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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Sep 27;91(20):9218–9222. doi: 10.1073/pnas.91.20.9218

Coaxial stacking of helixes enhances binding of oligoribonucleotides and improves predictions of RNA folding.

A E Walter 1, D H Turner 1, J Kim 1, M H Lyttle 1, P Müller 1, D H Mathews 1, M Zuker 1
PMCID: PMC44783  PMID: 7524072

Abstract

An RNA model system consisting of an oligomer binding to a 4-nt overhang at the 5' end of a hairpin stem provides thermodynamic parameters for helix-helix interfaces. In a sequence-dependent manner, oligomers bind up to 1000-fold more tightly adjacent to the hairpin stem than predicted for binding to a free tetramer at 37 degrees C. For the interface (/) in [formula: see text] additional free energy change, delta delta G 37 degrees, for binding is roughly the nearest-neighbor delta G 37 degrees for propagation of an uninterrupted helix of equivalent sequence, CGGC. When X and Z are omitted, the delta delta 37 degrees is even more favorable by approximately 1 kcal/mol (1 cal = 4.184J). On average, predictions of 11 RNA secondary structures improve from 67 to 74% accuracy by inclusion of similar stacking contributions.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bevilacqua P. C., Turner D. H. Comparison of binding of mixed ribose-deoxyribose analogues of CUCU to a ribozyme and to GGAGAA by equilibrium dialysis: evidence for ribozyme specific interactions with 2' OH groups. Biochemistry. 1991 Nov 5;30(44):10632–10640. doi: 10.1021/bi00108a005. [DOI] [PubMed] [Google Scholar]
  2. Coutts S. M., Gangloff J., Dirheimer G. Conformational transitions in tRNA Asp (brewer's yeast). Thermodynamic, kinetic, and enzymatic measurements on oligonucleotide fragments and the intact molecule. Biochemistry. 1974 Sep 10;13(19):3938–3948. doi: 10.1021/bi00716a019. [DOI] [PubMed] [Google Scholar]
  3. Delisi C., Crothers D. M. Prediction of RNA secondary structure. Proc Natl Acad Sci U S A. 1971 Nov;68(11):2682–2685. doi: 10.1073/pnas.68.11.2682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ecker D. J., Vickers T. A., Bruice T. W., Freier S. M., Jenison R. D., Manoharan M., Zounes M. Pseudo--half-knot formation with RNA. Science. 1992 Aug 14;257(5072):958–961. doi: 10.1126/science.1502560. [DOI] [PubMed] [Google Scholar]
  5. England T. E., Uhlenbeck O. C. Enzymatic oligoribonucleotide synthesis with T4 RNA ligase. Biochemistry. 1978 May 30;17(11):2069–2076. doi: 10.1021/bi00604a008. [DOI] [PubMed] [Google Scholar]
  6. Freier S. M., Kierzek R., Jaeger J. A., Sugimoto N., Caruthers M. H., Neilson T., Turner D. H. Improved free-energy parameters for predictions of RNA duplex stability. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9373–9377. doi: 10.1073/pnas.83.24.9373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gralla J., Crothers D. M. Free energy of imperfect nucleic acid helices. II. Small hairpin loops. J Mol Biol. 1973 Feb 5;73(4):497–511. doi: 10.1016/0022-2836(73)90096-x. [DOI] [PubMed] [Google Scholar]
  8. Groebe D. R., Uhlenbeck O. C. Characterization of RNA hairpin loop stability. Nucleic Acids Res. 1988 Dec 23;16(24):11725–11735. doi: 10.1093/nar/16.24.11725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gutell R. R., Larsen N., Woese C. R. Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev. 1994 Mar;58(1):10–26. doi: 10.1128/mr.58.1.10-26.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gutell R. R., Schnare M. N., Gray M. W. A compilation of large subunit (23S-like) ribosomal RNA sequences presented in a secondary structure format. Nucleic Acids Res. 1990 Apr 25;18 (Suppl):2319–2330. doi: 10.1093/nar/18.suppl.2319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gutell R. R., Weiser B., Woese C. R., Noller H. F. Comparative anatomy of 16-S-like ribosomal RNA. Prog Nucleic Acid Res Mol Biol. 1985;32:155–216. doi: 10.1016/s0079-6603(08)60348-7. [DOI] [PubMed] [Google Scholar]
