Conformational determinants of tandem GU mismatches in RNA: Insights from molecular dynamics simulations and quantum mechanical calculations

Biochemistry

Volumn 44, Issue 5, 2005, Pages 1433-1443

  Pan, Yongping ^a   Priyakumar, U Deva ^a   MacKerell Jr , Alexander D ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN BONDS; MOLECULAR DYNAMICS; RNA; THERMODYNAMIC STABILITY; THERMODYNAMICS;

BIOLOGICAL FUNCTIONS; MISMATCHES;

CONFORMATIONS;

RNA;

ARTICLE; BASE MISPAIRING; CONTROLLED STUDY; HYDROGEN BOND; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; QUANTUM MECHANICS; RNA SEQUENCE; RNA STRUCTURE; STRUCTURE ANALYSIS; TANDEM REPEAT; THERMOSTABILITY;

BASE PAIR MISMATCH; COMPUTER SIMULATION; DINUCLEOTIDE REPEATS; GUANINE; HYDROGEN BONDING; NUCLEIC ACID CONFORMATION; NUCLEIC ACID HETERODUPLEXES; QUANTUM THEORY; RNA; THERMODYNAMICS; URIDINE;

EID: 13444256246     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047932q     Document Type: Article

References (64)

1. Gautheret, D., Konings, D., and Gutell, R. R. (1995) G.U base pairing motifs in ribosomal RNA, RNA 1, 807-814.
2. Damberger, S. H., and Gutell, R. R. (1994) A comparative database of group I intron structures, Nucleic Acids Res. 22, 3508-3510.
3. Gutell, R. R. (1994) Collection of small subunit (16S- and 16S-like) ribosomal RNA structures: 1994, Nucleic Acids Res. 22, 3502-3507.
4. Rould, M. A., Perona, J. J., and Steitz, T. A. (1991) Structural basis of anticodon loop recognition by glutaminyl-tRNA synthetase, Nature 352, 213-218.
5. McClain, W. H., Chen, Y. M., Foss, K., and Schneider, J. (1988) Association of transfer RNA acceptor identity with a helical irregularity, Science 242, 1681-1684.
6. Gabriel, K., Schneider, J., and McClain, W. H. (1996) Functional evidence for indirect recognition of G.U in tRNA(Ala) by alanyl-tRNA synthetase, Science 271, 195-197.
7. Doudna, J. A., Cormack, B. P., and Szostak, J. W. (1989) RNA structure, not sequence, determines the 5′ splice-site specificity of a group I intron, Proc. Natl. Acad. Sci. U.S.A. 86, 7402-7406.
8. Simpson, L., and Thiemann, O. H. (1995) Sense from nonsense: RNA editing in mitochondria of kinetoplastid protozoa and slime molds, Cell 81, 837-840.
9. Wu, M., McDowell, J. A., and Turner, D. H. (1995) A periodic table of symmetric tandem mismatches in RNA, Biochemistry 34, 3204-3211.
10. 2, Biochemistry 39, 8970-8982.
11. Allawi, H. T., and SantaLucia, J., Jr. (1997) Thermodynamics and NMR of internal G·T mismatches in DNA, Biochemistry 36, 10581-10594.
12. Tanaka, Y., Kojima, C., Yamazaki, T., Kodama, T. S., Yasuno, K., Miyashita, S., Ono, A., Kainosho, M., and Kyogoku, Y. (2000) Solution structure of an RNA duplex including a C-U base pair, Biochemistry 39, 7074-7080.
13. 2, Biochemistry 36, 8030-8038.
14. 2 by two-dimensional NMR and simulated annealing, Biochemistry 35, 14077-14089.
15. 2 and determinants of stability for single guanosine-guanosine base pairs, Biochemistry 39, 11748-11762.
16. Matthews, 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.
17. Saenger, W. (1984) Principles of Nucleic Acid Structure, Springer-Verlag, New York.
18. Zhu, J., and Wartell, R. M. (1997) The relative stabilities of base pair stacking interactions and single mismatches in long RNA measured by temperature gradient gel electrophoresis, Biochemistry 36, 15326-15335.
19. 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.
20. Martinez, H. M. (1990) Detecting pseudoknots and other local base-pairing structures in RNA sequences, Methods Enzymol. 183, 306-317.
21. Zuker, M. (1989) On finding all suboptimal foldings of an RNA molecule, Science 244, 48-52.
22. Gultyaev, A. P., van Batenburg, F. H., and Pleij, C. W. (1995) The computer simulation of RNA folding pathways using a genetic algorithm, J. Mol. Biol. 250, 37-51.
