A 1.9 Å crystal structure of the HDV ribozyme precleavage suggests both lewis acid and general acid mechanisms contribute to phosphodiester cleavage

Biochemistry

Volumn 49, Issue 31, 2010, Pages 6508-6518

  Chen, Jui Hui ^a,c   Yajima, Rieko ^b,d   Chadalavada, Durga M ^b   Chase, Elaine ^a   Bevilacqua, Philip C ^b   Golden, Barbara L ^a  

^a PURDUE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d AAAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CLEAVAGE REACTION; CLEAVAGE SITES; CRYSTALLOGRAPHIC DISORDER; CYCLIC PHOSPHATES; HEPATITIS DELTA VIRUS; LEWIS ACID; NUCLEOBASES; NUCLEOPHILIC ATTACK; PHOSPHODIESTERS; PSEUDOKNOT; RIBOZYME ACTIVITY; RIBOZYMES; RNA CLEAVAGE; SUBSTRATE COMPLEXES; TO EFFECT; WILD TYPES;

ACIDS; HYDRATES; METAL IONS; NUCLEOTIDES; OXYGEN; RNA; SPHERES; VIRUSES;

CRYSTAL STRUCTURE;

DEOXYRIBONUCLEOTIDE; LEWIS ACID; MAGNESIUM ION; NUCLEIC ACID BASE; OXYGEN; PHOSPHATE; RIBOZYME; VIRUS RNA; MAGNESIUM; ORGANOPHOSPHATE;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HEPATITIS DELTA VIRUS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; CHEMICAL REACTION; CHEMISTRY; ENZYMOLOGY; HYDROLYSIS; METABOLISM; X RAY CRYSTALLOGRAPHY;

HEPATITIS DELTA VIRUS;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HEPATITIS DELTA VIRUS; HYDROLYSIS; MAGNESIUM; ORGANIC CHEMISTRY PROCESSES; PHOSPHORIC ACID ESTERS; RNA, CATALYTIC;

EID: 77955258795     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100670p     Document Type: Article

References (87)

