Predicting translational diffusion of evolutionary conserved RNA structures by the nucleotide number

Ribonucleic acids are highly conserved essential parts of cellular life. RNA function is determined to a large extent by its hydrodynamic behaviour. The presented study proposes a strategy to predict the hydrodynamic behaviour of RNA single strands on the basis of the polymer size. By atom-level shell-modelling of high-resolution structures, hydrodynamic radius and diffusion coefficient of evolutionary conserved RNA single strands (ssRNA) were calculated. The diffusion coefficients D of 17–174 nucleotides (nt) containing ssRNA depended on the number of nucleotides N with D = 4.56 × 10−10 N−0.39 m2 s−1. The hydrodynamic radius RH depended on N with RH = 5.00 × 10−10 N0.38 m. An average ratio of the radius of gyration and the hydrodynamic radius of 0.98 ± 0.08 was calculated in solution. The empirical law was tested by in solution measured hydrodynamic radii and radii of gyration and was found to be highly consistent with experimental data of evolutionary conserved ssRNA. Furthermore, the hydrodynamic behaviour of several evolutionary unevolved ribonucleic acids could be predicted. Based on atom-level shell-modelling of high-resolution structures and experimental hydrodynamic data, empirical models are proposed, which enable to predict the translational diffusion coefficient and molecular size of short RNA single strands solely on the basis of the polymer size.

[1]  Udayan Mohanty,et al.  Compact and ordered collapse of randomly generated RNA sequences , 2005, Nature Structural &Molecular Biology.

[2]  M. Famulok,et al.  Fluorescence Correlation Spectroscopy as a New Method for the Investigation of Aptamer/Target Interactions , 2001, Biological chemistry.

[3]  T. N. Bhat,et al.  The Protein Data Bank , 2000, Nucleic Acids Res..

[4]  D. Thirumalai,et al.  Metal ion dependence of cooperative collapse transitions in RNA. , 2009, Journal of molecular biology.

[5]  P. Hraber,et al.  Global similarities in nucleotide base composition among disparate functional classes of single-stranded RNA imply adaptive evolutionary convergence. , 1996, RNA.

[6]  Wojciech Kasprzak,et al.  Solution structure of the cap-independent translational enhancer and ribosome-binding element in the 3′ UTR of turnip crinkle virus , 2010, Proceedings of the National Academy of Sciences.

[7]  Rob Knight,et al.  Natural selection is not required to explain universal compositional patterns in rRNA secondary structure categories. , 2006, RNA.

[8]  Sebastian Doniach,et al.  Structural transitions and thermodynamics of a glycine-dependent riboswitch from Vibrio cholerae. , 2007, Journal of molecular biology.

[9]  C. Will,et al.  The Spliceosome: Design Principles of a Dynamic RNP Machine , 2009, Cell.

[10]  J. García de la Torre,et al.  Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. , 2000, Biophysical journal.

[11]  V. V. Zinoviev,et al.  Application of the small‐angle X‐ray scattering technique for the study of equilibrium enzyme‐substrate interactions of phenylalanyl‐tRNA synthetase from E. coli with tRNAPhe , 1988, FEBS letters.

[12]  D. Svergun,et al.  Looking behind the beamstop: X-ray solution scattering studies of structure and conformational changes of biological macromolecules. , 2003, Methods in enzymology.

[13]  A. Ferré-D’Amaré,et al.  Idiosyncratically tuned switching behavior of riboswitch aptamer domains revealed by comparative small-angle X-ray scattering analysis. , 2010, RNA.

[14]  I. Serdyuk,et al.  Comparison of the structure of ribosomal 5S RNA from E. coli and from rat liver using X-ray scattering and dynamic light scattering , 2004, European Biophysics Journal.

[15]  K. V. van Holde,et al.  Frictional coefficients of multisubunit structures. I. Theory , 1967, Biopolymers.

[16]  Changbong Hyeon,et al.  Size, shape, and flexibility of RNA structures. , 2006, The Journal of chemical physics.

[17]  Batey,et al.  Tertiary Motifs in RNA Structure and Folding. , 1999, Angewandte Chemie.

[18]  D. Herschlag,et al.  The ligand-free state of the TPP riboswitch: a partially folded RNA structure. , 2010, Journal of molecular biology.

[19]  T. Pan,et al.  Extended structures in RNA folding intermediates are due to nonnative interactions rather than electrostatic repulsion. , 2010, Journal of molecular biology.

[20]  Rae M. Robertson,et al.  Diffusion of isolated DNA molecules: dependence on length and topology. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Måns Ehrenberg,et al.  Rotational brownian motion and fluorescence intensify fluctuations , 1974 .

[22]  J. Barciszewski,et al.  Structural similarity of E. coli 5S rRNA in solution and within the ribosome , 2004, Biopolymers.

[23]  D. Svergun,et al.  Characterization of a fluorophore binding RNA aptamer by fluorescence correlation spectroscopy and small angle X-ray scattering. , 2009, Analytical biochemistry.

