NMR structures of (rGCUGAGGCU)2 and (rGCGGAUGCU)2: Probing the structural features that shape the thermodynamic stability of GA pairs

Biochemistry

Volumn 46, Issue 6, 2007, Pages 1511-1522

  Tolbert, Blanton S ^a   Kennedy, Scott D ^a   Schroeder, Susan J ^b   Krugh, Thomas R ^c   Turner, Douglas H ^a,c  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL STRUCTURE; HYDROGEN BONDS; NUCLEAR MAGNETIC RESONANCE; PROTEINS; THERMODYNAMIC STABILITY;

CARBONYL GROUP; PHYSICOCHEMICAL PROPERTIES; STRUCTURAL FEATURES; TANDEM;

RNA;

ADENINE; AMINE; BACTERIAL RNA; CARBONYL DERIVATIVE; GUANINE; RNA; RNA 16S; URACIL;

ARTICLE; BASE PAIRING; CONTROLLED STUDY; ESCHERICHIA COLI; HYDROGEN BOND; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; RNA ANALYSIS; RNA CONFORMATION; RNA PROBE; RNA SEQUENCE; RNA STABILITY; RNA STRUCTURE; SEQUENCE ANALYSIS; STRUCTURAL GENOMICS; THERMODYNAMICS; THERMOSTABILITY;

BASE PAIRING; BASE SEQUENCE; HYDROGEN BONDING; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; OLIGORIBONUCLEOTIDES; RNA; THERMODYNAMICS;

EID: 33846972283     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061350m     Document Type: Article

References (80)

