Stabilizing contributions of sulfur-modified nucleotides: Crystal structure of a DNA duplex with 2′-O-[2-(methoxy)ethyl]-2-thiothymidines

Nucleic Acids Research

Volumn 33, Issue 16, 2005, Pages 5297-5307

  Diop Frimpong, Benjamin ^d   Prakash, Thazha P ^a   Rajeev, Kallanthottathil G ^b   Manoharan, Muthiah ^b   Egli, Martin ^c  

^a ISIS PHARMACEUTICALS   (United States)

^b ALNYLAM PHARMACEUTICALS   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 DEOXYRIBOSE; 2' O [2 (METHOXY)ETHYL] 2 THIOTHYMIDINE DERIVATIVE; ADENINE; ANTISENSE OLIGONUCLEOTIDE; COMPLEMENTARY RNA; DOUBLE STRANDED DNA; GUANINE; NUCLEASE; OXYGEN; PHOSPHOROTHIOIC ACID DERIVATIVE; RIBOSE; RNA; SMALL INTERFERING RNA; SULFUR; THIOURIDINE; THYMIDINE DERIVATIVE; TRANSFER RNA; UNCLASSIFIED DRUG; DNA; DRUG DERIVATIVE; NUCLEOTIDE; THYMIDINE;

ARTICLE; BINDING AFFINITY; CODON; CRYSTAL STRUCTURE; DNA CONFORMATION; DNA MODIFICATION; DNA SEQUENCE; DRUG STRUCTURE; DRUG SYNTHESIS; DRUG TARGETING; ENZYME DEGRADATION; ENZYME SPECIFICITY; GENE INTERACTION; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; RNA INTERFERENCE; RNA STABILITY; STRUCTURE ANALYSIS; THERMODYNAMICS; BASE PAIRING; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; X RAY CRYSTALLOGRAPHY;

BASE PAIRING; CRYSTALLOGRAPHY, X-RAY; DNA; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; OLIGORIBONUCLEOTIDES, ANTISENSE; SULFUR; THIONUCLEOTIDES; THYMIDINE;

EID: 24944511501     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gki823     Document Type: Article

References (49)

