Home LiteratureArticle Details
PMID: 16249344 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Simulating movement of tRNA into the ribosome during decoding.

Sanbonmatsu KY, Joseph S, Tung CS

Abstract

Decoding is the key step during protein synthesis that enables information transfer from RNA to protein, a process critical for the survival of all organisms. We have used large-scale (2.64 x 10(6) atoms) all-atom simulations of the entire ribosome to understand a critical step of decoding. Although the decoding problem has been studied for more than four decades, the rate-limiting step of cognate tRNA selection has only recently been identified. This step, known as accommodation, involves the movement inside the ribosome of the aminoacyl-tRNA from the partially bound "A/T" state to the fully bound "A/A" state. Here, we show that a corridor of 20 universally conserved ribosomal RNA bases interacts with the tRNA during the accommodation movement. Surprisingly, the tRNA is impeded by the A-loop (23S helix 92), instead of enjoying a smooth transition to the A/A state. In particular, universally conserved 23S ribosomal RNA bases U2492, C2556, and C2573 act as a 3D gate, causing the acceptor stem to pause before allowing entrance into the peptidyl transferase center. Our simulations demonstrate that the flexibility of the acceptor stem of the tRNA, in addition to flexibility of the anticodon arm, is essential for tRNA selection. This study serves as a template for simulating conformational changes in large (>10(6) atoms) biological and artificial molecular machines.