1. Gesteland, R. F., Cech, T. R., and Atkins, J. F. (2006) The RNA World, 3rd ed., Cold Spring Harbor Press, Cold Spring Harbor, NY.
2. Sevignani, C., Calin, G. A., Siracusa, L. D., and Croce, C. M. (2006) Mammalian microRNAs: a small world for fine-tuning gene expression, Mamm. Genome 17, 189-202.
3. Stark, A., Brennecke, J., Bushati, N., Russell, R. B., and Cohen, S. M. (2005) Animal microRNAs confer robustness to gene expression and have a significant impact on 3′ UTR evolution, Cell 123, 1133-1146.
4. Winkler, W. C. (2005) Riboswitches and the role of noncoding RNAs in bacterial metabolic control, Curr. Opin. Chem. Biol. 9, 594-602.
5. Mathews, D. H., Sabina, J., Zuker, M., and Turner, D. H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure, J. Mol. Biol. 288, 911-940.
6. Mathews, D. H., Disney, M. D., Childs, J. L., Schroeder, S. J., Zuker, M., and Turner, D. H. (2004) Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure, Proc. Natl. Acad. Sci. U.S.A. 101, 7287-7292.
7. Xia, T., SantaLucia, J., Jr., Burkard, M. E., Kierzek, R., Schroeder, S. J., Jiao, X., 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.
8. Washietl, S., Hofacker, I. L., Lukasser, M., Huttenhofer, A., and Stadler, P. F. (2005) Mapping of conserved RNA secondary structures predicts thousands of functional noncoding RNAs in the human genome, Nat. Biotechnol. 23, 1383-1390.
9. Uzilov, A. V., Keegan, J. M., and Mathews, D. H. (2006) Detection of non-coding RNAs on the basis of predicted secondary structure formation free energy change, BMC Bioinf. 7, 173.
10. Chen, G., Znosko, B. M., Kennedy, S. D., Krugh, T. R., and Turner, D. H. (2005) Solution structure of an RNA internal loop with three consecutive sheared GA pairs, Biochemistry 44, 2845-2856.
11. Jang, S. B., Baeyens, K., Jeong, M. S., SantaLucia, J., Jr., Turner, D., and Holbrook, S. R. (2004) Structures of two RNA octamers containing tandem G.A base pairs, Acta Crystallogr., Sect. D 60, 829-835.
12. Chen, G., Znosko, B. M., Jiao, X., and Turner, D. H. (2004) Factors affecting thermodynamic stabilities of RNA 3 x 3 internal loops, Biochemistry 43, 12865-12876.
13. Schroeder, S. J., Fountain, M. A., Kennedy, S. D., Lukavsky, P. J., Puglisi, J. D., Krugh, T. R., and Turner, D. H. (2003) Thermodynamic stability and structural features of the J4/5 loop in a Pneumocystis carinii group I intron, Biochemistry 42, 14184-14196.
14. Znosko, B. M., Burkard, M. E., Schroeder, S. J., Krugh, T. R., and Turner, D. H. (2002) Sheared Aanti. Aanti base pairs in a destabilizing 2 x 2 internal loop: the NMR structure of 5′(rGGCAAGCCU)2, Biochemistry 41, 14969-14977.
15. Schroeder, S. J., and Turner, D. H. (2001) Thermodynamic stabilities of internal loops with GU closing pairs in RNA, Biochemistry 40, 11509-11517.
16. Burkard, M. E., Xia, T., and Turner, D. H. (2001) Thermodynamics of RNA internal loops with a guanosine-guanosine pair adjacent to another noncanonical pair, Biochemistry 40, 2478-2483.
17. Schroeder, S. J., and Turner, D. H. (2000) Factors affecting the thermodynamic stability of small asymmetric internal loops in RNA, Biochemistry 39, 9257-9274.
18. Burkard, M. E., and Turner, D. H. (2000) NMR structures of r(GCAGGCGUGC)2 and determinants of stability for single guanosine-guanosine base pairs, Biochemistry 39, 11748-11762.
19. Schroeder, S. J., Burkard, M. E., and Turner, D. H. (1999) The energetics of small internal loops in RNA, Biopolymers 52, 157-167.
20. Kierzek, R., Burkard, M. E., and Turner, D. H. (1999) Thermodynamics of single mismatches in RNA duplexes, Biochemistry 38, 14214-14223.
21. Xia, T., McDowell, J. A., and Turner, D. H. (1997) Thermodynamics of nonsymmetric tandem mismatches adjacent to G·C base pairs in RNA, Biochemistry 36, 12486-12497.
22. Wu, M., SantaLucia, J., Jr., and Turner, D. H. (1997) Solution structure of (rGGCAGGCC)2 by two-dimensional NMR and the iterative relaxation matrix approach, Biochemistry 36, 4449-4460.
23. Wu, M., and Turner, D. H. (1996) Solution structure of (rGCGGACGC)2 by two-dimensional NMR and the iterative relaxation matrix approach, Biochemistry 35, 9677-9689.
24. Schroeder, S., Kim, J., and Turner, D. H. (1996) G.A and U·U mismatches can stabilize RNA internal loops of three nucleotides, Biochemistry 35, 16105-16109.
25. Wu, M., McDowell, J. A., and Turner, D. H. (1995) A periodic table of symmetric tandem mismatches in RNA, Biochemistry 34, 3204-3211.
26. Walter, A. E., Wu, M., and Turner, D. H. (1994) The stability and structure of tandem GA mismatches in RNA depend on closing base pairs, Biochemistry 33, 11349-11354.
27. 2 in solution from NMR and restrained molecular dynamics, Biochemistry 32, 12612-12623.
28. + pairs, Biochemistry 30, 8242-8251.
