The structural basis of RNA-catalyzed RNA polymerization (original) (raw)

• Joyce, G.F. & Orgel, L.E. Prospects for understanding the origin of the RNA world. in The RNA World 2nd edn. (eds. Gesteland, R.F., Cech, T.R. & Atkins, J.F.) 49–77 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA, 1999).
• Orgel, L.E. Prebiotic chemistry and the origin of the RNA world. Crit. Rev. Biochem. Mol. Biol. 39, 99–123 (2004).
  Article CAS PubMed Google Scholar
• White, H.B. III. Coenzymes as fossils of an earlier metabolic state. J. Mol. Evol. 7, 101–104 (1976).
  Article CAS PubMed Google Scholar
• Nissen, P., Hansen, J., Ban, N., Moore, P.B. & Steitz, T.A. The structural basis of ribosome activity in peptide bond synthesis. Science 289, 920–930 (2000).
  Article CAS PubMed Google Scholar
• Fedor, M.J. & Williamson, J.R. The catalytic diversity of RNAs. Nat. Rev. Mol. Cell Biol. 6, 399–412 (2005).
  Article CAS PubMed Google Scholar
• Chen, X., Li, N. & Ellington, A.D. Ribozyme catalysis of metabolism in the RNA world. Chem. Biodivers. 4, 633–655 (2007).
  Article CAS PubMed Google Scholar
• Lincoln, T.A. & Joyce, G.F. Self-sustained replication of an RNA enzyme. Science 323, 1229–1232 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Bartel, D.P. Re-creating an RNA replicase. in The RNA World 2nd edn. (eds. Gesteland, R.F., Cech, T.R. & Atkins, J.F.) 143–162 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA, 1999).
• McGinness, K.E. & Joyce, G.F. In search of an RNA replicase ribozyme. Chem. Biol. 10, 5–14 (2003).
  Article CAS PubMed Google Scholar
• Bartel, D.P. & Szostak, J.W. Isolation of new ribozymes from a large pool of random sequences. Science 261, 1411–1418 (1993).
  Article CAS PubMed Google Scholar
• Ekland, E.H., Szostak, J.W. & Bartel, D.P. Structurally complex and highly active RNA ligases derived from random RNA sequences. Science 269, 364–370 (1995).
  Article CAS PubMed Google Scholar
• Ekland, E.H. & Bartel, D.P. RNA-catalysed RNA polymerization using nucleoside triphosphates. Nature 382, 373–376 (1996).
  Article CAS PubMed Google Scholar
• Johnston, W.K., Unrau, P.J., Lawrence, M.S., Glasner, M.E. & Bartel, D.P. RNA-catalyzed RNA polymerization: accurate and general RNA-templated primer extension. Science 292, 1319–1325 (2001).
  Article CAS PubMed Google Scholar
• Lawrence, M.S. & Bartel, D.P. New ligase-derived RNA polymerase ribozymes. RNA 11, 1173–1180 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Zaher, H.S. & Unrau, P.J. Selection of an improved RNA polymerase ribozyme with superior extension and fidelity. RNA 13, 1017–1026 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Wochner, A., Attwater, J., Coulson, A. & Holliger, P. Ribozyme-catalyzed transcription of an active ribozyme. Science 332, 209–212 (2011).
  Article CAS PubMed Google Scholar
• Shechner, D.M. et al. Crystal structure of the catalytic core of an RNA-polymerase ribozyme. Science 326, 1271–1275 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Bagby, S.C., Bergman, N.H., Shechner, D.M., Yen, C. & Bartel, D.P. A class I ligase ribozyme with reduced Mg2+ dependence: selection, sequence analysis, and identification of functional tertiary interactions. RNA 15, 2129–2146 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Stuhlmann, F. & Jaschke, A. Characterization of an RNA active site: interactions between a Diels-Alderase ribozyme and its substrates and products. J. Am. Chem. Soc. 124, 3238–3244 (2002).
