Mass spectrometry in the biology of RNA and its modifications

Journal of Proteomics

Volumn 75, Issue 12, 2012, Pages 3434-3449

  Giessing, Anders M B ^a   Kirpekar, Finn ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Cellular RNA; MS; Posttranscriptional modifications; RNA modifying enzymes

Indexed keywords

ADENINE; AMMONIA; CYTOSINE; GUANINE; MESSENGER RNA; MICRORNA; NUCLEIC ACID; NUCLEIC ACID BASE; NUCLEOSIDE; OLIGONUCLEOTIDE; POLYANION; RIBONUCLEASE; RIBOSE; RIBOSOME RNA; RNA; TRANSFER RNA; URACIL; VIRUS RNA;

ALKYLATION; ELECTROSPRAY MASS SPECTROMETRY; EVAPORATION; FAST ATOM BOMBARDMENT MASS SPECTROMETRY; FRAGMENTATION REACTION; GAS; GENE CONTROL; GENETIC VARIABILITY; GENOME; IONIZATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR BIOLOGY; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; REVIEW; RNA ANALYSIS; RNA METHYLATION; RNA PROCESSING;

BASE SEQUENCE; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; RNA; SEQUENCE ANALYSIS, RNA;

EID: 84862160503     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.01.032     Document Type: Review

References (163)

1. Deaton A.M., Bird A. CpG islands and the regulation of transcription. Genes Dev 2011, 25:1010-1022.
2. Kok R.M., Smith D.E., Barto R., Spijkerman A.M., Teerlink T., Gellekink H.J., Jakobs C., Smulders Y.M. Global DNA methylation measured by liquid chromatography-tandem mass spectrometry: analytical technique, reference values and determinants in healthy subjects. Clin Chem Lab Med 2007, 45:903-911.
3. Tost J., Schatz P., Schuster M., Berlin K., Gut I.G. Analysis and accurate quantification of CpG methylation by MALDI mass spectrometry. Nucleic Acids Res 2003, 31:e50.
4. 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 2011, 39:D195-D201.
5. Czerwoniec A., Dunin-Horkawicz S., Purta E., Kaminska K.H., Kasprzak J.M., Bujnicki J.M., Grosjean H., Rother K. MODOMICS: a database of RNA modification pathways. 2008 update. Nucleic Acids Res 2009, 37:D118-D121.
6. 2U. PLoS One 2011, 6:e20783.
7. Noma A., Sakaguchi Y., Suzuki T. Mechanistic characterization of the sulfur-relay system for eukaryotic 2-thiouridine biogenesis at tRNA wobble positions. Nucleic Acids Res 2009, 37:1335-1352.
8. Reader J.S., Metzgar D., Schimmel P., de Crecy-Lagard V. Identification of four genes necessary for biosynthesis of the modified nucleoside queuosine. J Biol Chem 2004, 279:6280-6285.
9. Guymon R., Pomerantz S.C., Ison J.N., Crain P.F., McCloskey J.A. Post-transcriptional modifications in the small subunit ribosomal RNA from Thermotoga maritima, including presence of a novel modified cytidine. RNA 2007, 13:396-403.
10. Kowalak J.A., Bruenger E., Crain P.F., McCloskey J.A. Identities and phylogenetic comparisons of posttranscriptional modifications in 16 S ribosomal RNA from Haloferax volcanii. J Biol Chem 2000, 275:24484-24489.
11. Reichow S.L., Hamma T., Ferre-D'Amare A.R., Varani G. The structure and function of small nucleolar ribonucleoproteins. Nucleic Acids Res 2007, 35:1452-1464.
12. Clouet d'Orval B., Bortolin M.-L., Gaspin C., Bachellerie J.-P. Box C/D RNA guides for the ribose methylation of archaeal tRNAs. The tRNATrp intron guides the formation of two ribose-methylated nucleosides in the mature tRNATrp. Nucleic Acids Res 2001, 29:4518-4529.
13. Karijolich J., Yu Y.-T. Spliceosomal snRNA modifications and their function. RNA Biol 2010, 7:192-204.
14. Staněk D., Neugebauer K.M. The Cajal body: a meeting place for spliceosomal snRNPs in the nuclear maze. Chromosoma 2006, 115:343-354.
15. Couget N., van Dijk E., Babajko S., Séraphin B. Cap-tabollism. Trends Biochem Sciences 2004, 29:436-444.
16. Kaneko T., Suzuki T., Kapushoc S.T., Rubio M.A., Ghazvini J., Watanabe K., Simpson L., Suzuki T. Wobble modification differences and subcellular localization of tRNAs in Leishmania tarentolae: implication for tRNA sorting mechanism. EMBO J 2003, 22:657-667.
17. 2U) in lysyl-tRNA is required for viability in yeast. RNA 2007, 13:1245-1255.
