Protein mistranslation protects bacteria against oxidative stress

Nucleic Acids Research

Volumn 43, Issue 3, 2015, Pages 1740-1748

  Fan, Yongqiang ^a   Wu, Jiang ^a   Ung, Matthew H ^b   De Lay, Nicholas ^a,c   Cheng, Chao ^b   Ling, Jiqiang ^a,c  

^a UNIVERSITY OF TEXAS   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DSRA; HYDROGEN PEROXIDE; RNA; SIGMA FACTOR RPOS; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; ESCHERICHIA COLI; KATE GENE; MUTATION; NONHUMAN; OSMC GENE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MISTRANSLATION; PROTEIN PROCESSING; RNA SEQUENCE; RPOS GENE; UPREGULATION; GENETICS; METABOLISM; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBOSOME;

ESCHERICHIA COLI;

ESCHERICHIA COLI; HYDROGEN PEROXIDE; MUTATION; OXIDATIVE STRESS; PROTEIN BIOSYNTHESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMES;

EID: 84936096893     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1404     Document Type: Article

References (70)

1. Ling,J., Reynolds,N. and Ibba,M. (2009) Aminoacyl-tRNA synthesis and translational quality control. Annu. Rev. Microbiol., 63, 61-78.
2. Zaher,H.S. and Green,R. (2009) Fidelity at the molecular level: lessons from protein synthesis. Cell, 136, 746-762.
3. Kurland,C.G. (1992) Translational accuracy and the fitness of bacteria. Annu. Rev. Genet., 26, 29-50.
4. Kramer,E.B., Vallabhaneni,H., Mayer,L.M. and Farabaugh,P.J. (2010) A comprehensive analysis of translational missense errors in the yeast Saccharomyces cerevisiae. RNA, 16, 1797-1808.
5. Mascarenhas,A.P., An,S., Rosen,A.E., Martinis,S.A. and Musier-Forsyth,K. (2008) In: RajBhandary,UL and Köhrer,C (eds). Protein Engineering. Springer-Verlag, NY, pp. 153-200.
6. Ling,J., So,B.R., Yadavalli,S.S., Roy,H., Shoji,S., Fredrick,K., Musier-Forsyth,K. and Ibba,M. (2009) Resampling and editing of mischarged tRNA prior to translation elongation. Mol. Cell, 33, 654-660.
7. Zaher,H.S. and Green,R. (2009) Quality control by the ribosome following peptide bond formation. Nature, 457, 161-166.
8. Gromadski,K.B. and Rodnina,M.V. (2004) Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol. Cell, 13, 191-200.
9. Zhou,X.L., Ruan,Z.R., Huang,Q., Tan,M. and Wang,E.D. (2013) Translational fidelity maintenance preventing Ser mis-incorporation at Thr codon in protein from eukaryote. Nucleic Acids Res., 41, 302-314.
10. Martinis,S.A. and Boniecki,M.T. (2010) The balance between pre- and post-transfer editing in tRNA synthetases. FEBS Lett., 584, 455-459.
11. Roy,H., Ling,J., Irnov,M. and Ibba,M. (2004) Post-transfer editing in vitro and in vivo by the beta subunit of phenylalanyl-tRNA synthetase. EMBO J., 23, 4639-4648.
12. Ogle,J.M. and Ramakrishnan,V. (2005) Structural insights into translational fidelity. Annu. Rev. Biochem., 74, 129-177.
13. Netzer,N., Goodenbour,J.M., David,A., Dittmar,K.A., Jones,R.B., Schneider,J.R., Boone,D., Eves,E.M., Rosner,M.R., Gibbs,J.S. et al. (2009) Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature, 462, 522-526.
14. Ogle,J.M., Murphy,F.V., Tarry,M.J. and Ramakrishnan,V. (2002) Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell, 111, 721-732.
15. Ogle,J.M., Brodersen,D.E., Clemons,W.M. Jr, Tarry,M.J., Carter,A.P. and Ramakrishnan,V. (2001) Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science, 292, 897-902.
