Polyamine–oligonucleotide conjugates: a promising direction for nucleic acid tools and therapeutics

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References

• 1 Burnett JC, Rossi JJ. RNA-based therapeutics: current progress and future prospects. Chem. Biol. 19(1), 60–71 (2012).
  Medline CASGoogle Scholar
• 2 Lightfoot HL, Hall J. Target mRNA inhibition by oligonucleotide drugs in man. Nucleic Acids Res. 40(21), 10585–10595 (2012).
  Medline CASGoogle Scholar
• 3 Bennett CF, Swayze EE. RNA targeting therapeutics: molecular mechanisms of antisense oligonucleotides as a therapeutic platform. Annu. Rev. Pharmacol. Toxicol. 50(1), 259–293 (2010).
  Medline CASGoogle Scholar
• 4 Deleavey GF, Damha MJ. Designing chemically modified oligonucleotides for targeted gene silencing. Chem. Biol. 19(8), 937–954 (2012).
  Medline CASGoogle Scholar
• 5 Lennox KA, Behlke MA. Chemical modification and design of anti-miRNA oligonucleotides. Gene Ther. 18(12), 1111–1120 (2011).
  Medline CASGoogle Scholar
• 6 Janssen HLA, Reesink HW, Lawitz EJ et al. Treatment of HCV infection by targeting microRNA. N. Engl. J. Med. 368(18), 1685–1694 (2013).
  Medline CASGoogle Scholar
• 7 Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411(6836), 494–498 (2001).
  Medline CASGoogle Scholar
• 8 Yu RZ, Geary RS, Levin AA. Pharmacokinetics and pharmacodynamics of antisense oligonucleotides. In: Pharmacokinetics and Pharmacodynamics of Biotech Drugs: Principles and Case Studies in Drug Development. Meibohm B (Ed.). Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany (2006).
  Google Scholar
• 9 Patwa A, Gissot A, Bestel I, Barthelemy P. Hybrid lipid oligonucleotide conjugates: synthesis, self-assemblies and biomedical applications. Chem. Soc. Rev. 40(12), 5844–5854 (2011).
  Medline CASGoogle Scholar
• 10 Raouane M, Desmaële D, Urbinati G, Massaad-Massade L, Couvreur P. Lipid conjugated oligonucleotides: a useful strategy for delivery. Bioconj. Chem. 23(6), 1091–1104 (2012).
  Medline CASGoogle Scholar
• 11 Schade M, Berti D, Huster D, Herrmann A, Arbuzova A. Lipophilic nucleic acids – a flexible construction kit for organization and functionalization of surfaces. Adv. Colloid Interface Sci. 208(0), 235–251 (2014).
  Medline CASGoogle Scholar
• 12 Marlin F, Simon P, Saison-Behmoaras T, Giovannangeli C. Delivery of oligonucleotides and analogues: the oligonucleotide conjugate-based approach. ChemBioChem 11(11), 1493–1500 (2010).
  Medline CASGoogle Scholar
• 13 Juliano RL, Ming X, Nakagawa O. Cellular uptake and intracellular trafficking of antisense and siRNA oligonucleotides. Bioconj. Chem. 23(2), 147–157 (2012).
  Medline CASGoogle Scholar
• 14 Ikeda Y, Nagasaki Y. Impacts of pegylation on the gene and oligonucleotide delivery system. J. Appl. Polym. Sci. 131(9), 40293 (2014).
  Google Scholar
• 15 De Piédoue G, Andrieu-Soler C, Concordet JP et al. Targeted gene correction with 5′ acridine-oligonucleotide conjugates. Oligonucleotides 17(2), 258–263 (2007).
  Medline CASGoogle Scholar
• 16 Goodchild J. Conjugates of oligonucleotides and modified oligonucleotides: a review of their synthesis and properties. Bioconj. Chem. 1(3), 165–187 (1990).
  Medline CASGoogle Scholar
• 17 Manoharan M. Oligonucleotide conjugates as potential antisense drugs with improved uptake, biodistribution, targeted delivery, and mechanism of action. Antisense Nucleic Acid Drug Dev. 12(2), 103–128 (2002).
