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Glycotargeting to improve cellular delivery efficiency of nucleic acids

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Abstract

Nucleic acids bearing glycans of various structures have been under vigorous investigation in the past decade. The carbohydrate moieties of such complexes can serve as recognition sites for carbohydrate-binding proteins—lectins—and initiate receptor-mediated endocytosis. Therefore, carbohydrates can enhance cell targeting and internalization of nucleic acids that are associated with them and thus improve the bioavailability of nucleic acids as therapeutic agents. This review summarizes nucleic acid glycosylation in nature and approaches for the preparation of both non-covalently associated and covalently-linked carbohydrate-nucleic acid complexes.

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References

  1. Patil, S.D., Rhodes, D.G., Burgess, D.J.: DNA-based therapeutics and delivery systems: a comprehensive review. AAPS J. 7, E61–E77 (2005)

    PubMed  CAS  Google Scholar 

  2. Monsigny, M., Midoux, P., Mayer, R., Roche, A.C.: Glycotargeting: influence of the sugar moiety on both the uptake and the intracellular trafficking of nucleic acid carried by glycosylated polymers. Biosci. Rep. 19, 125–132 (1999)

    PubMed  CAS  Google Scholar 

  3. Zatsepin, T.S., Oretskaya, T.S.: Synthesis and applications of oligonucleotide-carbohydrate conjugates. Chem. & Biodiversity. 1, 1401–1417 (2004)

    CAS  Google Scholar 

  4. Simpson, L.: A base called J. Proc. Natl. Acad. Sci. USA 95, 2037–2038 (1998)

    Google Scholar 

  5. Dooijes, D., Chaves, I., Kieft, R., Dirks-Mulder, A., Martin, W., Borst, P.: Base J originally found in Kinetoplastida is also a minor constituent of nuclear DNA of Euglena gracilis. Nucleic Acids Res. 28, 3017–3021 (2000)

    PubMed  CAS  Google Scholar 

  6. van Leeuwen, F., Wijsman, E.R., Kuyl-Yeheskiely, E., van der Marel, G.A., van Boom, J.H., Borst, P.: The telomeric GGGTTA repeats of Trypanosoma brucei contain the hypermodified base J in both strands. Nucleic Acids Res. 24, 2476–2482 (1996)

    PubMed  Google Scholar 

  7. Gommers-Ampt, J.H., Borst, P.: Hypermodified bases in DNA. FASEB J. 9, 1034–1042 (1995)

    PubMed  CAS  Google Scholar 

  8. van Leeuwen, F., Wijsman, E.R., Kieft, R., van der Marel, G.A., van Boom, J.H., Borst, P.: Localization of the modified base J in telomeric VSG gene expression sites of Trypanosoma brucei. Genes Dev. 11, 3232–3241 (1997)

    PubMed  Google Scholar 

  9. van Leeuwen, F., Kieft, R., Cross, M., Borst, P.: Biosynthesis and function of the modified DNA base β-D-glucosyl-hydroxymethyluracil in Trypanosoma brucei. Mol. Cell. Biol. 10, 5643–5651 (1998)

    Google Scholar 

  10. Bernards, A., van Harten-Loosbroek, N., Borst, P.: Modification of telomeric DNA in Trypanosoma brucei; a role in antigenic variation? Nucleic Acids Res. 12, 4153–4170 (1984)

    PubMed  CAS  Google Scholar 

  11. Pays, E., Laurent, M., Delinte, K., Van Meirvenne, N., Steinert, M.: Differential size variations between transcriptionally active and inactive telomeres of Trypanosoma brucei. Nucleic Acids Res. 11, 8137–8147 (1983)

    PubMed  CAS  Google Scholar 

  12. Cross, M., Kieft, R., Sabatini, R., Wilm, M., de Kort, M., van der Marel, G.A., van Boom, J.H., van Leeuwen, F., Borst, P.: The modified base J is the target for a novel DNA-binding protein in kinetoplastid protozoans. EMBO J. 18, 6573–6581 (1999)

    PubMed  CAS  Google Scholar 

  13. van Leeuwen, F., Kieft, R., Cross, M., Borst, P.: Tandemly repeated DNA is a target for the aprial replacement of thmine by β-D-glucosyl-hydroxymethyluracil in Trypanosoma brucei. Mol. Biochem. Parasitol. 109, 133–145 (2000)

    PubMed  Google Scholar 

  14. Sabatini, R., Meeuwenoord, N., van Boom, J.H., Borst, P.: Recognition of base J in duplex DNA by J-binding protein. J. Biol. Chem. 277, 958–966 (2002)

