Abstract
During protein synthesis, the ribosome accurately selects transfer RNAs (tRNAs) in accordance with the messenger RNA (mRNA) triplet in the decoding centre. tRNA selection is initiated by elongation factor Tu, which delivers tRNA to the aminoacyl tRNA-binding site (A site) and hydrolyses GTP upon establishing codon-anticodon interactions in the decoding centre. At the following proofreading step the ribosome re-examines the tRNA and rejects it if it does not match the A codon. It was suggested that universally conserved G530, A1492 and A1493 of 16S ribosomal RNA, critical for tRNA binding in the A site, actively monitor cognate tRNA, and that recognition of the correct codon-anticodon duplex induces an overall ribosome conformational change (domain closure). Here we propose an integrated mechanism for decoding based on six X-ray structures of the 70S ribosome determined at 3.1-3.4 Å resolution, modelling cognate or near-cognate states of the decoding centre at the proofreading step. We show that the 30S subunit undergoes an identical domain closure upon binding of either cognate or near-cognate tRNA. This conformational change of the 30S subunit forms a decoding centre that constrains the mRNA in such a way that the first two nucleotides of the A codon are limited to form Watson-Crick base pairs. When U·G and G·U mismatches, generally considered to form wobble base pairs, are at the first or second codon-anticodon position, the decoding centre forces this pair to adopt the geometry close to that of a canonical C·G pair. This by itself, or with distortions in the codon-anticodon mini-helix and the anticodon loop, causes the near-cognate tRNA to dissociate from the ribosome.
MeSH Terms
Anticodon/genetics,metabolism
Base Pairing
Base Sequence
Codon/genetics,metabolism
Crystallography, X-Ray
Models, Biological
Models, Genetic
Models, Molecular
Nucleic Acid Conformation
Protein Biosynthesis
Protein Conformation
RNA, Messenger/genetics,metabolism
RNA, Ribosomal, 23S/genetics,metabolism
RNA, Transfer, Amino Acid-Specific/chemistry,genetics,metabolism
Ribosomes/chemistry,genetics,metabolism
Thermus thermophilus
Chemicals
Anticodon
Codon
RNA, Messenger
RNA, Ribosomal, 23S
RNA, Transfer, Amino Acid-Specific
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Demeshkina Natalia
Département de Biologie et de Génomique Structurales, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch 67400, France.
Jenner Lasse
Westhof Eric
Yusupov Marat
Yusupova Gulnara
References (30)
30 references, click to expand
-
Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms.
Annu Rev Biochem. 2001;70:415-35
PMID: 11395413
-
How mutations in tRNA distant from the anticodon affect the fidelity of decoding.
Nat Struct Mol Biol. 2011 Apr;18(4):432-6
PMID: 21378964
-
Recognition of aminoacyl-tRNA: a common molecular mechanism revealed by cryo-EM.
EMBO J. 2008 Dec 17;27(24):3322-31
PMID: 19020518
-
Replication infidelity via a mismatch with Watson-Crick geometry.
Proc Natl Acad Sci U S A. 2011 Feb 1;108(5):1862-7
PMID: 21233421
-
GTPase activation of elongation factor EF-Tu by the ribosome during decoding.
EMBO J. 2009 Mar 18;28(6):755-65
PMID: 19229291
-
Conformational switch in the decoding region of 16S rRNA during aminoacyl-tRNA selection on the ribosome.
Nat Struct Biol. 2000 Feb;7(2):104-7
PMID: 10655610
-
Structural rearrangements of the ribosome at the tRNA proofreading step.
Nat Struct Mol Biol. 2010 Sep;17(9):1072-8
PMID: 20694005
-
An extended structural signature for the tRNA anticodon loop.
RNA. 2001 Mar;7(3):334-41
PMID: 11333014
-
Structural aspects of messenger RNA reading frame maintenance by the ribosome.
Nat Struct Mol Biol. 2010 May;17(5):555-60
PMID: 20400952
-
An active role for tRNA in decoding beyond codon:anticodon pairing.
Science. 2005 May 20;308(5725):1178-80
PMID: 15905403
-
Conformational sampling of aminoacyl-tRNA during selection on the bacterial ribosome.
J Mol Biol. 2010 Jun 18;399(4):576-95
PMID: 20434456
-
Amino acid specificity in translation.
Trends Biochem Sci. 2005 Dec;30(12):659-65
PMID: 16260144
-
Binding of tRNA to the ribosomal A and P sites protects two distinct sets of nucleotides in 16 S rRNA.
J Mol Biol. 1990 Jan 5;211(1):135-45
PMID: 2405162
-
Accommodation of aminoacyl-tRNA into the ribosome involves reversible excursions along multiple pathways.
RNA. 2010 Jun;16(6):1196-204
PMID: 20427512
-
Structure of the 70S ribosome complexed with mRNA and tRNA.
Science. 2006 Sep 29;313(5795):1935-42
PMID: 16959973
-
Optimal fine φ-slicing for single-photon-counting pixel detectors.
Acta Crystallogr D Biol Crystallogr. 2012 Jan;68(Pt 1):42-56
PMID: 22194332
-
Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome.
Nat Struct Mol Biol. 2009 May;16(5):528-33
PMID: 19363482
-
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
-
Selective perturbation of G530 of 16 S rRNA by translational miscoding agents and a streptomycin-dependence mutation in protein S12.
J Mol Biol. 1994 Jan 7;235(1):156-72
PMID: 8289238
-
Averaged kick maps: less noise, more signal... and probably less bias.
Acta Crystallogr D Biol Crystallogr. 2009 Sep;65(Pt 9):921-31
PMID: 19690370
-
The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA.
Science. 2009 Oct 30;326(5953):688-694
PMID: 19833920
-
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
PMID: 20124702
-
The role of fluctuations in tRNA selection by the ribosome.
Proc Natl Acad Sci U S A. 2007 Aug 21;104(34):13661-5
PMID: 17699629
-
A uniform response to mismatches in codon-anticodon complexes ensures ribosomal fidelity.
Mol Cell. 2006 Feb 3;21(3):369-77
PMID: 16455492
-
Fidelity at the molecular level: lessons from protein synthesis.
Cell. 2009 Feb 20;136(4):746-62
PMID: 19239893
-
Recognition of the codon-anticodon helix by ribosomal RNA.
Science. 1999 Sep 10;285(5434):1722-5
PMID: 10481006
-
Recognition of cognate transfer RNA by the 30S ribosomal subunit.
Science. 2001 May 4;292(5518):897-902
PMID: 11340196
-
Recognition and selection of tRNA in translation.
FEBS Lett. 2005 Feb 7;579(4):938-42
PMID: 15680978
-
The mechanism for activation of GTP hydrolysis on the ribosome.
Science. 2010 Nov 5;330(6005):835-838
PMID: 21051640
-
Counting cycles of EF-Tu to measure proofreading in translation.
Biochimie. 1986 Mar;68(2):261-73
PMID: 3089318