A Platform for Discovery and Quantification of Modified Ribonucleosides in RNA: Application to Stress-Induced Reprogramming of tRNA Modifications

Methods in Enzymology

Volumn 560, Issue , 2015, Pages 29-71

  Cai, Weiling Maggie ^a,b   Chionh, Yok Hian ^a,b   Hia, Fabian ^b   Gu, Chen ^c   Kellner, Stefanie ^c   McBee, Megan E ^b,c   Ng, Chee Sheng ^b,d   Pang, Yan Ling Joy ^c   Prestwich, Erin G ^c,g   Lim, Kok Seong ^c,h   Ramesh Babu, I ^c,i   Begley, Thomas J ^e   Dedon, Peter C ^b,c,f  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^c USA   (United States)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e SUNY POLYTECHNIC INSTITUTE   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^g Clark and Elbing LLP   (United States)

^h TechAtlas   (United States)

ⁱ Alnylum Pharmaceuticals   (United States)

Author keywords

Mass spectrometry; Stress response; Systems biology; Translation; tRNA modifications

Indexed keywords

OLIGONUCLEOTIDE; RIBONUCLEASE; RIBONUCLEOSIDE; RNA; TRANSFER RNA; UNTRANSLATED RNA;

ARTICLE; CELL STRESS; CELLULAR STRESS RESPONSE; GENE MAPPING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HYDROLYSIS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN ANALYSIS; QUANTITATIVE ANALYSIS; RNA FINGERPRINTING; RNA ISOLATION; RNA PURIFICATION; RNA SEQUENCE; WORKFLOW; CHEMISTRY; GENETICS; PROCEDURES; PROTEIN SYNTHESIS; RNA PROCESSING;

MASS SPECTROMETRY; PROTEIN BIOSYNTHESIS; RIBONUCLEOSIDES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, TRANSFER;

EID: 84938969156     PISSN: 00766879     EISSN: 15577988     Source Type: Book Series    
DOI: 10.1016/bs.mie.2015.03.004     Document Type: Chapter

References (130)

1. P.F. Agris Wobble position modified nucleosides evolved to select transfer RNA codon recognition: A modified-wobble hypothesis Biochimie 73 11 1991 1345 1349
2. P.F. Agris Decoding the genome: A modified view Nucleic Acids Research 32 1 2004 223 238
3. P.F. Agris Bringing order to translation: The contributions of transfer RNA anticodon-domain modifications EMBO Reports 9 7 2008 629 635
4. P.F. Agris, F.A. Vendeix, and W.D. Graham tRNA's wobble decoding of the genome: 40 years of modification Journal of Molecular Biology 366 1 2007 1 13
5. S. Akhtar, S. Sarkar, A. Mishra, and D. Sarkar A method to extract intact and pure RNA from mycobacteria Analytical Biochemistry 417 2 2011 286 288
6. A.J. Alpert Hydrophilic-interaction chromatography for the separation of peptides, nucleic acids and other polar compounds Journal of Chromatography 499 1990 177 196
7. K. Arnvig, and D. Young Non-coding RNA and its potential role in Mycobacterium tuberculosis pathogenesis RNA Biology 9 4 2012 427 436
8. H. Aviv, and P. Leder Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose Proceedings of the National Academy of Sciences of the United States of America 69 6 1972 1408 1412
9. A. Azarani, and K.H. Hecker RNA analysis by ion-pair reversed-phase high performance liquid chromatography Nucleic Acids Research 29 2 2001 E7
10. R.T. Batey, and J.S. Kieft Improved native affinity purification of RNA RNA 13 8 2007 1384 1389
11. F. Bauer, and D. Hermand A coordinated codon-dependent regulation of translation by Elongator Cell Cycle 11 24 2012 4524 4529 10.4161/cc.22689
12. U. Begley, M. Dyavaiah, A. Patil, J.P. Rooney, D. DiRenzo, C.M. Young, and et al. Trm9-catalyzed tRNA modifications link translation to the DNA damage response Molecular Cell 28 5 2007 860 870