18. Motorin Y., Helm M. tRNA stabilization by modified nucleotides. Biochemistry 2010, 49:4934-4944.
19. 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 2002, 277:16391-16395.
20. 5U1939 and Ψ2504, in Escherichia coli 23S rRNA. Biochem Biophys Res Commun 2010, 392:223-227.
21. Kimura S., Suzuki T. Fine-tuning of the ribosomal decoding center by conserved methyl-modifications in the Escherichia coli 16S rRNA. Nucleic Acids Res 2010, 38:1341-1352.
22. Caboche M., Bachellerie J.P. RNA methylation and control of eukaryotic RNA biosynthesis. Effects of cycloleucine, a specific inhibitor of methylation, on ribosomal RNA maturation. Eur J Biochem 1977, 74:19-29.
23. Treede I., Jakobsen L., Kirpekar F., Vester B., Weitnauer G., Bechthold A., Douthwaite S. The avilamycin resistance determinants AviRa and AviRb methylate 23S rRNA at the guanosine 2535 base and the uridine 2479 ribose. Mol Microbiol 2003, 49:309-318.
24. Cunningham P.R., Richard R.B., Weitzmann C.J., Nurse K., Ofengand J. The absence of modified nucleotides affects both in vitro assembly and in vivo function of the 30S ribosomal subunit of Eschericia coli. Biochimie 1991, 73:789-796.
25. Semrad K., Green R. Osmolytes stimulate the reconstitution of functional 50S ribosomes from in vitro transcripts of Escherichia coli 23S rRNA. RNA 2002, 8:401-411.
26. Ma X., Yang C., Alexandrov A., Grayhack E.J., Behm-Ansmant I., Yu Y.T. Pseudouridylation of yeast U2 snRNA is catalyzed by either an RNA-guided or RNA-independent mechanism. EMBO J 2005, 24:2403-2413.
27. Yu B., Yang Z., Li J., Minakhina S., Yang M., Padgett R.W., Steward R., Chen X. Methylation as a crucial step in plant microRNA biogenesis. Science 2005, 307:932-935.
28. Horwich M.D., Li C., Matranga C., Vagin V., Farley G., Wang P., Zamore P.D. The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr Biol 2007, 17:1265-1272.
29. Felden B., Hanawa K., Atkins J.F., Himeno H., Muto A., Gesteland R.F., McCloskey J.A., Crain P.F. Presence and location of modified nucleotides in Escherichia coli tmRNA: structural mimicry with tRNA acceptor branches. EMBO J 1998, 17:3188-3196.
30. Nishimura K. Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem 2010, 79:321-349.
31. Bokar J.A., Shambaugh M.E., Polayes D., Matera A.G., Rottman F.M. Purification and cDNA cloning of the AdoMet-binding subunit of the human mRNA (N6-adenosine)-methyltransferase. RNA 1997, 3:1233-1247.
32. Wei C.M., Gershowitz A., Moss B. 5'-Terminal and internal methylated nucleotide sequences in HeLa cell mRNA. Biochemistry 1976, 15:397-401.
33. Bleicher K., Bayer E. Various factors influencing the signal intensity of oligonucleotides in electrospray mass spectrometry. Biol Mass Spectrom 1994, 23:320-322.
34. Greig M., Griffey R.H. Utility of organic bases for improved electrospray mass spectrometry of oligonucleotides. Rapid Commun Mass Spectrom 1995, 9:97-102.
35. Limbach P.A., Crain P.F., McCloskey J.A. Molecular mass measurement of intact ribonucleic aids via electrospray ionization quadrupole mass spectrometry. J Am Soc Mass Spectrom 1995, 6:27-39.
36. Nordhoff E., Ingendoh A., Cramer R., Overberg A., Stahl B., Karas M., Hillenkamp F., Crain P.F. Matrix-assisted Laser Desorption/Ionization mass spectrometry of nucleic acids with wavelengths in the ultraviolet and infrared. Rapid Commun Mass Spectrom 1992, 6:771-776.
37. Pieles U., Zurcher W., Schar M., Moser H.E. Matrix-assisted laser desorption ionization time-of-flight mass spectrometry - a powerful tool for the mass and sequence analysis of natural and modified oligonucleotides. Nucleic Acids Res 1993, 21:3191-3196.
38. Potier N., Vandorsselaer A., Cordier Y., Roch O., Bischoff R. Negative electrospray ionization mass spectrometry of synthetic and chemically modified oligonucleotides. Nucleic Acids Res 1994, 22:3895-3903.
39. Stults J.T., Marsters J.C. Improved electrospray ionization of synthetic oligodeoxynucleotides. Rapid Commun Mass Spectrom 1991, 5:359-363.
