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Journal of Nucleic Acids
Volume 2011, Article ID 748632, 17 pages
http://dx.doi.org/10.4061/2011/748632
Research Article

Site-Selective Artificial Ribonucleases: Oligonucleotide Conjugates Containing Multiple Imidazole Residues in the Catalytic Domain

1Institute of Chemical Biology and Fundamental Medicine, Siberian Branch of the Russian Academy of Sciences, Novosibirsk 630090, Russia
2School of Pharmacy and Pharmaceutical Sciences, The University of Manchester, Manchester M13 9PL, UK
3Fidelity Systems Inc., 7961 Cessna Avenue, Gaithersburg, MD 20879, USA

Received 7 April 2011; Accepted 5 July 2011

Academic Editor: Dmitry A. Stetsenko

Copyright © 2011 Natalia G. Beloglazova et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. A. Zenkova and N. G. Beloglazova, “Site-specific artificial ribonucleases: conjugates of oligonucleotides with catalytic groups,” in Nucleic Acids and Molecular Biology: Artificial Nucleases, M. A. Zenkova, Ed., vol. 13, pp. 189–222, Springer, Berlin, Germany, 2004. View at Google Scholar
  2. V. N. Sil'nikov and V. V. Vlassov, “Design of site-specific RNA-cleaving reagents,” Russian Chemical Reviews, vol. 70, no. 6, pp. 491–508, 2001. View at Google Scholar · View at Scopus
  3. H. Lönnberg, “Cleavage of RNA phosphodiester bonds by small molecular entities: a mechanistic insight,” Organic and Biomolecular Chemistry, vol. 21, pp. 1687–1703, 2011. View at Publisher · View at Google Scholar
  4. G. N. Grimm, A. S. Boutorine, and C. Hélène, “Rapid routes of synthesis of oligonucleotide conjugates from non-protected oligonucleotides and ligands possessing different nucleophilic or electrophilic functional groups,” Nucleosides, Nucleotides and Nucleic Acids, vol. 19, no. 10–12, pp. 1943–1965, 2000. View at Google Scholar · View at Scopus
  5. A. S. Modak, J. K. Gard, M. C. Merriman, K. A. Winkeler, J. K. Bashkin, and M. K. Stern, “Toward chemical ribonucleases 2. Synthesis and characterization of nucleoside-bipyridine conjugates. Hydrolytic cleavage of RNA by their copper(II) complexes,” Journal of the American Chemical Society, vol. 113, no. 1, pp. 283–291, 1991. View at Google Scholar · View at Scopus
  6. J. K. Bashkin, J. Xie, A. T. Daniher, U. Sampath, and J. L. F. Kao, “Building blocks for ribozyme mimics: conjugates of terpyridine and bipyridine with nucleosides,” Journal of Organic Chemistry, vol. 61, no. 7, pp. 2314–2321, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Hovinen, “Synthesis of carbon-3-substituted 1,5,9-triazacyclododecanes, RNA cleavage agents suitable for oligonucleotide tethering,” Bioconjugate Chemistry, vol. 9, no. 1, pp. 132–136, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Inoue, M. Shimizu, T. Furukawa, T. Tamura, M. Matsui, and E. Ohtsuka, “Site-specific RNA cleavage using terpyridine · Cu(II)-linked 2'-O- methyloligonucleotides,” Nucleosides and Nucleotides, vol. 18, no. 6-7, pp. 1503–1505, 1999. View at Google Scholar · View at Scopus
  9. J. K. Bashkin, E. I. Frolova, and U. Sampath, “Sequence-specific cleavage of HIV mRNA by a ribozyme mimic,” Journal of the American Chemical Society, vol. 116, no. 13, pp. 5981–5982, 1994. View at Google Scholar · View at Scopus
