Cations and hydration in catalytic RNA: Molecular dynamics of the hepatitis delta virus ribozyme

Biophysical Journal

Volumn 91, Issue 2, 2006, Pages 626-638

  Krasovska, Maryna V ^a   Sefcikova, Jana ^b   Réblová, Kamila ^a,c   Schneider, Bohdan ^d   Walter, Nils G ^b   Šponer, Jiří ^a  

^a INSTITUTE OF BIOPHYSICS   (Czech Republic)

^b UNIVERSITY OF MICHIGAN   (United States)

^c MASARYK UNIVERSITY   (Czech Republic)

^d INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

CATION; DIVALENT CATION; MAGNESIUM; MONOVALENT CATION; RIBOZYME; SODIUM;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; HEPATITIS DELTA VIRUS; HYDRATION; MOLECULAR DYNAMICS; PROTON TRANSPORT;

HEPATITIS DELTA VIRUS;

EID: 33745700326     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.079368     Document Type: Article

References (79)

1. Lai, M. M. 1995. The molecular biology of hepatitis delta virus. Annu. Rev. Biochem. 64:259-286.
2. Perrotta, A. T., I. Shih, and M. D. Been. 1999. Imidazole rescue of a cytosine mutation in a self-cleaving ribozyme. Science. 286:123-126.
3. Nakano, S., D. M. Chadalavada, and P. C. Bevilacqua. 2000. General acid-base catalysis in the mechanism of a hepatitis delta virus ribozyme. Science. 287:1493-1497.
4. Ferre-D'Amare, A. R., K. Zhou, and J. A. Doudna. 1998. Crystal structure of a hepatitis delta virus ribozyme. Nature. 395:567-574.
5. Ferre-D'Amare, A. R., K. Zhou, and J. A. Doudna. 1998. A general module for RNA crystallization. J. Mol. Biol. 279:621-631.
6. Ke, A., K. Zhou, F. Ding, J. H. Cate, and J. A. Doudna. 2004. A conformational switch controls hepatitis delta virus ribozyme catalysis. Nature. 429:201-205.
7. Das, S. R., and J. A. Piccirilli. 2005. General acid catalysis by the hepatitis delta virus ribozyme. Nat. Chem. Biol. 1:45-52.
8. Nakano, S., D. J. Proctor, and P. C. Bevilacqua. 2001. Mechanistic characterization of the HDV genomic ribozyme: assessing the catalytic and structural contributions of divalent metal ions within a multichannel reaction mechanism. Biochemistry. 40:12022-12038.
9. Nakano, S., A. L. Cerrone, and P. C. Bevilacqua. 2003. Mechanistic characterization of the HDV genomic ribozyme: classifying the catalytic and structural metal ion sites within a multichannel reaction mechanism. Biochemistry. 42:2982-2994.
10. Pyle, A. M. 2002. Metal ions in the structure and function of RNA. J. Biol. Inorg. Chem. 7:679-690.
11. Hanna, R., and J. A. Doudna. 2000. Metal ions in ribozyme folding and catalysis. Curr. Opin. Chem. Biol. 4:166-170.
12. Murray, J. B., A. A. Seyhan, N. G. Walter, J. M. Burke, and W. G. Scott. 1998. The hammerhead, hairpin and VS ribozymes are catalytically proficient in monovalent cations alone. Chem. Biol. 5:587-595.
13. Perrotta, A. T., and M. D. Been. 1990. The self-cleaving domain from the genomic RNA of hepatitis delta virus: sequence requirements and the effects of denaturant. Nucleic Acids Res. 18:6821-6827.
14. Kawakami, J., P. K. Kumar, Y. A. Suh, F. Nishikawa, K. Kawakami, K. Taira, E. Ohtsuka, and S. Nishikawa. 1993. Identification of important bases in a single-stranded region (SSrC) of the hepatitis delta (delta) virus ribozyme. Eur. J. Biochem. 217:29-36.
15. Ferre-D'Amare, A. R., and J. A. Doudna. 2000. Crystallization and structure determination of a hepatitis delta virus ribozyme: use of the RNA-binding protein U1A as a crystallization module. J. Mol. Biol. 295:541-556.
16. 2+ binding in the group I intron core. J. Mol. Biol. 329:229-238.
17. Draper, D. E., D. Grilley, and A. M. Soto. 2005. Ions and RNA folding. Annu. Rev. Biophys. Biomol. Struct. 34:221-243.
