Ribozymes and the mechanisms that underlie RNA catalysis

Ribozymes are widespread, and catalyze some extremely important reactions in the cell. Mechanistically most fall into one of two classes, using either metal ions or general acid-base catalysis. The nucleolytic ribozymes fall into the latter class, mostly using nucleobases. A sub-set of these use a combination of guanine base plus adenine acid to catalyze the cleavage reaction. New ribozymes are still being discovered at regular intervals and we can speculate on the potential existence of ribozymes that catalyze chemistry beyond phosphoryl transfer reactions, perhaps using small-molecule coenzymes.

[1]  G. F. Joyce,et al.  Highly efficient self-replicating RNA enzymes. , 2014, Chemistry & biology.

[2]  Phoebe A Rice,et al.  Crystal Structure of the VS ribozyme , 2015, Nature chemical biology.

[3]  D. Lilley,et al.  The A730 loop is an important component of the active site of the VS ribozyme. , 2001, Journal of molecular biology.

[4]  S A Benner,et al.  Modern metabolism as a palimpsest of the RNA world. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[5]  P. Holliger,et al.  In-ice evolution of RNA polymerase ribozyme activity. , 2013, Nature chemistry.

[6]  M. Yarus,et al.  Coenzymes as coribozymes. , 2002, Biochimie.

[7]  D. Lilley,et al.  A guanine nucleobase important for catalysis by the VS ribozyme , 2007, The EMBO journal.

[8]  D. Herschlag,et al.  Metal-ion rescue revisited: biochemical detection of site-bound metal ions important for RNA folding. , 2012, RNA.

[9]  Jun Lu,et al.  General acid-base catalysis mediated by nucleobases in the hairpin ribozyme. , 2012, Journal of the American Chemical Society.

[10]  D. Herschlag,et al.  Defining the catalytic metal ion interactions in the Tetrahymena ribozyme reaction. , 2001, Biochemistry.

[11]  A. Ferré-D’Amaré,et al.  Transition State Stabilization by a Catalytic RNA , 2002, Science.

[12]  N. Ban,et al.  Structure of the Eukaryotic Thiamine Pyrophosphate Riboswitch with Its Regulatory Ligand , 2006, Science.

[13]  J. Piccirilli,et al.  General acid catalysis by the hepatitis delta virus ribozyme , 2005, Nature chemical biology.

[14]  Daniel Eiler,et al.  Structural basis for the fast self-cleavage reaction catalyzed by the twister ribozyme , 2014, Proceedings of the National Academy of Sciences.

[15]  S. Butcher,et al.  Metal binding and base ionization in the U6 RNA intramolecular stem-loop structure , 2002, Nature Structural Biology.

[16]  Jonathan P. Staley,et al.  RNA catalyzes nuclear pre-mRNA splicing , 2013, Nature.

[17]  T. Steitz,et al.  The structural basis of ribosome activity in peptide bond synthesis. , 2000, Science.

[18]  Terry L. Marsh,et al.  Rna catalysis and the origin of life , 2005, Origins of life and evolution of the biosphere.

[19]  D. Bartel,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S14 Tables S1 to S8 References Crystal Structure of the Catalytic Core of an Rna-polymerase Ribozyme , 2022 .

[20]  D. Lilley,et al.  The Evolution of Ribozyme Chemistry , 2009, Science.

[21]  M. Famulok,et al.  Novel RNA catalysts for the Michael reaction. , 2001, Chemistry & biology.

[22]  S. Strobel,et al.  Structural Evidence for a Two-Metal-Ion Mechanism of Group I Intron Splicing , 2005, Science.

[23]  J. M. Buzayan,et al.  Autolytic Processing of Dimeric Plant Virus Satellite RNA , 1986, Science.

[24]  P. Perlman,et al.  A structural analysis of the group II intron active site and implications for the spliceosome. , 2010, RNA.

[25]  J W Szostak,et al.  Structurally complex and highly active RNA ligases derived from random RNA sequences. , 1995, Science.

[26]  E. Westhof,et al.  In-line alignment and Mg2+ coordination at the cleavage site of the env22 twister ribozyme , 2014, Nature Communications.

[27]  D. Lilley,et al.  Do the hairpin and VS ribozymes share a common catalytic mechanism based on general acid-base catalysis? A critical assessment of available experimental data. , 2011, RNA.

[28]  Andrej Lupták,et al.  A Genomewide Search for Ribozymes Reveals an HDV-Like Sequence in the Human CPEB3 Gene , 2006, Science.

[29]  D. Perrin,et al.  Probing general acid catalysis in the hammerhead ribozyme. , 2008, Journal of the American Chemical Society.

[30]  L E Orgel,et al.  RNA catalysis and the origins of life. , 1986, Journal of theoretical biology.

[31]  S. Strobel,et al.  An uncharged amine in the transition state of the ribosomal peptidyl transfer reaction. , 2008, Chemistry & biology.

[32]  Lin Huang,et al.  The k-junction motif in RNA structure , 2014, Nucleic acids research.

[33]  W. Scott,et al.  Tertiary Contacts Distant from the Active Site Prime a Ribozyme for Catalysis , 2006, Cell.

[34]  A. Ferré-D’Amaré,et al.  Structural Basis of glmS Ribozyme Activation by Glucosamine-6-Phosphate , 2006, Science.

[35]  J. S. Weinger,et al.  Substrate-assisted catalysis of peptide bond formation by the ribosome , 2004, Nature Structural &Molecular Biology.

[36]  James L. Hougland,et al.  Functional Identification of Catalytic Metal Ion Binding Sites within RNA , 2005, PLoS biology.

