Non-canonical roles of tRNAs and tRNA mimics in bacterial cell biology

Molecular Microbiology

Volumn 101, Issue 4, 2016, Pages 545-558

  Katz, Assaf ^a   Elgamal, Sara ^b   Rajkovic, Andrei ^b   Ibba, Michael ^b  

^a UNIVERSITY OF CHILE   (Chile)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; TRANSFER RNA;

ACIDITHIOBACILLUS FERROOXIDANS; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GENOME; CATALYSIS; CYTOLOGY; ESCHERICHIA COLI; GENE SEQUENCE; METABOLITE; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; NONHUMAN; OPERON; PHYLOGENY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; RNA STRUCTURE; RNA TRANSLATION; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84981164223     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13419     Document Type: Review

References (164)

1. Ataide, S.F., Jester, B.C., Devine, K.M., and Ibba, M. (2005) Stationary-phase expression and aminoacylation of a transfer-RNA-like small RNA. EMBO Rep 6: 742–747.
2. Bailly, M., Blaise, M., Lorber, B., Becker, H.D., and Kern, D. (2007) The transamidosome: a dynamic ribonucleoprotein particle dedicated to prokaryotic tRNA-dependent asparagine biosynthesis. Mol Cell 28: 228–239.
3. Banerjee, R., Chen, S., Dare, K., Gilreath, M., Praetorius-Ibba, M., Raina, M., et al. (2010) tRNAs: cellular barcodes for amino acids. FEBS Lett 584: 387–395.
4. Belin, P., Moutiez, M., Lautru, S., Seguin, J., Pernodet, J.-L., and Gondry, M. (2012) The nonribosomal synthesis of diketopiperazines in tRNA-dependent cyclodipeptide synthase pathways. Nat Prod Rep 29: 961–979.
5. Benner, S.A., Ellington, A.D., and Tauer, A. (1989) Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci USA 86: 7054–7058.
6. Berger-Bächi, B., and Tschierske, M. (1998) Role of fem factors in methicillin resistance. Drug Resist Updat Rev Comment Antimicrob Anticancer Chemother 1: 325–335.
7. Berthelot, F., Bogdanovsky, D., Schapira, G., and Gros, F. (1973) Interchangeability of factors and tRNA's in bacterial and eukaryotic translation initiation systems. Mol Cell Biochem 1: 63–72.
8. Beuning, P.J., and Musier-Forsyth, K. (1999) Transfer RNA recognition by aminoacyl-tRNA synthetases. Biopolymers 52: 1–28.
9. Bhaskaran, H., and Perona, J.J. (2011) Two-step aminoacylation of tRNA without channeling in Archaea. J Mol Biol 411: 854–869.
10. Björk, G.R., Durand, J.M.B., Hagervall, T.G., Leipuviene, R., Lundgren, H.K., Nilsson, K., et al. (1999) Transfer RNA modification: influence on translational frameshifting and metabolism. FEBS Lett 452: 47–51.
11. Blaha, G., Stanley, R.E., and Steitz, T.A. (2009) Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science 325: 966–970.
12. Asp QUC anticodon. Nucleic Acids Res 32: 2768–2775.
13. Blaise, M., Becker, H.D., Lapointe, J., Cambillau, C., Giegé, R., and Kern, D. (2005) Glu-Q-tRNA(Asp) synthetase coded by the yadB gene, a new paralog of aminoacyl-tRNA synthetase that glutamylates tRNA(Asp) anticodon. Biochimie 87: 847–861.
14. Boël, G., Smith, P.C., Ning, W., Englander, M.T., Chen, B., Hashem, Y., et al. (2014) The ABC-F protein EttA gates ribosome entry into the translation elongation cycle. Nat Struct Mol Biol 21: 143–151.
15. Bonnefond, L., Arai, T., Sakaguchi, Y., Suzuki, T., Ishitani, R., and Nureki, O. (2011) Structural basis for nonribosomal peptide synthesis by an aminoacyl-tRNA synthetase paralog. Proc Natl Acad Sci USA 108: 3912–3917.
16. Buck, M., and Ames, B.N. (1984) A modified nucleotide in tRNA as a possible regulator of aerobiosis: synthesis of cis-2-methyl-thioribosylzeatin in the tRNA of Salmonella. Cell 36: 523–531.
17. Bullwinkle, T.J., and Ibba, M. (2016) Translation quality control is critical for bacterial responses to amino acid stress. Proc Natl Acad Sci USA 113: 2252–2257.
