A CA+ pair adjacent to a sheared GA or AA pair stabilizes size-symmetric RNA internal loops

Biochemistry

Volumn 48, Issue 24, 2009, Pages 5738-5752

  Chen, Gang ^a   Kennedy, Scott D ^b   Turner, Douglas H ^a,b  

^a UNIVERSITY OF ROCHESTER   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

FREE-ENERGY MODEL; IMINO PROTONS; INTERNAL LOOPS; LOCAL SEQUENCES; NEAREST NEIGHBORS; NEUTRAL PH; NMR STRUCTURES; PH-DEPENDENT; PROTONATED; SEQUENCE-DEPENDENT; STRUCTURAL ENVIRONMENT; UV ABSORBANCE; WATSON-CRICK PAIRS;

GENETIC ALGORITHMS; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEIC ACIDS; STABILIZATION;

RNA;

ADENINE; CYTOSINE; GUANINE; NUCLEOTIDE; RNA;

ARTICLE; BASE PAIRING; CHEMICAL MODEL; CRYSTAL STRUCTURE; ENERGY; HIGH TEMPERATURE; LIGHT ABSORPTION; NUCLEAR MAGNETIC RESONANCE; PH; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; RNA STABILITY; RNA STRUCTURE; THERMODYNAMICS;

ADENINE; BASE PAIRING; BASE SEQUENCE; CYTOSINE; GUANINE; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; OLIGONUCLEOTIDES; RNA; RNA STABILITY; THERMODYNAMICS;

EID: 67649197550     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8019405     Document Type: Article

References (75)

