Protein mistranslation: Friend or foe?

Trends in Biochemical Sciences

Volumn 39, Issue 8, 2014, Pages 355-362

  Ribas de Pouplana, Liuís ^a,b   Santos, Manuel A S ^c   Zhu, Jun Hao ^d   Farabaugh, Philip J ^e   Javid, Babak ^d,f  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^c UNIVERSITY OF AVEIRO   (Portugal)

^d Tsinghua University   (China)

^e UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^f Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease ^*  (China)

Author keywords

Mistranslation; Translational fidelity

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; LEUCINE; METHIONINE; PROTEOME; SERINE; TRANSFER RNA; PROTEIN;

AMINO ACID SEQUENCE; AMINOACYLATION; BACILLUS SUBTILIS; CANDIDA; CANDIDA ALBICANS; CODON; DROSOPHILA MELANOGASTER; ESCHERICHIA COLI; HUMAN; MUTAGENESIS; MYCOBACTERIUM SMEGMATIS; MYCOPLASMA; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; ANIMAL; BIOSYNTHESIS; GENETIC VARIABILITY; GENETICS; MOLECULAR EVOLUTION; RNA EDITING;

ANIMALS; EVOLUTION, MOLECULAR; GENETIC VARIATION; HUMANS; PROTEIN BIOSYNTHESIS; PROTEINS; PROTEOME; RNA EDITING;

EID: 84905014977     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2014.06.002     Document Type: Review

References (64)

