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PMID: 11726686 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Misreading of termination codons in eukaryotes by natural nonsense suppressor tRNAs.

Nucleic acids research ·Vol. 29 ·No. 23 ·2001-12-01 ·Pages 4767-82

Beier H, Grimm M

Abstract

Translational stop codon readthrough provides a regulatory mechanism of gene expression that is extensively utilised by positive-sense ssRNA viruses. The misreading of termination codons is achieved by a variety of naturally occurring suppressor tRNAs whose structure and function is the subject of this survey. All of the nonsense suppressors characterised to date (with the exception of selenocysteine tRNA) are normal cellular tRNAs that are primarily needed for reading their cognate sense codons. As a consequence, recognition of stop codons by natural suppressor tRNAs necessitates unconventional base pairings in anticodon-codon interactions. A number of intrinsic features of the suppressor tRNA contributes to the ability to read non-cognate codons. Apart from anticodon-codon affinity, the extent of base modifications within or 3' of the anticodon may up- or down-regulate the efficiency of suppression. In order to out-compete the polypeptide chain release factor an absolute prerequisite for the action of natural suppressor tRNAs is a suitable nucleotide context, preferentially at the 3' side of the suppressed stop codon. Three major types of viral readthrough sites, based on similar sequences neighbouring the leaky stop codon, can be defined. It is discussed that not only RNA viruses, but also the eukaryotic host organism might gain some profit from cellular suppressor tRNAs.

MeSH Terms
Animals Base Pairing Base Sequence Codon, Terminator/genetics Gene Expression Regulation, Viral Molecular Sequence Data Peptide Chain Termination, Translational RNA Viruses/genetics RNA, Chloroplast/genetics RNA, Transfer/chemistry,physiology RNA, Viral/chemistry,physiology
Chemicals
Codon, Terminator RNA, Chloroplast RNA, Viral RNA, Transfer
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Beier H
Institut für Biochemie, Bayerische Julius-Maximilians-Universität, Biozentrum, Am Hubland, D-97074 Würzburg, Germany. [email protected]
Grimm M
References (110)
110 references, click to expand
  1. How translational accuracy influences reading frame maintenance.
    EMBO J. 1999 Mar 15;18(6):1427-34 PMID: 10075915
  2. Virus taxonomy--1999. The universal system of virus taxonomy, updated to include the new proposals ratified by the International Committee on Taxonomy of Viruses during 1998.
    Arch Virol. 1999;144(2):421-9 PMID: 10470265
  3. RECODE: a database of frameshifting, bypassing and codon redefinition utilized for gene expression.
    Nucleic Acids Res. 2001 Jan 1;29(1):264-7 PMID: 11125107
  4. Endless possibilities: translation termination and stop codon recognition.
    Microbiology. 2001 Feb;147(Pt 2):255-69 PMID: 11158343
  5. Molecular mechanism of stop codon recognition by eRF1: a wobble hypothesis for peptide anticodons.
    FEBS Lett. 2001 Jan 19;488(3):105-9 PMID: 11163755
  6. The ciliate Euplotes octocarinatus expresses two polypeptide release factors of the type eRF1.
    Gene. 2001 Jan 10;262(1-2):161-8 PMID: 11179680
  7. A possible role for nonsense suppression in the synthesis of a human cytomegalovirus 58-kDa virion protein.
    Virology. 1992 Jan;186(1):309-12 PMID: 1309277
  8. Codon context effect in virus translational readthrough. A study in vitro of the determinants of TMV and Mo-MuLV amber suppression.
    FEBS Lett. 1992 Jul 20;306(2-3):133-9 PMID: 1321731
  9. Influence of codon context on UGA suppression and readthrough.
    J Mol Biol. 1992 May 20;225(2):261-9 PMID: 1375653
  10. The leaky UGA termination codon of tobacco rattle virus RNA is suppressed by tobacco chloroplast and cytoplasmic tRNAs(Trp) with CmCA anticodon.
