RNA structure determination by NMR

Methods in Molecular Biology

Volumn 452, Issue , 2008, Pages 29-61

  Scott, Lincoln G ^a   Hennig, Mirko ^b  

^a Cassia LLC   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

NMR; Resonance assignment; RNA; RNA purification; RNA synthesis; Structure determination

Indexed keywords

EID: 84934438470     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-60327-159-2_2     Document Type: Article

References (129)

1. Leulliot, N., Varani, G. (2001) Current topics in RNA-protein recognition: control of specificity and biological function through induced fit and conformational capture. Biochemistry 40, 7947-7956.
2. Williamson, J. R. (2000) Induced fit in RNA-protein recognition. Nat Struct Biol 7, 834-837.
3. Milligan, J. F., Groebe, D. R., Witherell, G. W., et al. (1987) Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res 15, 8783-8798.
4. Milligan, J. F., Uhlenbeck, O. C. (1989) Synthesis of small RNAs using T7 RNA polymerase. Methods Enzymol 180, 51-62.
5. Perez-Canadillas, J. M., Varani, G. (2001) Recent advances in RNA-protein recognition. Curr Opin Struct Biol 11, 53-58.
6. Batey, R. T., Battiste, J. L., Williamson, J. R. (1995) Preparation of isotopically enriched RNAs for heteronuclear NMR. Methods Enzymol 261, 300-322.
7. Batey, R. T., Cloutier, N., Mao, H., et al. (1996) Improved large scale culture of Methylophilus methylotrophus for 13C/15N labeling and random fractional deuteration of ribonucleotides. Nucleic Acids Res 24, 4836-4837.
8. Batey, R. T., Inada, M., Kujawinski, E., et al. (1992) Preparation of isotopically labeled ribonucleotides for multidimensional NMR spectroscopy of RNA. Nucleic Acids Res 20, 4515-4523.
9. Nikonowicz, E. P., Sirr, A., Legault, P., et al. (1992) Preparation of 13C and 15N labelled RNAs for heteronuclear multidimensional NMR studies. Nucleic Acids Res 20, 4507-4513.
10. Zidek, L., Stefl, R., Sklenar, V. (2001) NMR methodology for the study of nucleic acids. Curr Opin Struct Biol 11, 275-281.
11. Cromsigt, J., van Buuren, B., Schleucher, J., et al. (2001) Resonance assignment and structure determination for RNA. Methods Enzymol 338, 371-399.
12. Furtig, B., Richter, C., Wohnert, J., et al. (2003) NMR spectroscopy of RNA. Chembiochem 4, 936-962.
13. Latham, M. P., Brown, D. J., McCallum, S. A., et al. (2005) NMR methods for studying the structure and dynamics of RNA. Chembiochemistry 6, 1492-1505.
14. Wu, H., Finger, L. D., Feigon, J. (2005) Structure determination of protein/RNA complexes by NMR. Methods Enzymol 394, 525-545.
15. Bax, A., Kontaxis, G., Tjandra, N. (2001) Dipolar couplings in macromolecular structure determination. Methods Enzymol 339, 127-174.
16. Hansen, M. R., Mueller, L., Pardi, A. (1998) Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nat Struct Biol 5, 1065-1074.
17. Tjandra, N., Bax, A. (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278, 1111-1114.
18. Reif, B., Hennig, M., Griesinger, C. (1997) Direct measurement of angles between bond vectors in high-resolution NMR. Science 276, 1230-1233.
19. Schwalbe, H., Carlomagno, T., Hennig, M., et al. (2001) Cross-correlated relaxation for measurement of angles between tensorial interactions. Methods Enzymol 338, 35-81.
20. Dingley, A. J., Grzesiek, S. (1998) Direct observation of hydrogen bonds in nucleic acid base pairs by internucleotide (2)J(NN) couplings. J Am Chem Soc 120, 8293-8297.
21. Pervushin, K., Ono, A., Fernandez, C., et al. (1998) NMR scaler couplings across Watson-Crick base pair hydrogen bonds in DNA observed by transverse relaxation optimized spectroscopy. Proc Natl Acad Sci U S A 95, 14147-14151.