18. Bumsted, R.M., Dahl, J.L., Söll, D., and Strominger, J.L. (1968) Biosynthesis of the peptidoglycan of bacterial cell walls. X. Further study of the glycyl transfer ribonucleic acids active in peptidoglycan synthesis in Staphylococcus aureus. J Biol Chem 243: 779–782.
19. Caballero, V.C., Toledo, V.P., Maturana, C., Fisher, C.R., Payne, S.M., and Salazar, J.C. (2012) Expression of Shigella flexneri gluQ-rs gene is linked to dksA and controlled by a transcriptional terminator. BMC Microbiol 12: 226.
20. Campanacci, V., Dubois, D.Y., Becker, H.D., Kern, D., Spinelli, S., Valencia, C., et al. (2004) The Escherichia coli YadB gene product reveals a novel aminoacyl-tRNA synthetase like activity. J Mol Biol 337: 273–283.
21. Cavarelli, J., and Moras, D. (1993) Recognition of tRNAs by aminoacyl-tRNA synthetases. FASEB J Off Publ Fed Am Soc Exp Biol 7: 79–86.
22. Chadani, Y., Ono, K., Ozawa, S.-I., Takahashi, Y., Takai, K., Nanamiya, H., et al. (2010) Ribosome rescue by Escherichia coli ArfA (YhdL) in the absence of trans-translation system. Mol Microbiol 78: 796–808.
23. Chan, C.T.Y., Pang, Y.L.J., Deng, W., Babu, I.R., Dyavaiah, M., Begley, T.J., and Dedon, P.C. (2012) Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat Commun 3: 937.
24. Colussi, T.M., Costantino, D.A., Hammond, J.A., Ruehle, G.M., Nix, J.C., and Kieft, J.S. (2014) The structural basis of transfer RNA mimicry and conformational plasticity by a viral RNA. Nature 511: 366–369.
25. Crick, F. (1958) On Protein Synthesis. Symp Soc Exp Biol 12: 138–163.
26. Crick, F. (1970) Central dogma of molecular biology. Nature 227: 561–563.
27. Cruz, J.W., Sharp, J.D., Hoffer, E.D., Maehigashi, T., Vvedenskaya, I.O., Konkimalla, A., et al. (2015) Growth-regulating Mycobacterium tuberculosis VapC-mt4 toxin is an isoacceptor-specific tRNase. Nat Commun 6: 7480.
28. Dale, T., and Uhlenbeck, O.C. (2005) Amino acid specificity in translation. Trends Biochem Sci 30: 659–665.
29. Dare, K., and Ibba, M. (2012) Roles of tRNA in cell wall biosynthesis. Wiley Interdiscip Rev RNA 3: 247–264.
30. Dedon, P.C., and Begley, T.J. (2014) A system of RNA modifications and biased codon use controls cellular stress response at the level of translation. Chem Res Toxicol 27: 330–337.
31. Di Giulio, M. (1995) The phylogeny of tRNAs seems to confirm the predictions of the coevolution theory of the origin of the genetic code. Orig Life Evol Biosph 25: 549–564.
32. Di Giulio, M. (2006) The non-monophyletic origin of the tRNA molecule and the origin of genes only after the evolutionary stage of the last universal common ancestor (LUCA). J Theor Biol 240: 343–352.
33. Doerfel, L.K., Wohlgemuth, I., Kothe, C., Peske, F., Urlaub, H., and Rodnina, M.V. (2013) EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339: 85–88.
34. Doerfel, L.K., Wohlgemuth, I., Kubyshkin, V., Starosta, A.L., Wilson, D.N., Budisa, N., and Rodnina, M.V. (2015) Entropic Contribution of Elongation Factor P to Proline Positioning at the Catalytic Center of the Ribosome. J Am Chem Soc 137: 12997–13006.
35. Dougan, D.A., Micevski, D., and Truscott, K.N. (2012) The N-end rule pathway: from recognition by N-recognins, to destruction by AAA+proteases. Biochim Biophys Acta 1823: 83–91.
36. Dreher, T.W. (2009) Role of tRNA-like structures in controlling plant virus replication. Virus Res 139: 217–229.
37. Dreher, T.W., and Goodwin, J.B. (1998) Transfer RNA mimicry among tymoviral genomic RNAs ranges from highly efficient to vestigial. Nucleic Acids Res 26: 4356–4364.
38. Asp. Proc Natl Acad Sci USA 101: 7530–7535.
39. Durand, J.M., Dagberg, B., Uhlin, B.E., and Björk, G.R. (2000) Transfer RNA modification, temperature and DNA superhelicity have a common target in the regulatory network of the virulence of Shigella flexneri: the expression of the virF gene. Mol Microbiol 35: 924–935.
