The Importance of Being Modified: The Role of RNA Modifications in Translational Fidelity

Enzymes

Volumn 41, Issue , 2017, Pages 1-50

  Agris, Paul F ^a   Narendran, Amithi ^a   Sarachan, Kathryn ^a   Väre, Ville Y P ^a   Eruysal, Emily ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Codon degeneracy and decoding; Human disease and tRNA modifications; Modification chemistry and structure; Modifications 3 adjacent to the anticodon; Modifications prestructure tRNA; Wobble position tRNA modifications

Indexed keywords

TRANSFER RNA;

AMINO ACID SEQUENCE; ANTICODON; CHEMISTRY; CODON; GENETIC CODE; GENETICS; HUMAN; PROTEIN SYNTHESIS; RNA PROCESSING;

AMINO ACID SEQUENCE; ANTICODON; CODON; GENETIC CODE; HUMANS; PROTEIN BIOSYNTHESIS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, TRANSFER;

EID: 85018785543     PISSN: 18746047     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.enz.2017.03.005     Document Type: Chapter

References (180)

1. Liu, Z., Gutierrez-Vargas, C., Wei, J., Grassucci, R.A., Sun, M., Espina, N., Madison-Antenucci, S., Tong, L., Frank, J., Determination of the ribosome structure to a resolution of 2.5 A by single-particle cryo-EM. Protein Sci. 26:1 (2017), 82–92.
2. Zimmerman, E., Yonath, A., Biological implications of the ribosome's stunning stereochemistry. ChemBioChem 10:1 (2009), 63–72.
3. Greber, B.J., Ban, N., Structure and function of the mitochondrial ribosome. Annu. Rev. Biochem. 85 (2016), 103–132.
4. Brocchieri, L., Karlin, S., Protein length in eukaryotic and prokaryotic proteomes. Nucleic Acids Res. 33:10 (2005), 3390–3400.
5. Kurland, C., Hughes, D., Ehrenberg, M., Limitations of translational accuracy. Neidhardt, F.C., Curtis, R. III, Ingraham, J.L., Lin, E.C.C., Low, J.K.B., Magasarák, B., Reznikoff, W.S., Riley, M., Schaachler, M., Umbarger, H.E., (eds.) Escherichia coli and Salmonella: Cellular and Molecular Biology, 1996, ASM Press, Washington, DC, 979–1004.
6. Zaher, H.S., Green, R., Quality control by the ribosome following peptide bond formation. Nature 457:7226 (2009), 161–166.
7. McCulloch, S.D., Kunkel, T.A., The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res. 18:1 (2008), 148–161.
8. Mechali, M., Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 11:10 (2010), 728–738.
9. Kwak, H., Lis, J.T., Control of transcriptional elongation. Annu. Rev. Genet. 47 (2013), 483–508.
10. Maiuri, P., Knezevich, A., De Marco, A., Mazza, D., Kula, A., McNally, J.G., Marcello, A., Fast transcription rates of RNA polymerase II in human cells. EMBO Rep. 12:12 (2011), 1280–1285.
11. Duechler, M., Leszczynska, G., Sochacka, E., Nawrot, B., Nucleoside modifications in the regulation of gene expression: focus on tRNA. Cell. Mol. Life Sci. 73:16 (2016), 3075–3095.
12. Schimmel, P., Giegé, R., Moras, D., Yokoyama, S., An operational RNA code for amino acids and possible relationship to genetic code. Proc. Natl. Acad. Sci. U.S.A. 90:19 (1993), 8763–8768.
13. Agris, P.F., The importance of being modified: an unrealized code to RNA structure and function. RNA 21:4 (2015), 552–554.
14. Cantara, W.A., Crain, P.F., Rozenski, J., McCloskey, J.A., Harris, K.A., Zhang, X., Vendeix, F.A., Fabris, D., Agris, P.F., The RNA modification database, RNAMDB: 2011 update. Nucleic Acids Res. 39 (2011), D195–D201 (Database issue).
15. Machnicka, M.A., Milanowska, K., Osman Oglou, O., Purta, E., Kurkowska, M., Olchowik, A., Januszewski, W., Kalinowski, S., Dunin-Horkawicz, S., Rother, K.M., et al. MODOMICS: a database of RNA modification pathways—2013 update. Nucleic Acids Res. 41 (2013), D262–D267 (Database issue).
16. Saletore, Y., Meyer, K., Korlach, J., Vilfan, I.D., Jaffrey, S., Mason, C.E., The birth of the Epitranscriptome: deciphering the function of RNA modifications. Genome Biol., 13(10), 2012, 175.
17. Gilbert, W.V., Bell, T.A., Schaening, C., Messenger RNA modifications: form, distribution, and function. Science 352:6292 (2016), 1408–1412.
