5-methylcytosine in RNA: Detection, enzymatic formation and biological functions

Nucleic Acids Research

Volumn 38, Issue 5, 2009, Pages 1415-1430

  Motorin, Yuri ^a   Lyko, Frank ^b   Helm, Mark ^c,d  

^a UNIVERSITÉ DE LORRAINE   (France)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; BISULFITE; CYSTEINE; DNA METHYLTRANSFERASE 2; MAGNESIUM ION; MESSENGER RNA; METHYLTRANSFERASE; PROTEIN FMU; PROTEIN P120; PROTEIN TRM4; PROTEIN YCCW; PROTEIN YEBU; RIBOSOME RNA; RNA; RNA METHYLTRANSFERASE; TRANSFER RNA; UNCLASSIFIED DRUG; TRANSFER RNA METHYLTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CELL FUNCTION; CHEMICAL MODIFICATION; CRYSTAL STRUCTURE; DNA METHYLATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME METABOLISM; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; GENE MAPPING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR BIOLOGY; NONHUMAN; PHYSICAL CHEMISTRY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA ANALYSIS; RNA METHYLATION; RNA SEQUENCE; RNA STABILITY; RNA TRANSLATION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; THIN LAYER CHROMATOGRAPHY; BIOCATALYSIS; CHEMISTRY; CLASSIFICATION; METABOLISM; PHYSIOLOGY; REVIEW;

5-METHYLCYTOSINE; BIOCATALYSIS; RNA; SEQUENCE ANALYSIS, RNA; TRNA METHYLTRANSFERASES;

EID: 77950476036     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1117     Document Type: Article

References (122)

1. Hotchkiss, R.D. (1948) The quantitative separation of purines, pyrimidines, and nucleosides by paper chromatography. J. Biol. Chem., 175, 315-332.
2. Luciano, D.J., Mirsky, H., Vendetti, N.J. and Maas, S. (2004) RNA editing of a miRNA precursor. RNA, 10, 1174-1177.
3. Blow, M.J., Grocock, R.J., van Dongen, S., Enright, A.J., Dicks, E., Futreal, P.A., Wooster, R. and Stratton, M.R. (2006) RNA editing of human microRNAs. Genome Biol., 7, R27.
4. Yang, Z., Ebright, Y.W., Yu, B. and Chen, X. (2006) HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2′ OH of the 3′ terminal nucleotide. Nucleic Acids Res., 34, 667-675.
5. Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R.W., Steward, R. and Chen, X. (2005) Methylation as a crucial step in plant microRNA biogenesis. Science, 307, 932-935.
6. Horwich, M.D., Li, C., Matranga, C., Vagin, V., Farley, G., Wang, P. and Zamore, P.D. (2007) The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr. Biol., 17, 1265-1272.
7. Saito, K., Sakaguchi, Y., Suzuki, T., Siomi, H. and Siomi, M.C. (2007) Pimet, the Drosophila homolog of HEN1, mediates 2′-O-methylation of Piwi-interacting RNAs at their 3′ ends. Genes Dev., 21, 1603-1608.
8. Grosjean, H., Droogmans, L., Roovers, M. and Keith, G. (2007) Detection of enzymatic activity of transfer RNA modification enzymes using radiolabeled tRNA substrates. Methods Enzymol., 425, 55-101.
9. Hengesbach, M., Meusburger, M., Lyko, F. and Helm, M. (2008) Use of DNAzymes for site-specific analysis of ribonucleotide modifications. RNA, 14, 180-187.
10. Zhao, X. and Yu, Y.T. (2004) Detection and quantitation of RNA base modifications. RNA, 10, 996-1002.
11. Stach, D., Schmitz, O.J., Stilgenbauer, S., Benner, A., Dohner, H., Wiessler, M. and Lyko, F. (2003) Capillary electrophoretic analysis of genomic DNA methylation levels. Nucleic Acids Res., 31, E2.
12. Cornelius, M.G. and Schmeiser, H.H (2007) RNA analysis by MEKC with LIF detection. Electrophoresis, 28, 3901-3907.
13. Li, H.Y., Wang, S.M., Liu, H.M., Li, J., Han, D., Bu, S.S. and Zhang, M.Z. (2008) Analysis of modified nucleosides in the urine of patients with malignant cancer by liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom., 22, 3161-3171.