    EMBO J. 1992 Nov;11(11):4167-73 PMID: 1396598
  11. Mutational analysis of the gag-pol junction of Moloney murine leukemia virus: requirements for expression of the gag-pol fusion protein.
    J Virol. 1992 Nov;66(11):6601-8 PMID: 1404606
  12. Translational readthrough at nonsense mutations in the HSF1 gene of Saccharomyces cerevisiae.
    Mol Gen Genet. 1992 Sep;234(3):369-78 PMID: 1406583
  13. Pseudouridine in the anticodon G psi A of plant cytoplasmic tRNA(Tyr) is required for UAG and UAA suppression in the TMV-specific context.
    Nucleic Acids Res. 1992 Nov 25;20(22):5911-8 PMID: 1461724
  14. Translational suppression in retroviral gene expression.
    Adv Virus Res. 1992;41:193-239 PMID: 1575083
  15. The chloroplast genome.
    Plant Mol Biol. 1992 May;19(1):149-68 PMID: 1600166
  16. Bipartite signal for read-through suppression in murine leukemia virus mRNA: an eight-nucleotide purine-rich sequence immediately downstream of the gag termination codon followed by an RNA pseudoknot.
    J Virol. 1992 Aug;66(8):5127-32 PMID: 1629968
  17. UAG readthrough during TMV RNA translation: isolation and sequence of two tRNAs with suppressor activity from tobacco plants.
    EMBO J. 1984 Feb;3(2):351-6 PMID: 16453503
  18. The molecular basis for the differential translation of TMV RNA in tobacco protoplasts and wheat germ extracts.
    EMBO J. 1984 May;3(5):1091-6 PMID: 16453524
  19. Dramatic events in ciliate evolution: alteration of UAA and UAG termination codons to glutamine codons due to anticodon mutations in two Tetrahymena tRNAs.
    EMBO J. 1986 Jun;5(6):1307-11 PMID: 16453685
  20. Synthesis of TMV-specific RNAs and proteins at the early stage of infection in tobacco protoplasts: transient expression of the 30K protein and its mRNA.
    Virology. 1984 Feb;133(1):18-24 PMID: 18639805
  21. The nucleotide sequence and luteovirus-like nature of RNA 1 of an aphid non-transmissible strain of pea enation mosaic virus.
    J Gen Virol. 1991 Aug;72 ( Pt 8):1819-34 PMID: 1875194
  22. UGA is translated as cysteine in pheromone 3 of Euplotes octocarinatus.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3758-61 PMID: 1902568
  23. Crystal structure of an RNA double helix incorporating a track of non-Watson-Crick base pairs.
    Nature. 1991 Oct 10;353(6344):579-81 PMID: 1922368
  24. The signal for a leaky UAG stop codon in several plant viruses includes the two downstream codons.
    J Mol Biol. 1991 Mar 20;218(2):365-73 PMID: 2010914
  25. tRNA anticodons with the modified nucleoside 2-methylthio-N6-(4-hydroxyisopentenyl)adenosine distinguish between bases 3' of the codon.
    J Mol Biol. 1991 Apr 5;218(3):509-16 PMID: 2016742
  26. cis Acting RNA sequences control the gag-pol translation readthrough in murine leukemia virus.
    Virology. 1991 Jul;183(1):313-9 PMID: 2053284
  27. Sequence analysis suggests that tetra-nucleotides signal the termination of protein synthesis in eukaryotes.
    Nucleic Acids Res. 1990 Nov 11;18(21):6339-45 PMID: 2123028
  28. Structure and function of suppressor tRNAs in higher eukaryotes.
    Crit Rev Biochem Mol Biol. 1990;25(2):71-96 PMID: 2183969
  29. Genomic organization and physical mapping of the transfer RNA genes in Escherichia coli K12.
    J Mol Biol. 1990 Apr 20;212(4):579-98 PMID: 2184240
  30. Spleen necrosis virus gag polyprotein is necessary for particle assembly and release but not for proteolytic processing.