MeSH Terms
Biological Transport Computer Simulation Conserved Sequence Kinetics Models, Molecular Nucleic Acid Conformation Protein Biosynthesis RNA, Transfer/metabolism RNA, Transfer, Amino Acyl/metabolism Ribosomes/metabolism
Chemicals
RNA, Transfer, Amino Acyl RNA, Transfer
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sanbonmatsu Kevin Y
Department of Theoretical Biology and Biophysics, Theoretical Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USA. kys@lanl.gov
Joseph Simpson
Tung Chang-Shung
References (52)
52 references, click to expand
  1. Animation of the dynamical events of the elongation cycle based on cryoelectron microscopy of functional complexes of the ribosome.
    J Struct Biol. 1999 Dec 1;128(1):15-8 PMID: 10600553
  2. Recognition of cognate transfer RNA by the 30S ribosomal subunit.
    Science. 2001 May 4;292(5518):897-902 PMID: 11340196
  3. A dynamic model for the allosteric mechanism of GroEL.
    J Mol Biol. 2000 Sep 15;302(2):303-13 PMID: 10970735
  4. Movement of the decoding region of the 16 S ribosomal RNA accompanies tRNA translocation.
    J Mol Biol. 2000 Dec 8;304(4):507-15 PMID: 11099376
  5. Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation.
    Cell. 2001 Apr 6;105(1):115-26 PMID: 11301007
  6. Crystal structure of the ribosome at 5.5 A resolution.
    Science. 2001 May 4;292(5518):883-96 PMID: 11283358
  7. Analysis of codon:anticodon interactions within the ribosome provides new insights into codon reading and the genetic code structure.
    RNA. 2001 Jul;7(7):942-57 PMID: 11453067
  8. Energetics of ion conduction through the K+ channel.
    Nature. 2001 Nov 1;414(6859):73-7 PMID: 11689945
  9. Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms.
    Annu Rev Biochem. 2001;70:415-35 PMID: 11395413
  10. A pre-translocational intermediate in protein synthesis observed in crystals of enzymatically active 50S subunits.
    Nat Struct Biol. 2002 Mar;9(3):225-30 PMID: 11828326
  11. Nanoseconds molecular dynamics simulation of primary mechanical energy transfer steps in F1-ATP synthase.
    Nat Struct Biol. 2002 Mar;9(3):198-202 PMID: 11836535
  12. Control of the selectivity of the aquaporin water channel family by global orientational tuning.
    Science. 2002 Apr 19;296(5567):525-30 PMID: 11964478
  13. Ultrafast spectroscopy reveals subnanosecond peptide conformational dynamics and validates molecular dynamics simulation.
    Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):7998-8002 PMID: 12060746
  14. Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process.
    EMBO J. 2002 Jul 1;21(13):3557-67 PMID: 12093756
  15. Modeling a minimal ribosome based on comparative sequence analysis.
    J Mol Biol. 2002 Aug 9;321(2):215-34 PMID: 12144780
  16. Molecular dynamics simulations of biomolecules.
    Nat Struct Biol. 2002 Sep;9(9):646-52 PMID: 12198485
  17. Structural insights into peptide bond formation.
    Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11670-5 PMID: 12185246
  18. Selection of tRNA by the ribosome requires a transition from an open to a closed form.
    Cell. 2002 Nov 27;111(5):721-32 PMID: 12464183
  19. Binding interactions between the core central domain of 16S rRNA and the ribosomal protein S15 determined by molecular dynamics simulations.
    Nucleic Acids Res. 2003 Jan 15;31(2):629-38 PMID: 12527771
  20. Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression.
    Mol Cell. 2003 Jan;11(1):91-102 PMID: 12535524
  21. Mega-Dalton biomolecular motion captured from electron microscopy reconstructions.
    J Mol Biol. 2003 Feb 14;326(2):485-92 PMID: 12559916
  22. A twisted tRNA intermediate sets the threshold for decoding.
    RNA. 2003 Apr;9(4):384-5 PMID: 12649490
  23. Understanding discrimination by the ribosome: stability testing and groove measurement of codon-anticodon pairs.
    J Mol Biol. 2003 Apr 18;328(1):33-47 PMID: 12683995
  24. Study of the structural dynamics of the E coli 70S ribosome using real-space refinement.
    Cell. 2003 Jun 13;113(6):789-801 PMID: 12809609
  25. X-ray crystal structures of the WT and a hyper-accurate ribosome from Escherichia coli.
    Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):8682-7 PMID: 12853578
  26. Dynamic reorganization of the functionally active ribosome explored by normal mode analysis and cryo-electron microscopy.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9319-23 PMID: 12878726
  27. The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs.
    BMC Bioinformatics. 2002;3:2 PMID: 11869452
  28. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy.
    Nat Struct Biol. 2003 Nov;10(11):899-906 PMID: 14566331
  29. Simulation of the folding equilibrium of alpha-helical peptides: a comparison of the generalized Born approximation with explicit solvent.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):13934-9 PMID: 14617775
  30. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome.
    Mol Cell. 2004 Jan 30;13(2):191-200 PMID: 14759365
  31. The molecular basis of electroporation.
    BMC Biochem. 2004 Jul 19;5:10 PMID: 15260890
  32. Ribosome motions modulate electrostatic properties.
    Biopolymers. 2004 Aug 15;74(6):423-31 PMID: 15274086
  33. tRNA selection and kinetic proofreading in translation.
    Nat Struct Mol Biol. 2004 Oct;11(10):1008-14 PMID: 15448679
  34. Atomic model of the Thermus thermophilus 70S ribosome developed in silico.
    Biophys J. 2004 Oct;87(4):2714-22 PMID: 15454463
  35. A semi-quantitative treatment of missense and nonsense suppression in the strA and ram ribosomal mutants of Escherichia coli. Evaluation of some molecular parameters of translation in vivo.
    J Mol Biol. 1974 Apr 5;84(2):297-313 PMID: 4598370
  36. Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity.
    Proc Natl Acad Sci U S A. 1974 Oct;71(10):4135-9 PMID: 4530290
  37. Proofreading of the codon-anticodon interaction on ribosomes.
    Proc Natl Acad Sci U S A. 1977 Jan;74(1):198-202 PMID: 319457
  38. Dynamics of folded proteins.
    Nature. 1977 Jun 16;267(5612):585-90 PMID: 301613
  39. Intermediate states in the movement of transfer RNA in the ribosome.
    Nature. 1989 Nov 9;342(6246):142-8 PMID: 2682263
  40. The allosteric three-site model for the ribosomal elongation cycle: features and future.
    Biochemistry. 1990 May 29;29(21):4997-5008 PMID: 2198935
  41. Novel mutants of 23S RNA: characterization of functional properties.
    Nucleic Acids Res. 1992 Jun 25;20(12):3147-52 PMID: 1377819
  42. Mutations at U2555, a tRNA-protected base in 23S rRNA, affect translational fidelity.
    Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9214-8 PMID: 8415679
  43. Targeted molecular dynamics: a new approach for searching pathways of conformational transitions.
    J Mol Graph. 1994 Jun;12(2):84-9 PMID: 7918256
  44. The involvement of two distinct regions of 23 S ribosomal RNA in tRNA selection.
    J Mol Biol. 1995 Dec 15;254(5):838-47 PMID: 7500354
  45. VMD: visual molecular dynamics.
    J Mol Graph. 1996 Feb;14(1):33-8, 27-8 PMID: 8744570
  46. Visualization of elongation factor Tu on the Escherichia coli ribosome.
    Nature. 1997 Sep 25;389(6649):403-6 PMID: 9311785
  47. Molecular dynamics simulations of solvated yeast tRNA(Asp).
    Biophys J. 1999 Jan;76(1 Pt 1):50-64 PMID: 9876122
  48. Major groove binding of the tRNA/mRNA complex to the 16 S ribosomal RNA decoding site.
    J Mol Biol. 1999 Feb 5;285(5):2069-78 PMID: 9925785
  49. The role of tRNA as a molecular spring in decoding, accommodation, and peptidyl transfer.
    FEBS Lett. 2005 Feb 7;579(4):959-62 PMID: 15680982
  50. In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats.
    Structure. 2005 Apr;13(4):669-82 PMID: 15837205
  51. Exploring global motions and correlations in the ribosome.
    Biophys J. 2005 Sep;89(3):1455-63 PMID: 15951386
  52. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution.
    Science. 2000 Aug 11;289(5481):905-20 PMID: 10937989
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-11-01
Epub
2005-00-25
Pages
15854-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1266076
Subset
IM
Grants
NIGMS NIH HHS · R01 GM072686 · United States
NIGMS NIH HHS · R01-GM072686 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com