14. Wagner, T.M., Nair, V., Guymon, R., Pomerantz, S.C., Crain, P.F., Davis, D.R. and McCloskey, J.A. (2004) A novel method for sequence placement of modified nucleotides in mixtures of transfer RNA. Nucleic Acids Symp. Ser., 48, 263-264.
15. Dai, Q., Fong, R., Saikia, M., Stephenson, D., Yu, Y.T., Pan, T. and Piccirilli, J.A. (2007) Identification of recognition residues for ligation-based detection and quantitation of pseudouridine and N6-methyladenosine. Nucleic Acids Res., 35, 6322-6329.
16. Yu, Y.T., Shu, M.D. and Steitz, J.A. (1997) A new method for detecting sites of 2′-O-methylation in RNA molecules. RNA, 3, 324-331.
17. Motorin, Y., Muller, S., Behm-Ansmant, I. and Branlant, C. (2007) Identification of modified residues in RNAs by reverse transcription-based methods. Methods Enzymol., 425, 21-53.
18. Lambrinakos, A., Humphrey, K.E., Babon, J.J., Ellis, T.P. and Cotton, R.G. (1999) Reactivity of potassium permanganate and tetraethylammonium chloride with mismatched bases and a simple mutation detection protocol. Nucleic Acids Res., 27, 1866-1874.
19. Bui, C.T., Rees, K. and Cotton, R.G. (2003) Permanganate oxidation reactions of DNA: perspective in biological studies. Nucleosides Nucleotides Nucleic Acids, 22, 1835-1855.
20. Cotton, R.G., Rodrigues, N.R. and Campbell, R.D. (1988) Reactivity of cytosine and thymine in single-base-pair mismatches with hydroxylamine and osmium tetroxide and its application to the study of mutations. Proc. Natl Acad. Sci. USA, 85, 4397-4401.
21. Rubin, C.M. and Schmid, C.W. (1980) Pyrimidine-specific chemical reactions useful for DNA sequencing. Nucleic Acids Res., 8, 4613-4619.
22. Zuo, S., Boorstein, R.J. and Teebor, G.W. (1995) Oxidative damage to 5-methylcytosine in DNA. Nucleic Acids Res., 23, 3239-3243.
23. Tabone, T., Sallmann, G., Chiotis, M., Law, M. and Cotton, R. (2006) Chemical cleavage of mismatch (CCM) to locate base mismatches in heteroduplex DNA. Nat. Protoc., 1, 2297-2304.
24. Maxam, A.M. and Gilbert, W. (1977) A new method for sequencing DNA. Proc. Natl. Acad. Sci. USA, 74, 560-564.
25. Peattie, D.A. (1979) Direct chemical method for sequencing RNA. Proc. Natl Acad. Sci. USA, 76, 1760-1764.
26. Fritzsche, E., Hayatsu, H., Igloi, G.L., Iida, S. and Kossel, H. (1987) The use of permanganate as a sequencing reagent for identification of 5-methylcytosine residues in DNA. Nucleic Acids Res., 15, 5517-5528.
27. Okamoto, A. (2009) Chemical approach toward efficient DNA methylation analysis. Org. Biomol. Chem., 7, 21-26.
28. Rideout, W.M. 3rd, Coetzee, G.A., Olumi, A.F. and Jones, P.A. (1990) 5-Methylcytosine as an endogenous mutagen in the human LDL receptor and p53 genes. Science, 249, 1288-1290.
29. Suzuki, T., Nakamura, T., Yamada, M., Ide, H., Kanaori, K., Tajima, K., Morii, T. and Makino, K. (1999) Isolation and characterization of diazoate intermediate upon nitrous acid and nitric oxide treatment of 2′-deoxycytidine. Biochemistry, 38, 7151-7158.
30. Ali, M.M., Alam, M.R., Kawasaki, T., Nakayama, S., Nagatsugi, F. and Sasaki, S. (2004) Sequence- and base-specific delivery of nitric oxide to cytidine and 5-methylcytidine leading to efficient deamination. J. Am. Chem. Soc., 126, 8864-8865.
31. Singer, B. (1976) All oxygens in nucleic acids react with carcinogenic ethylating agents. Nature, 264, 333-339.
32. Singer, B. (1975) The chemical effects of nucleic acid alkylation and their relation to mutagenesis and carcinogenesis. Prog. Nucleic Acid Res. Mol. Biol., 15, 219-284.