40. Elde, N.C., Child, S.J., Geballe, A.P., and Malik, H.S. (2009) Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457: 485–489.
41. Elde, N.C., and Malik, H.S. (2009) The evolutionary conundrum of pathogen mimicry. Nat Rev Microbiol 7: 787–797.
42. Elf, J., and Ehrenberg, M. (2005) Near-critical behavior of aminoacyl-tRNA pools in E. coli at rate-limiting supply of amino acids. Biophys J 88: 132–146.
43. Endres, L., Dedon, P.C., and Begley, T.J. (2015) Codon-biased translation can be regulated by wobble-base tRNA modification systems during cellular stress responses. RNA Biol 12: 603–614.
44. Farah, C., Levicán, G., Ibba, M., and Orellana, O. (2014) Effect of hydrogen peroxide on the biosynthesis of heme and proteins: potential implications for the partitioning of Glu-tRNA(Glu) between these pathways. Int J Mol Sci 15: 23011–23023.
45. Fonvielle, M., Chemama, M., Villet, R., Lecerf, M., Bouhss, A., Valéry, J.-M., et al. (2009) Aminoacyl-tRNA recognition by the FemXWv transferase for bacterial cell wall synthesis. Nucleic Acids Res 37: 1589–1601.
46. Fonvielle, M., de La Sierra-Gallay, I., Sagheer, A.H. El-, Lecerf, M., Patin, D., Mellal, D., et al. (2013) The structure of FemX(Wv) in complex with a peptidyl-RNA conjugate: mechanism of aminoacyl transfer from Ala-tRNA(Ala) to peptidoglycan precursors. Angew Chem Int Ed Engl 52: 7278–7281.
47. Francklyn, C.S., and Minajigi, A. (2010) tRNA as an active chemical scaffold for diverse chemical transformations. FEBS Lett 584: 366–375.
48. Fukunaga, R., and Yokoyama, S. (2007) Structural insights into the second step of RNA-dependent cysteine biosynthesis in archaea: crystal structure of Sep-tRNA:Cys-tRNA synthase from Archaeoglobus fulgidus. J Mol Biol 370: 128–141.
49. Leu recognition nucleotides for Escherichia coli L/F transferase. RNA N Y N 20: 1210–1222.
50. Gao, Y.-G., Selmer, M., Dunham, C.M., Weixlbaumer, A., Kelley, A.C., and Ramakrishnan, V. (2009) The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326: 694–699.
51. Garg, R.P., Qian, X.L., Alemany, L.B., Moran, S., and Parry, R.J. (2008) Investigations of valanimycin biosynthesis: elucidation of the role of seryl-tRNA. Proc Natl Acad Sci USA 105: 6543–6547.
52. Giannouli, S., Kyritsis, A., Malissovas, N., Becker, H.D., and Stathopoulos, C. (2009) On the role of an unusual tRNAGly isoacceptor in Staphylococcus aureus. Biochimie 91: 344–351.
53. Giegé, R., and Frugier, M. (2000) Transfer RNA Structure and Identity. In Madame Curie Bioscience Database [Internet]. Landes Bioscience, Austin (TX), USA. [WWW document]. URL http://www.ncbi.nlm.nih.gov/books/NBK6236/.
54. Giudice, E., Macé, K., and Gillet, R. (2014) Trans-translation exposed: understanding the structures and functions of tmRNA-SmpB. Front Microbiol 5: 113.
55. Goldfine, H. (2014) Charge counter charge: bacterial response to antimicrobial cationic peptides and more. Virulence 5: 451–453.
56. Golovina, A.Y., Sergiev, P.V., Golovin, A.V., Serebryakova, M.V., Demina, I., Govorun, V.M., and Dontsova, O.A. (2009) The yfiC gene of E. coli encodes an adenine-N6 methyltransferase that specifically modifies A37 of tRNA1Val(cmo5UAC). RNA N Y N 15: 1134–1141.
57. Gould, R.M., Thornton, M.P., Liepkalns, V., and Lennarz, W.J. (1968) Participation of aminoacyl transfer ribonucleic acid in aminoacyl phosphatidylglycerol synthesis. II. Specificity of alanyl phosphatidylglycerol synthetase. J Biol Chem 243: 3096–3104.
58. Gu, C., Begley, T.J., and Dedon, P.C. (2014) tRNA modifications regulate translation during cellular stress. FEBS Lett 588: 4287–4296.
59. Guan, R., Roychowdhury, A., Ember, B., Kumar, S., Boons, G.-J., and Mariuzza, R.A. (2004) Structural basis for peptidoglycan binding by peptidoglycan recognition proteins. Proc Natl Acad Sci USA 101: 17168–17173.
