Structural and functional studies of Bud23-Trm112 reveal 18S rRNA N7-G1575 methylation occurs on late 40S precursor ribosomes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 51, 2014, Pages E5518-E5526

  Létoquart, Juliette ^a   Huvelle, Emmeline ^b   Wacheul, Ludivine ^c   Bourgeois, Gabrielle ^a   Zorbas, Christiane ^c   Graille, Marc ^a   Heurgué Hamard, Valérie ^b   Lafontaine, Denis L J ^c,d  

^a LABORATOIRE DE BIOCHIMIE   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c Center for Microscopy and Molecular Imaging   (Belgium)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Methyltransferase; Ribosome synthesis; rRNA modifying enzyme; S adenosyl L methionine; Translation

Indexed keywords

2 DIMETHYLAMINO 5,6 DIHYDROXYTETRALIN; 7 METHYLGUANOSINE; BUD23 PROTEIN; RIBOSOME PROTEIN; RNA 18S; RNA HELICASE; RNA PRECURSOR; S ADENOSYLMETHIONINE; SMALL NUCLEOLAR RNA; TRM112 PROTEIN; UNCLASSIFIED DRUG; XANTHOSINE; ZINC FINGER PROTEIN; BUD23 PROTEIN, S CEREVISIAE; METHYLTRANSFERASE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSFER RNA METHYLTRANSFERASE; TRM112 PROTEIN, S CEREVISIAE;

ARTICLE; COFFEA CANEPHORA; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVITY; HYDROPHOBICITY; NONHUMAN; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RIBOSOME; RNA CONFORMATION; RNA METHYLATION; RNA PROCESSING; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE; SMALL RIBOSOMAL SUBUNIT; YEAST; CATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; METHYLATION; PROTEIN CONFORMATION;

COFFEA CANEPHORA; EUKARYOTA;

CATALYSIS; METHYLATION; METHYLTRANSFERASES; MODELS, MOLECULAR; PROTEIN CONFORMATION; RIBOSOMES; RNA, RIBOSOMAL, 18S; SACCHAROMYCES CEREVISIAE PROTEINS; TRNA METHYLTRANSFERASES;

EID: 84919933439     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1413089111     Document Type: Article

References (39)