40. Apffel A., Chakel J.A., Fischer S., Lichtenwalter K., Hancock W.S. Analysis of oligonucleotides by HPLC-electrospray ionization mass spectrometry. Anal Chem 1997, 69:1320-1325.
41. Guymon R., Pomerantz S.C., Crain P.F., McCloskey J.A. Influence of phylogeny on posttranscriptional modification of rRNA in thermophilic prokaryotes: the complete modification map of 16S rRNA of Thermus thermophilus. Biochemistry 2006, 45:4888-4899.
42. Emmerechts G., Barbe S., Herdewijn P., Anne J., Rozenski J. Post-transcriptional modification mapping in the Clostridium acetobutylicum 16S rRNA by mass spectrometry and reverse transcriptase assays. Nucleic Acids Res 2007, 35:3494-3503.
43. Buck M., Connick M., Ames B.N. Complete analysis of tRNA-modified nucleosides by high-performance liquid chromatography: the 29 modified nucleosides of Salmonella typhimurium and Escherichia coli tRNA. Anal Biochem 1983, 129:1-13.
44. Pomerantz S.C., McCloskey J.A. Analysis of RNA hydrolysates by liquid chromatography-mass spectrometry. Methods Enzymol 1990, 193:796-824.
45. n based strategy for characterization of modified ribonucleic acids using reduced porous graphitic carbon as a stationary phase. J Am Soc Mass Spectrom 2011, 22.
46. Xing J., Apedo A., Tymiak A., Zhao N. Liquid chromatographic analysis of nucleosides and their mono-, di- and triphosphates using porous graphitic carbon stationary phase coupled with electrospray mass spectrometry. Rapid Commun Mass Spectrom 2004, 18:1599-1606.
47. Hancock R.L., Coleman D.L. Gas chromatographic studies on nucleosides. Anal Biochem 1965, 10:365-367.
48. Jacobson M., O'Brien J.F., Hedgcoth C. Determination of nucleoside composition of ribonucleic acid by gas-liquid chromatography. Anal Biochem 1968, 25:363-369.
49. Wu K.J., Shaler T.A., Becker C.H. Time-of-Flight mass spectrometry of underivatized single-stranded DNA oligomers by Matrix-Assisted Laser Desorption. Anal Chem 1994, 66:1637-1645.
50. Zhu Y.F., Chung C.N., Taranenko N.I., Allman S.L., Martin S.A., Haff L., Chen C.H. The study of 2,3,4-trihydroxyacetophenone and 2,4,6-trihydroxyacetophenone as matrices for DNA detection in Matrix-assisted Laser Desorption/Ionization Time-of-Flight mass spectrometry. Rapid Commun Mass Spectrom 1996, 10:383-388.
51. Lecchi P., Le H.M.T., Pannell L.K. 6-Aza-2-thiothymine: a matrix for MALDI spectra of oligonucleotides. Nucleic Acids Res 1995, 23:1276-1277.
52. McLuckey S.A., Van Berkel G.J., Glish G.L. Tandem mass spectrometry of small multiply charged oligonucleotides. J Am Soc Mass Spectrom 1992, 3:60-70.
53. Bruice PY. The chemistry of the nucleic acids. Organic chemistry 2011, 1147-1176. Pearson. 6. ed.
54. Kirpekar F., Krogh T.N. RNA fragmentation studied in a matrix-assisted laser desorption/ionisation tandem quadropole/orthogonal time-of-flight mass spectrometer. Rapid Commun Mass Spectrom 2001, 15:8-14.
55. Huang T.Y., Kharlamova A., Liu J., McLuckey S.A. Ion trap collision-induced dissociation of multiply deprotonated RNA: c/y-ions versus (a-B)/w-ions. J Am Soc Mass Spectrom 2008, 19:1832-1840.
56. Schurch S., Bernal-Mendez E., Leumann C.J. Electrospray tandem mass spectrometry of mixed-sequence RNA/DNA oligonucleotides. J Am Soc Mass Spectrom 2002, 13:936-945.
57. Andersen T.E., Kirpekar F., Haselmann K.F. RNA fragmentation in MALDI mass spectrometry studied by H/D-exchange: mechanisms of general applicability to nucleic acids. J Am Soc Mass Spectrom 2006, 17:1353-1368.
58. Slowikowski D.L., Schram K.H. Fast atom bombardment mass spectra of nucleosides. Comparison with electron impact and chemical ionization mass spectra. Nucleosides Nucleotides 1985, 4:347-376.
59. Dudley E., Tuytten R., Bond A., Lemiere F., Brenton A.G., Esmans E.L., Newton R.P. 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 Commun Mass Spectrom 2005, 19:3075-3085.
60. Liguori A., Napoli A., Sindona G. Survey of the proton affinities of adenine, cytosine, thymine and uracil dideoxyribonucleosides, deoxyribonucleosides and ribonucleosides. J Mass Spectrom 2000, 35:139-144.
