.,  2013, 42(4), 1601-1618.
 [http://dx.doi.org/10.1039/c2cs35467e] [PMID: 23325367]

[11]
Wang, X.; Guo, Z. Targeting and delivery of platinum-based anticancer drugs. Chem. Soc. Rev.,  2013, 42(1), 202-224.
 [http://dx.doi.org/10.1039/C2CS35259A] [PMID: 23042411]

[12]
Komor, A.C.; Barton, J.K. The path for metal complexes to a DNA target. Chem. Commun. (Camb.),  2013, 49(35), 3617-3630.
 [http://dx.doi.org/10.1039/c3cc00177f] [PMID: 23423158]

[13]
Nakatani, K.; Tor, Y. Eds.; Modified Nucleic Acids; Springer International Publishing: Cham, 2016.
 [http://dx.doi.org/10.1007/978-3-319-27111-8]

[14]
Granzhan, A.; Kotera, N.; Teulade-Fichou, M-P. Finding needles in a basestack: Recognition of mismatched base pairs in DNA by small molecules. Chem. Soc. Rev.,  2014, 43(10), 3630-3665.
 [http://dx.doi.org/10.1039/c3cs60455a] [PMID: 24634921]

[15]
Du, Y.H.; Huang, J.; Weng, X.C.; Zhou, X. Specific recognition of DNA by small molecules. Curr. Med. Chem.,  2010, 17(2), 173-189.
 [http://dx.doi.org/10.2174/092986710790112648] [PMID: 20015047]

[16]
Chen, J.; Gill, A.D.; Hickey, B.L.; Gao, Z.; Cui, X.; Hooley, R.J.; Zhong, W. Machine learning aids classification and discrimination of noncanonical DNA folding motifs by an arrayed host: Guest sensing system. J. Am. Chem. Soc.,  2021, 143(32), 12791-12799.
 [http://dx.doi.org/10.1021/jacs.1c06031] [PMID: 34346209]

[17]
Hrabina, O.; Malina, J.; Scott, P.; Brabec, V. Cationic FeII triplex-forming metallohelices as DNA bulge binders. Chem. Eur. J.,  2020, 26(69), 16554-16562.
 [http://dx.doi.org/10.1002/chem.202004060] [PMID: 33026666]

[18]
Kumar, M.; Kaushik, M.; Kukreti, S. Interaction of a photosensitizer methylene blue with various structural forms (cruciform, bulge duplex and hairpin) of designed DNA sequences. Spectrochim. Acta A Mol. Biomol. Spectrosc.,  2020, 242, 118716.
 [http://dx.doi.org/10.1016/j.saa.2020.118716] [PMID: 32731146]

[19]
Summers, P.A.; Lewis, B.W.; Gonzalez-Garcia, J.; Porreca, R.M.; Lim, A.H.M.; Cadinu, P.; Martin-Pintado, N.; Mann, D.J.; Edel, J.B.; Vannier, J.B.; Kuimova, M.K.; Vilar, R. Visualising G-quadruplex DNA dynamics in live cells by fluorescence lifetime imaging microscopy. Nat. Commun.,  2021, 12(1), 162.
 [http://dx.doi.org/10.1038/s41467-020-20414-7] [PMID: 33420085]

[20]
Zhang, L.; Liu, X.; Lu, S.; Liu, J.; Zhong, S.; Wei, Y.; Bing, T.; Zhang, N.; Shangguan, D. Thiazole orange styryl derivatives as fluorescent probes for G-quadruplex DNA. ACS Appl. Bio Mater.,  2020, 3(5), 2643-2650.
 [http://dx.doi.org/10.1021/acsabm.9b01243] [PMID: 35025398]

[21]
Zhai, Q.; Gao, C.; Ding, J.; Zhang, Y.; Islam, B.; Lan, W.; Hou, H.; Deng, H.; Li, J.; Hu, Z.; Mohamed, H.I.; Xu, S.; Cao, C.; Haider, S.M.; Wei, D. Selective recognition of c-MYC Pu22 G-quadruplex by a fluorescent probe. Nucleic Acids Res.,  2019, 47(5), 2190-2204.
 [http://dx.doi.org/10.1093/nar/gkz059] [PMID: 30759259]

[22]
Chaudhuri, R.; Bhattacharya, S.; Dash, J.; Bhattacharya, S. Recent update on targeting c-MYC G-quadruplexes by small molecules for anticancer therapeutics. J. Med. Chem.,  2021, 64(1), 42-70.
 [http://dx.doi.org/10.1021/acs.jmedchem.0c01145] [PMID: 33355454]

[23]
Reznichenko, O.; Cucchiarini, A.; Gabelica, V.; Granzhan, A. Quadruplex DNA-guided ligand selection from dynamic combinatorial libraries of acylhydrazones. Org. Biomol. Chem.,  2021, 19(2), 379-386.
 [http://dx.doi.org/10.1039/D0OB01908A] [PMID: 33325973]

[24]
Zhao, J.; Yang, Z.; Zhai, Q.; Wei, D. Specific recognition of telomeric multimeric G-quadruplexes by a simple-structure quinoline derivative. Anal. Chim. Acta,  2020, 1132, 93-100.
 [http://dx.doi.org/10.1016/j.aca.2020.07.017] [PMID: 32980115]

[25]
O’Hagan, M.P.; Haldar, S.; Morales, J.C.; Mulholland, A.J.; Galan, M.C. Enhanced sampling molecular dynamics simulations correctly predict the diverse activities of a series of stiff-stilbene G-quadruplex DNA ligands. Chem. Sci. (Camb.),  2020, 12(4), 1415-1426.
 [http://dx.doi.org/10.1039/D0SC05223J] [PMID: 34163904]

[26]
Thiagarajan, V.; Rajendran, A.; Satake, H.; Nishizawa, S.; Teramae, N. NBD-based green fluorescent ligands for typing of thymine-related SNPs by using an abasic site-containing probe DNA. ChemBioChem,  2010, 11(1), 94-100.
 [http://dx.doi.org/10.1002/cbic.200900530] [PMID: 19950344]

[27]
Schärer, O.D. Chemistry and biology of DNA repair. Angew. Chem. Int. Ed.,  2003, 42(26), 2946-2974.
 [http://dx.doi.org/10.1002/anie.200200523] [PMID: 12851945]

[28]
Thompson, P.S.; Cortez, D. New insights into abasic site repair and tolerance. DNA Repair (Amst.),  2020, 90, 102866-112877.
 [http://dx.doi.org/10.1016/j.dnarep.2020.102866] [PMID: 32417669]

[29]
Nakamura, J.; Swenberg, J.A. Endogenous apurinic/apyrimidinic sites in genomic DNA of mammalian tissues. Cancer Res.,  1999, 59(11), 2522-2526.
 [PMID: 10363965]

[30]
Guillet, M.; Boiteux, S. Origin of endogenous DNA abasic sites in Saccharomyces cerevisiae. Mol. Cell. Biol.,  2003, 23(22), 8386-8394.
 [http://dx.doi.org/10.1128/MCB.23.22.8386-8394.2003] [PMID: 14585995]

[31]
Krokan, H.E.; Bjørås, M. Base excision repair. Cold Spring Harb. Perspect. Biol.,  2013, 5(4), a012583-a012605.
 [http://dx.doi.org/10.1101/cshperspect.a012583] [PMID: 23545420]

[32]
Lindahl, T.; Wood, R.D. Quality control by DNA repair. Science,  1999, 286(5446), 1897-1905.
 [http://dx.doi.org/10.1126/science.286.5446.1897] [PMID: 10583946]

[33]
Demeunynck, M.; Bailly, C.; Wilson, W.D. Small molecule DNA and RNA binders: From synthesis to nucleic acid complexes; Wiley-VCH: Weinheim, 2003. 