18. Delatte, B., Wang, F., Ngoc, L.V., Collignon, E., Bonvin, E., Deplus, R., Calonne, E., Hassabi, B., Putmans, P., Awe, S., et al. Transcriptome-wide distribution and function of RNA hydroxymethylcytosine. Science 351:6270 (2016), 282–285.
19. 6A mRNA methylation facilitates resolution of naïve pluripotency toward differentiation. Science 347:6225 (2015), 1002–1006.
20. Maity, A., Das, B., N6-methyladenosine modification in mRNA: machinery, function and implications for health and diseases. FEBS J. 283:9 (2016), 1607–1630.
21. Zhao, B.S., He, C., Pseudouridine in a new era of RNA modifications. Cell Res. 25:2 (2015), 153–154.
22. 6-methyladenosine in mRNA disrupts tRNA selection and translation-elongation dynamics. Nat. Struct. Mol. Biol. 23:2 (2016), 110–115.
23. Rottman, F., Shatkin, A.J., Perry, R.P., Sequences containing methylated nucleotides at the 5′ termini of messenger RNAs: possible implications for processing. Cell 3:3 (1974), 197–199.
24. 6A RNA modification. Open Biol., 6(4), 2016, 160003.
25. 6A RNA modification controls cell fate transition in mammalian embryonic stem cells. Cell Stem Cell 15:6 (2014), 707–719.
26. 6A editing of HIV-1 mRNAs enhances viral gene expression. Cell Host Microbe 19:5 (2016), 675–685.
27. Schwartz, S., Cracking the epitranscriptome. RNA 22:2 (2016), 169–174.
28. 6A mRNA methylation directs translational control of heat shock response. Nature 526:7574 (2015), 591–594.
29. Agris, P.F., Decoding the genome: a modified view. Nucleic Acids Res. 32:1 (2004), 223–238.
30. Agris, P.F., Vendeix, F.A., Graham, W.D., tRNA's wobble decoding of the genome: 40 years of modification. J. Mol. Biol. 366:1 (2007), 1–13.
31. Gustilo, E.M., Vendeix, F.A., Agris, P.F., tRNA's modifications bring order to gene expression. Curr. Opin. Microbiol. 11:2 (2008), 134–140.
32. Ranjan, N., Rodnina, M.V., tRNA wobble modifications and protein homeostasis. Translation, 4(1), 2016, e1143076.
33. Wang, R., Luo, Z., He, K., Delaney, M.O., Chen, D., Sheng, J., Base pairing and structural insights into the 5-formylcytosine in RNA duplex. Nucleic Acids Res. 44:10 (2016), 4968–4977.
34. Jackman, J.E., Alfonzo, J.D., Transfer RNA modifications: nature's combinatorial chemistry playground. Wiley Interdiscip. Rev. RNA 4:1 (2013), 35–48.
35. Machnicka, M.A., Olchowik, A., Grosjean, H., Bujnicki, J.M., Distribution and frequencies of post-transcriptional modifications in tRNAs. RNA Biol. 11:12 (2014), 1619–1629.
36. 2 + in RNA structure and function. Prog. Nucleic Acid Res. Mol. Biol. 53 (1996), 79–129.
37. Chapeville, F., Lipmann, F., Ehrenstein, G.V., Weisblum, B., Ray, W.J., Benzer, S., On the role of soluble ribonucleic acid in coding for amino acids. Proc. Natl. Acad. Sci. U.S.A. 48:6 (1962), 1086–1092.
38. Effraim, P.R., Wang, J., Englander, M.T., Avins, J., Leyh, T.S., Gonzalez, R.L. Jr., Cornish, V.W., Natural amino acids do not require their native tRNAs for efficient selection by the ribosome. Nat. Chem. Biol. 5:12 (2009), 947–953.
39. Capecchi, M.R., Gussin, G.N., Suppression in vitro: identification of a serine-sRNA as a “nonsense” suppressor. Science 149:3682 (1965), 417–422.
40. Engelhardt, D.L., Webster, R.E., Wilhelm, R.C., Zinder, N., In vitro studies on the mechanism of suppression of a nonsense mutation. Proc. Natl. Acad. Sci. U.S.A. 54:6 (1965), 1791–1797.
41. Ambrogelly, A., Palioura, S., Soll, D., Natural expansion of the genetic code. Nat. Chem. Biol. 3:1 (2007), 29–35.
42. Wright, T.H., Vallee, M.R., Davis, B.G., From chemical mutagenesis to post-expression mutagenesis: a 50 year odyssey. Angew. Chem. Int. Ed. Engl. 55:20 (2016), 5896–5903.