18. Ennifar, E., P. Walter, and P. Dumas. 2003. A crystallographic study of the binding of 13 metal ions to two related RNA duplexes. Nucleic Acids Res. 32:2671-2682.
19. Auffinger, P., L. Bielecki, and E. Westhof. 2004. Anion binding to nucleic acids. Structure. 12:379-388.
20. Reblova, K., N. Spackova, J. E. Sponer, J. Koca, and J. Sponer. 2003. Molecular dynamics simulations of RNA kissing-loop motifs reveal structural dynamics and formation of cation-binding pockets. Nucleic Acids Res. 31:6942-6952.
21. 2+)-containing solutions. J. Am. Chem. Soc. 123:11333-11334.
22. Shih, I. H., and M. D. Been. 1999. Ribozyme cleavage of a 2,5-phosphodiester linkage: mechanism and a restricted divalent metal-ion requirement. RNA. 5:1140-1148.
23. Shih, I. H., and M. D. Been. 2002. Catalytic strategies of the hepatitis delta virus ribozymes. Annu. Rev. Biochem. 71:887-917.
24. Westhof, E. 1988. Water: An integral part of nucleic acid structure. Annu. Rev. Biophys. Biophys. Chem. 17:125-144.
25. Schneider, B., K. Patel, and H. M. Berman. 1998. Hydration of the phosphate group in double-helical DNA. Biophys. J. 75:2422-2434.
26. Auffinger, P., and E. Westhof. 2001. RNA solvation: A molecular dynamics simulation perspective. Biopolymers. 56:266-274.
27. Schneider, C., M. Brandl, and J. Suhnel. 2001. Molecular dynamics simulation reveals conformational switching of water-mediated uracil-cytosine base-pairs in an RNA duplex. J. Mol. Biol. 305:659-667.
28. Brandl, M., M. Meyer, and J. Suhnel. 2000. Water-mediated base pairs in RNA: A quantum-chemical study. J. Phys. Chem. A. 104:11177-11187.
29. Reblova, K., N. Spackova, J. Koca, N. B. Leontis, and J. Sponer. 2004. Long-residency hydration, cation binding, and dynamics of loop E/helix IV rRNA-L25 protein complex. Biophys. J. 87:3397-3412.
30. Csaszar, K., N. Spackova, R. Stefl, J. Sponer, and N. B. Leontis. 2001. Molecular dynamics of the frame-shifting pseudoknot from beet western yellows virus: the role of non-Watson-Crick base-pairing, ordered hydration, cation binding and base mutations on stability and unfolding. J. Mol. Biol. 313:1073-1091.
31. Guo, J. X., and W. H. Gmeiner. 2001. Molecular dynamics simulation of the human U2B″ protein complex with U2 snRNA hairpin IV in aqueous solution. Biophys. J. 81:630-642.
32. Reblova, K., N. Spackova, R. Stefl, K. Csaszar, J. Koca, N. B. Leontis, and J. Sponer. 2003. Non-Watson-Crick basepairing and hydration in RNA motifs: molecular dynamics of 5S rRNA loop E. Biophys. J. 84:3564-3582.
33. Spackova, N., T. E. Cheatham, F. Ryjacek, F. Lankas, L. van Meervelt, P. Hobza, and J. Sponer. 2003. Molecular dynamics simulations and thermodynamics analysis of DNA-drug complexes. Minor groove binding between 4′,6-diamidino-2-phenylindole and DNA duplexes in solution. J. Am. Chem. Soc. 125:1759-1769.
34. Razga, F., J. Koca, J. Sponer, and N. B. Leontis. 2005. Hinge-like motions in RNA kink-turns: The role of the second A-minor motif and nominally unpaired bases. Biophys. J. 88:3466-3485.
35. Razga, F., N. Spackova, K. Reblova, J. Koca, N. B. Leontis, and J. Sponer. 2004. Ribosomal RNA kink-turn motif-a flexible molecular hinge. J. Biomol. Struct. Dyn. 22:183-194.
36. Auffinger, P., L. Bielecki, and E. Westhof. 2004. Symmetric K+ and Mg2+ ion-binding sites in the 5S rRNA loop E inferred from molecular dynamics simulations. J. Mol. Biol. 335:555-571.
37. Krasovska, M. V., J. Sefcikova, N. Spackova, J. Sponer, and N. G. Walter. 2005. Structural dynamics of precursor and product of the RNA enzyme from the hepatitis delta virus as revealed by molecular dynamics simulations. J. Mol. Biol. 351:731-748.