60. Guillon, J.M., Meinnel, T., Mechulam, Y., Lazennec, C., Blanquet, S., and Fayat, G. (1992) Nucleotides of tRNA governing the specificity of Escherichia coli methionyl-tRNA(fMet) formyltransferase. J Mol Biol 224: 359–367.
61. Hacker, J., and Kaper, J.B. (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54: 641–679.
62. Hanawa-Suetsugu, K., Sekine, S., Sakai, H., Hori-Takemoto, C., Terada, T., Unzai, S., et al. (2004) Crystal structure of elongation factor P from Thermus thermophilus HB8. Proc Natl Acad Sci USA 101: 9595–9600.
63. Hebecker, S., Arendt, W., Heinemann, I.U., Tiefenau, J.H.J., Nimtz, M., Rohde, M., et al. (2011) Alanyl-phosphatidylglycerol synthase: mechanism of substrate recognition during tRNA-dependent lipid modification in Pseudomonas aeruginosa. Mol Microbiol 80: 935–950.
64. Heinemann, I.U., Jahn, M., and Jahn, D. (2008) The biochemistry of heme biosynthesis. Arch Biochem Biophys 474: 238–251.
65. Helgadóttir, S., Sinapah, S., Söll, D., and Ling, J. (2012) Mutational analysis of Sep-tRNA:Cys-tRNA synthase reveals critical residues for tRNA-dependent cysteine formation. FEBS Lett 586: 60–63.
66. Henkin, T.M., and Yanofsky, C. (2002) Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. BioEssays News Rev Mol Cell Dev Biol 24: 700–707.
67. Himeno, H., Kurita, D., and Muto, A. (2014) tmRNA-mediated trans-translation as the major ribosome rescue system in a bacterial cell. Front Genet 5: 66.
68. Hoagland, M.B., Stephenson, M.L., Scott, J.F., Hecht, L.I., and Zamecnik, P.C. (1958) A Soluble Ribonucleic Acid Intermediate in Protein Synthesis. J Biol Chem 231: 241–257.
69. Ibba, M., Becker, H.D., Stathopoulos, C., Tumbula, D.L., and Söll, D. (2000) The adaptor hypothesis revisited. Trends Biochem Sci 25: 311–316.
70. Ibba, M., Francklyn, C., and Cusack, S. (eds) (2005) The aminoacyl-tRNA synthetases. Landes Bioscience: Eurekah.com, Georgetown, TX., USA.
71. Ichihashi, N., Kurokawa, K., Matsuo, M., Kaito, C., and Sekimizu, K. (2003) Inhibitory effects of basic or neutral phospholipid on acidic phospholipid-mediated dissociation of adenine nucleotide bound to DnaA protein, the initiator of chromosomal DNA replication. J Biol Chem 278: 28778–28786.
72. Jahn, D. (1992) Complex formation between glutamyl-tRNA synthetase and glutamyl-tRNA reductase during the tRNA-dependent synthesis of 5-aminolevulinic acid in Chlamydomonas reinhardtii. FEBS Lett 314: 77–80.
73. Karzai, A.W., Susskind, M.M., and Sauer, R.T. (1999) SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA). EMBO J 18: 3793–3799.
74. Katz, A., and Orellana, O. (2012a) Glutamyl-tRNA in Bacteria. Multiple Identities for Multiple Functions. Croat Chem Acta 85: 159–169.
75. Katz, A., and Orellana, O. (2012b) Protein Synthesis and the Stress Response. In Cell-Free Protein Synthesis. Biyani, M. (ed.). InTech, DOI: 10.5772/50311.
76. Katz, A., Solden, L., Zou, S.B., Navarre, W.W., and Ibba, M. (2014) Molecular evolution of protein-RNA mimicry as a mechanism for translational control. Nucleic Acids Res 42: 3261–3271.
77. Kaufmann, G. (2000) Anticodon nucleases. Trends Biochem Sci 25: 70–74.
78. Keam, S.P., and Hutvagner, G. (2015) tRNA-Derived Fragments (tRFs): emerging new roles for an ancient RNA in the regulation of gene expression. Life 5: 1638–1651.
79. Keiler, K.C. (2015) Mechanisms of ribosome rescue in bacteria. Nat Rev Microbiol 13: 285–297.
80. Khade, P., and Joseph, S. (2010) Functional interactions by transfer RNAs in the ribosome. FEBS Lett 584: 420–426.
81. Koskiniemi, S., Lamoureux, J.G., Nikolakakis, K.C., Roodenbeke, C. t'Kint de, Kaplan, M.D., Low, D.A., and Hayes, C.S. (2013) Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci USA 110: 7032–7037.
