Identification of novel methyltransferases, Bmt5 and Bmt6, responsible for the m3U methylations of 25S rRNA in Saccharomyces cerevisiae

Nucleic Acids Research

Volumn 42, Issue 5, 2014, Pages 3246-3260

  Sharma, Sunny ^a   Yang, Jun ^a   Düttmann, Simon ^a   Watzinger, Peter ^a   Kötter, Peter ^a   Entian, Karl Dieter ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOMYCIN; PAROMOMYCIN; RIBOSOME RNA; RNA 25S; RNA METHYLTRANSFERASE; UNCLASSIFIED DRUG;

ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; BMT5 GENE; BMT6 GENE; CELLULAR DISTRIBUTION; CYTOPLASM; DELETION MUTANT; FUNGAL CELL; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; GENE DELETION; GENE EXPRESSION; GENE LOCATION; GENE MUTATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; RNA ISOLATION; RNA METHYLATION; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS;

GENE DELETION; METHYLATION; METHYLTRANSFERASES; NUCLEAR PROTEINS; RNA, RIBOSOMAL; S-ADENOSYLMETHIONINE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; URIDINE;

EID: 84898930928     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1281     Document Type: Article

References (38)

1. Ben-Shem, A., Garreau de Loubresse, N., Melnikov, S., Jenner, L., Yusupova, G. and Yusupov, M. (2011) The structure of the eukaryotic ribosome at 3.0 A resolution. Science, 334, 1524-1529.
2. Lilley, D.M. (2001) The ribosome functions as a ribozyme. Chembiochem, 2, 31-35. (Pubitemid 33722524
3. Klootwijk, J. and Planta, R.J. (1973) Analysis of the methylation sites in yeast ribosomal RNA. Eur. J. Biochem., 39, 325-333.
4. Brand, R.C., Klootwijk, J., Van Steenbergen, T.J., De Kok, A.J. and Planta, R.J. (1977) Secondary methylation of yeast ribosomal precursor RNA. Eur. J. Biochem., 75, 311-318.
5. Decatur, W.A. and Fournier, M.J. (2002) rRNA modifications and ribosome function. Trends Biochem. Sci., 27, 344-351.
6. Kos, M. and Tollervey, D. (2010) Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol. Cell, 37, 809-820.
7. 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. (Pubitemid 351149718
8. Sharma, S., Yang, J., Watzinger, P., Kötter, P. and Entian, K.-D. (2013) Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively. Nucleic Acids Res., 41, 9062-9076.
9. Schubert, H.L., Blumenthal, R.M. and Cheng, X. (2003) Many paths to methyltransfer: A chronicle of convergence. Trends Biochem. Sci., 28, 329-335.
10. Martin, J.L. and McMillan, F.M. (2002) SAM (dependent) I AM: The S-Adenosylmethionine-dependent methyltransferase fold. Curr. Opin. Struct. Biol., 12, 783-793.
11. Taylor, A.B., Meyer, B., Leal, B.Z., Kotter, P., Schirf, V., Demeler, B., Hart, P.J., Entian, K.D. and Wohnert, J. (2008) The crystal structure of Nep1 reveals an extended SPOUT-class methyltransferase fold and a pre-organized SAM-binding site. Nucleic Acids Res., 36, 1542-1554. (Pubitemid 351426107
12. Peifer, C., Sharma, S., Watzinger, P., Lamberth, S., Kotter, P. and Entian, K.D. (2013) Yeast Rrp8p, a novel methyltransferase responsible for m1A 645 base modification of 25S rRNA. Nucleic Acids Res., 41, 1151-1163.
13. Sharma, S., Watzinger, P., Kötter, P. and Entian, K.-D. (2013) Identification of a novel methyltransferase, Bmt2, responsible for the N-1-methyl-Adenosine base modification of 25S rRNA in Saccharomyces cerevisiae. Nucleic Acids Res., 41, 5428-5443.
14. Meyer, B., Wurm, J.P., Kotter, P., Leisegang, M.S., Schilling, V., Buchhaupt, M., Held, M., Bahr, U., Karas, M., Heckel, A. et al. (2011) The Bowen-Conradi syndrome protein Nep1 (Emg1) has a dual role in eukaryotic ribosome biogenesis, as an essential assembly factor and in the methylation of 1191 in yeast 18S rRNA. Nucleic Acids Res., 39, 1526-1537.
15. Wurm, J.P., Meyer, B., Bahr, U., Held, M., Frolow, O., Kotter, P., Engels, J.W., Heckel, A., Karas, M., Entian, K.D. et al. (2010) The ribosome assembly factor Nep1 responsible for Bowen-Conradi syndrome is a pseudouridine-N1-specific methyltransferase. Nucleic Acids Res., 38, 2387-2398.