38. Accelrys Software, I. 1997. InsightII. San Diego, CA.
39. Gresh, N., J. E. Sponer, N. Spackova, J. Leszczynski, and J. Sponer. 2003. Theoretical study of binding of hydrated Zn(II) and Mg(II) cations to 5′-guanosine monophosphate. Toward polarizable molecular mechanics for DNA and RNA. J. Phys. Chem. B. 107:8669-8681.
40. Varnai, P., and K. Zakrzewska. 2004. DNA and its counterions: a molecular dynamics study. Nucleic Acids Res. 32:4269-4280.
41. Wadkins, T. S., I. Shih, A. T. Perrotta, and M. D. Been. 2001. A pH-sensitive RNA tertiary interaction affects self-cleavage activity of the HDV ribozymes in the absence of added divalent metal ion. J. Mol. Biol. 305:1045-1055.
42. Case, D. A., D. A. Pearlman, J. W. Caldwell, T. E. Cheathan III, J. Wang, W. S. Ross, C. L. Simmerling, T. A. Darden, K. M. Merz, R. V. Stanton, A. L. Cheng, J. J. Vincent, M. Crowley, V. Tsui, H. Gohlke, R. J. Radmer, Y. Duan, J. Pitera, I. Massova, G. L. Seibel, U. C. Singh, P. K. Weiner, and P. A. Kollman. 2002. AMBER 7:2002. University of California, San Francisco, San Francisco, CA.
43. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1995. A 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J. Am. Chem. Soc. 117:5179-5197.
44. Wang, J. M., P. Cieplak, and P. A. Kollman. 2000. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21:1049-1074.
45. Cheatham, T.E., P. Cieplak, and P.A. Kollman. 1999. A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J. Biomol. Struct. Dyn. 16:845-862.
46. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
47. Aqvist, J. 1990. Ion water interaction potentials derived from free-energy perturbation simulations. J. Phys. Chem. 94:8021-8024.
48. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8593.
49. Berendsen, H. J. C., J. P. M. Postma, W. F. Vangunsteren, A. Dinola, and J. R. Haak. 1984. Molecular-dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
50. DeLano, W. L. 2002. The PyMOL Molecular Graphics System.
51. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: Visual molecular dynamics. J. Mol. Graph. 14:33-38.
52. Schneider, B., and H. M. Berman. 1995. Hydration of the DNA bases is local. Biophys. J. 69:2661-2669.
53. McRee, D. E. 1999. XtalView/Xfit - A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125:156-165.
54. Gilson, M. K., K. A. Sharp, and B. H. Honig. 1988. Calculating the electrostatic potential of molecules in solution - method and error assessment. J. Comput. Chem. 9:327-335.
55. Schneider, B., Z. Moravek, and H. M. Berman. 2004. RNA conformational classes. Nucleic Acids Res. 32:1666-1677.
56. 2+ in water. J. Am. Chem. Soc. 121:3175-3184.
57. Markham, G. D., J. P. Glusker, and C. W. Bock. 2002. The arrangement of first- and second-sphere water molecules in divalent magnesium complexes: Results from molecular orbital and density functional theory and from structural crystallography. J. Phys. Chem. B. 106:5118-5134.
58. Misra, V. K., and D. E. Draper. 1998. On the role of magnesium ions in RNA stability. Biopolymers. 48:113-135.
59. Misra, V. K., and D. E. Draper. 2002. The linkage between magnesium binding and RNA folding. J. Mol. Biol. 317:507-521.
60. Burgess, J. M. 1988. Ions in Solution. Ellis Horwood, Chichester, UK.
61. Auffinger, P., L. Bielecki, and E. Westhof. 2003. The Mg2+ binding sites of the 5S rRNA loop E motif as investigated by molecular dynamics simulations. Chem. Biol. 10:551-561.
62. Tanner, N. K., S. Schaff, G. Thill, E. Petit-Koskas, A. M. Crain-Denoyelle, and E. Westhof. 1994. A three-dimensional model of hepatitis delta virus ribozyme based on biochemical and mutational analyses. Curr. Biol. 4:488-498.