61. Taucher M., Breuker K. Top-down mass spectrometry for sequencing of larger (up to 61 nt) RNA by CAD and EDD. J Am Soc Mass Spectrom 2010, 21:918-929.
62. Yang J., Hakansson K. Fragmentation of oligoribonucleotides from gas-phase ion-electron reactions. J Am Soc Mass Spectrom 2006, 17:1369-1375.
63. Gardner M.W., Li N., Ellington A.D., Brodbelt J.S. Infrared multiphoton dissociation of small-interfering RNA anions and cations. J Am Soc Mass Spectrom 2010, 21:580-591.
64. Carbon J., David H., Studier M.H. Thiobase in Escherichia coli transfer RNA: 2-thiocytosine and 5-methylaminomethyl-2-thiouracil. Science 1968, 161:1146-1147.
65. Schweizer M.P., Chheda G.B., Baczynskyj L., Hall R.H. Aminoacyl nucleosides. VII. N-(Purin-6-ylcarbamoyl)threonine. A new component of transfer ribonucleic acid. Biochemistry 1969, 8:3283-3289.
66. Kimura-Harada F., McCloskey J.A., von Minden D.L., Nishimura S. N-[(9-β-D-Ribofuranosylpurin-6-yl)-N-Methylcarbamoyl]threonine, a modified nucleoside isolated from Escherichia coli threonine transfer ribonucleic acid. Biochemistry 1972, 11:3910-3915.
67. Gregson J.M., Crain P.F., Edmonds C.G., Gupta R., Hashizume T., Phillipson D.W., McCloskey J.A. Structure of the archaeal transfer RNA nucleoside G*-15 (2-amino-4,7-dihydro- 4-oxo-7-β-D-ribofuranosyl-1H-pyrrolo[2,3-d]pyrimidine-5-carboximidamide (archaeosine)). J Biol Chem 1993, 268:10076-10086.
68. Leu5 from Escherichia coli. Biochemistry 1999, 38:207-217.
69. Bangs J.D., Crain P.F., Hashizume T., McCloskey J.A., Boothroyd J.C. Mass spectrometry of mRNA cap 4 from trypanosomatids reveals 2 novel nucleosides. J Biol Chem 1992, 267:9805-9815.
70. Crain P.F. Detection and structure analysis of modified nucleosides in RNA by mass spectrometry. Modification and and editing of RNA 1998, 47-57. ASM press, Washington, D.C. H. Grosjean, R. Benne (Eds.).
71. Zhou S.L., Sitaramaiah D., Pomerantz S.C., Crain P.F., McCloskey J.A. Tandem mass spectrometry for structure assignments of wye nucleosides from transfer RNA. Nucleosides Nucleotides Nucleic Acids 2004, 23:41-50.
72. McCloskey J.A., Liu X.-H., Crain P.F., Bruenger E., Guymon R., Hashizume T., Stetter K.O. Posttranscriptional modification of transfer RNA in the submarine hyperthermophile Pyrolobus fumarii. Nucleic Acids Symp Ser 2000, 44:267-268.
73. Cao H., Wang Y. Collisionally activated dissociation of protonated 2'-deoxycytidine, 2'-deoxyuridine, and their oxidatively damaged derivatives. J Am Soc Mass Spectrom 2006, 17:1335-1341.
74. Gregson J.M., McCloskey J.A. Collision-induced dissociation of protonated guanine. Int J Mass Spectrom Ion Processes 1997, 165/166:475-485.
75. Jensen S.S., Ariza X., Nielsen P., Vilarrasa J., Kirpekar F. Collision-induced dissociation of cytidine and its derivatives. J Mass Spectrom 2007, 42:49-57.
76. Hettich R.L. The differetiation of methyl guanosine isomers by laser ionization fourier transform mass spectrometry. Biomed Environ Mass Spectrom 1989, 18:265-277.
77. Nelson C.C., McCloskey J.A. Collision-induced dissociation of uracil and its derivatives. J Am Soc Mass Spectrom 1994, 5:339-349.
78. Nelson C.C., McCloskey J.A. Collision-induced dissociation of adenine. J Am Chem Soc 1992, 114:3661-3668.
79. Kammerer B., Frickenschmidt A., Muller C.E., Laufer S., Gleiter C.H., Liebich H. Mass spectrometric identification of modified urinary nucleosides used as potential biomedical markers by LC-ITMS coupling. Anal Bioanal Chem 2005, 382:1017-1026.
80. Li H.Y., Wang S.M., Liu H.M., Li J., Han D., Bu S.S., Zhang M.Z. Analysis of modified nucleosides in the urine of patients with malignant cancer by liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom 2008, 22:3161-3171.