29. Peritz, A. E., Kierzek, R., Sugimoto, N., and Turner, D. H. (1991) Thermodynamic study of internal loops in oligoribonucleotides: symmetric loops are more stable than asymmetric loops, Biochemistry 30, 6428-6436.
30. 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.
31. Morse, S. E., and Draper, D. E. (1995) Purine-purine mismatches in RNA helices: evidence for protonated G·A pairs and next-nearest neighbor effects, Nucleic Acids Res. 23, 302-306.
32. Butcher, S. E., Dieckmann, T., and Feigon, J. (1997) Solution structure of a GAAA tetraloop receptor RNA, EMBO J. 16, 7490-7499.
33. Butcher, S. E., Allain, F. H., and Feigon, J. (1999) Solution structure of the loop B domain from the hairpin ribozyme, Nat. Struct. Biol. 6, 212-216.
34. Bourdelat-Parks, B. N., and Wartell, R. M. (2005) Thermodynamics of RNA duplexes with tandem mismatches containing a uracil-uracil pair flanked by C·G/G·C or G·C/A·U closing base pairs, Biochemistry 44, 16710-16717.
35. Hoogstraten, C. G., Legault, P., and Pardi, A. (1998) NMR solution structure of the lead-dependent ribozyme: evidence for dynamics in RNA catalysis, J. Mol. Biol. 284, 337-350.
36. Campbell, D. O., and Legault, P. (2005) Nuclear magnetic resonance structure of the Varkud satellite ribozyme stem-loop V RNA and magnesium-ion binding from chemical-shift mapping, Biochemistry 44, 4157-4170.
37. Heus, H. A., Wijmenga, S. S., Hoppe, H., and Hilbers, C. W. (1997) The detailed structure of tandem G.A mismatched base-pair motifs in RNA duplexes is context dependent, J. Mol. Biol. 271, 147-158.
38. Chen, G., Kennedy, S. D., Qiao, J., Krugh, T. R., and Turner, D. H. (2006) An alternating sheared AA pair and elements of stability for a single sheared purine-purine pair flanked by sheared GA pairs in RNA, Biochemistry 45, 6889-6903.
39. Villescas-Diaz, G., and Zacharias, M. (2003) Sequence context dependence of tandem guanine:adenine mismatch conformations in RNA: a continuum solvent analysis, Biophys. J. 85, 416-425.
40. Sponer, J., Mokdad, A., Sponer, J. E., Spackova, N., Leszczynski, J., and Leontis, N. B. (2003) Unique tertiary and neighbor interactions determine conservation patterns of Cis Watson-Crick A/G base-pairs, J. Mol. Biol. 330, 967-978.
41. Pan, Y., Priyakumar, U. D., and MacKerell, A. D., Jr. (2005) Conformational determinants of tandem GU mismatches in RNA: insights from molecular dynamics simulations and quantum mechanical calculations, Biochemistry 44, 1433-1443.
42. Yildirim, I., and Turner, D. H. (2005) RNA challenges for computational chemists, Biochemistry 44, 13225-13234.
43. Heus, H. A., and Hilbers, C. W. (2003) Structures of non-canonical tandem base pairs in RNA helices: review, Nucleosides, Nucleotides Nucleic Acids 22, 559-571.
44. Gautheret, D., Konings, D., and Gutell, R. R. (1994) A major family of motifs involving G·A mismatches in ribosomal RNA, J. Mol. Biol. 242, 1-8.
45. Elgavish, T., Cannone, J. J., Lee, J. C., Harvey, S. C., and Gutell, R. R. (2001) AA.AG@helix.ends: A:A and A:G base-pairs at the ends of 16 S and 23 S rRNA helices, J. Mol. Biol. 310, 735-753.
46. SantaLucia, J., Jr., Kierzek, R., and Turner, D. H. (1990) Effects of GA mismatches on the structure and thermodynamics of RNA internal loops, Biochemistry 29, 8813-8819.
47. Leontis, N. B., Stombaugh, J., and Westhof, E. (2002) The non-Watson-Crick base pairs and their associated isostericity matrices, Nucleic Acids Res. 30, 3497-3531.
48. Wincott, F., DiRenzo, A., Shaffer, C., Grimm, S., Tracz, D., Workman, C., Sweedler, D., Gonzalez, C., Scaringe, S., and Usman, N. (1995) Synthesis, deprotection, analysis and purification of RNA and ribozymes, Nucleic Acids Res. 23, 2677-2684.
49. Usman, N., Ogilvie, K. K., Jiang, M. Y., and Cedergren, R. J. (1987) Automated chemical synthesis of long oligoribonucleotides using 2′-O-silylated ribonucleoside 3′-O-phosphoramidites on a controlled-pore-glass support: Synthesis of a 43 nucleotide sequence similar to the 3′-half molecule of an Escherichia coli formylmethionine tRNA, J. Am. Chem. Soc. 109, 7845-7854.
50. McDowell, J. A., and Turner, D. H. (1996) Investigation of the structural basis for thermodynamic stabilities of tandem GU mismatches: solution structure of (rGAGGUCUC)2 by two-dimensional NMR and simulated annealing, Biochemistry 35, 14077-14089.
51. Borer, P. N., Dengler, B., Tinoco, I., Jr., and Uhlenbeck, O. C. (1974) Stability of ribonucleic acid double-stranded helices, J. Mol. Biol. 86, 843-853.
52. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
53. Goddard, T. D., and Kneller, D.G. (2004) Sparky 3, NMR assignment and integration software, University of California, San Francisco, CA.
54. Klosterman, P. S., Shah, S. A., and Steitz, T. A. (1999) Crystal structures of two plasmid copy control related RNA duplexes: An 18 base pair duplex at 1.20 Å resolution and a 19 base pair duplex at 1.55 Å resolution, Biochemistry 38, 14784-14792.