16. Pape,T., Wintermeyer,W. and Rodnina,M. (1999) Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome. EMBO J., 18, 3800-3807.
17. Gorini,L. and Kataja,E. (1964) Phenotypic repair by streptomycin of defective genotypes in E. coli. Proc. Natl. Acad. Sci. U.S.A., 51, 487-493.
18. Gromadski,K.B. and Rodnina,M.V. (2004) Streptomycin interferes with conformational coupling between codon recognition and GTPase activation on the ribosome. Nat. Struct. Mol. Biol., 11, 316-322.
19. Carter,A.P., Clemons,W.M., Brodersen,D.E., Morgan-Warren,R.J., Wimberly,B.T. and Ramakrishnan,V. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature, 407, 340-348.
20. McClory,S.P., Leisring,J.M., Qin,D. and Fredrick,K. (2010) Missense suppressor mutations in 16S rRNA reveal the importance of helices h8 and h14 in aminoacyl-tRNA selection. RNA, 16, 1925-1934.
21. Qin,D. and Fredrick,K. (2009) Control of translation initiation involves a factor-induced rearrangement of helix 44 of 16S ribosomal RNA. Mol. Microbiol., 71, 1239-1249.
22. Allen,P.N. and Noller,H.F. (1991) A single base substitution in 16S ribosomal RNA suppresses streptomycin dependence and increases the frequency of translational errors. Cell, 66, 141-148.
23. Drummond,D.A. and Wilke,C.O. (2009) The evolutionary consequences of erroneous protein synthesis. Nat. Rev. Genet., 10, 715-724.
24. Karkhanis,V.A., Mascarenhas,A.P. and Martinis,S.A. (2007) Amino acid toxicities of Escherichia coli that are prevented by leucyl-tRNA synthetase amino acid editing. J. Bacteriol., 189, 8765-8768.
25. Döring,V., Mootz,H.D., Nangle,L.A., Hendrickson,T.L., Crécy-Lagard,V., Schimmel,P. and Marliere,P. (2001) Enlarging the amino acid set of Escherichia coli by infiltration of the valine coding pathway. Science, 292, 501-504.
26. Reynolds,N.M., Ling,J., Roy,H., Banerjee,R., Repasky,S.E., Hamel,P. and Ibba,M. (2010) Cell-specific differences in the requirements for translation quality control. Proc. Natl. Acad. Sci. U.S.A., 107, 4063-4068.
27. Nangle,L.A., Motta,C.M. and Schimmel,P. (2006) Global effects of mistranslation from an editing defect in mammalian cells. Chem. Biol., 13, 1091-1100.
28. Lee,J.W., Beebe,K., Nangle,L.A., Jang,J., Longo-Guess,C.M., Cook,S.A., Davisson,M.T., Sundberg,J.P., Schimmel,P. and Ackerman,S.L. (2006) Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature, 443, 50-55.
29. Mikkola,R. and Kurland,C.G. (1992) Selection of laboratory wild-type phenotype from natural isolates of Escherichia coli in chemostats. Mol. Biol. Evol., 9, 394-402.
30. Li,L., Boniecki,M.T., Jaffe,J.D., Imai,B.S., Yau,P.M., Luthey-Schulten,Z.A. and Martinis,S.A. (2011) Naturally occurring aminoacyl-tRNA synthetases editing-domain mutations that cause mistranslation in Mycoplasma parasites. Proc. Natl. Acad. Sci. U.S.A., 108, 9378-9383.
31. Yadavalli,S.S. and Ibba,M. (2013) Selection of tRNA charging quality control mechanisms that increase mistranslation of the genetic code. Nucleic Acids Res., 41, 1104-1112.
32. Ling,J., Peterson,K.M., Simonovic,I., Söll,D. and Simonovic,M. (2012) The mechanism of pre-transfer editing in yeast mitochondrial threonyl-tRNA synthetase. J. Biol. Chem., 287, 28518-28525.