[24]  J. García de la Torre,et al.  Hydrodynamic properties of rigid particles: comparison of different modeling and computational procedures. , 1999, Biophysical journal.

[25]  A. Ferré-D’Amaré,et al.  Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch , 2009, Nature Structural &Molecular Biology.

[26]  W. Gelbart,et al.  Predicting the sizes of large RNA molecules , 2008, Proceedings of the National Academy of Sciences.

[27]  W. Filipowicz,et al.  Repression of protein synthesis by miRNAs: how many mechanisms? , 2007, Trends in cell biology.

[28]  A. Ravve,et al.  Principles of Polymer Chemistry , 1995 .

[29]  Eric Westhof,et al.  Frequency and isostericity of RNA base pairs , 2009, Nucleic acids research.

[30]  J. Kieft,et al.  A preformed compact ribosome-binding domain in the cricket paralysis-like virus IRES RNAs. , 2005, RNA.

[31]  W. Webb,et al.  Thermodynamic Fluctuations in a Reacting System-Measurement by Fluorescence Correlation Spectroscopy , 1972 .

[32]  H. Gutfreund,et al.  Physical Biochemistry , 1970, Nature.

[33]  José García de la Torre,et al.  Comparison of theories for the translational and rotational diffusion coefficients of rod‐like macromolecules. Application to short DNA fragments , 1984 .

[34]  R. Garrett,et al.  Molecular model for 5-S RNA. A small-angle x-ray scattering study of native, denatured and aggregated 5-S RNA from Escherichia coli ribosomes. , 1976, European journal of biochemistry.

[35]  Compaction of a bacterial group I ribozyme coincides with the assembly of core helices. , 2004, Biochemistry.

[36]  Jacques Vergne,et al.  Self-association of adenine-dependent hairpin ribozymes , 2008, European Biophysics Journal.

[37]  J. Kieft,et al.  Toward a structural understanding of IRES RNA function. , 2009, Current opinion in structural biology.

[38]  Wojciech Kasprzak,et al.  Bridging the gap in RNA structure prediction. , 2007, Current opinion in structural biology.

[39]  D W Hukins,et al.  Structures of synthetic polynucleotides in the A-RNA and A'-RNA conformations: x-ray diffraction analyses of the molecular conformations of polyadenylic acid--polyuridylic acid and polyinosinic acid--polycytidylic acid. , 1973, Journal of molecular biology.

[40]  M Gerstein,et al.  Calculation of standard atomic volumes for RNA and comparison with proteins: RNA is packed more tightly. , 2005, Journal of molecular biology.

[41]  L. Malinina,et al.  Recognition of small interfering RNA by a viral suppressor of RNA silencing , 2003, Nature.

[42]  W. C. Johnson,et al.  Principles of physical biochemistry , 1998 .

[43]  T. C. B. McLeish,et al.  Polymer Physics , 2009, Encyclopedia of Complexity and Systems Science.

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

[45]  M. Vallazza,et al.  Structure of Free Thermus flavus 5 S rRNA at 1.3 nm Resolution from Synchrotron X-ray Solution Scattering* , 2000, The Journal of Biological Chemistry.

[46]  C. Wang,et al.  Laser light‐scattering analysis of the dimerization of transfer ribonucleic acids with complementary anticodons , 1981, Biopolymers.

[47]  R. Batey,et al.  Crystal Structure of the Lysine Riboswitch Regulatory mRNA Element* , 2008, Journal of Biological Chemistry.

[48]  N. Kholod,et al.  Mg2+ binding and structural stability of mature and in vitro synthesized unmodified Escherichia coli tRNAPhe. , 1998, Nucleic acids research.

[49]  G. Benedek,et al.  Observation of the spectrum of light scattered by solutions of biological macromolecules. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[50]  F. Perrin,et al.  Mouvement Brownien d'un ellipsoide (II). Rotation libre et dépolarisation des fluorescences. Translation et diffusion de molécules ellipsoidales , 1936 .

[51]  A. Serganov.  The long and the short of riboswitches. , 2009, Current opinion in structural biology.

[52]  Stephen Neidle,et al.  The structures of quadruplex nucleic acids and their drug complexes. , 2009, Current opinion in structural biology.

[53]  G. Meister,et al.  Fluorescence correlation spectroscopy and fluorescence cross-correlation spectroscopy reveal the cytoplasmic origination of loaded nuclear RISC in vivo in human cells , 2008, Nucleic acids research.

[54]  Feng Ding,et al.  On the significance of an RNA tertiary structure prediction. , 2010, RNA.

[55]  J. Kieft,et al.  Comparison and functional implications of the 3D architectures of viral tRNA-like structures. , 2009, RNA.

[56]  J. García de la Torre,et al.  Calculation of hydrodynamic properties of small nucleic acids from their atomic structure. , 2002, Nucleic acids research.

[57]  Discovering the RNA Double Helix and Hybridization , 2006, Cell.

[58]  John A Tainer,et al.  Improving small-angle X-ray scattering data for structural analyses of the RNA world. , 2010, RNA.