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Nucleotides adjacent to the ligand-binding pocket are linked to activity tuning in the purine riboswitch.

Stoddard CD, Widmann J, Trausch JJ, Marcano-Velázquez JG, Knight R, Batey RT
J Mol Biol 425 1596-611 (2013)
Related entries: 4fej, 4fel, 4fen, 4fep

Cited: 33 times
EuropePMC logo PMID: 23485418

Abstract

Direct sensing of intracellular metabolite concentrations by riboswitch RNAs provides an economical and rapid means to maintain metabolic homeostasis. Since many organisms employ the same class of riboswitch to control different genes or transcription units, it is likely that functional variation exists in riboswitches such that activity is tuned to meet cellular needs. Using a bioinformatic approach, we have identified a region of the purine riboswitch aptamer domain that displays conservation patterns linked to riboswitch activity. Aptamer domain compositions within this region can be divided into nine classes that display a spectrum of activities. Naturally occurring compositions in this region favor rapid association rate constants and slow dissociation rate constants for ligand binding. Using X-ray crystallography and chemical probing, we demonstrate that both the free and bound states are influenced by the composition of this region and that modest sequence alterations have a dramatic impact on activity. The introduction of non-natural compositions result in the inability to regulate gene expression in vivo, suggesting that aptamer domain activity is highly plastic and thus readily tunable to meet cellular needs.

Reviews - 4feo mentioned but not cited (1)

  1. Using RNA Sequence and Structure for the Prediction of Riboswitch Aptamer: A Comprehensive Review of Available Software and Tools. Antunes D, Jorge NAN, Caffarena ER, Passetti F. Front Genet 8 231 (2017)

Articles - 4feo mentioned but not cited (4)

  1. Effect of mutations on binding of ligands to guanine riboswitch probed by free energy perturbation and molecular dynamics simulations. Chen J, Wang X, Pang L, Zhang JZH, Zhu T. Nucleic Acids Res 47 6618-6631 (2019)
  2. Nucleotides adjacent to the ligand-binding pocket are linked to activity tuning in the purine riboswitch. Stoddard CD, Widmann J, Trausch JJ, Marcano-Velázquez JG, Knight R, Batey RT. J Mol Biol 425 1596-1611 (2013)
  3. RLDOCK method for predicting RNA-small molecule binding modes. Jiang Y, Chen SJ. Methods 197 97-105 (2022)
  4. Exergy Analysis of a Bio-System: Soil-Plant Interaction. Bararzadeh Ledari M, Saboohi Y, Valero A, Azamian S. Entropy (Basel) 23 E3 (2020)


Reviews citing this publication (11)

  1. RNA Structural Dynamics As Captured by Molecular Simulations: A Comprehensive Overview. Šponer J, Bussi G, Krepl M, Banáš P, Bottaro S, Cunha RA, Gil-Ley A, Pinamonti G, Poblete S, Jurečka P, Walter NG, Otyepka M. Chem Rev 118 4177-4338 (2018)
  2. Hierarchy of RNA functional dynamics. Mustoe AM, Brooks CL, Al-Hashimi HM. Annu Rev Biochem 83 441-466 (2014)
  3. RNA aptamers as genetic control devices: the potential of riboswitches as synthetic elements for regulating gene expression. Berens C, Groher F, Suess B. Biotechnol J 10 246-257 (2015)
  4. Riboswitch engineering - making the all-important second and third steps. Berens C, Suess B. Curr Opin Biotechnol 31 10-15 (2015)
  5. Gene regulation by structured mRNA elements. Wachter A. Trends Genet 30 172-181 (2014)
  6. Small molecules that interact with RNA: riboswitch-based gene control and its involvement in metabolic regulation in plants and algae. Bocobza SE, Aharoni A. Plant J 79 693-703 (2014)
  7. The purine riboswitch as a model system for exploring RNA biology and chemistry. Porter EB, Marcano-Velázquez JG, Batey RT. Biochim Biophys Acta 1839 919-930 (2014)
  8. Riboswitches for Controlled Expression of Therapeutic Transgenes Delivered by Adeno-Associated Viral Vectors. Tickner ZJ, Farzan M. Pharmaceuticals (Basel) 14 554 (2021)
  9. Seeing the PDB. Richardson JS, Richardson DC, Goodsell DS. J Biol Chem 296 100742 (2021)
  10. One platform, five brands: how nature cuts the cost on riboswitches. Grigg JC, Ke A. J Mol Biol 425 1593-1595 (2013)
  11. Characterization of conformational dynamics of bistable RNA by equilibrium and non-equilibrium NMR. Fürtig B, Reining A, Sochor F, Oberhauser EM, Heckel A, Schwalbe H. Curr Protoc Nucleic Acid Chem 55 11.13.1-16 (2014)

