Transfer RNAs Mediate the Rapid Adaptation of Escherichia coli to Oxidative Stress

PLoS Genetics

Volumn 11, Issue 6, 2015, Pages

  Zhong, Jiayong ^a   Xiao, Chuanle ^a,b   Gu, Wei ^a   Du, Gaofei ^a   Sun, Xuesong ^a   He, Qing Yu ^a   Zhang, Gong ^a  

^a JINAN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; CIPROFLOXACIN; HYDROGEN PEROXIDE; PROTEOME; TRANSFER RNA;

ANTIBIOTIC RESISTANCE; ARTICLE; DOWN REGULATION; ESCHERICHIA COLI; EVOLUTIONARY ADAPTATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; RNA TRANSLATION; TRANSLATION ELONGATION; TRANSLATION INITIATION; ADAPTATION; GENETICS; METABOLISM;

ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA;

ADAPTATION, PHYSIOLOGICAL; DOWN-REGULATION; ESCHERICHIA COLI; OXIDATIVE STRESS; RNA, TRANSFER;

EID: 84937795234     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005302     Document Type: Article

References (68)

1. Cabiscol E, Tamarit J, Ros J, (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3: 3–8. 10963327
2. Kryston TB, Georgiev AB, Pissis P, Georgakilas AG, (2011) Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res 711: 193–201. doi: 10.1016/j.mrfmmm.2010.12.016 21216256
3. Imlay JA, (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11: 443–454. doi: 10.1038/nrmicro3032 23712352
4. Jozefczuk S, Klie S, Catchpole G, Szymanski J, Cuadros-Inostroza A, et al. (2010) Metabolomic and transcriptomic stress response of Escherichia coli. Mol Syst Biol 6: 364. doi: 10.1038/msb.2010.18 20461071
5. Lackner DH, Schmidt MW, Wu S, Wolf DA, Bahler J, (2012) Regulation of transcriptome, translation, and proteome in response to environmental stress in fission yeast. Genome Biol 13: R25. doi: 10.1186/gb-2012-13-4-r25 22512868
6. Davies KJ, (1999) The broad spectrum of responses to oxidants in proliferating cells: a new paradigm for oxidative stress. IUBMB Life 48: 41–47. 10791914
7. de Nadal E, Ammerer G, Posas F, (2011) Controlling gene expression in response to stress. Nat Rev Genet 12: 833–845. doi: 10.1038/nrg3055 22048664
8. Shenton D, Smirnova JB, Selley JN, Carroll K, Hubbard SJ, et al. (2006) Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. J Biol Chem 281: 29011–29021. 16849329
9. Thompson DM, Lu C, Green PJ, Parker R, (2008) tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14: 2095–2103. doi: 10.1261/rna.1232808 18719243
10. Yamasaki S, Ivanov P, Hu GF, Anderson P, (2009) Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol 185: 35–42. doi: 10.1083/jcb.200811106 19332886
11. Fu H, Feng J, Liu Q, Sun F, Tie Y, et al. (2009) Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett 583: 437–442. doi: 10.1016/j.febslet.2008.12.043 19114040
12. Saikia M, Krokowski D, Guan BJ, Ivanov P, Parisien M, et al. (2012) Genome-wide identification and quantitative analysis of cleaved tRNA fragments induced by cellular stress. J Biol Chem 287: 42708–42725. doi: 10.1074/jbc.M112.371799 23086926
13. Czech A, Wende S, Morl M, Pan T, Ignatova Z, (2013) Reversible and rapid transfer-RNA deactivation as a mechanism of translational repression in stress. PLoS Genet 9: e1003767. doi: 10.1371/journal.pgen.1003767 24009533
14. Lee YS, Shibata Y, Malhotra A, Dutta A, (2009) A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 23: 2639–2649. doi: 10.1101/gad.1837609 19933153
15. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P, (2011) Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell 43: 613–623. doi: 10.1016/j.molcel.2011.06.022 21855800
16. Vogel C, Silva GM, Marcotte EM, (2011) Protein expression regulation under oxidative stress. Mol Cell Proteomics 10: M111 009217.
17. Chan CT, Pang YL, Deng W, Babu IR, Dyavaiah M, et al. (2012) Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat Commun 3: 937. doi: 10.1038/ncomms1938 22760636
18. Tomita K, Ogawa T, Uozumi T, Watanabe K, Masaki H, (2000) A cytotoxic ribonuclease which specifically cleaves four isoaccepting arginine tRNAs at their anticodon loops. Proc Natl Acad Sci U S A 97: 8278–8283. 10880568
19. Jiang Y, Meidler R, Amitsur M, Kaufmann G, (2001) Specific interaction between anticodon nuclease and the tRNA(Lys) wobble base. J Mol Biol 305: 377–388. 11152597
20. Meineke B, Shuman S, (2012) Determinants of the cytotoxicity of PrrC anticodon nuclease and its amelioration by tRNA repair. RNA 18: 145–154. doi: 10.1261/rna.030171.111 22101242
