Differential stability of 2′F-ANA•RNA and ANA•RNA hybrid duplexes: Roles of structure, pseudohydrogen bonding, hydration, ion uptake and flexibility

Nucleic Acids Research

Volumn 38, Issue 7, 2010, Pages 2498-2511

  Watts, Jonathan K ^a,e   Martín Pintado, Nerea ^b   Gómez Pinto, Irene ^b   Schwartzentruber, Jeremy ^a   Portella, Guillem ^c,d   Orozco, Modesto ^c,d   González, Carlos ^b   Damha, Masad J ^a  

^a MCGILL UNIVERSITY   (Canada)

^b INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^c BARCELONA SUPERCOMPUTING CENTER   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2'FLUOROARABINONUCLEIC ACID; ARABINONUCLEIC ACID; DNA; HYDROGEN; NUCLEIC ACID; PSEUDOHYDROGEN; RNA; UNCLASSIFIED DRUG; ARABINONUCLEOTIDE; CATION; FLUORINE; WATER;

ARTICLE; BINDING AFFINITY; CHEMICAL BOND; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; GENETIC STABILITY; HYBRID GENE; HYBRIDIZATION; HYDRATION; ION TRANSPORT; NUCLEAR MAGNETIC RESONANCE; NUCLEIC ACID ANALYSIS; NUCLEIC ACID STRUCTURE; PRIORITY JOURNAL; STRUCTURE ANALYSIS; THEORETICAL STUDY; THERMODYNAMICS; THERMOSTABILITY; CHEMICAL STRUCTURE; CHEMISTRY; DNA DENATURATION; HYDROGEN BOND;

ARABINONUCLEOTIDES; CATIONS; FLUORINE; HYDROGEN BONDING; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID DENATURATION; RNA; THERMODYNAMICS; WATER;

EID: 77952302811     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1225     Document Type: Article

References (62)