33. Ballesteros,M., Fredriksson,A., Henriksson,J. and Nystrom,T. (2001) Bacterial senescence: protein oxidation in non-proliferating cells is dictated by the accuracy of the ribosomes. EMBO J., 20, 5280-5289.
34. Ling,J. and Söll,D. (2010) Severe oxidative stress induces protein mistranslation through impairment of an aminoacyl-tRNA synthetase editing site. Proc. Natl. Acad. Sci. U.S.A., 107, 4028-4033.
35. Wu,J., Fan,Y. and Ling,J. (2014) Mechanism of oxidant-induced mistranslation by threonyl-tRNA synthetase. Nucleic Acids Res., 42, 6523-6531.
36. Pan,T. (2013) Adaptive translation as a mechanism of stress response and adaptation. Annu. Rev. Genet., 47, 121-137.
37. Pouplana,L.R., Santos,M.A., Zhu,J.H., Farabaugh,P.J. and Javid,B. (2014) Protein mistranslation: friend or foe? Trends Biochem. Sci., 39, 355-362.
38. Kitagawa,M., Ara,T., Arifuzzaman,M., Ioka-Nakamichi,T., Inamoto,E., Toyonaga,H. and Mori,H. (2005) Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res., 12, 291-299.
39. Mandin,P. and Gottesman,S. (2010) Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J., 29, 3094-3107.
40. Wang,H.H., Isaacs,F.J., Carr,P.A., Sun,Z.Z., Xu,G., Forest,C.R. and Church,G.M. (2009) Programming cells by multiplex genome engineering and accelerated evolution. Nature, 460, 894-898.
41. Wang,H.H., Kim,H., Cong,L., Jeong,J., Bang,D. and Church,G.M. (2012) Genome-scale promoter engineering by coselection MAGE. Nat. Methods, 9, 591-593.
42. Datsenko,K.A. and Wanner,B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A., 97, 6640-6645.
43. Ling,J., Cho,C., Guo,L.T., Aerni,H.R., Rinehart,J. and Söll,D. (2012) Protein aggregation caused by aminoglycoside action is prevented by a hydrogen peroxide scavenger. Mol. Cell, 48, 713-722.
44. Subramaniam,A.R., Pan,T. and Cluzel,P. (2013) Environmental perturbations lift the degeneracy of the genetic code to regulate protein levels in bacteria. Proc. Natl. Acad. Sci. U.S.A., 110, 2419-2424.
45. McClure,R., Balasubramanian,D., Sun,Y., Bobrovskyy,M., Sumby,P., Genco,C.A., Vanderpool,C.K. and Tjaden,B. (2013) Computational analysis of bacterial RNA-Seq data. Nucleic Acids Res., 41, e140.
46. Masse,E., Vanderpool,C.K. and Gottesman,S. (2005) Effect of RyhB small RNA on global iron use in Escherichia coli. J. Bacteriol., 187, 6962-6971.
47. Miller,J. (1972) Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
48. Soper,T., Mandin,P., Majdalani,N., Gottesman,S. and Woodson,S.A. (2010) Positive regulation by small RNAs and the role of Hfq. Proc. Natl. Acad. Sci. U.S.A., 107, 9602-9607.
49. Bjorkman,J., Samuelsson,P., Andersson,D.I. and Hughes,D. (1999) Novel ribosomal mutations affecting translational accuracy, antibiotic resistance and virulence of Salmonella Typhimurium. Mol. Microbiol., 31, 53-58.
50. Kramer,E.B. and Farabaugh,P.J. (2007) The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA, 13, 87-96.
51. Battesti,A., Majdalani,N. and Gottesman,S. (2011) The RpoS-mediated general stress response in Escherichia coli. Annu. Rev. Microbiol., 65, 189-213.
52. Imlay,J.A. (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem., 77, 755-776.
53. Aslund,F., Zheng,M., Beckwith,J. and Storz,G. (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl. Acad. Sci. U.S.A., 96, 6161-6165.