21. Ling J, Soll 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. doi: 10.1073/pnas.1000315107 20160114
22. Bessette PH, Aslund F, Beckwith J, Georgiou G, (1999) Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm. Proc Natl Acad Sci U S A 96: 13703–13708. 10570136
23. Sorensen HP, Mortensen KK, (2005) Advanced genetic strategies for recombinant protein expression in Escherichia coli. J Biotechnol 115: 113–128. 15607230
24. Tang Y, Quail MA, Artymiuk PJ, Guest JR, Green J, (2002) Escherichia coli aconitases and oxidative stress: post-transcriptional regulation of sodA expression. Microbiology 148: 1027–1037. 11932448
25. Luders S, Fallet C, Franco-Lara E, (2009) Proteome analysis of the Escherichia coli heat shock response under steady-state conditions. Proteome Sci 7: 36. doi: 10.1186/1477-5956-7-36 19772559
26. Maier T, Schmidt A, Guell M, Kuhner S, Gavin AC, et al. (2011) Quantification of mRNA and protein and integration with protein turnover in a bacterium. Mol Syst Biol 7: 511. doi: 10.1038/msb.2011.38 21772259
27. Wu J, Jiang Z, Liu M, Gong X, Wu S, et al. (2009) Polynucleotide phosphorylase protects Escherichia coli against oxidative stress. Biochemistry 48: 2012–2020. doi: 10.1021/bi801752p 19219992
28. Mostertz J, Scharf C, Hecker M, Homuth G, (2004) Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiology 150: 497–512. 14766928
29. Doherty MK, Hammond DE, Clague MJ, Gaskell SJ, Beynon RJ, (2009) Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. J Proteome Res 8: 104–112. doi: 10.1021/pr800641v 18954100
30. Westman-Brinkmalm A, Abramsson A, Pannee J, Gang C, Gustavsson MK, et al. (2011) SILAC zebrafish for quantitative analysis of protein turnover and tissue regeneration. J Proteomics 75: 425–434. doi: 10.1016/j.jprot.2011.08.008 21890006
31. Cambridge SB, Gnad F, Nguyen C, Bermejo JL, Kruger M, et al. (2011) Systems-wide proteomic analysis in mammalian cells reveals conserved, functional protein turnover. J Proteome Res 10: 5275–5284. doi: 10.1021/pr101183k 22050367
32. Mann M, (2006) Functional and quantitative proteomics using SILAC. Nat Rev Mol Cell Biol 7: 952–958. 17139335
33. Hinkson IV, Elias JE, (2011) The dynamic state of protein turnover: It's about time. Trends Cell Biol 21: 293–303. doi: 10.1016/j.tcb.2011.02.002 21474317
34. Snijders AP, de Koning B, Wright PC, (2005) Perturbation and interpretation of nitrogen isotope distribution patterns in proteomics. J Proteome Res 4: 2185–2191. 16335965
35. Martin SF, Munagapati VS, Salvo-Chirnside E, Kerr LE, Le Bihan T, (2012) Proteome turnover in the green alga Ostreococcus tauri by time course 15N metabolic labeling mass spectrometry. J Proteome Res 11: 476–486. doi: 10.1021/pr2009302 22077659
36. Xiao CL, Chen XZ, Du YL, Sun X, Zhang G, et al. (2013) Binomial probability distribution model-based protein identification algorithm for tandem mass spectrometry utilizing peak intensity information. J Proteome Res 12: 328–335. doi: 10.1021/pr300781t 23163785
37. Imlay JA, Linn S, (1986) Bimodal pattern of killing of DNA-repair-defective or anoxically grown Escherichia coli by hydrogen peroxide. J Bacteriol 166: 519–527. 3516975
38. Imlay JA, Linn S, (1987) Mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide. J Bacteriol 169: 2967–2976. 3298208
39. Filiou MD, Varadarajulu J, Teplytska L, Reckow S, Maccarrone G, et al. (2012) The 15N isotope effect in Escherichia coli: a neutron can make the difference. Proteomics 12: 3121–3128. doi: 10.1002/pmic.201200209 22887715
40. Fedyunin I, Lehnhardt L, Bohmer N, Kaufmann P, Zhang G, et al. (2012) tRNA concentration fine tunes protein solubility. FEBS Lett 586: 3336–3340. doi: 10.1016/j.febslet.2012.07.012 22819830
41. Tamarit J, Cabiscol E, Ros J, (1998) Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J Biol Chem 273: 3027–3032. 9446617
42. Machnicka MA, Milanowska K, Osman Oglou O, Purta E, Kurkowska M, et al. (2013) MODOMICS: a database of RNA modification pathways--2013 update. Nucleic Acids Res 41: D262–267. doi: 10.1093/nar/gks1007 23118484
43. Puri P, Wetzel C, Saffert P, Gaston KW, Russell SP, et al. (2014) Systematic identification of tRNAome and its dynamics in Lactococcus lactis. Mol Microbiol.
