1l8v › Citations

Specificity of RNA-RNA helix recognition.

Battle DJ, Doudna JA
Proc Natl Acad Sci U S A 99 11676-81 (2002)
Cited: 70 times
EuropePMC logo PMID: 12189204

Abstract

Functional RNAs often form compact structures characterized by closely packed helices. Crystallographic analysis of several large RNAs revealed a prevalent interaction in which unpaired adenosine residues dock into the minor groove of a receptor helix. This A-minor motif, potentially the most important element responsible for global RNA architecture, has also been suggested to contribute to the fidelity of protein synthesis by discriminating against near-cognate tRNAs on the ribosome. The specificity of A-minor interactions is fundamental to RNA tertiary structure formation, as well as to their proposed role in translational accuracy. To investigate A-minor motif specificity, we analyzed mutations in an A-minor interaction within the Tetrahymena group I self-splicing intron. Thermodynamic and x-ray crystallographic results show that the A-minor interaction strongly prefers canonical base pairs over base mismatches in the receptor helix, enabling RNA interhelical packing through specific recognition of Watson-Crick minor groove geometry.

Articles - 1l8v mentioned but not cited (8)

  1. m(1)A and m(1)G disrupt A-RNA structure through the intrinsic instability of Hoogsteen base pairs. Zhou H, Kimsey IJ, Nikolova EN, Sathyamoorthy B, Grazioli G, McSally J, Bai T, Wunderlich CH, Kreutz C, Andricioaei I, Al-Hashimi HM. Nat Struct Mol Biol 23 803-810 (2016)
  2. Specificity of RNA-RNA helix recognition. Battle DJ, Doudna JA. Proc Natl Acad Sci U S A 99 11676-11681 (2002)
  3. Improving small-angle X-ray scattering data for structural analyses of the RNA world. Rambo RP, Tainer JA. RNA 16 638-646 (2010)
  4. Quantifying the relationship between sequence and three-dimensional structure conservation in RNA. Capriotti E, Marti-Renom MA. BMC Bioinformatics 11 322 (2010)
  5. iPARTS: an improved tool of pairwise alignment of RNA tertiary structures. Wang CW, Chen KT, Lu CL. Nucleic Acids Res 38 W340-7 (2010)
  6. Flexibility-rigidity index for protein-nucleic acid flexibility and fluctuation analysis. Opron K, Xia K, Burton Z, Wei GW. J Comput Chem 37 1283-1295 (2016)
  7. A conditional random fields method for RNA sequence-structure relationship modeling and conformation sampling. Wang Z, Xu J. Bioinformatics 27 i102-10 (2011)
  8. iPARTS2: an improved tool for pairwise alignment of RNA tertiary structures, version 2. Yang CH, Shih CT, Chen KT, Lee PH, Tsai PH, Lin JC, Yen CY, Lin TY, Lu CL. Nucleic Acids Res 44 W328-32 (2016)


Reviews citing this publication (12)

  1. The scanning mechanism of eukaryotic translation initiation. Hinnebusch AG. Annu Rev Biochem 83 779-812 (2014)
  2. What recent ribosome structures have revealed about the mechanism of translation. Schmeing TM, Ramakrishnan V. Nature 461 1234-1242 (2009)
  3. Structural insights into translational fidelity. Ogle JM, Ramakrishnan V. Annu Rev Biochem 74 129-177 (2005)
  4. Molecular mechanism of scanning and start codon selection in eukaryotes. Hinnebusch AG. Microbiol Mol Biol Rev 75 434-67, first page of table of contents (2011)
  5. Structural basis of the translational elongation cycle. Voorhees RM, Ramakrishnan V. Annu Rev Biochem 82 203-236 (2013)
  6. Analysis of RNA motifs. Leontis NB, Westhof E. Curr Opin Struct Biol 13 300-308 (2003)
  7. Elongation factors on the ribosome. Nilsson J, Nissen P. Curr Opin Struct Biol 15 349-354 (2005)
  8. Nucleic acid crystallography: current progress. Egli M. Curr Opin Chem Biol 8 580-591 (2004)
  9. Predicting and modeling RNA architecture. Westhof E, Masquida B, Jossinet F. Cold Spring Harb Perspect Biol 3 a003632 (2011)
  10. Face-time with TAR: Portraits of an HIV-1 RNA with diverse modes of effector recognition relevant for drug discovery. Chavali SS, Bonn-Breach R, Wedekind JE. J Biol Chem 294 9326-9341 (2019)
  11. Comparing the three-dimensional structures of Dicistroviridae IGR IRES RNAs with other viral RNA structures. Kieft JS. Virus Res 139 148-156 (2009)
  12. The importance of codon-anticodon interactions in translation elongation. Saint-Léger A, Ribas de Pouplana L. Biochimie 114 72-79 (2015)

Articles citing this publication (50)

