New tools provide a second look at HDV ribozyme structure, dynamics and cleavage

Nucleic Acids Research

Volumn 42, Issue 20, 2014, Pages 12833-12846

  Kapral, Gary J ^a,b   Jain, Swati ^a,b   Noeske, Jonas ^c   Doudna, Jennifer A ^c   Richardson, David C ^a   Richardson, Jane S ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOZYME; RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; U1A PROTEIN;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DYNAMICS; HEPATITIS DELTA VIRUS; HOST CELL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; PROTON TRANSPORT; RNA BINDING; RNA STRUCTURE; VIRUS PARTICLE; VIRUS REPLICATION; BASE PAIRING; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; ENZYMOLOGY; METABOLISM; RNA CLEAVAGE;

BASE PAIRING; HEPATITIS DELTA VIRUS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RIBONUCLEOPROTEIN, U1 SMALL NUCLEAR; RNA CLEAVAGE; RNA, CATALYTIC;

EID: 84925253393     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku992     Document Type: Article

References (49)

1. Sharmeen, L.L., Kuo, M.Y.M., Dinter-Gottlieb, G.G. and Taylor, J.J. (1988) Antigenomic RNA of human hepatitis delta virus can undergo self-cleavage. J. Virol., 62, 2674-2679.
2. Kuo, M.Y.M., Sharmeen, L.L., Dinter-Gottlieb, G.G. and Taylor, J.J. (1988) Characterization of self-cleaving RNA sequences on the genome and antigenome of human hepatitis delta virus. J. Virol., 62, 4439-4444.
3. Wu, H.N., Lin, Y.J., Lin, F.P., Makino, S., Chang, M.F. and Lai, M.M. (1989) Human hepatitis delta virus RNA subfragments contain an autocleavage activity. Proc. Natl Acad. Sci. U.S.A., 86, 1831-1835.
4. Webb, C.H.T., Riccitelli, N.J., Ruminski, D.J. and Lupták, A. (2009) Widespread occurrence of self-cleaving ribozymes. Science, 326, 953-953.
5. Vogler, C., Spalek, K., Aerni, A., Demougin, P., Muller, A., Huynh, K.D., Papassotiropoulos, A. and De Quervain, D.J.F. (2009) CPEB3 is associated with human episodic memory. Front. Behav. Neurosci., 3, doi:10.3389/neuro.08.004.2009.
6. Webb, C.H.T. and Lupták, A. (2011) HDV-like self-cleaving ribozymes. RNA Biol., 8, 719-727.
7. Salehi-Ashtiani, K., Lupták, 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.
8. Nakano, S.I., 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.
9. Veeraraghavan, N., Ganguly, A., Chen, J.H., Bevilacqua, P.C., Hammes-Schiffer, S. and Golden, B.L. (2011) Metal binding motif in the active site of the HDV ribozyme binds divalent and monovalent ions. Biochemistry, 50, 2672-2682.
10. 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.
11. 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.
12. Suh, Y.A., Kumar, P.K.R., Kawakami, J., Nishikawa, F., Taira, K. and Nishikawa, S. (1993) Systematic substitution of individual bases in two important single-stranded regions of the HDV ribozyme for evaluation of the role of specific bases. FEBS Lett., 326, 158-162.
13. Ferré-D'Amaré, A.R., Zhou, K. and Doudna, J.A. (1998) Crystal structure of a hepatitis delta virus ribozyme. Nature, 395, 567-574.
14. Shih, I.H. and Been, M.D. (2001) Involvement of a cytosine side chain in proton transfer in the rate-determining step of ribozyme self-cleavage. Proc. Natl Acad. Sci. U.S.A., 98, 1489-1494.
15. Perrotta, A.T., Shih, I.H. and Been, M.D. (1999) Imidazole rescue of a cytosine mutation in a self-cleaving ribozyme. Science, 286, 123-126.
16. Ke, A., Zhou, K., Ding, F., Cate, J.H.D. and Doudna, J.A. (2004) A conformational switch controls hepatitis delta virus ribozyme catalysis. Nature, 429, 201-205.
17. 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.
18. Banáš, P., Rulíšek, L., Hánošová, V., Svozil, D., Walter, N.G., Šponer, 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. B, 112, 11177-11187.
19. Lee, T.S., Giambaşu, G.M., Harris, M.E. and York, D.M. (2011) Characterization of the structure and dynamics of the HDV ribozyme in different stages along the reaction path. J. Phys. Chem. Lett., 2, 2538-2543.
20. Das, S.R. and Piccirilli, J.A. (2005) General acid catalysis by the hepatitis delta virus ribozyme. Nat. Chem. Biol., 1, 45-52.
21. Chen, J.H., Yajima, R., Chadalavada, D.M., Chase, E., Bevilacqua, P.C. and Golden, B.L. (2010) A 1.9 Å crystal structure of the HDV ribozyme precleavage suggests both Lewis acid and general acid mechanisms contribute to phosphodiester cleavage. Biochemistry, 49, 6508-6518.
22. Martick, M., Lee, T.S., York, D.M. and Scott, W.G. (2008) Solvent structure and hammerhead ribozyme catalysis. Chem. Biol., 15, 332-342.
23. Ganguly, A., Thaplyal, P., Rosta, E., Bevilacqua, P.C. and Hammes-Schiffer, S. (2014) Quantum mechanical/molecular mechanical free energy simulations of the self-cleavage reaction in the hepatitis delta virus ribozyme. J. Am. Chem. Soc., 136, 1483-1496.
