Structural analysis of a class III preQ1 riboswitch reveals an aptamer distant from a ribosome-binding site regulated by fast dynamics

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 27, 2015, Pages E3485-E3494

  Liberman, Joseph A ^a   Suddala, Krishna C ^b   Aytenfisu, Asaminew ^a   Chan, Dalen ^c   Belashov, Ivan A ^a   Salim, Mohammad ^a   Mathews, David H ^a   Spitale, Robert C ^c   Walter, Nils G ^b   Wedekind, Joseph E ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Crystal structure; Gene regulation; Molecular dynamics; PreQ1 riboswitch; Single molecule fret

Indexed keywords

APTAMER; BACTERIAL RNA; 7-(AMINOMETHYL)-7-DEAZAGUANINE; PYRIMIDINONE DERIVATIVE; PYRROLE DERIVATIVE; QUEUOSINE; RIBOSWITCH;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; FAECALIBACTERIUM PRAUSNITZII; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE CONTROL; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; RIBOSWITCH; RNA STRUCTURE; RNA TRANSLATION; THERMODYNAMICS; CHEMISTRY; CLOSTRIDIUM; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RNA FOLDING; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS); FAECALIBACTERIUM PRAUSNITZII; RUMEX;

APTAMERS, NUCLEOTIDE; BASE SEQUENCE; BINDING SITES; CLOSTRIDIUM; CRYSTALLOGRAPHY, X-RAY; KINETICS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NUCLEOSIDE Q; PYRIMIDINONES; PYRROLES; RIBOSOMES; RIBOSWITCH; RNA FOLDING; RNA, BACTERIAL; THERMODYNAMICS;

EID: 84936136220     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1503955112     Document Type: Article

References (71)