  Article CAS PubMed Google Scholar
• Serganov, A. et al. Structural basis for Diels-Alder ribozyme-catalyzed carbon-carbon bond formation. Nat. Struct. Mol. Biol. 12, 218–224 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Robertson, M.P. & Scott, W.G. The structural basis of ribozyme-catalyzed RNA assembly. Science 315, 1549–1553 (2007).
  Article CAS PubMed Google Scholar
• Xiao, H., Murakami, H., Suga, H. & Ferre-D'Amare, A.R. Structural basis of specific tRNA aminoacylation by a small in vitro selected ribozyme. Nature 454, 358–361 (2008).
  Article CAS PubMed Google Scholar
• Pitt, J.N. & Ferre-D'Amare, A.R. Structure-guided engineering of the regioselectivity of RNA ligase ribozymes. J. Am. Chem. Soc. 131, 3532–3540 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Glasner, M.E., Bergman, N.H. & Bartel, D.P. Metal ion requirements for structure and catalysis of an RNA ligase ribozyme. Biochemistry 41, 8103–8112 (2002).
  Article CAS PubMed Google Scholar
• Harding, M.M. Geometry of metal-ligand interactions in proteins. Acta Crystallogr. D Biol. Crystallogr. 57, 401–411 (2001).
  Article CAS PubMed Google Scholar
• Chen, J.H. et al. A 1.9 A crystal structure of the HDV ribozyme precleavage suggests both Lewis acid and general acid mechanisms contribute to phosphodiester cleavage. Biochemistry 49, 6508–6518 (2010).
  Article CAS PubMed Google Scholar
• Steitz, T.A. A mechanism for all polymerases. Nature 391, 231–232 (1998).
  Article CAS PubMed Google Scholar
• Castro, C. et al. Nucleic acid polymerases use a general acid for nucleotidyl transfer. Nat. Struct. Mol. Biol. 16, 212–218 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Hsiao, C. et al. Complexes of nucleic acids with group I and II cations. in Nucleic Acid-Metal Ion Interactions Vol. 1 (ed. Hud, N.V.) 1–38 (RSC Publishing, Cambridge, UK, 2009).
• Harding, M.M. The geometry of metal-ligand interactions relevant to proteins. II. Angles at the metal atom, additional weak metal-donor interactions. Acta Crystallogr. D Biol. Crystallogr. 56, 857–867 (2000).
  Article CAS PubMed Google Scholar
• Glasner, M.E., Yen, C.C., Ekland, E.H. & Bartel, D.P. Recognition of nucleoside triphosphates during RNA-catalyzed primer extension. Biochemistry 39, 15556–15562 (2000).
  Article CAS PubMed Google Scholar
• Basu, S. & Strobel, S.A. Thiophilic metal ion rescue of phosphorothioate interference within the Tetrahymena ribozyme P4–P6 domain. RNA 5, 1399–1407 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Sträter, N., Lipscomb, W.N., Klabunde, T. & Krebs, B. Two-metal ion catalysis in enzymatic acyl- and phosphoryl-transfer reactions. Angew. Chem. Int. Edn Engl. 35, 2024–2055 (1996).
  Article Google Scholar
• Frederiksen, J.K. & Piccirilli, J.A. Identification of catalytic metal ion ligands in ribozymes. Methods 49, 148–166 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Saenger, W. Principles of Nucleic Acid Structure (Springer-Verlag, New York, 1984).
• Jencks, W.P. Catalysis in Chemistry and Enzymology (McGraw-Hill, New York, 1969).
• Venkatasubban, K.S. & Schowen, R.L. The proton inventory technique. CRC Crit. Rev. Biochem. 17, 1–44 (1984).
  Article CAS PubMed Google Scholar
• Schowen, K.B. & Schowen, R.L. Solvent isotope effects of enzyme systems. Methods Enzymol. 87, 551–606 (1982).
