The interaction networks of structured RNAs.

All pairwise interactions occurring between bases which could be detected in three-dimensional structures of crystallized RNA molecules are annotated on new planar diagrams. The diagrams attempt to map the underlying complex networks of base–base interactions and, especially, they aim at conveying key relationships between helical domains: co-axial stacking, bending and all Watson–Crick as well as non-Watson–Crick base pairs. Although such wiring diagrams cannot replace full stereographic images for correct spatial understanding and representation, they reveal structural similarities as well as the conserved patterns and distances between motifs which are present within the interaction networks of folded RNAs of similar or unrelated functions. Finally, the diagrams could help devising methods for meaningfully transforming RNA structures into graphs amenable to network analysis.

[1]  M. Nomura,et al.  Reconstitution of 50S Ribosomal Subunits from Dissociated Molecular Components , 1970, Nature.

[2]  E Westhof,et al.  New loop-loop tertiary interactions in self-splicing introns of subgroup IC and ID: a complete 3D model of the Tetrahymena thermophila ribozyme. , 1996, Chemistry & biology.

[3]  V. Ramakrishnan,et al.  Structure of a bacterial 30S ribosomal subunit at 5.5 Å resolution , 1999, Nature.

[4]  N. Ban,et al.  Structure of the Eukaryotic Thiamine Pyrophosphate Riboswitch with Its Regulatory Ligand , 2006, Science.

[5]  John M. Burke,et al.  Four ribose 2'-hydroxyl groups essential for catalytic function of the hairpin ribozyme. , 1993, The Journal of biological chemistry.

[6]  Frédéric H.-T. Allain,et al.  Solution structure of the loop B domain from the hairpin ribozyme , 1999, Nature Structural Biology.

[7]  T. Earnest,et al.  Crystal Structure of the Ribosome at 5.5 Å Resolution , 2001, Science.

[8]  H. Noller,et al.  Identification of a site on 23S ribosomal RNA located at the peptidyl transferase center. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[9]  E. Westhof,et al.  Architecture of a Diels-Alderase ribozyme with a preformed catalytic pocket. , 2004, Chemistry & biology.

[10]  E Westhof,et al.  The A-minor motifs in the decoding recognition process. , 2006, Biochimie.

[11]  J. Holton,et al.  Structures of the Bacterial Ribosome at 3.5 Å Resolution , 2005, Science.

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

[13]  Eric Westhof,et al.  Crystal structures of complexes between aminoglycosides and decoding A site oligonucleotides: role of the number of rings and positive charges in the specific binding leading to miscoding , 2005, Nucleic acids research.

[14]  Quentin Vicens,et al.  Atomic level architecture of group I introns revealed. , 2006, Trends in biochemical sciences.

[15]  A. S. Krasilnikov,et al.  Basis for Structural Diversity in Homologous RNAs , 2004, Science.

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

[17]  James W. Brown.  The ribonuclease P database , 1998, Nucleic Acids Res..

[18]  Harry F Noller,et al.  RNA Structure: Reading the Ribosome , 2005, Science.

[19]  F. Michel,et al.  Frequent use of the same tertiary motif by self‐folding RNAs. , 1995, The EMBO journal.

[20]  V. Ramakrishnan,et al.  Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16 S RNA. , 2002, Journal of molecular biology.

[21]  R. Nussinov,et al.  Residues crucial for maintaining short paths in network communication mediate signaling in proteins , 2006, Molecular systems biology.

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

[23]  Eric Westhof,et al.  Recurrent structural RNA motifs, Isostericity Matrices and sequence alignments , 2005, Nucleic acids research.

[24]  E. Westhof,et al.  A common motif organizes the structure of multi-helix loops in 16 S and 23 S ribosomal RNAs. , 1998, Journal of molecular biology.

[25]  G. Culver,et al.  Assembly of the 30 S ribosomal subunit : Positioning ribosomal protein S 13 in the S 7 assembly branch , 2004 .

[26]  A. Spirin,et al.  Structural dynamics of translating ribosomes. , 1992, Biochimie.

[27]  Gil Amitai,et al.  Network analysis of protein structures identifies functional residues. , 2004, Journal of molecular biology.

[28]  H. Tabak,et al.  Structural conventions for group I introns. , 1987, Nucleic acids research.

[29]  D. Patel,et al.  RNA bulges as architectural and recognition motifs. , 2000, Structure.

[30]  S. Woodson,et al.  Structure and assembly of group I introns. , 2005, Current opinion in structural biology.

[31]  P. Moore,et al.  Structural motifs in RNA. , 1999, Annual review of biochemistry.