  12. He L., Kierzek R., SantaLucia J., Jr, Walter A. E., Turner D. H. Nearest-neighbor parameters for G.U mismatches: [formula; see text] is destabilizing in the contexts [formula; see text] and [formula; see text] but stabilizing in [formula; see text]. Biochemistry. 1991 Nov 19;30(46):11124–11132. doi: 10.1021/bi00110a015. [DOI] [PubMed] [Google Scholar]
  13. Jaeger J. A., Turner D. H., Zuker M. Improved predictions of secondary structures for RNA. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7706–7710. doi: 10.1073/pnas.86.20.7706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. James B. D., Olsen G. J., Pace N. R. Phylogenetic comparative analysis of RNA secondary structure. Methods Enzymol. 1989;180:227–239. doi: 10.1016/0076-6879(89)80104-1. [DOI] [PubMed] [Google Scholar]
  15. Kieleczawa J., Dunn J. J., Studier F. W. DNA sequencing by primer walking with strings of contiguous hexamers. Science. 1992 Dec 11;258(5089):1787–1791. doi: 10.1126/science.1465615. [DOI] [PubMed] [Google Scholar]
  16. Kierzek R., Caruthers M. H., Longfellow C. E., Swinton D., Turner D. H., Freier S. M. Polymer-supported RNA synthesis and its application to test the nearest-neighbor model for duplex stability. Biochemistry. 1986 Dec 2;25(24):7840–7846. doi: 10.1021/bi00372a009. [DOI] [PubMed] [Google Scholar]
  17. Kim S. H., Cech T. R. Three-dimensional model of the active site of the self-splicing rRNA precursor of Tetrahymena. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8788–8792. doi: 10.1073/pnas.84.24.8788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kim S. H., Suddath F. L., Quigley G. J., McPherson A., Sussman J. L., Wang A. H., Seeman N. C., Rich A. Three-dimensional tertiary structure of yeast phenylalanine transfer RNA. Science. 1974 Aug 2;185(4149):435–440. doi: 10.1126/science.185.4149.435. [DOI] [PubMed] [Google Scholar]
  19. Leontis N. B., Kwok W., Newman J. S. Stability and structure of three-way DNA junctions containing unpaired nucleotides. Nucleic Acids Res. 1991 Feb 25;19(4):759–766. doi: 10.1093/nar/19.4.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lu M., Guo Q., Marky L. A., Seeman N. C., Kallenbach N. R. Thermodynamics of DNA branching. J Mol Biol. 1992 Feb 5;223(3):781–789. doi: 10.1016/0022-2836(92)90989-w. [DOI] [PubMed] [Google Scholar]
  21. Michel F., Westhof E. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol. 1990 Dec 5;216(3):585–610. doi: 10.1016/0022-2836(90)90386-Z. [DOI] [PubMed] [Google Scholar]
  22. Moazed D., Stern S., Noller H. F. Rapid chemical probing of conformation in 16 S ribosomal RNA and 30 S ribosomal subunits using primer extension. J Mol Biol. 1986 Feb 5;187(3):399–416. doi: 10.1016/0022-2836(86)90441-9. [DOI] [PubMed] [Google Scholar]
  23. Pan T., Gutell R. R., Uhlenbeck O. C. Folding of circularly permuted transfer RNAs. Science. 1991 Nov 29;254(5036):1361–1364. doi: 10.1126/science.1720569. [DOI] [PubMed] [Google Scholar]
  24. Peritz A. E., Kierzek R., Sugimoto N., Turner D. H. Thermodynamic study of internal loops in oligoribonucleotides: symmetric loops are more stable than asymmetric loops. Biochemistry. 1991 Jul 2;30(26):6428–6436. doi: 10.1021/bi00240a013. [DOI] [PubMed] [Google Scholar]