13. M. Biba, C.J. Welch, J.P. Foley, B. Mao, E. Vazquez, and R.A. Arvary Evaluation of core-shell particle columns for ion-pair reversed-phase liquid chromatography analysis of oligonucleotides Journal of Pharmaceutical and Biomedical Analysis 72 2013 25 32
14. U. Birkedal, M. Christensen-Dalsgaard, N. Krogh, R. Sabarinathan, J. Gorodkin, and H. Nielsen Profiling of ribose methylations in RNA by high-throughput sequencing Angewandte Chemie International Edition in English 54 2 2015 451 455
15. G.R. Bjork, J.M. Durand, T.G. Hagervall, R. Leipuviene, H.K. Lundgren, K. Nilsson, and et al. Transfer RNA modification: Influence on translational frameshifting and metabolism FEBS Letters 452 1-2 1999 47 51
16. C. Brandmayr, M. Wagner, T. Bruckl, D. Globisch, D. Pearson, A.C. Kneuttinger, and et al. Isotope-based analysis of modified tRNA nucleosides correlates modification density with translational efficiency Angewandte Chemie International Edition in English 51 44 2012 11162 11165
17. G. Brawerman, J. Mendecki, and S.Y. Lee A procedure for the isolation of mammalian messenger ribonucleic acid Biochemistry 11 4 1972 637 641
18. D. Bregeon, V. Colot, M. Radman, and F. Taddei Translational misreading: A tRNA modification counteracts a + 2 ribosomal frameshift Genes and Development 15 17 2001 2295 2306
19. A.W. Bristow Accurate mass measurement for the determination of elemental formula - A tutorial Mass Spectrometry Reviews 25 1 2006 99 111
20. M. Buchhaupt, S. Sharma, S. Kellner, S. Oswald, M. Paetzold, C. Peifer, and et al. Partial methylation at Am100 in 18S rRNA of baker's yeast reveals ribosome heterogeneity on the level of eukaryotic rRNA modification PLoS One 9 2 2014 e89640
21. M. Buck, M. Connick, and B.N. Ames Complete analysis of tRNA-modified nucleosides by high-performance liquid chromatography: The 29 modified nucleosides of Salmonella typhimurium and Escherichia coli tRNA Analytical Biochemistry 129 1 1983 1 13
22. W.A. Cantara, P.F. Crain, J. Rozenski, J.A. McCloskey, K.A. Harris, X. Zhang, and et al. The RNA Modification Database, RNAMDB: 2011 update Nucleic Acids Research 39 Database issue 2011 D195 D201
23. T.M. Carlile, M.F. Rojas-Duran, B. Zinshteyn, H. Shin, K.M. Bartoli, and W.V. Gilbert Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells Nature 515 7525 2014 143 146
24. C.M. Castleberry, and P.A. Limbach Relative quantitation of transfer RNAs using liquid chromatography mass spectrometry and signature digestion products Nucleic Acids Research 38 16 2010 e162
25. C.T. Chan, Y.H. Chionh, C.H. Ho, K.S. Lim, I.R. Babu, E. Ang, and et al. Identification of N6, N6-dimethyladenosine in transfer RNA from Mycobacterium bovis Bacille Calmette-Guerin Molecules 16 6 2011 5168 5181
26. T.Y.C. Chan, W. Deng, F. Li, M.S. DeMott, I.R. Babu, T.J. Begley, and et al. Highly predictive reprogramming of tRNA modifications is linked to selective expression of codon-biased genes Chemical Research in Toxicology 28 5 2015 978 988
27. C.T. Chan, M. Dyavaiah, M.S. DeMott, K. Taghizadeh, P.C. Dedon, and T.J. Begley A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress PLoS Genetics 6 12 2010 e1001247 10.1371/journal.pgen.1001247
28. C.T. Chan, Y.L. Pang, W. Deng, I.R. Babu, M. Dyavaiah, T.J. Begley, and et al. Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins Nature Communications 3 2012 937
