Riboswitches and the RNA world.

Riboswitches are structured noncoding RNA domains that selectively bind metabolites and control gene expression (Mandal and Breaker 2004a; Coppins et al. 2007; Roth and Breaker 2009). Nearly all examples of the known riboswitches reside in noncoding regions of messenger RNAs where they control transcription or translation. Newfound classes of riboswitches are being reported at a rate of about three per year (Ames and Breaker 2009), and these have been shown to selectively respond to fundamental metabolites including coenzymes, nucleobases or their derivatives, amino acids, and other small molecule ligands. The characteristics of some riboswitches suggest they could be modern descendents of an ancient sensory and regulatory system that likely functioned before the emergence of enzymes and genetic factors made of protein (Nahvi et al. 2002; Vitreschak et al. 2004; Breaker 2006). If true, then some of the riboswitch structures and functions that serve modern cells so well may accurately reflect the capabilities of RNA sensors and switches that existed in the RNA World. This article will address some of the characteristics of modern riboswitches that may be relevant to ancient versions of these metabolite-sensing RNAs.

[1]  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.

[2]  T. Henkin,et al.  The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in Gram‐positive bacteria , 1998, Molecular microbiology.

[3]  E. Nudler,et al.  The mechanism of intrinsic transcription termination. , 1999, Molecular cell.

[4]  M. Gelfand,et al.  A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes. , 1999, Trends in genetics : TIG.

[5]  Jeffrey W. Roberts,et al.  Mechanism of intrinsic transcription termination and antitermination. , 1999, Science.

[6]  R. Breaker,et al.  Cooperative binding of effectors by an allosteric ribozyme. , 2001, Nucleic acids research.

[7]  Andrew D Ellington,et al.  Group I aptazymes as genetic regulatory switches , 2002, BMC biotechnology.

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

[9]  R. Breaker Engineered allosteric ribozymes as biosensor components. , 2002, Current opinion in biotechnology.

[10]  R. Breaker,et al.  An mRNA structure that controls gene expression by binding FMN , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Ali Nahvi,et al.  Genetic control by a metabolite binding mRNA. , 2002, Chemistry & biology.

[12]  Evgeny Nudler,et al.  Sensing Small Molecules by Nascent RNA A Mechanism to Control Transcription in Bacteria , 2002, Cell.

[13]  Nobuo Yamashita,et al.  Thiamine‐regulated gene expression of Aspergillus oryzae thiA requires splicing of the intron containing a riboswitch‐like domain in the 5′‐UTR , 2003, FEBS letters.

[14]  S. Silverman,et al.  Rube Goldberg goes (ribo)nuclear? Molecular switches and sensors made from RNA. , 2003, RNA.

[15]  Jeffrey E. Barrick,et al.  Metabolite-binding RNA domains are present in the genes of eukaryotes. , 2003, RNA.

[16]  J. Berger,et al.  Structure of the Rho Transcription Terminator Mechanism of mRNA Recognition and Helicase Loading , 2003, Cell.

[17]  M. Gelfand,et al.  Riboswitches: the oldest mechanism for the regulation of gene expression? , 2004, Trends in genetics : TIG.

[18]  A. Serganov,et al.  Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. , 2004, Chemistry & biology.

[19]  R. Breaker,et al.  Adenine riboswitches and gene activation by disruption of a transcription terminator , 2004, Nature Structural &Molecular Biology.

[20]  M. Gelfand,et al.  Comparative genomics of the methionine metabolism in Gram-positive bacteria: a variety of regulatory systems. , 2004, Nucleic acids research.

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

[22]  Zasha Weinberg,et al.  A Glycine-Dependent Riboswitch That Uses Cooperative Binding to Control Gene Expression , 2004, Science.

[23]  Ronald R. Breaker,et al.  Natural and engineered nucleic acids as tools to explore biology , 2004, Nature.

[24]  Jeffrey E. Barrick,et al.  Coenzyme B12 riboswitches are widespread genetic control elements in prokaryotes. , 2004, Nucleic acids research.

[25]  R. Breaker,et al.  Gene regulation by riboswitches , 2004, Nature Reviews Molecular Cell Biology.

[26]  H. White Coenzymes as fossils of an earlier metabolic state , 1976, Journal of Molecular Evolution.

[27]  Y. Ben-Asouli,et al.  RNase P: role of distinct protein cofactors in tRNA substrate recognition and RNA-based catalysis , 2005, Nucleic acids research.

[28]  D. Crothers,et al.  The kinetics of ligand binding by an adenine-sensing riboswitch. , 2005, Biochemistry.

[29]  D. Crothers,et al.  The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. , 2005, Molecular cell.

[30]  Jeffrey E. Barrick,et al.  Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria , 2005, Genome Biology.

[31]  R. Montange,et al.  Structure of the S-adenosylmethionine riboswitch regulatory mRNA element , 2006, Nature.

[32]  R. Breaker,et al.  Riboswitches as antibacterial drug targets , 2006, Nature Biotechnology.

[33]  Ronald R. Breaker,et al.  4 Riboswitches and the RNA World , 2006 .

[34]  T. Henkin,et al.  The SMK box is a new SAM-binding RNA for translational regulation of SAM synthetase , 2006, Nature Structural &Molecular Biology.

[35]  James L. Hougland,et al.  6 How the Group I Intron Works: A Case Study of RNA Structure and Function , 2006 .

[36]  R. Batey,et al.  Thermodynamic and kinetic characterization of ligand binding to the purine riboswitch aptamer domain. , 2006, Journal of molecular biology.