1. Fedor, M. J. (2009) Comparative enzymology and structural biology of RNA self-cleavage Annu. Rev. Biophys. 38, 271-299
2. Cech, T. R. (2009) Evolution of Biological Catalysis: Ribozyme to RNP Enzyme Cold Spring Harbor Symp. Quant. Biol. (in press)
3. DeRose, V. J. (2003) Metal ion binding to catalytic RNA molecules Curr. Opin. Struct. Biol. 13, 317-324
4. Adams, P. L., Stahley, M. R., Kosek, A. B., Wang, J., and Strobel, S. A. (2004) Crystal structure of a self-splicing group I intron with both exons Nature 430, 45-50 (Pubitemid 38915218)
5. Guo, F., Gooding, A. R., and Cech, T. R. (2004) Structure of the Tetrahymena ribozyme: Base triple sandwich and metal ion at the active site Mol. Cell 16, 351-362
6. Golden, B. L., Kim, H., and Chase, E. (2005) Crystal structure of a phage Twort group I ribozyme-product complex Nat. Struct. Mol. Biol. 12, 82-89
7. Stahley, M. R. and Strobel, S. A. (2005) Structural evidence for a two-metal-ion mechanism of group I intron splicing Science 309, 1587-1590
8. Bevilacqua, P. C. and Yajima, R. (2006) Nucleobase catalysis in ribozyme mechanism Curr. Opin. Chem. Biol. 10, 455-464
9. Murray, J. B., Seyhan, A. A., Walter, N. G., Burke, J. M., and Scott, W. G. (1998) The hammerhead, hairpin and VS ribozymes are catalytically proficient in monovalent cations alone Chem. Biol. 5, 587-595
10. Sharmeen, L., Kuo, M. Y., Dinter-Gottlieb, G., and Taylor, J. (1988) Antigenomic RNA of human hepatitis delta virus can undergo self-cleavage J. Virol. 62, 2674-2679
11. Kuo, M. Y., Sharmeen, L., Dinter-Gottlieb, G., and Taylor, J. (1988) Characterization of self-cleaving RNA sequences on the genome and antigenome of human hepatitis delta virus J. Virol. 62, 4439-4444
12. Salehi-Ashtiani, K., Luptak, A., Litovchick, A., and Szostak, J. W. (2006) A genomewide search for ribozymes reveals an HDV-like sequence in the human CPEB3 gene Science 313, 1788-1792
13. Webb, C. H., Riccitelli, N. J., Ruminski, D. J., and Luptak, A. (2009) Widespread occurrence of self-cleaving ribozymes Science 326, 953
14. Perrotta, A. T. and Been, M. D. (1996) Core sequences and a cleavage site wobble pair required for HDV antigenomic ribozyme self-cleavage Nucleic Acids Res. 24, 1314-1321
15. Been, M. D. and Wickham, G. S. (1997) Self-cleaving ribozymes of hepatitis delta virus RNA Eur. J. Biochem. 247, 741-753
16. Suh, Y. A., Kumar, P. K., Taira, K., and Nishikawa, S. (1993) Self-cleavage activity of the genomic HDV ribozyme in the presence of various divalent metal ions Nucleic Acids Res. 21, 3277-3280
17. Nakano, S., Cerrone, A. L., and Bevilacqua, P. C. (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
18. Shih, I. H. and Been, M. D. (1999) Ribozyme cleavage of a 2,5-phosphodiester linkage: Mechanism and a restricted divalent metal-ion requirement RNA 5, 1140-1148
19. Perrotta, A. T., Shih, I., and Been, M. D. (1999) Imidazole rescue of a cytosine mutation in a self-cleaving ribozyme Science 286, 123-126
20. Nakano, S., Chadalavada, D. M., and Bevilacqua, P. C. (2000) General acid-base catalysis in the mechanism of a hepatitis delta virus ribozyme Science 287, 1493-1497
21. a near neutrality for the catalytic cytosine in the genomic HDV ribozyme using Raman crystallography J. Am. Chem. Soc. 129, 13335-13342
22. Perrotta, A. T., Wadkins, T. S., and Been, M. D. (2006) Chemical rescue, multiple ionizable groups, and general acid-base catalysis in the HDV genomic ribozyme RNA 12, 1282-1291
23. Ferre-D'Amare, A. R., Zhou, K., and Doudna, J. A. (1998) Crystal structure of a hepatitis delta virus ribozyme Nature 395, 567-574
