Trm112 is required for Bud23-mediated methylation of the 18S rRNA at position G1575

Molecular and Cellular Biology

Volumn 32, Issue 12, 2012, Pages 2254-2267

  Figaro, Sabine ^a   Wacheul, Ludivine ^b   Schillewaert, Stéphanie ^b   Graille, Marc ^c   Huvelle, Emmeline ^a   Mongeard, Rémi ^a   Zorbas, Christiane ^b   Lafontaine, Denis L J ^b   Heurgué Hamard, Valérie ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BUD23 ENZYME; FUNGAL PROTEIN; METHYLTRANSFERASE; PROTEIN TRM112; RNA 18S; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; NONHUMAN; PRIORITY JOURNAL; RNA METHYLATION; SACCHAROMYCES CEREVISIAE; SMALL RIBOSOMAL SUBUNIT;

GUANINE; METHYLATION; METHYLTRANSFERASES; PROTEIN METHYLTRANSFERASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, RIBOSOMAL, 18S; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRNA METHYLTRANSFERASES;

SACCHAROMYCES CEREVISIAE;

EID: 84864000733     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06623-11     Document Type: Article

References (66)

1. Brunger AT. 2007. Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2:2728-2733.
2. Chern MK, et al. 2009. Single-step protein purification by back flush in ion exchange chromatography. Anal. Biochem. 392:174-176.
3. Colau G, Thiry M, Leduc V, Bordonné R, Lafontaine DLJ. 2004. The small nucle(ol)ar RNA cap trimethyltransferase is required for ribosome synthesis and intact nucleolar morphology. Mol. Cell. Biol. 24:7976-7986.
4. Colley A, Beggs J, Tollervey D, Lafontaine DLJ. 2000. Dhr1p, a putative DEAH-box RNA helicase, is associated with the box C+D snoRNA U3. Mol. Cell. Biol. 20:7238-7246.
5. Decatur WA, Fournier MJ. 2002. rRNA modifications and ribosome function. Trends Biochem. Sci. 27:344-351.
6. Dez C, Dlakic M, Tollervey D. 2007. Roles of the HEAT repeat proteins Utp10 and Utp20 in 40S ribosome maturation. RNA 13:1516-1527.
7. Dutca LM, Gallagher JE, Baserga SJ. 23 February 2011. The initial U3 snoRNA:pre-rRNA base pairing interaction required for pre-18S rRNA folding revealed by in vivo chemical probing. Nucleic Acids Res. doi: 10.1093/nar/gkr044.
8. Finkbeiner E, Haindl M, Muller S. 2011. The SUMO system controls nucleolar partitioning of a novel mammalian ribosome biogenesis complex. EMBO J. 30:1067-1078.
9. Gadal O, et al. 2002. Rlp7p is associated with 60S preribosomes, restricted to the granular component of the nucleolus, and required for pre-rRNA processing. J. Cell Biol. 157:941-951.
10. Gérus M, Caizergues-Ferrer M, Henry Y, Henras AK. Crosstalk between ribosome synthesis and cell cycle and its potential implications in human diseases. In Olson MO (ed), The nucleolus, protein reviews, in press. Springer.
11. Ghaemmaghami S, et al. 2003. Global analysis of protein expression in yeast. Nature 425:737-741.
12. Grandi P, et al. 2002. 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell 10:105-115.
13. Henras AK, et al. 2008. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65:2334-2359.
14. Heurgué-Hamard V, et al. 2005. The glutamine residue of the conserved GGQ motif in Saccharomyces cerevisiae release factor eRF1 is methylated by the product of the YDR140w gene. J. Biol. Chem. 280:2439-2445.
15. 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. 281:36140-36148.
16. Hu Z, et al. 2010. The Arabidopsis SMO2, a homologue of yeast TRM112, modulates progression of cell division during organ growth. Plant J. 61: 600-610.
17. Huh WK, et al. 2003. Global analysis of protein localization in budding yeast. Nature 425:686-691.
18. Hurt E, et al. 1999. A novel in vivo assay reveals inhibition of ribosomal nuclear export in ran-cycle and nucleoporin mutants. J. Cell Biol. 144: 389-401.
19. Jorgensen P, Tyers M, Warner JR. 2004. Forging the factory: ribosome synthesis and growth control in budding yeast, p 329-370. In Hall MN, Raff M, Thomas G (ed), Cell growth: control of cell size. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Kalhor HR, Clarke S. 2003. Novel methyltransferase for modified uridine residues at the wobble position of tRNA. Mol. Cell. Biol. 23:9283-9292.
21. Karbstein K. 2011. Inside the 40S ribosome assembly machinery. Curr. Opin. Chem. Biol. 15:657-663.
22. King TH, Liu B, McCully RR, Fournier MJ. 2003. Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol. Cell 11:425-435.
23. Kiss T, Fayet-Lebaron E, Jady BE. 2010. Box H/ACA small ribonucleoproteins. Mol. Cell 37:597-606.
24. Krogan NJ, et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440:637-643.
25. Krogan NJ, et al. 2004. High-definition macromolecular composition of yeast RNA-processing complexes. Mol. Cell 13:225-239.
26. Lafontaine DLJ. 2010. A 'garbage can' for ribosomes: how eukaryotes degrade their ribosomes? Trends Biochem. Sci. 35:267-277.
27. Lafontaine DLJ, Preiss T, Tollervey D. 1998. Yeast 18S rRNA dimethylase Dim1p: a quality control mechanism in ribosome synthesis? Mol. Cell. Biol. 18:2360-2370.
28. Lafontaine DLJ, Vandenhaute J, Tollervey D. 1995. The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev. 9:2470-2481.