81. Giessing A.M.B., Jensen S.S., Rasmussen A., Hansen L.H., Gondela A., Long K., Vester B., Kirpekar F. Identification of 8-methyladenosine as the modification catalyzed by the radical SAM methyltransferase Cfr that confers antibiotic resistance in bacteria. RNA 2009, 15:327-336.
82. Edmonds C.G., Vestal M.L., McCloskey J.A. Thermospray liquid chromatography-mass spectrometry of nucleosides and of enzymatic hydrolysates of nucleic acids. Nucleic Acids Res 1985, 13:8197-8206.
83. Phillipson D.W., Edmonds C.G., Crain P.F., Smith D.L., Davis D.R., McCloskey J.A. Isolation and structure elucidation of an epoxide derivative of the hypermodified nucleoside queuosine from Escherichia coli transfer RNA. J Biol Chem 1987, 262:3462-3471.
84. Bakin A., Kowalak J.A., McCloskey J.A., Ofengand J. The single pseudouridine residue in Escherichia coli 16s RNA is located at position 516. Nucleic Acids Res 1994, 22:3681-3684.
85. Crain P.F. Preparation and enzymatic hydrolysis of DNA and RNA for mass spectrometry. Methods Enzymol 1990, 193:782-790.
86. Ohira T., Suzuki T. Retrograde nuclear import of tRNA precursors is required for modified base biogenesis in yeast. Proc Natl Acad Sci U S A 2011, 108:10502-10507.
87. Sakurai M., Yano T., Kawabata H., Ueda H., Suzuki T. Inosine cyanoethylation identifies A-to-I RNA editing sites in the human transcriptome. Nat Chem Biol 2010, 6:733-740.
88. Edmonds C.G., Crain P.F., Gupta R., Hashizume T., Hocart C.H., Kowalak J.A., Pomerantz S.C., Stetter K.O., McCloskey J.A. Posttranscriptional modification of tRNA in thermophilic archaea (archaebacteria). J Bacteriol 1991, 173:3138-3148.
89. Sirum-Connolly K., Peltier J.M., Crain P.F., McCloskey J.A., Mason T.L. Implications of a functional large ribosomal RNA with only three modified nucleotides. Biochimie 1995, 77:30-39.
90. Kowalak J.A., Dalluge J.J., McCloskey J.A., Stetter K.O. The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles. Biochemistry 1994, 33:7869-7876.
91. Noon K.R., Bruenger E., McCloskey J.A. Posttranscriptional modifications in 16S and 23S rRNAs of the archaeal hyperthermophile Sulfolobus solfataricus. J Bacteriol 1998, 180:2883-2888.
92. opt, 95°C). J Bacteriol 2003, 185:5483-5490.
93. McCloskey J.A., Graham D.E., Zhou S.L., Crain P.F., Ibba M., Konisky J., Soll D., Olsen G.J. Post-transcriptional modification in archaeal tRNAs: identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales. Nucleic Acids Res 2001, 29:4699-4706.
94. Cong H.N., Bertaux O., Valencia R., Becue T., Fournier T., Biou D., Porquet D. Separation and characterization of the main methylated nucleobases from nuclear, cytoplasmic and poly (A)+ RNA by high-performance liquid chromatography and mass spectrometry. J Chromatogr B 1994, 661:193-204.
95. Amberg R., Urban C., Reuner B., Scharff P., Pomerantz S.C., McCloskey J.A., Gross H.J. Editing does not exist for mammalian selenocysteine transfer RNAs. Nucleic Acids Res 1993, 21:5583-5588.
96. Dalluge J.J., Hamamoto T., Horikoshi K., Morita R.Y., Stetter K.O., McCloskey J.A. Posttranscriptional modification of tRNA in psychrophilic bacteria. J Bacteriol 1997, 179:1918-1923.
97. Dalluge J.J., Hashizume T., McCloskey J.A. Quantitative measurement of dihydrouridine in RNA using isotope dilution liquid chromatography-mass spectrometry (LC/MS). Nucleic Acids Res 1996, 24:3242-3245.
98. Chan C.T.Y., Dyavaiah M., DeMott M.S., Taghizadeh K., Dedon P.C., Begley T.J. A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet 2010, 6:e1001247.
99. Chen Y.G., Kowtoniuk W.E., Agarwal I., Shen Y., Liu D.R. LC/MS analysis of cellular RNA reveals NAD-linked RNA. Nat Chem Biol 2009, 5:879-881.
100. Kowtoniuk W.E., Shen Y., Heemstra J.M., Agarwal I., Liu D.R. A chemical screen for biological small molecule-RNA conjugates reveals CoA-linked RNA. Proc Natl Acad Sci U S A 2009, 106:7768-7773.