1. Serganov A, Nudler E (2013) A decade of riboswitches. Cell 152(1-2):17-24.
2. Roth A, Breaker RR (2009) The structural and functional diversity of metabolitebinding riboswitches. Annu Rev Biochem 78:305-334.
3. Sudarsan N, Cohen-Chalamish S, Nakamura S, Emilsson GM, Breaker RR (2005) Thiamine pyrophosphate riboswitches are targets for the antimicrobial compound pyrithiamine. Chem Biol 12(12):1325-1335.
4. Blount KF, Wang JX, Lim J, Sudarsan N, Breaker RR (2007) Antibacterial lysine analogs that target lysine riboswitches. Nat Chem Biol 3(1):44-49.
5. Lee ER, Blount KF, Breaker RR (2009) Roseoflavin is a natural antibacterial compound that binds to FMN riboswitches and regulates gene expression. RNA Biol 6(2):187-194.
6. Breaker RR (2012) Riboswitches and the RNA world. Cold Spring Harb Perspect Biol 4(2):a003566.
7. Peselis A, Serganov A (2014) Structure and function of pseudoknots involved in gene expression control. Wiley Interdiscip Rev RNA 5(6):803-822.
8. Gilbert SD, Rambo RP, Van Tyne D, Batey RT (2008) Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat Struct Mol Biol 15(2):177-182.
9. Spitale RC, Torelli AT, Krucinska J, Bandarian V, Wedekind JE (2009) The structural basis for recognition of the PreQ0 metabolite by an unusually small riboswitch aptamer domain. J Biol Chem 284(17):11012-11016.
10. Haller A, Rieder U, Aigner M, Blanchard SC, Micura R (2011) Conformational capture of the SAM-II riboswitch. Nat Chem Biol 7(6):393-400.
11. Suddala KC, et al. (2013) Single transcriptional and translational preQ1 riboswitches adopt similar pre-folded ensembles that follow distinct folding pathways into the same ligand-bound structure. Nucleic Acids Res 41(22):10462-10475.
12. Kang M, Eichhorn CD, Feigon J (2014) Structural determinants for ligand capture by a class II preQ1 riboswitch. Proc Natl Acad Sci USA 111(6):E663-E671.
13. Jenkins JL, Krucinska J, McCarty RM, Bandarian V, Wedekind JE (2011) Comparison of a preQ1 riboswitch aptamer in metabolite-bound and free states with implications for gene regulation. J Biol Chem 286(28):24626-24637.
14. Kang M, Peterson R, Feigon J (2009) Structural Insights into riboswitch control of the biosynthesis of queuosine, a modified nucleotide found in the anticodon of tRNA. Mol Cell 33(6):784-790.
15. Klein DJ, Edwards TE, Ferré-D'Amaré AR (2009) Cocrystal structure of a class I preQ1 riboswitch reveals a pseudoknot recognizing an essential hypermodified nucleobase. Nat Struct Mol Biol 16(3):343-344.
16. Soulière MF, et al. (2013) Tuning a riboswitch response through structural extension of a pseudoknot. Proc Natl Acad Sci USA 110(35):E3256-E3264.
17. Ren A, Rajashankar KR, Patel DJ (2012) Fluoride ion encapsulation by Mg2+ ions and phosphates in a fluoride riboswitch. Nature 486(7401):85-89.
18. Liberman JA, Salim M, Krucinska J, Wedekind JE (2013) Structure of a class II preQ1 riboswitch reveals ligand recognition by a new fold. Nat Chem Biol 9(6):353-355.
19. Trausch JJ, et al. (2014) Structural basis for diversity in the SAM clan of riboswitches. Proc Natl Acad Sci USA 111(18):6624-6629.
20. Gao A, Serganov A (2014) Structural insights into recognition of c-di-AMP by the ydaO riboswitch. Nat Chem Biol 10(9):787-792.
21. Jones CP, Ferré-D'Amaré AR (2014) Crystal structure of a c-di-AMP riboswitch reveals an internally pseudo-dimeric RNA. EMBO J 33(22):2692-2703.
22. Ren A, Patel DJ (2014) c-di-AMP binds the ydaO riboswitch in two pseudo-symmetryrelated pockets. Nat Chem Biol 10(9):780-786.
23. 1 riboswitch classes. Chem Biol 21(7):880-889.
24. Noguchi S, Nishimura Y, Hirota Y, Nishimura S (1982) Isolation and characterization of an Escherichia coli mutant lacking tRNA-guanine transglycosylase. Function and biosynthesis of queuosine in tRNA. J Biol Chem 257(11):6544-6550.
25. Harada F, Nishimura S (1972) Possible anticodon sequences of tRNA His, tRNA Asm, and tRNA Asp from Escherichia coli B. Universal presence of nucleoside Q in the first postion of the anticondons of these transfer ribonucleic acids. Biochemistry 11(2): 301-308.
26. Bienz M, Kubli E (1981) Wild-type transfer-RNA GTyr reads the TMV RNA stop codon, but Q-base-modified transfer-RNA GTyr does not. Nature 294(5837):188-190.
27. Meier F, Suter B, Grosjean H, Keith G, Kubli E (1985) Queuosine modification of the wobble base in tRNAHis influences 'in vivo' decoding properties. EMBO J 4(3): 823-827.
28. Urbonavièius J, Qian Q, Durand JM, Hagervall TG, Björk GR (2001) Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J 20(17):4863-4873.
29. Katze JR, Basile B, McCloskey JA (1982) Queuine, a modified base incorporated posttranscriptionally into eukaryotic transfer RNA: Wide distribution in nature. Science 216(4541):55-56.
30. Rakovich T, et al. (2011) Queuosine deficiency in eukaryotes compromises tyrosine production through increased tetrahydrobiopterin oxidation. J Biol Chem 286(22): 19354-19363.
31. Durand JM, et al. (1994) vacC, a virulence-associated chromosomal locus of Shigella flexneri, is homologous to tgt, a gene encoding tRNA-guanine transglycosylase (Tgt) of Escherichia coli K-12. J Bacteriol 176(15):4627-4634.
32. Meyer MM, Roth A, Chervin SM, Garcia GA, Breaker RR (2008) Confirmation of a second natural preQ1 aptamer class in Streptococcaceae bacteria. RNA 14(4):685-695.