29. Leporé L, Lafontaine DLJ. 2011. A functional interface at the rDNA connects rRNA synthesis, pre-rRNA processing and nucleolar surveillance in budding yeast. PLoS One 6:e24962. doi:10.1371/journal.pone.0024962.
30. 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. 36:629-639.
31. Liang XH, Liu Q, Fournier MJ. 2007. rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity. Mol. Cell 28:965-977.
32. Liger D, et al. 7 April 2011. Mechanism of activation of methyltransferases involved in translation by the Trm112 'hub' protein. Nucleic Acids Res. doi:10.1093/nar/gkr176.
33. Lo KY, Li Z, Wang F, Marcotte EM, Johnson AW. 2009. Ribosome stalk assembly requires the dual-specificity phosphatase Yvh1 for the exchange of Mrt4 with P0. J. Cell Biol. 186:849-862.
34. Luka Z, Pakhomova S, Luka Y, Newcomer ME, Wagner C. 2007. Destabilization of human glycine N-methyltransferase by H176N mutation. Protein Sci. 16:1957-1964.
35. Marmier-Gourrier N, Clery A, Schlotter F, Senty-Segault V, Branlant C. 2011. A second base pair interaction between U3 small nucleolar RNA and the 5=-ETS region is required for early cleavage of the yeast pre-ribosomal RNA. Nucleic Acids Res. 39:9731-9745.
36. Mazauric MH, Dirick L, Purushothaman SK, Bjork 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. 285:18505-18515.
37. Milkereit P, et al. 2003. A Noc complex specifically involved in the formation and nuclear export of ribosomal 40 S subunits. J. Biol. Chem. 278:4072-4081.
38. Mullineux ST, Lafontaine DL. 2012. Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie http://dx.doi.org/10 .1016/j.biochi.2012.02.001.
39. Nishimura K, et al. 2007. Identification of the RsmG methyltransferase target as 16S rRNA nucleotide G527 and characterization of Bacillus subtilis rsmG mutants. J. Bacteriol. 189:6068-6073.
40. Oeffinger M, et al. 2007. Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 4:951-956.
41. Ohbayashi I, Konishi M, Ebine K, Sugiyama M. 2011. Genetic identification of Arabidopsis RID2 as an essential factor involved in pre-rRNA processing. Plant J. 67:49-60.
42. Pang CN, Gasteiger E, Wilkins MR. 2010. Identification of arginine- and lysine-methylation in the proteome of Saccharomyces cerevisiae and its functional implications. BMC Genomics 11:92.
43. Panse VG, Johnson AW. 2010. Maturation of eukaryotic ribosomes: acquisition of functionality. Trends Biochem. Sci. 35:260-266.
44. Panse VG, et al. 2006. Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic 7:1311-1321.
45. Pawlowski M, Gajda MJ, Matlak R, Bujnicki JM. 2008. MetaMQAP: ameta-server for the quality assessment of protein models. BMC Bioinformatics 9:403.
46. Phipps KR, Charette JM, Baserga SJ. 2011. The SSU processome in ribosome biogenesis-progress and prospects. Wiley Interdiscip. Rev. RNA 2:1-21.
47. Piekna-Przybylska D, Decatur WA, Fournier MJ. 2008. The 3D rRNA modification maps database: with interactive tools for ribosome analysis. Nucleic Acids Res. 36:D178-D183.
48. Polevoda B, Sherman F. 2007. Methylation of proteins involved in translation. Mol. Microbiol. 65:590-606.
49. 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. 25:4359-4370.
50. Rodríguez-Mateos M, et al. 2009. Role and dynamics of the ribosomal protein P0 and its related trans-acting factor Mrt4 during ribosome assembly in Saccharomyces cerevisiae. Nucleic Acids Res. 37:7519-7532.
51. Roy A, Kucukural A, Zhang Y. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5:725-738.
52. Schafer T, et al. 2006. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441:651-655.
53. Schillewaert S, Wacheul L, Lhomme F, Lafontaine DLJ. 2012. The evolutionarily conserved protein LAS1 is required for pre-rRNA processing at both ends of ITS2. Mol. Cell. Biol. 32:430-444.
54. Schubert HL, Blumenthal RM, Cheng X. 2003. Many paths to methyltransfer: a chronicle of convergence. Trends Biochem. Sci. 28:329-335.
55. Senger B, et al. 2001. The nucle(ol)ar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol. Cell 8:1363-1373.
56. Strunk BS, Karbstein K. 2009. Powering through ribosome assembly. RNA 15:2083-2104.
57. Strunk BS, et al. 2011. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333:1449-1453.
58. Studte P, et al. 2008. tRNA and protein methylase complexes mediate zymocin toxicity in yeast. Mol. Microbiol. 69:1266-1277.
59. Taddei A, Schober H, Gasser SM. 16 June 2010. The budding yeast nucleus. Cold Spring Harb. Perspect. Biol. 2:a000612. doi:10.1101/ cshperspect.a000612.
60. Thiry M, Lamaye F, Lafontaine DLJ. 2011. The nucleolus: when two became three. Nucleus 2:289-293.
61. Warner JR. 1999. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24:437-440.
62. Wery M, Ruidant S, Schillewaert S, Lepore N, Lafontaine DLJ. 2009. The nuclear poly(A) polymerase and Exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA 15:406-419.
63. Westman BJ, et al. 2010. A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol. Cell 39:618-631.
64. 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. 28:3151-3161.
65. Yi C, Pan T. 2011. Cellular dynamics of RNA modification. Acc. Chem. Res. 44:1380-1388.
66. Zhang J, et al. 2007. Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes Dev. 21:2580-2592.