  10. T. H. Smith, J. V. LaTour, D. Bochkariov, G. Chaga, and P. S. Nelson, “Bifunctional phosphoramidite reagents for the introduction of histidyl and dihistidyl residues into oligonucleotides,” Bioconjugate Chemistry, vol. 10, no. 4, pp. 647–652, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. D. M. Perrin, T. Garestier, and C. Hélène, “Bridging the gap between proteins and nucleic acids: a metal-independent RNAse A mimic with two protein-like functionalities,” Journal of the American Chemical Society, vol. 123, no. 8, pp. 1556–1563, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. N. G. Beloglazova, N. N. Polushin, V. N. Sil'nikov, M. A. Zenkova, and V. V. Vlassov, “Site selective cleavage of yeast tRNAPhe by conjugates of antisense oligonucleotide with imidazole containing cleaving groups,” Doklady Academii Nauk, vol. 369, no. 6, pp. 827–830, 1999. View at Google Scholar
  13. L. Yurchenko, V. Silnikov, T. Godovikova, G. Shishkin, J. J. Toulme, and V. Vlassov, “Cleavage of Leishmania mini-exon sequence by oligonucleotides conjugated to a diimidazole construction,” Nucleosides and Nucleotides, vol. 16, no. 7–9, pp. 1721–1725, 1997. View at Google Scholar · View at Scopus
  14. V. Vlassov, T. Abramova, T. Godovikova, R. Giege, and V. Silnikov, “Sequence-specific cleavage of yeast tRNAPhe with oligonucleotides conjugated to a diimidazole construct,” Antisense and Nucleic Acid Drug Development, vol. 7, no. 1, pp. 39–42, 1997. View at Google Scholar · View at Scopus
  15. K. Ushijima, H. Gouzu, K. Hosono et al., “Site-specific cleavage of tRNA by imidazole and/or primary amine groups bound at the 5′-end of oligodeoxyribonucleotides,” Biochimica et Biophysica Acta, vol. 1379, no. 2, pp. 217–223, 1998. View at Google Scholar · View at Scopus
  16. V. Silnikov, G. Zuber, J. P. Behr, R. Giege, and V. Vlassov, “Design of ribonuclease mimics for sequence specific cleavage of RNA,” Phosphorus, Sulfur and Silicon and Related Elements, vol. 109-110, no. 1–4, pp. 277–280, 1996. View at Google Scholar · View at Scopus
  17. J. Hovinen, A. Guzaev, E. Azhayeva, A. Azhayev, and H. Lönnberg, “Imidazole tethered oligodeoxyribonucleotides: synthesis and RNA cleaving activity,” Journal of Organic Chemistry, vol. 60, no. 7, pp. 2205–2209, 1995. View at Google Scholar · View at Scopus
  18. A. Y. Karyagin, T. V. Abramova, V. N. Sil'nikov, and G. V. Shishkin, “Reagents for addressed modification of biopolymers,” Russian Chemical Bulletin, vol. 49, no. 3, pp. 540–545, 2000. View at Google Scholar · View at Scopus
  19. M. A. Reynolds, T. A. Beck, P. B. Say et al., “Antisense oligonucleotides containing an internal, non-nucleotide-based linker promote site-specific cleavage of RNA,” Antisense and Nucleic Acid Drug Development, vol. 24, no. 4, pp. 760–765, 1996. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Endo, Y. Azuma, Y. Saga, A. Kuzuya, G. Kawai, and M. Komiyama, “Molecular design for a pinpoint RNA scission. Interposition of oligoamines between two DNA oligomers,” Journal of Organic Chemistry, vol. 62, no. 4, pp. 846–852, 1997. View at Google Scholar · View at Scopus
  21. N. N. Polushin, “The precursor strategy: terminus methoxyoxalamido modifiers for single and multiple functionalization of oligodeoxyribonucleotides,” Nucleic Acids Research, vol. 28, no. 16, pp. 3125–3133, 2000. View at Google Scholar · View at Scopus
  22. A. M. Morocho and N. N. Polushin, “Methoxyoxalamido chemistry in the synthesis of tethered phosphoramidites and functionalized oligonucleotides,” Current Protocols in Nucleic Acid Chemistry, vol. chapter 4, p. unit 4.29, 2006. View at Google Scholar · View at Scopus
  23. N. G. Beloglazova, N. N. Polushin, V. N. Sil'nikov, M. A. Zenkova, and V. V. Vlasov, “Site-specific cleavage of yeast tRNA(Phe) by derivatives of oligonucleotides bearing bisimidazole groups,” Doklady Akademii Nauk, vol. 369, no. 6, pp. 827–830, 1999. View at Google Scholar · View at Scopus