29. Y.G. Chen, W.E. Kowtoniuk, I. Agarwal, Y. Shen, and D.R. Liu LC/MS analysis of cellular RNA reveals NAD-linked RNA Nature Chemical Biology 5 12 2009 879 881
30. Y.H. Chionh, C.-H. Ho, D. Pruksakorn, R.I. Babu, C.S. Ng, F. Hia, and et al. A multidimensional platform for the purification of non-coding RNA species Nucleic Acids Research 41 17 2013 e168
31. P.F. Crain Preparation and enzymatic hydrolysis of DNA and RNA for mass spectrometry Methods in Enzymology 193 1990 782 790
32. P.F. Crain, J. Rozenski, and J.A. McCloskey The RNA modification database Nucleic Acids Research 27 1999 196 197 Available from: http://library.med.utah.edu/RNAmods/
33. L. Cunningham, K. Kittikamron, and Y. Lu Preparative-scale purification of RNA using an efficient method which combines gel electrophoresis and column chromatography Nucleic Acids Research 24 18 1996 3647 3648
34. A. Czerwoniec, S. Dunin-Horkawicz, E. Purta, K.H. Kaminska, J.M. Kasprzak, J.M. Bujnicki, and et al. MODOMICS: A database of RNA modification pathways. 2008 update Nucleic Acids Research 37 Database issue 2009 D118 D121
35. J.J. Dalluge, T. Hashizume, A.E. Sopchik, J.A. McCloskey, and D.R. Davis Conformational flexibility in RNA: The role of dihydrouridine Nucleic Acids Research 24 6 1996 1073 1079
36. D.R. Davis Stabilization of RNA stacking by pseudouridine Nucleic Acids Research 23 24 1995 5020 5026
37. P.C. Dedon, and T.J. Begley A system of RNA modifications and biased codon use controls cellular stress response at the level of translation Chemical Research in Toxicology 27 3 2014 330 337
38. M. Dong, C. Wang, W.M. Deen, and P.C. Dedon Absence of 2'-deoxyoxanosine and presence of abasic sites in DNA exposed to nitric oxide at controlled physiological concentrations Chemical Research in Toxicology 16 9 2003 1044 1055
39. E. Dudley, R. Tuytten, A. Bond, F. Lemière, A.G. Brenton, E.L. Esmans, and et al. Study of the mass spectrometric fragmentation of pseudouridine: Comparison of fragmentation data obtained by matrix-assisted laser desorption/ionisation post-source decay, electrospray ion trap multistage mass spectrometry, and by a method utilising electrospray quadrupole time-of-flight tandem mass spectrometry and in-source fragmentation Rapid Communications in Mass Spectrometry 19 21 2005 3075 3085
40. C.E. Dumelin, Y. Chen, A.M. Leconte, Y.G. Chen, and D.R. Liu Discovery and biological characterization of geranylated RNA in bacteria Nature Chemical Biology 8 11 2012 913 919
41. L.E. Easton, Y. Shibata, and P.J. Lukavsky Rapid, nondenaturing RNA purification using weak anion-exchange fast performance liquid chromatography RNA 16 3 2010 647 653
42. V. Emilsson, A.K. Naslund, and C.G. Kurland Thiolation of transfer RNA in Escherichia coli varies with growth rate Nucleic Acids Research 20 17 1992 4499 4505
43. J. Farand, and F. Gosselin De novo sequence determination of modified oligonucleotides Analytical Chemistry 81 10 2009 3723 3730
44. Y. Fu, G. Jia, X. Pang, R.N. Wang, X. Wang, C.J. Li, and et al. FTO-mediated formation of N6-hydroxymethyladenosine and N6-formyladenosine in mammalian RNA Nature Communications 4 2013 1798
45. S. Fujii, K. Inagaki, S. Miyashita, A.S. Groombridge, K. Nagasawa, K. Chiba, and et al. Separation and quantification of RNA molecules using size-exclusion chromatography hyphenated with inductively coupled plasma-mass spectrometry Electrophoresis 35 9 2014 1315 1318
