Solution structure of a purine rich hexaloop hairpin belonging to PGY/MDR1 mRNA and targeted by antisense oligonucleotides

Nucleic Acids Research

Volumn 34, Issue 20, 2006, Pages 5740-5751

  Joli, Flore ^a   Bouchemal, Nadia ^a   Laigle, Alain ^a   Hartmann, Brigitte ^b   Hantz, Edith ^a  

^a UNIVERSITÉ PARIS 13   (France)

^b INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ANTISENSE OLIGONUCLEOTIDE; CARBOHYDRATE; GUANINE; HYDROGEN; HYDROXYL GROUP; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; PHOSPHATE; PURINE; URACIL;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BASE MISPAIRING; BINDING SITE; CONTROLLED STUDY; HUMAN; HYDROGEN BOND; LINKAGE ANALYSIS; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; RNA STABILITY;

BASE PAIRING; CARBOHYDRATES; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; OLIGONUCLEOTIDES, ANTISENSE; P-GLYCOPROTEIN; PHOSPHATES; PURINES; RNA, MESSENGER; SOLUTIONS;

EID: 33845627307     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl617     Document Type: Article

References (64)

1. Juranka,P.F., Zastawny,R.L. and Ling,V. (1989) P-glycoprotein: multidrug-resistance and a superfamily of membrane-associated transport proteins. Faseb J., 3, 2583-2592.
2. Ling,V., Gerlach,J. and Kartner,N. (1984) Multidrug resistance. Breast Cancer Res. Treat., 4, 89-94.
3. Alahari,S.K., Dean,N.M., Fisher,M.H., Delong,R., Manoharan,M., Tivel,K.L. and Juliano,R.L. (1996) Inhibition of expression of the multidrug resistance-associated P-glycoprotein of by phosphorothioate and 5′ cholesterol-conjugated phosphorothioate antisense oligonucleotides. Mol. Pharmacol., 50, 808-819.
4. Brigui,I., Djavanbakht-Samani,T., Jolles,B., Pigaglio,S. and Laigle,A. (2003) Minimally modified phosphodiester antisense oligodeoxyribonucleotide directed against the multidrug resistance gene mdr1. Biochem. Pharmacol., 65, 747-754.
5. Ho,S.P., Britton,D.H., Stone,B.A., Behrens,D.L., Leffet,L.M., Hobbs,F.W., Miller,J.A. and Trainor,G.L. (1996) Potent antisense oligonucleotides to the human multidrug resistance-1 mRNA are rationally selected by mapping RNA-accessible sites with oligonucleotide libraries. Nucleic Acids Res., 24, 1901-1907.
6. Motomura,S., Motoji,T., Takanashi,M., Wang,Y.H., Shiozaki,H., Sugawara,I., Aikawa,E., Tomida,A., Tsuruo,T., Kanda,N. et al. (1998) Inhibition of P-glycoprotein and recovery of drug sensitivity of human acute leukemic blast cells by multidrug resistance gene (mdr1) antisense oligonucleotides. Blood, 91, 3163-3171.
7. Wei,H.L., Wu,Y.J., Jing,T., Bai,D.C. and Ma,L.F. (2003) Sensitization and apoptosis augmentation of K562/ADM cells by anti-multidrug resistance gene peptide nucleic acid and antisense oligodeoxyribonucleotide. Acta. Pharmacol. Sin., 24, 805-811.
8. Kostenko,E.V., Beabealashvilly,R.S., Vlassov,V.V. and Zenkova,M.A. (2000) Secondary structure of the 5′-region of PGY1/MDR1 mRNA. FEBS Lett., 475, 181-186.
9. Tu,G.C., Cao,Q.N., Zhou,F. and Israel,Y. (1998) Tetranucleotide GGGA motif in primary RNA transcripts. Novel target site for antisense design. J. Biol. Chem., 273, 25125-25131.