  Medline CASGoogle Scholar
• 18 Lönnberg H. Solid-phase synthesis of oligonucleotide conjugates useful for delivery and targeting of potential nucleic acid therapeutics. Bioconj. Chem. 20(6), 1065–1094 (2009).•• Review on chemical synthesis of oligonucleotide conjugates.
  Medline CASGoogle Scholar
• 19 Peacock H, Kannan A, Beal PA, Burrows CJ. Chemical modification of siRNA bases to probe and enhance RNA interference. J. Org. Chem. 76(18), 7295–7300 (2011).
  Medline CASGoogle Scholar
• 20 Juliano RL, Ming X, Nakagawa O. The chemistry and biology of oligonucleotide conjugates. Acc. Chem. Res. 45(7), 1067–1076 (2012).
  Medline CASGoogle Scholar
• 21 Singh Y, Murat P, Spinelli N, Defrancq E. Oligonucleotide conjugates: rationale, synthesis, and applications. In: From Nucleic Acids Sequences to Molecular Medicine. Erdmann VA, Barciszewski J (Eds). Springer Berlin, Heidelberg, Germany, 85–120 (2012).
  Google Scholar
• 22 Winkler J. Oligonucleotide conjugates for therapeutic applications. Ther. Deliv. 4(7), 791–809 (2013).•• Describes conjugation reactions and conjugate pharmacokinetics.
  CASGoogle Scholar
• 23 Lightfoot HL, Hall J. Endogenous polyamine function – the RNA perspective. Nucleic Acids Res. 42(18), 11275–11290 (2014).•• Summarizes manners in which polyamines directly alter the function/properties of endogenous RNA molecules. Discusses interactions between polyamines and a variety of cellular RNA species including tRNAs, mRNA, rRNA and ribozymes
  Medline CASGoogle Scholar
• 24 Iacomino G, Picariello G, D'Agostino L. DNA and nuclear aggregates of polyamines. Biochim. Biophys. Acta 1823(10), 1745–1755 (2012).
  Medline CASGoogle Scholar
• 25 Igarashi K, Kashiwagi K. Modulation of cellular function by polyamines. Int. J. Biochem. Cell Biol. 42(1), 39–51 (2010).
  Medline CASGoogle Scholar
• 26 Boussif O, Lezoualc'h F, Zanta MA et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl Acad. Sci. USA 92(16), 7297–7301 (1995).
  Medline CASGoogle Scholar
• 27 Pichon C, Billiet L, Midoux P. Chemical vectors for gene delivery: uptake and intracellular trafficking. Curr. Opin. Biotechnol. 21(5), 640–645 (2010).
  Medline CASGoogle Scholar
• 28 Islam MA, Park TE, Singh B et al. Major degradable polycations as carriers for DNA and siRNA. J. Control. Release 193, 74–89 (2014).
  Medline CASGoogle Scholar
• 29 Noir R, Kotera M, Pons B, Remy JS, Behr JP. Oligonucleotide-oligospermine conjugates (zip nucleic acids): a convenient means of finely tuning hybridization temperatures. J. Am. Chem. Soc. 130, 13500–13505 (2008).
  Medline CASGoogle Scholar
• 30 Schmid N, Behr JP. Location of spermine and other polyamines on DNA as revealed by photoaffinity cleavage with poly(amino)benzenediazonium salts. Biochemistry 30(17), 4357–4361 (1991).
  Medline CASGoogle Scholar
• 31 Cooke LA, Frauendorf C, Gîlea MA, Holmes SC, Vyle JS. Solid-phase synthesis of terminal oligonucleotide–phosphoramidate conjugates. Tetrahedron Lett. 47(5), 719–722 (2006).
  CASGoogle Scholar
• 32 Levina AS, Mikhaleva EA, Repkova MN, Zarytova VF. Synthesis of polyamine-containing oligonucleotides. Russ. J. Bioorg. Chem. 34(1), 80–86 (2008).
  CASGoogle Scholar
• 33 Voirin E, Behr JP, Kotera M. Versatile synthesis of oligodeoxyribonucleotide–oligospermine conjugates. Nat. Protoc. 2(6), 1360–1367 (2007).
  Medline CASGoogle Scholar
• 34 Sund C, Puri N, Chattopadhyaya J. Synthesis of C-branched spermine tethered oligo-DNA and the thermal stability of the duplexes and triplexes. Tetrahedron 52(37), 12275–12290 (1996).