46. C.W. Gehrke, and K.C. Kuo Ribonucleoside analysis by reversed-phase high-performance liquid chromatography Journal of Chromatography 471 1989 3 36
47. C.W. Gehrke, K.C. Kuo, R.A. McCune, K.O. Gerhardt, and P.F. Agris Quantitative enzymatic hydrolysis of tRNAs: Reversed-phase high-performance liquid chromatography of tRNA nucleosides Journal of Chromatography 230 2 1982 297 308
48. C.W. Gehrke, K.C. Kuo, and R.W. Zumwalt Chromatography of nucleosides Journal of Chromatography 188 1 1980 129 147
49. A.M. Giessing, S.S. Jensen, A. Rasmussen, L.H. Hansen, A. Gondela, K. Long, and et al. Identification of 8-methyladenosine as the modification catalyzed by the radical SAM methyltransferase Cfr that confers antibiotic resistance in bacteria RNA 15 2 2009 327 336
50. H. Grosjean, L. Droogmans, M. Roovers, and G. Keith Detection of enzymatic activity of transfer RNA modification enzymes using radiolabeled tRNA substrates Methods in Enzymology 425 2007 55 101
51. C. Gu, T.J. Begley, and P.C. Dedon tRNA modifications regulate translation during cellular stress FEBS Letters 588 23 2014 4287 4296
52. Y. Guo, and S. Gaiki Retention behavior of small polar compounds on polar stationary phases in hydrophilic interaction chromatography Journal of Chromatography A 1074 1-2 2005 71 80
53. J.F. Havelund, A.M. Giessing, T. Hansen, A. Rasmussen, L.G. Scott, and F. Kirpekar Identification of 5-hydroxycytidine at position 2501 concludes characterization of modified nucleotides in E. coli 23S rRNA Journal of Molecular Biology 411 3 2011 529 536
54. C. He Grand challenge commentary: RNA epigenetics? Nature Chemical Biology 6 12 2010 863 865
55. F. Hia, Y.H. Chionh, Y.L. Pang, M.S. DeMott, M.E. McBee, and P.C. Dedon Mycobacterial RNA isolation optimized for non-coding RNA: High fidelity isolation of 5S rRNA from Mycobacterium bovis BCG reveals novel post-transcriptional processing and a complete spectrum of modified ribonucleosides Nucleic Acids Research 43 2015 e32 (pii: gku1317)
56. A. Hienzsch, C. Deiml, V. Reiter, and T. Carell Total synthesis of the hypermodified RNA bases wybutosine and hydroxywybutosine and their quantification together with other modified RNA bases in plant materials Chemistry 19 13 2013 4244 4248
57. A.W. Hill, and R.J. Mortishire-Smith Automated assignment of high-resolution collisionally activated dissociation mass spectra using a systematic bond disconnection approach Rapid Communications in Mass Spectrometry 19 21 2005 3111 3118
58. M. Hossain, and P.A. Limbach Mass spectrometry-based detection of transfer RNAs by their signature endonuclease digestion products RNA 13 2 2007 295 303
59. B. Huang, J. Lu, and A.S. Bystrom A genome-wide screen identifies genes required for formation of the wobble nucleoside 5-methoxycarbonylmethyl-2-thiouridine in Saccharomyces cerevisiae RNA 14 10 2008 2183 2194
60. E. Katsivela, and M.G. Hofle Separation of transfer RNA and 5S ribosomal RNA using capillary electrophoresis Journal of Chromatography A 700 1-2 1995 125 136
61. S. Kellner, J. Burhenne, and M. Helm Detection of RNA modifications RNA Biology 7 2 2010 237 247
62. S. Kellner, J. Neumann, D. Rosenkranz, S. Lebedeva, R.F. Ketting, H. Zischler, and et al. Profiling of RNA modifications by multiplexed stable isotope labelling Chemical Communications (Cambridge) 50 26 2014 3516 3518
