RNA tertiary interactions in the large ribosomal subunit: The A-minor motif

Analysis of the 2.4-Å resolution crystal structure of the large ribosomal subunit from Haloarcula marismortui reveals the existence of an abundant and ubiquitous structural motif that stabilizes RNA tertiary and quaternary structures. This motif is termed the A-minor motif, because it involves the insertion of the smooth, minor groove edges of adenines into the minor groove of neighboring helices, preferentially at C-G base pairs, where they form hydrogen bonds with one or both of the 2′ OHs of those pairs. A-minor motifs stabilize contacts between RNA helices, interactions between loops and helices, and the conformations of junctions and tight turns. The interactions between the 3′ terminal adenine of tRNAs bound in either the A site or the P site with 23S rRNA are examples of functionally significant A-minor interactions. The A-minor motif is by far the most abundant tertiary structure interaction in the large ribosomal subunit; 186 adenines in 23S and 5S rRNA participate, 68 of which are conserved. It may prove to be the universally most important long-range interaction in large RNA structures.

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

[2]  F. Schluenzen,et al.  Structure of Functionally Activated Small Ribosomal Subunit at 3.3 Å Resolution , 2000, Cell.

[3]  B. Lee,et al.  The interpretation of protein structures: estimation of static accessibility. , 1971, Journal of molecular biology.

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

[5]  R J Read,et al.  Crystallography & NMR system: A new software suite for macromolecular structure determination. , 1998, Acta crystallographica. Section D, Biological crystallography.

[6]  Mike Carson,et al.  RIBBONS 2.0 , 1991 .

[7]  P. Kraulis A program to produce both detailed and schematic plots of protein structures , 1991 .

[8]  B. Clark,et al.  The ternary complex of aminoacylated tRNA and EF-Tu-GTP. Recognition of a bond and a fold. , 1996, Biochimie.

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

[10]  P. Moore,et al.  The loop E-loop D region of Escherichia coli 5S rRNA: the solution structure reveals an unusual loop that may be important for binding ribosomal proteins. , 1997, Structure.

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

[12]  M Yarus,et al.  An inhibitor of ribosomal peptidyl transferase using transition-state analogy. , 1995, Biochemistry.

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

[14]  V. Ramakrishnan,et al.  Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics , 2000, Nature.

[15]  E. Kandel,et al.  Control of Memory Formation Through Regulated Expression of a CaMKII Transgene , 1996, Science.

[16]  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.

[17]  G. Stormo,et al.  CUUCGG hairpins: extraordinarily stable RNA secondary structures associated with various biochemical processes. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

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

[19]  S Thirup,et al.  Crystal Structure of the Ternary Complex of Phe-tRNAPhe, EF-Tu, and a GTP Analog , 1995, Science.

[20]  R. Gourse,et al.  Sequence analysis of 28S ribosomal DNA from the amphibian Xenopus laevis. , 1983, Nucleic acids research.

[21]  J. Zou,et al.  Improved methods for building protein models in electron density maps and the location of errors in these models. , 1991, Acta crystallographica. Section A, Foundations of crystallography.

[22]  J. McCutcheon,et al.  A Detailed View of a Ribosomal Active Site The Structure of the L11–RNA Complex , 1999, Cell.

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

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

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

[26]  I. Wool,et al.  The conformation of the sarcin/ricin loop from 28S ribosomal RNA. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

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

[28]  Murray N. Schnare,et al.  A compilation of large subunit (23S and 23S-like) ribosomal RNA structures: 1993 , 1993, Nucleic Acids Res..