54. Loewen,P.C., Switala,J. and Triggs-Raine,B.L. (1985) Catalases HPI and HPII in Escherichia coli are induced independently. Arch. Biochem. Biophys., 243, 144-149.
55. Conter,A., Gangneux,C., Suzanne,M. and Gutierrez,C. (2001) Survival of Escherichia coli during long-term starvation: effects of aeration, NaCl, and the rpoS and osmC gene products. Res. Microbiol., 152, 17-26.
56. Lesniak,J., Barton,W.A. and Nikolov,D.B. (2003) Structural and functional features of the Escherichia coli hydroperoxide resistance protein OsmC. Protein Sci., 12, 2838-2843.
57. Fredriksson,A., Ballesteros,M., Peterson,C.N., Persson,O., Silhavy,T.J. and Nystrom,T. (2007) Decline in ribosomal fidelity contributes to the accumulation and stabilization of the master stress response regulator sigmaS upon carbon starvation. Genes Dev., 21, 862-874.
58. Mandin,P. and Gottesman,S. (2010) Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J., 29, 3094-3107.
59. Majdalani,N., Chen,S., Murrow,J., St John,K. and Gottesman,S. (2001) Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol. Microbiol., 39, 1382-1394.
60. Repoila,F. and Gottesman,S. (2001) Signal transduction cascade for regulation of RpoS: temperature regulation of DsrA. J. Bacteriol., 183, 4012-4023.
61. Rosenthal,G.A. (1977) The biological effects and mode of action of L-canavanine, a structural analogue of L-arginine. Q. Rev. Biol., 52, 155-178.
62. Davis,B.D. (1987) Mechanism of bactericidal action of aminoglycosides. Microbiol. Rev., 51, 341-350.
63. Bezerra,A.R., Simoes,J., Lee,W., Rung,J., Weil,T., Gut,I.G., Gut,M., Bayes,M., Rizzetto,L., Cavalieri,D. et al. (2013) Reversion of a fungal genetic code alteration links proteome instability with genomic and phenotypic diversification. Proc. Natl. Acad. Sci. U.S.A., 110, 11079-11084.
64. Santos,M.A., Cheesman,C., Costa,V., Moradas-Ferreira,P. and Tuite,M.F. (1999) Selective advantages created by codon ambiguity allowed for the evolution of an alternative genetic code in Candida spp. Mol. Microbiol., 31, 937-947.
65. Javid,B., Sorrentino,F., Toosky,M., Zheng,W., Pinkham,J.T., Jain,N., Pan,M., Deighan,P. and Rubin,E.J. (2014) Mycobacterial mistranslation is necessary and sufficient for rifampicin phenotypic resistance. Proc. Natl. Acad. Sci. U.S.A., 111, 1132-1137.
66. Ruan,B., Palioura,S., Sabina,J., Marvin-Guy,L., Kochhar,S., Larossa,R.A. and Söll,D. (2008) Quality control despite mistranslation caused by an ambiguous genetic code. Proc. Natl. Acad. Sci. U.S.A., 105, 16502-16507.
67. Chiang,S.M. and Schellhorn,H.E. (2010) Evolution of the RpoS regulon: origin of RpoS and the conservation of RpoS-dependent regulation in bacteria. J. Mol. Evol., 70, 557-571.
68. Hampton,M.B., Kettle,A.J. and Winterbourn,C.C. (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood, 92, 3007-3017.
69. McCullen,C.A., Benhammou,J.N., Majdalani,N. and Gottesman,S. (2010) Mechanism of positive regulation by DsrA and RprA small noncoding RNAs: pairing increases translation and protects rpoS mRNA from degradation. J. Bacteriol., 192, 5559-5571.
70. Davies,J., Gilbert,W. and Gorini,L. (1964) Streptomycin, suppression, and the code. Proc. Natl. Acad. Sci. U.S.A., 51, 883-890.