44. Zhang G, Fedyunin I, Miekley O, Valleriani A, Moura A, et al. (2010) Global and local depletion of ternary complex limits translational elongation. Nucleic Acids Res 38: 4778–4787. doi: 10.1093/nar/gkq196 20360046
45. Zhang G, Hubalewska M, Ignatova Z, (2009) Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nat Struct Mol Biol 16: 274–280. doi: 10.1038/nsmb.1554 19198590
46. Goswami M, Mangoli SH, Jawali N, (2006) Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrob Agents Chemother 50: 949–954. 16495256
47. Dwyer DJ, Kohanski MA, Hayete B, Collins JJ, (2007) Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli. Mol Syst Biol 3: 91. 17353933
48. Katz A, Orellana O, Biyani M, (2012) Protein Synthesis and the Stress Response. In: Cell-Free Protein Synthesis: InTech. pp. 111–134.
49. Moll I, Engelberg-Kulka H, (2012) Selective translation during stress in Escherichia coli. Trends Biochem Sci 37: 493–498. doi: 10.1016/j.tibs.2012.07.007 22939840
50. Nakamura T, Cho DH, Lipton SA, (2012) Redox regulation of protein misfolding, mitochondrial dysfunction, synaptic damage, and cell death in neurodegenerative diseases. Exp Neurol 238: 12–21. doi: 10.1016/j.expneurol.2012.06.032 22771760
51. Bhattacharya A, Wei R, Hamilton RT, Chaudhuri AR, (2014) Neuronal cells but not muscle cells are resistant to oxidative stress mediated protein misfolding and cell death: role of molecular chaperones. Biochem Biophys Res Commun 446: 1250–1254. doi: 10.1016/j.bbrc.2014.03.097 24685484
52. Collins LJ, Biggs PJ, (2011) RNA networks in prokaryotes II: tRNA processing and small RNAs. Adv Exp Med Biol 722: 221–230. doi: 10.1007/978-1-4614-0332-6_14 21915792
53. Deutscher MP, (1984) Processing of tRNA in prokaryotes and eukaryotes. CRC Crit Rev Biochem 17: 45–71. 6094100
54. Durfee T, Hansen AM, Zhi H, Blattner FR, Jin DJ, (2008) Transcription profiling of the stringent response in Escherichia coli. J Bacteriol 190: 1084–1096. 18039766
55. Lowe TM, Eddy SR, (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955–964. 9023104
56. Chan PP, Lowe TM, (2009) GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res 37: D93–97. doi: 10.1093/nar/gkn787 18984615
57. Zhang G, Lukoszek R, Mueller-Roeber B, Ignatova Z, (2011) Different sequence signatures in the upstream regions of plant and animal tRNA genes shape distinct modes of regulation. Nucleic Acids Res 39: 3331–3339. doi: 10.1093/nar/gkq1257 21138970
58. Phizicky EM, Hopper AK, (2010) tRNA biology charges to the front. Genes Dev 24: 1832–1860. doi: 10.1101/gad.1956510 20810645
59. Chen P, Jager G, Zheng B, (2010) Transfer RNA modifications and genes for modifying enzymes in Arabidopsis thaliana. BMC Plant Biol 10: 201. doi: 10.1186/1471-2229-10-201 20836892
60. Hopper AK, Phizicky EM, (2003) tRNA transfers to the limelight. Genes Dev 17: 162–180. 12533506
61. Sneppen K, Dodd IB, Shearwin KE, Palmer AC, Schubert RA, et al. (2005) A mathematical model for transcriptional interference by RNA polymerase traffic in Escherichia coli. J Mol Biol 346: 399–409. 15670592
62. Perez-Ortin JE, Alepuz PM, Moreno J, (2007) Genomics and gene transcription kinetics in yeast. Trends Genet 23: 250–257. 17379352
63. Jepras RI, Carter J, Pearson SC, Paul FE, Wilkinson MJ, (1995) Development of a robust flow cytometric assay for determining numbers of viable bacteria. Appl Environ Microbiol 61: 2696–2701. 16535078
64. Rault A, Beal C, Ghorbal S, Ogier JC, Bouix M, (2007) Multiparametric flow cytometry allows rapid assessment and comparison of lactic acid bacteria viability after freezing and during frozen storage. Cryobiology 55: 35–43. 17577587
65. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M, (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856–2860. 17406544
66. Sun X, Jia HL, Xiao CL, Yin XF, Yang XY, et al. (2011) Bacterial proteome of streptococcus pneumoniae through multidimensional separations coupled with LC-MS/MS. OMICS 15: 477–482. doi: 10.1089/omi.2010.0113 21699404
67. Bore E, Hebraud M, Chafsey I, Chambon C, Skjaeret C, et al. (2007) Adapted tolerance to benzalkonium chloride in Escherichia coli K-12 studied by transcriptome and proteome analyses. Microbiology 153: 935–946. 17379704
68. Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, et al. (2006) Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 21: 87–96. 16387656