101. Yevdakova N.A., Motyka V., Malbeck J., Travnickova A., Novak O., Strnad M., von Schwartzenberg K. Evidence for importance of tRNA-dependent cytokinin biosynthetic pathway in the moss Physcomitrella patens. J Plant Growth Regul 2008, 27:271-281.
102. Hagervall T.G., Edmonds C.G., McCloskey J.A., Bjork G.R. Transfer RNA(5-methylaminomethyl-2-thiouridine)-methyltransferase from Escherichia coli K-12 has two enzymatic activities. J Biol Chem 1987, 262:8488-8495.
103. Auxilien S., Crain P.F., Trewyn R.W., Grosjean H. Mechanism, specificity and general properties of the yeast enzyme catalysing the formation of inosine 34 in the anticodon of transfer RNA. J Mol Biol 1996, 262:437-458.
104. Slany R.K., Bosl M., Crain P.F., Kersten H. A new function of S-adenosylmethionine - the ribosyl moiety of adomet Is the precursor of the cyclopentenediol moiety of the transfer RNA wobble base queuine. Biochemistry 1993, 32:7811-7817.
105. Aas P.A., Otterlei M., Falnes P.O., Vagbo C.B., Skorpen F., Akbari M., Sundheim O., Bjoras M., Slupphaug G., Seeberg E., Krokan H.E. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 2003, 421:859-863.
106. Hartman M.C.T., Josephson K., Szostak J.W. Enzymatic aminoacylation of tRNA with unnatural amino acids. Proc Natl Acad Sci U S A 2006, 103:4356-4361.
107. 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 2010, 38:6195-6205.
108. Okamoto S., Tamaru A., Nakajima C., Nishimura K., Tanaka Y., Tokuyama S., Suzuki Y., Ochi K. Loss of a conserved 7-methylguanosine modification in 16S rRNA confers low-level streptomycin resistance in bacteria. Mol Microbiol 2007, 63:1096-1106.
109. Songe-Moller L., van den Born E., Leihne V., Vagbo C.B., Kristoffersen T., Krokan H.E., Kirpekar F., Falnes P.O., Klungland A. Mammalian ALKBH8 possesses tRNA methyltransferase activity required for the biogenesis of multiple wobble uridine modifications implicated in translational decoding. Mol Cell Biol 2010, 30:1814-1827.
110. van den Born E., Vagbo C.B., Songe-Moller L., Leihne V., Lien G.F., Leszczynska G., Malkiewicz A., Krokan H.E., Kirpekar F., Klungland A., Falnes P.O. ALKBH8-mediated formation of a novel diastereomeric pair of wobble nucleosides in mammalian tRNA. Nat Commun 2011, 2:172.
111. Fu Y., Dai Q., Zhang W., Ren J., Pan T., He C. The AlkB domain of mammalian ABH8 catalyzes hydroxylation of 5-methoxycarbonylmethyluridine at the wobble position of tRNA. Angew Chem Int Ed Engl 2010, 49:8885-8888.
112. Leidel S., Pedrioli P.G.A., Bucher T., Brost R., Costanzo M., Schmidt A., Aebersold R., Boone C., Hofmann K., Peter M. Ubiquitin-related modifier Urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA. Nature 2009, 458:228-232.
113. 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 2004, 279:12363-12368.
114. Schlieker C.D., Van der Veen A.G., Damon J.R., Spooner E., Ploegh H.L. A functional proteomics approach links the ubiquitin-related modifier Urm1 to a tRNA modification pathway. Proc Natl Acad Sci U S A 2008, 105:18255-18260.
115. 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 2009, 37:2894-2909.
116. 4-acetylcytidine of tRNA anticodon. EMBO J 2008, 27:2194-2203.
117. Huang B., Lu J., Bystrom A.S. A genome-wide screen identifies genes required for formation of the wobble nucleoside 5-methoxycarbonylmethyl-2-thiouridine in Saccharomyces cerevisiae. RNA 2008, 14:2183-2194.
118. de Crecy-Lagard V., Brochier-Armanet C., Urbonavicius J., Fernandez B., Phillips G., Lyons B., Noma A., Alvarez S., Droogmans L., Armengaud J., Grosjean H. Biosynthesis of wyosine derivatives in tRNA: an ancient and highly diverse pathway in Archaea. Mol Biol Evol 2010, 27:2062-2077.
119. Kowalak J.A., Pomerantz S.C., Crain P.F., McCloskey J.A. A novel method for the determination of posttranscriptional modification in RNA by mass spectrometry. Nucleic Acids Res 1993, 21:4577-4585.
120. Kirpekar F. RNA mapping. The encyclopedia of mass spectrometry. Biological applications Part B: Carbohydrates, nucleic acids and other biological compounds 2006, 10-14. Elsevier Ltd., Oxford, UK. 1 ed. M.L. Gross, R.M. Caprioli (Eds.).