    J Virol. 1990 Jun;64(6):2642-52 PMID: 2186174
  31. The signal for the termination of protein synthesis in procaryotes.
    Nucleic Acids Res. 1990 Apr 25;18(8):2079-86 PMID: 2186375
  32. Identification of amino acids inserted during suppression of UAA and UGA termination codons at the gag-pol junction of Moloney murine leukemia virus.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):8860-3 PMID: 2247457
  33. tRNA, suppression, and the code.
    Annu Rev Genet. 1985;19:57-80 PMID: 2417544
  34. Queuine in plants and plant tRNAs: Differences between embryonic tissue and mature leaves.
    Plant Mol Biol. 1987 Jul;8(4):345-53 PMID: 24301197
  35. Mutation in the D arm enables a suppressor with a CUA anticodon to read both amber and ochre codons in Escherichia coli.
    J Mol Biol. 1986 Aug 5;190(3):513-7 PMID: 2431155
  36. Transfer RNA structure and coding specificity. I. Evidence that a D-arm mutation reduces tRNA dissociation from the ribosome.
    J Mol Biol. 1989 Apr 5;206(3):489-501 PMID: 2469803
  37. Mutagenesis of the in-frame opal termination codon preceding nsP4 of Sindbis virus: studies of translational readthrough and its effect on virus replication.
    J Virol. 1989 Mar;63(3):1326-37 PMID: 2521676
  38. Suppression of UAA and UGA termination codons in mutant murine leukemia viruses.
    J Virol. 1989 Jun;63(6):2870-3 PMID: 2542597
  39. The effect of specific mutations at and around the gag-pol gene junction of Moloney murine leukaemia virus.
    Nucleic Acids Res. 1989 Aug 11;17(15):5933-45 PMID: 2549503
  40. Presence of the hypermodified nucleotide N6-(delta 2-isopentenyl)-2-methylthioadenosine prevents codon misreading by Escherichia coli phenylalanyl-transfer RNA.
    Proc Natl Acad Sci U S A. 1989 Jan;86(2):409-13 PMID: 2643111
  41. Translational readthrough of the murine leukemia virus gag gene amber codon does not require virus-induced alteration of tRNA.
    J Virol. 1989 May;63(5):2405-10 PMID: 2784837
  42. Wild-type tRNATyrG reads the TMV RNA stop codon, but Q base-modified tRNATyrQ does not.
    Nature. 1981 Nov 12;294(5837):188-190 PMID: 29451243
  43. The nucleotide sequence of tyrosine tRNAQ* psi A from bovine liver.
    Arch Biochem Biophys. 1985 Jan;236(1):448-53 PMID: 2981510
  44. Partial suppression of an ochre mutation in Saccharomyces cerevisiae by multicopy plasmids containing a normal yeast tRNAGln gene.
    J Mol Biol. 1985 May 5;183(1):31-42 PMID: 2989539
  45. The nucleotide sequence of two homogeneic Drosophila melanogaster tRNATyr isoacceptors: application of a rapid tRNA anticodon sequencing method using S-1 nuclease.
    Arch Biochem Biophys. 1986 May 15;247(1):233-7 PMID: 3010877
  46. Stop making sense: or Regulation at the level of termination in eukaryotic protein synthesis.
    FEBS Lett. 1988 Aug 1;235(1-2):1-15 PMID: 3042454
  47. Transfer ribonucleic acid-mediated suppression of termination codons in Escherichia coli.
    Microbiol Rev. 1988 Sep;52(3):354-74 PMID: 3054467
  48. Influence of modification next to the anticodon in tRNA on codon context sensitivity of translational suppression and accuracy.