1. Lee J.W., et al. Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 2006, 443:50-55.
2. Nangle L.A., et al. Global effects of mistranslation from an editing defect in mammalian cells. Chem. Biol. 2006, 13:1091-1100.
3. Kohanski M.A., et al. Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 2008, 135:679-990.
4. Drummond D.A., Wilke C.O. Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 2008, 134:341-352.
5. Novoa E.M., et al. A role for tRNA modifications in genome structure and codon usage. Cell 2012, 149:202-213.
6. Ibba M., Soll D. Quality control mechanisms during translation. Science 1999, 286:1893-1897.
7. Reynolds N.M., et al. Cellular mechanisms that control mistranslation. Nat. Rev. Microbiol. 2010, 8:849-856.
8. LaRiviere F.J., et al. Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science 2001, 294:165-168.
9. Zaher H.S., Green R. Quality control by the ribosome following peptide bond formation. Nature 2009, 457:161-166.
10. Min B., et al. Protein synthesis in Escherichia coli with mischarged tRNA. J. Bacteriol. 2003, 185:3524-3526.
11. Hartman M.C., et al. Enzymatic aminoacylation of tRNA with unnatural amino acids. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4356-4361.
12. Wang L., et al. Expanding the genetic code. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:225-249.
13. Fan C., et al. Exploring the substrate range of wild-type aminoacyl-tRNA synthetases. Chembiochem 2014, 10.1002/cbic.201402083.
14. Ruan B., et al. Quality control despite mistranslation caused by an ambiguous genetic code. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:16502-16507.
15. Woese C.R. On the evolution of the genetic code. Proc. Natl. Acad. Sci. U.S.A. 1965, 54:1546-1552.
16. Gomes A.C., et al. A genetic code alteration generates a proteome of high diversity in the human pathogen Candida albicans. Genome Biol. 2007, 8:R206.
17. Rocha R., et al. Unveiling the structural basis for translational ambiguity tolerance in a human fungal pathogen. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14091-14096.
18. Suzuki T., et al. The 'polysemous' codon-a codon with multiple amino acid assignment caused by dual specificity of tRNA identity. EMBO J. 1997, 16:1122-1134.
19. Bezerra A.R., et al. Reversion of a fungal genetic code alteration links proteome instability with genomic and phenotypic diversification. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:11079-11084.
20. Li L., et al. Naturally occurring aminoacyl-tRNA synthetases editing-domain mutations that cause mistranslation in Mycoplasma parasites. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9378-9383.
21. Li L., et al. Leucyl-tRNA synthetase editing domain functions as a molecular rheostat to control codon ambiguity in Mycoplasma pathogens. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:3817-3822.
22. Yadavalli S.S., Ibba M. Selection of tRNA charging quality control mechanisms that increase mistranslation of the genetic code. Nucleic Acids Res. 2013, 41:1104-1112.
23. Netzer N., et al. Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 2009, 462:522-526.
24. Jones T.E., et al. Misacylation of specific nonmethionyl tRNAs by a bacterial methionyl-tRNA synthetase. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:6933-6938.
25. Wiltrout E., et al. Misacylation of tRNA with methionine in Saccharomyces cerevisiae. Nucleic Acids Res. 2012, 40:10494-10506.
26. Pan T. Adaptive translation as a mechanism of stress response and adaptation. Annu. Rev. Genet. 2013, 47:121-137.
27. Dale T., Uhlenbeck O.C. Amino acid specificity in translation. Trends Biochem. Sci. 2005, 30:659-665.
28. Dunn J.G., et al. Ribosome profiling reveals pervasive and regulated stop codon readthrough in Drosophila melanogaster. Elife 2013, 2:e01179.
29. Jungreis I., et al. Evidence of abundant stop codon readthrough in Drosophila and other metazoa. Genome Res. 2011, 21:2096-2113.
30. Meyerovich M., et al. Visualizing high error levels during gene expression in living bacterial cells. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11543-11548.
31. Kramer E.B., Farabaugh P.J. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 2007, 13:87-96.
32. Gromadski K.B., Rodnina M.V. Streptomycin interferes with conformational coupling between codon recognition and GTPase activation on the ribosome. Nat. Struct. Mol. Biol. 2004, 11:316-322.
33. Mikkola R., Kurland C.G. Selection of laboratory wild-type phenotype from natural isolates of Escherichia coli in chemostats. Mol. Biol. Evol. 1992, 9:394-402.
34. Manickam N., et al. Studies of translational misreading in vivo show that the ribosome very efficiently discriminates against most potential errors. RNA 2014, 20:9-15.
35. Bacher J.M., Schimmel P. An editing-defective aminoacyl-tRNA synthetase is mutagenic in aging bacteria via the SOS response. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1907-1912.
36. Javid B., et al. Mycobacterial mistranslation is necessary and sufficient for rifampicin phenotypic resistance. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:1132-1137.
37. Ling J., Soll D. Severe oxidative stress induces protein mistranslation through impairment of an aminoacyl-tRNA synthetase editing site. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4028-4033.
38. Branscomb E.W., Galas D.J. Progressive decrease in protein synthesis accuracy induced by streptomycin in Escherichia coli. Nature 1975, 254:161-163.
39. Bacher J.M., et al. Genetic code ambiguity confers a selective advantage on Acinetobacter baylyi. J. Bacteriol. 2007, 189:6494-6496.
40. Peltz S.W., et al. Ribosomal protein L3 mutants alter translational fidelity and promote rapid loss of the yeast killer virus. Mol. Cell. Biol. 1999, 19:384-3891.
41. Pezo V., et al. Artificially ambiguous genetic code confers growth yield advantage. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8593-8597.
42. Santos M.A., et al. Selective advantages created by codon ambiguity allowed for the evolution of an alternative genetic code in Candida spp. Mol. Microbiol. 1999, 31:937-947.
43. Silva R.M., et al. The yeast PNC1 longevity gene is up-regulated by mRNA mistranslation. PLoS ONE 2009, 4:e5212.
44. Murphy H.S., Humayun M.Z. Escherichia coli cells expressing a mutant glyV (glycine tRNA) gene have a UVM-constitutive phenotype: implications for mechanisms underlying the mutA or mutC mutator effect. J. Bacteriol. 1997, 179:7507-7514.
45. Bender A., et al. Adaptive antioxidant methionine accumulation in respiratory chain complexes explains the use of a deviant genetic code in mitochondria. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:16496-16501.
46. Miranda I., et al. Candida albicans CUG mistranslation is a mechanism to create cell surface variation. MBio 2013, 4:e00285.
47. Byrgazov K., et al. Ribosome heterogeneity: another level of complexity in bacterial translation regulation. Curr. Opin. Microbiol. 2013, 16:133-139.
48. Yu X.C., et al. Identification of codon-specific serine to asparagine mistranslation in recombinant monoclonal antibodies by high-resolution mass spectrometry. Anal. Chem. 2009, 81:9282-9290.
49. Guo D., et al. Mechanisms of unintended amino acid sequence changes in recombinant monoclonal antibodies expressed in Chinese Hamster Ovary (CHO) cells. Biotechnol. Bioeng. 2010, 107:163-171.
50. Raina M., et al. Reduced amino acid specificity of mammalian tyrosyl-tRNA synthetase is associated with elevated mistranslation of Tyr codons. J. Biol. Chem. 2014, 289:17780-17790.
51. Reynolds N.M., et al. Cell-specific differences in the requirements for translation quality control. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4063-4068.
52. Galhardo R.S., et al. Mutation as a stress response and the regulation of evolvability. Crit. Rev. Biochem. Mol. Biol. 2007, 42:399-435.
53. Domingo E., et al. Viruses as quasispecies: biological implications. Curr. Top. Microbiol. Immunol. 2006, 299:51-82.
54. Ojosnegros S., et al. Quasispecies as a matter of fact: viruses and beyond. Virus Res. 2011, 162:203-215.
55. Li J.B., et al. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 2009, 324:1210-1213.
56. Schimmel P., Guo M. A tipping point for mistranslation and disease. Nat. Struct. Mol. Biol. 2009, 16:348-349.
57. Loftfield R.B., Vanderjagt D. The frequency of errors in protein biosynthesis. Biochem. J. 1972, 128:1353-1356.
58. Bouadloun F., et al. Codon-specific missense errors in vivo. EMBO J. 1983, 2:1351-1356.
59. Edelmann P., Gallant J. Mistranslation in E. coli. Cell 1977, 10:131-137.
60. Khazaie K., et al. The accuracy of Q beta RNA translation. 1. Errors during the synthesis of Q beta proteins by intact Escherichia coli cells. Eur. J. Biochem. 1984, 144:485-489.
61. Parker J., Friesen J.D. "Two out of three" codon reading leading to mistranslation in vivo. Mol. Gen. Genet. 1980, 177:439-445.
62. Toth M.J., et al. Evidence for a unique first position codon-anticodon mismatch in vivo. J. Mol. Biol. 1988, 201:451-454.
63. Stansfield I., et al. Missense translation errors in Saccharomyces cerevisiae. J. Mol. Biol. 1998, 282:13-24.
64. Curran J.F., Yarus M. Base substitutions in the tRNA anticodon arm do not degrade the accuracy of reading frame maintenance. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:6538-6542.