  Article CAS PubMed Google Scholar
• Das, S.R. & Piccirilli, J.A. General acid catalysis by the hepatitis delta virus ribozyme. Nat. Chem. Biol. 1, 45–52 (2005).
  Article CAS PubMed Google Scholar
• Gong, B. et al. Direct measurement of a pKa near neutrality for the catalytic cytosine in the genomic HDV ribozyme using Raman crystallography. J. Am. Chem. Soc. 129, 13335–13342 (2007).
  Article CAS PubMed Google Scholar
• Stahley, M.R. & Strobel, S.A. Structural evidence for a two-metal-ion mechanism of group I intron splicing. Science 309, 1587–1590 (2005).
  Article CAS PubMed Google Scholar
• Toor, N., Keating, K.S., Taylor, S.D. & Pyle, A.M. Crystal structure of a self-spliced group II intron. Science 320, 77–82 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Yang, W. An equivalent metal ion in one- and two-metal-ion catalysis. Nat. Struct. Mol. Biol. 15, 1228–1231 (2008).
  Article PubMed PubMed Central Google Scholar
• Fedor, M.J. Comparative enzymology and structural biology of RNA self-cleavage. Annu. Rev. Biophys. 38, 271–299 (2009).
  Article CAS PubMed Google Scholar
• Bevilacqua, P.C. & Yajima, R. Nucleobase catalysis in ribozyme mechanism. Curr. Opin. Chem. Biol. 10, 455–464 (2006).
  Article CAS PubMed Google Scholar
• Ke, A., Zhou, K., Ding, F., Cate, J.H. & Doudna, J.A. A conformational switch controls hepatitis delta virus ribozyme catalysis. Nature 429, 201–205 (2004).
  Article CAS PubMed Google Scholar
• Lupták, A., Ferre-D'Amare, A.R., Zhou, K., Zilm, K.W. & Doudna, J.A. Direct pKa measurement of the active-site cytosine in a genomic hepatitis delta virus ribozyme. J. Am. Chem. Soc. 123, 8447–8452 (2001).
  Article PubMed Google Scholar
• Klein, D.J. & Ferre-D'Amare, A.R. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313, 1752–1756 (2006).
  Article CAS PubMed Google Scholar
• Cochrane, J.C., Lipchock, S.V. & Strobel, S.A. Structural investigation of the GlmS ribozyme bound to Its catalytic cofactor. Chem. Biol. 14, 97–105 (2007).
  Article CAS PubMed Google Scholar
• Nesbitt, S., Hegg, L.A. & Fedor, M.J. An unusual pH-independent and metal-ion-independent mechanism for hairpin ribozyme catalysis. Chem. Biol. 4, 619–630 (1997).
  Article CAS PubMed Google Scholar
• Rupert, P.B., Massey, A.P., Sigurdsson, S.T. & Ferre-D'Amare, A.R. Transition state stabilization by a catalytic RNA. Science 298, 1421–1424 (2002).
  Article CAS PubMed Google Scholar
• Salter, J., Krucinska, J., Alam, S., Grum-Tokars, V. & Wedekind, J.E. 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 (2006).
  Article CAS PubMed Google Scholar
• Emilsson, G.M., Nakamura, S., Roth, A. & Breaker, R.R. Ribozyme speed limits. RNA 9, 907–918 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Ferré-D'Amaré, A.R. & Doudna, J.A. 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 (2000).
  Article PubMed Google Scholar
• Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collection in oscillation mode. Methods Enzymol. 276, 307–326 (1997).
  Article CAS PubMed Google Scholar
• McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Adams, P.D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948–1954 (2002).
  Article PubMed Google Scholar
• Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).
  Article PubMed Google Scholar
• Bullard, D.R. & Bowater, R.P. Direct comparison of nick-joining activity of the nucleic acid ligases from bacteriophage T4. Biochem. J. 398, 135–144 (2006).
  Article CAS PubMed PubMed Central Google Scholar