  1. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Ogle JM, Murphy FV, Tarry MJ, Ramakrishnan V. Cell 111 721-732 (2002)
  2. Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Serganov A, Yuan YR, Pikovskaya O, Polonskaia A, Malinina L, Phan AT, Hobartner C, Micura R, Breaker RR, Patel DJ. Chem Biol 11 1729-1741 (2004)
  3. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Gromadski KB, Rodnina MV. Mol Cell 13 191-200 (2004)
  4. The role of modifications in codon discrimination by tRNA(Lys)UUU. Murphy FV, Ramakrishnan V, Malkiewicz A, Agris PF. Nat Struct Mol Biol 11 1186-1191 (2004)
  5. Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Gilbert SD, Rambo RP, Van Tyne D, Batey RT. Nat Struct Mol Biol 15 177-182 (2008)
  6. Programmed ribosomal frameshifting in decoding the SARS-CoV genome. Baranov PV, Henderson CM, Anderson CB, Gesteland RF, Atkins JF, Howard MT. Virology 332 498-510 (2005)
  7. Structure of the ribosome-bound cricket paralysis virus IRES RNA. Schüler M, Connell SR, Lescoute A, Giesebrecht J, Dabrowski M, Schroeer B, Mielke T, Penczek PA, Westhof E, Spahn CM. Nat Struct Mol Biol 13 1092-1096 (2006)
  8. A uniform response to mismatches in codon-anticodon complexes ensures ribosomal fidelity. Gromadski KB, Daviter T, Rodnina MV. Mol Cell 21 369-377 (2006)
  9. RNA helical packing in solution: NMR structure of a 30 kDa GAAA tetraloop-receptor complex. Davis JH, Tonelli M, Scott LG, Jaeger L, Williamson JR, Butcher SE. J Mol Biol 351 371-382 (2005)
  10. Kinetic redistribution of native and misfolded RNAs by a DEAD-box chaperone. Bhaskaran H, Russell R. Nature 449 1014-1018 (2007)
  11. Involvement of 16S rRNA nucleotides G1338 and A1339 in discrimination of initiator tRNA. Lancaster L, Noller HF. Mol Cell 20 623-632 (2005)
  12. Comprehensive features of natural and in vitro selected GNRA tetraloop-binding receptors. Geary C, Baudrey S, Jaeger L. Nucleic Acids Res 36 1138-1152 (2008)
  13. Cooperative tertiary interaction network guides RNA folding. Behrouzi R, Roh JH, Kilburn D, Briber RM, Woodson SA. Cell 149 348-357 (2012)
  14. Idiosyncratic tuning of tRNAs to achieve uniform ribosome binding. Olejniczak M, Dale T, Fahlman RP, Uhlenbeck OC. Nat Struct Mol Biol 12 788-793 (2005)
  15. Chemical basis of glycine riboswitch cooperativity. Kwon M, Strobel SA. RNA 14 25-34 (2008)
  16. Mutational analysis reveals two independent molecular requirements during transfer RNA selection on the ribosome. Cochella L, Brunelle JL, Green R. Nat Struct Mol Biol 14 30-36 (2007)
  17. Direct measurement of tertiary contact cooperativity in RNA folding. Sattin BD, Zhao W, Travers K, Chu S, Herschlag D. J Am Chem Soc 130 6085-6087 (2008)
  18. Compact and ordered collapse of randomly generated RNA sequences. Schultes EA, Spasic A, Mohanty U, Bartel DP. Nat Struct Mol Biol 12 1130-1136 (2005)
  19. Annotation of tertiary interactions in RNA structures reveals variations and correlations. Xin Y, Laing C, Leontis NB, Schlick T. RNA 14 2465-2477 (2008)
  20. Ribozyme-catalysed RNA synthesis using triplet building blocks. Attwater J, Raguram A, Morgunov AS, Gianni E, Holliger P. Elife 7 e35255 (2018)
  21. Codon reading by tRNAAla with modified uridine in the wobble position. Kothe U, Rodnina MV. Mol Cell 25 167-174 (2007)
  22. Asymmetry in RNA pseudoknots: observation and theory. Aalberts DP, Hodas NO. Nucleic Acids Res 33 2210-2214 (2005)
  23. The dimeric proto-ribosome: Structural details and possible implications on the origin of life. Agmon I. Int J Mol Sci 10 2921-2934 (2009)
  24. Representation, searching and discovery of patterns of bases in complex RNA structures. Harrison AM, South DR, Willett P, Artymiuk PJ. J Comput Aided Mol Des 17 537-549 (2003)
  25. The UAA/GAN internal loop motif: a new RNA structural element that forms a cross-strand AAA stack and long-range tertiary interactions. Lee JC, Gutell RR, Russell R. J Mol Biol 360 978-988 (2006)
  26. Low specificity of metal ion binding in the metal ion core of a folded RNA. Travers KJ, Boyd N, Herschlag D. RNA 13 1205-1213 (2007)
  27. Removal of covalent heterogeneity reveals simple folding behavior for P4-P6 RNA. Greenfeld M, Solomatin SV, Herschlag D. J Biol Chem 286 19872-19879 (2011)