22. Churcher, M. J., Lamont, C., Hamy, F., et al. (1993) High affinity binding of TAR RNA by the human immunodeficiency virus type-1 tat protein requires base-pairs in the RNA stem and amino acid residues flanking the basic region. J Mol Biol 230, 90-110.
23. Long, K. S., Crothers, D. M. (1995) Interaction of human immunodeficiency virus type 1 Tat-derived peptides with TAR RNA. Biochemistry 34, 8885-8895.
24. Tao, J., Frankel, A. D. (1992) Specific binding of arginine to TAR RNA. Proc Natl Acad Sci U S A 89, 2723-2726.
25. Tao, J., Frankel, A. D. (1993) Electrostatic interactions modulate the RNAbinding and transactivation specificities of the human immunodeficiency virus and simian immunodeficiency virus Tat proteins. Proc Natl Acad Sci U S A 90, 1571-1575.
26. Puglisi, J. D., Chen, L., Frankel, A. D., et al. (1993) Role of RNA structure in arginine recognition of TAR RNA. Proc Natl Acad Sci U S A 90, 3680-3684.
27. Puglisi, J. D., Tan, R., Calnan, B. J., et al. (1992) Conformation of the TAR RNAarginine complex by NMR spectroscopy. Science 257, 76-80.
28. Aboul-ela, F., Karn, J., Varani, G. (1995) The structure of the human immunodeficiency virus type-1 TAR RNA reveals principles of RNA recognition by Tat protein. J Mol Biol 253, 313-332.
29. Brodsky, A. S., Williamson, J. R. (1997) Solution structure of the HIV-2 TARargininamide complex. J Mol Biol 267, 624-639.
30. Aboul-ela, F., Karn, J., Varani, G. (1996) Structure of HIV-1 TAR RNA in the absence of ligands reveals a novel conformation of the trinucleotide bulge. Nucleic Acids Res 24, 3974-3781.
31. Long, K. S., Crothers, D. M. (1999) Characterization of the solution conformations of unbound and Tat peptide-bound forms of HIV-1 TAR RNA. Biochemistry 38, 10059-10069.
32. Sambrook, J., Fritsch, E. F., Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
33. Yin, Y., Carter, C. W., Jr. (1996) Incomplete factorial and response surface methods in experimental design: yield optimization of tRNA(Trp) from in vitro T7 RNA polymerase transcription. Nucleic Acids Res 24, 1279-1286.
34. Wyatt, J. R., Chastain, M., Puglisi, J. D. (1991) Synthesis and purification of large amounts of RNA oligonucleotides. Biotechniques 11, 764-769.
35. Anderson, A. C., Scaringe, S. A., Earp, B. E., et al. (1996) HPLC purification of RNA for crystallography and NMR. RNA 2, 110-117.
36. Shields, T. P., Mollova, E., Ste Marie, L., et al. (1999) High-performance liquid chromatography purification of homogenous-length RNA produced by trans cleavage with a hammerhead ribozyme. RNA 5, 1259-1267.
37. Wuthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley, New York.
38. Nikonowicz, E. P., Pardi, A. (1992) Threedimensional heteronuclear NMR studies of RNA. Nature 355, 184-186.
39. Nikonowicz, E. P., Pardi, A. (1993) An efficient procedure for assignment of the proton, carbon and nitrogen resonances in 13C/15N labeled nucleic acids. J Mol Biol 232, 1141-1156.
40. Wijmenga, S. S., van Buuren, B. N. M. (1998) The use of NMR methods for conformational studies of nucleic acids. Prog Nucl Magn Reson Spectrosc 32, 287-387.
41. Zhou, H., Vermeulen, A., Jucker, F. M., et al. (1999) Incorporating residual dipolar couplings into the NMR solution structure determination of nucleic acids. Biopolymers 52, 168-180.
42. Hansen, M. R., Hanson, P., Pardi, A. (2000) Filamentous bacteriophage for aligning RNA, DNA, and proteins for measurement of nuclear magnetic resonance dipolar coupling interactions. Methods Enzymol 317, 220-240.