16. Lafontaine, D., Delcour, J., Glasser, A.L., Desgrè s, J. and Vandenhaute, J. (1994) The DIM1 gene responsible for the conserved m6(2)Am6(2)A dimethylation in the 30-Terminal loop of 18 S rRNA is essential in yeast. J. Mol. Biol., 241, 492-497.
17. White, J., Li, Z., Sardana, R., Bujnicki, J.M., Marcotte, E.M. and Johnson, A.W. (2008) Bud23 methylates G1575 of 18S rRNA and is required for efficient nuclear export of pre-40S subunits. Mol. Cell. Biol., 28, 3151-3161.
18. Khanna-Gupta, A. (2006) p120 nucleolar-proliferating antigen is a direct target of G-CSF signaling during myeloid differentiation. J. Leukoc. Biol., 79, 1011-1021.
19. Yang, L., Song, T., Chen, L., Kabra, N., Zheng, H., Koomen, J., Seto, E. and Chen, J. (2013) Regulation of SirT1-NML binding by rRNA coordinates ribosome biogenesis with nutrient availability. Mol. Cell. Biol., 33, 3838-3848.
20. 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.
21. Bakin, A., Lane, B.G. and Ofengand, J. (1994) Clustering of pseudouridine residues around the peptidyltransferase center of yeast cytoplasmic and mitochondrial ribosomes. Biochemistry, 33, 13475-13483. (Pubitemid 24373264
22. Lapeyre, B. and Purushothaman, S.K. (2004) Spb1p-directed formation of Gm2922 in the ribosome catalytic center occurs at a late processing stage. Mol. Cell, 16, 663-669.
23. Gehrke, C.W. and Kuo, K.C. (1989) Ribonucleoside analysis by reversed-phase high-performance liquid chromatography. J. Chromatogr., 471, 3-36. (Pubitemid 19144813
24. Gehrke, C.W. and Kuo, K.C.T. (1989) Analytical Methods for Major and Modified Nucleosides-HPLC, GC, MS, NMR, UV and FT-IR. Elsevier; Distributors for the U.S. and Canada Elsevier Science Pub. Co Amsterdam, New York, NY, USA.
25. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M. and Séraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol., 17, 1030-1032.
26. Huh, W.-K., Falvo, J.V., Gerke, L.C., Carroll, A.S., Howson, R.W., Weissman, J.S. and O'Shea, E.K. (2003) Global analysis of protein localization in budding yeast. Nature, 425, 686-691. (Pubitemid 37314307
27. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
28. 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. (Pubitemid 12136788
29. Kelley, L.A. and Sternberg, M.J.E. (2009) Protein structure prediction on the Web: A case study using the Phyre server. Nat. Protoc., 4, 363-371.
30. Fatica, A., Cronshaw, A.D., Dlakić, M. and Tollervey, D. (2002) Ssf1p prevents premature processing of an early pre-60S ribosomal particle. Mol. Cell, 9, 341-351.
31. Nordlund, M.E., Johansson, J.O., von Pawel-Rammingen, U. and Byström, A.S. (2000) Identification of the TRM2 gene encoding the tRNA(m5U54)methyltransferase of Saccharomyces cerevisiae. RNA, 6, 844-860.
32. Cavaluzzi, M.J. (2004) Revised UV extinction coefficients for nucleoside-50-monophosphates and unpaired DNA and RNA. Nucleic Acids Res., 32, e13.
33. Jenner, L., Melnikov, S., de Loubresse, N.G., Ben-Shem, A., Iskakova, M., Urzhumtsev, A., Meskauskas, A., Dinman, J., Yusupova, G. and Yusupov, M. (2012) Crystal structure of the 80S yeast ribosome. Curr. Opin. Struct. Biol., 22, 759-767.
34. Yi, C. and Pan, T. (2011) Cellular dynamics of RNA modification. Acc. Chem. Res., 44, 1380-1388.
35. Bradatsch, B., Leidig, C., Granneman, S., Gnädig, M., Tollervey, D., Böttcher, B., Beckmann, R. and Hurt, E. (2012) Structure of the pre-60S ribosomal subunit with nuclear export factor Arx1 bound at the exit tunnel. Nat. Struct. Mol. Biol., 19, 1234-1241.
36. Perez-Fernandez, J., Roman, A., Las Rivas, De, J., Bustelo, X.R. and Dosil, M. (2007) The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol. Cell. Biol., 27, 5414-5429.
37. Auxilien, S., Rasmussen, A., Rose, S., Brochier-Armanet, C., Husson, C., Fourmy, D., Grosjean, H. and Douthwaite, S. (2011) Specificity shifts in the rRNA and tRNA nucleotide targets of archaeal and bacterial m5U methyltransferases. RNA, 17, 45-53.
38. Maden, B. (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.