Histidine Methylation of Yeast Ribosomal Protein Rpl3p Is Required for Proper 60S Subunit Assembly

REFERENCES

• Lapeyre B. 2005. Conserved ribosomal RNA modification and their putative roles in ribosome biogenesis and translation, p 263–284. In Grosjean H (ed), Fine-tuning of RNA functions by modification and editing. Springer, Berlin, Germany.
   Google Scholar
• Johansson MO, Byström A. 2005. Transfer RNA modifications and modifying enzymes in Saccharomyces cerevisiae, p 87–120. In Grosjean H (ed), Fine-tuning of RNA functions by modification and editing. Springer, Berlin, Germany.
   Google Scholar
• Bokar J. 2005. The biosynthesis and functional roles of methylated nucleosides in eukaryotic mRNA, p 141–177. In Grosjean H (ed), Fine-tuning of RNA functions by modification and editing. Springer, Berlin, Germany.
   Google Scholar
• Polevoda B, Sherman F. 2007. Methylation of proteins involved in translation. Mol. Microbiol. 65:590–606. http://dx.doi.org/10.1111/j.1365-2958.2007.05831.x.
   PubMedGoogle Scholar
• Katz JE, Dlakic M, Clarke SG. 2003. Automated identification of putative methyltransferases from genomic open reading frames. Mol. Cell. Proteomics 2:525–540.
   PubMed Web of Science ®Google Scholar
• Petrossian TC, Clarke SG. 2009. Multiple motif scanning to identify methyltransferases from the yeast proteome. Mol. Cell. Proteomics 8:1516–1526. http://dx.doi.org/10.1074/mcp.M900025-MCP200.
   PubMedGoogle Scholar
• Wlodarski T, Kutner J, Towpik J, Knizewski L, Rychlewski L, Kudlicki A, Rowicka M, Dziembowski A, Ginalski K. 2011. Comprehensive structural and substrate specificity classification of the Saccharomyces cerevisiae methyltransferome. PLoS One 6:e23168. http://dx.doi.org/10.1371/journal.pone.0023168.
   PubMed Web of Science ®Google Scholar
• Clarke SG. 2013. Protein methylation at the surface and buried deep: thinking outside the histone box. Trends Biochem. Sci. 38:243–252. http://dx.doi.org/10.1016/j.tibs.2013.02.004.
   PubMed Web of Science ®Google Scholar
• Decatur WA, Fournier MJ. 2002. rRNA modifications and ribosome function. Trends Biochem. Sci. 27:344–351. http://dx.doi.org/10.1016/S0968-0004(02)02109-6.
   PubMed Web of Science ®Google Scholar
• Motorin Y, Helm M. 2010. tRNA stabilization by modified nucleotides. Biochemistry 49:4934–4944. http://dx.doi.org/10.1021/bi100408z.
   PubMed Web of Science ®Google Scholar
• Suzuki T. 2005. Biosynthesis and function of tRNA wobble modifications, p 23–69. In Grosjean H (ed), Fine-tuning of RNA functions by modification and editing. Springer, Berlin, Germany.
   Google Scholar
• Dinçbas-Renqvist V, Engstrom A, Mora L, Heurgué-Harnard V, Buckingham R, Ehrenberg M. 2000. A post-translational modification in the GGQ motif of RF2 from Escherichia coli stimulates termination of translation. EMBO J. 19:6900–6907. http://dx.doi.org/10.1093/emboj/19.24.6900.
   PubMedGoogle Scholar
• Heurgué-Hamard V, Champ S, Engstrom A, Ehrenberg M, Buckingham RH. 2002. The hemK gene in Escherichia coli encodes the N5-glutamine methyltransferase that modifies peptide release factors. EMBO J. 21:769–778. http://dx.doi.org/10.1093/emboj/21.4.769.
   PubMedGoogle Scholar
• Lee SW, Berger SJ, Martinovic S, Pasa-Tolic L, Anderson GA, Shen Y, Zhao R, Smith RD. 2002. Direct mass spectrometric analysis of intact proteins of the yeast large ribosomal subunit using capillary LC/FTICR. Proc. Natl. Acad. Sci. U. S. A. 99:5942–5947. http://dx.doi.org/10.1073/pnas.082119899.