  28. Conserved residues in yeast initiator tRNA calibrate initiation accuracy by regulating preinitiation complex stability at the start codon. Dong J, Munoz A, Kolitz SE, Saini AK, Chiu WL, Rahman H, Lorsch JR, Hinnebusch AG. Genes Dev 28 502-520 (2014)
  29. Steric complementarity in the decoding center is important for tRNA selection by the ribosome. Khade PK, Shi X, Joseph S. J Mol Biol 425 3778-3789 (2013)
  30. MicroRNA miR-92a-1 biogenesis and mRNA targeting is modulated by a tertiary contact within the miR-17~92 microRNA cluster. Chaulk SG, Xu Z, Glover MJ, Fahlman RP. Nucleic Acids Res 42 5234-5244 (2014)
  31. Correlation of RNA secondary structure statistics with thermodynamic stability and applications to folding. Wu JC, Gardner DP, Ozer S, Gutell RR, Ren P. J Mol Biol 391 769-783 (2009)
  32. RNA stabilization by a poly(A) tail 3'-end binding pocket and other modes of poly(A)-RNA interaction. Torabi SF, Vaidya AT, Tycowski KT, DeGregorio SJ, Wang J, Shu MD, Steitz TA, Steitz JA. Science 371 eabe6523 (2021)
  33. Unusual Base-Pairing Interactions in Monomer-Template Complexes. Zhang W, Tam CP, Wang J, Szostak JW. ACS Cent Sci 2 916-926 (2016)
  34. Kinetic and thermodynamic framework for P4-P6 RNA reveals tertiary motif modularity and modulation of the folding preferred pathway. Bisaria N, Greenfeld M, Limouse C, Pavlichin DS, Mabuchi H, Herschlag D. Proc Natl Acad Sci U S A 113 E4956-65 (2016)
  35. Quantitative analysis of deoxynucleotide substitutions in the codon-anticodon helix. Fahlman RP, Olejniczak M, Uhlenbeck OC. J Mol Biol 355 887-892 (2006)
  36. 2'-Fluoro substituents can mimic native 2'-hydroxyls within structured RNA. Forconi M, Schwans JP, Porecha RH, Sengupta RN, Piccirilli JA, Herschlag D. Chem Biol 18 949-954 (2011)
  37. Gene regulation by a glycine riboswitch singlet uses a finely tuned energetic landscape for helical switching. Torgerson CD, Hiller DA, Stav S, Strobel SA. RNA 24 1813-1827 (2018)
  38. Nuclease-Resistant c-di-AMP Derivatives That Differentially Recognize RNA and Protein Receptors. Meehan RE, Torgerson CD, Gaffney BL, Jones RA, Strobel SA. Biochemistry 55 837-849 (2016)
  39. Ribosome Structure Reveals Preservation of Active Sites in the Presence of a P-Site Wobble Mismatch. Svidritskiy E, Korostelev AA. Structure 23 2155-2161 (2015)
  40. Binding of misacylated tRNAs to the ribosomal A site. Dale T, Uhlenbeck OC. RNA 11 1610-1615 (2005)
  41. The structure of an E. coli tRNAfMet A1-U72 variant shows an unusual conformation of the A1-U72 base pair. Monestier A, Aleksandrov A, Coureux PD, Panvert M, Mechulam Y, Schmitt E. RNA 23 673-682 (2017)
  42. RNA gymnastics in mammalian signal recognition particle assembly. Wild K, Sinning I. RNA Biol 11 1330-1334 (2014)
  43. Molecular recognition properties of IGS-mediated reactions catalyzed by a Pneumocystis carinii group I intron. Johnson AK, Baum DA, Tye J, Bell MA, Testa SM. Nucleic Acids Res 31 1921-1934 (2003)
  44. Secondary structure encodes a cooperative tertiary folding funnel in the Azoarcus ribozyme. Mustoe AM, Al-Hashimi HM, Brooks CL. Nucleic Acids Res 44 402-412 (2016)
  45. "Deoxyribo nanonucleic acid"; antiparallel, parallel, and unparalleled. Egli M. Chem Biol 11 1027-1029 (2004)
  46. Exploratory studies to investigate a linked prebiotic origin of RNA and coded peptides. 3rd communication. Behaviour of 5-amino-1H-imidazole-4-carbonitrile derivatives. Ace K, Sutherland JD. Chem Biodivers 1 1678-1693 (2004)
  47. News Navigating the RNA folding landscape. Gonzalez RL. Nat Chem Biol 4 451-452 (2008)
  48. Age-Dependent and Tissue-Specific Alterations in the rDNA Clusters of the Panax ginseng C. A. Meyer Cultivated Cell Lines. Chelomina GN, Rozhkovan KV, Burundukova OL, Gorpenchenko TY, Khrolenko YA, Zhuravlev YN. Biomolecules 10 E1410 (2020)
  49. Are stop codons recognized by base triplets in the large ribosomal RNA subunit? Liang H, Landweber LF, Fresco JR. RNA 11 1478-1484 (2005)
  50. Context-dependence of T-loop Mediated Long-range RNA Tertiary Interactions. Hansen LN, Kletzien OA, Urquijo M, Schwanz LT, Batey RT. J Mol Biol 435 168070 (2023)


Quick links