1. a shift at the active site of a lead-dependent ribozyme. J. Am. Chem. Soc. 119, 6621-6628.
2. Bevilacqua, P. C. (2003) Mechanistic considerations for general acid-base catalysis by RNA: Revisiting the mechanism of the hairpin ribozyme. Biochemistry 42, 2259-2265. (Pubitemid 36255199)
3. Cai, Z., and Tinoco, I. Jr. (1996) Solution structure of loop A from the hairpin ribozyme from tobacco ringspot virus satellite. Biochemistry 35, 6026-6036. (Pubitemid 26147574)
4. Allawi, H. T., and SantaLucia, J. Jr. (1998) Nearest-neighbor thermodynamics of internal AC mismatches in DNA: Sequence dependence and pH effects. Biochemistry 37, 9435-9444. (Pubitemid 28307699)
5. + pairs. Biochemistry 30, 8242-8251.
6. Bevilacqua, P. C., Brown, T. S., Chadalavada, D., Lecomte, J., Moody, E., and Nakano, S. (2005) Linkage between proton binding and folding in RNA: Implications for RNA catalysis. Biochem. Soc. Trans. 33, 466-470.
7. a shifting. RNA 11, 157-172.
8. Flinders, J., and Dieckmann, T. (2001) A pH controlled conformational switch in the cleavage site of the VS ribozyme substrate RNA. J. Mol. Biol. 308, 665-679.
9. Michiels, P. J. A., Schouten, C. H. J., 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. (Pubitemid 32001952)
10. Reiter, N. J., Blad, H., Abildgaard, F., and Butcher, S. E. (2004) Dynamics in the U6 RNA intramolecular stem-loop: A base flipping conformational change. Biochemistry 43, 13739-13747. (Pubitemid 39431057)
11. Zimmermann, G. R., Shields, T. P., Jenison, R. D., Wick, C. L., and Pardi, A. (1998) A semiconserved residue inhibits complex formation by stabilizing interactions in the free state of a theophylline-binding RNA. Biochemistry 37, 9186-9192. (Pubitemid 28299693)
12. Puglisi, J. D., Wyatt, J. R., and Tinoco, I. Jr. (1990) Solution conformation of an RNA hairpin loop. Biochemistry 29, 4215-4226. (Pubitemid 20145660)
13. 6A. Biochemistry 44, 8078-8089.
14. Bink, H. H., Hellendoorn, K., van der Meulen, J., and Pleij, C. W. (2002) Protonation of non-Watson-Crick base pairs and encapsidation of turnip yellow mosaic virus RNA. Proc. Natl. Acad. Sci. U.S.A. 99, 13465-13470.
15. Reiche, K., and Stadler, P. F. (2007) RNAstrand: Reading direction of structured RNAs in multiple sequence alignments. Algorithms Mol. Biol. 2, 6.
16. Chen, G., and Turner, D. H. (2006) Consecutive GA pairs stabilize medium-size RNA internal loops. Biochemistry 45, 4025-4043.
17. 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.
18. 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.
19. Chen, G., Znosko, B. M., Jiao, X. Q., and Turner, D. H. (2004) Factors affecting thermodynamic stabilities of RNA 3 x 3 internal loops. Biochemistry 43, 12865-12876. (Pubitemid 39331806)
20. 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. (Pubitemid 40293660)
21. Borer, P. N. (1975) Optical properties of nucleic acids, absorption and circular dichroism spectra, in Handbook of Biochemistry and Molecular Biology: Nucleic Acids, 3rd ed. (Fasman, G. D., Ed.) pp 589-595, CRC Press, Cleveland, OH.
22. Richards, E. G. (1975) Use of tables in calculation of absorption, optical rotatory dispersion and circular dichroism of polyribonucleotides, in Handbook of Biochemistry and Molecular Biology: Nucleic Acids, 3rd ed. (Fasman, G. D., Ed.) pp 596-603, CRC Press, Cleveland, OH.
23. 2 by two-dimensional NMR and simulated annealing. Biochemistry 35, 14077-14089.
24. Petersheim, M., and Turner, D. H. (1983) Base-stacking and base-pairing contributions to helix stability: Thermodynamics of double-helix formation with CCGG, CCGGp, CCGGAp, ACCGGp, CCGGUp, and ACCGGUp. Biochemistry 22, 256-263. (Pubitemid 13146564)
25. 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. (Pubitemid 28487580)
26. 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.
27. Lukavsky, P. J., and Puglisi, J. D. (2001) RNAPack: An integrated NMR approach to RNA structure determination. Methods 25, 316-332. (Pubitemid 34183556)
28. Smallcombe, S. H. (1993) Solvent suppression with symmetrically shifted pulses. J. Am. Chem. Soc. 115, 4776-4785.
29. 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.
30. Gralla, J., and Crothers, D. M. (1973) Free energy of imperfect nucleic acid helices: III. Small internal loops resulting from mismatches. J. Mol. Biol. 78, 301-319.
31. 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.
32. Blake, R. D. (1996) Denaturation of DNA, in Encyclopedia of Molecular Biology and Molecular Medicine (Meyers, R. A., Ed.) pp 1-19, VCH, New York.
33. Record, M. T. Jr. (1967) Electrostatic effects on polynucleotide transitions. II. Behavior of titrated systems. Biopolymers 5, 993-1008.
34. Nagaswamy, U., Larios-Sanz, M., Hury, J., Collins, S., Zhang, Z. D., Zhao, Q., and Fox, G. E. (2002) NCIR: A database of non-canonical interactions in known RNA structures. Nucleic Acids Res. 30, 395-397. (Pubitemid 34679595)
35. Tamura, M., Hendrix, D. K., Klosterman, P. S., Schimmelman, N. R., Brenner, S. E., and Holbrook, S. R. (2004) SCOR: Structural classification of RNA, version 2.0. Nucleic Acids Res. 32, D182-D184. (Pubitemid 38081634)
36. Adams, P. L., Stahley, M. R., Kosek,A. B., Wang, J. M., and Strobel, S. A. (2004) Crystal structure of a self-splicing group I intron with both exons. Nature 430, 45-50. (Pubitemid 38915218)
37. Butcher, S. E., Allain, F. H. T., and Feigon, J. (1999) Solution structure of the loop B domain from the hairpin ribozyme. Nat. Struct. Biol. 6, 212-216.
38. Schuwirth, B. S., Borovinskaya, M. A., Hau, C. W., Zhang, W., Vila- Sanjurjo, A., Holton, J. M., and Cate, J. H. D. (2005) Structures of the bacterial ribosome at 3.5 Å resolution. Science 310, 827-834. (Pubitemid 41567336)