[37]  Jeffrey E. Barrick,et al.  Tandem Riboswitch Architectures Exhibit Complex Gene Control Functions , 2006, Science.

[38]  Eduardo A. Groisman,et al.  An RNA Sensor for Intracellular Mg2+ , 2006, Cell.

[39]  A. Lambowitz,et al.  Involvement of DEAD-box proteins in group I and group II intron splicing. Biochemical characterization of Mss116p, ATP hydrolysis-dependent and -independent mechanisms, and general RNA chaperone activity. , 2007, Journal of molecular biology.

[40]  Adam Roth,et al.  A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain , 2007, Nature Structural &Molecular Biology.

[41]  Michael E Webb,et al.  Thiamine biosynthesis in algae is regulated by riboswitches , 2007, Proceedings of the National Academy of Sciences.

[42]  Piotr Borsuk,et al.  l-Arginine influences the structure and function of arginase mRNA in Aspergillus nidulans , 2007, Biological chemistry.

[43]  Jeffrey E. Barrick,et al.  The distributions, mechanisms, and structures of metabolite-binding riboswitches , 2007, Genome Biology.

[44]  Ronald R. Breaker,et al.  Guanine riboswitch variants from Mesoplasma florum selectively recognize 2′-deoxyguanosine , 2007, Proceedings of the National Academy of Sciences.

[45]  E. Groisman,et al.  The intricate world of riboswitches. , 2007, Current opinion in microbiology.

[46]  Samuel Bocobza,et al.  Riboswitch-dependent gene regulation and its evolution in the plant kingdom. , 2007, Genes & development.

[47]  Irnov Irnov,et al.  Mechanism of mRNA destabilization by the glmS ribozyme. , 2007, Genes & development.

[48]  R. Breaker,et al.  Riboswitch Control of Gene Expression in Plants by Splicing and Alternative 3′ End Processing of mRNAs[W][OA] , 2007, The Plant Cell Online.

[49]  Catherine A. Wakeman,et al.  Structure and Mechanism of a Metal-Sensing Regulatory RNA , 2007, Cell.

[50]  R. Breaker,et al.  Control of alternative RNA splicing and gene expression by eukaryotic riboswitches , 2007, Nature.

[51]  R. Breaker,et al.  Ligand binding and gene control characteristics of tandem riboswitches in Bacillus anthracis. , 2007, RNA.

[52]  R. Breaker,et al.  Riboswitches in Eubacteria Sense the Second Messenger Cyclic Di-GMP , 2008, Science.

[53]  R. Batey,et al.  Structure of the SAM-II riboswitch bound to S-adenosylmethionine , 2008, Nature Structural &Molecular Biology.

[54]  T. Henkin,et al.  Crystal structures of the SAM-III/SMK riboswitch reveal the SAM-dependent translation inhibition mechanism , 2008, Nature Structural &Molecular Biology.

[55]  R. Breaker,et al.  Purine sensing by riboswitches , 2008, Biology of the cell.

[56]  P. Burguière,et al.  S-box and T-box riboswitches and antisense RNA control a sulfur metabolic operon of Clostridium acetobutylicum , 2008, Nucleic acids research.

[57]  Adam Roth,et al.  Confirmation of a second natural preQ1 aptamer class in Streptococcaceae bacteria. , 2008, RNA.

[58]  B. Suess,et al.  Engineered riboswitches: Overview, problems and trends , 2008, RNA biology.

[59]  R. Breaker,et al.  Riboswitches that sense S-adenosylhomocysteine and activate genes involved in coenzyme recycling. , 2008, Molecular cell.

[60]  Zasha Weinberg,et al.  The aptamer core of SAM-IV riboswitches mimics the ligand-binding site of SAM-I riboswitches. , 2008, RNA.

[61]  R. Breaker,et al.  Riboswitches that sense S-adenosylmethionine and S-adenosylhomocysteine. , 2008, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[62]  R. Breaker,et al.  A variant riboswitch aptamer class for S-adenosylmethionine common in marine bacteria. , 2009, RNA.

[63]  J. Johansson RNA thermosensors in bacterial pathogens. , 2009, Contributions to microbiology.

[64]  Ronald R. Breaker,et al.  Roseoflavin is a natural antibacterial compound that binds to FMN riboswitches and regulates gene expression , 2009, RNA biology.

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

[66]  R. Breaker,et al.  Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes , 2010, Genome Biology.

[67]  C. Yanofsky,et al.  Biochemical Features and Functional Implications of the RNA-Based T-Box Regulatory Mechanism , 2009, Microbiology and Molecular Biology Reviews.

[68]  R. Breaker Riboswitches: from ancient gene-control systems to modern drug targets. , 2009, Future microbiology.

[69]  R. Batey,et al.  A structural basis for the recognition of 2'-deoxyguanosine by the purine riboswitch. , 2009, Journal of molecular biology.

[70]  K. Hampel,et al.  A rate-limiting conformational step in the catalytic pathway of the glmS ribozyme. , 2009, Biochemistry.

[71]  R. Breaker,et al.  The structural and functional diversity of metabolite-binding riboswitches. , 2009, Annual review of biochemistry.

[72]  R. Breaker,et al.  Bacterial Riboswitch Discovery and Analysis , 2010 .

[73]  Andrea L Edwards,et al.  Riboswitches: structures and mechanisms. , 2011, Cold Spring Harbor perspectives in biology.