24. Wadkins, T. S., Perrotta, A. T., Ferre-D'Amare, A. R., Doudna, J. A., and Been, M. D. (1999) A nested double pseudoknot is required for self-cleavage activity of both the genomic and antigenomic hepatitis delta virus ribozymes RNA 5, 720-727
25. Perrotta, A. T. and Been, M. D. (1991) A pseudoknot-like structure required for efficient self-cleavage of hepatitis delta virus RNA Nature 350, 434-436
26. Das, S. R. and Piccirilli, J. A. (2005) General acid catalysis by the hepatitis delta virus ribozyme Nat. Chem. Biol. 1, 45-52
27. Ke, A., Zhou, K., Ding, F., Cate, J. H., and Doudna, J. A. (2004) A conformational switch controls hepatitis delta virus ribozyme catalysis Nature 429, 201-205
28. Banas, P., Rulisek, L., Hanosova, V., Svozil, D., Walter, N. G., Sponer, J., and Otyepka, M. (2008) General base catalysis for cleavage by the active-site cytosine of the hepatitis delta virus ribozyme: QM/MM calculations establish chemical feasibility J. Phys. Chem. 112, 11177-11187
29. Krasovska, M. V., Sefcikova, J., Spackova, N., Sponer, J., and Walter, N. G. (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
30. Golden, B. L., Podell, E. R., Gooding, A. R., and Cech, T. R. (1997) Crystals by design: A strategy for crystallization of a ribozyme derived from the Tetrahymena group I intron J. Mol. Biol. 270, 711-723
31. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode. In Methods in Enzymology, Macromolecular Crystallography, Part A (Carter, C. W. J. and Sweet, R. M., Eds.) pp 307-326, Academic Press, New York.
32. Collaborative Computational Project, Number 4 (1994) The CCP4 Suite: Programs for Protein Crystallography Acta Crystallogr. D50, 760-763
33. Brunger, A. T. (2007) Version 1.2 of the Crystallography and NMR system Nat. Protoc. 2, 2728-2733
34. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D54, 905-921
35. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
36. DeLano, W. L. (2007) The Pymol Molecular Graphics System, DeLano Scientific, San Carlos, CA.
37. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr. 47 (Part 2) 110-119
38. Smith, J. B. and Dinter-Gottlieb, G. (1991) Antigenomic hepatitis delta virus ribozymes self-cleave in 18 M formamide Nucleic Acids Res. 19, 1285-1289
39. Brown, T. S., Chadalavada, D. M., and Bevilacqua, P. C. (2004) Design of a highly reactive HDV ribozyme sequence uncovers facilitation of RNA folding by alternative pairings and physiological ionic strength J. Mol. Biol. 341, 695-712
40. Chen, J. H., Gong, B., Bevilacqua, P. C., Carey, P. R., and Golden, B. L. (2009) A catalytic metal ion interacts with the cleavage site G'U wobble in the HDV ribozyme Biochemistry 48, 1498-1507
41. Rupert, P. B. and Ferre-D'Amare, A. R. (2001) Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis Nature 410, 780-786
42. Alam, S., Grum-Tokars, V., Krucinska, J., Kundracik, M. L., and Wedekind, J. E. (2005) Conformational heterogeneity at position U37 of an all-RNA hairpin ribozyme with implications for metal binding and the catalytic structure of the S-turn Biochemistry 44, 14396-14408
43. Martick, M. and Scott, W. G. (2006) Tertiary contacts distant from the active site prime a ribozyme for catalysis Cell 126, 309-320
44. Klein, D. J. and Ferre-D'Amare, A. R. (2006) Structural basis of glmS ribozyme activation by glucosamine-6-phosphate Science 313, 1752-1756
45. Cochrane, J. C., Lipchock, S. V., and Strobel, S. A. (2007) Structural investigation of the GlmS ribozyme bound to its catalytic cofactor Chem. Biol. 14, 97-105
46. Gong, B., Chen, Y., Christian, E. L., Chen, J. H., Chase, E., Chadalavada, D. M., Yajima, R., Golden, B. L., Bevilacqua, P. C., and Carey, P. R. (2008) Detection of innersphere interactions between magnesium hydrate and the phosphate backbone of the HDV ribozyme using Raman crystallography J. Am. Chem. Soc. 130, 9670-9672