Articles citing this publication (17)

  1. Three-state mechanism couples ligand and temperature sensing in riboswitches. Reining A, Nozinovic S, Schlepckow K, Buhr F, Fürtig B, Schwalbe H. Nature 499 355-359 (2013)
  2. Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices. Ceres P, Garst AD, Marcano-Velázquez JG, Batey RT. ACS Synth Biol 2 463-472 (2013)
  3. Influence of Na+ and Mg2+ ions on RNA structures studied with molecular dynamics simulations. Fischer NM, Polêto MD, Steuer J, van der Spoel D. Nucleic Acids Res 46 4872-4882 (2018)
  4. Cobalamin riboswitches exhibit a broad range of ability to discriminate between methylcobalamin and adenosylcobalamin. Polaski JT, Webster SM, Johnson JE, Batey RT. J Biol Chem 292 11650-11658 (2017)
  5. Structure-guided mutational analysis of gene regulation by the Bacillus subtilis pbuE adenine-responsive riboswitch in a cellular context. Marcano-Velázquez JG, Batey RT. J Biol Chem 290 4464-4475 (2015)
  6. Tuning riboswitch-mediated gene regulation by rational control of aptamer ligand binding properties. Rode AB, Endoh T, Sugimoto N. Angew Chem Int Ed Engl 54 905-909 (2015)
  7. Allosteric mechanism of the V. vulnificus adenine riboswitch resolved by four-dimensional chemical mapping. Tian S, Kladwang W, Das R. Elife 7 e29602 (2018)
  8. High Affinity Binding of N2-Modified Guanine Derivatives Significantly Disrupts the Ligand Binding Pocket of the Guanine Riboswitch. Matyjasik MM, Hall SD, Batey RT. Molecules 25 E2295 (2020)
  9. Requirements for efficient ligand-gated co-transcriptional switching in designed variants of the B. subtilis pbuE adenine-responsive riboswitch in E. coli. Drogalis LK, Batey RT. PLoS One 15 e0243155 (2020)
  10. Structural basis for 2'-deoxyguanosine recognition by the 2'-dG-II class of riboswitches. Matyjasik MM, Batey RT. Nucleic Acids Res 47 10931-10941 (2019)
  11. A Highly Coupled Network of Tertiary Interactions in the SAM-I Riboswitch and Their Role in Regulatory Tuning. Wostenberg C, Ceres P, Polaski JT, Batey RT. J Mol Biol 427 3473-3490 (2015)
  12. Sequence elements distal to the ligand binding pocket modulate the efficiency of a synthetic riboswitch. Weigand JE, Gottstein-Schmidtke SR, Demolli S, Groher F, Duchardt-Ferner E, Wöhnert J, Suess B. Chembiochem 15 1627-1637 (2014)
  13. Base-intercalated and base-wedged stacking elements in 3D-structure of RNA and RNA-protein complexes. Baulin E, Metelev V, Bogdanov A. Nucleic Acids Res 48 8675-8685 (2020)
  14. Inactivation of the riboswitch-controlled GMP synthase GuaA in Clostridioides difficile is associated with severe growth defects and poor infectivity in a mouse model of infection. Smith-Peter E, Séguin DL, St-Pierre É, Sekulovic O, Jeanneau S, Tremblay-Tétreault C, Lamontagne AM, Jacques PÉ, Lafontaine DA, Fortier LC. RNA Biol 18 699-710 (2021)
  15. Ligand-mediated and tertiary interactions cooperatively stabilize the P1 region in the guanine-sensing riboswitch. Hanke CA, Gohlke H. PLoS One 12 e0179271 (2017)
  16. Transcriptional and translational S-box riboswitches differ in ligand-binding properties. Bhagdikar D, Grundy FJ, Henkin TM. J Biol Chem 295 6849-6860 (2020)
  17. Disentangling contact and ensemble epistasis in a riboswitch. Wonderlick DR, Widom JR, Harms MJ. Biophys J 122 1600-1612 (2023)


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