Specific Recognition of Single Nucleotide by Alkylating Oligonucleotides and Sensing of 8-Oxoguanine

  • Shigeki Sasaki
  • Yosuke Taniguchi
  • Fumi Nagatsugi
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 31)


Gene expression is regulated by hierarchical mechanisms, for which not only the sequence but also the special structure of DNA and RNA play a vital role. This sophisticated systems also feature specific chemical modification of nucleotides as epigenetic gene regulations such as 5-methylation of cytosine. Meantime, endogenous and exogenous chemical species react with the nucleotides to have significant impact on the genetic function by causing mutations. Among mutations, a single nucleotide alteration is the most frequently found in the disease-relating genes. Therefore, for the diagnostic and therapeutic purposes, oligonucleotides are desired to discriminate a single nucleotide difference. However, because of non-covalent hybridization of the oligonucleotide with DNA and RNA, discrimination of a single nucleotide difference is not always easy. We have focused on selective alkylation as a reliable strategy for a single base recognition. Molecular design has been performed so that a non-covalent complex in a hybridized complex induces a selective reaction to the target base. On the other hand, guanine is the most susceptible base for oxidation to produce 8-oxoguanine which has a strong mutagenicity. 8-Oxoguanine formed in cells is regarded as a biomarker of oxidative stress of the cell, and a convenient sensing method is desired for diagnostic purposes. Also, determination of 8-oxo-2′-deoxyguanosine in DNA is important to reveal the oxidative damaged site in DNA. In this chapter, design concept and specific alkylating reactions will be introduced.


Primer Extension Reaction Selective Alkylation Chemical Modification Method Thermal Stabilization Effect Selective Base Pair 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461:1071–1078. doi: 10.1038/nature08467 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Stone MP, Huang H, Brown KL, Shanmugam G (2011) Chemistry and structural biology of DNA damage and biological consequences. Chem Biodivers 8:1571–1615. doi: 10.1002/cbdv.201100033 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Jena NR (2012) DNA damage by reactive species: mechanisms, mutation and repair. J Biosci 37:503–517. doi: 10.1007/s12038-012-9218-2 CrossRefPubMedGoogle Scholar
  4. 4.
    Motgomery JA (1995) Antimetabolites. In: Foye WO (ed) Cancer chemotherapeutic agents. American Chemical Society, Washington, DC, pp 111–204Google Scholar
  5. 5.
    Grillari J, Katinger H, Voglauer R (2007) Contributions of DNA interstrand cross-links to aging of cells and organisms. Nucleic Acids Res 35:7566–7576. doi: 10.1093/nar/gkm1065 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Toussaint M, Levasseur G, Tremblay M, Paquette M, Conconi A (2005) Psoralen photocrosslinking, a tool to study the chromatin structure of RNA polymerase I—transcribed ribosomal genes. Biochem Cell Biol 83:449–459. doi: 10.1139/o05-141 CrossRefPubMedGoogle Scholar
  7. 7.
    Murakami A, Yamayoshi A, Iwase R, Nishida J, Yamaoka T, Wake N (2001) Photodynamic antisense regulation of human cervical carcinoma cell growth using psoralen-conjugated oligo(nucleoside phosphorothioate). Eur J Pharm Sci 13:25–34. doi: 10.1016/S0928-0987(00)00204-9 CrossRefPubMedGoogle Scholar
  8. 8.
    Higuchi M, Kobori A, Yamayoshi A, Murakami A (2009) Synthesis of antisense oligonucleotides containing 2′-O-psoralenylmethoxyalkyl adenosine for photodynamic regulation of point mutations in RNA. Bioorg Med Chem 17:475–483. doi: 10.1016/j.bmc.2008.12.001 CrossRefPubMedGoogle Scholar
  9. 9.
    Li Y, Tseng YD, Kwon SY, D’Espaux L, Bunch JS, McEuen PL, Luo D (2004) Controlled assembly of dendrimer-like DNA. Nat Mater 3:38–42. doi: 10.1038/nmat1045 CrossRefPubMedGoogle Scholar
  10. 10.