33. Peattie, D.A. and Gilbert, W. (1980) Chemical probes for higher-order structure in RNA. Proc. Natl Acad. Sci. USA, 77, 4679-4682.
34. Peattie, D.A. and Herr, W. (1981) Chemical probing of the tRNA-ribosome complex. Proc. Natl Acad. Sci. USA, 78, 2273-2277.
35. Frommer, M., McDonald, L.E., Millar, D.S., Collis, C.M., Watt, F., Grigg, G.W., Molloy, P.L. and Paul, C.L. (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl Acad. Sci. USA, 89, 1827-1831.
36. Clark, S.J., Harrison, J., Paul, C.L. and Frommer, M. (1994) High sensitivity mapping of methylated cytosines. Nucleic Acids Res., 22, 2990-2997.
37. Eckhardt, F., Lewin, J., Cortese, R., Rakyan, V.K., Attwood, J., Burger, M., Burton, J., Cox, T.V., Davies, R., Down, T.A. et al. (2006) DNA methylation profiling of human chromosomes 6, 20 and 22. Nat. Genet., 38, 1378-1385.
38. Meissner, A., Gnirke, A., Bell, G.W., Ramsahoye, B., Lander, E.S. and Jaenisch, R. (2005) Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res., 33, 5868-5877.
39. 5C. Mol. Cell Biol., 25, 8191-8201.
40. Schaefer, M., Pollex, T., Hanna, K. and Lyko, F. (2009) RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res., 37, e12.
41. Warnecke, P.M., Stirzaker, C., Melki, J.R., Millar, D.S., Paul, C.L. and Clark, S.J. (1997) Detection and measurement of PCR bias in quantitative methylation analysis of bisulphite-treated DNA. Nucleic Acids Res., 25, 4422-4426.
42. Sprinzl, M. and Vassilenko, K.S. (2005) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res., 33, D139-D140.
43. Smith, J.E., Cooperman, B.S. and Mitchell, P. (1992) Methylation sites in Escherichia coli ribosomal RNA: localization and identification of four new sites of methylation in 23S rRNA. Biochemistry, 31, 10825-10834.
44. Kowalak, J.A., Pomerantz, S.C., Crain, P.F. and McCloskey, J.A. (1993) A novel method for the determination of post-transcriptional modification in RNA by mass spectrometry. Nucleic Acids Res., 21, 4577-4585.
45. Kowalak, J.A., Bruenger, E. and McCloskey, J.A. (1995) Posttranscriptional modification of the central loop of domain V in Escherichia coli 23 S ribosomal RNA J. Biol. Chem., 270, 17758-17764.
46. Suzuki, T., Ikeuchi, Y., Noma, A. and Sakaguchi, Y. (2007) Mass spectrometric identification and characterization of RNA-modifying enzymes. Methods Enzymol., 425, 211-229.
47. Noon, K.R., Bruenger, E. and McCloskey, J.A. (1998) Posttranscriptional modifications in 16S and 23S rRNAs of the archaeal hyperthermophile Sulfolobus solfataricus J. Bacteriol., 180, 2883-2888.
48. Veldman, G.M., Klootwijk, J., de Regt, V.C., Planta, R.J., Branlant, C., Krol, A. and Ebel, J.P. (1981) The primary and secondary structure of yeast 26S rRNA. Nucleic Acids Res., 9, 6935-6952.
49. Maden, B.E. (1988) Locations of methyl groups in 28 S rRNA of Xenopus laevis and man. Clustering in the conserved core of molecule. J. Mol. Biol., 201, 289-314.
50. Maden, B.E. (1986) Identification of the locations of the methyl groups in 18 S ribosomal RNA from Xenopus laevis and man. J. Mol. Biol., 189, 681-699.
51. Kowalak, J.A., Bruenger, E., Crain, P.F. and McCloskey, J.A. (2000) Identities and phylogenetic comparisons of posttranscriptional modifications in 16S ribosomal RNA from Haloferax volcanii. J. Biol. Chem., 275, 24484-24489.
52. Piekna-Przybylska, D., Decatur, W.A. and Fournier, M.J. (2008) The 3D rRNA modification maps database: with interactive tools for ribosome analysis. Nucleic Acids Res., 36, D178-D183.
53. Dubin, D.T. and Taylor, R.H. (1975) The methylation state of poly A-containing messenger RNA from cultured hamster cells. Nucleic Acids Res., 2, 1653-1668.