63. S. Kellner, A. Ochel, K. Thuring, F. Spenkuch, J. Neumann, S. Sharma, and et al. Absolute and relative quantification of RNA modifications via biosynthetic isotopomers Nucleic Acids Research 42 18 2014 e142
64. J.S. Kieft, and R.T. Batey A general method for rapid and nondenaturing purification of RNAs RNA 10 6 2004 988 995
65. I. Kim, S.A. McKenna, E. Viani Puglisi, and J.D. Puglisi Rapid purification of RNAs using fast performance liquid chromatography (FPLC) RNA 13 2 2007 289 294
66. Y.K. Kim, J. Yeo, B. Kim, M. Ha, and V.N. Kim Short structured RNAs with low GC content are selectively lost during extraction from a small number of cells Molecular Cell 46 6 2012 893 895
67. T. Kind, and O. Fiehn Metabolomic database annotations via query of elemental compositions: Mass accuracy is insufficient even at less than 1 ppm BMC Bioinformatics 7 2006 234
68. A.K. Kinger, A. Verma, and J.S. Tyagi A method for the isolation of pure intact RNA from mycobacteria Biotechniques 14 5 1993 724 725
69. Y. Kirino, and Z. Mourelatos Mouse Piwi-interacting RNAs are 2'-O-methylated at their 3' termini Nature Structural and Molecular Biology 14 4 2007 347 348
70. J. Klootwijk, and R.J. Planta Analysis of the methylation sites in yeast ribosomal RNA European Journal of Biochemistry 39 2 1973 325 333
71. C. Köhrer, and U.L. Rajbhandary The many applications of acid urea polyacrylamide gel electrophoresis to studies of tRNAs and aminoacyl-tRNA synthetases Methods 44 2 2008 129 138
72. J. Koubek, K.F. Lin, Y.R. Chen, R.P. Cheng, and J.J. Huang Strong anion-exchange fast performance liquid chromatography as a versatile tool for preparation and purification of RNA produced by in vitro transcription RNA 19 10 2013 1449 1459 (rna.038117.113 [pii])
73. W.E. Kowtoniuk, Y. Shen, J.M. Heemstra, I. Agarwal, and D.R. Liu A chemical screen for biological small molecule-RNA conjugates reveals CoA-linked RNA Proceedings of the National Academy of Sciences of the United States of America 106 19 2009 7768 7773
74. M.K. Kruger, S. Pedersen, T.G. Hagervall, and M.A. Sorensen The modification of the wobble base of tRNAGlu modulates the translation rate of glutamic acid codons in vivo Journal of Molecular Biology 284 3 1998 621 631
75. M. Kuschel, and W. Ausserer Use of lab-on-a-chip technology for protein sizing and quantitation Journal of Biomolecular Techniques 13 3 2002 172 178
76. P.P. Lewicki, and A.J. Sinskey Precision of RNA separation by polyacrylamide gel electrophoresis Analytical Biochemistry 33 2 1970 273 278
77. Z. Li, X. Dou, Y. Ni, Q. Chen, S. Cheng, and Y. Yamaguchi Is pulsed electric field still effective for RNA separation in capillary electrophoresis? Journal of Chromatography A 1229 2012 274 279
78. Z. Li, X. Dou, Y. Ni, K. Sumitomo, and Y. Yamaguchi Acetic acid denaturing pulsed field capillary electrophoresis for RNA separation Electrophoresis 31 21 2010 3531 3536
79. H.K. Lim, J. Chen, C. Sensenhauser, K. Cook, and V. Subrahmanyam Metabolite identification by data-dependent accurate mass spectrometric analysis at resolving power of 60,000 in external calibration mode using an LTQ/Orbitrap Rapid Communications in Mass Spectrometry 21 12 2007 1821 1832
80. J.L. Little, C.D. Cleven, and S.D. Brown Identification of "known unknowns" utilizing accurate mass data and chemical abstracts service databases Journal of the American Society for Mass Spectrometry 22 2 2011 348 359