  CASGoogle Scholar
• 35 Sund C, Puri N, Chattopadhyaya J. The chemistry of C-branched spermine tethered oligo-DNAs and their properties in forming duplexes and triplexes. Nucleos. Nucleot. 16(5–6), 755–760 (1997).
  CASGoogle Scholar
• 36 Tung C-H, Breslauer KJ, Stein S. Polyamine-linked oligonucleotides for DNA triple helix formation. Nucleic Acids Res. 21(23), 5489–5494 (1993).
  Medline CASGoogle Scholar
• 37 Kubo T, Takamori K, Kanno K-I et al. Efficient cleavage of RNA, enhanced cellular uptake, and controlled intracellular localization of conjugate DNAzymes. Bioorg. Med. Chem. Lett. 15(1), 167–170 (2005).
  Medline CASGoogle Scholar
• 38 Pons B, Kotera M, Zuber G, Behr JP. Online synthesis of diblock cationic oligonucleotides for enhanced hybridization to their complementary sequence. ChemBioChem 7(8), 1173–1176 (2006).
  Medline CASGoogle Scholar
• 39 Moreau V, Voirin E, Paris C et al. Zip nucleic acids: New high affinity oligonucleotides as potent primers for PCR and reverse transcription. Nucleic Acids Res. 37(19), e130 (2009).
  MedlineGoogle Scholar
• 40 Lin C-N, Lin W-H, Hung L-N, Wang S-Y, Chiou M-T. Comparison of viremia of type II porcine reproductive and respiratory syndrome virus in naturally infected pigs by zip nucleic acid probe-based real-time PCR. BMC Vet. Res. 9(1), 181 (2013).
  MedlineGoogle Scholar
• 41 Begheldo M, Ditengou FA, Cimoli G et al. Whole-mount in situ detection of microRNAs on Arabidopsis tissues using zip nucleic acid probes. Anal. Biochem. 434(1), 60–66 (2013).
  Medline CASGoogle Scholar
• 42 Paris C, Moreau V, Deglane G, Voirin E, Erbacher P, Lenne-Samuel N. Zip nucleic acids are potent hydrolysis probes for quantitative PCR. Nucleic Acids Res. 38(7), e95 (2010).
  MedlineGoogle Scholar
• 43 Gagnon KT, Watts JK, Pendergraff HM et al. Antisense and antigene inhibition of gene expression by cell-permeable oligonucleotide-oligospermine conjugates. J. Am. Chem. Soc. 133(22), 8404–8407 (2011).• Zip nucleic acids as antisense and antigene agents in cellular assays.
  Medline CASGoogle Scholar
• 44 Nothisen M, Kotera M, Voirin E, Remy J-S, Behr J-P. Cationic siRNAs provide carrier-free gene silencing in animal cells. J. Am. Chem. Soc. 131(49), 17730–17731 (2009).
  Medline CASGoogle Scholar
• 45 Paris C, Moreau V, Deglane G et al. Conjugating phosphospermines to siRNAs for improved stability in serum, intracellular delivery and RNAi-mediated gene silencing. Mol. Pharm. 9(12), 3464–3475 (2012).
  Medline CASGoogle Scholar
• 46 Santoro SW, Joyce GF. A general purpose RNA-cleaving DNA enzyme. Proc. Natl Acad. Sci. USA 94(9), 4262–4266 (1997).
  Medline CASGoogle Scholar
• 47 Perche P, Nothisen M, Bagilet J, Behr J-P, Kotera M, Remy J-S. Cell-penetrating cationic siRNA and lipophilic derivatives efficient at nanomolar concentrations in the presence of serum and albumin. J. Controlled Release 170(1), 92–98 (2013).
  Medline CASGoogle Scholar
• 48 Haas J, Engels JW. A novel entry to 2′-O-aminopropyl modified nucleosides amenable for further modifications. Tetrahedron Lett. 48(50), 8891–8894 (2007).
  CASGoogle Scholar
• 49 Bramsen JB, Laursen MB, Nielsen AF et al. A large-scale chemical modification screen identifies design rules to generate siRNAs with high activity, high stability and low toxicity. Nucleic Acids Res. 37(9), 2867–2881 (2009).