23. Walter, A. E., Turner, D. H., Kim, J., Lyttle, M. H., Muller, P., Mathews, D. H., and Zuker, M. (1994) Coaxial stacking of helixes enhances binding of oligoribonucleotides and improves predictions of RNA folding, Proc. Natl. Acad. Sci. U.S.A. 91, 9218-9222.
24. He, L., Kierzek, R., SantaLucia, J., Jr., Walter, A. E., and Turner, D. H. (1991) Nearest-neighbor parameters for G·U mismatches: 5′GU3′ is destabilizing in the contexts CGUG, UGUA, and AGUU but stabilizing in GGUC, Biochemistry 30, 11124-11132.
25. Manning, G. S. (1978) The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides, Q. Rev. Biophys. 11, 179-246.
26. Record, M. T., Jr., Anderson, C. F., and Lohman, T. M. (1978) Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening, and ion effects on water activity, Q. Rev. Biophys. 11, 103-178.
27. MacKerell, A. D., Jr., and Nilsson, L. (2001) in Computational Biochemistry and Biophysics (Becker, O. M., MacKerell, A. D., Jr., Roux, B., and Watanabe, M., Eds.) pp 441-463, Marcel Dekker, Inc., New York.
28. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S., and Karplus, M. (1983) CHARMM: a program for macromolecular energy, minimization, and dynamics calculations, J. Comput. Chem. 4, 187-217.
29. Foloppe, N., and MacKerell, A. D., Jr. (2000) All-atom empirical force field for nucleic acids. 1. Parameter optimization based on small molecule and condensed phase macromolecular target data, J. Comput. Chem. 21, 86-104.
30. Foloppe, N., Nilsson, L., and MacKerell, A. D., Jr. (2001) Ab initio conformational analysis of nucleic acid components: intrinsic energetic contributions to nucleic acid structure and dynamics, Biopolymers 61, 61-76.
31. Beglov, D., and Roux, B. (1997) Finite representation of an infinite bulk system: solvent boundary potential for computer simulations, J. Chem. Phys. 100, 9050-9063.
32. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water, J. Chem. Phys. 79, 926-935.
33. Arnott, S., and Hukins, D. W. (1973) Refinement of the structure of B-DNA and implications for the analysis of X-ray diffraction data from fibers of biopolymers, J. Mol. Biol. 81, 93-105.
34. Quanta (2001) Accelrys Inc., San Diego, CA.
35. Field, M. J., and Karplus, M. (1992) CRSTAL: Program for crystal calculations in CHARMM, Harvard University, Cambridge, MA.
36. Ryckaert, J., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of n-Alkanes, J. Comput. Phys. 23, 327-341.
37. Darden, T., Perera, L., Li, L., and Pedersen, L. (1999) New tricks for modelers from the crystallography toolkit: the particle mesh Ewald algorithm and its use in nucleic acid simulations, Struct. Fold Des. 7, R55-R60.
38. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T. A., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh ewald method, J. Chem. Phys. 103, 8577-8593.
39. Steinbach, P. J., and Brooks, B. R. (1994) New Spherical-Cutoff Methods of Long-Range Forces in Macromolecular Simulations, J. Comput. Chem. 15, 667-683.
40. Hoover, W. G. (1985) Canonical dynamics: equilibrium phase-space distributions, Phys. Rev. A 31, 1695-1697.
41. Feller, S. E., Zhang, Y., Pastor, R. W., and Brooks, R. W. (1995) Constant pressure molecular dynamics simulations: the Langevin piston method, J. Chem. Phys. 103, 4613-4621.
42. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Jr., Stratmann, R. E., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Strain, M. C., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, G. A., Ayala, P. Y., Cui, Q., Morokuma, K., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Baboul, A. G., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Gomperts, R., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Gonzalez, C., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Andres, J. L., Gonzalez, C., Head-Gordon, M., Replogle, E. S., and Pople, J. A. (1998) Gaussian 98, revision A.6, Gaussian, Inc., Pittsburgh, PA.