    Tagawa M, Shohda K, Fujimoto K, Suyama A (2011) Stabilization of DNA nanostructures by photo-cross-linking. Soft Matter 7:10931. doi: 10.1039/c1sm06303k CrossRefGoogle Scholar
  11. 11.
    Rajendran A, Endo M, Katsuda Y, Hidaka K, Sugiyama H (2011) Photo-cross-linking-assisted thermal stability of DNA origami structures and its application for higher-temperature self-assembly. J Am Chem Soc 133:14488–14491. doi: 10.1021/ja204546h CrossRefPubMedGoogle Scholar
  12. 12.
    Glick GD (2003) Engineering terminal disulfide bonds into DNA. In: Beaucage SL (ed) Current protocols in nucleic acid chemistry, vol 2. Wiley, New York, pp 5.7.1–5.7.13. doi: 10.1002/0471142700.nc0507s13
  13. 13.
    Nakatani K, Yoshida T, Saito I (2002) Photochemistry of benzophenone immobilized in a major groove of DNA: formation of thermally reversible interstrand cross-link. J Am Chem Soc 124:2118–2119. doi: 10.1021/ja017611r CrossRefPubMedGoogle Scholar
  14. 14.
    Fujimoto K, Konishi-Hiratsuka K, Sakamoto T, Yoshimura Y (2010) Site-specific photochemical RNA editing. Chem Commun (Camb) 46:7545–7547. doi: 10.1039/c0cc03151h CrossRefGoogle Scholar
  15. 15.
    Zhou Q, Rokita SE (2003) A general strategy for target-promoted alkylation in biological systems. Proc Natl Acad Sci U S A 100:15452–15457. doi: 10.1073/pnas.2533112100 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Rokita SE (ed) (2009) Quinone methides. Wiley, New York, pp 297–327CrossRefGoogle Scholar
  17. 17.
    Peng X, In SH, Li H, Seidman MM, Greenberg MM (2008) Interstrand cross-link formation in duplex and triplex DNA by modified pyrimidines. J Am Chem Soc 130:10299–10306. doi: 10.1021/ja802177u CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Op de Beeck M, Madder A (2012) Sequence specific DNA cross-linking triggered by visible light. J Am Chem Soc 134:10737–10740. doi: 10.1021/ja301901p CrossRefPubMedGoogle Scholar
  19. 19.
    Evans MD, Dizdaroglu M, Cooke MS (2004) Oxidative DNA damage and disease: induction, repair and significance. Mutat Res Rev Mutat Res 567:1–61. doi: 10.1016/j.mrrev.2003.11.001 CrossRefGoogle Scholar
  20. 20.
    Shibutani S, Takeshita M, Grollman AP (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349:431–434. doi: 10.1038/349431a0 CrossRefPubMedGoogle Scholar
  21. 21.
    Nagatsugi F, Kawasaki T, Usui D, Maeda M, Sasaki S (1999) Highly efficient and selective cross-linking to cytidine based on a new strategy for auto-activation within a duplex. J Am Chem Soc 121:6753–6754. doi: 10.1021/ja990356e CrossRefGoogle Scholar
  22. 22.
    Nagatsugi F, Tokuda N, Maeda M, Sasaki S (2001) A new reactive nucleoside analogue for highly reactive and selective cross-linking reaction to cytidine under neutral conditions. Bioorg Med Chem Lett 11:2577–2579. doi: 10.1016/S0960-894X(01)00505-4 CrossRefPubMedGoogle Scholar
  23. 23.
    Nagatsugi F, Matsuyama Y, Maeda M, Sasaki S (2002) Selective cross-linking to the adenine of the TA interrupting site within the triple helix. Bioorg Med Chem Lett 12:487–489. doi: 10.1016/S0960-894X(01)00783-1 CrossRefPubMedGoogle Scholar
  24. 24.