   PubMed Web of Science ®Google Scholar
• Webb KJ, Al-Hadid Q, Zurita-Lopez CI, Young BD, Lipson RS, Clarke SG. 2011. The ribosomal l1 protuberance in yeast is methylated on a lysine residue catalyzed by a seven-beta-strand methyltransferase. J. Biol. Chem. 286:18405–18413. http://dx.doi.org/10.1074/jbc.M110.200410.
   PubMedGoogle Scholar
• Webb KJ, Zurita-Lopez CI, Al-Hadid Q, Laganowsky A, Young BD, Lipson RS, Souda P, Faull KF, Whitelegge JP, Clarke SG. 2010. A novel 3-methylhistidine modification of yeast ribosomal protein Rpl3 is dependent upon the YIL110W methyltransferase. J. Biol. Chem. 285:37598–37606. http://dx.doi.org/10.1074/jbc.M110.170787.
   PubMedGoogle Scholar
• Porras-Yakushi TR, Whitelegge JP, Clarke S. 2006. A novel SET domain methyltransferase in yeast: Rkm2-dependent trimethylation of ribosomal protein L12ab at lysine 10. J. Biol. Chem. 281:35835–35845. http://dx.doi.org/10.1074/jbc.M606578200.
   PubMed Web of Science ®Google Scholar
• Chern MK, Chang KN, Liu LF, Tam TC, Liu YC, Liang YL, Tam MF. 2002. Yeast ribosomal protein L12 is a substrate of protein-arginine methyltransferase 2. J. Biol. Chem. 277:15345–15353. http://dx.doi.org/10.1074/jbc.M111379200.
   PubMedGoogle Scholar
• Porras-Yakushi TR, Whitelegge JP, Miranda TB, Clarke S. 2005. A novel SET domain methyltransferase modifies ribosomal protein Rpl23ab in yeast. J. Biol. Chem. 280:34590–34598. http://dx.doi.org/10.1074/jbc.M507672200.
   PubMed Web of Science ®Google Scholar
• Webb KJ, Laganowsky A, Whitelegge JP, Clarke SG. 2008. Identification of two SET domain proteins required for methylation of lysine residues in yeast ribosomal protein Rpl42ab. J. Biol. Chem. 283:35561–35568. http://dx.doi.org/10.1074/jbc.M806006200.
   PubMed Web of Science ®Google Scholar
• Webb KJ, Lipson RS, Al-Hadid Q, Whitelegge JP, Clarke SG. 2010. Identification of protein N-terminal methyltransferases in yeast and humans. Biochemistry 49:5225–5235. http://dx.doi.org/10.1021/bi100428x.
   PubMedGoogle Scholar
• Young BD, Weiss DI, Zurita-Lopez CI, Webb KJ, Clarke SG, McBride AE. 2012. Identification of methylated proteins in the yeast small ribosomal subunit: a role for SPOUT methyltransferases in protein arginine methylation. Biochemistry 51:5091–5104. http://dx.doi.org/10.1021/bi300186g.
   PubMed Web of Science ®Google Scholar
• Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M. 2011. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 334:1524–1529. http://dx.doi.org/10.1126/science.1212642.
   PubMed Web of Science ®Google Scholar
• Meskauskas A, Dinman JD. 2008. Ribosomal protein L3 functions as a ‘rocker switch' to aid in coordinating of large subunit-associated functions in eukaryotes and Archaea. Nucleic Acids Res. 36:6175–6186. http://dx.doi.org/10.1093/nar/gkn642.
   PubMedGoogle Scholar
• Lhoest J, Colson C. 1981. Cold-sensitive ribosome assembly in an Escherichia coli mutant lacking a single methyl group in ribosomal protein L3. Eur. J. Biochem. 121:33–37. http://dx.doi.org/10.1111/j.1432-1033.1981.tb06425.x.
   PubMedGoogle Scholar
• Cloutier P, Lavallee-Adam M, Faubert D, Blanchette M, Coulombe B. 2013. A newly uncovered group of distantly related lysine methyltransferases preferentially interact with molecular chaperones to regulate their activity. PLoS Genet. 9:e1003210. http://dx.doi.org/10.1371/journal.pgen.1003210.
