Abstract
Transfer RNAs from all organisms contain many modified nucleosides. Their vastly different chemical structures, their presence in different tRNAs, their occurrence in different locations in tRNA and their influence on different reactions in which tRNA participates suggest that each modified nucleoside may have its own specific function. However, since the frequency of frameshifting in several different mutants [mnmA, mnmE, tgt, truA (hisT), trmD, miaA, miaB and miaE] defective in tRNA modification was higher compared with the corresponding wild-type controls, these modifications have a common function: they all improve reading frame maintenance. Frameshifting occurs by peptidyl-tRNA slippage, which is influenced by the hypomodified tRNA in two ways: (i) a hypomodified tRNA in the ternary complex may decrease the rate by which the complex is recruited to the A-site and thereby increasing peptidyl-tRNA slippage; or (ii) a hypomodified peptidyl-tRNA may be more prone to slip than its fully modified counterpart. We propose that the improvement of reading frame maintenance has been and is the major selective factor for the emergence of new modified nucleosides.
MeSH Terms
Base Sequence
Codon/genetics
Escherichia coli/genetics
Frameshift Mutation
Genotype
Models, Genetic
Oligodeoxyribonucleotides/chemistry
Phenotype
RNA, Bacterial/genetics
RNA, Transfer/chemistry,genetics
RNA, Transfer, Amino Acid-Specific/genetics
RNA, Transfer, Amino Acyl/chemistry,genetics
RNA, Transfer, Leu/genetics
RNA, Transfer, Phe/genetics
RNA, Transfer, Pro/genetics
RNA, Transfer, Val/genetics
Reading Frames
Reference Values
Salmonella typhimurium/genetics
beta-Galactosidase/genetics
beta-Lactamases/genetics
Chemicals
Codon
Oligodeoxyribonucleotides
RNA, Bacterial
RNA, Transfer, Amino Acid-Specific
RNA, Transfer, Amino Acyl
RNA, Transfer, Leu
RNA, Transfer, Phe
RNA, Transfer, Pro
RNA, Transfer, Val
tRNA, peptidyl-
RNA, Transfer
beta-Galactosidase
beta-Lactamases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Urbonavicius J
Department of Microbiology, Umeå University, S-90 187 Umeå, Sweden.
Qian Q
Durand J M
Hagervall T G
Björk G R
References (32)
32 references, click to expand
-
Identification of the miaB gene, involved in methylthiolation of isopentenylated A37 derivatives in the tRNA of Salmonella typhimurium and Escherichia coli.
J Bacteriol. 1999 Dec;181(23):7256-65
PMID: 10572129
-
The RNA Modification Database: 1999 update.
Nucleic Acids Res. 1999 Jan 1;27(1):196-7
PMID: 9847178
-
A primordial tRNA modification required for the evolution of life?
EMBO J. 2001 Jan 15;20(1-2):231-9
PMID: 11226173
-
A novel link between the biosynthesis of aromatic amino acids and transfer RNA modification in Escherichia coli.
J Mol Biol. 1980 Jul 5;140(3):391-410
PMID: 6160251
-
The site of interaction of aminoacyl-tRNA with elongation factor Tu.
EMBO J. 1982;1(9):1095-100
PMID: 6765239
-
Molecular mechanism of codon recognition by tRNA species with modified uridine in the first position of the anticodon.
Proc Natl Acad Sci U S A. 1985 Aug;82(15):4905-9
PMID: 3860833
-
Nucleotide sequences of two serine tRNAs with a GGA anticodon: the structure-function relationships in the serine family of E. coli tRNAs.
Nucleic Acids Res. 1985 Aug 12;13(15):5697-706
PMID: 3898020
-
Pleiotropic effects induced by modification deficiency next to the anticodon of tRNA from Salmonella typhimurium LT2.
J Bacteriol. 1986 Jun;166(3):1013-21
PMID: 2423501
-
Base substitutions in the tRNA anticodon arm do not degrade the accuracy of reading frame maintenance.
Proc Natl Acad Sci U S A. 1986 Sep;83(17):6538-42
PMID: 2428035
-
Slippery runs, shifty stops, backward steps, and forward hops: -2, -1, +1, +2, +5, and +6 ribosomal frameshifting.