    Kawasaki T, Nagatsugi F, Ali MM, Maeda M, Sugiyama K, Hori K, Sasaki S (2005) Hybridization-promoted and cytidine-selective activation for cross-linking with the use of 2-amino-6-vinylpurine derivatives. J Org Chem 70:14–23. doi: 10.1021/jo048298p CrossRefPubMedGoogle Scholar
  25. 25.
    Sasaki S, Nagatsugi F (2006) Application of unnatural oligonucleotides to chemical modification of gene expression. Curr Opin Chem Biol 10:615–621. doi: 10.1016/j.cbpa.2006.10.006 CrossRefPubMedGoogle Scholar
  26. 26.
    Nagatsugi F, Imoto S (2011) Induced cross-linking reactions to target genes using modified oligonucleotides. Org Biomol Chem 9:2579–2585. doi: 10.1039/c0ob00819b CrossRefPubMedGoogle Scholar
  27. 27.
    Ali MM, Oishi M, Nagatsugi F, Mori K, Nagasaki Y, Kataoka K, Sasaki S (2006) Intracellular inducible alkylation system that exhibits antisense effects with greater potency and selectivity than the natural oligonucleotide. Angew Chem Int Ed 45:3136–3140. doi: 10.1002/anie.200504441 CrossRefGoogle Scholar
  28. 28.
    Nagatsugi F, Sasaki S, Miller PS, Seidman MM (2003) Site-specific mutagenesis by triple helix-forming oligonucleotides containing a reactive nucleoside analog. Nucleic Acids Res 31:e31. doi: 10.1093/nar/gng031 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Taniguchi Y, Kurose Y, Nishioka T, Nagatsugi F, Sasaki S (2010) The alkyl-connected 2-amino-6-vinylpurine (AVP) crosslinking agent for improved selectivity to the cytosine base in RNA. Bioorg Med Chem 18:2894–2901. doi: 10.1016/j.bmc.2010.03.008 CrossRefPubMedGoogle Scholar
  30. 30.
    Imoto S, Hori T, Hagihara S, Taniguchi Y, Sasaki S, Nagatsugi F (2010) Alteration of cross-linking selectivity with the 2′-OMe analogue of 2-amino-6-vinylpurine and evaluation of antisense effects. Bioorg Med Chem Lett 20:6121–6124. doi: 10.1016/j.bmcl.2010.08.027 CrossRefPubMedGoogle Scholar
  31. 31.
    Imoto S, Chikuni T, Kansui H, Kunieda T, Nagatsugi F (2012) Fast DNA interstrand cross-linking reaction by 6-vinylpurine. Nucleosides Nucleotides Nucleic Acids 31:752–762. doi: 10.1080/15257770.2012.726756 CrossRefPubMedGoogle Scholar
  32. 32.
    Hagihara S, Kusano S, Lin WC, Chao XG, Hori T, Imoto S, Nagatsugi F (2012) Production of truncated protein by the crosslink formation of mRNA with 2′-OMe oligoribonucleotide containing 2-amino-6-vinylpurine. Bioorg Med Chem Lett 22:3870–3872. doi: 10.1016/j.bmcl.2012.04.123 CrossRefPubMedGoogle Scholar
  33. 33.
    Hagihara S, Lin W-C, Kusano S, Chao X, Hori T, Imoto S, Nagatsugi F (2013) The crosslink formation of 2′-OMe oligonucleotide containing 2-amino-6-vinylpurine protects mRNA from miRNA-mediated silencing. ChemBioChem 14:1427–1429. doi: 10.1002/cbic.201300382 CrossRefPubMedGoogle Scholar
  34. 34.
    Kusano S, Haruyama T, Ishiyama S, Hagihara S, Nagatsugi F (2014) Development of the crosslinking reactions to RNA triggered by oxidation. Chem Commun (Camb) 50:3951–3954. doi: 10.1039/c3cc49463b CrossRefGoogle Scholar
  35. 35.