[34]
Kitsera, N.; Rodriguez-Alvarez, M.; Emmert, S.; Carell, T.; Khobta, A. Nucleotide excision repair of abasic DNA lesions. Nucleic Acids Res.,  2019, 47(16), 8537-8547.
 [http://dx.doi.org/10.1093/nar/gkz558] [PMID: 31226203]

[35]
Marin, J.J.G.; Sanchez de Medina, F.; Castaño, B.; Bujanda, L.; Romero, M.R.; Martinez-Augustin, O.; Moral-Avila, R.D.; Briz, O. Chemoprevention, chemotherapy, and chemoresistance in colorectal cancer. Drug Metab. Rev.,  2012, 44(2), 148-172.
 [http://dx.doi.org/10.3109/03602532.2011.638303] [PMID: 22497631]

[36]
Fu, D.; Calvo, J.A.; Samson, L.D. Balancing repair and tolerance of DNA damage caused by alkylating agents. Nat. Rev. Cancer,  2012, 12(2), 104-120.
 [http://dx.doi.org/10.1038/nrc3185] [PMID: 22237395]

[37]
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]

[38]
Silber, J.R.; Bobola, M.S.; Blank, A.; Schoeler, K.D.; Haroldson, P.D.; Huynh, M.B.; Kolstoe, D.D. The apurinic/apyrimidinic endonuclease activity of Ape1/Ref-1 contributes to human glioma cell resistance to alkylating agents and is elevated by oxidative stress. Clin. Cancer Res.,  2002, 8(9), 3008-3018.
 [PMID: 12231548]

[39]
Poletto, M.; Legrand, A.J.; Dianov, G.L. DNA base excision repair: The Achilles’ heel of tumour cells and their microenvironment? Curr. Pharm. Des.,  2017, 23(32), 4758-4772.
 [http://dx.doi.org/10.2174/1381612823666170710123602] [PMID: 28699540]

[40]
Sharbeen, G.; McCarroll, J.; Goldstein, D.; Phillips, P.A. Exploiting base excision repair to improve therapeutic approaches for pancreatic cancer. Front. Nutr.,  2015, 2, 10-21.
 [http://dx.doi.org/10.3389/fnut.2015.00010] [PMID: 25988138]

[41]
Barakat, K.H.; Gajewski, M.M.; Tuszynski, J.A. DNA polymerase beta (pol β) inhibitors: A comprehensive overview. Drug Discov. Today,  2012, 17(15-16), 913-920.
 [http://dx.doi.org/10.1016/j.drudis.2012.04.008] [PMID: 22561893]

[42]
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]

[43]
Haq, I. Thermodynamics of drug-DNA interactions. Arch. Biochem. Biophys.,  2002, 403(1), 1-15.
 [http://dx.doi.org/10.1016/S0003-9861(02)00202-3] [PMID: 12061796]

[44]
Han, X.; Gao, X. Sequence specific recognition of ligand-DNA complexes studied by NMR. Curr. Med. Chem.,  2001, 8(5), 551-581.
 [http://dx.doi.org/10.2174/0929867003373337] [PMID: 11281842]

[45]
Chang, Y-M.; Chen, C.K-M.; Hou, M-H. Conformational changes in DNA upon ligand binding monitored by circular dichroism. Int. J. Mol. Sci.,  2012, 13(3), 3394-3413.
 [http://dx.doi.org/10.3390/ijms13033394] [PMID: 22489158]

[46]
Nordén, B.; Kurucsev, T. Analysing DNA complexes by circular and linear dichroism. J. Mol. Recognit.,  1994, 7(2), 141-155.
 [http://dx.doi.org/10.1002/jmr.300070211] [PMID: 7826674]

[47]
Jenkins, T.C. Optical Absorbance and Fluorescence Techniques for Measuring DNA–Drug Interactions.Drug-DNA Interaction Protocols; Fox, K.R., Ed.; Humana Press: Totowa, NJ, 1997, pp. 195-218.
 [http://dx.doi.org/10.1385/0-89603-447-X:195]

[48]
Kumar, S.; Pandya, P.; Pandav, K.; Gupta, S.P.; Chopra, A. Structural studies on ligand-DNA systems: A robust approach in drug design. J. Biosci.,  2012, 37(3), 553-561.
 [http://dx.doi.org/10.1007/s12038-012-9212-8] [PMID: 22750991]

[49]
Sirajuddin, M.; Ali, S.; Badshah, A. Drug-DNA interactions and their study by UV-Visible, fluorescence spectroscopies and cyclic voltametry. J. Photochem. Photobiol. B,  2013, 124, 1-19.
 [http://dx.doi.org/10.1016/j.jphotobiol.2013.03.013] [PMID: 23648795]

[50]
Xu, W.; Chan, K.M.; Kool, E.T. Fluorescent nucleobases as tools for studying DNA and RNA. Nat. Chem.,  2017, 9(11), 1043-1055.
 [http://dx.doi.org/10.1038/nchem.2859] [PMID: 29064490]

[51]
Duval, R.; Duplais, C. Fluorescent natural products as probes and tracers in biology. Natl. Prod. Rev.,  2017, 34(2), 161-193.
 [http://dx.doi.org/10.1039/C6NP00111D] [PMID: 28125109]

[52]
Boutorine, A.S.; Novopashina, D.S.; Krasheninina, O.A.; Nozeret, K.; Venyaminova, A.G. Fluorescent probes for nucleic Acid visualization in fixed and live cells. Molecules,  2013, 18(12), 15357-15397.
 [http://dx.doi.org/10.3390/molecules181215357] [PMID: 24335616]

[53]
Su, X.; Xiao, X.; Zhang, C.; Zhao, M. Nucleic acid fluorescent probes for biological sensing. Appl. Spectrosc.,  2012, 66(11), 1249-1262.
 [http://dx.doi.org/10.1366/12-06803] [PMID: 23146180]

[54]
Vummidi, B.R.; Alzeer, J.; Luedtke, N.W. Fluorescent probes for G-quadruplex structures. ChemBioChem,  2013, 14(5), 540-558.
 [http://dx.doi.org/10.1002/cbic.201200612] [PMID: 23440895]

[55]
Ehrenschwender, T.; Varga, B.R.; Kele, P.; Wagenknecht, H-A. New far-red and near-infrared fluorescent probes with large Stokes shifts for dual covalent labeling of DNA. Chem. Asian J.,  2010, 5(8), 1761-1764.
 [http://dx.doi.org/10.1002/asia.201000081] [PMID: 20589826]

[56]
Schwechheimer, C.; Rönicke, F.; Schepers, U.; Wagenknecht, H-A. A new structure-activity relationship for cyanine dyes to improve photostability and fluorescence properties for live cell imaging. Chem. Sci. (Camb.),  2018, 9(31), 6557-6563.
 [http://dx.doi.org/10.1039/C8SC01574K] [PMID: 30310587]

[57]
Walter, H-K.; Olshausen, B.; Schepers, U.; Wagenknecht, H-A. A postsynthetically 2'-“clickable” uridine with arabino configuration and its application for fluorescent labeling and imaging of DNA. Beilstein J. Org. Chem.,  2017, 13, 127-137.
 [http://dx.doi.org/10.3762/bjoc.13.16] [PMID: 28228854]

[58]
Saeed, H.K.; Sreedharan, S.; Thomas, J.A. Photoactive metal complexes that bind DNA and other biomolecules as cell probes, therapeutics, and theranostics. Chem. Commun. (Camb.),  2020, 56(10), 1464-1480.
 [http://dx.doi.org/10.1039/C9CC09312E] [PMID: 31967621]

[59]
Ban, Ž.; Griesbeck, S. Tomić S.; Nitsch, J.; Marder, T.B.; Piantanida, I. A quadrupolar bis-triarylborane chromophore as a fluorimetric and chirooptic probe for simultaneous and selective sensing of DNA, RNA and proteins. Chem. Eur. J.,  2020, 26(10), 2195-2203.
 [http://dx.doi.org/10.1002/chem.201903936] [PMID: 31756013]

[60]
Gao, Y.; He, Z.; He, X.; Zhang, H.; Weng, J.; Yang, X.; Meng, F.; Luo, L.; Tang, B.Z. Dual-color emissive AIEgen for specific and label-free double-stranded DNA recognition and single-nucleotide polymorphisms detection. J. Am. Chem. Soc.,  2019, 141(51), 20097-20106.
 [http://dx.doi.org/10.1021/jacs.9b09239] [PMID: 31721575]

[61]
Peveler, W.J.; Algar, W.R. More than a light switch: Engineering unconventional fluorescent configurations for biological sensing. ACS Chem. Biol.,  2018, 13(7), 1752-1766.
 [http://dx.doi.org/10.1021/acschembio.7b01022] [PMID: 29461796]