    PubMed  CAS  Google Scholar 

  15. Sabatini, R., Meeuwenoord, N., Van Boom, J.H., Borst, P.: Site-specific interactions of JBP with base and sugar moieties in duplex J-DNA. J. Biol. Chem. 277, 28150–28156 (2002)

    PubMed  CAS  Google Scholar 

  16. Lichtenstein, J., Cohen, S.S.: Nucleotides derived from enzymatic digests of nucleic acids of T2, T4, and T6 bacteriophages. J. Biol. Chem. 235, 1134–1141 (1960)

    PubMed  CAS  Google Scholar 

  17. Lehman, I.R., Pratt, E.A.: On the structure of the glucosylated hydroxymethylcytosine nucleotides of coliphages T2, T4, and T6. J. Biol. Chem. 235, 3254–3259 (1960)

    PubMed  CAS  Google Scholar 

  18. Lunt, M.R., Siebke, J.C., Burton, K.: Glucosylated nucleotide sequences from T2-bacteriophage deoxyribonucleic acid. Biochem. J. 92, 27–36 (1964)

    PubMed  CAS  Google Scholar 

  19. Lunt, M.R., Newton, E.A.: Glucosylated nucleotide sequences from T-even bacteriophage deoxyribonucleic acids. Biochem. J. 95, 717–723 (1965)

    PubMed  CAS  Google Scholar 

  20. Richardson, C.C.: Influence of glucosylation of deoxyribonucleic acid on hydrolysis by deoxyribonucleases of Escherichia coli. J. Biol. Chem. 241, 2084–2092 (1966)

    PubMed  CAS  Google Scholar 

  21. Swinton, D., Hattman, S., Benzinger, R., Buchanan-Wollaston, V., Beringer, J.: Replacement of the deoxycytidine residues in Rhizobium bacteriophage RL38JI DNA. FEBS Lett. 184, 294–298 (1985)

    PubMed  CAS  Google Scholar 

  22. Ehrlich, M., Ehrlich, K.C.: A novel, highly modified, bacteriophage DNA in which thymine is partly replaced by a phosphoglucuronate moiety covalently bound to 5-(4′,5′-dihydroxypentyl)uracil. J. Biol. Chem. 256, 9966–9972 (1981)

    PubMed  CAS  Google Scholar 

  23. Brandon, C., Gallop, P.M., Marmur, J., Hayashi, H., Nakanishi, K.: Structure of a new pyrimidine from Bacillus subtilis phage SP-15 nucleic acid. Nature: New Biol. 239, 70–71 (1972)

    CAS  Google Scholar 

  24. Kasai, H., Ohashi, Z., Harada, F., Nishimura, S., Oppenheimer, N.J., Crain, P.F., Liehr, J.G., von Minden, D.L., McCloskey, J.A.: Structure of the modified nucleoside Q isolated from Escherichia coli transfer ribonucleic acid. 7-( 4,5-cis-dihydroxy-1-cyclopenten-3-ylaminomethyl)-7-deazaguanosin. Biochemistry 14, 4198–4208 (1975)

    PubMed  CAS  Google Scholar 

  25. Kasai, H., Kuchino, Y., Nihei, K., Nishimura, S.: Distribution of the modified nucleoside Q and its derivatives in animal and plant transfer RNA’s. Nucleic Acids Res. 2, 1931–1939 (1975)

    PubMed  CAS  Google Scholar 

  26. Kasai, H., Nakanishi, K., Macfarlane, R.D., Torgerson, D.F., Ohashi, Z., McCloskey, J.A., Gross, H.J., Nishimura, S.: The structure of Q* nucleoside isolated from Rabbit liver transfer ribonucleic acid. J. Am. Chem. Soc. 98, 5044–5046 (1976)

    PubMed  CAS  Google Scholar 

  27. Harada, F., Nishimura, S.: Possible anticodon sequences of tRNAHis, tRNAAsn and tRNAAsp from Escherichia coli B. Universal presence of nucleoside Q in the first position of the anticondons of these transfer ribonucleic acids. Biochemistry 11, 301–308 (1972)

    PubMed  CAS  Google Scholar 

  28. Kung, F.L., Nonekowski, S., Garcia, G.A.: tRNA-guanine transglycosylase from Escherichia coli: recognition of noncognate-cognate chimeric tRNA and discovery of a novel recognition site within the TΨC arm of tRNA. RNA 6, 233–244 (2000)

    PubMed  CAS  Google Scholar 

  29. Morris, R.C., Brown, K.G., Elliott, M.S.: The effect of queuosine on tRNA structure and function. J. Biomol. Struct. Dyn. 16, 757–774 (1999)

    PubMed  CAS  Google Scholar 

  30. Wu-Pong, S., Weiss, T.L., Hunt, C.A.: Antisense c-myc oligodeoxyribonucleotide cellular uptake. Pharm. Res. 9, 1010–1017 (1992)

