Thermodynamics of RNA duplexes modified with unlocked nucleic acid nucleotides

Nucleic Acids Research

Volumn 38, Issue 19, 2010, Pages 6697-6706

  Pasternak, Anna ^a   Wengel, Jesper ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE; RNA; UNCLASSIFIED DRUG; UNLOCKED NUCLEIC ACID NUCLEOTIDE;

ARTICLE; BASE MISPAIRING; CIRCULAR DICHROISM; MOLECULAR INTERACTION; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; RNA STRUCTURE; THERMODYNAMICS; ULTRAVIOLET RADIATION;

BASE PAIR MISMATCH; CIRCULAR DICHROISM; NUCLEOTIDES; RNA, DOUBLE-STRANDED; THERMODYNAMICS;

EID: 78049354836     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq561     Document Type: Article

References (57)

1. Micklefield, J. (2001) Backbone modification of nucleic acids: synthesis, structure and therapeutic applications. Curr. Med. Chem., 8, 1157-1179.
2. Doktycz, M.J. (1997) Nucleic acids: thermal stability and denaturation. Encyclopedia of Life Science. John Wiley & Sons, Chichester, pp. 3123-3140.
3. Turner, D.H., Sugimoto, N., Kierzek, R. and Dreiker, S.D. (1987) Free energy increments for hydrogen-bonds in nucleic acid base pairs. J. Am. Chem. Soc., 109, 3783-3785.
4. Kool, E.T. (2001) Hydrogen bonding, base stacking, and steric effects in DNA replication. Annu. Rev. Biophys. Biomol. Stuct., 30, 1-22.
5. Freier, S.M. and Altman, K.-H. (1997) The ups and downs of nucleic acid duplex stability: structure-stability studies on chemically-modified DNA: RNA duplexes. Nucleic Acids Res., 25, 4429-4443.
6. Ørum, H. and Wengel, J. (2001) Locked nucleic acids: a promising molecular family for gene-function analysis and antisense drug development. Curr. Opin. Mol. Ther., 3, 239-243.
7. Wengel, J. (2004) Nucleic acid nanotechnology-towards Ångstrom-scale engineering. Org. Biomol. Chem., 2, 277-280.
8. Kurreck, J. (2003) Antisense technologies. Improvement through novel chemical modifications. Eur. J. Biochem., 270, 1628-1644.
9. Masayuki, E. and Hiroshi, S. (2009) Chemical approaches to DNA nanotechnology. ChemBiochem., 10, 2420-2443.
10. Prakash, T.P. and Bhat, B. (2007) 2'-Modified oligonucleotides for antisense therapeutics. Curr. Top. Med. Chem., 7, 641-649.
11. Rayburn, E.R. and Zhang, R. (2008) Antisense, RNAi, and gene silencing strategies for therapy: mission possible or impossible? Drug Discov. Today, 13, 513-521.
12. Takahashi, M., Minakawa, N. and Matsuda, A. (2009) Synthesis and characterization of 20-modified-40-thioRNA: a comprehensive comparison of nuclease stability. Nucleic Acids Res., 37, 1353-1362.
13. Agrawal, S. and Iyer, R.P. (1995) Modified oligonucleotides as therapeutic and diagnostic agents. Curr. Opin. Biotechnol., 6, 12-19.
14. Vandendriessche, F., Augustyns, K., Van Aerschot, A., Busson, R., Hoogmartens, J. and Herdewijn, P. (1993) Acyclic oligonucleotides: possibilities and limitations. Tetrahedron, 49, 7223-7238.
15. Petersen, A.B., Petersen, M.Å., Henriksen, U., Hammerum, S. and Dahl, O. (2003) Acyclic, achiral enamide nucleoside analogues. The importance of the C=C bond in the analogue for its ability to mimic natural nucleosides. Org. Biomol. Chem., 1, 3293-3296.
16. Benhida, R., Devys, M., Fourrey, J.-L., Lecubin, F. and Sun, J.-S. (1998) Incorporation of serinol derived acyclic nucleoside analogues into oligonucleotides: influence on duplex and triplex formation. Tetrahedron Lett., 39, 6167-6170.
17. Nielsen, P., Dreiøe, L.H. and Wengel, J. (1995) Synthesis and evaluation of oligodeoxynucleotides containing acyclic nucleosides: introduction of three novel analogues and a summary. Bioorg. Med. Chem. Lett., 3, 19-28.
18. Augustyns, K., Van Aerschot, A., Van Schepdael, A., Urbanke, C. and Herdewijn, P. (1991) Influence of the incorporation of (S)-9-(3, 4-dihydroxybutyl) adenine on the enzymatic stability and base-pairing properties of oligodeoxynucleotides. Nucleic Acids Res., 19, 2587-2593.
19. Langkjær, N., Pasternak, A. and Wengel, J. (2009) UNA (unlocked nucleic acid): a flexible RNA mimic that allows engineering of nucleic acid duplex stability. Bioorg. Med. Chem., 17, 5420-5425.