    J Bacteriol. 1986 Jun;166(3):1022-7 PMID: 3086285
  49. Stop is not the end: physiological implications of translational readthrough.
    J Theor Biol. 1988 Apr 21;131(4):477-85 PMID: 3193779
  50. Normal yeast tRNA(CAGGln) can suppress amber codons and is encoded by an essential gene.
    J Mol Biol. 1986 Dec 20;192(4):725-35 PMID: 3295253
  51. Immunopurification of the suppressor tRNA dependent rabbit beta-globin readthrough protein.
    Biochemistry. 1988 Feb 23;27(4):1179-83 PMID: 3365379
  52. Molecular structure of the G.A base pair in DNA and its implications for the mechanism of transversion mutations.
    Proc Natl Acad Sci U S A. 1986 Apr;83(8):2402-6 PMID: 3458205
  53. Natural UAG suppressor glutamine tRNA is elevated in mouse cells infected with Moloney murine leukemia virus.
    Proc Natl Acad Sci U S A. 1987 May;84(9):2668-72 PMID: 3472229
  54. Complete nucleotide sequence of the nonstructural protein genes of Semliki Forest virus.
    Nucleic Acids Res. 1986 Jul 25;14(14):5667-82 PMID: 3488539
  55. First position wobble in codon-anticodon pairing: amber suppression by a yeast glutamine tRNA.
    Gene. 1986;49(3):383-8 PMID: 3552889
  56. Detection of unique tRNA species in tumor tissues by Escherichia coli guanine insertion enzyme.
    Proc Natl Acad Sci U S A. 1978 Sep;75(9):4247-51 PMID: 360213
  57. The complete nucleotide sequence of tobacco rattle virus RNA-1.
    J Gen Virol. 1987 Oct;68 ( Pt 10):2563-75 PMID: 3668507
  58. Novel amber suppressor tRNAs of mammalian origin.
    EMBO J. 1987 Oct;6(10):3049-55 PMID: 3691479
  59. Novel mechanism of post-transcriptional modification of tRNA. Insertion of bases of Q precursors into tRNA by a specific tRNA transglycosylase reaction.
    J Biol Chem. 1979 Apr 25;254(8):3067-73 PMID: 372186
  60. In vitro mutagenesis of the putative replicase genes of tobacco mosaic virus.
    Nucleic Acids Res. 1986 Nov 11;14(21):8291-305 PMID: 3786131
  61. Murine leukemia virus protease is encoded by the gag-pol gene and is synthesized through suppression of an amber termination codon.
    Proc Natl Acad Sci U S A. 1985 Mar;82(6):1618-22 PMID: 3885215
  62. 15N-labeled Escherichia coli tRNAfMet, tRNAGlu, tRNATyr, and tRNAPhe. Double resonance and two-dimensional NMR of N1-labeled pseudouridine.
    J Biol Chem. 1985 Aug 15;260(17):9734-41 PMID: 3894360
  63. Structure of an adenine-cytosine base pair in DNA and its implications for mismatch repair.
    Nature. 1986 Apr 10-16;320(6062):552-5 PMID: 3960137
  64. Activity of a transfer RNA modifying enzyme during the development of Drosophila and its relationship to the su(s) locus.