1. Crooke,S.T. (1998) Basic principles of antisense therapeutics. In Crooke,S.T. (ed.), Antisense Research and Application, Vol. 131, Springer, Berlin, pp. 1-50.
2. Manoharan,M. (1999) 2′-Carbohydrate modifications in antisense oligonucleotide therapy: Importance of conformation, configuration and conjugation. Biochim. Biophys. Acta., 1489, 117-130.
3. Manoharan,M. (2004) RNA interference and chemically modified small interfering RNAs. Curr. Opin. Chem. Biol., 8, 570-579.
4. Soutschek,J., Akinc,A., Bramlage,B., Charisse,K., Constien,R., Donoghue,M., Elbashir,S., Geick,A., Hadwiger,P., Harborth,J. et al. (2004) Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature, 432, 173-178.
5. Egli,M. (1998) Towards the structure-based design of nucleic acid therapeutics. In Weber,G. (ed.), Advan. Enzyme Regul. Vol. 38, Elsevier Science Ltd., Oxford, UK, pp. 181-203.
6. Levin,A.A. (1999) A review of issues in the pharmacokinetics and toxicology of phosphorothioate antisense oligonucleotides. Biochim. Biophys. Acta., 1489, 69-84.
7. Filmore,D. (2004) Assessing antisense. Modern Drug Discovery June, 49-50.
8. Crooke,S.T. (1995) Phosphorothioate oligonucleotides. In Crooke,S.T. (ed.), Therapeutic Applications of Oligonucleotides. R. G. Landes, Austin, pp. 63-79.
9. Kumar,R.K. and Davis,D.R. (1997) Synthesis and studies on the effect of 2-thiouridine and 4-thiouridine on sugar conformation and RNA duplex stability. Nucleic Acids Res., 25, 1272-1280.
10. Shohda,K., Okamoto,I., Wada,T., Seio,K. and Sekine,M. (2000) Synthesis and properties of 2′-O-methyl-2-thiouridine and oligoribonucleotides containing 2′-O-methyl-2-thiouridine. Bioorg. Med. Chem. Lett., 10, 1795-1798.
11. Rajeev,K.G., Prakash,T.P. and Manoharan,M. (2003) 2′-Modified-2-thiothymidine oligonucleotides. Org. Lett., 5, 3005-3008.
12. Grosjean,H. and Benne,R. (eds) (1998) Modification and Editing of RNA. ASM Press, Washington, DC.
13. Rozenski,J., Crain,P.F. and McCloskey,J.A. (1999) The RNA modification database: 1999 update. Nucleic Acids Res., 27, 196-197.
14. Agris,P. (2004) Decoding the genome: A modified view. Nucleic Acids Res., 32, 223-238.
15. Testa,S.M., Disney,M.D., Turner,D.H. and Kierzek,R. (1999) Thermodynamics of RNA-RNA duplexes with 2- or 4-thiouridines: implications for antisense design and targeting of a group I intron. Biochemistry, 38, 16655-16662.
16. Yokoyama,S., Watanabe,T., Murao,K., Ishikura,H., Yamaizumi,Z., Nishimura,S. and Miyazawa,T. (1985) Molecular mechanism of codon recognition by tRNA species with modified uridine in the first position of the anticodon. Proc. Natl Acad. Sci. USA, 82, 4905-4909.
17. Sierzputowska-Gracz,H., Sochaka,E., Malkiewicz,A., Kuo,K., Gehrke,C.W. and Agris,P.F. (1987) Chemistry and structure of modified uridines in the anticodon, wobble position of transter RNA are determined by thiolation. J. Am. Chem. Soc., 109, 7171-7177.
18. Agris,P.F., Sierzputowska-Gracz,H., Smith,W., Malkiewicz,A., Sochacka,E. and Nawrot,B. (1992) Thiolation of uridine carbon-2 restricts the motional dynamics of the transfer RNA wobble position nucleoside. J. Am. Chem. Soc., 114, 2652-2656.
19. Smith,W.S., Sierzputowska-Gracz,H., Sochacka,E., Malkiewicz,A. and Agris,P. (1992) Chemistry and structure of modified uridine dinucleosides are determined by thiolation. J. Am. Chem. Soc., 114, 7989-7997.
20. Tereshko,V., Portmann,S., Tay,E.C., Martin,P., Natt,F., Altmann,K.-H. and Egli,M. (1998) Correlating structure and stability of DNA duplexes with incorporated 2′-O-modified RNA analogues. Biochemistry, 37, 10626-10634.
21. De Mesmaeker,A., Häner,R., Martin,P. and Moser,H.E. (1995) Antisense oligonucleotides. Acc. Chem. Res., 28, 366-374.
22. Martin,P. (1995) New access to 2′-O-alkylated ribonucleosides and properties of 2′-O-alkylated oligoribonucleotides. Helv. Chim. Acta., 78, 486-504.
23. Teplova,M., Minasov,G., Tereshko,V., Inamati,G.B., Cook,P.D., Manoharan,M. and Egli,M. (1999) Crystal structure and improved antisense properties of 2′-O-(2-methoxyethyl)-RNA. Nature Struct. Biol., 6, 535-539.
24. Berger,I., Kang,C.H., Sinha,N., Wolters,M. and Rich,A. (1996) A highly efficient 24-condition matrix for the crystallization of nucleic acid fragments. Acta Cryst. 6, 52, 465-468.
25. Kabsch,W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Cryst., 26, 795-800.
26. Navaza,J. (1997) AMoRe: An automated molecular replacement program package. Meth. Enzymol., 276, 581-594.
27. CCP4. (1994), Collaborative computing project number 4. The CCP4 suite: programs for protein crystallography. Arta Cryst. D, 50, 760-763.