24. Chen, J., Ganguly, A., Miswan, Z., Hammes-Schiffer, S., Bevilacqua, P.C. and Golden, B.L. (2013) Identification of the catalytic Mg 2+Ion in the hepatitis delta virus ribozyme. Biochemistry, 52, 557-567.
25. Thaplyal, P., Ganguly, A., Golden, B.L., Hammes-Schiffer, S. and Bevilacqua, P.C. (2013) Thio effects and an unconventional metal ion rescue in the genomic hepatitis delta virus ribozyme. Biochemistry, 52, 6499-6514.
26. Ferré-D'Amaré, A.R. and Scott, W.G. (2010) Small self-cleaving ribozymes. Cold Spring Harb. Perspect. Biol., 2, a003574.
27. Murray, L.J.W., Arendall, W.B. III, Richardson, D.C. and Richardson, J.S. (2003) RNA backbone is rotameric. Proc. Natl Acad. Sci. U.S.A., 100, 13904-13909.
28. Read, R.J., Adams, P.D., Arendall, W.B. III, Brunger, A.T., Emsley, P., Joosten, R.P., Kleywegt, G.J., Krissinel, E.B., Lutteke, T., Otwinowski, Z. et al. (2011) A new generation of crystallographic validation tools for the protein data bank. Structure, 19, 1395-1412.
29. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Cryst. D, 66, 213-221.
30. Richardson, J.S., Schneider, B., Murray, L.W., Kapral, G.J., Immormino, R.M., Headd, J.J., Richardson, D.C., Ham, D., Hershkovits, E., Dean Williams, L. et al. (2008) RNA backbone: consensus all-angle conformers and modular string nomenclature (an RNA Ontology Consortium contribution). RNA, 14, 465-481.
31. Jain, S., Kapral, G.J., Richardson, D.C. and Richardson, J.S. (2014) Getting the pucker right in RNA structures. Computl Crystallogr. Newslett., 5, 4-7.
32. Chen, V.B., Davis, I.W. and Richardson, D.C. (2009) KING (Kinemage, Next Generation): a versatile interactive molecular and scientific visualization program. Protein Sci., 18, 2403-2409.
33. Keating, K.S. and Pyle, A.M. (2012) RCrane: semi-automated RNA model building. Acta Cryst. D, 68, 985-995.
34. Wang, X., Kapral, G., Murray, L., Richardson, D., Richardson, J. and Snoeyink, J. (2008) RNABC: forward kinematics to reduce all-atom steric clashes in RNA backbone. J. Math. Biol., 56, 253-278.
35. Chou, F.C., Richardson, J.S. and Das, R. (2012) ERRASER, a powerful new system for correcting RNA models. Computl Crystallogr. Newslett., 3, 35-36.
36. Chou, F.C., Sripakdeevong, P., Dibrov, S.M., Hermann, T. and Das, R. (2012) Correcting pervasive errors in RNA crystallography through enumerative structure prediction. Nature Methods, 10, 74-76.
37. Richardson, J.S., Prisant, M.G. and Richardson, D.C. (2013) Crystallographic model validation: from diagnosis to healing. Curr. Opin. Struct. Biol., 23, 707-714.
38. Leaver-Fay, A., Tyka, M., Lewis, S.M., Lange, O.F., Thompson, J., Jacak, R., Kaufmann, K.W., Renfrew, P.D., Smith, C.A., Sheffler, W.H. et al. (2011) ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol., 487, 540-574.
39. Chen, V.B., Arendall, W.B. III, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2009) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Cryst. D, 66, 12-21.
40. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B. III, Snoeyink, J., Richardson, J.S. et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res., 35, W375-W383.
41. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Echols, N., Headd, J.J., Hung, L.W., Jain, S., Kapral, G.J., Grosse Kunstleve, R.W. et al. (2011) The Phenix software for automated determination of macromolecular structures. Methods, 55, 94-106.
42. Sripakdeevong, P., Kladwang, W. and Das, R. (2011) An enumerative stepwise ansatz enables atomic-accuracy RNA loop modeling. Proc. Natl Acad. Sci. U.S.A., 108, 20573-20578.
43. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Cryst. D, 66, 486-501.
44. Lovell, S.C., Word, J.M., Richardson, J.S. and Richardson, D.C. (2000) The penultimate rotamer library. Proteins, 40, 389-408.
45. Davis, I.W., Arendall, W.B. III, Richardson, D.C. and Richardson, J.S. (2006) The backrub motion: how protein backbone shrugs when a sidechain dances. Structure, 14, 265-274.
46. Oubridge, C., Ito, N., Evans, P.R., Teo, C.H. and Nagai, K. (1994) Crystal structure at 1.92 A resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature, 372, 432-438.
47. Jeoung, Y.H., Kumar, P.K.R., Suh, Y.A., Taira, K. and Nishikawa, S. (1994) Identification of phosphate oxygens that are important for self-cleavage activity of the HDV ribozyme by phosphorothioate substitution interference analysis. Nucleic Acids Res., 22, 3722-3727.
48. Lévesque, D., Reymond, C. and Perreault, J.P. (2012) Characterization of the Trans Watson-CrickGU base pair located in the catalytic core of the antigenomic HDV ribozyme. PLoS One, 7, e40309.
49. Tanaka, Y., Tagaya, M., Hori, T., Sakamoto, T., Kurihara, Y., Katahira, M. and Uesugi, S. (2002) Cleavage reaction of HDV ribozymes in the presence of Mg2+ is accompanied by a conformational change. Genes Cells, 7, 567-579.