  24. N. G. Beloglazova, M. M. Fabani, M. A. Zenkova et al., “Sequence-specific artificial ribonucleases. I. Bis-imidazole-containing oligonucleotide conjugates prepared using precursor-based strategy,” Nucleic Acids Research, vol. 32, no. 13, pp. 3887–3897, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Nishikawa, H. Morioka, H. J. Kim et al., “Two histidine residues are essential for ribonuclease T1 activity as is the case for ribonuclease A,” Biochemistry, vol. 26, no. 26, pp. 8620–8624, 1987. View at Google Scholar · View at Scopus
  26. A. Wlodawer, M. Miller, and L. Sjölin, “Active site of RNase: neutron diffraction study of a complex with uridine vanadate, a transition-state analog,” Proceedings of the National Academy of Sciences of the United States of America, vol. 80, no. 12, pp. 3628–3631, 1983. View at Google Scholar · View at Scopus
  27. L. Vitagliano, A. Merlino, A. Zagari, and L. Mazzarella, “Productive and nonproductive binding to ribonuclease A: X-ray structure of two complexes with uridylyl(2',5')guanosine,” Protein Science, vol. 9, no. 6, pp. 1217–1225, 2000. View at Google Scholar · View at Scopus
  28. M. Komiyama and T. Inokawa, “Selective hydrolysis of tRNA by ethylenediamine bound to a DNA oligomer,” Journal of Biochemistry, vol. 116, no. 4, pp. 719–720, 1994. View at Google Scholar · View at Scopus
  29. R. Giegé, B. Felden, M. A. Zenkova, V. N. Sil'nikov, and V. V. Vlassov, “Cleavage of RNA with synthetic ribonuclease mimics,” Methods in Enzymology, vol. 318, pp. 147–165, 2000. View at Google Scholar · View at Scopus
  30. M. Zenkova, N. Beloglazova, V. Sil'nikov, V. Vlassov, and R. Giegë, “RNA cleavage by 1,4-diazabicyclo[2.2.2]octane-imidazole conjugates,” Methods in Enzymology, vol. 341, pp. 468–490, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. N. G. Beloglazova, V. N. Sil'Nikov, M. A. Zenkova, and V. V. Vlassov, “Cleavage of yeast tRNAPhe with complementary oligonucleotide conjugated to a small ribonuclease mimic,” Federation of European Biochemical Societies Letters, vol. 481, no. 3, pp. 277–280, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. N. V. Tamkovich, A. N. Zenkov, V. V. Vlasov, and M. A. Zenkova, “An RNA sequence determines the speed of its cleavage by artificial ribonucleases,” Russian Journal of Bioorganic Chemistry, vol. 36, no. 2, pp. 207–218, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. V. A. Petyuk, M. A. Zenkova, R. Giege, and V. V. Vlassov, “Hybridization of antisense oligonucleotides with the 3' part of tRNAPhe,” Federation of European Biochemical Societies Letters, vol. 444, no. 2-3, pp. 217–221, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. V. Petyuk, R. Serikov, V. Tolstikov et al., “Invasion of strongly binding oligonucleotides into tRNA structure,” Nucleosides, Nucleotides and Nucleic Acids, vol. 19, no. 7, pp. 1145–1158, 2000. View at Google Scholar · View at Scopus
  35. R. N. Serikov, V. A. Petyuk, V. V. Vlassov, and M. A. Zenkova, “Hybridization of antisense oligonucleotides with yeast tRNAPhe: factors determining the efficiency of interaction,” Russian Chemical Bulletin, vol. 51, no. 7, pp. 1156–1165, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. A. V. Vlasov, V. V. Vlasov, and R. Giege, “RNA hydrolysis catalyzed by imidazole as a reaction for studying the secondary structure of RNA and complexes of RNA with oligonucleotides,” Doklady Akademii Nauk, vol. 349, no. 3, pp. 411–413, 1996. View at Google Scholar · View at Scopus
  37. N. G. Beloglazova, A. Y. Epanchintsev, V. N. Sil'nikov, M. A. Zenkova, and V. V. Vlasov, “Highly effective site-selective cleavage of RNA by imidazoles-containing antisense oligonucleotide conjugates,” Molecular Biology, vol. 36, no. 4, pp. 731–739, 2002. View at Google Scholar