63. Leontis, N. B., J. Stombaugh, and E. Westhof. 2002. The non-Watson-Crick base pairs and their associated isostericity matrices. Nucleic Acids Res. 30:3497-3531.
64. Rueda, M., E. Cubero, C. A. Laughton, and M. Orozco. 2004. Exploring the counterion atmosphere around DNA: What can be learned from molecular dynamics simulations? Biophys. J. 87:800-811.
65. Matysiak, M., J. Wrzesinski, and J. Ciesiolka. 1999. Sequential folding of the genomic ribozyme of the hepatitis delta virus: structural analysis of RNA transcription intermediates. J. Mol. Biol. 291:283-294.
66. Lafontaine, D. A., S. Ananvoranich, and J. P. Perreault. 1999. Presence of a coordinated metal ion in a trans-acting antigenomic delta ribozyme. Nucleic Acids Res. 27:3236-3243.
67. Jeong, S., J. Sefcikova, R. A. Tinsley, D. Rueda, and N. G. Walter. 2003. Trans-acting hepatitis delta virus ribozyme: catalytic core and global structure are dependent on the 5′ substrate sequence. Biochemistry. 42:7727-7740.
68. Harris, D. A., R. A. Tinsley, and N. G. Walter. 2004. Terbium-mediated footprinting probes a catalytic conformational switch in the antigenomic hepatitis delta virus ribozyme. J. Mol. Biol. 341:389-403.
69. Pallan, P. S., W. S. Marshall, J. Harp, F. C. Jewett, Z. Wawrzak, B. A. Brown, A. Rich, and M. Egli. 2005. Crystal structure of a luteoviral RNA pseudoknot and model for a minimal ribosomal frameshifting motif. Biochemistry. 44:11315-11322.
70. Yaremchuk, A., M. Tukalo, M. Grotli, and S. Cusack. 2001. A succession of substrate induced conformational changes ensures the amino acid specificity of Thermus thermophilus prolyl-tRNA synthetase: Comparison with histidyl-tRNA synthetase. J. Mol. Biol. 309:989-1002.
71. Nissen, P., J. A. Ippolito, N. Ban, P. B. Moore, and T. A. Steitz. 2001. RNA tertiary interactions in the large ribosomal subunit: The A-minor motif. Proc. Natl. Acad. Sci. USA. 98:4899-4903.
72. Sponer, J., H. A. Gabb, J. Leszczynski, and P. Hobza. 1997. Base-base and deoxyribose-base stacking interactions in B-DNA and Z-DNA: A quantum-chemical study. Biophys. J. 73:76-87.
73. Barone, F., F. Lankas, N. Spackova, J. Sponer, P. Karran, M. Bignami, and F. Mazzei. 2005. Structural and dynamic effects of single 7-hydro-8-oxoguanine bases located in a frameshift target DNA sequence. Biophys. Chem. 118:31-41.
74. Beveridge, D. L., G. Barreiro, K. S. Byun, D. A. Case, T. E. Cheatham, S. B. Dixit, E. Giudice, F. Lankas, R. Lavery, and J. H. Maddocks. 2004. Molecular dynamics simulations of the 136 unique tetranucleotide sequences of DNA oligonucleotides. I. Research design and results on d(C(p)G) steps. Biophys. J. 87:3799-3813.
75. Fadrna, E., N. Spackova, R. Stefl, J. Koca, T. E. Cheatham, and J. Sponer. 2004. Molecular dynamics simulations of guanine quadruplex loops: Advances and force field limitations. Biophys. J. 87:227-242.
76. Spackova, N., and J. Sponer. 2006. Molecular dynamics simulations of sarcin-ricin rRNA motif. Nucleic Acids Res. 34:697-708.
77. Jurecka, P., J. Sponer, and P. Hobza. 2004. Potential energy surface of the cytosine dimer: MP2 complete basis set limit interaction energies, CCSD(T) correction term, and comparison with the AMBER force field. J. Phys. Chem. B. 108:5466-5471.
78. Sponer, J., P. Jurecka, and P. Hobza. 2004. Accurate interaction energies of hydrogen-bonded nucleic acid base pairs. J. Am. Chem. Soc. 126:10142-10151.
79. Sponer, J. E., N. Spackova, J. Leszczynski, and J. Sponer. 2005. Principles of RNA base pairing: Structures and energies of the trans Watson-Crick/sugar edge base pairs. J. Phys. Chem. B. 109:11399-11410.