  25. Petersheim M., Turner D. H. Base-stacking and base-pairing contributions to helix stability: thermodynamics of double-helix formation with CCGG, CCGGp, CCGGAp, ACCGGp, CCGGUp, and ACCGGUp. Biochemistry. 1983 Jan 18;22(2):256–263. doi: 10.1021/bi00271a004. [DOI] [PubMed] [Google Scholar]
  26. Riesner D., Maass G., Thiebe R., Philippsen P., Zachau H. G. The conformational transitions in yeast tRNAPhe as studied with tRNAPhe fragments. Eur J Biochem. 1973 Jul 2;36(1):76–88. doi: 10.1111/j.1432-1033.1973.tb02887.x. [DOI] [PubMed] [Google Scholar]
  27. Robertus J. D., Ladner J. E., Finch J. T., Rhodes D., Brown R. S., Clark B. F., Klug A. Structure of yeast phenylalanine tRNA at 3 A resolution. Nature. 1974 Aug 16;250(467):546–551. doi: 10.1038/250546a0. [DOI] [PubMed] [Google Scholar]
  28. SantaLucia J., Jr, Kierzek R., Turner D. H. Context dependence of hydrogen bond free energy revealed by substitutions in an RNA hairpin. Science. 1992 Apr 10;256(5054):217–219. doi: 10.1126/science.1373521. [DOI] [PubMed] [Google Scholar]
  29. SantaLucia J., Jr, Kierzek R., Turner D. H. Stabilities of consecutive A.C, C.C, G.G, U.C, and U.U mismatches in RNA internal loops: Evidence for stable hydrogen-bonded U.U and C.C.+ pairs. Biochemistry. 1991 Aug 20;30(33):8242–8251. doi: 10.1021/bi00247a021. [DOI] [PubMed] [Google Scholar]
  30. Serra M. J., Lyttle M. H., Axenson T. J., Schadt C. A., Turner D. H. RNA hairpin loop stability depends on closing base pair. Nucleic Acids Res. 1993 Aug 11;21(16):3845–3849. doi: 10.1093/nar/21.16.3845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tinoco I., Jr, Uhlenbeck O. C., Levine M. D. Estimation of secondary structure in ribonucleic acids. Nature. 1971 Apr 9;230(5293):362–367. doi: 10.1038/230362a0. [DOI] [PubMed] [Google Scholar]
  32. Turner D. H., Sugimoto N., Freier S. M. RNA structure prediction. Annu Rev Biophys Biophys Chem. 1988;17:167–192. doi: 10.1146/annurev.bb.17.060188.001123. [DOI] [PubMed] [Google Scholar]
  33. Turner D. H., Sugimoto N., Jaeger J. A., Longfellow C. E., Freier S. M., Kierzek R. Improved parameters for prediction of RNA structure. Cold Spring Harb Symp Quant Biol. 1987;52:123–133. doi: 10.1101/sqb.1987.052.01.017. [DOI] [PubMed] [Google Scholar]
  34. Uhlenbeck O. C., Cameron V. Equimolar addition of oligoribonucleotides with T4 RNA ligase. Nucleic Acids Res. 1977 Jan;4(1):85–98. doi: 10.1093/nar/4.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wang Y. Y., Lyttle M. H., Borer P. N. Enzymatic and NMR analysis of oligoribonucleotides synthesized with 2'-tert-butyldimethylsilyl protected cyanoethylphosphoramidite monomers. Nucleic Acids Res. 1990 Jun 11;18(11):3347–3352. doi: 10.1093/nar/18.11.3347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wu T., Ogilvie K. K., Pon R. T. Prevention of chain cleavage in the chemical synthesis of 2'-silylated oligoribonucleotides. Nucleic Acids Res. 1989 May 11;17(9):3501–3517. doi: 10.1093/nar/17.9.3501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wyatt J. R., Puglisi J. D., Tinoco I., Jr RNA pseudoknots. Stability and loop size requirements. J Mol Biol. 1990 Jul 20;214(2):455–470. doi: 10.1016/0022-2836(90)90193-P. [DOI] [PubMed] [Google Scholar]
  38. Zuker M., Jaeger J. A., Turner D. H. A comparison of optimal and suboptimal RNA secondary structures predicted by free energy minimization with structures determined by phylogenetic comparison. Nucleic Acids Res. 1991 May 25;19(10):2707–2714. doi: 10.1093/nar/19.10.2707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zuker M. On finding all suboptimal foldings of an RNA molecule. Science. 1989 Apr 7;244(4900):48–52. doi: 10.1126/science.2468181. [DOI] [PubMed] [Google Scholar]

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