43. Crick, F.H., Codon–anticodon pairing: the wobble hypothesis. J. Mol. Biol. 19:2 (1966), 548–555.
44. Nasvall, S.J., Chen, P., Bjork, G.R., The wobble hypothesis revisited: uridine-5-oxyacetic acid is critical for reading of G-ending codons. RNA 13:12 (2007), 2151–2164.
45. Vendeix, F.A., Dziergowska, A., Gustilo, E.M., Graham, W.D., Sproat, B., Malkiewicz, A., Agris, P.F., Anticodon domain modifications contribute order to tRNA for ribosome-mediated codon binding. Biochemistry 47:23 (2008), 6117–6129.
46. Weixlbaumer, A., Murphy, F.V.T., Dziergowska, A., Malkiewicz, A., Vendeix, F.A., Agris, P.F., Ramakrishnan, V., Mechanism for expanding the decoding capacity of transfer RNAs by modification of uridines. Nat. Struct. Mol. Biol. 14:6 (2007), 498–502.
47. Anderson, S., Bankier, A.T., Barrell, B.G., de Bruijn, M.H., Coulson, A.R., Drouin, J., Eperon, I.C., Nierlich, D.P., Roe, B.A., Sanger, F., et al. Sequence and organization of the human mitochondrial genome. Nature 290:5806 (1981), 457–465.
48. Attardi, G., Animal mitochondrial DNA: an extreme example of genetic economy. Int. Rev. Cytol. 93 (1985), 93–145.
49. Anderson, S., de Bruijn, M.H., Coulson, A.R., Eperon, I.C., Sanger, F., Young, I.G., Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J. Mol. Biol. 156:4 (1982), 683–717.
50. Jones, C.N., Wilkinson, K.A., Hung, K.T., Weeks, K.M., Spremulli, L.L., Lack of secondary structure characterizes the 5′ ends of mammalian mitochondrial mRNAs. RNA 14:5 (2008), 862–871.
51. Nakamura, Y., Gojobori, T., Ikemura, T., Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res., 28(1), 2000, 292.
52. Bjork, G.R., Genetic dissection of synthesis and function of modified nucleosides in bacterial transfer RNA. Prog. Nucleic Acid Res. Mol. Biol. 50 (1995), 263–338.
53. Moriya, J., Yokogawa, T., Wakita, K., Ueda, T., Nishikawa, K., Crain, P.F., Hashizume, T., Pomerantz, S.C., McCloskey, J.A., Kawai, G., et al. A novel modified nucleoside found at the first position of the anticodon of methionine tRNA from bovine liver mitochondria. Biochemistry 33:8 (1994), 2234–2239.
54. Sinha, A., Kohrer, C., Weber, M.H., Masuda, I., Mootha, V.K., Hou, Y.M., RajBhandary, U.L., Biochemical characterization of pathogenic mutations in human mitochondrial methionyl-tRNA formyltransferase. J. Biol. Chem. 289:47 (2014), 32729–32741.
55. Met wobble cytosine in a patient carrying mutations in NSUN3. Nat. Commun., 7, 2016, 12039.
56. Takeuchi, N., Kawakami, M., Omori, A., Ueda, T., Spremulli, L.L., Watanabe, K., Mammalian mitochondrial methionyl-tRNA transformylase from bovine liver. Purification, characterization, and gene structure. J. Biol. Chem. 273:24 (1998), 15085–15090.
57. Takeuchi, N., Vial, L., Panvert, M., Schmitt, E., Watanabe, K., Mechulam, Y., Blanquet, S., Recognition of tRNAs by methionyl-tRNA transformylase from mammalian mitochondria. J. Biol. Chem. 276:23 (2001), 20064–20068.
58. Met results in tRNA misfolding leading to defects in translational initiation and elongation. J. Biol. Chem. 283:49 (2008), 34445–34456.
59. Met: structure/function relationship of a unique modification in the decoding of unconventional codons. J. Mol. Biol. 406:2 (2011), 257–274.
60. Astrom, S.U., Bystrom, A.S., Rit1, a tRNA backbone-modifying enzyme that mediates initiator and elongator tRNA discrimination. Cell 79:3 (1994), 535–546.
61. Suzuki, T., Nagao, A., Suzuki, T., Human mitochondrial tRNAs: biogenesis, function, structural aspects, and diseases. Annu. Rev. Genet. 45 (2011), 299–329.
62. 5CAU as revealed with a mitochondrial in vitro translation system. Nucleic Acids Res. 37:5 (2009), 1616–1627.