43. Meiler, J., Prompers, J. J., Peti, W., et al. (2001) Model-free approach to the dynamic interpretation of residual dipolar couplings in globular proteins. J Am Chem Soc 123, 6098-6107.
44. Peti, W., Meiler, J., Bruschweiler, R., et al. (2002) Model-free analysis of protein backbone motion from residual dipolar couplings. J Am Chem Soc 124, 5822-5833.
45. Tolman, J. R. (2002) A novel approach to the retrieval of structural and dynamic information from residual dipolar couplings using several oriented media in biomolecular NMR spectroscopy. J Am Chem Soc 124, 12020-12030.
46. Lippens, G., Dhalluin, C., Wieruszeski, J. M. (1995) Use of a Water Flip-Back Pulse in the Homonuclear Noesy Experiment. J Biomol Nmr 5, 327-331.
47. Peterson, R. D., Theimer, C. A., Wu, H. H., et al. (2004) New applications of 2D filtered/edited NOESY for assignment and 58 Scott and Hennig structure elucidation of RNA and RNA-protein complexes. J Biomol Nmr 28, 59-67.
48. Duchardt, E., Richter, C., Reif, B., et al. (2001) Measurement of 2J(H,C)- and 3J(H,C)-coupling constants by alpha/beta selective HC(C)H-TOCSY. J Biomol NMR 21, 117-126.
49. Schwalbe, H., Marino, J. P., Glaser, S. J., et al. (1995) Measurement of H,H-Coupling Constants Associated with nu1, nu2, and nu3 in Uniformly 13C-Labeled RNA by HCC-TOCSY-CCH-E.COSY J Am Chem Soc 117, 7251-7252.
50. Schwalbe, H., Marino, J. P., King, G. C., et al. (1994) Determination of a complete set of coupling constants in 13C-labeled oligonucleotides. J Biomol NMR 4, 631-644.
51. Hines, J. V., Varani, G., Landry, S. M., et al. (1993) The stereospecific ass gnment of H5' and H5″ in RNA using the sign of two-bond carbon-proton scalar coupling. J Am Chem Soc 115, 11002-11003.
52. Trantirek, L., Stefl, R., Masse, J. E., et al. (2002) Determination of the glycosidic torsion angles in uniformly C-13-labeled nucleic acids from vicinal coupling constants (3)J(C2/4-H1') and (3)J(C6/8- H1'). J Biomol NMR 23, 1-12.
53. Carlomagno, T., Hennig, M., Williamson, J. R. (2002) A novel PH-cT-COSY methodology for measuring JPH coupling constants in unlabeled nucleic acids. application to HIV-2 TAR RNA. J Biomol NMR 22, 65-81.
54. Sklenar, V., Miyashiro, H., Zon, G., et al. (1986) Assignment of the 31P and 1H resonances in oligonucleotides by twodimensional NMR spectroscopy. FEBS Lett 208, 94-98.
55. Schwalbe, H., Samstag, W., Engels, J. W., et al. (1993) Determination of 3J(C,P) and 3J(H,P) coupling constants in nucleotide oligomers with FIDS-HSQC. J Biomol NMR 3, 479-486.
56. Hoogstraten, C. G., Pardi, A. (1998) Measurement of carbon-phosphorus J coupling constants in RNA using spin-echo difference constant-time HCCH-COSY. J Magn Reson 133, 236-240.
57. Legault, P., Jucker, F. M., Pardi, A. (1995) Improved measurement of 13C, 31P J coupling constants in isotopically labeled RNA. FEBS Lett 362, 156-160.
58. Szyperski, T., Fernandez, C., Ono, A., et al. (1999) The 2D [31P] spin-echo-difference constant-time [13C, 1H]-HMQC experiment for simultaneous determination of 3J(H3'P) and 3J(C4'P) in 13C-labeled nucleic acids and their protein complexes. J Magn Reson 140, 491-494.
59. Hu, W., Bouaziz, S., Skripkin, E., et al. (1999) Determination of 3J(H3i, Pi+1) and 3J(H5i/5i, Pi) coupling constants in 13Clabeled nucleic acids using constant-time HMQC. J Magn Reson 139, 181-185.