    Hattori K, Hirohama T, Imoto S, Kusano S, Nagatsugi F (2009) Formation of highly selective and efficient interstrand cross-linking to thymine without photo-irradiation. Chem Commun (Camb) (42):6463–6465. doi: 10.1039/b915381k
  36. 36.
    Murat P, Balasubramanian S (2014) Existence and consequences of G-quadruplex structures in DNA. Curr Opin Genet Dev 25:22–29. doi: 10.1016/j.gde.2013.10.012 CrossRefPubMedGoogle Scholar
  37. 37.
    Henderson A, Wu Y, Huang YC, Chavez EA, Platt J, Johnson FB, Brosh RM, Sen D, Lansdorp PM (2014) Detection of G-quadruplex DNA in mammalian cells. Nucleic Acids Res 42:860–869. doi: 10.1093/nar/gkt957 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Parkinson GN, Lee MPH, Neidle S (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417:876–880. doi: 10.1038/nature755 CrossRefPubMedGoogle Scholar
  39. 39.
    Phan AT, Modi YS, Patel DJ (2004) Propeller-type parallel-stranded G-quadruplexes in the human c-myc promoter. J Am Chem Soc 126:8710–8716. doi: 10.1021/ja048805k CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Lam EYN, Beraldi D, Tannahill D, Balasubramanian S (2013) G-quadruplex structures are stable and detectable in human genomic DNA. Nat Commun 4:1796. doi: 10.1038/ncomms2792 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Brooks TA, Kendrick S, Hurley L (2010) Making sense of G-quadruplex and i-motif functions in oncogene promoters. FEBS J 277:3459–3469. doi: 10.1111/j.1742-4658.2010.07759.x CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Gehring K, Leroy JL, Guéron M (1993) A tetrameric DNA structure with protonated cytosine-cytosine base pairs. Nature 363:561–565. doi: 10.1038/363561a0 CrossRefPubMedGoogle Scholar
  43. 43.
    Leroy JL, Guéron M, Mergny JL, Hélène C (1994) Intramolecular folding of a fragment of the cytosine-rich strand of telomeric DNA into an i-motif. Nucleic Acids Res 22:1600–1606. doi: 10.1093/nar/22.9.1600 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Mergny J, Lacroix L, Han X, Leroy J, Helene C (1995) Intramolecular folding of pyrimidine oligodeoxynucleotides into an i-DNA motif. J Am Chem Soc 117:8887–8898. doi: 10.1021/ja00140a001 CrossRefGoogle Scholar
  45. 45.
    Zhou J, Wei C, Jia G, Wang X, Feng Z, Li C (2010) Formation of i-motif structure at neutral and slightly alkaline pH. Mol Biosyst 6:580–586. doi: 10.1039/b919600e CrossRefPubMedGoogle Scholar
  46. 46.
    Day HA, Huguin C, Waller ZAE (2013) Silver cations fold i-motif at neutral pH. Chem Commun 49:7696–7698CrossRefGoogle Scholar
  47. 47.
    Dong Y, Yang Z, Liu D (2014) DNA nanotechnology based on i-motif structures. Acc Chem Res 47:1853–1860. doi: 10.1021/ar500073a CrossRefPubMedGoogle Scholar
  48. 48.
    Day HA, Pavlou P, Waller ZAE (2014) i-Motif DNA: structure, stability and targeting with ligands. Bioorg Med Chem 22:4407–4418. doi: 10.1016/j.bmc.2014.05.047 CrossRefPubMedGoogle Scholar
  49. 49.
    Cui J, Waltman P, Le VH, Lewis EA (2013) The effect of molecular crowding on the stability of human c-MYC promoter sequence I-motif at neutral pH. Molecules 18:12751–12767. doi: 10.3390/molecules181012751 CrossRefPubMedGoogle Scholar
  50. 50.
    Rajendran A, Nakano S, Sugimoto N (2010) Molecular crowding of the cosolutes induces an intramolecular i-motif structure of triplet repeat DNA oligomers at neutral pH. Chem Commun (Camb) 46:1299–1301. doi: 10.1039/b922050j CrossRefGoogle Scholar
  51. 51.