63. Met to decode AUG and AUA codons. Biochimie 77:1–2 (1995), 104–108.
64. Met possibly recognizing both AUG and AUA codons. Nucleic Acids Symp. Ser. 42 (1999), 77–78.
65. MetCAU. Nucleic Acids Symp. Ser. 37 (1997), 197–198.
66. Tomita, K., Ueda, T., Ishiwa, S., Crain, P.F., McCloskey, J.A., Watanabe, K., Codon reading patterns in Drosophila melanogaster mitochondria based on their tRNA sequences: a unique wobble rule in animal mitochondria. Nucleic Acids Res. 27:21 (1999), 4291–4297.
67. Watanabe, Y., Tsurui, H., Ueda, T., Furushima, R., Takamiya, S., Kita, K., Nishikawa, K., Watanabe, K., Primary and higher order structures of nematode (Ascaris suum) mitochondrial tRNAs lacking either the T or D stem. J. Biol. Chem. 269:36 (1994), 22902–22906.
68. Met. Nucleic Acids Res. 36:20 (2008), 6548–6557.
69. Lancaster, L., Noller, H.F., Involvement of 16S rRNA nucleotides G1338 and A1339 in discrimination of initiator tRNA. Mol. Cell 20:4 (2005), 623–632.
70. Cantara, W.A., Murphy, F.V.T., Demirci, H., Agris, P.F., Expanded use of sense codons is regulated by modified cytidines in tRNA. Proc. Natl. Acad. Sci. U.S.A. 110:27 (2013), 10964–10969.
71. 4-acetylcytidine. Biochim. Biophys. Acta 262:2 (1972), 209–213.
72. Muramatsu, T., Yokoyama, S., Horie, N., Matsuda, A., Ueda, T., Yamaizumi, Z., Kuchino, Y., Nishimura, S., Miyazawa, T., A novel lysine-substituted nucleoside in the first position of the anticodon of minor isoleucine tRNA from Escherichia coli. J. Biol. Chem. 263:19 (1988), 9261–9267.
73. Ile, base pairs with adenosine but not with guanosine. Proc. Natl. Acad. Sci. U.S.A. 107:7 (2010), 2872–2877.
74. Voorhees, R.M., Mandal, D., Neubauer, C., Kohrer, C., RajBhandary, U.L., Ramakrishnan, V., The structural basis for specific decoding of AUA by isoleucine tRNA on the ribosome. Nat. Struct. Mol. Biol. 20:5 (2013), 641–643.
75. Met. Nat. Chem. Biol. 12:7 (2016), 546–551.
76. El Yacoubi, B., Lyons, B., Cruz, Y., Reddy, R., Nordin, B., Agnelli, F., Williamson, J.R., Schimmel, P., Swairjo, M.A., de Crecy-Lagard, V., The universal YrdC/Sua5 family is required for the formation of threonylcarbamoyladenosine in tRNA. Nucleic Acids Res. 37:9 (2009), 2894–2909.
77. Juhling, F., Morl, M., Hartmann, R.K., Sprinzl, M., Stadler, P.F., Putz, J., tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res. 37 (2009), D159–D162 (Database issue).
78. Lott, M.T., Leipzig, J.N., Derbeneva, O., Xie, H.M., Chalkia, D., Sarmady, M., Procaccio, V., Wallace, D.C., mtDNA variation and analysis using Mitomap and Mitomaster. Curr. Protoc. Bioinformatics, 44, 2013 1.23.21–26.
79. Alston, C.L., Rocha, M.C., Lax, N.Z., Turnbull, D.M., Taylor, R.W., The genetics and pathology of mitochondrial disease. J. Pathol., 2016.
80. de Almeida, R.A., Fraczek, M.G., Parker, S., Delneri, D., O'Keefe, R.T., Non-coding RNAs and disease: the classical ncRNAs make a comeback. Biochem. Soc. Trans. 44:4 (2016), 1073–1078.
81. Met gene mutation in a patient with dystrophic muscle and exercise intolerance. Neurology 50:6 (1998), 1875–1878.
82. Met may modulate the phenotypic expression of the LHON-associated ND4 G11778A mutation. Invest. Ophthalmol. Vis. Sci. 47:2 (2006), 475–483.
83. Lombes, A., Bories, D., Girodon, E., Frachon, P., Ngo, M.M., Breton-Gorius, J., Tulliez, M., Goossens, M., The first pathogenic mitochondrial methionine tRNA point mutation is discovered in splenic lymphoma. Hum. Mutat. 11:Suppl 1 (1998), S175–S183.
84. Grosjean, H., Westhof, E., An integrated, structure- and energy-based view of the genetic code. Nucleic Acids Res. 44:17 (2016), 8020–8040.
85. Suzuki, T.S., Wada, T., Saigo, T., Watanabe, K., Kimitsuna, W., Taurine as a constituent of mitochondrial tRNAs: new insights into the functions of taurine and human mitochondrial diseases. EMBO J. 21:23 (2002), 6581–6589.