   PubMed Web of Science ®Google Scholar
• Lowry OH, Rosebrough NJ, Farr NL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265–275.
   PubMed Web of Science ®Google Scholar
• Gary JD, Clarke S 1995. Purification and characterization of an isoaspartyl dipeptidase from Escherichia coli. J. Biol. Chem. 270:4076–4087.
   PubMedGoogle Scholar
• Chanfreau G, Rotondo G, Legrain P, Jacquier A. 1998. Processing of a dicistronic small nucleolar RNA precursor by the RNA endonuclease Rnt1. EMBO J. 17:3726–3737. http://dx.doi.org/10.1093/emboj/17.13.3726.
   PubMedGoogle Scholar
• Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Tollervey D, Lehtonen H, Carmo-Fonseca M, Hurt EC. 1991. The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 10:573–583.
   PubMed Web of Science ®Google Scholar
• Gietz RD, Woods RA. 2002. Transformation of yeast by the LiOAc/SS carrier DNA/PEG method. Methods Enzymol. 350:87–96. http://dx.doi.org/10.1016/S0076-6879(02)50957-5.
   PubMed Web of Science ®Google Scholar
• Keeling KM, Lanier J, Du M, Salas-Marco J, Gao L, Kaenjak-Angeletti A, Bedwell DM. 2004. Leaky termination at premature stop codons antagonizes nonsense-mediated mRNA decay in S. cerevisiae. RNA 10:691–703. http://dx.doi.org/10.1261/rna.5147804.
   PubMedGoogle Scholar
• Salas-Marco J, Bedwell DM. 2005. Discrimination between defect in elongation fidelity and termination efficiency provides mechanistic insights into translational readthrough. J. Mol. Biol. 348:801–815. http://dx.doi.org/10.1016/j.jmb.2005.03.025.
   PubMed Web of Science ®Google Scholar
• Gottschling H, Freese E. 1962. A tritium isotope effect on ion exchange chromatography. Nature 196:829–831. http://dx.doi.org/10.1038/196829a0.
   PubMedGoogle Scholar
• Venema J, Tollervey D. 1995. Processing of pre-ribosomal RNA in Saccharomyces cerevisiae. Yeast 11:1629–1650.
   PubMedGoogle Scholar
• Granneman S, Baserga SJ. 2004. Ribosome biogenesis: of knobs and RNA processing. Exp. Cell Res. 296:43–50. http://dx.doi.org/10.1016/j.yexcr.2004.03.016.
   PubMedGoogle Scholar
• Gallagher JE, Dunbar DA, Granneman S, Mitchell BM, Osheim Y, Beyer AL, Baserga SJ. 2004. RNA polymerase 1 transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev. 18:2506–2517. http://dx.doi.org/10.1101/gad.1226604.
   PubMed Web of Science ®Google Scholar
• Oeffinger M, Zenklusen D, Ferguson A, Wei KE, El Hage A, Tollervey D, Chait BT, Singer RH, Rout MP. 2009. Rrp17p is a eukaryotic exonuclease required for 5′end processing of pre-60S ribosomal RNA. Mol. Cell 36:768–781. http://dx.doi.org/10.1016/j.molcel.2009.11.011.
   PubMed Web of Science ®Google Scholar
• Rosado IV, Kressler D, de la Cruz J. 2007. Functional analysis of Saccharomyces cerevisiae ribosomal protein Rpl3p in ribosome biogenesis. Nucleic Acids Res. 35:4203–4213. http://dx.doi.org/10.1093/nar/gkm388.
   PubMedGoogle Scholar
• Schaper S, Fromont-Racine M, Linder P, de la Cruz J, Namane A, Yaniv M. 2001. A yeast homolog of chromatin assembly factor 1 is involved in early ribosome assembly. Curr. Biol. 11:1885–1890. http://dx.doi.org/10.1016/S0960-9822(01)00584-X.
   PubMed Web of Science ®Google Scholar
• Iouk TL, Aitchison JD, Maquire S, Wozniak RW. 2001. Rrb1, a yeast nuclear WD-repeat protein involved in the regulation of ribosome biosynthesis. Mol. Cell. Biol. 21:1260–1271. http://dx.doi.org/10.1128/MCB.21.4.1260-1271.2001.