81. J.L. Little, A.J. Williams, A. Pshenichnov, and V. Tkachenko Identification of "known unknowns" utilizing accurate mass data and ChemSpider Journal of the American Society for Mass Spectrometry 23 1 2012 179 185
82. Y. Luo, N.V. Eldho, H.O. Sintim, and T.K. Dayie RNAs synthesized using photocleavable biotinylated nucleotides have dramatically improved catalytic efficiency Nucleic Acids Research 39 19 2011 8559 8571
83. M.A. Machnicka, K. Milanowska, O. Osman Oglou, E. Purta, M. Kurkowska, A. Olchowik, and et al. MODOMICS: A database of RNA modification pathways - 2013 update Nucleic Acids Research 41 Database issue 2013 D262 D267
84. D. Mandal, C. Kohrer, D. Su, I.R. Babu, C.T. Chan, Y. Liu, and et al. Identification and codon reading properties of 5-cyanomethyl uridine, a new modified nucleoside found in the anticodon wobble position of mutant haloarchaeal isoleucine tRNAs RNA 20 2 2014 177 188
85. D. Mandal, C. Kohrer, D. Su, S.P. Russell, K. Krivos, C.M. Castleberry, and et al. Agmatidine, a modified cytidine in the anticodon of archaeal tRNA(Ile), base pairs with adenosine but not with guanosine Proceedings of the National Academy of Sciences of the United States of America 107 7 2010 2872 2877
86. S.M. McCarthy, M. Gilar, and J. Gebler Reversed-phase ion-pair liquid chromatography analysis and purification of small interfering RNA Analytical Biochemistry 390 2 2009 181 188
87. F.W. McLafferty Interpretation of mass spectra 1993 University Science Books Mill Valley, CA
88. 6-threonylcarbamoyladenosine as a widely distributed tRNA hypermodification Nature Chemical Biology 9 2 2013 105 111
89. Y. Motorin, and M. Helm tRNA stabilization by modified nucleotides Biochemistry 49 24 2010 4934 4944
90. F.V. Murphy 4th, V. Ramakrishnan, A. Malkiewicz, and P.F. Agris The role of modifications in codon discrimination by tRNA(Lys)UUU Nature Structural and Molecular Biology 11 12 2004 1186 1191
91. N. Nameki Identity elements of tRNA(Thr) towards Saccharomyces cerevisiae threonyl-tRNA synthetase Nucleic Acids Research 23 15 1995 2831 2836
92. N. Nameki, H. Asahara, M. Shimizu, N. Okada, and H. Himeno Identity elements of Saccharomyces cerevisiae tRNA(His) Nucleic Acids Research 23 3 1995 389 394
93. T. Ohara, Y. Sakaguchi, T. Suzuki, H. Ueda, K. Miyauchi, and T. Suzuki The 3' termini of mouse Piwi-interacting RNAs are 2'-O-methylated Nature Structural and Molecular Biology 14 4 2007 349 350
94. A. Patil, C.T. Chan, M. Dyavaiah, J.P. Rooney, P.C. Dedon, and T.J. Begley Translational infidelity-induced protein stress results from a deficiency in Trm9-catalyzed tRNA modifications RNA Biology 9 7 2012 990 1001
95. R.P. Perry, J. La Torre, D.E. Kelley, and J.R. Greenberg On the lability of poly(A) sequences during extraction of messenger RNA from polyribosomes Biochimica et Biophysica Acta 262 2 1972 220 226
96. S.C. Pomerantz, and J.A. McCloskey Analysis of RNA hydrolyzates by liquid chromatography-mass spectrometry Methods in Enzymology 193 1990 796 824
97. J. Putz, C. Florentz, F. Benseler, and R. Giege A single methyl group prevents the mischarging of a tRNA Natural Structural Biology 1 9 1994 580 582
98. M. Rederstorff, and A. Hüttenhofer Small non-coding RNAs in disease development and host-pathogen interactions Current Opinion in Molecular Therapeutics 12 6 2010 684 694