    J Mol Biol. 1973 Mar 15;74(4):635-51 PMID: 4199662
  65. Analysis of specific misreading in Escherichia coli.
    J Mol Biol. 1973 Apr 25;75(4):659-72 PMID: 4581523
  66. The readthrough protein A1 is essential for the formation of viable Q beta particles.
    Biochim Biophys Acta. 1974 Dec 6;374(2):238-51 PMID: 4611493
  67. A single UGA codon functions as a natural termination signal in the coliphage q beta coat protein cistron.
    J Mol Biol. 1973 Nov 15;80(4):837-55 PMID: 4773031
  68. Tryptophan transfer RNA as the UGA suppressor.
    J Mol Biol. 1971 Jun 14;58(2):439-58 PMID: 4933412
  69. Correlation between the presence of tRNA His GUG and the erythropoietic function in foetal sheep liver.
    Nucleic Acids Res. 1979 Nov 24;7(6):1635-48 PMID: 503863
  70. Codon--anticodon pairing: the wobble hypothesis.
    J Mol Biol. 1966 Aug;19(2):548-55 PMID: 5969078
  71. Nucleotide sequence of Moloney murine leukaemia virus.
    Nature. 1981 Oct 15-21;293(5833):543-8 PMID: 6169994
  72. The nucleotide sequence of the Akv murine leukemia virus genome.
    Virology. 1984 Apr 15;134(1):196-207 PMID: 6200992
  73. The forms of tRNATrp found in avian sarcoma virus and uninfected chicken cells have structural identity but functional distinctions.
    J Biol Chem. 1980 Oct 10;255(19):9358-68 PMID: 6251085
  74. Complete nucleotide sequence of the genomic RNA of Sindbis virus.
    Virology. 1984 Feb;133(1):92-110 PMID: 6322438
  75. Leaky UAG termination codon in tobacco mosaic virus RNA.
    Nature. 1978 Mar 30;272(5652):469-71 PMID: 634374
  76. The Schizosaccharomyces pombe sup3-i suppressor recognizes ochre, but not amber codons in vitro and in vivo.
    EMBO J. 1984 Feb;3(2):423-8 PMID: 6370683
  77. Codon context effects in missense suppression.
    J Mol Biol. 1984 May 5;175(1):19-27 PMID: 6374155
  78. The effect of point mutations affecting Escherichia coli tryptophan tRNA on anticodon-anticodon interactions and on UGA suppression.
    J Mol Biol. 1984 Aug 5;177(2):329-42 PMID: 6379198
  79. A different approach to RNA sequencing.
    Nature. 1978 Jul 6;274(5666):87-9 PMID: 662002
  80. Nucleotide sequence of tobacco mosaic virus RNA.
    Proc Natl Acad Sci U S A. 1982 Oct;79(19):5818-22 PMID: 6964389
  81. On codon- anticodon interactions.
    Mol Biol Biochem Biophys. 1980;32:347-67 PMID: 7003350
  82. Polypeptides induced by tobacco rattle virus during multiplication in tobacco protoplasts.
    Intervirology. 1982;17(4):240-6 PMID: 7129824
  83. A UGA termination suppression tRNATrp active in rabbit reticulocytes.
    Nature. 1980 Jan 3;283(5742):41-6 PMID: 7350525
  84. Premature translation termination mutations are efficiently suppressed in a highly conserved region of yeast Ste6p, a member of the ATP-binding cassette (ABC) transporter family.
    J Biol Chem. 1994 Jul 8;269(27):17802-8 PMID: 7517933
  85. Purine-purine mismatches in RNA helices: evidence for protonated G.A pairs and next-nearest neighbor effects.
    Nucleic Acids Res. 1995 Jan 25;23(2):302-6 PMID: 7532297
  86. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae.
    J Mol Biol. 1995 Aug 18;251(3):334-45 PMID: 7650736
  87. New insights into mRNA decoding--implications for heterologous protein synthesis.
    Trends Biotechnol. 1993 Dec;11(12):500-5 PMID: 7764419
  88. Codon context and protein synthesis: enhancements of the genetic code.
    Biochimie. 1994;76(5):351-4 PMID: 7849098
  89. Characterization of a point mutation in aspartylglucosaminidase gene: evidence for a readthrough of a translational stop codon.
    Hum Mol Genet. 1994 Dec;3(12):2237-42 PMID: 7881426
  90. Three Tetrahymena tRNA(Gln) isoacceptors as tools for studying unorthodox codon recognition and codon context effects during protein synthesis in vitro.
    Nucleic Acids Res. 1994 Jun 11;22(11):1974-80 PMID: 8029002
  91. Pseudoknot-dependent read-through of retroviral gag termination codons: importance of sequences in the spacer and loop 2.