1. Trempe, J.-F., Wilds, C.J., Denisov, A.Y., Pon, R.T., Damha, M.J. and Gehring, K. (2001) NMR solution structure of an oligonucleotide hairpin with a 2′F-ANA/RNA stem: implications for RNase H specificity toward DNA/RNA hybrid duplexes. J. Am. Chem. Soc., 123, 4896-4903.
2. Denisov, A.Y., Noronha, A.M., Wilds, C.J., Trempe, J.-F., Pon, R.T., Gehring, K. and Damha, M.J. (2001) Solution structure of an arabinonucleic acid (ANA)/RNA duplex in a chimeric hairpin: comparison with 2′-fluoro-ANA/RNA and DNA/RNA hybrids. Nucleic Acids Res., 29, 4284-4293.
3. Damha, M.J., Wilds, C.J., Noronha, A., Brukner, I., Borkow, G., Arion, D. and Parniak, M.A. (1998) Hybrids of RNA and arabinonucleic acids (ANA and 2′F-ANA) are substrates of Ribonuclease H. J. Am. Chem. Soc., 120, 12976-12977.
4. Noy, A., Perez, A., Marquez, M., Luque, F.J. and Orozco, M. (2005) Structure, recognition properties, and flexibility of the DNA-RNA hybrid. J. Am. Chem. Soc., 127, 4910-4920.
5. Noy, A., Luque, F.J. and Orozco, M. (2008) Theoretical analysis of antisense duplexes: determinants of the RNase H susceptibility. J. Am. Chem. Soc., 130, 3486-3496.
6. Wilds, C.J. Synthesis, Physicochemical and Biological Properties of Oligonucleotides Containing 2-fluoro-2-deoxy-β-D-arabinose. PhD Thesis, McGill University, 1999, Chapter 6.
7. Noronha, A.M., Wilds, C.J., Lok, C.-N., Viazovkina, K., Arion, D., Parniak, M.A. and Damha, M.J. (2000) Synthesis and biophysical properties of arabinonucleic acids (ANA): circular dichroic spectra, melting temperatures, and ribonuclease H susceptibility of ANA.RNA hybrid duplexes. Biochemistry, 39, 7050-7062.
8. Wilds, C.J. and Damha, M.J. (2000) 2′-Deoxy-2′-fluoro-b-D-arabinonucleosides and oligonucleotides (2′F-ANA): synthesis and physicochemical studies. Nucleic Acids Res., 28, 3625-3635.
9. Watts, J.K. and Damha, M.J. (2008) 2′F-Arabinonucleic acids (2′F-ANA) - History, properties, and new frontiers. Can. J. Chem., 86, 641-656.
10. Topigen Pharmaceuticals moves novel inhaled PDE inhibitor, TPI 1100, into clinical development for COPD. Press release (22 December 2008) available at http://www.topigen.com.
11. Venkateswarlu, D. and Ferguson, D.M. (1999) Effects of C2′-substitution on arabinonucleic acid structure and conformation. J. Am. Chem. Soc., 121, 5609-5610.
12. Li, F., Sarkhel, S., Wilds, C.J., Wawrzak, Z., Prakash, T.P., Manoharan, M. and Egli, M. (2006) 2′-fluoroarabino- and arabinonucleic acid show different conformations, resulting in deviating RNA affinities and processing of their heteroduplexes with RNA by RNase H. Biochemistry, 45, 4141-4152.
13. González, C., Stec, W., Reynolds, M.A. and James, T.L. (1995) Structure and dynamics of a DNA-RNA hybrid duplex with a chiral phosphorothioate moiety - NMR and molecular dynamics with conventional and time-averaged restraints. Biochemistry, 34, 4969-4982.
14. Marky, L.A. and Breslauer, K.J. (1987) Calculating thermodynamic data for transitions of any molecularity from equilibrium melting curves. Biopolymers, 26, 1601-1620.
15. Kaur, H., Arora, A., Wengel, J. and Maiti, S. (2006) Thermodynamic, counterion, and hydration effects for the incorporation of locked nucleic acid nucleotides into DNA duplexes. Biochemistry, 45, 7347-7355.
16. Rozners, E. and Moulder, J. (2004) Hydration of short DNA, RNA and 2′-OMe oligonucleotides determined by osmotic stressing. Nucleic Acids Res., 32, 248-254.
17. Piotto, M., Saudek, V. and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR, 2, 661-665.
18. 1H resonances in oligonucleotides by two-dimensional NMR spectroscopy. FEBS Lett., 208, 94-98.
19. Yu, C. and Levy, G.C. (2002) Two-dimensional heteronuclear NOE (HOESY) experiments: investigation of dipolar interactions between heteronuclei and nearby protons. J. Am. Chem. Soc., 106, 6533-6537.
20. Goddard, D.T. and Kneller, G. SPARKY 3. University of California, San Francisco.