54. Dubin, D.T. and Stollar, V. (1975) Methylation of Sindbis virus "26S"messenger RNA. Biochem. Biophys. Res. Commun., 66, 1373-1379.
55. Dubin, D.T., Stollar, V., Hsuchen, C.C., Timko, K. and Guild, G.M. (1977) Sindbis virus messenger RNA: the 5′-termini and methylated residues of 26 and 42 S RNA. Virology, 77, 457-470.
56. Sommer, S., Salditt-Georgieff, M., Bachenheimer, S., Darnell, J.E., Furuichi, Y., Morgan, M. and Shatkin, A.J. (1976) The methylation of adenovirus-specific nuclear and cytoplasmic RNA. Nucleic Acids Res., 3, 749-765.
57. Salditt-Georgieff, M., Jelinek, W., Darnell, J.E., Furuichi, Y., Morgan, M. and Shatkin, A. (1976) Methyl labeling of HeLa cell hnRNA: a comparison with mRNA. Cell, 7, 227-237.
58. Furuichi, Y., Morgan, M., Shatkin, A.J., Jelinek, W., Salditt-Georgieff, M. and Darnell, J.E. (1975) Methylated, blocked 5 termini in HeLa cell mRNA. Proc. Natl Acad. Sci. USA, 72, 1904-1908.
59. Desrosiers, R., Friderici, K. and Rottman, F. (1974) Identification of methylated nucleosides in messenger RNA from Novikoff hepatoma cells. Proc. Natl Acad. Sci. USA, 71, 3971-3975.
60. Adams, J.M. and Cory, S. (1975) Modified nucleosides and bizarre 5′-termini in mouse myeloma mRNA. Nature, 255, 28-33.
61. Lavi, S. and Shatkin, A.J. (1975) Methylated simian virus 40-specific RNA from nuclei and cytoplasm of infected BSC-1 cells. Proc. Natl Acad. Sci. USA, 72, 2012-2016.
62. Sakamoto, K. and Okada, N. (1985) 5-Methylcytidylic modification of in vitro transcript from the rat identifier sequence; evidence that the transcript forms a tRNA-like structure. Nucleic Acids Res., 13, 7195-7206.
63. Rozhdestvensky, T.S., Crain, P.F. and Brosius, J. (2007) Isolation and posttranscriptional modification analysis of native BC1 RNA from mouse brain. RNA Biol., 4, 11-15.
64. Brule, H., Grosjean, H., Giege, R. and Florentz, C. (1998) A pseudoknotted tRNA variant is a substrate for tRNA (cytosine-5)-methyltransferase from Xenopus laevis. Biochimie, 80, 977-985.
65. 5U methyltransferases. Nucleic Acids Res., 32, 2453-2463.
66. 5C methyltransferases from searching genomic and proteomic sequences. Nucleic Acids Res., 27, 3138-3145.
67. Pavlopoulou, A. and Kossida, S. (2009) Phylogenetic analysis of the eukaryotic RNA (cytosine-5)-methyltransferases. Genomics, 93, 350-357.
68. 5C967 methyltransferase from Escherichia coli. Biochemistry, 38, 1884-1892.
69. 5C967 methyltransferase from Escherichia coli. Biochemistry, 38, 4053-4057.
70. 5C methyltransferase, Fmu, provides insight into catalytic mechanism and specific binding of RNA substrate. Strucure, 11, 1609-1620.
71. 5C methyltransferase specific for 16 S rRNA nucleotide 1407. J. Mol. Biol., 359, 777-786.
72. 5C methyltransferase YebU from Escherichia coli reveals a C-terminal RNA-recruiting PUA domain. J. Mol. Biol., 360, 774-787.
73. 5C methyltransferase specific for 23S rRNA nucleotide 1962. J. Mol. Biol., 383, 641-651.
74. 5C methyltransferase RlmI (YccW) reveals evolutionary links between RNA modification enzymes. J. Mol. Biol., 383, 652-666.
75. Grosjean, H., Gaspin, C., Marck, C., Decatur, W.A. and de Crecy-Lagard, V. (2008) RNomics and Modomics in the halophilic archaea Haloferax volcanii: identification of RNA modification genes. BMC Genomics, 9, 470.
