Transfer RNAs Mediate the Rapid Adaptation of to Oxidative Stress

English version České info

All organisms need to respond quickly to sudden environmental changes. Translational regulation can occur in response to environmental stresses within minutes, which is much faster than transcriptional regulation, and thus normally provides immediate adaptation. Eukaryotic cells can manipulate their tRNA molecules, mainly in a reversible manner, to suppress translation. Here, we showed for the first time that bacteria respond to oxidative stress by adjusting the translational system in a manner that differs from that of eukaryotes. The bacteria nonspecifically, irreversibly, and enzymatically degrade tRNAs to block protein synthesis. Interestingly, we showed that elevated tRNA concentrations lead to opposing effects by causing increased protein aggregation, which impairs fitness under normal conditions but facilitates adaptation under oxidative stress, including that caused by antibiotics. Our results provide a new understanding of the role of global adjustments to the entire translation system during stress adaptation in bacteria. This mechanism may also be involved in the development of antibiotic resistance in bacteria.

Vyšlo v časopise: Transfer RNAs Mediate the Rapid Adaptation of to Oxidative Stress. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005302
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005302

Souhrn

Zdroje

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 (2012) Protein Synthesis and the Stress Response. In: Biyani M, editor. 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