The UAA/GAN internal loop motif: a new RNA structural element that forms a cross-strand AAA stack and long-range tertiary interactions.

Analysis of aligned RNA sequences and high-resolution crystal structures has revealed a new RNA structural element, termed the UAA/GAN motif. Found in internal loops of the 23 S rRNA, as well as in RNase P RNA and group I and II introns, this six-nucleotide motif adopts a distinctive local structure that includes two base-pairs with non-canonical conformations and three conserved adenine bases, which form a cross-strand AAA stack in the minor groove. Most importantly, the motif invariably forms long-range tertiary contacts, as the AAA stack typically forms A-minor interactions and the flipped-out N nucleotide forms additional contacts that are specific to the structural context of each loop. The widespread presence of this motif and its propensity to form long-range contacts suggest that it plays a critical role in defining the architectures of structured RNAs.

[1]  H. Heus,et al.  Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops. , 1991, Science.

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

[3]  R. Gutell,et al.  Diversity of base-pair conformations and their occurrence in rRNA structure and RNA structural motifs. , 2004, Journal of molecular biology.

[4]  G. Kleywegt,et al.  Detecting folding motifs and similarities in protein structures. , 1997, Methods in enzymology.

[5]  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.

[6]  Jennifer A. Doudna,et al.  A universal mode of helix packing in RNA , 2001, Nature Structural Biology.

[7]  R. Gutell,et al.  Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. , 1994, Microbiological reviews.

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

[9]  D Gautheret,et al.  Identification of base-triples in RNA using comparative sequence analysis. , 1995, Journal of molecular biology.

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

[11]  C. Kundrot,et al.  RNA Tertiary Structure Mediation by Adenosine Platforms , 1996, Science.

[12]  R. Gutell,et al.  Comparative anatomy of 16-S-like ribosomal RNA. , 1985, Progress in nucleic acid research and molecular biology.

[13]  K. Swinger,et al.  Common and distinctive features of GNRA tetraloops based on a GUAA tetraloop structure at 1.4 A resolution. , 2003, RNA.

[14]  C R Woese,et al.  Architecture of ribosomal RNA: constraints on the sequence of "tetra-loops". , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[15]  T. Steitz,et al.  Metals, Motifs, and Recognition in the Crystal Structure of a 5S rRNA Domain , 1997, Cell.

[16]  G. Fox,et al.  Frequent occurrence of the T-loop RNA folding motif in ribosomal RNAs. , 2002, RNA.

[17]  R. Gutell,et al.  Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence. , 1980, Nucleic acids research.

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

[19]  Nan Yu,et al.  The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs , 2002, BMC Bioinformatics.

[20]  K. Flaherty,et al.  Model for an RNA tertiary interaction from the structure of an intermolecular complex between a GAAA tetraloop and an RNA helix , 1994, Nature.

[21]  Frank Schluenzen,et al.  High Resolution Structure of the Large Ribosomal Subunit from a Mesophilic Eubacterium , 2001, Cell.

[22]  S C Harvey,et al.  AA.AG@helix.ends: A:A and A:G base-pairs at the ends of 16 S and 23 S rRNA helices. , 2001, Journal of molecular biology.

[23]  Scott A. Strobel,et al.  Crystal structure of a self-splicing group I intron with both exons , 2004, Nature.

[24]  H. Noller,et al.  Involvement of 16S rRNA nucleotides G1338 and A1339 in discrimination of initiator tRNA. , 2005, Molecular cell.

[25]  I. Tinoco,et al.  RNA folding causes secondary structure rearrangement. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  V. Ramakrishnan,et al.  Recognition of Cognate Transfer RNA by the 30S Ribosomal Subunit , 2001, Science.

[27]  T. Cech,et al.  A preorganized active site in the crystal structure of the Tetrahymena ribozyme. , 1998, Science.

[28]  R. Gutell,et al.  A story: unpaired adenosine bases in ribosomal RNAs. , 2000, Journal of molecular biology.

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

[30]  G. Varani,et al.  The conformation of loop E of eukaryotic 5S ribosomal RNA. , 1993, Biochemistry.

[31]  J. Doudna,et al.  Specificity of RNA–RNA helix recognition , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[32]  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.

[33]  R. Lavery,et al.  Defining the structure of irregular nucleic acids: conventions and principles. , 1989, Journal of biomolecular structure & dynamics.

[34]  H. Bernstein.  Recent changes to RasMol, recombining the variants. , 2000, Trends in biochemical sciences.

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

[36]  R Lavery,et al.  The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. , 1988, Journal of biomolecular structure & dynamics.

[37]  R. Gutell,et al.  Secondary structure model for 23S ribosomal RNA. , 1981, Nucleic acids research.

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

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

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

[41]  D. Turner,et al.  Effects of GA mismatches on the structure and thermodynamics of RNA internal loops. , 1990, Biochemistry.

[42]  James W. Brown,et al.  The Ribonuclease P Database , 1994, Nucleic Acids Res..

[43]  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.

[44]  D Gautheret,et al.  A major family of motifs involving G.A mismatches in ribosomal RNA. , 1994, Journal of molecular biology.

[45]  R. Gutell,et al.  The accuracy of ribosomal RNA comparative structure models. , 2002, Current opinion in structural biology.

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

[47]  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.

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

[49]  Brent M. Znosko,et al.  Solution structure of an RNA internal loop with three consecutive sheared GA pairs. , 2005, Biochemistry.

[50]  R A Sayle,et al.  RASMOL: biomolecular graphics for all. , 1995, Trends in biochemical sciences.

[51]  D. Bartel,et al.  One sequence, two ribozymes: implications for the emergence of new ribozyme folds. , 2000, Science.

[52]  C. Kundrot,et al.  Crystal Structure of a Group I Ribozyme Domain: Principles of RNA Packing , 1996, Science.

[53]  Jung Lee.  Structural studies of ribosomal RNA based on cross-analysis of comparative models and three-dimensional crystal structures , 2003 .