121. Pomerantz S.C., McCloskey J.A. Detection of the common RNA nucleoside pseudouridine in mixtures of oligonucleotides by mass spectrometry. Anal Chem 2005, 77:4687-4697.
122. Qiu F., McCloskey J.A. Selective detection of ribose-methylated nucleotides in RNA by a mass spectrometry-based method. Nucleic Acids Res 1999, 27:e20.
123. Andersen T.E., Porse B.T., Kirpekar F. A novel partial modification at 2501 in Escherichia coli 23S ribosomal RNA. RNA 2004, 10:907-913.
124. Kowalak J.A., Bruenger E., McCloskey J.A. Posttranscriptional modification of the central loop of domain V in Escherichia coli 23 S ribosomal RNA. J Biol Chem 1995, 270:17758-17764.
125. Hansen M.A., Kirpekar F., Ritterbusch W., Vester B. Posttranscriptional modifications in the A-loop of 23S rRNAs from selected archaea and eubacteria. RNA 2002, 8:202-213.
126. Patteson K.G., Rodicio L.P., Limbach P.A. Identification of the mass-silent post-transcriptionally modified nucleoside pseudouridine in RNA by matrix-assisted laser desorption/ionisation mass spectrometry. Nucleic Acids Res 2001, 29:e49.
127. Mengel-Jorgensen J., Jensen S.S., Rasmussen A., Poehlsgaard J., Iversen J.J., Kirpekar F. Modifications in Thermus thermophilus 23 S ribosomal RNA are centered in regions of RNA-RNA contact. J Biol Chem 2006, 281:22108-22117.
128. Taucher M., Ganisl B., Breuker K. Identification, localization, and relative quantitation of pseudouridine in RNA by tandem mass spectrometry of hydrolysis products. Int J Mass Spectrom 2011, 304:91-97.
129. Kowalak J.A., Bruenger E., Hashizume T., Peltier J.M., Ofengand J., McCloskey J.A. Structural characterization of U*-1915 in domain IV from Escherichia coli 23S ribosomal RNA as 3-methylpseudouridine. Nucleic Acids Res 1996, 24:688-693.
130. Bruenger E., Kowalak J.A., Kuchino Y., McCloskey J.A., Mizushima H., Stetter K.O., Crain P.F. 5S rRNA modification in the hyperthermophilic archaea Sulfolobus solfataricus and Pyrodictium occultum. FASEB J 1993, 7:196-200.
131. Crain P.F., Alfonzo J.D., Rozenski J., Kapushoc S.T., McCloskey J.A., Simpson L. Modification of the universally unmodified uridine-33 in a mitochondria-imported edited tRNA and the role of the anticodon arm structure on editing efficiency. RNA 2002, 8:752-761.
132. McCloskey J.A., Rozenski J. The Small Subunit rRNA Modification Database. Nucleic Acids Res 2005, 33:D135-D138.
133. Ile, base pairs with adenosine but not with guanosine. Proc Natl Acad Sci U S A 2010, 107:2872-2877.
134. 2-guanine)-dimethyltransferase (Trm1) catalyzes transfer of methyl groups not only to guanine 26 but also to guanine 27 in tRNA. J Biol Chem 2009, 284:20467-20478.
135. Douthwaite S., Kirpekar F. Identifying modifications in RNA by MALDI mass spectrometry. Methods Enzymol 2007, 425:3-20.
136. Havelund J.F., Giessing A.M., Hansen T., Rasmussen A., Scott L.G., Kirpekar F. Identification of 5-hydroxycytidine at position 2501 concludes characterization of modified nucleotides in E. coli 23S rRNA. J Mol Biol 2011, 411:529-536.
137. Johansen S.K., Maus C.E., Plikaytis B.B., Douthwaite S. Capreomycin binds across the ribosomal subunit interface using tlyA-encoded 2'-O-methylations in 16S and 23S rRNAs. Mol Cell 2006, 23:173-182.
138. Kehrenberg C., Schwarz S., Jacobsen L., Hansen L.H., Vester B. A new mechanism for chloramphenicol, florfenicol and clindamycin resistance: methylation of 23S ribosomal RNA at A2503. Mol Microbiol 2005, 57:1064-1073.
139. Savic M., Lovric J., Tomic T.I., Vasiljevic B., Conn G.L. Determination of the target nucleosides for members of two families of 16S rRNA methyltransferases that confer resistance to partially overlapping groups of aminoglycoside antibiotics. Nucleic Acids Res 2009, 37:5420-5431.
140. 1A57/58 methyltransferase. Nucleic Acids Res 2010, 38:6206-6218.
141. Purta E., O'Connor M., Bujnicki J.M., Douthwaite S. YgdE is the 2'-O-ribose methyltransferase RlmM specific for nucleotide C2498 in bacterial 23S rRNA. Mol Microbiol 2009, 72:1147-1158.