99. W.F. Reynolds, and R.G. Enriquez Choosing the best pulse sequences, acquisition parameters, postacquisition processing strategies, and probes for natural product structure elucidation by NMR spectroscopy Journal of Natural Products 65 2 2002 221 244
100. V.A. Rezgui, K. Tyagi, N. Ranjan, A.L. Konevega, J. Mittelstaet, M.V. Rodnina, and et al. tRNA tKUUU, tQUUG, and tEUUC wobble position modifications fine-tune protein translation by promoting ribosome A-site binding Proceedings of the National Academy of Sciences of the United States of America 110 30 2013 12289 12294
101. J. Rudinger, C. Florentz, and R. Giege Histidylation by yeast HisRS of tRNA or tRNA-like structure relies on residues - 1 and 73 but is dependent on the RNA context Nucleic Acids Research 22 23 1994 5031 5037
102. S.P. Russell, and P.A. Limbach Evaluating the reproducibility of quantifying modified nucleosides from ribonucleic acids by LC-UV-MS Journal of Chromatography, B: Analytical Technologies in the Biomedical and Life Sciences 923-924 2013 74 82
103. J.C. Salazar, A. Ambrogelly, P.F. Crain, J.A. McCloskey, and D. Söll A truncated aminoacyl-tRNA synthetase modifies RNA Proceedings of the National Academy of Sciences of the United States of America 101 20 2004 7536 7541
104. A. Schroeder, O. Mueller, S. Stocker, R. Salowsky, M. Leiber, M. Gassmann, and et al. The RIN: An RNA integrity number for assigning integrity values to RNA measurements BMC Molecular Biology 7 2006 3
105. J. Shanagar Purification of a synthetic oligonucleotide by anion exchange chromatography: Method optimisation and scale-up Journal of Biochemical and Biophysical Methods 64 3 2005 216 225
106. J. Skeidsvoll, and P.M. Ueland Analysis of RNA by capillary electrophoresis Electrophoresis 17 9 1996 1512 1517
107. D.O. Sparkman Mass spectrometry desk reference 2nd ed. Vol. 18 2007 Global View Publishing Pittsburgh, PA
108. F. Spenkuch, G. Hinze, S. Kellner, C. Kreutz, R. Micura, T. Basche, and et al. Dye label interference with RNA modification reveals 5-fluorouridine as non-covalent inhibitor Nucleic Acids Research 42 20 2014 12735 12745
109. C. Srisawat, and D.R. Engelke Streptavidin aptamers: Affinity tags for the study of RNAs and ribonucleoproteins RNA 7 4 2001 632 641
110. C. Srisawat, I.J. Goldstein, and D.R. Engelke Sephadex-binding RNA ligands: Rapid affinity purification of RNA from complex RNA mixtures Nucleic Acids Research 29 2 2001 E4
111. D. Su, C.T. Chan, C. Gu, K.S. Lim, Y.H. Chionh, M.E. McBee, and et al. Quantitative analysis of ribonucleoside modifications in tRNA by HPLC-coupled mass spectrometry Nature Protocols 9 4 2014 828 841
112. T. Suzuki, Y. Ikeuchi, A. Noma, and Y. Sakaguchi Mass spectrometric identification and characterization of RNA-modifying enzymes Methods in Enzymology 425 2007 211 229
113. T. Suzuki, and T. Suzuki Chaplet column chromatography: Isolation of a large set of individual RNAs in a single step Methods in Enzymology 425 2007 231 239
114. T. Taniguchi, K. Miyauchi, D. Nakane, M. Miyata, A. Muto, S. Nishimura, and et al. Decoding system for the AUA codon by tRNAIle with the UAU anticodon in Mycoplasma mobile Nucleic Acids Research 41 4 2013 2621 2631
115. C. Tissot Analysis of miRNA content in total RNA preparations using the Agilent 2100 bioanalyzer 2008 Agilent Technologies Palo Alto, CA http://www.chem.agilent.com/Library/applications/5989-7870EN.pdf