    PubMed  CAS  Google Scholar 

  31. Wu-Pong, S., Weiss, T.L., Hunt, C.A.: Calcium dependent cellular uptake of a c-myc antisense oligonucleotide. Cell. Mol. Biol. 40, 843–850 (1994)

    PubMed  CAS  Google Scholar 

  32. Stein, C.A., Tonkinson, J.L., Zhang, L.M., Yakubov, L., Gervasoni, J., Taub, R., Rotenberg, S.A.: Dynamics of the internalization of phosphodiester oligodeoxynucleotides in HL60 cells. Biochemistry 32, 4855–4861 (1993)

    PubMed  CAS  Google Scholar 

  33. Hanss, B., Leal-Pinto, E., Bruggeman, L.A., Copeland, T.D., Klotman, P.E.: Identification and characterization of a cell membrane nucleic acid channel. Proc. Natl. Acad. Sci. U.S.A. 95, 1921–1926 (1998)

    PubMed  CAS  Google Scholar 

  34. Juliano, R.L.: Peptide-oligonucleotide conjugates for the delivery of antisense and siRNA. Curr. Opin. Mol. Ther. 7, 132–136 (2005)

    PubMed  CAS  Google Scholar 

  35. Dass, C.R.: Oligonucleotide delivery to tumours using macromolecular carriers. Biotechnol. Appl. Biochem. 40, 113–122 (2004)

    PubMed  CAS  Google Scholar 

  36. Lochmann, D., Jauk, E., Zimmer, A.: Drug delivery of oligonucleotides by peptides. Eur. J. Pharm. Biopharm. 58, 237–251 (2004)

    PubMed  CAS  Google Scholar 

  37. Shoji, Y., Nakashima, H.: Current status of delivery systems to improve target efficacy of oligonucleotides. Curr. Pharm. Des. 10, 785–796 (2004)

    PubMed  CAS  Google Scholar 

  38. Lysik, M.A., Wu-Pong, S.: Innovations in oligonucleotide drug delivery. J. Pharm. Sci. 92, 1559–1573 (2003)

    PubMed  CAS  Google Scholar 

  39. Wang, L., Prakash, R.K., Stein, C.A., Koehn, R.K., Ruffner, D.E.: Progress in the delivery of therapeutic oligonucleotides: organ/cellular distribution and targeted delivery of oligonucleotides in vivo. Antisense Nucleic Acid Drug Dev. 13, 169–189 (2003)

    PubMed  CAS  Google Scholar 

  40. Akhtar, S., Hughes, M.D., Khan, A., Bibby, M., Hussain, M., Nawaz, Q., Double, J., Sayyed, P.: The delivery of antisense therapeutics. Adv. Drug Deliv. Rev. 44, 3–21 (2000)

    PubMed  CAS  Google Scholar 

  41. Garcia-Chaumont, C., Seksek, O., Grzybowska, J., Borowski, E., Bolard, J.: Delivery systems for antisense oligonucleotides. Pharmacol. Ther. 87, 255–277 (2000)

    PubMed  CAS  Google Scholar 

  42. Lebedeva, I., Benimetskaya, L., Stein, C.A., Vilenchik, M.: Cellular delivery of antisense oligonucleotides. Eur. J. Pharm. Biopharm. 50, 101–119 (2000)

    PubMed  CAS  Google Scholar 

  43. Gewirtz, A.M., Stein, C.A., Glazer, P.M.: Facilitating oligonucleotide delivery: helping antisense deliver on its promise. Proc. Natl. Acad. Sci. U.S.A. 93, 3161–3163 (1996)

    PubMed  CAS  Google Scholar 

  44. Yamazaki, N., Kojima, S., Bovin, N.V., Andre, S., Gabius, S., Gabius, H.J.: Endogenous lectins as targets for drug delivery. Adv. Drug Deliv. Rev. 43, 225–244 (2000)

    PubMed  CAS  Google Scholar 

  45. Davis, B.G., Robinson, M.A.: Drug delivery systems based on sugar-macromolecule conjugates. Curr. Opin. Drug Discov. Dev. 5, 279–288 (2002)

    CAS  Google Scholar 

  46. Wadhwa, M.S., Rice, K.G.: Receptor mediated glycotargeting. J. Drug Target. 11, 255–268 (2003)

    Google Scholar 

  47. Wu, G.Y., Wu, C.H.: Receptor-mediated in vitro gene transformation by a soluble DNA carrier system. J. Biol. Chem. 262, 4429–4432 (1987)