43. Woon, D. E., and Dunning, T. H., Jr. (1993) Gaussian basis sets for use in correlated molecular calculations. III. The atoms aluminum through argon, J. Chem. Phys. 98, 1358-1371.
44. Møller, C., and Plesset, M. S. (1934) Note on an Approximation Treatment for Many-Electron Systems, Phys. Rev. 46, 618-622.
45. Saebø, S., Tong, W., and Pulay, P. (1993) Efficient elimination of basis set superposition error by the local correlation method: Accurate ab inito calculations of the water dimer, J. Chem. Phys. 98, 2170-2175.
46. Hobza, P., and Sponer, J. (2002) Toward True DNA Base-Stacking Energies: MP2, CCSD(T), and Complete Basis Set Calculations, J. Am. Chem. Soc. 124, 11802-11808.
47. Hobza, P., and Sponer, J. (1999) Structure, Energetics and Dynamics of the Nucleic Acid Base Pairs: Nonempirical Ab initio Calculations, Chem. Rev. 99, 3247-3276.
48. Boys, S. F., and Bernardi, F. (1970) The Calculation of Small Molecular Interaction by the Differences of Separate Total Energies. Some Procedures with Reduced Errors, Mol. Phys. 19, 553-566.
49. Arnott, S., Hukins, D. W. L., Dover, S. D., Fuller, W., and Hodgson, A. R. (1973) Structures of Synthetic Polynucleotides in the A-RNA and A′-RNA Conformations: X-ray Diffraction Analyses of the Molecular Conformations of Polyadenylic acid-polyuridic acid and Polyinosinic acid-polycytidylic acid, J. Mol. Biol. 81, 102-122.
50. Biswas, R., Wahl, M. C., Ban, C., and Sundaralingam, M. (1997) Crystal structure of an alternating octamer r(GUAUGUA)dC with adjacent G x U wobble pairs, J. Mol. Biol. 267, 1149-1156.
51. Kneale, G., Brown, T., Kennard, O., and Rabinovich, D. (1985) G. T base-pairs in a DNA helix: the crystal structure of d(G-G-G-G-T-C-C-C), J. Mol. Biol. 186, 805-814.
52. 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.
53. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules, J. Am. Chem. Soc. 117, 5179-5197.
54. Calladine, C. R. (1982) Mechanics of Sequence-dependent Stacking of Bases in B-DNA, J. Mol. Biol. 161, 343-352.
55. 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.
56. Marky, L. A., and Breslauer, K. J. (1982) Calorimetric Determination of Base-Stacking Enthalpies in Double-Helical DNA Molecules, Biopolymers 21, 2185-2194.
57. Yang, J. T., and Gellman, S. H. (1998) Energetic Superiority of Two-Center Hydrogen Bonding Relative to Three-Center Hydrogen Bonding in a Model System. J. Am. Chem. Soc. 120, 9090-9091.
58. Huang, N., and MacKerell, A. D., Jr. (2002) An Ab Initio Quantum Mechanical Study of Hydrogen-Bonded Complexes of Biological Interest, J. Phys. Chem. B 106, 7820-7827.
59. Rappé, A. K., and Bernstein, E. R. (2000) Ab Initio Calculation of Nonbonded Interactions: Are We There Yet?, J. Phys. Chem. A 104, 6117-6128.
60. Sinnokrot, M. O., Valeev, E., and Sherril, C. D. (2002) Estimates of the Ab Initio Limit for π-π Interactions: The Benzene Dimer, J. Am. Chem. Soc. 124, 10887-10893.
61. Leininger, M. L., Nielsen, I. M. B., Colvin, M. E., and Janssen, C. L. (2002) Accurate Structures and Binding Energies for Stacked Uracil Dimers, J. Phys. Chem. A 106, 3850-3854.
62. Lee, B., and Richards, F. M. (1971) The Interpretation of Protein Structures: Estimation of Static Accessibility, J. Mol. Biol. 55, 379-400.
63. Sahasrabudhe, P. V., and Gmeiner, W. H. (1997) Solution Structures of 5-Fluorouracil-Substituted RNA Duplexes Containing G-U Wobble Base Pairs, Biochemistry 36, 5981-5991.
64. Gutell, R. R., Gray, M. W., and Schnare, M. N. (1993) A compilation of large subunit (23S and 23S-like) ribosomal RNA structures: 1993, Nucleic Acids Res. 21, 3055-3074.