  Medline CASGoogle Scholar
• 50 Prakash TP, Manoharan M, Fraser AS, Kawasaki AM, Lesnik EA, Owens SR. Zwitterionic oligonucleotides with 2′-O-[3-(N,N-dimethylamino)propyl]-RNA modification: synthesis and properties. Tetrahedron Lett. 41(25), 4855–4859 (2000).
  CASGoogle Scholar
• 51 Griffey RH, Monia BP, Cummins LL et al. 2′-O-aminopropyl ribonucleotides: a zwitterionic modification that enhances the exonuclease resistance and biological activity of antisense oligonucleotides. J. Med. Chem. 39(26), 5100–5109 (1996).
  Medline CASGoogle Scholar
• 52 Seio K, Tokugawa M, Kanamori T, Tsunoda H, Ohkubo A, Sekine M. Synthesis and properties of cationic 2′-O-[N-(4-aminobutyl)carbamoyl] modified oligonucleotides. Bioorg. Med. Chem. Lett. 22(7), 2470–2473 (2012).
  Medline CASGoogle Scholar
• 53 Noe CR, Winkler J, Urban E, Gilbert M, Haberhauer G, Brunar H. Zwitterionic oligonucleotides: a study on binding properties of 2′-O-aminohexyl modifications. Nucleos. Nucleot. Nucl. 24(8), 1167–1185 (2005).
  Medline CASGoogle Scholar
• 54 Teplova M, Wallace ST, Tereshko V et al. Structural origins of the exonuclease resistance of a zwitterionic RNA. Proc. Natl Adac. Sci. USA 96(25), 14240–14245 (1999).
  Medline CASGoogle Scholar
• 55 Prhavc M, Prakash TP, Minasov G, Cook PD, Egli M, Manoharan M. 2′-O-[2-[2-(N,N-dimethylamino)ethoxy]ethyl] modified oligonucleotides: symbiosis of charge interaction factors and stereoelectronic effects. Org. Lett. 5(12), 2017–2020 (2003).
  Medline CASGoogle Scholar
• 56 Azéma L, Bathany K, Rayner B. 2′-O-appended polyamines that increase triple-helix-forming oligonucleotide affinity are selected by dynamic combinatorial chemistry. ChemBioChem 11(18), 2513–2516 (2010).
  Medline CASGoogle Scholar
• 57 Winkler J, Noe CR. Oligonucleotide charge reversal: 2′-O-lysylaminohexyl modified oligonucleotides. Nucleos. Nucleot. Nucl. 26(8–9), 939–942 (2007).
  Medline CASGoogle Scholar
• 58 Winkler J, Gilbert M, Kocourková A, Stessl M, Noe CR. 2′-O-lysylaminohexyl oligonucleotides: modifications for antisense and siRNA. ChemMedChem 3(1), 102–110 (2008).
  Medline CASGoogle Scholar
• 59 Winkler J, Saadat K, Diaz-Gavilan M, Urban E, Noe CR. Oligonucleotide-polyamine conjugates: influence of length and position of 2′-attached polyamines on duplex stability and antisense effect. Eur. J. Med. Chem. 44(2), 670–677 (2009).• Oligonucleotides with 2′-attached polyamines of different length in cellular assays
  Medline CASGoogle Scholar
• 60 Kanazaki M, Ueno Y, Shuto S, Matsuda A. Highly nuclease-resistant phosphodiester-type oligodeoxynucleotides containing 4′α-C-aminoalkylthymidines form thermally stable duplexes with DNA and RNA. A candidate for potent antisense molecules. J. Am. Chem. Soc. 122(11), 2422–2432 (2000).
  CASGoogle Scholar
• 61 Winkler J, Giessrigl B, Novak C, Urban E, Noe C. 2′-O-lysylaminohexyladenosine modified oligonucleotides. Monatsh. Chem. 141(7), 809–815 (2010).
  CASGoogle Scholar
• 62 Egli M. Structural aspects of nucleic acid analogs and antisense oligonucleotides. Angew. Chem. Int. Ed. Engl. 35(17), 1894–1909 (1996).
  Google Scholar
• 63 Martin P. Ein neuer Zugang zu 2′-O-Alkylribonucleosiden und eigenschaften deren oligonucleotide. Helv. Chim. Acta 78(2), 486–504 (1995).