60. Clore, G. M., Murphy, E. C., Gronenborn, A. M., et al. (1998) Determination of three-bond 1H3'-31P couplings in nucleic acids and protein-nucleic acid complexes by quantitative J correlation spectroscopy. J Magn Reson 134, 164-167.
61. Gotfredsen, C. H., Meissner, A., Duus, J. O., et al. (2000) New methods for measuring 1H-31P coupling constants in nucleic acids. Magn Reson Chem 38, 692-695.
62. Richter, C., Reif, B., Worner, K., et al. (1998) A new experiment for the measurement of nJ(C,P) coupling constants including 3J(C4'i,Pi) and 3J(C4'i,Pi+1) in oligonucleotides. J Biomol NMR 12, 223-230.
63. Legault, P., Pardi, A. (1994) 31P chemical shift as a probe of structural motifs in RNA. J Magn Reson B 103, 82-86.
64. Richter, C., Reif, B., Griesinger, C., et al. (2000) NMR spectroscopic determination of angles and in RNA from CHdipolar coupling, P-CSA cross-correlated relaxation. J Am Chem Soc 122, 12728-12731.
65. Duchardt, E., Richter, C., Ohlenschlager, O., et al. (2004) Determination of the glycosidic bond angle chi in RNA from cross-correlated relaxation of CH dipolar coupling and N chemical shift anisotropy. J Am Chem Soc 126, 1962-1970.
66. Ravindranathan, S., Kim, C. H., Bodenhausen, G. (2003) Cross correlations between 13C-1H dipolar interactions and 15N chemical shift anisotropy in nucleic acids. J Biomol NMR 27, 365-375.
67. Felli, I. C., Richter, C., Griesinger, C., et al. (1999) Determination of RNA sugar pucker mode from cross-correlated relaxation in solution NMR spectroscopy. J Am Chem Soc 121, 1956-1957.
68. Richter, C., Griesinger, C., Felli, I., et al. (1999) Determination of sugar conformation in large RNA oligonucleotides from analysis of dipole-dipole cross correlated relaxation by solution NMR spectroscopy. J Biomol NMR 15, 241-250.
69. Andersson, P., Weigelt, J., Otting, G. (1998) Spin-state selection filters for the measurement of heteronuclear one-bond coupling constants. J Biomol NMR 12, 435-441.
70. Tjandra, N., Bax, A. (1997) Measurement of dipolar contributions to 1JCH splittings from magnetic-field dependence of J modulation in two-dimensional NMR spectra. J Magn Reson 124, 512-515.
71. Tjandra, N., Grzesiek, S., Bax, A. (1996) Magnetic field dependence of nitrogenproton J splittings in N-15-enriched human ubiquitin resulting from relaxation interference and residual dipolar coupling. J Am Chem Soc 118, 6264-6272.
72. Hennig, M., Carlomagno, T., Williamson, J. R. (2001) Residual dipolar coupling TOCSY for direct through space correlations of base protons and phosphorus nuclei in RNA. J Am Chem Soc 123, 3395-3396.
73. Wu, Z., Tjandra, N., Bax, A. (2001) Measurement of 1H3'-31P dipolar couplings in a DNA oligonucleotide by constant-time NOESY difference spectroscopy. J Biomol NMR 19, 367-370.
74. Wu, Z., Tjandra, N., Bax, A. (2001) 31P chemical shift anisotropy as an aid in determining nucleic acid structure in liquid crystals. J Am Chem Soc 123, 3617-3618.
75. Dingley, A. J., Masse, J. E., Feigon, J., et al. (2000) Characterization of the hydrogen bond network in guanosine quartets by internucleotide 3hJ(NC)' and 2hJ(NN) scalar couplings. J Biomol NMR 16, 279-289.
76. Dingley, A. J., Masse, J. E., Peterson, R. D., et al. (1999) Internucleotide scalar couplings across hydrogen bonds in Watson-Crickand Hoogsteen base pairs of a DNA triplex. J Am Chem Soc 121, 6019-6027.