    Bhavsar-Jog YP, Van Dornshuld E, Brooks TA, Tschumper GS, Wadkins RM (2014) Epigenetic modification, dehydration, and molecular crowding effects on the thermodynamics of i-motif structure formation from C-rich DNA. Biochemistry 53:1586–1594. doi: 10.1021/bi401523b CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Kikuta K, Haishun P, Brazier J, Taniguchi Y, Onizuka K, Nagatsugi F, Sasaki S (2015) Stabilization of the i-motif structure by the intrastrand cross-link formation. Bioorg Med Chem Lett 25(16):3307–3310CrossRefPubMedGoogle Scholar
  53. 53.
    Kaushik M, Suehl N, Marky LA (2007) Calorimetric unfolding of the bimolecular and i-motif complexes of the human telomere complementary strand, d(C(3)TA(2))(4). Biophys Chem 126:154–164. doi: 10.1016/j.bpc.2006.05.031 CrossRefPubMedGoogle Scholar
  54. 54.
    Sasaki S, Onizuka K, Taniguchi Y (2011) The oligodeoxynucleotide probes for the site-specific modification of RNA. Chem Soc Rev 40:5698. doi: 10.1039/c1cs15066a CrossRefPubMedGoogle Scholar
  55. 55.
    Jitsuzaki D, Onizuka K, Nishimoto A, Oshiro I, Taniguchi Y, Sasaki S (2014) Remarkable acceleration of a DNA/RNA inter-strand functionality transfer reaction to modify a cytosine residue: the proximity effect via complexation with a metal cation. Nucleic Acids Res 42:8808–8815. doi: 10.1093/nar/gku538 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Ali M, Alam R, Kawasaki T, Nakayama S, Nagatsugi F, Sasaki S (2004) Sequence- and base-specific delivery of nitric oxide to cytidine and 5-methylcytidine leading to efficient deamination. J Am Chem Soc 126:8864–8865. doi: 10.1021/ja0498888 CrossRefPubMedGoogle Scholar
  57. 57.
    Onizuka K, Taniguchi Y, Sasaki S (2009) Site-specific covalent modification of RNA guided by functionality-transfer oligodeoxynucleotides. Bioconjug Chem 20:799–803. doi: 10.1021/bc900009p CrossRefPubMedGoogle Scholar
  58. 58.
    Onizuka K, Taniguchi Y, Sasaki S (2010) A new usage of functionalized oligodeoxynucleotide probe for site-specific modification of a guanine base within RNA. Nucleic Acids Res 38:1760–1766. doi: 10.1093/nar/gkp930 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Onizuka K, Taniguchi Y, Sasaki S (2010) Activation and alteration of base selectivity by metal cations in the functionality-transfer reaction for RNA modification. Bioconjug Chem 21:1508–1512. doi: 10.1021/bc100131j CrossRefPubMedGoogle Scholar
  60. 60.
    Onizuka K, Shibata A, Taniguchi Y, Sasaki S (2011) Pin-point chemical modification of RNA with diverse molecules through the functionality transfer reaction and the copper-catalyzed azide-alkyne cycloaddition reaction. Chem Commun (Camb) 47:5004–5006. doi: 10.1039/c1cc10582e CrossRefGoogle Scholar
  61. 61.
    Onizuka K, Nishioka T, Li Z, Jitsuzaki D, Taniguchi Y, Sasaki S (2012) An efficient and simple method for site-selective modification of O6-methyl-2′-deoxyguanosine in DNA. Chem Commun 48:3969–3971CrossRefGoogle Scholar
  62. 62.
    Oshiro I, Jitsuzaki D, Onizuka K, Nishimoto A, Taniguchi Y, Sasaki S (2015) Site-specific modification of the 6-amino group of adenosine in RNA by an interstrand functionality-transfer reaction with an S-functionalized 4-thiothymidine. ChemBioChem 16:1199–1204. doi: 10.1002/cbic.201500084 CrossRefPubMedGoogle Scholar
  63. 63.