  CASGoogle Scholar
• 64 Herdewijn P. Heterocyclic modifications of oligonucleotides and antisense technology. Antisense Nucleic Acid Drug Dev. 10(4), 297–310 (2000).
  Medline CASGoogle Scholar
• 65 Kohgo S, Shinozuka K, Ozaki H, Sawai H. Synthesis of a novel 2′-deoxyuridine derivative bearing a cyanomethoxycarbonylmethyl group at C-5 position and its use for versatile post-synthetic functionalization of oligodeoxyribonucleotides. Tetrahedron Lett. 39(23), 4067–4070 (1998).
  CASGoogle Scholar
• 66 Sawai H, Nakamura A, Sekiguchi S, Yumoto K, Endoh M, Ozaki H. Efficient synthesis of new 5-substituted uracil nucleosides useful for linker arm incorporation. J. Chem. Soc., Chem. Commun. (17), 1997–1998 (1994).
  Google Scholar
• 67 Shinozuka K, Umeda A, Aoki T, Sawai H. Facile post-synthetic derivatization of oligodeoxynucleotide containing 5-methoxycarbonylmethyl-2′-deoxyuridine. Nucleos. Nucleot. 17(1–3), 291–300 (1998).
  CASGoogle Scholar
• 68 Heystek LE, Hui-Qiang Z, Dande P, Gold B. Control over the localization of positive charge in DNA: the effect on duplex DNA and RNA stability. J. Am. Chem. Soc. 120, 12165–12166 (1998).
  CASGoogle Scholar
• 69 Takeda T, Ikeda K, Mizuno Y, Ueda T. Synthesis and properties of deoxyoligonucleotides containing putrescinylthymine: nucleosides and nucleotides. Chem. Pharm. Bull. 35(9), 3558–3567 (1987).
  Medline CASGoogle Scholar
• 70 Haginoya N, Ono A, Nomura Y, Ueno Y, Matsuda A. Nucleosides and nucleotides. 160. Synthesis of oligodeoxyribonucleotides containing 5-(N-aminoalkyl)carbamoyl-2′-deoxyuridines by a new postsynthetic modification method and their thermal stability and nuclease-resistance properties. Bioconj. Chem. 8(3), 271–280 (1997).
  Medline CASGoogle Scholar
• 71 Ono A, Haginoya N, Kiyokawa M, Minakawa N, Matsuda A. Nucleosides and nucleotides. 127. A novel and convenient post-synthetic modification method for the synthesis of oligodeoxyribonucleotides carrying amino linkers at the 5-position of 2′-deoxyuridine. Bioorg. Med. Chem. Lett. 4(2), 361–366 (1994).
  CASGoogle Scholar
• 72 Ueno Y, Kumagai I, Haginoya N, Matsuda A. Effects of 5-(N-aminohexyl)carbamoyl-2′-deoxyuridine on endonuclease stability and the ability of oligodeoxynucleotide to activate RNase H. Nucleic Acids Res. 25(19), 3777–3782 (1997).
  Medline CASGoogle Scholar
• 73 Hashimoto H, Nelson MG, Switzer C. Zwitterionic DNA. J. Am. Chem. Soc. 115(16), 7128–7134 (1993).
  CASGoogle Scholar
• 74 Ozaki H, Nakamura A, Arai M, Endo M, Sawai H. Novel C5-substituted 2′-deoxyuridine derivatives bearing amino-linker arms: synthesis, incorporation into oligodeoxyribonucleotides, and their hybridization properties. Bull. Chem. Soc. Jpn. 68(7), 1981–1987 (1995).
  CASGoogle Scholar
• 75 Li Z, Huang L, Dande P, Gold B, Stone MP. Structure of a tethered cationic 3-aminopropyl chain incorporated into an oligodeoxynucleotide: evidence for 3′-orientation in the major groove accompanied by DNA bending. J. Am. Chem. Soc. 124(29), 8553–8560 (2002).
  Medline CASGoogle Scholar
• 76 Nara H, Ono A, Matsuda A. Nucleosides and nucleotides. 135. DNA duplex and triplex formation and resistance to nucleolytic degradation of oligodeoxynucleotides containing syn-norspermidine at the 5-position of 2′-deoxyuridine. Bioconj. Chem. 6(1), 54–61 (1995).