116. S. Tumu, A. Patil, W. Towns, M. Dyavaiah, and T.J. Begley The gene-specific codon counting database: A genome-based catalog of one-, two-, three-, four- and five-codon combinations present in Saccharomyces cerevisiae genes Database (Oxford) 2012 2012 bas002
117. R. Tuytten, F. Lemiere, W. Van Dongen, E. Witters, E.L. Esmans, R.P. Newton, and et al. Development of an on-line SPE-LC-ESI-MS method for urinary nucleosides: Hyphenation of aprotic boronic acid chromatography with hydrophilic interaction LC-ESI-MS Analytical Chemistry 80 4 2008 1263 1271
118. J. Urbonavicius, Q. Qian, J.M. Durand, T.G. Hagervall, and G.R. Bjork Improvement of reading frame maintenance is a common function for several tRNA modifications EMBO Journal 20 17 2001 4863 4873
119. F. Varricchio, and H.J. Ernst Separation of low molecular weight RNA by polyacrylamide gel electrophoresis Analytical Biochemistry 68 2 1975 485 492
120. S.P. Waghmare, P. Pousinis, D.P. Hornby, and M.J. Dickman Studying the mechanism of RNA separations using RNA chromatography and its application in the analysis of ribosomal RNA and RNA:RNA interactions Journal of Chromatography A 1216 9 2009 1377 1382
121. S.C. Walker, F.H. Scott, C. Srisawat, and D.R. Engelke RNA affinity tags for the rapid purification and investigation of RNAs and RNA-protein complexes Methods in Molecular Biology 488 2008 23 40
122. X. Wang, and C. He Dynamic RNA modifications in posttranscriptional regulation Molecular Cell 56 1 2014 5 12
123. A.M. Ward, J. Gunaratne, and M.A. Garcia-Blanco Identification of dengue RNA binding proteins using RNA chromatography and quantitative mass spectrometry Methods in Molecular Biology 1138 2014 253 270
124. W.J. Warren, and G. Vella Principles and methods for the analysis and purification of synthetic deoxyribonucleotides by high-performance liquid chromatography Molecular Biotechnology 4 2 1995 179 199
125. A. Werner Reversed-phase and ion-pair separations of nucleotides, nucleosides and nucleobases: Analysis of biological samples in health and disease Journal of Chromatography 618 1-2 1993 3 14
126. C. Yarian, H. Townsend, W. Czestkowski, E. Sochacka, A.J. Malkiewicz, R. Guenther, and et al. Accurate translation of the genetic code depends on tRNA modified nucleosides Journal of Biological Chemistry 277 19 2002 16391 16395
127. Q. Zhang, R. Pu, Y. Du, Y. Han, T. Su, H. Wang, and et al. Non-coding RNAs in hepatitis B or C-associated hepatocellular carcinoma: Potential diagnostic and prognostic markers and therapeutic targets Cancer Letters 321 1 2012 1 12
128. H.Q. Zhao, X. Wang, H.M. Li, B. Yang, H.J. Yang, and L. Huang Characterization of nucleosides and nucleobases in natural Cordyceps by HILIC-ESI/TOF/MS and HILIC-ESI/MS Molecules 18 8 2013 9755 9769
129. G. Zheng, J.A. Dahl, Y. Niu, Y. Fu, A. Klungland, Y.G. Yang, and et al. Sprouts of RNA epigenetics: The discovery of mammalian RNA demethylases RNA Biology 10 6 2013 915 918
130. G. Zhou, H. Pang, Y. Tang, X. Yao, Y. Ding, S. Zhu, and et al. Hydrophilic interaction ultra-performance liquid chromatography coupled with triple-quadrupole tandem mass spectrometry (HILIC-UPLC-TQ-MS/MS) in multiple-reaction monitoring (MRM) for the determination of nucleobases and nucleosides in ginkgo seeds Food Chemistry 150 2014 260 266