76. Kowalak, J.A., Dalluge, J.J., McCloskey, J.A. and Stetter, K.O. (1994) The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles. Biochemistry, 33, 7869-7876.
77. Constantinesco, F., Motorin, Y. and Grosjean, H. (1999) Transfer RNA modification enzymes from Pyrococcus furiosus: detection of the enzymatic activities in vitro. Nucleic Acids Res., 27, 1308-1315.
78. Ishikawa, I., Sakai, N., Tamura, T., Yao, M., Watanabe, N. and Tanaka, I. (2004) Crystal structure of human p120 homologue protein PH1374 from Pyrococcus horikoshii. Proteins, 54, 814-816.
79. 5C methyltransferase. J. Biol. Chem., 282, 18711-18721.
80. Wu, P., Brockenbrough, J.S., Paddy, M.R. and Aris, J.P. (1998) NCL1, a novel gene for a non-essential nuclear protein in Saccharomyces cerevisiae. Gene, 220, 109-117.
81. 5C-methyltransferase (Trm4) in yeast Saccharomyces cerevisiae: identification of the gene and substrate specificity of the enzyme. RNA, 5, 1105-1118.
82. 5C methyltransferase enhances the catalytic efficiency of the amino-terminal domain. J. Biol. Chem., 282, 23663-23671.
83. 5C methyltransferase. RNA, 13, 967-973.
84. Frye, M. and Watt, F.M. (2006) The RNA methyltransferase Misu (NSun2) mediates Myc-induced proliferation and is upregulated in tumors. Curr. Biol., 16, 971-981.
85. Sakita-Suto, S., Kanda, A., Suzuki, F., Sato, S., Takata, T. and Tatsuka, M. (2007) Aurora-B regulates RNA methyltransferase NSUN2. Mol. Biol. Cell., 18, 1107-1117.
86. (CAA). Nucleic Acids Res., 34, 6034-6043.
87. de Beus, E., Brockenbrough, J.S., Hong, B. and Aris, J.P. (1994) Yeast NOP2 encodes an essential nucleolar protein with homology to a human proliferation marker. J. Cell. Biol., 127, 1799-1813.
88. Hong, B., Brockenbrough, J.S., Wu, P. and Aris, J.P. (1997) Nop2p is required for pre-rRNA processing and 60S ribosome subunit synthesis in yeast. Mol. Cell. Biol., 17, 378-388.
89. King, M., Ton, D. and Redman, K.L. (1999) A conserved motif in the yeast nucleolar protein Nop2p contains an essential cysteine residue. Biochem. J., 337, 29-35.
90. King, M.Y. and Redman, K.L. (2002) RNA methyltransferases utilize two cysteine residues in the formation of 5-methylcytosine. Biochemistry, 41, 11218-11225.
91. Hong, B., Wu, K., Brockenbrough, J.S., Wu, P. and Aris, J.P. (2001) Temperature sensitive nop2 alleles defective in synthesis of 25S rRNA and large ribosomal subunits in Saccharomyces cerevisiae. Nucleic Acids Res., 29, 2927-2937.
92. Koonin, E.V. (1994) Prediction of an rRNA methyltransferase domain in human tumor-specific nucleolar protein P120. Nucleic Acids Res., 22, 2476-2478.
93. Gustafson, W.C., Taylor, C.W., Valdez, B.C., Henning, D., Phippard, A., Ren, Y., Busch, H. and Durban, E. (1998) Nucleolar protein p120 contains an arginine-rich domain that binds to ribosomal RNA. Biochem. J., 331, 387-393.
94. Doll, A. and Grzeschik, K.H. (2001) Characterization of two novel genes, WBSCR20 and WBSCR22, deleted in Williams-Beuren syndrome. Cytogenet. Cell Genet., 95, 20-27.
95. Harris, T., Marquez, B., Suarez, S. and Schimenti, J. (2007) Sperm motility defects and infertility in male mice with a mutation in Nsun7, a member of the Sun domain-containing family of putative RNA methyltransferases. Biol. Reprod., 77, 376-382.
96. Wilkinson, C.R., Bartlett, R., Nurse, P. and Bird, A.P. (1995) The fission yeast gene pmt1+ encodes a DNA methyltransferase homologue. Nucleic Acids Res., 23, 203-210.
97. Yoder, J.A. and Bestor, T.H. (1998) A candidate mammalian DNA methyltransferase related to pmt1p of fission yeast. Hum. Mol. Genet., 7, 279-284.