    PubMed  CAS  Google Scholar 

  48. Wu, G.Y., Wu, C.H.: Receptor-mediated gene delivery and expression in vivo. J. Biol. Chem. 263, 14621–14624 (1988)

    PubMed  CAS  Google Scholar 

  49. Wu, G.Y., Wu, C.H.: Evidence for targeted gene delivery to Hep G2 hepatoma cells in vitro. Biochemistry 27, 887–892 (1988)

    PubMed  CAS  Google Scholar 

  50. Monsigny, M., Roche, A.C., Midoux, P., Mayer, R.: Glycoconjugates as carriers for specific delivery of therapeutic drugs and genes. Adv. Drug Deliv. Rev. 14, 1–24 (1994)

    CAS  Google Scholar 

  51. Erbacher, P., Roche, A.C., Monsigny, M., Midoux, P.: Putative role of chloroquine in gene transfer into a human hepatoma cell line by DNA/lactosylated polylysine complexes. Exp. Cell Res. 225, 186–194 (1996)

    PubMed  CAS  Google Scholar 

  52. Midoux, P., Mendes, C., Legrand, A., Raimond, J., Mayer, R., Monsigny, M., Roche, A.C.: Specific gene transfer mediated by lactosylated poly-L-lysine into hepatoma cells. Nucleic Acids Res. 21, 871–878 (1993)

    PubMed  CAS  Google Scholar 

  53. Choi, Y.H., Liu, F., Park, J.S., Kim, S.W.: Lactose-poly(ethylene glycol)-grafted poly-L-lysine as hepatoma cell-targeted gene carrier. Bioconjug. Chem. 9, 708–718 (1998)

    PubMed  CAS  Google Scholar 

  54. Han, J., Il Yeom, Y.: Specific gene transfer mediated by galactosylated poly-L-lysine into hepatoma cells. Int. J. Pharm. 202, 151–160 (2000)

    PubMed  CAS  Google Scholar 

  55. Chiou, H.C., Tangco, M.V., Levine, S.M., Robertson, D., Kormis, K., Wu, C.H., Wu, G.Y.: Enhanced resistance to nuclease degradation of nucleic acids complexed to asialoglycoprotein-polylysine carriers. Nucleic Acids Res. 22, 5439–5446 (1994)

    PubMed  CAS  Google Scholar 

  56. Ferkol, T., Lindberg, G.L., Chen, J., Perales, J.C., Crawford, D.R., Ratnoff, O.D., Hanson, R.W.: Regulation of phosphoenolpyruvate carboxykinase/humanfactor IX gene introduced into the livers of adult rats by receptor mediated gene transfer. FASEB J. 7, 1081–1091 (1993)

    PubMed  CAS  Google Scholar 

  57. McKee, T.D., DeRome, M.E., Wu, G.Y., Findeis, M.A.: Preparation of asialoorosomucoid-polylysine conjugates. Bioconjug. Chem. 5, 306–311 (1994)

    PubMed  CAS  Google Scholar 

  58. Perales, J.C., Ferkol, T., Beegan, H., Ratnoff, O.D., Hanson, R.W.: Gene transfer in vivo: sustained expression and regulation of genes introduced into liver by receptor targeted uptake. Proc. Natl. Acad. Sci. U.S.A. 91, 4086–4090 (1994)

    PubMed  CAS  Google Scholar 

  59. Curiel, D.T., Agarwal, S., Wagner, E., Cotton, M.: Adenovirus enhancement of transferrin-polylysine-mediated gene delivery. Proc. Natl. Acad. Sci. U.S.A. 88, 8850–8854 (1991)

    PubMed  CAS  Google Scholar 

  60. Boussif, O., Lezoualc’h, F., Zanta, M.A., Mergny, M.D., Scherman, D., Demeneix, B., Behr, J.P.: A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. U.S.A. 92, 7297–7301 (1995)

    PubMed  CAS  Google Scholar 

  61. Grosse, S., Aron, Y., Honoré, I., Thévenot, G., Danel, C., Roche, A-C., Monsigny, M., Fajac, I.: Lactosylated polyethylenimine for gene transfer into airway epithelial cells: role of the sugar moiety in cell delivery and intracellular trafficking of the complexes. J. Gene Med. 6, 345–356 (2004)

    PubMed  CAS  Google Scholar 

  62. Fajac, I., Thévenot, G., Bédouet, L., Danel, C., Riquet, M., Merten, M., Figarella, C., Dall’ Ava-Santucci, J., Monsigny, M., Briand, P.: Uptake of plasmid/glycosylated polymer complexes and gene transfer efficiency in differentiated airway epithelial cells. J. Gene Med. 5, 38–48 (2003)

    PubMed  CAS  Google Scholar 

  63. Leclercq, F., Dubertret, C., Pitard, B., Scherman, D., Herscovici, J.: Synthesis of Glycosylated polyethylenimine with reduced toxicity and high transfecting efficiency. Bioorg. Med. Chem. Lett. 10, 1233–1235 (2000)