   PubMed Web of Science ®Google Scholar
• White J, Li Z, Sardana R, Bujnicki JM, Marcotte EM, Johnson AW. 2008. Bud23 methylates G1575 of 18S rRNA and is required for efficient nuclear export of pre-40S subunits. Mol. Cell. Biol. 28:3151–3161. http://dx.doi.org/10.1128/MCB.01674-07.
   PubMed Web of Science ®Google Scholar
• Perreault A, Gascon S, D'Amours A, Aletta JM, Bachand F. 2009. A methyltransferase-independent function for Rmt3 in ribosomal subunit homeostasis. J. Biol. Chem. 284:15026–15037. http://dx.doi.org/10.1074/jbc.M109.004812.
   PubMedGoogle Scholar
• Bachand F, Silver PA. 2004. PRMT3 is a ribosomal protein methyltransferase that affects the cellular levels of ribosomal subunits. EMBO J. 23:2641–2650. http://dx.doi.org/10.1038/sj.emboj.7600265.
   PubMed Web of Science ®Google Scholar
• Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK. 2003. Global analysis of protein localization in budding yeast. Nature 425:686–691. http://dx.doi.org/10.1038/nature02026.
   PubMed Web of Science ®Google Scholar
• Keck JM, Jones MH, Wong CC, Binkley J, Chen D, Jaspersen SL, Holinger EP, Xu T, Niepel M, Rout MP, Vogel J, Sidow A, Yates JRIII, Winey M. 2011. A cell cycle phosphoproteome of the yeast centrosome. Science 332:1557–1561. http://dx.doi.org/10.1126/science.1205193.
   PubMedGoogle Scholar
• Schneider DA, French SL, Osheim YN, Bailey AO, Vu L, Dodd J, Yates JR, Beyer AL, Nomura M. 2006. RNA polymerase II elongation factors Spt4p and Spt5p play roles in transcription elongation by RNA polymerase I and rRNA processing. Proc. Natl. Acad. Sci. U. S. A. 103:12707–12712. http://dx.doi.org/10.1073/pnas.0605686103.
   PubMed Web of Science ®Google Scholar
• Hansen JL, Moore PB, Steitz TA. 2003. Structures of five antibiotics bound at the peptidyl transferase center of the large ribosomal subunit. J. Mol. Biol. 330:1061–1075. http://dx.doi.org/10.1016/S0022-2836(03)00668-5.
   PubMed Web of Science ®Google Scholar
• Ogle JM, Carter AP, Ramakrishnan V. 2003. Insights into the decoding mechanism from recent ribosome structures. Trends Biochem. Sci. 28:259–266. http://dx.doi.org/10.1016/S0968-0004(03)00066-5.
   PubMed Web of Science ®Google Scholar
• Schneider-Poetsch T, Ju J, Eyler DE, Dang Y, Bhat S, Merrick WC, Green R, Shen B, Liu JO. 2010. Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat. Chem. Biol. 6:209–217. http://dx.doi.org/10.1038/nchembio.304.
   PubMed Web of Science ®Google Scholar
• Hernández F, Cannon M. 1982. Inhibition of protein synthesis in Saccharomyces cerevisiae by the 12,13-epoxytrichothecenes trichodermol, diacetoxyscirpenol and verrucarin A. J. Antibiot. (Tokyo) 35:875–881. http://dx.doi.org/10.7164/antibiotics.35.875.
   PubMedGoogle Scholar
• Piekna-Przybylska D, Decatur WA, Fournier MJ. 2007. New bioinformatic tools for analysis of nucleotide modifications in eukaryotic rRNA. RNA 13:305–312. http://dx.doi.org/10.1261/rna.373107.
   PubMedGoogle Scholar
• Meskauskas A, Dinman JD. 2010. A molecular clamp ensures allosteric coordination of peptidyltransfer and ligand binding to the ribosomal A site. Nucleic Acids Res. 38:7800–7813. http://dx.doi.org/10.1093/nar/gkq641.
   PubMedGoogle Scholar