[62]
Chyan, W.; Raines, R.T. Enzyme-activated fluorogenic probes for live-cell and in vivo imaging. ACS Chem. Biol.,  2018, 13(7), 1810-1823.
 [http://dx.doi.org/10.1021/acschembio.8b00371] [PMID: 29924581]

[63]
Schulte, L.N.; Heinrich, B.; Janga, H.; Schmeck, B.T.; Vázquez, O. A far-red fluorescent DNA binder for interaction studies of live multidrug-resistant pathogens and host cells. Angew. Chem. Int. Ed. Engl.,  2018, 57(36), 11564-11568.
 [http://dx.doi.org/10.1002/anie.201804090] [PMID: 29972713]

[64]
Boturyn, D.; Boudali, A.; Constant, J-F.; Defrancq, E.; Lhomme, J. Synthesis of fluorescent probes for the detection of abasic sites in DNA. Tetrahedron,  1997, 53(15), 5485-5492.
 [http://dx.doi.org/10.1016/S0040-4020(97)00235-4]

[65]
Boynton, A.N.; Marcélis, L.; McConnell, A.J.; Barton, J.K.A. A ruthenium(II) complex as a luminescent probe for DNA mismatches and abasic sites. Inorg. Chem.,  2017, 56(14), 8381-8389.
 [http://dx.doi.org/10.1021/acs.inorgchem.7b01037] [PMID: 28657712]

[66]
Wu, F.; Shao, Y.; Ma, K.; Cui, Q.; Liu, G.; Xu, S. Simultaneous fluorescence light-up and selective multicolor nucleobase recognition based on sequence-dependent strong binding of berberine to DNA abasic site. Org. Biomol. Chem.,  2012, 10(16), 3300-3307.
 [http://dx.doi.org/10.1039/c2ob00028h] [PMID: 22410866]

[67]
Nishizawa, S.; Yoshimoto, K.; Seino, T.; Xu, C-Y.; Minagawa, M.; Satake, H.; Tong, A.; Teramae, N. Fluorescence detection of cytosine/guanine transversion based on a hydrogen bond forming ligand. Talanta,  2004, 63(1), 175-179.
 [http://dx.doi.org/10.1016/j.talanta.2003.09.027] [PMID: 18969416]

[68]
Morita, K.; Sato, Y.; Seino, T.; Nishizawa, S.; Teramae, N. Fluorescence and electrochemical detection of pyrimidine/purine transversion by a ferrocenyl aminonaphthyridine derivative. Org. Biomol. Chem.,  2008, 6(2), 266-268.
 [http://dx.doi.org/10.1039/B716682F] [PMID: 18174994]

[69]
Yoshimoto, K.; Xu, C-Y.; Nishizawa, S.; Haga, T.; Satake, H.; Teramae, N. Fluorescence detection of guanine-adenine transition by a hydrogen bond forming small compound. Chem. Commun. (Camb.),  2003, 24(24), 2960-2961.
 [http://dx.doi.org/10.1039/B309229A] [PMID: 14703807]

[70]
Lhomme, J.; Constant, J.F.; Demeunynck, M. Abasic DNA structure, reactivity, and recognition. Biopolymers,  1999, 52(2), 65-83.
 [http://dx.doi.org/10.1002/1097-0282(1999)52:2<65:AID-BIP1>3.0.CO;2-U] [PMID: 10898853]

[71]
Greenberg, M.M. Abasic and oxidized abasic site reactivity in DNA: enzyme inhibition, cross-linking, and nucleosome catalyzed reactions. Acc. Chem. Res.,  2014, 47(2), 646-655.
 [http://dx.doi.org/10.1021/ar400229d] [PMID: 24369694]

[72]
Catalano, M.J.; Liu, S.; Andersen, N.; Yang, Z.; Johnson, K.M.; Price, N.E.; Wang, Y.; Gates, K.S. Chemical structure and properties of interstrand cross-links formed by reaction of guanine residues with abasic sites in duplex DNA. J. Am. Chem. Soc.,  2015, 137(11), 3933-3945.
 [http://dx.doi.org/10.1021/jacs.5b00669] [PMID: 25710271]

[73]
Johnson, K.M.; Price, N.E.; Wang, J.; Fekry, M.I.; Dutta, S.; Seiner, D.R.; Wang, Y.; Gates, K.S. On the formation and properties of interstrand DNA-DNA cross-links forged by reaction of an abasic site with the opposing guanine residue of 5'-CAp sequences in duplex DNA. J. Am. Chem. Soc.,  2013, 135(3), 1015-1025.
 [http://dx.doi.org/10.1021/ja308119q] [PMID: 23215239]

[74]
Nejad, M.I.; Price, N.E.; Haldar, T.; Lewis, C.; Wang, Y.; Gates, K.S. Interstrand DNA cross-links derived from reaction of a 2-aminopurine residue with an abasic site. ACS Chem. Biol.,  2019, 14(7), 1481-1489.
 [http://dx.doi.org/10.1021/acschembio.9b00208] [PMID: 31259519]

[75]
Admiraal, S.J.; O’Brien, P.J. Reactivity and cross-linking of 5'-terminal abasic sites within DNA. Chem. Res. Toxicol.,  2017, 30(6), 1317-1326.
 [http://dx.doi.org/10.1021/acs.chemrestox.7b00057] [PMID: 28485930]

[76]
Thompson, P.S.; Amidon, K.M.; Mohni, K.N.; Cortez, D.; Eichman, B.F. Protection of abasic sites during DNA replication by a stable thiazolidine protein-DNA cross-link. Nat. Struct. Mol. Biol.,  2019, 26(7), 613-618.
 [http://dx.doi.org/10.1038/s41594-019-0255-5] [PMID: 31235915]

[77]
Mohni, K.N.; Wessel, S.R.; Zhao, R.; Wojciechowski, A.C.; Luzwick, J.W.; Layden, H.; Eichman, B.F.; Thompson, P.S.; Mehta, K.P.M.; Cortez, D. HMCES maintains genome integrity by shielding abasic sites in single-strand DNA. Cell,  2019, 176(1-2), 144-153.e13.
 [http://dx.doi.org/10.1016/j.cell.2018.10.055] [PMID: 30554877]

[78]
Sutherland, B.M.; Georgakilas, A.G.; Bennett, P.V.; Laval, J.; Sutherland, J.C. Quantifying clustered DNA damage induction and repair by gel electrophoresis, electronic imaging and number average length analysis. Mutat. Res.,  2003, 531(1-2), 93-107.
 [http://dx.doi.org/10.1016/j.mrfmmm.2003.08.005] [PMID: 14637248]

[79]
Kotera, N.; Granzhan, A.; Teulade-Fichou, M-P. Comparative study of affinity and selectivity of ligands targeting abasic and mismatch sites in DNA using a fluorescence-melting assay. Biochimie,  2016, 128-129, 133-137.
 [http://dx.doi.org/10.1016/j.biochi.2016.08.004] [PMID: 27523781]

[80]
Brotschi, C.; Mathis, G.; Leumann, C.J. Bipyridyl- and biphenyl-DNA: A recognition motif based on interstrand aromatic stacking. Chem. Eur. J.,  2005, 11(6), 1911-1923.
 [http://dx.doi.org/10.1002/chem.200400858] [PMID: 15685710]

[81]
Shao, Y.; Niu, Z.; Zou, S. Preferential binding specificity of silver cation to a single nucleobase over base pairs evaluated by abasic site-containing DNA. Electrochem. Commun.,  2009, 11(2), 417-420.
 [http://dx.doi.org/10.1016/j.elecom.2008.12.005]

[82]
Ma, K.; Cui, Q.; Liu, G.; Wu, F.; Xu, S.; Shao, Y. DNA abasic site-directed formation of fluorescent silver nanoclusters for selective nucleobase recognition. Nanotechnology,  2011, 22(30), 305502-305508.
 [http://dx.doi.org/10.1088/0957-4484/22/30/305502] [PMID: 21719966]

[83]
Heinrich, F.; Riedel, M.; Lisdat, F. Detection of abasic DNA by means of impedance spectroscopy. Electrochem. Commun.,  2018, 90, 65-68.
 [http://dx.doi.org/10.1016/j.elecom.2018.04.005]

[84]
Singh, S.; Singh, M.K.; Das, P. Biosensing of solitary and clustered abasic site DNA damage lesions with copper nanoclusters and carbon dots. Sens. Actuators B Chem.,  2018, 255, 763-774.
 [http://dx.doi.org/10.1016/j.snb.2017.08.100]

[85]
Vaidyanathan, S.; Weerakoon-Ratnayake, K.M.; Uba, F.I.; Hu, B.; Kaufman, D.; Choi, J.; Park, S.; Soper, S.A. Thermoplastic nanofluidic devices for identifying abasic sites in single DNA molecules. Lab Chip,  2021, 21(8), 1579-1589.
 [http://dx.doi.org/10.1039/D0LC01038C] [PMID: 33651049]

[86]
Chaires, J.B.; Shi, X. Thermal Denaturation of Drug-DNA Complexes: Tools and Tricks.Sequence-specific DNA Binding Agents; Waring, M; Waring, M.J., Ed.; Royal Society of Chemistry: Cambridge, 2006, pp. 130-151.