82. Kramer, G.F., Baker, J.C., and Ames, B.N. (1988) Near-UV stress in Salmonella typhimurium: 4-thiouridine in tRNA, ppGpp, and ApppGpp as components of an adaptive response. J Bacteriol 170: 2344–2351.
83. Ladner, J.E., Jack, A., Robertus, J.D., Brown, R.S., Rhodes, D., Clark, B.F., and Klug, A. (1975) Structure of yeast phenylalanine transfer RNA at 2.5 A resolution. Proc Natl Acad Sci USA 72: 4414–4418.
84. LaRiviere, F.J., Wolfson, A.D., and Uhlenbeck, O.C. (2001) Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science 294: 165–168.
85. Lassak, J., Keilhauer, E.C., Fürst, M., Wuichet, K., Gödeke, J., Starosta, A.L., et al. (2015) Arginine-rhamnosylation as new strategy to activate translation elongation factor P. Nat Chem Biol 11: 266–270.
86. Laxman, S., Sutter, B.M., Wu, X., Kumar, S., Guo, X., Trudgian, D.C., et al. (2013) Sulfur amino acids regulate translational capacity and metabolic homeostasis through modulation of tRNA thiolation. Cell 154: 416–429.
87. Lee, C.P., Seong, B.L., and RajBhandary, U.L. (1991) Structural and sequence elements important for recognition of Escherichia coli formylmethionine tRNA by methionyl-tRNA transformylase are clustered in the acceptor stem. J Biol Chem 266: 18012–18017.
88. Levicán, G., Katz, A., Armas, M. de, Núñez, H., and Orellana, O. (2007) Regulation of a glutamyl-tRNA synthetase by the heme status. Proc Natl Acad Sci USA 104: 3135–3140.
89. Levicán, G., Katz, A., Valenzuela, P., Söll, D., and Orellana, O. (2005) A tRNA(Glu) that uncouples protein and tetrapyrrole biosynthesis. FEBS Lett 579: 6383–6387.
90. Li, S., Kumar, N.V., Varshney, U., and RajBhandary, U.L. (1996) Important role of the amino acid attached to tRNA in formylation and in initiation of protein synthesis in Escherichia coli. J Biol Chem 271: 1022–1028.
91. Liu, K., Bittner, A.N., and Wang, J.D. (2015) Diversity in (p)ppGpp metabolism and effectors. Curr Opin Microbiol 24: 72–79.
92. Mak, J., and Kleiman, L. (1997) Primer tRNAs for reverse transcription. J Virol 71: 8087–8095.
93. Marck, C., and Grosjean, H. (2002) tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. RNA N Y N 8: 1189–1232.
94. Mateus, D.D., Paredes, J.A., Español, Y., Ribas de Pouplana, L., Moura, G.R., and Santos, M.A.S. (2013) Molecular reconstruction of a fungal genetic code alteration. RNA Biol 10: 969–980.
95. Mladenova, S.R., Stein, K.R., Bartlett, L., and Sheppard, K. (2014) Relaxed tRNA specificity of the Staphylococcus aureus aspartyl-tRNA synthetase enables RNA-dependent asparagine biosynthesis. FEBS Lett 588: 1808–1812.
96. Moras, D., Comarmond, M.B., Fischer, J., Weiss, R., Thierry, J.C., Ebel, J.P., and Giegé, R. (1980) Crystal structure of yeast tRNAAsp. Nature 288: 669–674.
97. Morgens, D.W. (2013) The protein invasion: a broad review on the origin of the translational system. J Mol Evol 77: 185–196.
98. Moura, G.R., Paredes, J.A., and Santos, M.A.S. (2010) Development of the genetic code: insights from a fungal codon reassignment. FEBS Lett 584: 334–341.
99. Moutiez, M., Seguin, J., Fonvielle, M., Belin, P., Jacques, I.B., Favry, E., et al. (2014) Specificity determinants for the two tRNA substrates of the cyclodipeptide synthase AlbC from Streptomyces noursei. Nucleic Acids Res 42: 7247–7258.
100. Murata, M., Fujimoto, H., Nishimura, K., Charoensuk, K., Nagamitsu, H., Raina, S., et al. (2011) Molecular strategy for survival at a critical high temperature in Eschierichia coli. PloS One 6: e20063.
101. Nakayashiki, T., Saito, N., Takeuchi, R., Kadokura, H., Nakahigashi, K., Wanner, B.L., and Mori, H. (2013) The tRNA thiolation pathway modulates the intracellular redox state in Escherichia coli. J Bacteriol 195: 2039–2049.