    PubMed  CAS  Google Scholar 

  64. Bettinger, T., Remy, J.S., Erbacher, P.: Size reduction of galactosylated PEI/DNA complexes improves lectin-mediated gene transfer into hepatocytes. Bioconjug. Chem. 10, 558–561 (1999)

    PubMed  CAS  Google Scholar 

  65. Kunath, K., von Harpe, A., Fischer, D., Kissel, T.: Galactose-PEI-DNA complexes for targeted gene delivery: degree of substitution affects complex size and transfection efficiency. J. Control. Release 88, 159–172 (2003)

    PubMed  CAS  Google Scholar 

  66. Morimoto, K., Nishikawa, M., Kawakami, S., Nakano, T., Hattori, Y., Fumoto, S., Yamashita, F., Hashida, M.: Molecular weight-dependent gene transfection activity of unmodified and galactosylated polyethyleneimine on hepatoma cells and mouse liver. Mol. Ther. 7, 254–261 (2003)

    PubMed  CAS  Google Scholar 

  67. Kim, S.H., Goto, M., Akaike, T.: Specific binding of glucose-derivatized polymers to the asialoglycoprotein receptor of mouse primary hepatocytes. J. Biol. Chem. 276, 35312–35319 (2001)

    PubMed  CAS  Google Scholar 

  68. Fabio, K., Gaucheron, J., Di Giorgio, C., Vierling, P.: Novel galactosylated polyamine bolaamphiphiles for gene delivery. Bioconjug. Chem. 14, 358–367 (2003)

    PubMed  CAS  Google Scholar 

  69. Reinis, M., Damkova, M., Korec, E.: Receptor-mediated transport of oligodeoxynucleotides into hepatic cells. J. Virol. Methods 42, 99–105 (1993)

    PubMed  CAS  Google Scholar 

  70. Ogris, M., Steinlein, P., Carotta, S., Brunner, S., Wagner, E.: DNA/polyethylenimine transfection particles: influence of ligands, polymer size, and PEGylation on internalization and gene expression. AAPS PharmSci. 3, E21 (2001)

    PubMed  CAS  Google Scholar 

  71. Dheur, S., Dias, N., van Aerschot, A., Herdewijn, P., Bettinger, T., Remy, J.S., Helene, C., Saison-Behmoaras, E.T.: Polyethylenimine but not cationic lipid improves antisense activity of 3′-capped phosphodiester oligonucleotides. Antisense Nucleic Acid Drug Dev. 9, 515–525 (1999)

    PubMed  CAS  Google Scholar 

  72. Godbey, W.T., Wu, K.K., Mikos, A.G.: Tracking the intracellular path of poly(ethylenimine)/DNA complexes for gene delivery. Proc. Natl. Acad. Sci. U.S.A. 96, 5177–5181 (1999)

    PubMed  CAS  Google Scholar 

  73. Kukowska-Latallo, J.F., Bielinska, A.U., Johnson, J., Spindler, R., Tomalia, D.A., Baker, J.R., Jr.: Efficient transfer of genetic material into mammalian cells using Starburst polyamidoamine dendrimers. Proc. Natl. Acad. Sci. U.S.A. 93, 4897–4902 (1996)

    PubMed  CAS  Google Scholar 

  74. Bielinska, A., Kukowska-Latallo, J.F., Johnson, J., Tomalia, D.A., Baker, J.R., Jr.: Regulation of in vitro gene expression using antisense oligonucleotides or antisense expression plasmids transfected using starburst PAMAM dendrimers, Nucleic Acids Res. 24, 2176–2182 (1996)

    PubMed  CAS  Google Scholar 

  75. Haensler, J., Szoka, F.C.: Polyamidoamine cascade polymers mediate efficient transfection of cells in culture. Bioconjug. Chem. 4, 372–379 (1993)

    PubMed  CAS  Google Scholar 

  76. Lim, D.W., Yeom, Y.I., Park, T.G.: Poly(DMAEMA-NVP)-b-PEG-galactose as gene delivery vector for hepatocytes. Bioconjug. Chem. 11, 688–695 (2000)

    PubMed  CAS  Google Scholar 

  77. Sundaram, S., Viriyayuthakorn, S., Roth, C.M.: Oligonucleotide structure influences the interactions between cationic polymers and oligonucleotides. Biomacromol. 6, 2961–2968 (2005)

    CAS  Google Scholar 

  78. Bonfils, E., Mendes, C., Roche, A-C., Monsigny, M., Midoux, P.: Uptake by macrophages of a biotinylated oligo-α-deoxythymidylate by using mannosylated streptavidin. Bioconjug. Chem. 3, 277–284 (1992)