21. Borgias, B.A. and James, T.L. (1990) MARDIGRAS, a pratrix analysis of relaxation for discerning geometry of an aqueous structure. J. Magn. Reson., 87, 475-487.
22. Case, D.A., Pearlman, D.A., Caldwell, J.W., III, T.E.C., Ross, W.S., Simmerling, C.L., Darden, T.A., Merz, K.M., Stanton, R.V., Cheng, A.L. et al. (1997) AMBER 5. University of California, San Francisco.
23. Soliva, R., Monaco, V., Gómez-Pinto, I., Meeuwenoord, N.J., Marel, G.A., Boom, J.H., González, C. and Orozco, M. (2001) Solution structure of a DNA duplex with a chiral alkyl phosphonate moiety. Nucleic Acids Res., 29, 2973-2985.
24. Darden, T.E., York, D. and Pedersen, L. (1993) Particle mesh Ewald: an N.log(N) method for Ewald sums in large systems. J. Chem. Phys., 98, 10089-10092.
25. Pérez, A., Marchán, I., Svozil, D., Sponer, J., Cheatham, T., Laughton, C. and Orozco, M. (2007) Refinement of the AMBER force field for nucleic acids: improving the description of alpha/gamma conformers. Biophys. J., 92, 3817-3829.
26. Cheatham, T.E., Cieplak, P. and Kollman, P.A. (1999) A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J. Biomol. Struct. Dyn., 16, 845-862.
27. nd generation force field for the simulation of proteins, nucleic acids and organic molecules. J. Am. Chem. Soc., 117, 5179-5197.
28. Jorgensen, W.L., Chandrasekhar, J. and Madura, J.D. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935.
29. Shields, G.C., Laughton, C.A. and Orozco, M. (1997) Molecular dynamics simulations of the d(T.A.T) triple helix. J. Am. Chem. Soc., 119, 7463-7469.
30. Hess, B., Kutzner, C., Van der Spoel, D. and Lindhal, E. (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput., 4, 435-447.
31. Miyamoto, S. and Kollman, P.A. (1992) SETTLE: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comp Chem, 13, 952-962.
32. Hess, B. (2008) P-LINCS: a parallel linear constraint solver for molecular simulation. J. Chem. Theory Comput., 4, 116-122.
33. Bussi, G., Donadio, D. and Parrinello, M. (2007) Canonical sampling through velocity rescaling. J. Chem. Phys., 126, 014101.
34. Berendsen, H.J.C. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys., 81, 3684-3690.
35. Lavery, R. and Sklenar, H. (1990) CURVES, helical analysis of irregular nucleic acids. 3.0. Laboratory of Theoretical Biochemistry CNRS, Paris.
36. Koradi, R., Billeter, M. and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph., 14, 29-32, 51-55.
37. Orozco, M. and Luque, F.J. (2000) Theoretical methods for the description of the solvent effect in biomolecular systems. Chem. Rev., 100, 4187-4226.
38. González, C., Stec, W., Kobylanska, A., Hogrefe, R.I., Reynolds, M. and James, T.L. (1994) Structural study of a DNA-RNA hybrid duplex with a chiral phosphorothioate moiety by NMR -extraction of distance and torsion angle constraints and imino proton-exchange rates. Biochemistry, 33, 11062-11072.
39. Fenna, C.P., Wilkinson, V.J., Arnold, J.R., Cosstick, R. and Fisher, J. (2008) The effect of 2′-fluorine substitutions on DNA i-motif conformation and stability. Chem. Commun., 3567-3569.
40. Spink, C.H. and Chaires, J.B. (1999) Effects of hydration, ion release, and excluded volume on the melting of triplex and duplex DNA. Biochemistry, 38, 496-508.
41. 2O - isotopic effects on critical temperatures and transition widths. Nucleic Acids Res., 8, 4283-4303.
42. McFail-Isom, L., Sines, C.C. and Williams, L.D. (1999) DNA structure: cations in charge? Curr. Opin. Struct. Biol., 9, 298-304.
43. Tereshko, V., Minasov, G. and Egli, M. (1999) A "hydrat-ion" spine in a B-DNA minor groove. J. Am. Chem. Soc., 121, 3590-3595.
44. Brady, G.P. and Sharp, K.A. (1995) Decomposition of interaction free energies in proteins and other complex systems. J. Mol. Biol., 254, 77-85.
45. Boresch, S. and Karplus, M. (1995) The meaning of component analysis: decomposition of the free energy in terms of specific interactions. J. Mol. Biol., 254, 801-807.