98. Okano, M., Xie, S. and Li, E. (1998) Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res., 26, 2536-2540.
99. Jeltsch, A., Nellen, W. and Lyko, F. (2006) Two substrates are better than one: dual specificities for Dnmt2 methyltransferases. Trends Biochem. Sci., 31, 306-308.
100. Dong, A., Yoder, J.A., Zhang, X., Zhou, L., Bestor, T.H. and Cheng, X. (2001) Structure of human DNMT2, an enigmatic DNA methyltransferase homolog that displays denaturant-resistant binding to DNA. Nucleic Acids Res., 29, 439-448.
101. Goll, M.G. and Bestor, T.H. (2005) Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem., 74, 481-514.
102. Asp by the DNA methyltransferase homolog Dnmt2. Science, 311, 395-398.
103. Phalke, S., Nickel, O., Walluscheck, D., Hortig, F., Onorati, M.C. and Reuter, G. (2009) Retrotransposon silencing and telomere integrity in somatic cells of Drosophila depends on the cytosine-5 methyltransferase DNMT2. Nat. Genet., 41, 696-702.
104. Ochs, R.L., Reilly, M.T., Freeman, J.W. and Busch, H. (1988) Intranucleolar localization of human proliferating cell nucleolar antigen p120. Cancer Res., 48, 6523-6529.
105. Schaefer, M., Steringer, J.P. and Lyko, F. (2008) The Drosophila cytosine-5 methyltransferase Dnmt2 is associated with the nuclear matrix and can access DNA during mitosis. PLoS ONE, 3, e1414.
106. 5C DNA methyl transferases use different cysteine residues as catalysts. Proc. Natl Acad. Sci. USA, 97, 8263-8265.
107. Asp molecules using a DNA methyltransferase-like catalytic mechanism. RNA, 14, 1663-1670.
108. Redman, K.L. (2006) Assembly of protein-RNA complexes using natural RNA and mutant forms of an RNA cytosine methyltransferase. Biomacromolecules, 7, 3321-3326.
109. Helm, M. (2006) Post-transcriptional nucleotide modification and alternative folding of RNA. Nucleic Acids Res., 34, 721-733.
110. 2+ and a conformational transition at the anticodon stem-loop of yeast phenylalanine tRNA. Biochemistry, 32, 10249-10253.
111. Phe anticodon domain. Nat. Struct. Biol., 3, 38-44.
112. Phe. J. Mol. Biol., 334, 901-918.
113. Met in S. cerevisiae. Genes Dev., 18, 1227-1240.
114. Alexandrov, A., Chernyakov, I., Gu, W., Hiley, S.L., Hughes, T.R., Grayhack, E.J. and Phizicky, E.M. (2006) Rapid tRNA decay can result from lack of nonessential modifications. Mol. Cell, 21, 87-96.
115. Chernyakov, I., Whipple, J.M., Kotelawala, L., Grayhack, E.J. and Phizicky, E.M. (2008) Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 5′-3′ exonucleases Rat1 and Xrn1. Genes Dev., 22, 1369-1380.
116. Strobel, M.C. and Abelson, J. (1986) Effect of intron mutations on processing and function of Saccharomyces cerevisiae SUP53 tRNA in vitro and in vivo. Mol. Cell. Biol., 6, 2663-2673.
117. Vicens, Q. and Westhof, E. (2001) Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site. Strucure, 9, 647-658.
118. Kariko, K., Buckstein, M., Ni, H. and Weissman, D. (2005) Suppression of RNA recognition by Toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity, 23, 165-175.
119. Rassoulzadegan, M., Grandjean, V., Gounon, P., Vincent, S., Gillot, I. and Cuzin, F. (2006) RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature, 441, 469-474.
120. Suzuki, M.M. and Bird, A. (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet., 9, 465-476.
121. Huang, Y., Ji, L., Huang, Q., Vassylyev, D.G., Chen, X. and Ma, J.B. (2009) Structural insights into mechanisms of the small RNA methyltransferase HEN1. Nature, 461, 823-827.
122. Rai, K., Chidester, S., Zavala, C.V., Manos, E.J., James, S.R., Karpf, A.R., Jones, D.A. and Cairns, B.R. (2007) Dnmt2 functions in the cytoplasm to promote liver, brain, and retina development in zebrafish. Genes Dev., 21, 261-266.