33. Roth A, et al. (2007) A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain. Nat Struct Mol Biol 14(4):308-317.
34. Smith KD, Shanahan CA, Moore EL, Simon AC, Strobel SA (2011) Structural basis of differential ligand recognition by two classes of bis-(3′-5′)-cyclic dimeric guanosine monophosphate-binding riboswitches. Proc Natl Acad Sci USA 108(19):7757-7762.
35. Savinov A, Perez CF, Block SM (2014) Single-molecule studies of riboswitch folding. Biochim Biophys Acta 1839(10):1030-1045.
36. Lippa GM, et al. (2012) Crystallographic analysis of small ribozymes and riboswitches. Methods Mol Biol 848:159-184.
37. Wedekind JE, McKay DB (2000) Purification, crystallization, and X-ray diffraction analysis of small ribozymes. Methods Enzymol 317:149-168.
38. 1 riboswitches. Methods Enzymol 549:435-450.
39. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326.
40. Kabsch W (2010) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr D Biol Crystallogr 66(Pt 2):133-144.
41. Wilkinson KA, Merino EJ, Weeks KM (2006) Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): Quantitative RNA structure analysis at single nucleotide resolution. Nat Protoc 1(3):1610-1616.
42. Spitale RC, et al. (2013) RNA SHAPE analysis in living cells. Nat Chem Biol 9(1):18-20.
43. Toukmaji A, Sagui C, Board J, Darden T (2000) Efficient particle-mesh Ewald based approach to fixed and induced dipolar interactions. J Chem Phys 113:10913-10927.
44. Sagui C, Pedersen LG, Darden TA (2004) Towards an accurate representation of electrostatics in classical force fields: Efficient implementation of multipolar interactions in biomolecular simulations. J Chem Phys 120(1):73-87.
45. Miyamoto S, Kollman PA (1992) Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem 13:952-962.
46. Akiyama BM, Stone MD (2009) Assembly of complex RNAs by splinted ligation. Methods Enzymol 469:27-46.
47. Suddala KC, Walter NG (2014) Riboswitch structure and dynamics by smFRET microscopy. Methods Enzymol 549:343-373.
48. Soltis SM, et al. (2008) New paradigm for macromolecular crystallography experiments at SSRL: Automated crystal screening and remote data collection. Acta Crystallogr D Biol Crystallogr 64(Pt 12):1210-1221.
49. Weiss MS (2001) Global indicators of X-ray data quality. J Appl Cryst 34:130-135.
50. Karplus PA, Diederichs K (2012) Linking crystallographic model and data quality. Science 336(6084):1030-1033.
51. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.
52. McCarty RM, Bandarian V (2012) Biosynthesis of pyrrolopyrimidines. Bioorg Chem 43: 15-25.
53. Keel AY, Rambo RP, Batey RT, Kieft JS (2007) A general strategy to solve the phase problem in RNA crystallography. Structure 15(7):761-772.
54. Aalberts DP, Nandagopal N (2010) A two-length-scale polymer theory for RNA loop free energies and helix stacking. RNA 16(7):1350-1355.
55. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
56. Cheatham TE, 3rd, Cieplak P, Kollman PA (1999) A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J Biomol Struct Dyn 16(4):845-862.
57. Pérez A, et al. (2007) Refinement of the AMBER force field for nucleic acids: Improving the description of alpha/gamma conformers. Biophys J 92(11):3817-3829.
58. Zgarbová M, et al. (2011) Refinement of the Cornell et al. nucleic acids force field based on reference quantum chemical calculations of glycosidic torsion profiles. J Chem Theory Comput 7(9):2886-2902.
59. Aytenfisu AH, Spasic A, Seetin MG, Serafini J, Mathews DH (2014) Modified AMBER force field correctly models the conformational preference for tandem GA pairs in RNA. J Chem Theory Comput 10(3):1292-1301.
60. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79(2):926-935.
61. rd (2008) Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J Phys Chem B 112(30):9020-9041.
62. rd (2009) Molecular dynamics simulations of the dynamic and energetic properties of alkali and halide ions using water-model-specific ion parameters. J Phys Chem B 113(40):13279-13290.
63. Case DA, et al. (2014) AMBER (University of California, San Francisco).
64. Bayly CI, Cieplak P, Cornell WD, Kollman PA (1993) A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model. J Phys Chem 97(40):10269-10280.
65. Dupradeau FY, et al. (2010) The R.E.D. tools: Advances in RESP and ESP charge derivation and force field library building. Phys Chem Chem Phys 12(28):7821-7839.
66. Vanquelef E, et al. (2011) R.E.D. Server: A web service for deriving RESP and ESP charges and building force field libraries for new molecules and molecular fragments. Nucleic Acids Res 39(Web Server issue):W511-7.
67. Case DA, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26(16):1668-1688.
68. Qin F (2004) Restoration of single-channel currents using the segmental k-means method based on hidden Markov modeling. Biophys J 86(3):1488-1501.
69. Blanco M, Walter NG (2010) Analysis of complex single-molecule FRET time trajectories. Methods Enzymol 472:153-178.
70. Han K, Byun Y (2003) PSEUDOVIEWER2: Visualization of RNA pseudoknots of any type. Nucleic Acids Res 31(13):3432-3440.
71. Terwilliger TC, et al. (2008) Iterative-build OMIT maps: Map improvement by iterative model building and refinement without model bias. Acta Crystallogr D Biol Crystallogr 64(Pt 5):515-524.