    Poulsen HE, Nadal LL, Broedbaek K, Nielsen PE, Weimann A (2014) Detection and interpretation of 8-oxodG and 8-oxoGua in urine, plasma and cerebrospinal fluid. Biochim Biophys Acta 1840:801–808. doi: 10.1016/j.bbagen.2013.06.009 CrossRefPubMedGoogle Scholar
  64. 64.
    Bruner SD, Norman DP, Verdine GL (2000) Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature 403:859–866. doi: 10.1038/35002510 CrossRefPubMedGoogle Scholar
  65. 65.
    Lin KY, Matteucci MD (1998) A cytosine analogue capable of clamp-like binding to a guanine in helical nucleic acids. J Am Chem Soc 120:8531–8532CrossRefGoogle Scholar
  66. 66.
    Flanagan WM, Wolf JJ, Olson P, Grant D, Lin KY, Wagner RW, Matteucci MD (1999) A cytosine analog that confers enhanced potency to antisense oligonucleotides. Proc Natl Acad Sci U S A 96:3513–3518. doi: 10.1073/pnas.96.7.3513 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Nakagawa O, Ono S, Li Z, Tsujimoto A, Sasaki S (2007) Specific fluorescent probe for 8-oxoguanosine. Angew Chem Int Ed 46:4500–4503. doi: 10.1002/anie.200700671 CrossRefGoogle Scholar
  68. 68.
    Li Z, Nakagawa O, Koga Y, Taniguchi Y, Sasaki S (2010) Synthesis of new derivatives of 8-oxoG-clamp for better understanding the recognition mode and improvement of selective affinity. Bioorg Med Chem 18:3992–3998. doi: 10.1016/j.bmc.2010.04.025 CrossRefPubMedGoogle Scholar
  69. 69.
    Koga Y, Fuchi Y, Nakagawa O, Sasaki S (2011) Optimization of fluorescence property of the 8-oxodGclamp derivative for better selectivity for 8-oxo-2′-deoxyguanosine. Tetrahedron 67:6746–6752. doi: 10.1016/j.tet.2011.03.111 CrossRefGoogle Scholar
  70. 70.
    Ohno M, Miura T, Furuichi M, Tominaga Y, Tsuchimoto D, Sakumi K, Nakabeppu Y (2006) A genome-wide distribution of 8-oxoguanine correlates with the preferred regions for recombination and single nucleotide polymorphism in the human genome. Genome Res 16:567–575. doi: 10.1101/gr.4769606 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Kawanishi S, Oikawa S, Murata M, Tsukitome H, Saito I (1999) Site-specific oxidation at GG and GGG sequences in double-stranded DNA by benzoyl peroxide as a tumor promoter. Biochemistry 38:16733–16739. doi: 10.1021/bi990890z CrossRefPubMedGoogle Scholar
  72. 72.
    Fleming AM, Burrows CJ (2013) G-quadruplex folds of the human telomere sequence alter the site reactivity and reaction pathway of guanine oxidation compared to duplex DNA. Chem Res Toxicol 26:593–607. doi: 10.1021/tx400028y CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Toyokuni S, Tanaka T, Hattori Y, Nishiyama Y, Yoshida A, Uchida K, Hiai H, Ochi H, Osawa T (1997) Quantitative immunohistochemical determination of 8-hydroxy-2′-deoxyguanosine by a monoclonal antibody N45.1: its application to ferric nitrilotriacetate-induced renal carcinogenesis model. Lab Invest 76:365–374PubMedGoogle Scholar
  74. 74.
    Zhang B, Guo LH, Greenberg MM (2012) Quantification of 8-oxodGuo lesions in double-stranded DNA using a photoelectrochemical DNA sensor. Anal Chem 84:6048–6053. doi: 10.1021/ac300866u CrossRefPubMedGoogle Scholar
  75. 75.