86. Saxena, R., Voight, B.F., Lyssenko, V., Burtt, N.P., de Bakker, P.I., Chen, H., Roix, J.J., Kathiresan, S., Hirschhorn, J.N., Daly, M.J., et al. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316:5829 (2007), 1331–1336.
87. Steinthorsdottir, V., Thorleifsson, G., Reynisdottir, I., Benediktsson, R., Jonsdottir, T., Walters, G.B., Styrkarsdottir, U., Gretarsdottir, S., Emilsson, V., Ghosh, S., et al. A variant in CDKAL1 influences insulin response and risk of type 2 diabetes. Nat. Genet. 39:6 (2007), 770–775.
88. LysUUU. Nat. Struct. Mol. Biol. 11:12 (2004), 1186–1191.
89. Val are important for translocation. J. Mol. Biol. 338:3 (2004), 439–444.
90. 6A. Biochemistry 39:44 (2000), 13396–13404.
91. Mallick, B., Chakrabarti, J., Sahoo, S., Ghosh, Z., Das, S., Identity elements of archaeal tRNA. DNA Res. 12:4 (2005), 235–246.
92. Björk, G.R., Chapter 11: Biosynthesis and function of modified nucleosides. Söll, D., RajBhandary, U., (eds.) tRNA: Structure, Biosynthesis, and Function, 1995, American Society for Microbiology, Washington, DC, 165–205.
93. Raba, M., Limburg, K., Burghagen, M., Katze, J.R., Simsek, M., Heckman, J.E., Rajbhandary, U.L., Gross, H.J., Nucleotide sequence of three isoaccepting lysine tRNAs from rabbit liver and SV40-transformed mouse fibroblasts. Eur. J. Biochem. 97:1 (1979), 305–318.
94. Agris, P.F., Wobble position modified nucleosides evolved to select transfer RNA codon recognition: a modified-wobble hypothesis. Biochimie 73 (1991), 1345–1349.
95. Nakai, Y., Umeda, N., Suzuki, T., Nakai, M., Hayashi, H., Watanabe, K., Kagamiyama, H., Yeast Nfs1p is involved in thio-modification of both mitochondrial and cytoplasmic tRNAs. J. Biol. Chem. 279:13 (2004), 12363–12368.
96. Suzuki, T., Suzuki, T., A complete landscape of post-transcriptional modifications in mammalian mitochondrial tRNAs. Nucleic Acids Res. 42 (2014), 7346–7357.
97. Ostrov, N., Landon, M., Guell, M., Kuznetsov, G., Teramoto, J., Cervantes, N., Zhou, M., Singh, K., Napolitano, M.G., Moosburner, M., et al. Design, synthesis, and testing toward a 57-codon genome. Science 353:6301 (2016), 819–822.
98. Bezerra, A.R., Guimaraes, A.R., Santos, M.A., Non-standard genetic codes define new concepts for protein engineering. Life (Basel) 5:4 (2015), 1610–1628.
99. Lys with hypomodified derivatives of 5-methylaminomethyl-2-thiouridine in the wobble position. J. Mol. Biol. 284:1 (1998), 33–42.
100. Lys(UUU) gene contains a 2.5-kilobase-pair intron: an open reading frame and a conserved boundary sequence in the intron. Proc. Natl. Acad. Sci. U.S.A. 82:11 (1985), 3557–3561.
101. Fuller, W., Hodgson, A., Conformation of the anticodon loop in tRNA. Nature 215:5103 (1967), 817–821.
102. Kurata, S., Weixlbaumer, A., Ohtsuki, T., Shimazaki, T., Wada, T., Kirino, Y., Takai, K., Watanabe, K., Ramakrishnan, V., Suzuki, T., Modified uridines with C5-methylene substituents at the first position of the tRNA anticodon stabilize U.G wobble pairing during decoding. J. Biol. Chem. 283:27 (2008), 18801–18811.
103. Watanabe, K., Yokobori, S., tRNA modification and genetic code variations in animal mitochondria. J. Nucleic Acids, 2011, 2011, 623095.
104. Lys. Struct. Chem. 27:3 (2016), 839–854.
105. Agris, P.F., Sierzputowska-Gracz, H., Smith, W., Malkiewicz, A., Sochacka, E., Nawrot, B., Thiolation of uridine carbon-2 restricts the motional dynamics of the transfer RNA wobble position nucleoside. J. Am. Chem. Soc. 114:7 (1992), 2652–2656.
106. 2U) in lysyl-tRNA is required for viability in yeast. RNA 13:8 (2007), 1245–1255.