102. Navarre, W.W., Zou, S.B., Roy, H., Xie, J.L., Savchenko, A., Singer, A., et al. (2010) PoxA, yjeK, and elongation factor P coordinately modulate virulence and drug resistance in Salmonella enterica. Mol Cell 39: 209–221.
103. Newton, D.T., Niemkiewicz, M., Lo, R.Y., and Mangroo, D. (1999) Recognition of the initiator tRNA by the Pseudomonas aeruginosa methionyl-tRNA formyltransferase: importance of the base-base mismatch at the end of the acceptor stem. FEMS Microbiol Lett 178: 289–298.
104. O'Brian, M.R., and Thöny-Meyer, L. (2002) Biochemistry, regulation and genomics of haem biosynthesis in prokaryotes. Adv Microb Physiol 46: 257–318.
105. Cys formation. Proc Natl Acad Sci USA 102: 19003–19008.
106. Ogawa, T., Tomita, K., Ueda, T., Watanabe, K., Uozumi, T., and Masaki, H. (1999) A cytotoxic ribonuclease targeting specific transfer RNA anticodons. Science 283: 2097–2100.
107. Palioura, S., Sherrer, R.L., Steitz, T.A., Söll, D., and Simonovic, M. (2009) The human SepSecS-tRNASec complex reveals the mechanism of selenocysteine formation. Science 325: 321–325.
108. Persson, B.C., Ólafsson, Ó., Lundgren, H.K., Hederstedt, L., and Björk, G.R. (1998) The ms2io6A37 modification of tRNA in Salmonella typhimurium regulates growth on citric acid cycle intermediates. J Bacteriol 180: 3144–3151.
109. Raina, M., and Ibba, M. (2014) tRNAs as regulators of biological processes. Front Genet 5: 171.
110. RajBhandary, U.L., and Söll, D. (2008) Aminoacyl-tRNAs, the bacterial cell envelope, and antibiotics. Proc Natl Acad Sci USA 105: 5285–5286.
111. Rajkovic, A., Erickson, S., Witzky, A., Branson, O.E., Seo, J., Gafken, P.R., et al. (2015) Cyclic Rhamnosylated elongation factor P establishes antibiotic resistance in Pseudomonas aeruginosa. mBio 6: e00823.
112. Rampias, T., Sheppard, K., and Söll, D. (2010) The archaeal transamidosome for RNA-dependent glutamine biosynthesis. Nucleic Acids Res 38: 5774–5783.
113. Randau, L., Schauer, S., Ambrogelly, A., Salazar, J.C., Moser, J., Sekine, S., et al. (2004) tRNA recognition by glutamyl-tRNA reductase. J Biol Chem 279: 34931–34937.
114. Richards, J., Sundermeier, T., Svetlanov, A., and Karzai, A.W. (2008) Quality control of bacterial mRNA decoding and decay. Biochim Biophys Acta 1779: 574–582.
115. Rodin, A.S., Szathmáry, E., and Rodin, S.N. (2011) On origin of genetic code and tRNA before translation. Biol Direct 6: 14.
116. Rogers, T.E., Ataide, S.F., Dare, K., Katz, A., Seveau, S., Roy, H., and Ibba, M. (2012) A pseudo-tRNA modulates antibiotic resistance in Bacillus cereus. PloS One 7: e41248.
117. Rosenberg, A.H., and Gefter, M.L. (1969) An iron-dependent modification of several transfer RNA species in Escherichia coli. J Mol Biol 46: 581–584.
118. Roy, H., and Ibba, M. (2008) RNA-dependent lipid remodeling by bacterial multiple peptide resistance factors. Proc Natl Acad Sci USA 105: 4667–4672.
119. Roy, H., Zou, S.B., Bullwinkle, T.J., Wolfe, B.S., Gilreath, M.S., Forsyth, C.J., et al. (2011) The tRNA synthetase paralog PoxA modifies elongation factor-P with (R)-β-lysine. Nat Chem Biol 7: 667–669.
120. Ruhe, Z.C., Low, D.A., and Hayes, C.S. (2013) Bacterial contact-dependent growth inhibition. Trends Microbiol 21: 230–237.
121. Salazar, J.C., Ambrogelly, A., Crain, P.F., McCloskey, J.A., and Söll, D. (2004) A truncated aminoacyl-tRNA synthetase modifies RNA. Proc Natl Acad Sci USA 101: 7536–7541.
122. Samhita, L., Virumäe, K., Remme, J., and Varshney, U. (2013) Initiation with elongator tRNAs. J Bacteriol 195: 4202–4209.