46. Mark, A.E. and van Gunsteren, W.F. (1994) Decomposition of the free energy of a system in terms of specific interactions. Implications for theoretical and experimental studies. J. Mol. Biol., 240, 167-176.
47. Gao, Y.G., Van der Marel, G.A., Van Boom, J.H. and Wang, A.H.J. (1991) Molecular structure of a DNA decamer containing an anticancer nucleoside arabinosylcytosine: conformational perturbation by arabinosylcytosine in B-DNA. Biochemistry, 30, 9922-9931.
48. Berger, I., Tereshko, V., Ikeda, H., Marquez, V.E. and Egli, M. (1998) Crystal structures of B-DNA with incorporated 2′-deoxy-2′-fluoro-arabino-furanosyl thymines: implications of conformational preorganization for duplex stability. Nucleic Acids Res., 26, 2473-2480.
49. Tennila, T., Azhayeva, E., Vepsalainen, J., Laatikainen, R., Azhayev, A. and Mikhailopulo, I.A. (2000) Oligonucleotides containing 9-(2-deoxy-2-fluoro-b-D-arabinofuranosyl)-adenine and -guanine: synthesis, hybridization and antisense properties. Nucleosides Nucleotides Nucleic Acids, 19, 1861-1884.
50. Wright, J.A., Taylor, N.F. and Fox, J.J. (1969) Nucleosides. LX. Fluorocarbohydrates. Synthesis of 2-deoxy-2-fluoro-D-arabinose and 9-(2-deoxy-2-fluoro-α and β-D-arabinofuranosyl)adenines. J. Org. Chem., 34, 2632-2636.
51. Barchi, J.J. Jr, Marquez, V.E., Driscoll, J.S., Ford, H. Jr, Mitsuya, H., Shirasaka, T., Aoki, S. and Kelley, J.A. (1991) Potential anti-AIDS drugs. Lipophilic, adenosine deaminase-activated prodrugs. J. Med. Chem., 34, 1647-1655.
52. Herdewijn, P., Van Aerschot, A. and Kerremans, L. (1989) Synthesis of nucleosides fluorinated in the sugar moiety. The application of diethylaminosulfur trifluoride to the synthesis of fluorinated nucleosides. Nucleosides Nucleotides, 8, 65-96.
53. Bergstrom, D.E., Swartling, D.J., Wisor, A. and Hoffmann, M.R. (1991) Evaluation of thymidine, dideoxythymidine and fluorine substituted deoxyribonucleoside geometry by the Mindo/3 technique: the effect of fluorine substitution on nucleoside geometry and biological activity. Nucleosides Nucleotides, 10, 693-697.
54. Pallan, P.S. and Egli, M. (2009) Pairing geometry of the hydrophobic thymine analogue 2, 4-difluorotoluene in duplex DNA as analyzed by X-ray crystallography. J. Am. Chem. Soc., 131, 12548-12549.
55. Parsch, J. and Engels, J.W. (2002) C-F. H-C hydrogen bonds in ribonucleic acids. J. Am. Chem. Soc., 124, 5664-5672.
56. Sun, Z. and McLaughlin, L.W. (2007) Probing the nature of three-centered hydrogen bonds in minor-groove ligand-DNA interactions: the contribution of fluorine hydrogen bonds to complex stability. J. Am. Chem. Soc., 129, 12531-12536.
57. Mrevlishvili, G.M., Carvalho, A.P.S.M.C., da Silva, M.A.V.R., Mdzinarashvili, T.D., Razmadze, G.Z. and Tarielashvili, T.Z. (2001) The role of bound water on the energetics of DNA duplex melting. J. Therm. Anal. Calorim., 66, 133-144.
58. Egli, M., Portmann, S. and Usman, N. (1996) RNA hydration: a detailed look. Biochemistry, 35, 8489-8494.
59. Freier, S.M. and Altmann, 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.
60. Egli, M., Minasov, G., Tereshko, V., Pallan, P.S., Teplova, M., Inamati, G.B., Lesnik, E.A., Owens, S.R., Ross, B.S., Prakash, T.P. et al. (2005) Probing the influence of stereoelectronic effects on the biophysical properties of oligonucleotides: comprehensive analysis of the RNA affinity, nuclease resistance, and crystal structure of ten 2′-O-ribonucleic acid modifications. Biochemistry, 44, 9045-9057.
61. Kolarovic, A., Schweizer, E., Greene, E., Gironda, M., Pallan, P.S., Egli, M. and Rozners, E. (2009) interplay of structure, hydration and thermal stability in formacetal modified oligonucleotides: RNA may tolerate nonionic modifications better than DNA. J. Am. Chem. Soc., 131, 14932-14937.
62. Schlegel, M.K., Xie, X., Zhang, L. and Meggers, E. (2009) Insight into the high duplex stability of the simplified nucleic acid GNA. Angew. Chem. Int. Ed., 48, 960-963.