[87]
Aufdembrink, L.M.; Hoog, T.G.; Pawlak, M.R.; Bachan, B.F.; Heili, J.M.; Engelhart, A.E. Methods for thermal denaturation studies of nucleic acids in complex with fluorogenic dyes. Methods Enzymol.,  2019, 623, 23-43.
 [http://dx.doi.org/10.1016/bs.mie.2019.05.029] [PMID: 31239049]

[88]
Spink, C.H.; Wellman, S.E. Thermal denaturation as tool to study DNA-ligand interactions. Methods Enzymol.,  2001, 340, 193-211.
 [http://dx.doi.org/10.1016/S0076-6879(01)40423-X] [PMID: 11494849]

[89]

Fox, K.R., Ed.; Methods in Enzymology; Humana Press: Totowa, NJ,; , 1997. 

[90]
Becher, J.; Berdnikova, D.V.; Ihmels, H.; Stremmel, C. Synthesis and investigation of quadruplex-DNA-binding, 9-O-substituted berberine derivatives. Beilstein J. Org. Chem.,  2020, 16, 2795-2806.
 [http://dx.doi.org/10.3762/bjoc.16.230] [PMID: 33281983]

[91]
Talpaert-Borlé, M.; Liuzzi, M. Reaction of apurinic/apyrimidinic sites with [14C]methoxyamine. A method for the quantitative assay of AP sites in DNA. Biochim. Biophys. Acta,  1983, 740(4), 410-416.
 [http://dx.doi.org/10.1016/0167-4781(83)90089-1] [PMID: 6349690]

[92]
Vasseur, J.J.; Rayner, B.; Imbach, J.L.; Verma, S.; McCloskey, J.A.; Lee, M.; Chang, D-K.; Lown, J.W. Structure of the adduct formed between 3-aminocarbazole and the apurinic site oligonucleotide model d. J. Org. Chem.,  1987, 52(22), 4994-4998. [Tp(Ap)pT
 [http://dx.doi.org/10.1021/jo00231a028]

[93]
Malvy, C.; Prévost, P.; Gansser, C.; Viel, C.; Paoletti, C. Efficient breakage of DNA apurinic sites by the indoleamine related 9-amino-ellipticine. Chem. Biol. Interact.,  1986, 57(1), 41-53.
 [http://dx.doi.org/10.1016/0009-2797(86)90047-5] [PMID: 3512111]

[94]
Kubo, K.; Ide, H.; Wallace, S.S.; Kow, Y.W. A novel, sensitive, and specific assay for abasic sites, the most commonly produced DNA lesion. Bio chemistry,  1992, 31(14), 3703-3708.
 [http://dx.doi.org/10.1021/bi00129a020] [PMID: 1567824]

[95]
Ide, H.; Akamatsu, K.; Kimura, Y.; Michiue, K.; Makino, K.; Asaeda, A.; Takamori, Y.; Kubo, K. Synthesis and damage specificity of a novel probe for the detection of abasic sites in DNA. Bio chemistry,  1993, 32(32), 8276-8283.
 [http://dx.doi.org/10.1021/bi00083a031] [PMID: 8347625]

[96]
Wei, S.; Perera, M.L.W.; Sakhtemani, R.; Bhagwat, A.S. A novel class of chemicals that react with abasic sites in DNA and specifically kill B cell cancers. PLoS One,  2017, 12(9), e0185010-e0185029.
 [http://dx.doi.org/10.1371/journal.pone.0185010] [PMID: 28926604]

[97]
Bertrand, J.R.; Vasseur, J.J.; Gouyette, A.; Rayner, B.; Imbach, J.L.; Paoletti, C.; Malvy, C. Mechanism of cleavage of apurinic sites by 9-aminoellipticine. J. Biol. Chem.,  1989, 264(24), 14172-14178.
 [http://dx.doi.org/10.1016/S0021-9258(18)71658-X] [PMID: 2760062]

[98]
Talpaert-Borlé, M. Formation, detection and repair of AP sites. Mutat. Res.,  1987, 181(1), 45-56.
 [http://dx.doi.org/10.1016/0027-5107(87)90286-7] [PMID: 2444877]

[99]
Vasseur, J-J.; Rayner, B.; Imbach, J-L.; Verla, S.; McCloskey, J.A.; Lown, J.W.; Chang, D.K. DNA apurinic sites: Synthesis of a model compound and study of its reactivity with 3-aminocarbazole. Nucleosides Nucleotides,  1987, 6(1-2), 467-468.
 [http://dx.doi.org/10.1080/07328318708056258]

[100]
Asaeda, A.; Ide, H.; Tano, K.; Takamori, Y.; Kubo, K. Repair kinetics of abasic sites in mammalian cells selectively monitored by the aldehyde reactive probe (ARP). Nucleosides Nucleotides,  1998, 17(1-3), 503-513.
 [http://dx.doi.org/10.1080/07328319808005194] [PMID: 9708359]

[101]
Asaeda, A.; Ide, H.; Terato, H.; Takamori, Y.; Kubo, K. Highly sensitive assay of DNA abasic sites in mammalian cells-optimization of the aldehyde reactive probe method. Anal. Chim. Acta,  1998, 365(1-3), 35-41.
 [http://dx.doi.org/10.1016/S0003-2670(97)00648-X]

[102]
Wang, D-M.; Jia, J.; Huang, R-F.; Zhang, X. A base-repair based electrochemiluminescent genotoxicity sensor that detects abasic sites in double-stranded DNA films. Chem. Commun. (Camb.),  2020, 56(83), 12558-12561.
 [http://dx.doi.org/10.1039/D0CC05186A] [PMID: 32940265]

[103]
Boturyn, D.; Defrancq, E.; Ducros, V.; Fontaine, C.; Lhomme, J. Quantitative one step derivatization of oligonucleotides by a fluorescent label through abasic site formation. Nucleosides Nucleotides,  1997, 16(10-11), 2069-2077.
 [http://dx.doi.org/10.1080/07328319708002556]

[104]
Boturyn, D.; Constant, J.F.; Defrancq, E.; Lhomme, J.; Barbin, A.; Wild, C.P. A simple and sensitive method for in vitro quantitation of abasic sites in DNA. Chem. Res. Toxicol.,  1999, 12(6), 476-482.
 [http://dx.doi.org/10.1021/tx980275g] [PMID: 10368309]

[105]
Yoshimoto, K.; Nishizawa, S.; Koshino, H.; Sato, Y.; Teramae, N.; Maeda, M. Assignment of hydrogen-bond structure in a ligand-nucleobase complex inside duplex DNA: combined use of quantum chemical calculations and 15N NMR experiments. Nucleic Acids Symp. Ser.,  2005, 49(49), 255-256.
 [http://dx.doi.org/10.1093/nass/49.1.255] [PMID: 17150730]

[106]
Sato, Y.; Seino, T.; Nishizawa, S.; Teramae, N. Thermodynamic characterization of the binding of naphthyridines to the AP site-containing DNA duplexes. Nucleic Acids Symp. Ser.,  2006, 50(50), 219-220.
 [http://dx.doi.org/10.1093/nass/nrl109] [PMID: 17150896]