    PubMed  CAS  Google Scholar 

  79. Strydom, S., Van Jaarsveld, P., Van Helden, E., Ariatti, M., Hawtrey, A.: Studies on the transfer of DNA into cells through use of avidin-polylysine conjugates complexed to biotinylated transferrin and DNA. J. Drug Target. 1, 165–174 (1993)

    PubMed  CAS  Google Scholar 

  80. Schoeman, R., Joubert, D., Ariatti, M., Hawtrey, A.O.: Further studies on targeted DNA transfer to cells using a highly efficient delivery system of biotinylated transferrin and biotinylated polylysine complexed to streptavidin. J. Drug Target. 2, 509–516 (1995)

    PubMed  CAS  Google Scholar 

  81. Haensler, J., Szoka, F.C.: Synthesis and characterization of a trigalactosylated bisacridine compound to target DNA to hepatocytes. Bioconjug. Chem. 4, 85–93 (1993)

    PubMed  CAS  Google Scholar 

  82. Sakurai, K., Kimura, T., Koumoto, K., Mizu, M., Kobayashi, R., Shinkai, S.: Application of schizophyllan as a novel gene carrier. Nucleic Acids Res. (Suppl.) 223–224 (2001)

  83. Matsumoto, T., Numata, M., Anada, T., Mizu, M., Koumoto, K., Sakurai, K., Nagasaki, T., Shinkai, S.: Chemically modified polysaccharide schizophyllan for antisense oligonucleotides delivery to enhance the cellular uptake efficiency. Biochim. Biophys. Acta. 1670, 91–104 (2004)

    PubMed  CAS  Google Scholar 

  84. Hasegawa, T., Umeda, M., Matsumoto, T., Numata, M., Mizu, M., Koumoto, K., Sakurai, K., Shinkai, S.: Lactose-appended schizophyllan is a potential candidate as a hepatocyte-targeted antisense carrier. Chem. Commun. 382–383 (2004)

  85. Mizu, M., Koumoto, K., Kimura, T., Sakurai, K., Shinkai, S.: Protection of polynucleotides against nuclease-mediated hydrolysis by complexation with schizophyllan. Biomaterials 25, 3109–3116 (2004)

    PubMed  CAS  Google Scholar 

  86. Mizu, M., Koumoto, K., Anada, T., Sakurai, K., Shinkai, S.: Antisense oligonucleotides bound in the polysaccharide complex and the enhanced antisense effect due to the low hydrolysis. Biomaterials 25, 3117–3123 (2004)

    PubMed  CAS  Google Scholar 

  87. Karinaga, R., Koumoto, K., Mizu, M., Anada, T., Shinkai, S., Sakurai, K.: PEG-appended β-(1→3)-D-glucan schizophyllan to deliver antisense-oligonucleotides with avoiding lysosomal degradation. Biomaterials 26, 4866–4873 (2005)

    PubMed  CAS  Google Scholar 

  88. Karinaga, R., Anada, T., Minari, J., Mizu, M., Koumoto, K., Fukuda, J., Nakazawa, K., Hasegawa, T., Numata, M., Shinkai, S., Sakurai, K.: Galactose-PEG dual conjugation of β-(1→3)-D-glucan schizophyllan for antisense oligonucleotides delivery to enhance the cellular uptake. Biomaterials 27, 1626–1635 (2006)

    PubMed  CAS  Google Scholar 

  89. Hasegawa, T., Fujisawa, T., Numata, M., Matsumoto, T., Umeda, M., Karinaga, R., Mizu, M., Koumoto, K., Kimura, T., Okumura, S., Sakurai, K., Shinkai, S.: Schizophyllans carrying oligosaccharide appendages as potential candidates for cell-targeted antisense carrier. Org. Biomol. Chem. 2, 3091–3098 (2004)

    PubMed  CAS  Google Scholar 

  90. Koumoto, K., Kimura, T., Sakurai, K., Shinkai, S.: Polysaccharide-polynucleotide complexes (IV): antihydrolysis effect of the schizophyllan/poly(C) complex and the complex dissociation induced by amines. Bioorg. Chem. 29, 178–185 (2001)

    PubMed  CAS  Google Scholar 

  91. Akhtar, S., Routledge, A., Patel, R., Gardiner, J.M.: Synthesis of mono- and dimannoside phosphoramidite derivatives for solid-phase conjugation to oligonucleotides. Tetrahedron Lett. 36, 7333–7336 (1995)

    CAS  Google Scholar 

  92. Sheppard, T.L., Wong, C.-H., Joyce, G.F.: Nucleoglycoconjugates: design and synthesis of a new class of DNA-carbohydrate conjugates. Angew. Chem. Int. Ed. 39, 3660–3663 (2000)