77. Hennig, M., Williamson, J. R. (2000) Detection of N-H-N hydrogen bonding in RNA via scalar couplings in the absence of observable imino proton resonances. Nucleic Acids Res 28, 1585-1593.
78. Liu, A. Z., Majumdar, A., Hu, W. D., et al. (2000) NMR detection of N-H-O=C hydrogen bonds in C-13,N-15-labeled nucleic acids. J Am Chem Soc 122, 3206-3210.
79. Majumdar, A., Kettani, A., Skripkin, E. (1999) Observation and measurement of internucleotide 2JNN coupling constants between 15N nuclei with widely separated chemical shifts. J Biomol NMR 14, 67-70.
80. Majumdar, A., Kettani, A., Skripkin, E., et al. (1999) Observation of internucleotide NH-N hydrogen bonds in the absence of directly detectable protons. J Biomol NMR 15, 207-2-11.
81. Wohnert, J., Ramachandran, R., Gorlach, M., et al. (1999) Triple-resonance experiments for correlation of H5 and exchangeable pyrimidine base hydrogens in (13)C,(15) N-labeled RNA. J Magn Reson 139, 430-433.
82. Sklenar, V., Peterson, R. D., Rejante, M. R., et al. (1994) Correlation of nucleotide base and sugar protons in a N-15-labeled Hiv-1 RNA oligonucleotide by H-1-N-15 Hsqc experiments. J Biomol NMR 4, 117-122.
83. Fohrer, J., Hennig, M., Carlomagno, T. (2006) Influence of the 2'-hydroxyl group conformation on the stability of A-form helices in RNA. J Mol Biol 356, 280-287.
84. Hennig, M., Fohrer, J., Carlomagno, T. (2005) Assignment and NOE analysis of 2'-hydroxyl protons in RNA: implications for stabilization of RNA A-form duplexes. J Am Chem Soc 127, 2028-2029.
85. Giedroc, D. P., Cornish, P. V., Hennig, M. (2003) Detection of scalar couplings involving 2'-hydroxyl protons across hydrogen bonds in a frameshifting mRNA pseudoknot. J Am Chem Soc 125, 4676-4677.
86. Simorre, J. P., Zimmermann, G. R., Mueller, L., et al. (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.
87. Simorre, J. P., Zimmermann, G. R., Mueller, L., et al. (1996) Triple-resonance experiments for assignment of adenine base resonances in C-13/N-15-labeled RNA. J Am Chem Soc 118, 5316-5317.
88. Simorre, J. P., Zimmermann, G. R., Pardi, A., et al. (1995) Triple resonance HNCCCH experiments for correlating exchangeable and nonexchangeable cytidine and uridine base protons in RNA. J Biomol NMR 6, 427-432.
89. Sklenar, V., Dieckmann, T., Butcher, S. E., et al. (1996) Through-bond correlation of imino and aromatic resonances in C-13-,N- 15-labeled RNA via heteronuclear TOCSY. J Biomol Nmr 7, 83-87.
90. Wohnert, J., Gorlach, M., Schwalbe, H. (2003) Triple resonance experiments for the simultaneous correlation of H6/H5 and exchangeable protons of pyrimidine nucleotides in C-13, N-15-labeled RNA applicable to larger RNA molecules. J Biomol Nmr 26, 79-83.
91. Fiala, R., Jiang, F., Patel, D. J. (1996) Direct correlation of exchangeable and nonexchangeable protons on purine bases in 13C,15N-labeled RNA using a HCCNHTOCSY experiment. J Am Chem Soc 118, 689-690.
92. Simon, B., Zanier, K., Sattler, M. (2001) A TROSY relayed HCCH-COSY experiment 60 Scott and Hennig for correlating adenine H2/H8 resonances in uniformly 13C-labeled RNA molecules. J Biomol NMR 20, 173-176.
93. Legault, P., Farmer, B. T., Mueller, L., et al. (1994) Through-bond correlation of adenine protons in a C-13-labeled ribozyme. J Am Chem Soc 116, 2203-2204.