[107]
Yoshimoto, K.; Nishizawa, S.; Minagawa, M.; Teramae, N. Use of abasic site-containing DNA strands for nucleobase recognition in water. J. Am. Chem. Soc.,  2003, 125(30), 8982-8983.
 [http://dx.doi.org/10.1021/ja029786m] [PMID: 15369332]

[108]
Atsumi, H.; Yoshimoto, K.; Saito, S.; Ohkuma, M.; Maeda, M.; Nagasaki, Y. Luminescence-based colorimetric discrimination of single-nucleotide transversions by the combined use of the derivatives of DOTA-conjugated naphthyridine and its terbium complex. Tetrahedron Lett.,  2009, 50(19), 2177-2180.
 [http://dx.doi.org/10.1016/j.tetlet.2009.02.152]

[109]
Yoshimoto, K.; Atsumi, H.; Saito, S.; Okuma, M.; Maeda, M.; Nagasaki, Y. Fluorescence-based affinity labeling of nucleobase by hydrogen-bond forming metal complex. Nucleic Acids Symp. Ser.,  2007, 51(51), 303-304.
 [http://dx.doi.org/10.1093/nass/nrm152] [PMID: 18029707]

[110]
Gao, Q.; Satake, H.; Dai, Q.; Ono, K.; Nishizawa, S.; Teramae, N. Strong binding of naphthyridine derivatives to a guanine base in DNA duplexes containing an AP site. Nucleic Acids Symp. Ser.,  2005, 49(49), 219-220.
 [http://dx.doi.org/10.1093/nass/49.1.219] [PMID: 17150712]

[111]
Sato, Y.; Nishizawa, S.; Yoshimoto, K.; Seino, T.; Ichihashi, T.; Morita, K.; Teramae, N. Influence of substituent modifications on the binding of 2-amino-1,8-naphthyridines to cytosine opposite an AP site in DNA duplexes: thermodynamic characterization. Nucleic Acids Res.,  2009, 37(5), 1411-1422.
 [http://dx.doi.org/10.1093/nar/gkn1079] [PMID: 19136458]

[112]
Li, X.; Xiong, M.; Huang, Y.; Zhang, L.; Zhao, S. Simple label-free fluorescence detection of apurinic/apyrimidinic endonuclease 1 activity and its inhibitor using the abasic site-binding fluorophore. Anal. Methods,  2019, 11(6), 739-743.
 [http://dx.doi.org/10.1039/C8AY02633E]

[113]
Satake, H.; Nishizawa, S.; Teramae, N. Ratiometric fluorescence detection of pyrimidine/purine transversion by using a 2-amino-1,8-naphthyridine derivative. Anal. Sci.,  2006, 22, 195-197.
 [http://dx.doi.org/10.2116/analsci.22.195] [PMID: 16512406]

[114]
Wang, C.X.; Sato, Y.; Kudo, M.; Nishizawa, S.; Teramae, N. Ratiometric fluorescent signaling of small molecule, environmentally sensitive dye conjugates for detecting single-base mutations in DNA. Chem. Eur. J.,  2012, 18(31), 9481-9484.
 [http://dx.doi.org/10.1002/chem.201200219] [PMID: 22733702]

[115]
Nishizawa, S.; Sato, Y.; Teramae, N. Recent progress in abasic site-binding small molecules for detecting single-base mutations in DNA. Anal. Sci.,  2014, 30(1), 137-142.
 [http://dx.doi.org/10.2116/analsci.30.137] [PMID: 24420255]

[116]
Morita, K.; Sato, Y.; Seino, T.; Nishizawa, S.; Teramae, N. Electrochemical and fluorescence detection of cytosine-related SNPs using a ferrocenyl naphthyridine derivative. Nucleic Acids Symp. Ser.,  2007, 51(1), 295-296.
 [http://dx.doi.org/10.1093/nass/nrm148] [PMID: 18029703]

[117]
Sato, Y.; Kudo, M.; Toriyabe, Y.; Kuchitsu, S.; Wang, C.X.; Nishizawa, S.; Teramae, N. Abasic site-binding ligands conjugated with cyanine dyes for “off-on” fluorescence sensing of orphan nucleobases in DNA duplexes and DNA-RNA hybrids. Chem. Commun. (Camb.),  2014, 50(5), 515-517.
 [http://dx.doi.org/10.1039/C3CC47717G] [PMID: 24247159]

[118]
Shelke, S.A.; Sigurdsson, S.T. Noncovalent and site-directed spin labeling of nucleic acids. Angew. Chem. Int. Ed. Engl.,  2010, 49(43), 7984-7986.
 [http://dx.doi.org/10.1002/anie.201002637] [PMID: 20845340]

[119]
Sigurdsson, S.T. Nitroxides and nucleic acids: Chemistry and electron paramagnetic resonance (EPR) spectroscopy. Pure Appl. Chem.,  2011, 83(3), 677-686.
 [http://dx.doi.org/10.1351/PAC-CON-10-09-28]

[120]
Kamble, N.R.; Sigurdsson, S.T. Purine-derived nitroxides for noncovalent spin-labeling of abasic sites in duplex nucleic acids. Chemistry,  2018, 24(16), 4157-4164.
 [http://dx.doi.org/10.1002/chem.201705410] [PMID: 29451325]

[121]
Juliusson, H.Y.; Sigurdsson, S.T. Nitroxide-derived N-oxide phenazines for noncovalent spin-labeling of DNA. ChemBioChem,  2020, 21(18), 2635-2642.
 [http://dx.doi.org/10.1002/cbic.202000128] [PMID: 32353177]

[122]
Shelke, S.A.; Sigurdsson, S.T. Structural changes of an abasic site in duplex DNA affect noncovalent binding of the spin label ç. Nucleic Acids Res.,  2012, 40(8), 3732-3740.
 [http://dx.doi.org/10.1093/nar/gkr1210] [PMID: 22210856]

[123]
Shelke, S.A.; Sigurdsson, S.T. Effect of N3 modifications on the affinity of spin label ç for abasic sites in duplex DNA. ChemBioChem,  2012, 13(5), 684-690.
 [http://dx.doi.org/10.1002/cbic.201100728] [PMID: 22408066]

[124]
Zhao, C.; Dai, Q.; Seino, T.; Cui, Y-Y.; Nishizawa, S.; Teramae, N. Fluorescence detection of thymidine-related single-nucleotide polymorphisms by 3, 5-diaminopyrazine derivatives. Nucleic Acids Symp. Ser.,  2005, 49(49), 221-222.
 [http://dx.doi.org/10.1093/nass/49.1.221] [PMID: 17150713]

[125]
Rajendran, A.; Thiagarajan, V.; Rajendar, B.; Nishizawa, S.; Teramae, N. Simultaneous recognition of nucleobase and sites of DNA damage: Effect of tethered cation on the binding affinity. Biochim. Biophys. Acta,  2009, 1790(2), 95-100.
 [http://dx.doi.org/10.1016/j.bbagen.2008.09.003] [PMID: 18852030]

[126]
Zhao, C.; Dai, Q.; Seino, T.; Cui, Y-Y.; Nishizawa, S.; Teramae, N. Strong and selective binding of amiloride to thymine base opposite AP sites in DNA duplexes: Simultaneous binding to DNA phosphate backbone. Chem. Commun. (Camb.),  2006, (11), 1185-1187.
 [http://dx.doi.org/10.1039/b516575j] [PMID: 16518485]

[127]
Zhao, C.; Rajendran, A.; Dai, Q.; Nishizawa, S.; Teramae, N. A pyrazine-based fluorescence-enhancing ligand with a high selectivity for thymine in AP site-containing DNA duplexes. Anal. Sci.,  2008, 24(6), 693-695.
 [http://dx.doi.org/10.2116/analsci.24.693] [PMID: 18544854]

[128]
Rajendran, A.; Zhao, C.; Rajendar, B.; Thiagarajan, V.; Sato, Y.; Nishizawa, S.; Teramae, N. Effect of the bases flanking an abasic site on the recognition of nucleobase by amiloride. Biochim. Biophys. Acta,  2010, 1800(6), 599-610.
 [http://dx.doi.org/10.1016/j.bbagen.2010.03.007] [PMID: 20307626]