10. Varani,G. and McClain,W.H. (2000) The G × U wobble base pair. A fundamental building block of RNA structure crucial to RNA function in diverse biological systems. EMBO Rep., 1, 18-23.
11. Masquida,B. and Westhof,E. (2000) On the wobble GoU and related pairs. Rna., 6, 9-15.
12. White,S.A., Nilges,M., Huang,A., Brunger,A.T. and Moore,P.B. (1992) NMR analysis of helix I from the 5S RNA of Escherichia coli. Biochemistry, 31, 1610-1621.
13. Allain,F.H. and Varani,G. (1995) Divalent metal ion binding to a conserved wobble pair defining the upstream site of cleavage of group I self-splicing introns. Nucleic Acids Res., 23, 341-350.
14. Ramos,A. and Varani,G. (1997) Structure of the acceptor stem of Escherichia coli tRNA Ala: Role of the G3.U70 base pair in synthetase recognition. Nucleic Acids Res., 25, 2083-2090.
15. Sigel,R.K., Sashital,D.G., Abramovitz,D.L., Palmer,A.G., Butcher,S.E. and Pyle,A.M. (2004) Solution structure of domain 5 of a group II intron ribozyme reveals a new RNA motif. Nature Struct. Mol. Biol., 11, 187-192.
16. Puglisi,E.V. and Puglisi,J.D. (1998) HIV-1 A-rich RNA loop mimics the tRNA anticodon structure. Nature Struct. Biol., 5, 1033-1036.
17. Plateau,P. and Gueron,M. (1982) Exchangeable proton NMR without base-line distorsion, using new strong-pulse sequences. J. Am Chem. Soc., 104, 7310-7311.
18. Marion,D. and Wuthrich,K. (1983) Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of 1H-1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun., 113, 967-974.
19. Sklenar,V., Miyashiro,H., Zon,G., Miles,H.T. and Bax,A. (1986) Assignment of the 31P and 1H resonances in oligonucleotides by two-dimensional NMR spectroscopy. FEBS Lett., 208, 94-98.
20. Bodenhausen,G. and Ruben,D. (1980) Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Lett., 69, 185-189.
21. Norwood,T.J., Boyd,J., Heritage,J.E., Soffe,N. and Campbell,I.D. (1990) Comparison of techniques for 1H detected heteronuclear 1H-15N spectroscopy. J. Magn. Reson., 87, 488-501.
22. Lukavsky,P.J. and Puglisi,J.D. (2001) RNAPack: An integrated NMR approach to RNA structure determination. Methods., 25, 316-332.
23. Wohnert,J., Dingley,A.J., Stoldt,M., Gorlach,M., Grzesiek,S. and Brown,L.R. (1999) Direct identification of NH. N hydrogen bonds in non-canonical base pairs of RNA by NMR spectroscopy. Nucleic Acids Res., 27, 3104-3110.
24. Pardi,A. and Nikonowicz,E.P. (1992) Simple procedure for resonance assignment of the sugar protons in carbon-13 labeled RNAs. J. Am Chem. Soc., 114, 9202-9203.
25. Brutscher,B. and Simorre,J.P. (2001) Transverse relaxation optimized HCN experiment for nucleic acids: Combining the advantages of TROSY and MQ spin evolution. J. Biomol. NMR., 21, 367-372.
26. Simorre,J.P., Zimmermann,G.R., Mueller,L. and Pardi,A. (1996) Correlation of the guanosine exchangeable and nonexchangeable base protons in 13C-/15N-labeled RNA with an HNC-TOCSY-CH experiment. J. Biomol. NMR., 7, 153-156.
27. Simorre,J.P., Zimmermann,G.R., Pardi,A., Farmer,B.T., 2nd and Mueller,L. (1995) Triple resonance HNCCCH experiments for correlating exchangeable and nonexchangeable cytidine and uridine base protons in RNA. J. Biomol. NMR., 6, 427-432.