1. Woolford JL, Jr, Baserga SJ (2013) Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195(3):643-681.
2. Henras A, Plisson-Chastang C, O'Donohue M-F, Chakraborthy A, Gleizes P-E (2014) Overview of pre-rRNA processing in eukaryotes. WIREs RNA, 10.1002/wrna.1269.
3. Thomson E, Ferreira-Cerca S, Hurt E (2013) Eukaryotic ribosome biogenesis at a glance. J Cell Sci 126(Pt 21):4815-4821.
4. Lafontaine DLJ, Non-coding RNAs in eukaryotic ribosome synthesis and function. Nat Struct Mol Biol 21, in press.
5. Motorin Y, Helm M (2011) RNA nucleotide methylation. Wiley Interdiscip Rev RNA 2(5):611-631.
6. Watkins NJ, Bohnsack MT (2012) The box C/D and H/ACA snoRNPs: Key players in the modification, processing and the dynamic folding of ribosomal RNA. Wiley Interdiscip Rev RNA 3(3):397-414.
7. Lafontaine D, Vandenhaute J, Tollervey D (1995) The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev 9(20):2470-2481.
8. White J, et al. (2008) Bud23 methylates G1575 of 18S rRNA and is required for efficient nuclear export of pre-40S subunits. Mol Cell Biol 28(10):3151-3161.
9. Leulliot N, Bohnsack MT, Graille M, Tollervey D, Van Tilbeurgh H (2008) The yeast ribosome synthesis factor Emg1 is a novel member of the superfamily of alpha/beta knot fold methyltransferases. Nucleic Acids Res 36(2):629-639.
10. Ishitani R, Yokoyama S, Nureki O (2008) Structure, dynamics, and function of RNA modification enzymes. Curr Opin Struct Biol 18(3):330-339.
11. Schubert HL, Blumenthal RM, Cheng X (2003) Many paths to methyltransfer: A chronicle of convergence. Trends Biochem Sci 28(6):329-335.
12. Peifer C, et al. (2013) Yeast Rrp8p, a novel methyltransferase responsible for m1A 645 base modification of 25S rRNA. Nucleic Acids Res 41(2):1151-1163.
13. Sharma S, et al. (2014) Identification of novel methyltransferases, Bmt5 and Bmt6, responsible for the m3U methylations of 25S rRNA in Saccharomyces cerevisiae. Nucleic Acids Res 42(5):3246-3260.
14. Sharma S, Yang J, Watzinger P, Kötter P, Entian KD (2013) Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively. Nucleic Acids Res 41(19): 9062-9076.
15. Sharma S, Watzinger P, Kötter P, Entian KD (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(10):5428-5443.
16. Meyer B, 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 Ψ1191 in yeast 18S rRNA. Nucleic Acids Res 39(4):1526-1537.
17. Figaro S, et al. (2012) Trm112 is required for Bud23-mediated methylation of the 18S rRNA at position G1575. Mol Cell Biol 32(12):2254-2267.
18. Sardana R, White JP, Johnson AW (2013) The rRNA methyltransferase Bud23 shows functional interaction with components of the SSU processome and RNase MRP. RNA 19(6):828-840.
19. Lafontaine DLJ, Preiss T, Tollervey D (1998) Yeast 18S rRNA dimethylase Dim1p: A quality control mechanism in ribosome synthesis? Mol Cell Biol 18(4):2360-2370.
20. Heurgué-Hamard V, et al. (2006) The zinc finger protein Ynr046w is plurifunctional and a component of the eRF1 methyltransferase in yeast. J Biol Chem 281(47): 36140-36148.
21. Mazauric MH, Dirick L, Purushothaman SK, Björk GR, Lapeyre B (2010) Trm112p is a 15-kDa zinc finger protein essential for the activity of two tRNA and one protein methyltransferases in yeast. J Biol Chem 285(24):18505-18515.
22. Purushothaman SK, Bujnicki JM, Grosjean H, Lapeyre B (2005) Trm11p and Trm112p are both required for the formation of 2-methylguanosine at position 10 in yeast tRNA. Mol Cell Biol 25(11):4359-4370.
23. Phipps KR, Charette J, Baserga SJ (2011) The small subunit processome in ribosome biogenesis - progress and prospects. Wiley Interdiscip Rev RNA 2(1):1-21.
24. Sardana R, Zhu J, Gill M, Johnson AW (2014) Physical and functional interaction between the methyltransferase Bud23 and the essential DEAH-box RNA helicase Ecm16. Mol Cell Biol 34(12):2208-2220.
25. Colley A, Beggs JD, Tollervey D, Lafontaine DLJ (2000) Dhr1p, a putative DEAH-box RNA helicase, is associated with the box C+D snoRNP U3. Mol Cell Biol 20(19): 7238-7246.
26. Õunap K, Käsper L, Kurg A, Kurg R (2013) The human WBSCR22 protein is involved in the biogenesis of the 40S ribosomal subunits in mammalian cells. PLoS ONE 8(9): e75686.
27. Tafforeau L, et al. (2013) The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors. Mol Cell 51(4):539-551.
28. Nakazawa Y, Arai H, Fujita N (2011) The novel metastasis promoter Merm1/Wbscr22 enhances tumor cell survival in the vasculature by suppressing Zac1/p53-dependent apoptosis. Cancer Res 71(3):1146-1155.
29. Tiedemann RE, et al. (2012) Identification of molecular vulnerabilities in human multiple myeloma cells by RNA interference lethality screening of the druggable genome. Cancer Res 72(3):757-768.
30. Doll A, Grzeschik KH (2001) Characterization of two novel genes, WBSCR20 and WBSCR22, deleted in Williams-Beuren syndrome. Cytogenet Cell Genet 95(1-2):20-27.
31. Liger D, et al. (2011) Mechanism of activation of methyltransferases involved in translation by the Trm112 ' hub' protein. Nucleic Acids Res 39(14):6249-6259.
32. Holm L, Rosenstrom P (2010) Dali server: Conservation mapping in 3D. Nucleic Acids Res 38(Web Server issue):W545-549.
33. Schmitt E, Galimand M, Panvert M, Courvalin P, Mechulam Y (2009) Structural bases for 16 S rRNA methylation catalyzed by ArmA and RmtB methyltransferases. J Mol Biol 388(3):570-582.
34. Fabrega C, Hausmann S, Shen V, Shuman S, Lima CD (2004) Structure and mechanism of mRNA cap (guanine-N7) methyltransferase. Mol Cell 13(1):77-89.
35. McCarthy AA, McCarthy JG (2007) The structure of two N-methyltransferases from the caffeine biosynthetic pathway. Plant Physiol 144(2):879-889.
36. Ben-Shem A, et al. (2011) The structure of the eukaryotic ribosome at 3.0 A˚ resolution. Science 334(6062):1524-1529.
37. Motorin Y, Muller S, Behm-Ansmant I, Branlant C (2007) Identification of modified residues in RNAs by reverse transcription-based methods. Methods Enzymol 425: 21-53.
38. Das K, et al. (2004) Crystal structure of RlmAI: Implications for understanding the 23S rRNA G745/G748-methylation at the macrolide antibiotic-binding site. Proc Natl Acad Sci USA 101(12):4041-4046.
39. Martin JL, McMillan FM (2002) SAM (dependent) I AM: The S-adenosylmethionine-dependent methyltransferase fold. Curr Opin Struct Biol 12(6):783-793.