55. Gorenstein, D. G. (1984) Phosphorus-31 NMR: Principles and Applications, Academic Press, Orlando, FL.
56. Brunger, 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 Crystallogr., Sect. D 54, 905-921.
57. DeLano, W. L. (2002) The PyMol Molecular Graphics System, DeLano Scientific, San Carlos, CA.
58. Lu, X. J., and Olson, W. K. (2003) 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures, Nucleic Acids Res. 31, 5108-5121.
59. Burkard, M. E., Kierzek, R., and Turner, D. H. (1999) Thermodynamics of unpaired terminal nucleotides on short RNA helixes correlates with stacking at helix termini in larger RNAs, J. Mol. Biol. 290, 967-982.
60. Longfellow, C. E., Kierzek, R., and Turner, D. H. (1990) Thermodynamic and spectroscopic study of bulge loops in oligoribonucleotides, Biochemistry 29, 278-285.
61. Varani, G., Aboulela, F., and Allain, F. H. T. (1996) NMR investigation of RNA structure, Prog. Nucl. Magn. Reson. Spectrosc. 29, 51-127.
62. Kieft, J. S., and Tinoco, I., Jr. (1997) Solution structure of a metal-binding site in the major groove of RNA complexed with cobalt (III) hexammine, Structure 5, 713-721.
63. Rudisser, S., and Tinoco, I., Jr. (2000) Solution structure of cobalt-(III)hexammine complexed to the GAAA tetraloop, and metal-ion binding to G·A mismatches, J. Mol. Biol. 295, 1211-1223.
64. Jucker, F. M., Heus, H. A., Yip, P. F., Moors, E. H., and Pardi, A. (1996) A network of heterogeneous hydrogen bonds in GNRA tetraloops, J. Mol. Biol. 264, 968-980.
65. Heus, H. A., and Pardi, A. (1991) Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops, Science 253, 191-194.
66. Wijmenga, S. S., Kruithof, M., and Hilbers, C. W. (1997) Analysis of 1H chemical shifts in DNA: assesment of reliability of 1H chemical shift calculations for use in structure refinement, J. Biomol. NMR 10, 337-350.
67. Cromsigt, J. A. M. T. C., Hilbers, C. W., and Wijmenga, S. S. (2001) Prediction of proton chemical shifts in RNA. Their use in structure refinement and validation, J. Biomol. NMR 21, 11-29.
68. SantaLucia, J., Jr., Kierzek, R., and Turner, D. H. (1992) Context dependence of hydrogen bond free energy revealed by substitutions in an RNA hairpin, Science 256, 217-219.
69. Lescoute, A., Leontis, N. B., Massire, C., and Westhof, E. (2005) Recurrent structural RNA motifs, isostericity matrices and sequence alignments, Nucleic Acids Res. 33, 2395-2409.
70. Morosyuk, S. V., Cunningham, P. R., and SantaLucia, J., Jr. (2001) Structure and function of the conserved 690 hairpin in Escherichia coli 16 S ribosomal RNA. II. NMR solution structure, J. Mol. Biol. 307, 197-211.
71. Schuwirth, B. S., Borovinskaya, M. A., Hau, C. W., Zhang, W., Vila-Sanjurjo, A., Holton, J. M., and Cate, J. H. (2005) Structures of the bacterial ribosome at 3.5 A resolution, Science 310, 827-834.
72. Chen, X., McDowell, J. A., Kierzek, R., Krugh, T. R., and Turner, D. H. (2000) Nuclear magnetic resonance spectroscopy and molecular modeling reveal that different hydrogen bonding patterns are possible for G·U pairs: one hydrogen bond for each G·U pair in r(GGCGUGCC)(2) and two for each G·U pair in r(GAGUGCUC)(2), Biochemistry 39, 8970-8982.
73. Michiels, P. J., Scheuten, C. H., Hilbers, C. W., and Heus, H. A. (2000) Structure of the ribozyme substrate hairpin of Neurospora VS RNA: a close look at the cleavage site, RNA 6, 1821-1832.
74. Brameld, K. A., and Goddard, W. A. (1999) Ab initio quantum mechanical study of the structures and energies for the pseudorotation of 5′-dehydroxy analogues of 2′-deoxyribose and ribose sugars, J. Am. Chem. Soc. 121, 985-993.
75. Foloppe, N., and MacKerell, A. D., Jr. (1999) Intrinsic conformational properties of deoxyribonucleosides: implicated role for cytosine in the equilibrium among the A, B, and Z forms of DNA, Biophys. J. 76, 3206-3218.
76. 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.
77. SantaLucia, J., Kierzek, R., and Turner, D. H. (1991) Functional group substitutions as probes for hydrogen bonding between GA mismatches in RNA internal loops, J. Am. Chem. Soc. 113, 4313-4322.
78. Turner, D. H. (2000) Conformational Changes, in Nucleic Acids: Structures, Properties, and Functions (Bloomfield, V. A., Crothers, D. M., and Tinoco, I., Jr., Eds.) pp 259-334, University Science Books, Sausalito, CA.
79. Cannone, J. J., Subramanian, S., Schnare, M. N., Collett, J. R., D'Souza, L. M., Du, Y., Feng, B., Lin, N., Madabusi, L. V., Muller, K. M., Pande, N., Shang, Z., Yu, N., and Gutell, R. R. (2002) The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs, BMC Bioinf. 3, 2.
80. Gralla, J., and Crothers, D. M. (1973) Free energy of imperfect nucleic acid helices. 3. Small internal loops resulting from mismatches, J. Mol. Biol. 78, 301-319.