  38. Y. Kumazawa, T. Yokogawa, H. Tsurui, K. Miura, and K. Watanabe, “Effect of the higher-order structure of tRNAs on the stability of hybrids with oligodeoxyribonucleotides: separation of tRNA by an efficient solution hybridization,” Nucleic Acids Research, vol. 20, no. 9, pp. 2223–2232, 1992. View at Google Scholar · View at Scopus
  39. I. Zegers, D. Maes, M. H. Dao-Thi, F. Poortmans, R. Palmer, and L. Wyns, “The structures of RNase A complexed with 3'-CMP and d(CpA): active site conformation and conserved water molecules,” Protein Science, vol. 3, no. 12, pp. 2322–2339, 1994. View at Google Scholar · View at Scopus
  40. C. F. Aguilar, P. J. Thomas, D. S. Moss, A. Mills, and R. A. Palmer, “Novel non-productively bound ribonuclease inhibitor complexes—high resolution X-ray refinement studies on the binding of RNAse-A to cytidylyl-2',5'-guanosine (2',5'CpG) and deoxycytidylyl-3',5'-guanosine (3',5' dCpdG),” Biochimica et Biophysica Acta, vol. 1118, no. 1, pp. 6–20, 1991. View at Publisher · View at Google Scholar · View at Scopus
  41. C. F. Aguilar, P. J. Thomas, A. Mills, D. S. Moss, and R. A. Palmer, “Newly observed binding mode in pancreatic ribonuclease,” Journal of Molecular Biology, vol. 224, no. 1, pp. 265–267, 1992. View at Publisher · View at Google Scholar · View at Scopus
  42. J. C. Fontecilla-Camps, R. de Llorens, M. H. le Du, and C. M. Cuchillo, “Crystal structure of ribonuclease A·d(ApTpApApG) complex. Direct evidence for extended substrate recognition,” Journal of Biological Chemistry, vol. 269, no. 34, pp. 21526–21531, 1994. View at Google Scholar · View at Scopus
  43. D. L. Birdsall and A. McPherson, “Crystal structure of ribonuclease A·d(ApTpApApG) complex. Direct evidence for extended substrate recognition,” Journal of Biological Chemistry, vol. 267, no. 31, pp. 22230–22236, 1992. View at Google Scholar
  44. R. Kierzek, “Structural consideration concerning cleavage of RNA,” in Nucleic Acids and Molecular Biology: Artificial Nucleases, M. A. Zenkova, Ed., vol. 13, pp. 33–48, Springer, Berlin, Germany, 2004. View at Google Scholar
  45. I. Zagórowska, S. Kuusela, and H. Lönnberg, “Metal ion-dependent hydrolysis of RNA phosphodiester bonds within hairpin loops. A comparative kinetic study on chimeric ribo/2'-O-methylribo oligonucleotides,” Nucleic Acids Research, vol. 26, no. 14, pp. 3392–3396, 1998. View at Publisher · View at Google Scholar · View at Scopus
  46. I. Zagorowska, S. Mikkola, and H. Lönnberg, “Hydrolysis of phosphodiester bonds within RNA hairpin loops in buffer solutions: the effect of secondary structure on the inherent reactivity of RNA phosphodiester bonds,” Helvetica Chimica Acta, vol. 82, no. 12, pp. 2105–2111, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Mihkola, U. Kaukinen, and H. Lönnberg, “The effect of secondary structure on cleavage of the phosphodiester bonds of RNA,” Cell Biochemistry and Biophysics, vol. 34, no. 1, pp. 95–119, 2001. View at Publisher · View at Google Scholar
  48. U. Kaukinen, S. Lyytikäinen, S. Mikkola, and H. Lönnberg, “The reactivity of phosphodiester bonds within linear single-stranded oligoribonucleotides in strongly dependent on the base sequence,” Nucleic Acids Research, vol. 30, no. 2, pp. 468–474, 2002. View at Google Scholar · View at Scopus
  49. R. Häner, J. Hall, A. Pfützer, and D. Hüsken, “Development of artificial ribinucleases,” Pure and Applied Chemistry, vol. 70, no. 1, pp. 111–116, 1998. View at Google Scholar
  50. R. Serikov, V. Petyuk, Y. Vorobijev et al., “Mechanism of antisense oligonucleotide interaction with natural RNAs,” Journal of Biomolecular Structure and Dynamics, vol. 29, no. 1, pp. 27–50, 2011. View at Google Scholar