[32]  A. Ferré-D’Amaré,et al.  Crystal structure of a hepatitis delta virus ribozyme , 1998, Nature.

[33]  T. Earnest,et al.  X-ray crystal structures of 70S ribosome functional complexes. , 1999, Science.

[34]  E. Westhof,et al.  Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. , 1990, Journal of molecular biology.

[35]  A. S. Krasilnikov,et al.  On the occurrence of the T-loop RNA folding motif in large RNA molecules. , 2003, RNA.

[36]  A. Ferré-D’Amaré,et al.  Crystal structure of a hairpin ribozyme–inhibitor complex with implications for catalysis , 2001, Nature.

[37]  G. Culver,et al.  Assembly of the 30S ribosomal subunit: positioning ribosomal protein S13 in the S7 assembly branch. , 2004, RNA.

[38]  S. Strogatz.  Exploring complex networks , 2001, Nature.

[39]  Albert,et al.  Emergence of scaling in random networks , 1999, Science.

[40]  S. Strobel,et al.  RNA kink turns to the left and to the right. , 2004, RNA.

[41]  E. Westhof,et al.  Inter-domain cross-linking and molecular modelling of the hairpin ribozyme. , 1997, Journal of molecular biology.

[42]  T. Steitz,et al.  The kink‐turn: a new RNA secondary structure motif , 2001, The EMBO journal.

[43]  E. Westhof,et al.  A three-dimensional model of hepatitis delta virus ribozyme based on biochemical and mutational analyses , 1994, Current Biology.

[44]  James W. Brown,et al.  The RNA Ontology Consortium: an open invitation to the RNA community. , 2006, RNA.

[45]  E. Westhof,et al.  RNA folding: beyond Watson-Crick pairs. , 2000, Structure.

[46]  Rick Russell,et al.  The UAA/GAN internal loop motif: a new RNA structural element that forms a cross-strand AAA stack and long-range tertiary interactions. , 2006, Journal of molecular biology.

[47]  E Westhof,et al.  Derivation of the three-dimensional architecture of bacterial ribonuclease P RNAs from comparative sequence analysis. , 1998, Journal of molecular biology.

[48]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[49]  Thomas A Steitz,et al.  Structural insights into peptide bond formation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[50]  A. Ferré-D’Amaré,et al.  A nested double pseudoknot is required for self-cleavage activity of both the genomic and antigenomic hepatitis delta virus ribozymes. , 1999, RNA.

[51]  E. Westhof,et al.  The building blocks and motifs of RNA architecture. , 2006, Current opinion in structural biology.

[52]  T. Steitz,et al.  The contribution of metal ions to the structural stability of the large ribosomal subunit. , 2004, RNA.

[53]  Eric Westhof,et al.  Sequence to Structure (S2S): display, manipulate and interconnect RNA data from sequence to structure , 2005, Bioinform..

[54]  F. Major,et al.  RNA canonical and non-canonical base pairing types: a recognition method and complete repertoire. , 2002, Nucleic acids research.

[55]  F. Michel,et al.  Rules for RNA recognition of GNRA tetraloops deduced by in vitro selection: comparison with in vivo evolution , 1997, The EMBO journal.

[56]  E. Westhof,et al.  Riboswitch structures: purine ligands replace tertiary contacts. , 2005, Chemistry & biology.

[57]  A. Barabasi,et al.  Network biology: understanding the cell's functional organization , 2004, Nature Reviews Genetics.

[58]  A Klug,et al.  The crystal structure of an all-RNA hammerhead ribozyme. , 1995, Nucleic acids symposium series.

[59]  Scott A Strobel,et al.  Crystal structure of a group I intron splicing intermediate. , 2004, RNA.

[60]  T. Steitz,et al.  The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. , 2000, Science.

[61]  A. Barabasi,et al.  Hierarchical Organization of Modularity in Metabolic Networks , 2002, Science.

[62]  Victoria A. Higman,et al.  Uncovering network systems within protein structures. , 2003, Journal of molecular biology.

[63]  B. Dujon,et al.  Comparison of fungal mitochondrial introns reveals extensive homologies in RNA secondary structure. , 1982, Biochimie.

[64]  B. Golden,et al.  Crystal structure of a phage Twort group I ribozyme–product complex , 2005, Nature Structural &Molecular Biology.

[65]  A. T. Perrotta,et al.  A pseudoknot-like structure required for efficient self-cleavage of hepatitis delta virus RNA , 1991, Nature.