Cold Spring Harb Symp Quant Biol. 1987;52:687-93
PMID: 3135981
-
Use of tRNA suppressors to probe regulation of Escherichia coli release factor 2.
J Mol Biol. 1988 Sep 5;203(1):75-83
PMID: 3054124
-
Prevention of translational frameshifting by the modified nucleoside 1-methylguanosine.
Science. 1989 May 26;244(4907):986-9
PMID: 2471265
-
Rates of aminoacyl-tRNA selection at 29 sense codons in vivo.
J Mol Biol. 1989 Sep 5;209(1):65-77
PMID: 2478714
-
Temperature jump relaxation studies on the interactions between transfer RNAs with complementary anticodons. The effect of modified bases adjacent to the anticodon triplet.
J Biomol Struct Dyn. 1985 Oct;3(2):387-408
PMID: 3917029
-
ms2i6A deficiency enhances proofreading in translation.
J Mol Biol. 1991 Dec 20;222(4):1161-71
PMID: 1762149
-
Analysis of effects of tRNA:message stability on frameshift frequency at the Escherichia coli RF2 programmed frameshift site.
Nucleic Acids Res. 1993 Apr 25;21(8):1837-43
PMID: 8493101
-
How translational accuracy influences reading frame maintenance.
EMBO J. 1999 Mar 15;18(6):1427-34
PMID: 10075915
-
Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli.
J Bacteriol. 1951 Sep;62(3):293-300
PMID: 14888646
-
Deficiency of 1-methylguanosine in tRNA from Salmonella typhimurium induces frameshifting by quadruplet translocation.
J Mol Biol. 1993 Aug 5;232(3):756-65
PMID: 7689113
-
Isolation of the gene (miaE) encoding the hydroxylase involved in the synthesis of 2-methylthio-cis-ribozeatin in tRNA of Salmonella typhimurium and characterization of mutants.
J Bacteriol. 1993 Dec;175(24):7776-85
PMID: 8253666
-
A ribosomal frameshifting error during translation of the argI mRNA of Escherichia coli.
Mol Gen Genet. 1994 May 25;243(4):434-41
PMID: 7515462
-
Prokaryotic ribosomes recode the HIV-1 gag-pol-1 frameshift sequence by an E/P site post-translocation simultaneous slippage mechanism.
Nucleic Acids Res. 1995 May 11;23(9):1487-94
PMID: 7784201
-
Evidence that uncharged tRNA can inhibit a programmed translational frameshift in Escherichia coli.
J Mol Biol. 1995 Aug 11;251(2):210-6
PMID: 7643397
-
On the mechanism of leftward frameshifting at several hungry codons.
J Mol Biol. 1996 Mar 8;256(4):676-84
PMID: 8642590
-
Hidden infidelities of the translational stop signal.
Prog Nucleic Acid Res Mol Biol. 1996;52:293-335
PMID: 8821264
-
Analysis of interactions between the codon-anticodon duplexes within the ribosome: their role in translation.
J Mol Biol. 1997 Mar 14;266(5):877-90
PMID: 9086267
-
Analyses of frameshifting at UUU-pyrimidine sites.
Nucleic Acids Res. 1997 May 15;25(10):2005-11
PMID: 9115369
-
Expression of a coronavirus ribosomal frameshift signal in Escherichia coli: influence of tRNA anticodon modification on frameshifting.
J Mol Biol. 1997 Jul 18;270(3):360-73
PMID: 9237903
-
Three modified nucleosides present in the anticodon stem and loop influence the in vivo aa-tRNA selection in a tRNA-dependent manner.
J Mol Biol. 1997 Aug 15;271(2):209-21
PMID: 9268653
-
Structural alterations far from the anticodon of the tRNAProGGG of Salmonella typhimurium induce +1 frameshifting at the peptidyl-site.
J Mol Biol. 1997 Nov 14;273(5):978-92
PMID: 9367785
-
A new model for phenotypic suppression of frameshift mutations by mutant tRNAs.
Mol Cell. 1998 Mar;1(4):471-82
PMID: 9660932
-
Near-cognate peptidyl-tRNAs promote +1 programmed translational frameshifting in yeast.
Mol Cell. 1999 Dec;4(6):1005-15
PMID: 10635325