107. Nedialkova, D.D., Leidel, S.A., Optimization of codon translation rates via tRNA modifications maintains proteome integrity. Cell 161:7 (2015), 1606–1618.
108. Manickam, N., Joshi, K., Bhatt, M.J., Farabaugh, P.J., Effects of tRNA modification on translational accuracy depend on intrinsic codon-anticodon strength. Nucleic Acids Res. 44:4 (2016), 1871–1881.
109. Rozov, A., Demeshkina, N., Khusainov, I., Westhof, E., Yusupov, M., Yusupova, G., Novel base-pairing interactions at the tRNA wobble position crucial for accurate reading of the genetic code. Nat. Commun., 7, 2016, 10457.
110. 6A. Biochemistry 44:22 (2005), 8078–8089.
111. Lys3UUU is pre-structured by natural modifications for cognate and wobble codon binding through keto-enol tautomerism. J. Mol. Biol. 416:4 (2012), 467–485.
112. Johansson, M.J., Esberg, A., Huang, B., Bjork, G.R., Bystrom, A.S., Eukaryotic wobble uridine modifications promote a functionally redundant decoding system. Mol. Cell. Biol. 28:10 (2008), 3301–3312.
113. Serra, M.J., Turner, D.H., Predicting thermodynamic properties of RNA. Methods Enzymol. 259 (1995), 242–261.
114. Rodriguez-Hernandez, A., Spears, J.L., Gaston, K.W., Limbach, P.A., Gamper, H., Hou, Y.M., Kaiser, R., Agris, P.F., Perona, J.J., Structural and mechanistic basis for enhanced translational efficiency by 2-thiouridine at the tRNA anticodon wobble position. J. Mol. Biol. 425:20 (2013), 3888–3906.
115. Numata, T., Ikeuchi, Y., Fukai, S., Suzuki, T., Nureki, O., Snapshots of tRNA sulphuration via an adenylated intermediate. Nature 442:7101 (2006), 419–424.
116. 2U:U base pairs. J. Am. Chem. Soc. 136:39 (2014), 13916–13924.
117. Ashraf, S.S., Ansari, G., Guenther, R., Sochacka, E., Malkiewicz, A., Agris, P.F., The uridine in “U-turn”: contributions to tRNA-ribosomal binding. RNA 5:4 (1999), 503–511.
118. Jacobson, G.N., Clark, P.L., Quality over quantity: optimizing co-translational protein folding with non-‘optimal’ synonymous codons. Curr. Opin. Struct. Biol. 38 (2016), 102–110.
119. Quax, T.E., Claassens, N.J., Soll, D., van der Oost, J., Codon bias as a means to fine-tune gene expression. Mol. Cell 59:2 (2015), 149–161.
120. Supek, F., The code of silence: widespread associations between synonymous codon biases and gene function. J. Mol. Evol. 82:1 (2016), 65–73.
121. Begley, U., Dyavaiah, M., Patil, A., Rooney, J.P., DiRenzo, D., Young, C.M., Conklin, D.S., Zitomer, R.S., Begley, T.J., Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol. Cell 28:5 (2007), 860–870.
122. Chan, C.T., Deng, W., Li, F., DeMott, M.S., Babu, I.R., Begley, T.J., Dedon, P.C., Highly predictive reprogramming of tRNA modifications is linked to selective expression of codon-biased genes. Chem. Res. Toxicol. 28:5 (2015), 978–988.
123. Chan, C.T., Pang, Y.L., Deng, W., Babu, I.R., Dyavaiah, M., Begley, T.J., Dedon, P.C., Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat. Commun., 3, 2012, 937.
124. Endres, L., Dedon, P.C., Begley, T.J., Codon-biased translation can be regulated by wobble-base tRNA modification systems during cellular stress responses. RNA Biol. 12:6 (2015), 603–614.
125. Katz, M.J., Gandara, L., De Lella Ezcurra, A.L., Wappner, P., Hydroxylation and translational adaptation to stress: some answers lie beyond the STOP codon. Cell. Mol. Life Sci. 73:9 (2016), 1881–1893.
126. LysUUU by elongator is essential for efficient translation of stress mRNAs. PLoS Genet., 9(7), 2013, e1003647.
127. Anton, B.P., Russell, S.P., Vertrees, J., Kasif, S., Raleigh, E.A., Limbach, P.A., Roberts, R.J., Functional characterization of the YmcB and YqeV tRNA methylthiotransferases of Bacillus subtilis. Nucleic Acids Res. 38:18 (2010), 6195–6205.
128. Harris, K.A., Bobay, B.G., Sarachan, K.L., Sims, A.F., Bilbille, Y., Deutsch, C., Iwata-Reuyl, D., Agris, P.F., NMR-based structural analysis of threonylcarbamoyl-AMP synthase and its substrate interactions. J. Biol. Chem. 290:33 (2015), 20032–20043.