[129]
Sankaran, N.B.; Sato, Y.; Sato, F.; Rajendar, B.; Morita, K.; Seino, T.; Nishizawa, S.; Teramae, N. Small-molecule binding at an abasic site of DNA: Strong binding of lumiflavin for improved recognition of thymine-related single nucleotide polymorphisms. J. Phys. Chem. B,  2009, 113(5), 1522-1529.
 [http://dx.doi.org/10.1021/jp808576t] [PMID: 19175344]

[130]
Nishizawa, S.; Sankaran, N.B.; Seino, T.; Cui, Y-Y.; Dai, Q.; Xu, C-Y.; Yoshimoto, K.; Teramae, N. Use of vitamin B2 for fluorescence detection of thymidine-related single-nucleotide polymorphisms. Anal. Chim. Acta,  2006, 556(1), 133-139.
 [http://dx.doi.org/10.1016/j.aca.2005.05.064] [PMID: 17723339]

[131]
Rajendar, B.; Nishizawa, S.; Teramae, N. Alloxazine as a ligand for selective binding to adenine opposite AP sites in DNA duplexes and analysis of single-nucleotide polymorphisms. Org. Biomol. Chem.,  2008, 6(4), 670-673.
 [http://dx.doi.org/10.1039/b719786a] [PMID: 18264565]

[132]
Rajendar, B.; Rajendran, A.; Ye, Z.; Kanai, E.; Sato, Y.; Nishizawa, S.; Sikorski, M.; Teramae, N. Effect of substituents of alloxazine derivatives on the selectivity and affinity for adenine in AP-site-containing DNA duplexes. Org. Biomol. Chem.,  2010, 8(21), 4949-4959.
 [http://dx.doi.org/10.1039/c0ob00057d] [PMID: 20820650]

[133]
Ye, Z.; Rajendar, B.; Qing, D.; Nishizawa, S.; Teramae, N. 6,7-Dimethyllumazine as a potential ligand for selective recognition of adenine opposite an abasic site in DNA duplexes. Chem. Commun. (Camb.),  2008, (48), 6588-6590.
 [http://dx.doi.org/10.1039/b816876h] [PMID: 19057788]

[134]
Rajendar, B.; Rajendran, A.; Sato, Y.; Nishizawa, S.; Teramae, N. Effect of methyl substitution in a ligand on the selectivity and binding affinity for a nucleobase: A case study with isoxanthopterin and its derivatives. Bioorg. Med. Chem.,  2009, 17(1), 351-359.
 [http://dx.doi.org/10.1016/j.bmc.2008.10.062] [PMID: 19010683]

[135]
Kanai, E.; Nishizawa, S.; Teramae, N. A pteridine derivative with electron-withdrawing groups for binding and sensing of nucleobases in AP site-containing DNA duplexes. Nucleic Acids Symp. Ser.,  2008, 52(1), 115-116.
 [http://dx.doi.org/10.1093/nass/nrn059] [PMID: 18776280]

[136]
Dai, Q.; Xu, C-Y.; Sato, Y.; Yoshimoto, K.; Nishizawa, S.; Teramae, N. Enhancement of the binding ability of a ligand for nucleobase recognition by introducing a methyl group. Anal. Sci.,  2006, 22(2), 201-203.
 [http://dx.doi.org/10.2116/analsci.22.201] [PMID: 16512408]

[137]
Rajendar, B.; Sato, Y.; Nishizawa, S.; Teramae, N. Improvement of base selectivity and binding affinity by controlling hydrogen bonding motifs between nucleobases and isoxanthopterin: Application to the detection of T/C mutation. Bioorg. Med. Chem. Lett.,  2007, 17(13), 3682-3685.
 [http://dx.doi.org/10.1016/j.bmcl.2007.04.033] [PMID: 17470392]

[138]
Sato, Y.; Zhang, Y.; Nishizawa, S.; Seino, T.; Nakamura, K.; Li, M.; Teramae, N. Competitive assay for theophylline based on an abasic site-containing DNA duplex aptamer and a fluorescent ligand. Chemistry,  2012, 18(40), 12719-12724.
 [http://dx.doi.org/10.1002/chem.201201298] [PMID: 22915350]

[139]
Rowe, D.J.F.; Watson, I.D.; Williams, J.; Berry, D.J. The clinical use and measurement of theophylline. Ann. Clin. Biochem.,  1988, 25(Pt 1), 4-26.
 [http://dx.doi.org/10.1177/000456328802500102] [PMID: 3281555]

[140]
Hendeles, L.; Weinberger, M.; Theophylline, A. Theophylline. A “state of the art” review. Pharmacotherapy,  1983, 3(1), 2-44.
 [http://dx.doi.org/10.1002/j.1875-9114.1983.tb04531.x] [PMID: 6344032]

[141]
Wang, Y.; Hu, Y.; Wu, T.; Zhang, L.; Liu, H.; Zhou, X.; Shao, Y. Recognition of DNA abasic site nanocavity by fluorophore-switched probe: Suitable for all sequence environments. Spectrochim. Acta A Mol. Biomol. Spectrosc.,  2016, 153, 645-650.
 [http://dx.doi.org/10.1016/j.saa.2015.09.038] [PMID: 26454091]

[142]
Basili, S.; Bergen, A.; Dall’Acqua, F.; Faccio, A.; Granzhan, A.; Ihmels, H.; Moro, S.; Viola, G. Relationship between the structure and the DNA binding properties of diazoniapolycyclic duplex- and triplex-DNA binders: Efficiency, selectivity, and binding mode. Bio chemistry,  2007, 46(44), 12721-12736.
 [http://dx.doi.org/10.1021/bi701518v] [PMID: 17939688]

[143]
Granzhan, A.; Ihmels, H.; Jäger, K. Diazonia- and tetraazoniapolycyclic cations as motif for quadruplex-DNA ligands. Chem. Commun. (Camb.),  2009, (10), 1249-1251.
 [http://dx.doi.org/10.1039/b812891j] [PMID: 19240889]

[144]
Granzhan, A.; Ihmels, H. Selective stabilization of triple-helical DNA by diazoniapolycyclic intercalators. ChemBioChem,  2006, 7(7), 1031-1033.
 [http://dx.doi.org/10.1002/cbic.200600065] [PMID: 16700089]

[145]
Jäger, K.; Bats, J.W.; Ihmels, H.; Granzhan, A.; Uebach, S.; Patrick, B.O. Polycyclic azoniahetarenes: Assessing the binding parameters of complexes between unsubstituted ligands and G-quadruplex DNA. Chem. Eur. J.,  2012, 18(35), 10903-10915.
 [http://dx.doi.org/10.1002/chem.201103019] [PMID: 22807262]

[146]
Ihmels, H.; Otto, D.; Dall’Acqua, F.; Faccio, A.; Moro, S.; Viola, G. Comparative studies on the DNA-binding properties of linear and angular dibenzoquinolizinium ions. J. Org. Chem.,  2006, 71(22), 8401-8411.
 [http://dx.doi.org/10.1021/jo0612271] [PMID: 17064012]

[147]
Granzhan, A.; Ihmels, H. Playing around with the size and shape of quinolizinium derivatives: Versatile ligands for duplex, triplex, quadruplex and abasic site-containing DNA. Synlett,  2016, 27(12), 1775-1793.
 [http://dx.doi.org/10.1055/s-0035-1561445]

[148]
Benner, K.; Ihmels, H.; Kölsch, S.; Pithan, P.M. Targeting abasic site-containing DNA with annelated quinolizinium derivatives: The influence of size, shape and substituents. Org. Biomol. Chem.,  2014, 12(11), 1725-1734.
 [http://dx.doi.org/10.1039/C3OB42140F] [PMID: 24492925]

[149]
Zeglis, B.M.; Boland, J.A.; Barton, J.K. Targeting abasic sites and single base bulges in DNA with metalloinsertors. J. Am. Chem. Soc.,  2008, 130(24), 7530-7531.
 [http://dx.doi.org/10.1021/ja801479y] [PMID: 18491905]

[150]
McConnell, A.J.; Lim, M.H.; Olmon, E.D.; Song, H.; Dervan, E.E.; Barton, J.K. Luminescent properties of ruthenium(II) complexes with sterically expansive ligands bound to DNA defects. Inorg. Chem.,  2012, 51(22), 12511-12520.
 [http://dx.doi.org/10.1021/ic3019524] [PMID: 23113594]