  Medline CASGoogle Scholar
• 77 Ueno Y, Mikawa M, Matsuda A. Nucleosides and nucleotides. 170. Synthesis and properties of oligodeoxynucleotides containing 5-[N-[2-[N,N-bis(2-aminoethyl)-amino]ethyl]carbamoyl]-2′-deoxyuridine and 5-[N-[3-[N,N-bis(3-aminopropyl)amino]propyl]carbamoyl]-2′-deoxyuridine. Bioconj. Chem. 9(1), 33–39 (1998).
  Medline CASGoogle Scholar
• 78 Ito T, Ueno Y, Komatsu Y, Matsuda A. Synthesis, thermal stability and resistance to enzymatic hydrolysis of the oligonucleotides containing 5‐(N‐aminohexyl)carbamoyl‐2′‐O‐methyluridines. Nucleic Acids Res. 31(10), 2514–2523 (2003).
  Medline CASGoogle Scholar
• 79 Juan ECM, Kondo J, Kurihara T et al. Crystal structures of DNA:DNA and DNA:RNA duplexes containing 5-(N-aminohexyl)carbamoyl-modified uracils reveal the basis for properties as antigene and antisense molecules. Nucleic Acids Res. 35(6), 1969–1977 (2007).
  Medline CASGoogle Scholar
• 80 Ozaki H, Mine M, Shinozuka K, Sawai H. Effect of imino group of a linker arm at the C5 position of a pyrimidine nucleoside on the thermal stabilities of DNA/DNA and DNA/RNA duplexes. Nucleos. Nucleot. Nucl. 23(1–2), 339–346 (2004).
  Medline CASGoogle Scholar
• 81 Matsukura M, Okamoto T, Miike T, Sawai H, Shinozuka K. Selective binding of trisamine-modified phosphorothioate antisense DNA to target mRNA improves antisense activity and reduces toxicity. Biochem. Biophys. Res. Commun. 293(5), 1341–1347 (2002).
  Medline CASGoogle Scholar
• 82 Shinozuka K, Matsukura M, Okamoto T, Sawai H. Synthesis and anti-HIV property of novel oligo-DNA phosphorothioate analogs bearing an intercalative moiety and/or polyamine residues. Nucleos. Nucleot. 17(9–11), 2081–2084 (1998).
  CASGoogle Scholar
• 83 Masud MM, Masuda T, Inoue Y, Kuwahara M, Sawai H, Ozaki H. Synthesis of modified siRNA bearing C-5 polyamine-substituted pyrimidine nucleoside in their 3′-overhang regions and its RNAi activity. Bioorg. Med. Chem. Lett. 21(2), 715–717 (2011).
  Medline CASGoogle Scholar
• 84 Moriguchi T, Sakai H, Suzuki H, Shinozuka K. Spermine moiety attached to the C-5 position of deoxyuridine enhances the duplex stability of the phosphorothioate DNA/complementary DNA and shows the susceptibility of the substrate to RNase H. Chem. Pharm. Bull. (Tokyo) 56(9), 1259–1263 (2008).
  Medline CASGoogle Scholar
• 85 Sakai H, Moriguchi T, Suzuki H, Matsukura M, Shinozuka K. Investigation of antisense DNA having C-5 polyamine substituted 2′-deoxyuridine derivative. Nucleic Acids Symp. Ser. 1(1), 127–128 (2001).
  Google Scholar
• 86 Marsh AJ, Williams DM, Grasby JA. The synthesis and properties of oligoribonucleotide-spermine conjugates. Org. Biomol. Chem. 2(14), 2103–2112 (2004).
  Medline CASGoogle Scholar
• 87 Markiewicz WT, Godzina P, Markiewicz M. Synthesis of polyaminooligonucleotides and their combinatorial libraries. Nucleos. Nucleot. 18(6–7), 1449–1454 (1999).
  CASGoogle Scholar
• 88 Brzezinska J, Gdaniec Z, Popenda L, Markiewicz WT. Polyaminooligonucleotide: NMR structure of duplex DNA containing a nucleoside with spermine residue, N-[4,9,13-triazatridecan-1-yl]-2′-deoxycytidine. Biochim. Biophys. Acta 1840(3), 1163–1170 (2014).• Nuclear magnetic resonance (NMR) structure of a C-4 spermine modification lying in the major groove.