28. Simorre,J.P., Zimmermann,G.R., Mueller,L. and Pardi,A. (1996) Triple-resonance experiments for assignment of adenine base resonances in 13C/15N-labeled RNA. J. Am. Chem. Soc., 118, 5316-5317.
29. Baleja,J.D. and Sykes,B.D. (1991) Correlation time adjustment factors for NOE-based structure refinement. J. Magn. Reson., 91, 624-629.
30. Lavery,R., Zakrzewska,K. and Sklenar,H. (1995) JUMNA (junction minimisation of nucleic acids). Comput. Phys. Commun., 91, 135-158.
31. Cheatham,T.E., III, 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.
32. Case,D.A., Pearlman,D.A., Caldwell,J.W., Cheatham,T.E.I., Wang,J., Ross,W.S., Simmerling,C.L., Darden,T.A., Merz,K.M., Stanton,R.V. et al. (2002) AMBER 7. University of California, San Francisco, CA.
33. Lavery,R. and Hartmann,B. (1994) Modelling DNA conformational mechanics. Biophys. Chem., 50, 33-45.
34. Varnai,P., Djuranovic,D., Lavery,R. and Hartmann,B. (2002) Alpha/gamma transitions in the B-DNA backbone. Nucleic Acids Res., 30, 5398-5406.
35. Tisne,C., Hantz,E., Hartmann,B. and Delepierre,M. (1998) Solution structure of a non-palindromic 16 base-pair DNA related to the HIV-1 kappa B site: Evidence for BI-BII equilibrium inducing a global dynamic curvature of the duplex. J. Mol. Biol., 279, 127-142.
36. Tisne,C., Hartmann,B. and Delepierre,M. (1999) NF-kappa B binding mechanism: A nuclear magnetic resonance and modeling study of a GGG → CTC mutation. Biochemistry, 38, 3883-3894.
37. Berendsen,H.J.C., Postma,J.P.M., Van Gunsteren,W.F., A,D.N. and Haak,J.R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys., 81, 3684-3690.
38. Ryckaert,J.P., Ciccotti,G. and Berendsen,H.J.C. (1977) Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J. Comput. Phys., 23, 327-341.
39. Darden,T., York,D. and Pedersen,L.J. (1993) Particle mesh Ewald: An N-log(N) method for Ewald sums in large systems. J. Chem. Phys., 98, 10089-10092.
40. Cheatham,T.E., III, Miller,J.L., Fox,T., Darden,T. and Kollman,P.A. (1995) molecular dynamics simulations on solvated biomolecular systems: the particle Mesh Ewald method leads to stable trajectories of DNA, RNA, and proteins. J. Am Chem. Soc., 117, 4193-4194.
41. Nikonowicz,E.P. and Pardi,A. (1993) An efficient procedure for assignment of the proton, carbon and nitrogen resonanes in 13C/15N labeled nucleic acids. J. Mol. Biol., 232, 1141-1156.
42. Varani,G. and Tinoco,I., Jr (1991) RNA structure and NMR spectroscopy. Q. Rev. Biophys., 24, 479-532.
43. Djuranovic,D. and Hartmann,B. (2003) Conformational characteristics and correlations in crystal structures of nucleic acid oligonucleotides: evidence for sub-states. J. Biomol. Struct. Dyn., 20, 771-788.
44. Joli,F., Hartmann,B. and Hantz,E. (2006) Structure and dynamics of phosphate linkages and sugars in an abasic hexaloop RNA hairpin. Biophys. J., 90.
45. Holbrook,S.R., Cheong,C., Tinoco,I., Jr and Kim,S.H. (1991) Crystal structure of an RNA double helix incorporating a track of non-Watson-Crick base pairs. Nature, 353, 579-581.
46. Lima,S., Hildenbrand,J., Korostelev,A., Hattman,S. and Li,H. (2002) Crystal structure of an RNA helix recognized by a zinc-finger protein: an 18-bp duplex at 1.6 A resolution. Rna, 8, 924-932.