94. Marino, J. P., Prestegard, J. H., Crothers, D. M. (1994) Correlation of adenine H2/H8 resonances in uniformly C-13 labeled Rnas by 2d Hcch-Tocsy: a new tool for H-1 assignment. J Am Chem Soc 116, 2205-2206.
95. Marino, J. P., Diener, J. L., Moore, P. B., et al. (1997) Multiple-quantum coherence dramatically enhances the sensitivity of CH and CH2 correlations in uniformly 13C-labeled RNA. J Am Chem Soc 119, 7361-7366.
96. Sklenar, V., Dieckmann, T., Butcher, S. E., et al. (1998) Optimization of triple-resonance HCN experiments for application to larger RNA oligonucleotides. J Magn Reson 130, 119-124.
97. Fiala, R., Czernek, J., Sklenar, V. (2000) Transverse relaxation optimized tripleresonance NMR experiments for nucleic acids. J Biomol NMR 16, 291-302.
98. Riek, R., Pervushin, K., Fernandez, C., et al. (2001) [(13)C,(13)C]- and [(13)C,(1)H]-TROSY in a triple resonance experiment for ribose-base and intrabase correlations in nucleic acids. J Am Chem Soc 123, 658-664.
99. Farmer, B. T., Muller, L., Nikonowicz, E. P., et al. (1993) Unambiguous resonance assignments in carbon-13, nitrogen-15-labeled nucleic acids by 3D triple-resonance NMR. J Am Chem Soc 115, 11040-11041.
100. Sklenar, V., Rejante, M. R., Peterson, R. D., et al. (1993) Two-dimensional tripleresonance HCNCH experiment for direct correlation of ribose H1' and base H8, H6 protons in 13C,15N-labeled RNA oligonucleotides. J Am Chem Soc 115, 12181-12182.
101. Fesik, S. W., Eaton, H. L., Olejniczak, E. T., et al. (1990) 2D and 3D NMR spectroscopy employing carbon-13/carbon-13 magnetization transfer by isotropic mixing. Spin system identification in large proteins. J Am Chem Soc 112, 886-888.
102. Kay, L. E., Ikura, M., Bax, A. (1990) Proton-proton correlation via carbon-carbon couplings: a three-dimensional NMR approach for the assignment of aliphatic resonances in proteins labeled with carbon-13. J Am Chem Soc 112, 888-889.
103. Pardi, A. (1995) Multidimensional heteronuclear NMR experiments for structure determination of isotopically labeled RNA. Methods Enzymol 261, 350-380.
104. Pardi, A., 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.
105. Hu, W., Kakalis, L. T., Jiang, L., et al. (1998) 3D HCCH-COSY-TOCSY experiment for the assignment of ribose and amino acid side chains in 13C labeled RNA and protein. J Biomol NMR 12, 559-564.
106. Glaser, S. J., Schwalbe, H., Marino, J. P., et al. (1996) Directed TOCSY, a method for selection of directed correlations by optimal combinations of isotropic and longitudinal mixing. J Magn Reson B 112, 160-180.
107. Kellogg, G. W. (1992) Proton-detected hetero-TOCSY experiments with application to nucleic acids. J Magn Reson 98, 176-182.
108. Kellogg, G. W., Szewczak, A. A., Moore, P. B. (1992) Two-dimensional hetero-TOCSY-NOESY. Correlation of phosphorus-31 resonances with anomeric and aromatic proton resonances in RNA. J Am Chem Soc 114, 2727-2728.
109. Kellogg, G. W., Schweitzer, B. I. (1993) Two- and three-dimensional 31P-driven NMR procedures for complete assignment of backbone resonances in oligodeoxyribonucleotides. J Biomol NMR 3, 577-595.
110. Heus, H. A., Wijmenga, S. S., Vandeven, F. J. M., et al. (1994) Sequential backbone assignment in C-13-labeled Rna via through-bond coherence transfer using 3-dimensional triple-resonance spectroscopy (H-1, C-13, P-31) and 2-dimensional hetero Tocsy. J Am Chem Soc 116, 4983-4984.