[151]
Benner, K.; Bergen, A.; Ihmels, H.; Pithan, P.M. Selective stabilization of abasic site-containing DNA by insertion of sterically demanding biaryl ligands. Chem. Eur. J.,  2014, 20(32), 9883-9887.
 [http://dx.doi.org/10.1002/chem.201403622] [PMID: 25044435]

[152]
Bag, S.S.; Pradhan, M.K.; Talukdar, S. Trifunctional fluorescent unnatural nucleoside: Label free detection of T-T/C-C base mismatches, abasic site and bulge DNA. J. Photochem. Photobiol. B,  2017, 173, 165-169.
 [http://dx.doi.org/10.1016/j.jphotobiol.2017.05.035] [PMID: 28582712]

[153]
Bag, S.S.; Kundu, R.; Talukdar, S. Unnatural triazolyl nucleoside stabilizes an abasic site containing DNA duplex equally as the stabilization of a natural A–T pair. RSC Advances,  2013, 3(44), 21352-21355.
 [http://dx.doi.org/10.1039/c3ra44120b]

[154]
Bag, S.S.; Sinha, S.; Gogoi, H.; Datta, S.; Kundu, R.; Talukdar, S. Stabilization of an abasic site paired against an unnatural triazolyl nitrobenzene nucleoside. Biophys. Chem.,  2020, 264, 106428-106437.
 [http://dx.doi.org/10.1016/j.bpc.2020.106428] [PMID: 32682232]

[155]
Cai, X.; Liu, B. Aggregation-induced emission: Recent advances in materials and biomedical applications. Angew. Chem. Int. Ed. Engl.,  2020, 59(25), 9868-9886.
 [http://dx.doi.org/10.1002/anie.202000845] [PMID: 32128951]

[156]
Würthner, F. Aggregation-induced emission (AIE): A historical perspective. Angew. Chem. Int. Ed. Engl.,  2020, 59(34), 14192-14196.
 [http://dx.doi.org/10.1002/anie.202007525] [PMID: 32662175]

[157]
Zhao, Z.; Zhang, H.; Lam, J.W.Y.; Tang, B.Z. Aggregation-induced emission: New vistas at the aggregate level. Angew. Chem. Int. Ed. Engl.,  2020, 59(25), 9888-9907.
 [http://dx.doi.org/10.1002/anie.201916729] [PMID: 32048428]

[158]
Bag, S.S.; Gogoi, H.; Jana, S. Label-free sensing of abasic DNA using pyrenylamido triazolyl aromatic amino acid scaffold as AIE probe. J. Photochem. Photobiol. Chem.,  2020, 388, 112186-112201.
 [http://dx.doi.org/10.1016/j.jphotochem.2019.112186]

[159]
Jackson, B.A.; Barton, J.K. Recognition of DNA base mismatches by a rhodium intercalator. J. Am. Chem. Soc.,  1997, 119(52), 12986-12987.
 [http://dx.doi.org/10.1021/ja972489a]

[160]
Jackson, B.A.; Alekseyev, V.Y.; Barton, J.K. A versatile mismatch recognition agent: Specific cleavage of a plasmid DNA at a single base mispair. Bio chemistry,  1999, 38(15), 4655-4662.
 [http://dx.doi.org/10.1021/bi990255t] [PMID: 10200152]

[161]
Jackson, B.A.; Barton, J.K. Recognition of base mismatches in DNA by 5,6-chrysenequinone diimine complexes of rhodium(III): A proposed mechanism for preferential binding in destabilized regions of the double helix. Bio chemistry,  2000, 39(20), 6176-6182.
 [http://dx.doi.org/10.1021/bi9927033] [PMID: 10821692]

[162]
Zeglis, B.M.; Pierre, V.C.; Barton, J.K. Metallo-intercalators and metallo-insertors. Chem. Commun. (Camb.),  2007, 44(44), 4565-4579.
 [http://dx.doi.org/10.1039/b710949k] [PMID: 17989802]

[163]
Junicke, H.; Hart, J.R.; Kisko, J.; Glebov, O.; Kirsch, I.R.; Barton, J.K. A rhodium(III) complex for high-affinity DNA base-pair mismatch recognition. Proc. Natl. Acad. Sci. USA,  2003, 100(7), 3737-3742.
 [http://dx.doi.org/10.1073/pnas.0537194100] [PMID: 12610209]

[164]
Zeglis, B.M.; Boland, J.A.; Barton, J.K. Recognition of abasic sites and single base bulges in DNA by a metalloinsertor. Bio chemistry,  2009, 48(5), 839-849.
 [http://dx.doi.org/10.1021/bi801885w] [PMID: 19146409]

[165]
Cordier, C.; Pierre, V.C.; Barton, J.K. Insertion of a bulky rhodium complex into a DNA cytosine-cytosine mismatch: An NMR solution study. J. Am. Chem. Soc.,  2007, 129(40), 12287-12295.
 [http://dx.doi.org/10.1021/ja0739436] [PMID: 17877349]

[166]
Pierre, V.C.; Kaiser, J.T.; Barton, J.K. Insights into finding a mismatch through the structure of a mispaired DNA bound by a rhodium intercalator. Proc. Natl. Acad. Sci. USA,  2007, 104(2), 429-434.
 [http://dx.doi.org/10.1073/pnas.0610170104] [PMID: 17194756]

[167]
Cardin, C.J.; Kelly, J.M.; Quinn, S.J. Photochemically active DNA-intercalating ruthenium and related complexes - insights by combining crystallography and transient spectroscopy. Chem. Sci. (Camb.),  2017, 8(7), 4705-4723.
 [http://dx.doi.org/10.1039/C7SC01070B] [PMID: 28936338]

[168]
Kellett, A.; Molphy, Z.; Slator, C.; McKee, V.; Farrell, N.P. Molecular methods for assessment of non-covalent metallodrug-DNA interactions. Chem. Soc. Rev.,  2019, 48(4), 971-988.
 [http://dx.doi.org/10.1039/C8CS00157J] [PMID: 30714595]

[169]
Li, G.; Sun, L.; Ji, L.; Chao, H. Ruthenium(ii) complexes with dppz: From molecular photoswitch to biological applications. Dalton Trans.,  2016, 45(34), 13261-13276.
 [http://dx.doi.org/10.1039/C6DT01624C] [PMID: 27426487]

[170]
Lim, M.H.; Song, H.; Olmon, E.D.; Dervan, E.E.; Barton, J.K. Sensitivity of Ru(bpy)2dppz2+ luminescence to DNA defects. Inorg. Chem.,  2009, 48(12), 5392-5397.
 [http://dx.doi.org/10.1021/ic900407n] [PMID: 19453124]

[171]
Nandhini, T.; Anju, K.R.; Manikandamathavan, V.M.; Vaidyanathan, V.G.; Nair, B.U. Interactions of Ru(II) polypyridyl complexes with DNA mismatches and abasic sites. Dalton Trans.,  2015, 44(19), 9044-9051.
 [http://dx.doi.org/10.1039/C5DT00807G] [PMID: 25893583]

[172]
Dayanidhi, D.P.E.; Malapati, R.P.; Vaidyanathan Ganesan, V. Selective recognition of DNA defects by cyclometalated Ir(iii) complexes. Dalton Trans.,  2019, 48(36), 13536-13540.
 [http://dx.doi.org/10.1039/C9DT01225G] [PMID: 31455966]

[173]
Fung, S.K.; Zou, T.; Cao, B.; Chen, T.; To, W-P.; Yang, C.; Lok, C-N.; Che, C-M. Luminescent platinum(II) complexes with functionalized N-heterocyclic carbene or diphosphine selectively probe mismatched and abasic DNA. Nat. Commun.,  2016, 7(1), 10655-10664.
 [http://dx.doi.org/10.1038/ncomms10655] [PMID: 26883164]

[174]
Malina, J.; Scott, P.; Brabec, V. Shape-selective recognition of DNA abasic sites by metallohelices: Inhibition of human AP endonuclease 1. Nucleic Acids Res.,  2015, 43(11), 5297-5306.
 [http://dx.doi.org/10.1093/nar/gkv438] [PMID: 25940617]