123. Sauerwald, A., Zhu, W., Major, T.A., Roy, H., Palioura, S., Jahn, D., et al. (2005) RNA-dependent cysteine biosynthesis in archaea. Science 307: 1969–1972.
124. Sauguet, L., Moutiez, M., Li, Y., Belin, P., Seguin, J., Du, M.-H. Le, et al. (2011) Cyclodipeptide synthases, a family of class-I aminoacyl-tRNA synthetase-like enzymes involved in non-ribosomal peptide synthesis. Nucleic Acids Res 39: 4475–4489.
125. Scheffers, D.-J., and Pinho, M.G. (2005) Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 69: 585–607.
126. Schimmel, P., Giegé, R., Moras, D., and Yokoyama, S. (1993) An operational RNA code for amino acids and possible relationship to genetic code. Proc Natl Acad Sci USA 90: 8763–8768.
127. Schulze, J.O., Schubert, W.-D., Moser, J., Jahn, D., and Heinz, D.W. (2006) Evolutionary relationship between initial enzymes of tetrapyrrole biosynthesis. J Mol Biol 358: 1212–1220.
128. Shafritz, D.A., and Anderson, W.F. (1970) Isolation and partial characterization of reticulocyte factors M1 and M2. J Biol Chem 245: 5553–5559.
129. Shepherd, J., and Ibba, M. (2013a) Lipid II-independent trans editing of mischarged tRNAs by the penicillin resistance factor MurM. J Biol Chem 288: 25915–25923.
130. Shepherd, J., and Ibba, M. (2013b) Direction of aminoacylated transfer RNAs into antibiotic synthesis and peptidoglycan-mediated antibiotic resistance. FEBS Lett 587: 2895–2904.
131. Shepotinovskaya, I., and Uhlenbeck, O.C. (2013) tRNA residues evolved to promote translational accuracy. RNA N Y N 19: 510–516.
132. Sheppard, K., Yuan, J., Hohn, M.J., Jester, B., Devine, K.M., and Söll, D. (2008) From one amino acid to another: tRNA-dependent amino acid biosynthesis. Nucleic Acids Res 36: 1813–1825.
133. Sherrer, R.L., Ho, J.M.L., and Söll, D. (2008) Divergence of selenocysteine tRNA recognition by archaeal and eukaryotic O-phosphoseryl-tRNASec kinase. Nucleic Acids Res 36: 1871–1880.
134. Shetty, S., Bhattacharyya, S., and Varshney, U. (2015) Is the cellular initiation of translation an exclusive property of the initiator tRNAs? RNA Biol 12: 675–680.
135. Shippy, D.C., and Fadl, A.A. (2014) tRNA Modification enzymes GidA and MnmE: potential role in virulence of bacterial pathogens. Int J Mol Sci 15: 18267–18280.
136. Shoji, S., Walker, S.E., and Fredrick, K. (2009) Ribosomal translocation: one step closer to the molecular mechanism. ACS Chem Biol 4: 93–107.
137. Sørensen, M.A., Elf, J., Bouakaz, E., Tenson, T., Sanyal, S., Björk, G.R., and Ehrenberg, M. (2005) Over expression of a tRNA(Leu) isoacceptor changes charging pattern of leucine tRNAs and reveals new codon reading. J Mol Biol 354: 16–24.
138. Subramaniam, A.R., Deloughery, A., Bradshaw, N., Chen, Y., O'Shea, E., Losick, R., and Chai, Y. (2013a) A serine sensor for multicellularity in a bacterium. eLife 2: e01501.
139. Subramaniam, A.R., Pan, T., and Cluzel, P. (2013b) Environmental perturbations lift the degeneracy of the genetic code to regulate protein levels in bacteria. Proc Natl Acad Sci USA 110: 2419–2424.
140. Subramaniam, A.R., Zid, B.M., and O'Shea, E.K. (2014) An integrated approach reveals regulatory controls on bacterial translation elongation. Cell 159: 1200–1211.
141. Sun, F.-J., and Caetano-Anollés, G. (2008) The origin and evolution of tRNA inferred from phylogenetic analysis of structure. J Mol Evol 66: 21–35.
142. Suto, K., Shimizu, Y., Watanabe, K., Ueda, T., Fukai, S., Nureki, O., and Tomita, K. (2006) Crystal structures of leucyl/phenylalanyl-tRNA-protein transferase and its complex with an aminoacyl-tRNA analog. EMBO J 25: 5942–5950.