    CAS  Google Scholar 

  93. Adinolfi, M., Barone, G., De Napoli, L., Guariniello, L., Iadonisi, A., Piccialli, G.: Solid phase glycosidation of oligonucleotides. Tetrahedron Lett. 40, 2607–2610 (1999)

    CAS  Google Scholar 

  94. Katajisto, J., Heinonen, P., Lonnberg, H.: Solid-phase synthesis of oligonucleotide glycoconjugates bearing three different glycosyl groups: orthogonally protected bis(hydroxymethyl)-N,N′-bis(3-hydroxypropyl)malondiamide phosphoramidite as key building block. J. Org. Chem. 69, 7609–7615 (2004)

    PubMed  CAS  Google Scholar 

  95. Adinolfi, M., De Napoli, L., Di Fabio, G., Guariniello, L., Iadonisi, A., Messere, A., Montesarchio, D., Piccialli, G.: Solid-phase synthesis of glyco-oligonucleotide conjugates. Synlett 745–748 (2001)

  96. Adinolfi, M., De Napoli, L., Di Fabio, G., Iadonisi, A., Montesarchio, D., Piccialli, G.: Solid phase synthesis of oligonucleotides tethered to oligo-glucose phosphate tails. Tetrahedron 58, 6697–6704 (2002)

    CAS  Google Scholar 

  97. Adinolfi, M., De Napoli, L., Di Fabio, G., Iadonisi, A., Montesarchio, D.: Modulating the activity of oligonucleotides by carbohydrate conjugation: solid phase synthesis of sucrose-oligonucleotide hybrids. Org. Biomol. Chem. 2, 1879–1886 (2004)

    PubMed  CAS  Google Scholar 

  98. D’Onofrio, J., de Champdoré, M., De Napoli, L., Montesarchio, D., Di Fabio, G.: Glycomimetics as decorating motifs for oligonucleotides: solid-phase synthesis, stability, and hybridization properties of carbopeptoid-oligonucleotide conjugates. Bioconjug. Chem. 16, 1299–1309 (2005)

    PubMed  CAS  Google Scholar 

  99. Wang, Y., Sheppard, T.L.: Chemoenzymatic Synthesis and Antibody Detection of DNA Glycoconjugates. Bioconjug. Chem. 14, 1314–1322 (2003)

    PubMed  CAS  Google Scholar 

  100. Matsuura, K., Hibino, M., Ikeda, T., Yamada, Y., Kobayashi, K.: Self-organized glycoclusters along DNA: effect of the spatial arrangement of galactoside residues on cooperative lectin recognition. Chem. Eur. J. 10, 352–359 (2004)

    CAS  Google Scholar 

  101. Yamada, Y., Matsuura, K., Kobayashi, K.: Cooperative lectin recognition of periodical glycoclusters along DNA duplexes: alternate hybridization and full hybridization. Bioorg. Med. Chem. 13, 1913–1922 (2005)

    PubMed  CAS  Google Scholar 

  102. Matsuura, K., Hibino, M., Yamada, Y., Kobayashi, K.: Construction of glyco-clusters by self-organization of site-specifically glycosylated oligonucleotides and their cooperative amplification of lectin-recognition. J. Am. Chem. Soc. 123, 357–358 (2001)

    PubMed  CAS  Google Scholar 

  103. Akasaka, T., Matsuura, K., Emi, N., Kobayashi, K.: Conjugation of plasmid DNAs with lactose via diazocoupling enhances resistance to restriction enzymes and acquires binding affinity to galactose-specific lactin. Biochem. Biophys. Res. Commun. 260, 323–328 (1999)

    PubMed  CAS  Google Scholar 

  104. Matsuura, K., Akasaka, T., Hibino, M., Kobayashi, K.: Facile synthesis of stable and lectin-recognizable DNA-carbohydrate conjugates via diazo coupling. Bioconjug. Chem. 11, 202–211 (2000)

    PubMed  CAS  Google Scholar 

  105. Matsuura, M., Akasaka, T., Hibino, M., Kobayashi, K.: Synthesis of DNA-carbohydrate conjugate via diazocoupling: a new class of modified DNA with enhanced stability and lectin-recognition ability. Chem. Lett. 247–248 (1999)

  106. Forget, D., Boturyn, D., Renaudet, O., Defrancq, E., Dumy, P.: Highly efficient synthesis of peptide- and carbohydrate-oligonucleotide conjugates using chemoselective oxime and thiazolidine formation. Nucleosides Nucleotides Nucleic Acids 22, 1427–1429 (2003)

