Thermodynamic characterization of the complete set of sequence symmetric tandem mismatches in RNA and an improved model for predicting the free energy contribution of sequence asymmetric tandem mismatches

Biochemistry

Volumn 47, Issue 14, 2008, Pages 4329-4336

  Christiansen, Martha E ^a   Znosko, Brent M ^a  

^a Saint Louis University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FREE ENERGY; PARAMETER ESTIMATION; THERMODYNAMICS;

ASYMMETRIC TANDEM; RNA SECONDARY STRUCTURE; THERMODYNAMIC PARAMETERS;

RNA;

PROTEIN; RNA;

AMINO ACID SEQUENCE; ARTICLE; BASE MISPAIRING; BASE PAIRING; ENERGY TRANSFER; GENE SEQUENCE; MISMATCH REPAIR; MOLECULAR MODEL; PREDICTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; RNA GENE; RNA STRUCTURE; THERMODYNAMICS;

BASE PAIR MISMATCH; BASE SEQUENCE; MODELS, GENETIC; NUCLEIC ACID CONFORMATION; RNA; THERMODYNAMICS;

SABINA;

EID: 41849129277     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7020876     Document Type: Article

References (45)

1. 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.
2. Gutell, R. R. (1994) Collection of small-subunit (16s- and 16s-like) ribosomal-RNA structures-1994. Nucleic Acids Res. 22, 3502-3507.
3. 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 angstrom resolution. Science 289, 905-920.
4. Gutell, R. R., Gray, M. W., and Schnare, M. N. (1993) A compilation of large subunit (23s-like and 23s-like) ribosomal-RNA structures-1993. Nucleic Acids Res. 21, 3055-3074.
5. Gutell, R. R., and Woese, C. R. (1990) Higher order structural elements in ribosomal RNAs: Pseudo-knots and the use of noncanonical pairs. Proc. Natl. Acad. Sci. U.S.A. 87, 663-667.
6. Shi, P. Y., Brinton, M. A., Veal, J. M., Zhong, Y. Y., and Wilson, W. D. (1996) Evidence for the existence of a pseudoknot structure at the 3′ terminus of the flavivirus genomic RNA. Biochemistry 35, 4222-4230.
7. Disney, M. D., Haidaris, C. G., and Turner, D. H. (2001) Recognition elements for 5′ exon substrate binding to the Candida albicans group I intron. Biochemistry 40, 6507-6519.
8. DeNap, J. C. B., Thomas, J. R., Musk, D. J., and Hergenrother, P. J. (2004) Combating drug-resistant bacteria: Small molecule mimics of plasmid incompatibility as antiplasmid compounds. J. Am. Chem. Soc. 126, 15402-15404.
9. Zhang, J. C., Zhang, G. H., Guo, R., Shapiro, B. A., and Simon, A. E. (2006) A pseudoknot in a preactive form of a viral RNA is part of a structural switch activating minus-strand synthesis. J. Virol. 80, 9181-9191.
10. Sobczak, K., de Mezer, M., Michlewski, G., Krol, J., and Krzyzosiak, W. J. (2003) RNA structure of trinucleotide repeats associated with human neurological diseases. Nucleic Acids Res. 31, 5469-5482.
11. Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., Smith, H. O., Yandell, M., Evans, C. A., Holt, R. A., Gocayne, J. D., Amanatides, P., Ballew, R. M., Huson, D. H., Wortman, J. R., Zhang, Q., Kodira, C. D., Zheng, X. Q. H., Chen, L., Skupski, M., Subramanian, G., Thomas, P. D., Zhang, J. H., Miklos, G. L. G., Nelson, C., Broder, S., Clark, A. G., Nadeau, C., McKusick, V. A., Zinder, N., Levine, A. J., Roberts, R. J., Simon, M., Slayman, C., Hunkapiller, M., Bolanos, R., Delcher, A., Dew, I., Fasulo, D., Flanigan, M., Florea, L., Halpern, A., Hannenhalli, S., Kravitz, S., Levy, S., Mobarry, C., Reinert, K., Remington, K., Abu-Threideh, J., Beasley, E., Biddick, K., Bonazzi, V., Brandon, R., Cargill, M., Chandramouliswaran, I., Charlab, R., Chaturvedi, K., Deng, Z. M., Di Francesco, V., Dunn, P., Eilbeck, K., Evangelista, C., Gabrielian, A. E., Gan, W., Ge, W. M., Gong, F. C., Gu, Z. P., Guan, P., Heiman, T. J., Higgins, M. E., Ji, R. R., Ke, Z. X., Ketchum, K. A., Lai, Z. W., Lei, Y. D., Li, Z. Y., Li, J. Y., Liang, Y., Lin, X. Y., Lu, F., Merkulov, G. V., Milshina, N., Moore, H. M., Naik, A. K., Narayan, V. A., Neelam, B., Nusskern, D., Rusch, D. B., Salzberg, S., Shao, W., Shue, B. X., Sun, J. T., Wang, Z. Y., Wang, A. H., Wang, X., Wang, J., Wei, M. H., Wides, R., Xiao, C. L., Yan, C. H., et al. (2001) The sequence of the human genome. Science 291, 1304.
12. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., Funke, R., Gage, D., Harris, K., Heaford, A., Howland, J., Kann, L., Lehoczky, J., LeVine, R., McEwan, P., McKernan, K., Meldrim, J., Mesirov, J. P., Miranda, C., Morris, W., Naylor, J., Raymond, C., Rosetti, M., Santos, R., Sheridan, A., Sougnez, C., Stange-Thomann, N., Stojanovic, N., Subramanian, A., Wyman, D., Rogers, J., Sulston, J., Ainscough, R., Beck, S., Bentley, D., Burton, J., Clee, C., Carter, N., Coulson, A., Deadman, R., Deloukas, P., Dunham, A., Dunham, I., Durbin, R., French, L., Grafham, D., Gregory, S., Hubbard, T., Humphray, S., Hunt, A., Jones, M., Lloyd, C., McMurray, A., Matthews, L., Mercer, S., Milne, S., Mullikin, J. C., Mungall, A., Plumb, R., Ross, M., Shownkeen, R., Sims, S., Waterston, R. H., Wilson, R. K., Hillier, L. W., McPherson, J. D., Marra, M. A., Mardis, E. R., Fulton, L. A., Chinwalla, A. T., Pepin, K. H., Gish, W. R., Chissoe, S. L., Wendl, M. C., Delehaunty, K. D., Miner, T. L., Delehaunty, A., Kramer, J. B., Cook, L. L., Fulton, R. S., Johnson, D. L., Minx, P. J., Clifton, S. W., Hawkins, T., Branscomb, E., Predki, P., Richardson, P., Wenning, S., Slezak, T., Doggett, N., Cheng, J. F., Olsen, A., Lucas, S., Elkin, C., Uberbacher, E., Frazier, M., et al. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860-921.
13. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., and Wheeler, D. L. (2007) GenBank. Nucleic Acids Res. 35, D21-D25.
14. Mathews, D. H., Disney, M. D., Childs, J. C., 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.
15. Lu, Z. J., Turner, D. H., and Mathews, D. H. (2006) A set of nearest neighbor parameters for predicting the enthalpy change of RNA secondary structure formation. Nucleic Acids Res. 34, 4912-4924.
16. Zuker, M. (1989) On finding all suboptimal foldings of an RNA molecule. Science 244, 48-52.
17. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415.
18. Hofacker, I. L. (2003) Vienna RNA secondary structure server. Nucleic Acids Res. 31, 3429-3431.
19. ISI Web of Knowledge, version 3.0, Thomson Corp., Stamford, CT. http://portal.isiknoweldge.com/portal.cgi (accessed October 2007).
20. Wu, M., McDowell, J. A., and Turner, D. H. (1995) A periodic table of symmetric tandem mismatches in RNA. Biochemistry 34, 3204-3211.
21. 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.
22. 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.
23. Schroeder, S. J., Burkard, M. E., and Turner, D. H. (2001) The energetics of small internal loops in RNA. Biopolymers 52, 157-167.
24. Xia, T. B., 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.
25. SantaLucia, J., Jr., Kierzek, R., and Turner, D. H. (1991) 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 30, 8242-8251.
26. 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.
27. 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.
28. 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.
29. Schroeder, S. J., and Turner, D. H. (2001) Thermodynamic stabilities of internal loops with GU closing pairs in RNA. Biochemistry 40, 11509-11517.
30. Sugimoto, N., Kierzek, R., and Turner, D. H. (1987) Sequence dependence for the energetics of dangling ends and terminal base pairs in ribonucleic acid. Biochemistry 26, 4554-4558.
31. 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.
32. Freier, S. M., Sinclair, A., Nielson, T., and Turner, D. H. (1985) Improved free energies for G-C base pairs. J. Mol. Biol. 185, 645-647.
33. Freier, S. M., Kierzek, R., Jaeger, J. A., Sugimoto, N., Caruthers, M. H., Neilson, T., and Turner, D. H. (1986) Improved free energy parameters for predictions of RNA duplex stability. Proc. Natl. Acad. Sci. U.S.A. 83, 9373-9377.
34. He, L., Kierzek, R., SantaLucia, J., Jr., Walter, A. E., and Turner, D. H. (1991) Nearest neighbor parameters for G-U mismatches: 5′GU3′/ 3′UG5′ is destabilizing in the contexts CGUG/GUGC, UGUA/AUGU, and AGUU/UUGA but stabilizing in GGUC/CUGG. Biochemistry 30, 11124-11132.
35. 2 by two-dimensional NMR and simulated annealing. Biochemistry 35, 14077-14089.
36. 2. Biochemistry 36, 8030-8038.
37. Wright, D. J., Rice, J. L., Yanker, D. M., and Znosko, B. M. (2007) Nearest neighbor parameters for inosine-uridine pairs in RNA duplexes. Biochemistry 46, 4625-4634.
38. Davis, A. R., and Znosko, B. M. (2007) Thermodynamic characterization of single mismatches found in naturally occurring RNA. Biochemistry 46, 13425-13436.
39. Badhwar, J., Karri, S., Cass, C. K., Wunderlich, E. L., and Znosko, B. M. (2007) Thermodynamic characterization of RNA duplexes containing naturally occurring 1 x 2 nucleotide internal loops. Biochemistry 46, 14715-14724.
40. McDowell, J. A. (1995) RNA Calculations, version 1.1.
41. McDowell, J. A. (1996) MeltWin, version 3.5 (Melt Curve Processing Program). This program is available for download at www.meltwin.com.
42. 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.
43. Borer, P. N., Dengler, B., Tinoco, I., and Uhlenbeck, O. (1974) Stability of ribonucleic-acid double-stranded helices. J. Mol. Biol. 86, 843-853.
44. Marky, L. A., and Breslauer, K. J. (1987) Calculating thermodynamic data for transitions of any molecularity from equilibrium melting curves. Biopolymers 26, 1601-1620.
45. Shankar, N., Xia, T., Kennedy, S. D., Krugh, T. R., Mathews, D. H., and Turner, D. H. (2007) NMR reveals the absence of hydrogen bonding in adjacent UU and AG mismatches in an isolated internal loop from ribosomal RNA. Biochemistry 46, 12665-12678.