47. 2+ ions in the HDV ribozyme Biochemistry 48, 11961-11970
48. Burkard, M. E., Turner, D. H., and Tinoco, I. (1999) Structures of Base Pairs Involving at Least Two Hydrogen Bonds. In RNA World (Gesteland, R. F., Cech, T. R., and Atkins, J. F., Eds.) 2nd ed., pp 675-680, Cold Spring Harbor Laboratory Press, Plainview, NY.
49. Leontis, N. B. and Westhof, E. (2001) Geometric nomenclature and classification of RNA base pairs RNA 7, 499-512
50. Ferre-D'Amare, A. R. and Doudna, J. A. (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
51. Nakano, S., Proctor, D. J., and Bevilacqua, P. C. (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
52. Perrotta, A. T. and Been, M. D. (2007) A single nucleotide linked to a switch in metal ion reactivity preference in the HDV ribozymes Biochemistry 46, 5124-5130
53. Nakano, S. and Bevilacqua, P. C. (2007) Mechanistic characterization of the HDV genomic ribozyme: A mutant of the C41 motif provides insight into the positioning and thermodynamic linkage of metal ions and protons Biochemistry 46, 3001-3012
54. Cerrone-Szakal, A. L., Siegfried, N. A., and Bevilacqua, P. C. (2008) Mechanistic characterization of the HDV genomic ribozyme: Solvent isotope effects and proton inventories in the absence of divalent metal ions support C75 as the general acid J. Am. Chem. Soc. 130, 14504-14520
55. Tanner, N. K., Schaff, S., Thill, G., Petit-Koskas, E., Crain-Denoyelle, A. M., and Westhof, E. (1994) A three-dimensional model of hepatitis delta virus ribozyme based on biochemical and mutational analyses Curr. Biol. 4, 488-498
56. Chin, K., Sharp, K. A., Honig, B., and Pyle, A. M. (1999) Calculating the electrostatic properties of RNA provides new insights into molecular interactions and function Nat. Struct. Biol. 6, 1055-1061
57. Wu, H. N. and Huang, Z. S. (1992) Mutagenesis analysis of the self-cleavage domain of hepatitis delta virus antigenomic RNA Nucleic Acids Res. 20, 5937-5941
58. Wu, H. N., Lee, J. Y., Huang, H. W., Huang, Y. S., and Hsueh, T. G. (1993) Mutagenesis analysis of a hepatitis delta virus genomic ribozyme Nucleic Acids Res. 21, 4193-4199
59. Nishikawa, F., Fauzi, H., and Nishikawa, S. (1997) Detailed analysis of base preferences at the cleavage site of a trans-acting HDV ribozyme: A mutation that changes cleavage site specificity Nucleic Acids Res. 25, 1605-1610
60. Cerrone-Szakal, A. L., Chadalavada, D. M., Golden, B. L., and Bevilacqua, P. C. (2008) Mechanistic characterization of the HDV genomic ribozyme: The cleavage site base pair plays a structural role in facilitating catalysis RNA 14, 1746-1760
61. Salter, J., Krucinska, J., Alam, S., Grum-Tokars, V., and Wedekind, J. E. (2006) Water in the active site of an all-RNA hairpin ribozyme and effects of Gua8 base variants on the geometry of phosphoryl transfer Biochemistry 45, 686-700
62. Steitz, T. A. and Steitz, J. A. (1993) A general two-metal-ion mechanism for catalytic RNA Proc. Natl. Acad. Sci. U.S.A. 90, 6498-6502
63. Shan, S., Kravchuk, A. V., Piccirilli, J. A., and Herschlag, D. (2001) Defining the catalytic metal ion interactions in the Tetrahymena ribozyme reaction Biochemistry 40, 5161-5171
64. Fauzi, H., Kawakami, J., Nishikawa, F., and Nishikawa, S. (1997) Analysis of the cleavage reaction of a trans-acting human hepatitis delta virus ribozyme Nucleic Acids Res. 25, 3124-3130
65. Dahm, S. C. and Uhlenbeck, O. C. (1991) Role of divalent metal ions in the hammerhead RNA cleavage reaction Biochemistry 30, 9464-9469