    EMBO J. 1994 Sep 1;13(17):4137-44 PMID: 8076609
  92. Plant viruses as model systems for the study of non-canonical translation mechanisms in higher plants.
    J Gen Virol. 1994 Sep;75 ( Pt 9):2141-9 PMID: 8077913
  93. The signal for translational readthrough of a UGA codon in Sindbis virus RNA involves a single cytidine residue immediately downstream of the termination codon.
    J Virol. 1993 Aug;67(8):5062-7 PMID: 8331741
  94. Context effects on misreading and suppression at UAG codons in human cells.
    Mol Cell Biol. 1995 Dec;15(12):6593-600 PMID: 8524224
  95. Cysteine tRNAs of plant origin as novel UGA suppressors.
    Nucleic Acids Res. 1995 Nov 25;23(22):4591-7 PMID: 8524647
  96. Local and distant sequences are required for efficient readthrough of the barley yellow dwarf virus PAV coat protein gene stop codon.
    J Virol. 1996 Sep;70(9):5884-92 PMID: 8709208
  97. Translational termination efficiency in both bacteria and mammals is regulated by the base following the stop codon.
    Biochem Cell Biol. 1995 Nov-Dec;73(11-12):1095-103 PMID: 8722026
  98. UGA suppression by tRNACmCATrp occurs in diverse virus RNAs due to a limited influence of the codon context.
    Nucleic Acids Res. 1996 Sep 1;24(17):3424-30 PMID: 8811098
  99. Recoding: dynamic reprogramming of translation.
    Annu Rev Biochem. 1996;65:741-68 PMID: 8811194
  100. Gene expression from viral RNA genomes.
    Plant Mol Biol. 1996 Oct;32(1-2):367-91 PMID: 8980488
  101. The tRNATyr-isoacceptors and their genes in the ciliate Tetrahymena thermophila: cytoplasmic tRNATyr has a QPsiA anticodon and is coded by multiple intron-containing genes.
    Nucleic Acids Res. 1997 Nov 1;25(21):4194-200 PMID: 9336446
  102. Compilation of tRNA sequences and sequences of tRNA genes.
    Nucleic Acids Res. 1998 Jan 1;26(1):148-53 PMID: 9399820
  103. tRNA genes and retroelements in the yeast genome.
    Nucleic Acids Res. 1998 Feb 1;26(3):689-96 PMID: 9443958
  104. Wheat cytoplasmic arginine tRNA isoacceptor with a U*CG anticodon is an efficient UGA suppressor in vitro.
    Nucleic Acids Res. 1998 Mar 15;26(6):1390-5 PMID: 9490782
  105. Complementary base pairing and the origin of substitution mutations.
    Nature. 1976 Sep 23;263(5575):285-9 PMID: 958482
  106. Pleiotropic phenotype of acetyl-CoA-carboxylase-defective yeast cells--viability of a BPL1-amber mutation depending on its readthrough by normal tRNA(Gln)(CAG).
    Eur J Biochem. 1998 Jun 15;254(3):520-6 PMID: 9688262
  107. Rabbit beta-globin is extended beyond its UGA stop codon by multiple suppressions and translational reading gaps.
    Biochemistry. 1998 Aug 4;37(31):10866-70 PMID: 9692979
  108. The hypotrichous ciliate Euplotes octocarinatus has only one type of tRNACys with GCA anticodon encoded on a single macronuclear DNA molecule.
    Nucleic Acids Res. 1998 Oct 15;26(20):4557-65 PMID: 9753721
  109. The influence of 5' codon context on translation termination in Saccharomyces cerevisiae.
    Eur J Biochem. 1998 Oct 1;257(1):249-54 PMID: 9799126
  110. Nucleotide sequences and functional characterization of two tobacco UAG suppressor tRNA(Gln) isoacceptors and their genes.
    Plant Mol Biol. 1998 Nov;38(5):689-97 PMID: 9862487
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2001-12-01
Pages
4767-82
Language
English
Region
England
NLM ID
0411011
PMCID
PMC96686
Subset
IM
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