47. Tanaka,Y., Fujii,S., Hiroaki,H., Sakata,T., Tanaka,T., Uesugi,S., Tomita,K. and Kyogoku,Y. (1999) A′-form RNA double helix in the single crystal structure of r(UGAGCUUCGGCUC). Nucleic Acids Res., 27, 949-955.
48. Znosko,B.M., Kennedy,S.D., Wille,P.C., Krugh,T.R. and Turner,D.H. (2004) Structural features and thermodynamics of the J4/5 loop from the Candida albicans and Candida dubliniensis group I introns. Biochemistry, 43, 15822-15837.
49. Lefebvre,A., Mauffret,O., Lescot,E., Hartmann,B. and Fermandjian,S. (1996) Solution structure of the CpG containing d(CTTCGAAG)2 oligonucleotide: NMR data and energy calculations are compatible with a BI/BII equilibrium at CpG. Biochemistry, 35, 12560-12569.
50. Djuranovic,D. and Hartmann,B. (2004) DNA fine structure and dynamics in crystals and in solution: The impact of BI/BII backbone conformations. Biopolymers, 73, 356-368.
51. Murray,L.J., Arendall,W.B., 3rd, Richardson,D.C. and Richardson,J.S. (2003) RNA backbone is rotameric. Proc. Natl Acad. Sci. USA, 100, 13904-13909.
52. Schneider,B., Moravek,Z. and Berman,H.M. (2004) RNA conformational classes. Nucleic Acids Res., 32, 1666-1677.
53. Lavery,R. and Sklenar,H. (1988) The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dyn., 6, 63-91.
54. Lavery,R. (1988) Junctions and bends in nucleic acids: A new theoretical approach. J. Biomol. Struct. Dyn., 3, 191-211.
55. Mizuno,H. and Sundaralingam,M. (1978) Stacking of Crick Wobble pair and Watson-Crick pair: Stability rules of G-U pairs at ends of helical stems in tRNAs and the relation to codon-anticodon Wobble interaction. Nucleic Acids Res., 5, 4451-4461.
56. Perez,A., Noy,A., Lankas,F., Luque,F.J. and Orozco,M. (2004) The relative flexibility of B-DNA and A-RNA duplexes: Database analysis. Nucleic Acids Res., 32, 6144-6151.
57. Klein,D.J., Moore,P.B. and Steitz,T.A. (2004) The contribution of metal ions to the structural stability of the large ribosomal subunit. RNA, 10, 1366-1379.
58. Hunter,C.A. (1993) Sequence-dependent DNA structure. The role of base stacking interactions. J. Mol. Biol., 230, 1025-1054.
59. Djuranovic,D. and Hartmann,B. (2005) Molecular dynamics studies on free and bound targets of the bovine papillomavirus type I e2 protein: The protein binding effect on DNA and the recognition mechanism. Biophys. J., 89, 2542-2551.
60. Sorin,E.J., Engelhardt,M.A., Herschlag,D. and Pande,V.S. (2002) RNA simulations: Probing hairpin unfolding and the dynamics of a GNRA tetraloop. J. Mol. Biol., 317, 493-506.
61. Foloppe,N. and MacKerell, J.A.D. (1998) Conformational properties of the deoxyribose and ribos moieties of nucleic acids: A quantum mechanical study. J. Phy. Chem. B., 102, 6669-6678.
62. Foloppe,N. and Nilsson,L. (2005) Toward a full characterization of nucleic acid components in aqueous solution: Similations of nucleosides. J. Phys. Chem. B., 109, 9119-9131.
63. Stallings,S.C. and Moore,P.B. (1997) The structure of an essential splicing element: Stem loop IIa from yeast U2 snRNA. Structure, 5, 1173-1185.
64. Mir,K.U. and Southern,E.M. (1999) Determining the influence of structure on hybridization using oligonucleotide arrays. Nat. Biotechnol., 17, 788-792.