28. Egli,M., Tereshko,V., Teplova,M., Minasov,G., Joachimiak,A., Sanishvili,R., Weeks,C.M., Miller,R., Maier,M.A., An,H., Cook,P.D. and Manoharan,M. (2000) X-ray crystallographic analysis of the hydration of A- and B-form DNA at atomic resolution. Biopolymers (Nucleic Acid Sciences), 48, 234-252.
29. Brünger,A.T., Adams,P.D., Clore,G.M., DeLano,W.L., Gros,P., Grosse-Kunstleve,R.W., Jiang,J.S., Kuszewski,J., Nilges,M., Pannu,N.S., Read,R.J., Rice,L.M., Simonson,T. and Warren,G.L. (1998) Crystallography & NMR System: A new software suite for macromolecular structure determination. Acta Cryst. D, 54, 905-921.
30. Brünger,A.T. (1992) Free R value: A novel statistical quantity for assessing the accuracy of crystal structures. Nature, 355, 472-475.
31. Murshudov,G.N., Vagin,A.A. and Dodson,E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta. Cryst. D, 53, 240-255.
32. Murshudov,G.N., Vagin,A.A., Lebedev,A., Wilson,K.S. and Dodson,E.J. (1999) Efficient anisotropic refinement of macromolecular structures using FFT. Acta Cryst. D, 55, 247-255.
33. Winn,M.D., Isupov,M.N. and Murshudiv,G.N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta. Cryst. D, 57, 122-133.
34. Egli,M., Usman,N. and Rich,A. (1993) Conformational influence of the ribose 2′-hydroxyl group: Crystal structures of DNA-RNA chimeric duplexes. Biochemistry, 32, 3221-3237.
35. Tereshko,V., Wilds,C.J., Minasov,G., Prakash,T.P., Maier,M.A., Howard,A., Wawrzak,Z., Manoharan,M. and Egli,M. (2001) Detection of alkali metal ions in DNA crystals using state-of-the-art X-ray diffraction experiments. Nucleic Acids Res., 29, 1208-1215.
36. Lu,X-J., Shakked,Z. and Olson,W.K. (2000) A-DNA conformational motifs in ligand-bound double helices. J. Mol. Biol., 300, 819-840.
37. 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. and Manoharan,M. (2005) Probing the influence of stereoelectronic effects on the biophysical properties of oligonucleotides: Comprehensive analysis of the RNA affinity, nuclease resistance and crystal structure often 2′-O-ribonucleic acid modifications. Biochemistry, 44, 9045-9057.
38. Lagoja,I.M. (2005) Pyrimidine as a constituent of naturally biologically active compounds. Chemistry & Biodiversity, 2, 1-50.
39. Pattanayek,R., Sethaphong,L., Pan,C., Prhavc,M., Prakash,T.P., Manoharan,M. and Egli,M. (2004) Structural rationalization of a large difference in RNA affinity despite a small difference in chemistry between two 2′-O-modified nucleic acid analogs. J. Am. Chem. Soc., 126, 15006-15007.
40. Thibaudeau,C. and Chattopadhyaya,J. (1999) Stereoelectronic Effects in Nucleosides and Nucleotides and their Structural Implications. Uppsala University Press, Uppsala, Sweden.
41. Vakonakis,I. and LiWang,A.C. (2004) N1⋯N3 hydrogen bonds of A:U base pairs of RNA are stronger than those of A:T base pairs of DNA. J. Am. Chem. Soc., 126, 5688-5689.
42. Prakash,T.P., Manoharan,M., Fraser,A.S., Kawasaki,A.M., Lesnik,E., Sioufi,N., Leeds,J.M., Teplova,M. and Egli,M. (2002) 2′-O-[2-(Methylthio)ethyl]-modified oligonucleotide: An analog of 2′-O-[2-(methoxy)ethyl]-modified oligonucleotide with improved protein binding properties and high binding affinity to target RNA. Biochemistry, 41, 11642-11648.
43. Prhavc,M., Prakash,T.P., Minasov,G., Egli,M. and Manoharan,M. (2003) 2′-O-{2-[2-(N,N-Dimethylamino)ethoxy]ethyl} modified antisense oligonucleotides: Symbiosis of charge interaction factors and stereoelectronic effects. Org. Lett., 5, 2017-2020.
44. Prakash,T.P., Pueschl,A., Lesnik,E., Tereshko,V., Egli,M. and Manoharan,M. (2004) 2′-O-[2-(guanidinium)ethyl]-5-methyluridine modified oligonucleotides: Synthesis and stabilizing effect on duplex and triplex nucleic acid structures. Org. Lett., 6, 1971-1974.
45. Minasov,G., Teplova,M., Nielsen,P., Wengel,J. and Egli,M. (2000) Structural basis of cleavage by RNase H of hybrids of arabinonucleic acids and RNA. Biochemistry, 39, 3525-3532.
46. Lima,W.F. and Crooke,S.T. (1997) Binding affinity and specificity of Escherichia coli RNase H1: Impact on the kinetics of catalysis of antisense oligonucleotide-RNA hybrids. Biochemistry, 36, 5004-5019.
47. Lima,W.F., Nichols,J.G., Wu,H., Prakash,T.P., Migawa,M.T., Wyrzykiewicz,T.K., Bhat,B. and Crooke,S.T. (2004) Structural requirements at the catalytic site of the heteroduplex substrate for human RNase H1 catalysis. J. Biol. Chem., 279, 36317-36326.
48. Hoshika,S., Minakawa,N. and Matsuda,A. (2004) Synthesis and physical and physiological properties of 4′-thioRNA: Application to post-modification of RNA aptamer toward NF-κB. Nucleic Acids Res., 32, 3815-3825.
49. Haeberli,P., Berger,I., Pallan,P.S. and Egli,M. (2005) Syntheses of 4′-thioribonucleosides and thermodynamic stability and crystal structure of RNA oligomers with incorporated 4′-thiocytosine. Nucleic Acids Res., 33, 3965-3975.