20. Jensen, T.B., Langkjær, N. and Wengel, J. (2008) Unlocked nucleic acid (UNA) and UNA derivatives: thermal denaturation studies. Nucleic Acids Symp. Ser., 52, 133-134.
21. Mangos, M.M., Min, K.-L., Viazovkina, E., Galarneau, A., Elzagheid, M.I., Parniak, M.A. and Damha, M.J. (2002) Efficient RNase H-directed cleavage of RNA promoted by antisense DNA or 20F-ANA constructs containing acyclic nucleotide inserts. J. Am. Chem. Soc., 125, 654-661.
22. Fluiter, K., Mook, O.R.F., Vreijling, J., Langkjær, N., Højland, T., Wengel, J. and Baas, F. (2009) Filling the gap in LNA antisense oligo gapmers: the effects of unlocked nucleic acid (UNA) and 4'-C-hydroxymethyl-DNA modifications on RNase H recruitment and efficacy of an LNA gapmer. Mol. Biosyst., 5, 838-843.
23. Bramsen, J.B., Laursen, M.B., Nielsen, A.F., Hansen, T.B., Bus, C., Langkjær, N., Babu, B.R., Højland, T., Abramov, M., Van Aerschot, A. et al. (2009) A large-scale chemical modification screen identifies design rules to generate siRNAs with high activity, high stability and low toxicity. Nucleic Acids Res., 37, 2867-2881.
24. Kenski, D.M., Cooper, A.J., Li, J.J., Willingham, A.T., Haringsma, H.J., Young, T.A., Kuklin, N.A., Jones, J.J., Cancilla, M.T., McMasters, D.R. et al. (2010) Analysis of acyclic nucleoside modifications in siRNAs finds sensitivity at position 1 that is restored by 50-terminal phosphorylation both in vitro and in vivo. Nucleic Acids Res., 38, 660-671.
25. Bramsen, J.B., Pakula, M.M., Hansen, T.B., Bus, C., Langkjær, N., Odadzic, D., Smicius, R., Wengel, S.L., Chattopadhyaya, J., Engels, J.W. et al. (2010) A screen of chemical modifications identifies position-specific modification by UNA to most potently reduce siRNA off-target effects. Nucleic Acids Res. [Epub ahead of print].
26. Borer, P.N. (1975) Optical properties of nucleic acids, absorption and circular dichroism spectra. In Fasman, G.D. (ed.), CRC Handbook of Biochemistry and Molecular Biology: Nucleic Acids, Vol. 1, 3rd edn. CRC Press, Cleveland, OH, pp. 589-595.
27. Richards, E.G. (1975) Use of tables in calculations of absorption, optical rotatory dispersion and circular dichroism of polyribonucleotides. In Fasman, G.D. (ed.), CRC Handbook of Biochemistry and Molecular Biology: Nucleic Acids, Vol. 1, 3rd edn. CRC Press, Cleveland, OH, pp. 596-603.
28. 2 by two-dimensional NMR and simulated annealing. Biochemistry, 35, 14077-14089.
29. SantaLucia, J.J. (2000) The use of spectroscopic techniques in the study of DNA stability. In Gore, M.G. (ed.), Spectrophotometry and spectrofluorimetry a practical approach, Vol. 13. Oxford University Press Inc., New York, pp. 329-359.
30. Rodger, A. and Nordén, B. (1997) Circular Dichroism of Biomolecules. Oxford University Press Inc., New York.
31. SantaLucia, J. (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc. Natl Acad. Sci. USA, 95, 1460-1465.
32. Borer, P.N., Dengler, B., Tinoco, I. and Uhlenbeck, O.C. (1974) Stability of ribonucleic-acid double-stranded helices. J. Mol. Biol., 86, 843-853.
33. Gray, D.M. (1997) Derivation of nearest-neighbor properties from data on nucleic acid oligomers. I. Simple sets of independent sequences and the influence of absent nearest neighbors. Biopolymers, 42, 783-793.
34. Gray, D.M. (1997) Derivation of nearest-neighbor properties from data on nucleic acid oligomers. II. Thermodynamic parameters of DNA·RNA hybrids and DNA duplexes. Biopolymers, 42, 795-810.
35. Xia, T.B., SantaLucia, J., Burkard, M.E., Kierzek, R., Schroeder, S.J., Jiao, X.Q., Cox, C. and Turner, D.H. (1998) Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick base pairs. Biochemistry, 37, 14719-14735.
36. Kierzek, E., Mathews, D.H., Ciesielska, A., Turner, D.H. and Kierzek, R. (2006) Nearest neighbor parameters for Watson-Crick complementary heteroduplexes formed between 2'-O-methyl RNA and RNA oligonucleotides. Nucleic Acids Res., 34, 3609-3614.
37. SantaLucia, J.J., Allawi, H.T. and Seneviratne, P.A. (1996) Improved nearest-neighbor parameters for predicting DNA duplex stability. Biochemistry, 35, 3555-3562.