[66]  J. Poehlsgaard,et al.  Modifications in Thermus thermophilus 23 S Ribosomal RNA Are Centered in Regions of RNA-RNA Contact* , 2006, Journal of Biological Chemistry.

[67]  A. Serganov,et al.  Structural basis for Diels-Alder ribozyme-catalyzed carbon-carbon bond formation , 2005, Nature Structural &Molecular Biology.

[68]  R. Montange,et al.  Structure of a natural guanine-responsive riboswitch complexed with the metabolite hypoxanthine , 2004, Nature.

[69]  John D. Westbrook,et al.  Tools for the automatic identification and classification of RNA base pairs , 2003, Nucleic Acids Res..

[70]  J Frank,et al.  Three-dimensional reconstruction of the Escherichia coli 30 S ribosomal subunit in ice. , 1996, Journal of molecular biology.

[71]  E Westhof,et al.  Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site. , 2001, Structure.

[72]  R. Gutell,et al.  The lonepair triloop: a new motif in RNA structure. , 2003, Journal of molecular biology.

[73]  J. Kowalak,et al.  Posttranscriptional Modification of the Central Loop of Domain V in Escherichia coli 23 S Ribosomal RNA (*) , 1995, The Journal of Biological Chemistry.

[74]  J. Szostak,et al.  Phylogenetic and genetic evidence for base-triples in the catalytic domain of group I introns , 1990, Nature.

[75]  A. S. Krasilnikov,et al.  Crystal structure of the RNA component of bacterial ribonuclease P , 2005, Nature.

[76]  Thomas A. Steitz,et al.  RNA tertiary interactions in the large ribosomal subunit: The A-minor motif , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[77]  N. B. Leontisa,et al.  Motif prediction in ribosomal RNAs Lessons and prospects for automated motif prediction in homologous RNA molecules , 2002 .

[78]  T. Cech,et al.  Structure of the Tetrahymena ribozyme: base triple sandwich and metal ion at the active site. , 2004, Molecular cell.

[79]  Anastasia Khvorova,et al.  Fast cleavage kinetics of a natural hammerhead ribozyme. , 2004, Journal of the American Chemical Society.

[80]  E. Westhof,et al.  Geometric nomenclature and classification of RNA base pairs. , 2001, RNA.

[81]  A. Serganov,et al.  Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch , 2006, Nature.

[82]  C. Vonrhein,et al.  Structure of the 30S ribosomal subunit , 2000, Nature.

[83]  A. Serganov,et al.  The crystal structure of UUCG tetraloop. , 2000, Journal of molecular biology.

[84]  E. Westhof,et al.  Analysis of RNA motifs. , 2003, Current opinion in structural biology.

[85]  E. Westhof,et al.  Topology of three-way junctions in folded RNAs. , 2006, RNA.

[86]  N. Pace,et al.  Analysis of the tertiary structure of the ribonuclease P ribozyme-substrate complex by site-specific photoaffinity crosslinking. , 1997, RNA.

[87]  A. S. Krasilnikov,et al.  Crystal structure of the specificity domain of ribonuclease P , 2003, Nature.

[88]  R. Gutell,et al.  Representation of the secondary and tertiary structure of group I introns , 1994, Nature Structural Biology.

[89]  E. Westhof,et al.  A three‐dimensional perspective on exon binding by a group II self‐splicing intron , 2000, The EMBO journal.

[90]  T. Steitz,et al.  The structural basis of ribosome activity in peptide bond synthesis. , 2000, Science.

[91]  E. Westhof,et al.  Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity , 2003, Nature Structural Biology.

[92]  N. Pace,et al.  The secondary structure of ribonuclease P RNA, the catalytic element of a ribonucleoprotein enzyme , 1988, Cell.

[93]  N. Pace,et al.  Crystal structure of a bacterial ribonuclease P RNA. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[94]  P. Gendron,et al.  Quantitative analysis of nucleic acid three-dimensional structures. , 2001, Journal of molecular biology.

[95]  W. Scott,et al.  Tertiary Contacts Distant from the Active Site Prime a Ribozyme for Catalysis , 2006, Cell.

[96]  J. Frank,et al.  A model of the translational apparatus based on a three-dimensional reconstruction of the Escherichia coli ribosome. , 1995, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[97]  M. Nomura,et al.  Assembly Mapping of 30S Ribosomal Proteins from E. coli , 1970, Nature.

[98]  Jef Rozenski,et al.  The Small Subunit rRNA Modification Database , 2004, Nucleic Acids Res..

[99]  D. Lilley,et al.  Folding of the natural hammerhead ribozyme is enhanced by interaction of auxiliary elements. , 2004, RNA.