[175]
Kotera, N.; Poyer, F.; Granzhan, A.; Teulade-Fichou, M-P. Efficient inhibition of human AP endonuclease 1 (APE1) via substrate masking by abasic site-binding macrocyclic ligands. Chem. Commun. (Camb.),  2015, 51(88), 15948-15951.
 [http://dx.doi.org/10.1039/C5CC06084B] [PMID: 26377038]

[176]
Caron, C.; Duong, X.N.T.; Guillot, R.; Bombard, S.; Granzhan, A. Interaction of functionalized naphthalenophanes with abasic sites in DNA: DNA cleavage, DNA cleavage inhibition, and formation of ligand-DNA adducts. Chem. Eur. J.,  2019, 25(8), 1949-1962.
 [http://dx.doi.org/10.1002/chem.201805555] [PMID: 30508326]

[177]
Berthet, N.; Michon, J.; Lhomme, J.; Teulade-Fichou, M-P.; Vigneron, J.P.; Lehn, J-M. Recognition of abasic sites in dna by a cyclobisacridine molecule. Chem. Eur. J.,  1999, 5(12), 3625-3630.
 [http://dx.doi.org/10.1002/(SICI)1521-3765(19991203)5:12<3625:AID-CHEM3625>3.0.CO;2-G]

[178]
Teulade-Fichou, M-P.; Vigneron, J-P.; Lehn, J-M. Molecular recognition of nucleosides and nucleotides by a water-soluble cyclo-bis-intercaland receptor based on acridine subunits. Supramol. Chem.,  1995, 5(2), 139-147.
 [http://dx.doi.org/10.1080/10610279508029486]

[179]
Jourdan, M.; Garcia, J.; Lhomme, J.; Teulade-Fichou, M.P.; Vigneron, J.P.; Lehn, J.M. Threading bis-intercalation of a macrocyclic bisacridine at abasic sites in DNA: Nuclear magnetic resonance and molecular modeling study. Bio chemistry,  1999, 38(43), 14205-14213.
 [http://dx.doi.org/10.1021/bi991111h] [PMID: 10571994]

[180]
Berthet, N.; Boudali, A.; Constant, J.F.; Decout, J.L.; Demeunynck, M.; Fkyerat, A.; Garcia, J.; Laayoun, A.; Michon, P.; Lhomme, J. Design of molecules that specifically recognize and cleave apurinic sites in DNA. J. Mol. Recognit.,  1994, 7(2), 99-107.
 [http://dx.doi.org/10.1002/jmr.300070207] [PMID: 7826679]

[181]
Dawson, S.; Malkinson, J.P.; Paumier, D.; Searcey, M. Bisintercalator natural products with potential therapeutic applications: Isolation, structure determination, synthetic and biological studies. Nat. Prod. Rep.,  2007, 24(1), 109-126.
 [http://dx.doi.org/10.1039/B516347C] [PMID: 17268609]

[182]
Tumir, L-M.; Piantanida, I. Recognition of single stranded and double stranded DNA/RNA sequences in aqueous medium by small bis-aromatic derivatives. Mini Rev. Med. Chem.,  2010, 10(4), 299-308.
 [http://dx.doi.org/10.2174/138955710791330990] [PMID: 20470245]

[183]
Zolova, O.E.; Mady, A.S.A.; Garneau-Tsodikova, S. Recent developments in bisintercalator natural products. Biopolymers,  2010, 93(9), 777-790.
 [http://dx.doi.org/10.1002/bip.21489] [PMID: 20578002]

[184]
Constant, J-F.; O’Connor, T.R.; Lhomme, J.; Laval, J. 9-[(10-(aden-9-yl)-4,8-diazadecyl)amino]-6-chloro-2-methoxy-acridine incises DNA at apurinic sites. Nucleic Acids Res.,  1988, 16(6), 2691-2703.
 [http://dx.doi.org/10.1093/nar/16.6.2691] [PMID: 3362679]

[185]
Fkyerat, A.; Demeunynck, M.; Constant, J-F.; Michon, P.; Lhomme, J. A new class of artificial nucleases that recognize and cleave apurinic sites in DNA with great selectivity and efficiency. J. Am. Chem. Soc.,  1993, 115(22), 9952-9959.
 [http://dx.doi.org/10.1021/ja00075a011]

[186]
Berthet, N.; Constant, J-F.; Demeunynck, M.; Michon, P.; Lhomme, J. Search for DNA repair inhibitors: Selective binding of nucleic bases-acridine conjugates to a DNA duplex containing an abasic site. J. Med. Chem.,  1997, 40(21), 3346-3352.
 [http://dx.doi.org/10.1021/jm970225t] [PMID: 9341909]

[187]
Barret, J-M.; Etiévant, C.; Fahy, J.; Lhomme, J.; Hill, B.T. Novel artificial endonucleases inhibit base excision repair and potentiate the cytotoxicity of DNA-damaging agents on L1210 cells. Anticancer Drugs,  1999, 10(1), 55-65.
 [http://dx.doi.org/10.1097/00001813-199901000-00008] [PMID: 10194548]

[188]
Coppel, Y.; Constant, J-F.; Coulombeau, C.; Demeunynck, M.; Garcia, J.; Lhomme, J. NMR and molecular modeling studies of the interaction of artificial AP lyases with a DNA duplex containing an apurinic abasic site model. Bio chemistry,  1997, 36(16), 4831-4843.
 [http://dx.doi.org/10.1021/bi962678q] [PMID: 9125503]

[189]
Belmont, P.; Jourdan, M.; Demeunynck, M.; Constant, J.F.; Garcia, J.; Lhomme, J.; Carez, D.; Croisy, A. Abasic site recognition in DNA as a new strategy to potentiate the action of anticancer alkylating drugs? J. Med. Chem.,  1999, 42(25), 5153-5159.
 [http://dx.doi.org/10.1021/jm9901428] [PMID: 10602700]

[190]
Belmont, P.; Demeunynck, M.; Constant, J-F.; Lhomme, J. Synthesis and study of a new adenine-acridine tandem, inhibitor of exonuclease III. Bioorg. Med. Chem. Lett.,  2000, 10(3), 293-295.
 [http://dx.doi.org/10.1016/S0960-894X(99)00681-2] [PMID: 10698457]

[191]
Alarcon, K.; Demeunynck, M.; Lhomme, J.; Carrez, D.; Croisy, A. Diaminopurine-acridine heterodimers for specific recognition of abasic site containing DNA. Influence on the biological activity of the position of the linker on the purine ring. Bioorg. Med. Chem. Lett.,  2001, 11(14), 1855-1858.
 [http://dx.doi.org/10.1016/S0960-894X(01)00310-9] [PMID: 11459646]

[192]
Alarcon, K.; Demeunynck, M.; Lhomme, J.; Carrez, D.; Croisy, A. Potentiation of BCNU cytotoxicity by molecules targeting abasic lesions in DNA. Bioorg. Med. Chem.,  2001, 9(7), 1901-1910.
 [http://dx.doi.org/10.1016/S0968-0896(01)00097-9] [PMID: 11425593]

[193]
Martelli, A.; Jourdan, M.; Constant, J-F.; Demeunynck, M.; Dumy, P. Photoreactive threading agent that specifically binds to abasic sites in DNA. Bioorg. Med. Chem. Lett.,  2006, 16(1), 154-157.
 [http://dx.doi.org/10.1016/j.bmcl.2005.09.026] [PMID: 16213714]

[194]
Benner, K.; Granzhan, A.; Ihmels, H.; Viola, G. Targeting abasic sites in DNA by aminoalkyl-substituted carboxamidoacridizinium derivatives and acridizinium–adenine conjugates. Eur. J. Org. Chem.,  2007, 2007(28), 4721-4730.
 [http://dx.doi.org/10.1002/ejoc.200700207]
Rights & Permissions Print Cite
Article Metrics
5
Journal Information
For Authors
For Editors
For Reviewers
Explore Articles
Open Access
Open Access Articles
For Visitors
DOI https://dx.doi.org/10.2174/1570179419666220216091422	Print ISSN 1570-1794
Publisher Name Bentham Science Publisher	Online ISSN 1875-6271
Current Organic Synthesis

Ligands for Abasic Site-containing DNA and their Use as Fluorescent Probes

Abstract Play Pause

Graphical Abstract

Related Journals

Related Books

Abstract