  Medline CASGoogle Scholar
• 89 Prakash TP, Barawkar DA, Vaijayanti K, Ganesh KN. Synthesis of site-specific oligonucleotide–polyamine conjugates. Bioorg. Med. Chem. Lett. 4(14), 1733–1738 (1994).
  CASGoogle Scholar
• 90 Godzina P, Adrych-Rozek K, Markiewicz WT. Synthetic oligonucleotide combinatorial libraries. 3. Synthesis of polyamevonucleosides. Nucleos. Nucleot. 18(11–12), 2397–2414 (1999).
  CASGoogle Scholar
• 91 Potier P, Adib A, Kochkine A, Huc I, Behr J-P. Synthesis of oligonucleotides bearing polyamine groups for recognition of DNA sequences. Nucleos. Nucleot. 18(6–7), 1467–1468 (1999).
  CASGoogle Scholar
• 92 Schmid N, Behr J-P. Recognition of DNA sequences by strand replacement with polyamino-oligonucleotides. Tetrahedron Lett. 36(9), 1447–1450 (1995).
  CASGoogle Scholar
• 93 Potier P, Abdenaji A, Behr JP. Synthesis and hybridization properties of oligonucleotides containing polyamines at the C-2 position of purines: a presynthetic approach for the incorporation of spermine into oligodeoxynucleotides containing 2-(4,9,13-triazatridecyl)-2′-deoxyguanosine. Chem. Eur. J. 6(22), 4188–4194 (2000).
  Medline CASGoogle Scholar
• 94 Diaz AR, Eritja R, Garcia RG. Synthesis of oligodeoxynucleotides containing 2-substituted guanine derivatives using 2-fluoro-2′-deoxyinosine as common nucleoside precursor. Nucleos. Nucleot. 16(10–11), 2035–2051 (1997).
  CASGoogle Scholar
• 95 Markiewicz WT, Astriab A, Godzina P, Markiewicz M. Synthetic oligonucleotide combinatorial libraries and their applications. Farmaco 55(3), 174–177 (2000).
  Medline CASGoogle Scholar
• 96 Strauss JK, Roberts C, Nelson MG, Switzer C, Maher LJ. DNA bending by hexamethylene-tethered ammonium ions. Proc. Natl Acad. Sci. USA 93(18), 9515–9520 (1996).
  Medline CASGoogle Scholar
• 97 Hardwidge PR, Lee D-K, Prakash TP et al. DNA bending by asymmetrically tethered cations: influence of tether flexibility. Chem. Biol. 8(10), 967–980 (2001).
  Medline CASGoogle Scholar
• 98 Soto AM, Kankia BI, Dande P, Gold B, Marky LA. Incorporation of a cationic aminopropyl chain in DNA hairpins: thermodynamics and hydration. Nucleic Acids Res. 29(17), 3638–3645 (2001).
  Medline CASGoogle Scholar
• 99 Markiewicz WT, Godzina P, Markiewicz M, Astriab A. Synthesis of a polyaminooligonucleotide combinatorial library. Nucleos. Nucleot. 17(9–11), 1871–1880 (1998).
  CASGoogle Scholar
• 100 Strauss JK, Prakash TP, Roberts C, Switzer C, Maher LJ. DNA bending by a phantom protein. Chem. Biol. 3(8), 671–678 (1996).
  Medline CASGoogle Scholar
• 101 Cohen SS, McCormick FP. Polyamines and virus multiplication. In: Advances in Virus Research. Lauffer MA, Bang FB, Maramorosch K, Smith KM (Eds). Academic Press, 331–387 (1979).
  Google Scholar
• 102 Kropinski AMB, Bose RJ, Warren RaJ. 5-(4-aminobutylaminomethyl)uracil, an unusual pyrimidine from the dioxyribonucleic acid of bacteriophage phiW-14. Biochemistry 12(1), 151–157 (1973).
  Medline CASGoogle Scholar
• 103 Neuhard J, Maltman KL, Warren RA. Bacteriophage phiW-14-infected pseudomonas acidovorans synthesizes hydroxymethyldeoxyuridine triphosphate. J. Virol. 34(2), 347–353 (1980).
  Medline CASGoogle Scholar
• 104 Suck D. DNA recognition by DNase I. J. Mol. Recognit. 7(2), 65–70 (1994).
  Medline CASGoogle Scholar