111. Marino, J. P., Schwalbe, H., Anklin, C., et al. (1994) A 3-dimensional triple-resonance H-1,C-13,P-31 experiment: sequential through-bond correlation of ribose protons and intervening phosphorus along the Rna oligonucleotide backbone. J Am Chem Soc 116, 6472-6473.
112. Marino, J. P., Schwalbe, H., Anklin, C., et al. (1995) Sequential correlation of anomeric ribose protons and intervening phosphorus in RNA oligonucleotides by a 1H, 13C, 31P triple resonance experiment: HCP-CCHTOCSY. J Biomol NMR 5, 87-92.
113. Wijmenga, S. S., Heus, H. A., Leeuw, H. A., et al. (1995) Sequential backbone assignment of uniformly 13C-labeled RNAs by a two-dimensional P(CC)H-TOCSY triple resonance NMR experiment. J Biomol NMR 5, 82-86.
114. Marino, J. P., Schwalbe, H., Griesinger, C. (1999) J-coupling restraints in RNA structure determination. Acc Chem Res 32, 614-623.
115. Schwieters, C. D., Kuszewski, J. J., Tjandra, N., et al. (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160, 65-73.
116. Brunger, A. T., Adams, P. D., Clore, G. M., et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallographica Section D-Biological Crystallography 54, 905-921.
117. Stein, E. G., Rice, L. M., Brunger, A. T. (1997) Torsion-angle molecular dynamics as a new efficient tool for NMR structure calculation. J Magn Reson 124, 154-164.
118. Pearlman, D. A., Case, D. A., Caldwell, J. W., et al. (1995) AMBER, a computer program for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to elucidate the structures and energies of molecules. Computer Physics Communications 91, 1-41.
119. Tsui, V., Case, D. A. (2000) Molecular dynamics simulations of nucleic acids with a generalized born solvation model. J Am Chem Soc 122, 2489-2498.
120. Clore, G. M., Garrett, D. S. (1999) R-factor, free R, and complete cross-validation for dipolar coupling refinement of NMR structures. J Am Chem Soc 121, 9008-9012.
121. Clore, G. M., Kuszewski, J. (2003) Improving the accuracy of NMR structures of RNA by means of conformational database potentials of mean force as assessed by complete dipolar coupling cross-validation. J Am Chem Soc 125, 1518-1525.
122. Cromsigt, J. A., Hilbers, C. W., Wijmenga, S. S. (2001) Prediction of proton chemical shifts in RNA. Their use in structure refinement and validation. J Biomol NMR 21, 11-29.
123. Baklanov, M. M., Golikova, L. N., Malygin, E. G. (1996) Effect on DNA transcription of nucleotide sequences upstream to T7 promoter. Nucleic Acids Res 24, 3659-3660.
124. Moran, S., Ren, R. X., Sheils, C. J., et al. (1996) Non-hydrogen bonding 'terminator' nucleosides increase the 3'-end homogeneity of enzymatic RNA and DNA synthesis. Nucleic Acids Res 24, 2044-2052.
125. Ferre-D'Amare, A. R., Doudna, J. A. (1996) Use of cis- and trans-ribozymes to remove 5' and 3' heterogeneities from milligrams of in vitro transcribed RNA. Nucleic Acids Res 24, 977-978.
126. Price, S. R., Ito, N., Oubridge, C., et al. (1995) Crystallization of RNA-protein complexes. I. Methods for the largescale preparation of RNA suitable for crystallographic studies. J Mol Biol 249, 398-408.
127. Scott, L. G., Tolbert, T. J., Williamson, J. R. (2000) Preparation of specifically 2H- and 13C-labeled ribonucleotides. Methods Enzymol 317, 18-38.
128. Sklenar, V., Brooks, B. R., Zon, G., et al. (1987) Absorption mode two-dimensional NOE spectroscopy of exchangeable protons in oligonucleotides. FEBS Lett 216, 249-252.
129. Rance, M., Sorensen, O. W., Bodenhausen, G., et al. (1983) Improved spectral resolution in cosy 1H NMR spectra of proteins via double quantum filtering. Biochem Biophys Res Commun 117, 479-485.