66. Slim, G. and Gait, M. J. (1991) Configurationally defined phosphorothioate-containing oligoribonucleotides in the study of the mechanism of cleavage of hammerhead ribozymes Nucleic Acids Res. 19, 1183-1188
67. Wang, S., Karbstein, K., Peracchi, A., Beigelman, L., and Herschlag, D. (1999) Identification of the hammerhead ribozyme metal ion binding site responsible for rescue of the deleterious effect of a cleavage site phosphorothioate Biochemistry 38, 14363-14378
68. O'Rear, J. L., Wang, S., Feig, A. L., Beigelman, L., Uhlenbeck, O. C., and Herschlag, D. (2001) Comparison of the hammerhead cleavage reactions stimulated by monovalent and divalent cations RNA 7, 537-545
69. Osborne, E. M., Schaak, J. E., and Derose, V. J. (2005) Characterization of a native hammerhead ribozyme derived from schistosomes RNA 11, 187-196
70. Boots, J. L., Canny, M. D., Azimi, E., and Pardi, A. (2008) Metal ion specificities for folding and cleavage activity in the Schistosoma hammerhead ribozyme RNA 14, 2212-2222
71. Osborne, E. M., Ward, W. L., Ruehle, M. Z., and DeRose, V. J. (2009) The identity of the nucleophile substitution may influence metal interactions with the cleavage site of the minimal hammerhead ribozyme Biochemistry 48, 10654-10664
72. Wadkins, T. S. and Been, M. D. (2002) Ribozyme activity in the genomic and antigenomic RNA strands of hepatitis delta virus Cell. Mol. Life Sci. 59, 112-125
73. Shih, I. and Been, M. D. (2001) Energetic contribution of non-essential 5′ sequence to catalysis in a hepatitis delta virus ribozyme EMBO J. 20, 4884-4891
74. Chadalavada, D. M., Knudsen, S. M., Nakano, S., and Bevilacqua, P. C. (2000) A role for upstream RNA structure in facilitating the catalytic fold of the genomic hepatitis delta virus ribozyme J. Mol. Biol. 301, 349-367
75. Strobel, S. A. (2005) Ribonucleic general acid Nat. Chem. Biol. 1, 5-6
76. Feig, A. L. and Uhlenbeck, O. C. (1999) The role of metal ions in RNA biochemistry. In The RNA World (Gesteland, R. F., Cech, T. R., and Atkins, J. F., Eds.) 2nd ed., pp 287-319, Cold Spring Harbor Laboratory Press, Plainview, NY.
77. Basolo, R. and Pearson, R. G. (1988) Mechanisms of Inorganic Reactions, John Wiley & Sons, New York.
78. Hampel, A. and Cowan, J. A. (1997) A unique mechanism for RNA catalysis: The role of metal cofactors in hairpin ribozyme cleavage Chem. Biol. 4, 513-517
79. Nesbitt, S., Hegg, L. A., and Fedor, M. J. (1997) An unusual pH-independent and metal-ion-independent mechanism for hairpin ribozyme catalysis Chem. Biol. 4, 619-630
80. Young, K. J., Gill, F., and Grasby, J. A. (1997) Metal ions play a passive role in the hairpin ribozyme catalysed reaction Nucleic Acids Res. 25, 3760-3766
81. 2+-containing solutions J. Am. Chem. Soc. 123, 11333-11334
82. Curtis, E. A. and Bartel, D. P. (2001) The hammerhead cleavage reaction in monovalent cations RNA 7, 546-552
83. 2+ in hammerhead ribozyme catalysis from molecular simulation J. Am. Chem. Soc. 130, 3053-3064
84. Gordon, P. M., Sontheimer, E. J., and Piccirilli, J. A. (2000) Kinetic characterization of the second step of group II intron splicing: role of metal ions and the cleavage site 2′-OH in catalysis Biochemistry 39, 12939-12952
85. Gordon, P. M., Fong, R., and Piccirilli, J. A. (2007) A second divalent metal ion in the group II intron reaction center Chem. Biol. 14, 607-612
86. Toor, N., Keating, K. S., Taylor, S. D., and Pyle, A. M. (2008) Crystal structure of a self-spliced group II intron Science 320, 77-82
87. Pontius, B. W., Lott, W. B., and von Hippel, P. H. (1997) Observations on catalysis by hammerhead ribozymes are consistent with a two-divalent-metal-ion mechanism Proc. Natl. Acad. Sci. U.S.A. 94, 2290-2294