[37]  B. Golden,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. , 2010, Biochemistry.

[38]  Jennifer A. Doudna,et al.  A conformational switch controls hepatitis delta virus ribozyme catalysis , 2004, Nature.

[39]  H. Noller,et al.  Unusual resistance of peptidyl transferase to protein extraction procedures. , 1992, Science.

[40]  B. Golden,et al.  Crystal structure of a phage Twort group I ribozyme–product complex , 2005, Nature Structural &Molecular Biology.

[41]  J. Steitz,et al.  A general two-metal-ion mechanism for catalytic RNA. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[42]  A. Ferré-D’Amaré,et al.  Essential role of an active-site guanine in glmS ribozyme catalysis. , 2007, Journal of the American Chemical Society.

[43]  Eric Westhof,et al.  Functional Hammerhead Ribozymes Naturally Encoded in the Genome of Arabidopsis thalianaw⃞ , 2005, The Plant Cell Online.

[44]  R. Symons,et al.  Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites , 1987, Cell.

[45]  F. Crick.  Origin of the Genetic Code , 1967, Nature.

[46]  Anna Marie Pyle,et al.  Crystal Structure of a Self-Spliced Group II Intron , 2008, Science.

[47]  R. Breaker,et al.  Genetic Control by Metabolite‐Binding Riboswitches , 2003, Chembiochem : a European journal of chemical biology.

[48]  T. Cech,et al.  A preorganized active site in the crystal structure of the Tetrahymena ribozyme. , 1998, Science.

[49]  Gerhard Steger,et al.  From alpaca to zebrafish: hammerhead ribozymes wherever you look. , 2011, RNA.

[50]  John M. Burke,et al.  Model for general acid-base catalysis by the hammerhead ribozyme: pH-activity relationships of G8 and G12 variants at the putative active site. , 2005, Biochemistry.

[51]  D. Lilley,et al.  The chemical origins of life and its early evolution: an introduction , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[52]  G. Soukup,et al.  Ligand requirements for glmS ribozyme self-cleavage. , 2005, Chemistry & biology.

[53]  S. Nakano,et al.  General acid-base catalysis in the mechanism of a hepatitis delta virus ribozyme. , 2000, Science.

[54]  R. Breaker.  Prospects for riboswitch discovery and analysis. , 2011, Molecular cell.

[55]  G. F. Joyce,et al.  A DNA-templated aldol reaction as a model for the formation of pentose sugars in the RNA world. , 2005, Angewandte Chemie.

[56]  R. Breaker,et al.  A widespread self-cleaving ribozyme class is revealed by bioinformatics , 2013, Nature chemical biology.

[57]  Andrej Lupták,et al.  Widespread Occurrence of Self-Cleaving Ribozymes , 2009, Science.

[58]  Ronald R. Breaker,et al.  Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression , 2002, Nature.

[59]  R. Raines.  Ribonuclease A. , 1998, Chemical reviews.

[60]  A. Ferré-D’Amaré,et al.  Crystal structure of a hairpin ribozyme–inhibitor complex with implications for catalysis , 2001, Nature.

[61]  Yijin Liu,et al.  Crystal structure and mechanistic investigation of the twister ribozyme. , 2014, Nature chemical biology.

[62]  M. Famulok,et al.  A ribozyme for the aldol reaction. , 2005, Chemistry & biology.

[63]  J. Piccirilli,et al.  Metal ion catalysis during the exon-ligation step of nuclear pre-mRNA splicing: extending the parallels between the spliceosome and group II introns. , 2000, RNA.

[64]  Scott A. Strobel,et al.  Crystal structure of a self-splicing group I intron with both exons , 2004, Nature.

[65]  F. H. C. CRICK,et al.  Origin of the Genetic Code , 1967, Nature.

[66]  D. Lilley,et al.  Nucleobase-mediated general acid-base catalysis in the Varkud satellite ribozyme , 2010, Proceedings of the National Academy of Sciences.

[67]  D. Bartel,et al.  RNA-Catalyzed RNA Polymerization: Accurate and General RNA-Templated Primer Extension , 2001, Science.

[68]  A. Serganov,et al.  Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch , 2006, Nature.

[69]  S. Svärd,et al.  Eukaryotic RNase P RNA mediates cleavage in the absence of protein , 2007, Proceedings of the National Academy of Sciences.

[70]  N. Pace,et al.  Mapping metal-binding sites in the catalytic domain of bacterial RNase P RNA. , 2009, RNA.

[71]  R. Raines,et al.  Value of general Acid-base catalysis to ribonuclease a. , 1994, Journal of the American Chemical Society.

[72]  D. York,et al.  Role of Mg2+ in hammerhead ribozyme catalysis from molecular simulation. , 2008, Journal of the American Chemical Society.

[73]  R. Breaker,et al.  New classes of self-cleaving ribozymes revealed by comparative genomics analysis , 2015, Nature chemical biology.

[74]  R. Breaker,et al.  Control of gene expression by a natural metabolite-responsive ribozyme , 2004, Nature.

[75]  Kathryn D. Smith,et al.  Structural and chemical basis for glucosamine 6-phosphate binding and activation of the glmS ribozyme. , 2009, Biochemistry.

[76]  S. Strobel,et al.  Structural investigation of the GlmS ribozyme bound to Its catalytic cofactor. , 2007, Chemistry & biology.

[77]  N. Pace,et al.  The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme , 1983, Cell.

[78]  A. Jäschke,et al.  A small catalytic RNA motif with Diels-Alderase activity. , 1999, Chemistry & biology.