    Xue L, Greenberg MM (2007) Facile quantification of lesions derived from 2′-deoxyguanosine in DNA. J Am Chem Soc 129:7010–7011. doi: 10.1021/ja072174n CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    An N, Fleming AM, White HS, Burrows CJ (2015) Nanopore detection of 8-oxoguanine in the human telomere repeat sequence. ACS Nano 9:4296–4307. doi: 10.1021/acsnano.5b00722 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Lim KS, Cui L, Taghizadeh K, Wishnok JS, Chan W, Demott MS, Babu IR, Tannenbaum SR, Dedon PC (2012) In situ analysis of 8-Oxo-7,8-dihydro-2′-deoxyguanosine oxidation reveals sequence- and agent-specific damage spectra. J Am Chem Soc 134:18053–18064. doi: 10.1021/ja307525h CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Furman JL, Mok PW, Badran AH, Ghosh I (2011) Turn-on DNA damage sensors for the direct detection of 8-oxoguanine and photoproducts in native DNA. J Am Chem Soc 133:12518–12527. doi: 10.1021/ja1116606 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Nasr T, Li Z, Nakagawa O, Taniguchi Y, Ono S, Sasaki S (2009) Selective fluorescence quenching of the 8-oxoG-clamp by 8-oxodeoxyguanosine in ODN. Bioorg Med Chem Lett 19:727–730. doi: 10.1016/j.bmcl.2008.12.036 CrossRefPubMedGoogle Scholar
  80. 80.
    Taniguchi Y, Kawaguchi R, Sasaki S (2011) Adenosine-1,3-diazaphenoxazine derivative for selective base pair formation with 8-oxo-2′-deoxyguanosine in DNA. J Am Chem Soc 133:7272–7275. doi: 10.1021/ja200327u CrossRefPubMedGoogle Scholar
  81. 81.
    Taniguchi Y, Koga Y, Fukabori K, Kawaguchi R, Sasaki S (2012) OFF-to-ON type fluorescent probe for the detection of 8-oxo-dG in DNA by the Adap-masked ODN probe. Bioorg Med Chem Lett 22:543–546. doi: 10.1016/j.bmcl.2011.10.093 CrossRefPubMedGoogle Scholar
  82. 82.
    Taniguchi Y, Fukabori K, Kikukawa Y, Koga Y, Sasaki S (2014) 2,6-diaminopurine nucleoside derivative of 9-ethyloxy-2-oxo-1,3-diazaphenoxazine (2-amino-Adap) for recognition of 8-oxo-dG in DNA. Bioorg Med Chem 22:1634–1641. doi: 10.1016/j.bmc.2014.01.024 CrossRefPubMedGoogle Scholar
  83. 83.
    Steemers FJ, Chang W, Lee G, Barker DL, Shen R, Gunderson KL (2006) Whole-genome genotyping with the single-base extension assay. Nat Methods 3:31–33. doi: 10.1038/nmeth842 CrossRefPubMedGoogle Scholar
  84. 84.
    Liang F, Liu Y-Z, Zhang P (2013) Universal base analogues and their applications in DNA sequencing technology. RSC Adv 3:14910. doi: 10.1039/c3ra41492b CrossRefGoogle Scholar
  85. 85.
    Loakes D (2001) Survey and summary: the applications of universal DNA base analogues. Nucleic Acids Res 29:2437–2447. doi: 10.1093/nar/29.12.2437 CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Taniguchi Y, Kikukawa Y, Sasaki S (2015) Discrimination between 8-oxo-2′-deoxyguanosine and 2′-deoxyguanosine in DNA by the single nucleotide primer extension reaction with Adap triphosphate. Angew Chem Int Ed 54:5147–5151. doi: 10.1002/anie.201412086 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Shigeki Sasaki
    • 1
  • Yosuke Taniguchi
    • 1
  • Fumi Nagatsugi
    • 2
  1. 1.Graduate School of Pharmaceutical SciencesKyushu UniversityHigashi-kuJapan
  2. 2.Institute of Multidisciplinary Research for Advanced MaterialsTohoku UniversityAoba-kuJapan

Personalised recommendations