142. 6 methyltransferase specific for modification of A1618 of 23 S ribosomal RNA, a methylated residue located close to the ribosomal exit tunnel. J Mol Biol 2008, 375:291-300.
143. Das G., Thotala D.K., Kapoor S., Karunanithi S., Thakur S.S., Singh N.S., Varshney U. Role of 16S ribosomal RNA methylations in translation initiation in Escherichia coli. EMBO J 2008, 27:840-851.
144. Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 2000, 289:905-920.
145. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., Cate J.H. Structures of the bacterial ribosome at 3.5 Å resolution. Science 2005, 310:827-834.
146. Selmer M., Dunham C.M., Murphy F.V., Weixlbaumer A., Petry S., Kelley A.C., Weir J.R., Ramakrishnan V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 2006, 313:1935-1942.
147. Yusupov M.M., Yusupova G.Z., Baucom A., Lieberman K., Earnest T.N., Cate J.H.D., Noller H.F. Crystal structure of the ribosome at 5.5. Å resolution. Science 2001, 292:883-896.
148. Wilson D.N., Schlünzen F., Harms J.M., Starosta A.L., Connell S.R., Fucini P. The oxazolidinone antibiotics perturb the ribosomal peptidyl-transferase center and effect tRNA positioning. Proc Natl Acad Sci U S A 2008, 105:13339-13344.
149. Petersson E.J., Shahgholi M., Lester H.A., Dougherty D.A. MALDI-TOF mass spectrometry methods for evaluation of in vitro aminoacyl tRNA production. RNA 2002, 8:542-547.
150. Taniguchi H., Hayashi N. A liquid chromatography/electrospray mass spectrometric study on the post-transcriptional modification of tRNA. Nucleic Acids Res 1998, 26:1481-1486.
151. Katoh T., Sakaguchi Y., Miyauchi K., Suzuki T., Kashiwabara S., Baba T., Suzuki T. Selective stabilization of mammalian microRNAs by 3' adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev 2009, 23:433-438.
152. Pappin D.J., Højrup P., Bleasby A.J. Rapid identification of proteins by peptide-mass fingerprinting. Curr Biol 1993, 3:327-332.
153. Mann M., Wilm M. Error-tolerant identification of peptides in sequence databases by peptide sequence tags. Anal Chem 1994, 66:4390-4399.
154. Jackson G.W., McNichols R.J., Fox G.E., Willson R.C. Universal bacterial identification by mass spectrometry of 16S ribosomal RNA cleavage products. Int J Mass Spectrom Ion Processes 2006, 261:218-226.
155. Jackson G.W., McNichols R.J., Fox G.E., Willson R.C. Bacterial genotyping by 16S rRNA mass cataloging. BMC Bioinformatics 2006, 7:321.
156. Matthiesen R., Kirpekar F. Identification of RNA molecules by specific enzyme digestion and mass spectrometry: software for and implementation of RNA mass mapping. Nucleic Acids Res 2009, 37:e48.
157. Nakayama H., Akiyama M., Taoka M., Yamauchi Y., Nobe Y., Ishikawa H., Takahashi N., Isobe T. Ariadne: a database search engine for identification and chemical analysis of RNA using tandem mass spectrometry data. Nucleic Acids Res 2009, 37:e47.
158. Taoka M., Yamauchi Y., Nobe Y., Masaki S., Nakayama H., Ishikawa H., Takahashi N., Isobe T. An analytical platform for mass spectrometry-based identification and chemical analysis of RNA in ribonucleoprotein complexes. Nucleic Acids Res 2009, 37:e140.
159. Hossain M., Limbach P.A. Mass spectrometry-based detection of transfer RNAs by their signature endonuclease digestion products. RNA 2007, 13:295-303.
160. Meng Z.J., Limbach P.A. Quantitation of ribonucleic acids using O-18 labeling and mass spectrometry. Anal Chem 2005, 77:1891-1895.
161. Castleberry C.M., Limbach P.A. Relative quantitation of transfer RNAs using liquid chromatography mass spectrometry and signature digestion products. Nucleic Acids Res 2010, 38:e162.
162. Waghmare S.P., Dickman M.J. Characterization and quantification of RNA post-transcriptional modifications using stable isotope labeling of RNA in conjunction with mass spectrometry analysis. Anal Chem 2011, 83:4894-4901.
163. Krog J.S., Espanol Y., Giessing A.M., Dziergowska A., Malkiewicz A., Ribas de Pouplana L., Kirpekar F. 3-(3-amino-3-carboxypropyl)-5,6-dihydrouridine is one of two novel post-transcriptional modifications in tRNALys(UUU) from Trypanosoma brucei. FEBS J 2011, 278:4782-4796.