143. Takeuchi, N., Vial, L., Panvert, M., Schmitt, E., Watanabe, K., Mechulam, Y., and Blanquet, S. (2001) Recognition of tRNAs by methionyl-tRNA transformylase from mammalian mitochondria. J Biol Chem 276: 20064–20068.
144. Tomita, K., Ogawa, T., Uozumi, T., Watanabe, K., and Masaki, H. (2000) A cytotoxic ribonuclease which specifically cleaves four isoaccepting arginine tRNAs at their anticodon loops. Proc Natl Acad Sci USA 97: 8278–8283.
145. Varshney, U., Lee, C.P., Seong, B.L., and RajBhandary, U.L. (1991) Mutants of initiator tRNA that function both as initiators and elongators. J Biol Chem 266: 18018–18024.
146. Vial, L., Gomez, P., Panvert, M., Schmitt, E., Blanquet, S., and Mechulam, Y. (2003) Mitochondrial methionyl-tRNAfMet formyltransferase from Saccharomyces cerevisiae: gene disruption and tRNA substrate specificity. Biochemistry (Mosc) 42: 932–939.
147. Villet, R., Fonvielle, M., Busca, P., Chemama, M., Maillard, A.P., Hugonnet, J.-E., et al. (2007) Idiosyncratic features in tRNAs participating in bacterial cell wall synthesis. Nucleic Acids Res 35: 6870–6883.
148. Vladar, H.P. de (2012) Amino acid fermentation at the origin of the genetic code. Biol Direct 7: 6.
149. Wagner, A.M., Fegley, M.W., Warner, J.B., Grindley, C.L.J., Marotta, N.P., and Petersson, E.J. (2011) N-terminal protein modification using simple aminoacyl transferase substrates. J Am Chem Soc 133: 15139–15147.
150. Wang, X., and He, C. (2014) Dynamic RNA modifications in posttranscriptional regulation. Mol Cell 56: 5–12.
151. Watanabe, K., Toh, Y., Suto, K., Shimizu, Y., Oka, N., Wada, T., and Tomita, K. (2007) Protein-based peptide-bond formation by aminoacyl-tRNA protein transferase. Nature 449: 867–871.
152. Watanabe, Y.-I., Suematsu, T., and Ohtsuki, T. (2014) Losing the stem-loop structure from metazoan mitochondrial tRNAs and co-evolution of interacting factors. Front Genet 5: 109.
153. Wei, F.-Y., and Tomizawa, K. (2011) Functional loss of Cdkal1, a novel tRNA modification enzyme, causes the development of type 2 diabetes. Endocr J 58: 819–825.
154. Weisblum, B. (1999) Back to Camelot: defining the specific role of tRNA in protein synthesis. Trends Biochem Sci 24: 247–250.
155. Weixlbaumer, A., Petry, S., Dunham, C.M., Selmer, M., Kelley, A.C., and Ramakrishnan, V. (2007) Crystal structure of the ribosome recycling factor bound to the ribosome. Nat Struct Mol Biol 14: 733–737.
156. Wettstein, F.O., and Stent, G.S. (1968) Physiologically induced changes in the property of phenylalanine tRNA in Escherichia coli. J Mol Biol 38: 25–40.
157. Williams, K.P. (2002) Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res 30: 866–875.
158. Winther, K.S., and Gerdes, K. (2011) Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA. Proc Natl Acad Sci USA 108: 7403–7407.
159. Woese, C.R., Olsen, G.J., Ibba, M., and Söll, D. (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol Mol Biol Rev MMBR 64: 202–236.
160. Yuan, J., Sheppard, K., and Söll, D. (2008) Amino acid modifications on tRNA. Acta Biochim Biophys Sin 40: 539–553.
161. Zhang, C.-M., Liu, C., Slater, S., and Hou, Y.-M. (2008) Aminoacylation of tRNA with phosphoserine for synthesis of cysteinyl-tRNA(Cys). Nat Struct Mol Biol 15: 507–514.
162. Zhang, W., Ntai, I., Kelleher, N.L., and Walsh, C.T. (2011) tRNA-dependent peptide bond formation by the transferase PacB in biosynthesis of the pacidamycin group of pentapeptidyl nucleoside antibiotics. Proc Natl Acad Sci USA 108: 12249–12253.
163. Zhou, J., Korostelev, A., Lancaster, L., and Noller, H.F. (2012) Crystal structures of 70S ribosomes bound to release factors RF1, RF2 and RF3. Curr Opin Struct Biol 22: 733–742.
164. Zhou, J., Lancaster, L., Donohue, J.P., and Noller, H.F. (2013) Crystal structures of EF-G-ribosome complexes trapped in intermediate states of translocation. Science 340: 1236086.