129. 6A), a universal tRNA modification, in bacteria. Mol. Microbiol. 98:6 (2015), 1199–1221.
130. 6A in yeast. Microb. Cell 3:1 (2016), 29–45.
131. 6A). Bioorg. Med. Chem. Lett. 24:12 (2014), 2703–2706.
132. Yarian, C., Marszalek, M., Sochacka, E., Malkiewicz, A., Guenther, R., Miskiewicz, A., Agris, P.F., Modified nucleoside dependent Watson-Crick and wobble codon binding by tRNALysUUU species. Biochemistry 39:44 (2000), 13390–13395.
133. 6-threonylcarbamoyladenosine as a widely distributed tRNA hypermodification. Nat. Chem. Biol. 9:2 (2013), 105–111.
134. Lys modification by Cdkal1 causes the development of type 2 diabetes in mice. J. Clin. Invest. 121:9 (2011), 3598–3608.
135. Xu, Y., MacKerell, A.D. Jr., Nilsson, L., Structural effects of modified ribonucleotides and magnesium in transfer RNAs. Bioorg. Med. Chem. 24:20 (2016), 4826–4834.
136. Lys3UUU anticodon domain by HIV's nucleocapsid protein and a peptide mimic. J. Mol. Biol. 410:4 (2011), 698–715.
137. Spears, J.L., Xiao, X., Hall, C.K., Agris, P.F., Amino acid signature enables proteins to recognize modified tRNA. Biochemistry 53:7 (2014), 1125–1133.
138. Sprinzl, M., Vassilenko, K.S., Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 33:Database issue (2005), D139–D140.
139. Ishikura, H., Yamada, Y., Nishimura, S., Structure of serine tRNA from Escherichia coli. I. Purification of serine tRNA's with different codon responses. Biochim. Biophys. Acta 228:2 (1971), 471–481.
140. Mitra, S.K., Lustig, F., Akesson, B., Axberg, T., Elias, P., Lagerkvist, U., Relative efficiency of anticodons in reading the valine codons during protein synthesis in vitro. J. Biol. Chem. 254:14 (1979), 6397–6401.
141. Leu isoacceptor changes charging pattern of leucine tRNAs and reveals new codon reading. J. Mol. Biol. 354:1 (2005), 16–24.
142. Yokoyama, S., Watanabe, T., Murao, K., Ishikura, H., Yamaizumi, Z., Nishimura, S., Miyazawa, T., Molecular mechanism of codon recognition by tRNA species with modified uridine in the first position of the anticodon. Proc. Natl. Acad. Sci. U.S.A. 82 (1985), 4905–4909.
143. Procmo5UGG promotes reading of all four proline codons in vivo. RNA 10:10 (2004), 1662–1673.
144. Ala with modified uridine in the wobble position. Mol. Cell 25:1 (2007), 167–174.
145. Kimura, S., Suzuki, T., Iron-sulfur proteins responsible for RNA modifications. Biochim. Biophys. Acta 1853:6 (2015), 1272–1283.
146. Huang, B., Johansson, M.J., Bystrom, A.S., An early step in wobble uridine tRNA modification requires the Elongator complex. RNA 11:4 (2005), 424–436.
147. Esberg, A., Huang, B., Johansson, M.J., Bystrom, A.S., Elevated levels of two tRNA species bypass the requirement for elongator complex in transcription and exocytosis. Mol. Cell 24:1 (2006), 139–148.
148. Chen, C., Tuck, S., Bystrom, A.S., Defects in tRNA modification associated with neurological and developmental dysfunctions in Caenorhabditis elegans elongator mutants. PLoS Genet., 5(7), 2009, e1000561.
149. Phe. J. Mol. Biol. 319:5 (2002), 1015–1034.
150. Yarian, C., Townsend, H., Czestkowski, W., Sochacka, E., Malkiewicz, A.J., Guenther, R., Miskiewicz, A., Agris, P.F., Accurate translation of the genetic code depends on tRNA modified nucleosides. J. Biol. Chem. 277:19 (2002), 16391–16395.
151. Soll, D., Cherayil, J.D., Bock, R.M., Studies on polynucleotides. LXXV. Specificity of tRNA for codon recognition as studied by the ribosomal binding technique. J. Mol. Biol. 29:1 (1967), 97–112.
152. Soll, D., RajBhandary, U.L., Studies on polynucleotides. LXXVI. Specificity of transfer RNA for codon recognition as studied by amino acid incorporation. J. Mol. Biol. 29:1 (1967), 113–124.