39. Wimberly, B. T., Brodersen, D. E., Clemons, W. M., Morgan- Warren, R. J., Carter, A. P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. (2000) Structure of the 30S ribosomal subunit. Nature 407, 327-339. (Pubitemid 30736003)
40. Ban, N., Nissen, P., Hansen, J., Moore, P. B., and Steitz, T. A. (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289, 905-920. (Pubitemid 30659939)
41. a perturbation of nucleobases is an intrinsic property of the sequence context in DNA and RNA. J. Am. Chem. Soc. 126, 8674-8681.
42. + mismatches. J. Mol. Biol. 283, 977-984.
43. 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. (Pubitemid 34919207)
44. Kierzek, R., Burkard, M. E., and Turner, D. H. (1999) Thermodynamics of single mismatches in RNA duplexes. Biochemistry 38, 14214-14223. (Pubitemid 129520301)
45. 2. J. Am. Chem. Soc. 113, 5486-5488.
46. Wong, S. K., Sato, S., and Lazinski, D. W. (2001) Substrate recognition by ADAR1 and ADAR2. RNA 7, 846-858. (Pubitemid 32552872)
47. Yildirim, I., and Turner, D. H. (2005) RNA challenges for computational chemists. Biochemistry 44, 13225-13234. (Pubitemid 41429447)
48. as in RNA: On the structural origins and functional roles of protonated nucleotides. J. Mol. Biol. 366, 1475-1496.
49. 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. (Pubitemid 9055879)
50. Flinders, J., and Dieckmann, T. (2004) The solution structure of the VS ribozyme active site loop reveals a dynamic "hot-spot". J. Mol. Biol. 341, 935-949.
51. + base pairs. Biochemistry 37, 11726-11731.
52. 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. (Pubitemid 39665081)
53. 2. Biochemistry 39, 8970-8982.
54. O'Toole, A. S., Miller, S., Haines, N., Zink, M. C., and Serra, M. J. (2006) Comprehensive thermodynamic analysis of 30 double-nucleotide overhangs neighboring Watson-Crick terminal base pairs. Nucleic Acids Res. 34, 3338-3344.
55. Ohmichi, T., Nakano, S., Miyoshi, D., and Sugimoto, N. (2002) Long RNA dangling end has large energetic contribution to duplex stability. J. Am. Chem. Soc. 124, 10367-10372.
56. Holbrook, S. R., Cheong, C. J., 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. (Pubitemid 21912562)
57. Cruse, W. B. T., Saludjian, P., Biala, E., Strazewski, P., Prange, T., and Kennard, O. (1994) Structure of a mispaired RNA double helix at 1.6 A ̊ resolution and implications for the prediction of RNA secondary structure. Proc. Natl. Acad. Sci. U.S.A. 91, 4160-4164.
58. Brandl, M., Meyer, M., and Suhnel, J. (1999) Quantum-chemical study of a water-mediated uracil-cytosine base pair. J. Am. Chem. Soc. 121, 2605-2606.
59. Schneider, C., Brandl, M., and Suhnel, J. (2001) Molecular dynamics simulation reveals conformational switching of water-mediated uracil-cytosine base-pairs in an RNA duplex. J.Mol. Biol. 305, 659-667.
60. Yingling, Y. G., and Shapiro, B. A. (2005) Dynamic behavior of the telomerase RNA hairpin structure and its relationship to Dyskeratosis congenita. J. Mol. Biol. 348, 27-42.
61. Lescrinier, E., Tessari, M., van Kuppeveld, F. J. M., Melchers, W. J. G., Hilbers, C. W., and Heus, H. A. (2003) Structure of the pyrimidine-rich internal loop in the poliovirus 3′-UTR: The importance of maintaining pseudo-2-fold symmetry in RNA helices containing two adjacent non-canonical base-pairs. J. Mol. Biol. 331, 759-769.
62. Lukavsky, P. J., Kim, I., Otto, G. A., and Puglisi, J. D. (2003) Structure of HCV IRES domain II determined by NMR. Nat. Struct. Biol. 10, 1033-1038.
63. Du, Z. H., Yu, J. H., Ulyanov, N. B., Andino, R., and James, T. L. (2004) Solution structure of a consensus stem-loop D RNA domain that plays important roles in regulating translation and replication in enteroviruses and rhinoviruses. Biochemistry 43, 11959-11972. (Pubitemid 39280541)
64. Ohlenschlager, O., Wohnert, J., Bucci, E., Seitz, S., Hafner, S., Ramachandran, R., Zell, R., and Gorlach, M. (2004) The structure of the stemloop D subdomain of coxsackievirus B3 cloverleaf RNA and its interaction with the proteinase 3C. Structure 12, 237-248. (Pubitemid 38228484)
65. 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.
66. Wedekind, J. E., and McKay, D. B. (2003) Crystal structure of the leadzyme at 1.8 A ̊ resolution: Metal ion binding and the implications for catalytic mechanism and allo site ion regulation. Biochemistry 42, 9554-9563. (Pubitemid 37006304)
67. Lemieux, S., Chartrand, P., Cedergren, R., and Major, F. (1998) Modeling active RNA structures using the intersection of conformational space: Application to the lead-activated ribozyme. RNA 4, 739-749. (Pubitemid 28317823)
68. Yajima, R., Proctor, D. J., Kierzek, R., Kierzek, E., and Bevilacqua, P. C. (2007) A conformationally restricted guanosine analog reveals the catalytic relevance of three structures of an RNA enzyme. Chem. Biol. 14, 23-30.
69. Schroeder, S. J., and Turner, D. H. (2000) Factors affecting the thermodynamic stability of small asymmetric internal loops in RNA. Biochemistry 39, 9257-9274. (Pubitemid 30626318)
70. Ferre-D'Amare, A. R. (2004) The hairpin ribozyme. Biopolymers 73, 71-78. (Pubitemid 38101471)
71. Weichenrieder, O., Wild, K., Strub, K., and Cusack, S. (2000) Structure and assembly of the Alu domain of the mammalian signal recognition particle. Nature 408, 167-173. (Pubitemid 30839411)
72. 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. (Pubitemid 43856674)
73. 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.
74. 2: Probing the structural features that shape the thermodynamic stability of GA pairs. Biochemistry 46, 1511-1522.
75. 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. (Pubitemid 37441878)