38. Sugimoto, N., Honda, K.-i. and Sasaki, M. (1994) Application of the thermodynamic parameters of DNA stability prediction to double-helix formation of deoxyribooligonucleotides. Nucleosides Nucleotides, 13, 1311-1317.
39. Sugimoto, N., Nakano, S., Yoneyama, M. and Honda, K. (1996) Improved thermodynamic parameters and helix initiation factor to predict stability of DNA duplexes. Nucleic Acids Res., 24, 4501-4505.
40. Sugimoto, N., Nakano, S., Katoh, M., Matsumura, A., Nakamuta, H., Ohmici, T., Yoneyama, M. and Sasaki, M. (1995) Thermodynamic parameters to predict stability of RNA/DNA hybrid duplexes. Biochemistry, 34, 11211-11216.
41. McTigue, P.M., Peterson, R.J. and Kahn, J.D. (2004) Sequence-dependent thermodynamic parameters for locked nucleic acid (LNA)-DNA duplex formation. Biochemistry, 43, 5388-5405.
42. Pasternak, A., Kierzek, E., Pasternak, K., Turner, D.H. and Kierzek, R. (2007) A chemical synthesis of LNA-2, 6-diaminopurine riboside, and the influence of 2'-O-methyl-2, 6-diaminopurine and LNA-2, 6-diaminopurine ribosides on the thermodynamic properties of 2'-O-methyl RNA/RNA heteroduplexes. Nucleic Acids Res., 35, 4055-4063.
43. Owczarzy, R., Vallone, P.M., Gallo, F.J., Paner, T.M., Lane, M.J. and Benight, A.S. (1997) Predicting sequence-dependent melting stability of short duplex DNA oligomers. Biopolymers, 44, 217-239.
44. Werk, D., Wengel, J., Wengel, S.L., Grunert, H.-P., Zeichhardt, H. and Kurreck, J. (2010) Application of small interfering RNAs modified by unlocked nucleic acid (UNA) to inhibit the heart-pathogenic coxsackievirus B3. FEBS Lett., 584, 591-598.
45. Guckian, K.M., Schweitzer, B.A., Ren, R.X.-F., Sheils, C.J., Tahmassebi, D.C. and Kool, E.T. (2000) Factors contributing to aromatic stacking in water: evaluation in the context of DNA. J. Am. Chem. Soc., 122, 2213-2222.
46. Turner, D.H., Sugimoto, N. and Freier, S.M. (1988) RNA structure prediction. Annu. Rev. Biophys. Biophys. Chem., 17, 167-192.
47. Chen, G., Kierzek, R., Yildirim, I., Krugh, T.R., Turner, D.H. and Kennedy, S.D. (2007) Stacking effects on local structure in RNA: changes in the structure of tandem GA pairs when flanking GC pairs are replaced by isoG-isoC pairs. J. Phys. Chem. B, 111, 6718-6727.
48. Ziomek, K., Kierzek, E., Biala, E. and Kierzek, R. (2002) The thermal stability of RNA duplexes containing modified base pairs placed at internal and terminal positions of the oligoribonucleotides. Biophys. Chem., 97, 233-241.
49. 6-alkyladenosines. Nucleic Acids Res., 31, 4472-4480.
50. Davis, A.R. and Znosko, B.M. (2007) Thermodynamic characterization of single mismatches found in naturally occurring RNA. Biochemistry, 46, 13425-13436.
51. Kierzek, R., Burkard, M.E. and Turner, D.H. (1999) Thermodynamics of single mismatches in RNA duplexes. Biochemistry, 38, 14214-14223.
52. Kierzek, E., Ciesielska, A., Pasternak, K., Mathews, D.H., Turner, D.H. and Kierzek, R. (2005) The influence of locked nucleic acid residues on the thermodynamic properties of 2'-O-methyl RNA/RNA heteroduplexes. Nucleic Acids Res., 33, 5082-5093.
53. Vanhommerig, S.A.M., van Genderen, M.H.P. and Buck, H.M. (1991) A stable antiparallel cytosine-thymine base pair occurring only at the end of a duplex. Biopolymers, 31, 1087-1094.
54. Schroeder, S.J. and Turner, D.H. (2000) Factors affecting the thermodynamic stability of small asymmetric internal loops in RNA. Biochemistry, 39, 9257-9274.
55. Liu, J.D., Zhao, L. and Xia, T. (2008) The dynamic structural basis of differential enhancement of conformational stability by 5'- and 3'-dangling ends in RNA. Biochemistry, 47, 5962-5975.
56. Clanton-Arrowood, K., McGurk, J. and Schroeder, S.J. (2008) 3'-Terminal nucleotides determine thermodynamic stabilities of mismatches at the ends of RNA helices. Biochemistry, 47, 13418-13427.
57. Kierzek, E., Pasternak, A., Pasternak, K., Gdaniec, Z., Yildirim, I., Turner, D.H. and Kierzek, R. (2009) Contributions of stacking, preorganization, and hydrogen bonding to the thermodynamic stability of duplexes between RNA and 2'-O-methyl RNA with locked nucleic acids. Biochemistry, 48, 4377-4387.