153. Ikemura, T., Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 2:1 (1985), 13–34.
154. Wada, K., Wada, Y., Ishibashi, F., Gojobori, T., Ikemura, T., Codon usage tabulated from the GenBank genetic sequence data. Nucleic Acids Res. 20:Suppl (1992), 2111–2118.
155. Maloy, S.R., Stewart, V.J., Taylor, R.K., Genetic Analysis of Pathogenic Bacteria: A Laboratory Manual. 1996, Cold Spring Harbor Laboratory Press, Plainville, NY.
156. Martinis, S.A., Plateau, P., Cavarelli, J., Florentz, C., Aminoacyl-tRNA synthetases: a new image for a classical family. Biochimie 81:7 (1999), 683–700.
157. Auffinger, P., Westhof, E., Singly and bifurcated hydrogen-bonded base-pairs in tRNA anticodon hairpins and ribozymes. J. Mol. Biol. 292:3 (1999), 467–483.
158. Asp. Biophys. J. 76:1 Pt. 1 (1999), 50–64.
159. Delagoutte, B., Moras, D., Cavarelli, J., tRNA aminoacylation by arginyl-tRNA synthetase: induced conformations during substrates binding. EMBO J. 19:21 (2000), 5599–5610.
160. Murphy, F.V.T., Ramakrishnan, V., Structure of a purine-purine wobble base pair in the decoding center of the ribosome. Nat. Struct. Mol. Biol. 11:12 (2004), 1251–1252.
161. ArgII of E. coli B. Nucleic Acids Res. 2:10 (1975), 1787–1792.
162. Murao, K., Tanabe, T., Ishii, F., Namiki, M., Nishimura, S., Primary sequence of arginine transfer RNA from Escherichia coli. Biochem. Biophys. Res. Commun. 47:6 (1972), 1332–1337.
163. Sissler, M., Giege, R., Florentz, C., Arginine aminoacylation identity is context-dependent and ensured by alternate recognition sets in the anticodon loop of accepting tRNA transcripts. EMBO J. 15:18 (1996), 5069–5076.
164. Lys identity elements. Nucleic Acids Res. 20:9 (1992), 2335–2339.
165. Jager, G., Leipuviene, R., Pollard, M.G., Qian, Q., Bjork, G.R., The conserved Cys-X1-X2-Cys motif present in the TtcA protein is required for the thiolation of cytidine in position 32 of tRNA from Salmonella enterica serovar Typhimurium. J. Bacteriol. 186:3 (2004), 750–757.
166. Arg1,2. J. Mol. Biol. 416:4 (2012), 579–597.
167. Cheong, C., Varani, G., Tinoco, I. Jr., Solution structure of an unusually stable RNA hairpin, 5'GGAC(UUCG)GUCC. Nature 346:6285 (1990), 680–682.
168. Moore, P.B., Structural motifs in RNA. Annu. Rev. Biochem. 68 (1999), 287–300.
169. Sauge-Merle, S., Falconet, D., Fontecave, M., An active ribonucleotide reductase from Arabidopsis thaliana. Eur. J. Biochem. 266:1 (1999), 62–69.
170. Soll, D., Jones, D.S., Ohtsuka, E., Faulkner, R.D., Lohrmann, R., Hayatsu, H., Khorana, H.G., Specificity of sRNA for recognition of codons as studied by the ribosomal binding technique. J. Mol. Biol. 19:2 (1966), 556–573.
171. Phe in ribosomal binding. Cell Biochem. Biophys. 33:3 (2000), 241–252.
172. Phe. J. Mol. Biol. 334:5 (2003), 901–918.
173. Lowe, T.M., Eddy, S.R., tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:5 (1997), 955–964.
174. Garcia, G.M., Mar, P.K., Mullin, D.A., Walker, J.R., Prather, N.E., The E. coli dnaY gene encodes an arginine transfer RNA. Cell 45:3 (1986), 453–459.
175. Arg. Nucleic Acids Res. 18:17 (1990), 5031–5036.
176. Ramakrishnan, V., The ribosome emerges from a black box. Cell 159:5 (2014), 979–984.
177. Steitz, T.A., A structural understanding of the dynamic ribosome machine. Nat. Rev. Mol. Cell Biol. 9:3 (2008), 242–253.
178. Thompson, K.M., Gottesman, S., The MiaA tRNA modification enzyme is necessary for robust RpoS expression in Escherichia coli. J. Bacteriol. 196:4 (2014), 754–761.
179. 6A37 tRNA modification is essential for proper decoding of UUX-Leucine codons during rpoS and iraP translation. RNA 22:5 (2016), 729–742.
180. Dunn, D.B., The occurrence of 1-methyladenine in ribonucleic acid. Biochim. Biophys. Acta 46 (1961), 198–200.