    PubMed  CAS  Google Scholar 

  107. Edupuganti, O.P., Renaudet, O., Defrancq, E., Dumy, P.: The oxime bond formation as an efficient chemical tool for the preparation of 3′,5′-bifunctionalised oligodeoxyribonucleotides. Bioorg. Med. Chem. Lett. 14, 2839–2842 (2004)

    PubMed  CAS  Google Scholar 

  108. Edupuganti, O.P., Singh, Y., Defrancq, E., Dumy, P.: New strategy for the synthesis of 3′,5′-bifunctionalized oligonucleotide conjugates through sequential formation of chemoselective oxime bonds. Chem. Eur. J. 10, 5988–5995 (2004)

    CAS  Google Scholar 

  109. Katajisto, J., Virta, P., Lonnberg, H.: Solid-phase synthesis of multiantennary oligonucleotide glycoconjugates utilizing on-support oximation. Bioconjug. Chem. 15, 890–896 (2004)

    PubMed  CAS  Google Scholar 

  110. Singh, Y., Renaudet, O., Defrancq, E., Dumy, P.: Preparation of a multitopic glycopeptide-oligonucleotide conjugate. Org. Lett. 7, 1359–1362 (2005)

    PubMed  CAS  Google Scholar 

  111. Lundquist, J.J., Toone, E.J.: The cluster glycoside effect. Chem. Rev. 102, 555–578 (2002)

    PubMed  CAS  Google Scholar 

  112. Sando, S., Matsui, K., Niinomi, Y., Sato, N., Aoyama, Y.: Facile preparation of DNA-tagged carbohydrates. Bioorg. Med. Chem. Lett. 13, 2633–2636 (2003)

    PubMed  CAS  Google Scholar 

  113. Zatsepin, T.S., Stetsenko, D.A., Gait, M.J., Oretskaya, T.S.: Use of carbonyl group addition-elimination reactions for synthesis of nucleic acid conjugates. Bioconjug. Chem. 16, 471–489 (2005)

    PubMed  CAS  Google Scholar 

  114. Schwartz, D.A., Hogrefe, R.I.: Functional biopolymer modification reagents and uses thereof, WO 02/10431 A2 (2002)

  115. Okamoto, A., Tainaka, K., Saito, I.: A facile incorporation of the aldehyde function into DNA: 3-formylindole nucleoside as an aldehyde-containing universal nucleoside. Tetrahedron Lett. 43, 4581–4583 (2002)

    CAS  Google Scholar 

  116. Biessen, E.A.L., Beuting, D.M., Roelen, H.C.P.F., van de Marel, G.A., van Boom, J.H., Van Berkel, T.J.C.: Synthesis of cluster galactosides with high affinity for the Hepatic asialoglycoprotein receptor. J. Med. Chem. 38, 1538–1546 (1995)

    PubMed  CAS  Google Scholar 

  117. Hangeland, J.J., Flesher, J.E., Deamond, S.F., Lee, Y.C., Ts’O, P.O., Frost, J.J.: Tissue distribution and metabolism of the [32P]-labeled oligodeoxynucleoside methylphosphonate-neoglycopeptide conjugate, [YEE(ah-GalNAc)3]-SMCC-AET-pUmpT7, in the mouse. Antisense Nucleic Acid Drug Dev. 7, 141–149 (1997)

    PubMed  CAS  Google Scholar 

  118. Duff, R.J., Deamond, S.F., Roby, C., Zhou, Y., Ts’o, P.O.P.: Intrabody tissue-specific delivery of antisense conjugates in animals: ligand-linker-antisense oligomerconjugates. Methods Enzymol. 313, 297–321 (2000)

    Article  PubMed  CAS  Google Scholar 

  119. Biessen, E.A., Vietsch, H., Rump, E.T., Fluiter, K., Kuiper, J., Bijsterbosch, M.K., van Berkel, T.J.: Targeted delivery of oligodeoxynucleotides to parenchymal liver cells in vivo. Biochem. J. 340, 783–792 (1999)

    PubMed  CAS  Google Scholar 

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Acknowledgements

Work in the laboratory of HY is supported by funding from Canada Foundation for Innovation and Research Corporation. The authors thank Professors Colin B. Reese and Joffre Mercier for helpful comments on the manuscript.

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  1. Department of Chemistry, Brock University, 500 Glenridge Ave., St. Catharines, ON, Canada, L2S 3A1

    Hongbin Yan & Kha Tram

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  1. Hongbin Yan
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  2. Kha Tram
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Correspondence to Hongbin Yan.

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Yan, H., Tram, K. Glycotargeting to improve cellular delivery efficiency of nucleic acids. Glycoconj J 24, 107–123 (2007). https://doi.org/10.1007/s10719-006-9023-y

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