Methylation of yeast ribosomal protein S2 is elevated during stationary phase growth conditions

Biochemical and Biophysical Research Communications

Volumn 445, Issue 3, 2014, Pages 535-541

  Ladror, Daniel T ^a   Frey, Brian L ^a   Scalf, Mark ^a   Levenstein, Mark E ^a   Artymiuk, Jacklyn M ^a   Smith, Lloyd M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Growth conditions; Mass spectrometry; Post translational modifications; Proteomics; Ribosome; Stationary phase

Indexed keywords

RIBOSOME PROTEIN; RIBOSOME PROTEIN S2; RIBOSOME RNA; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CONTROLLED STUDY; FUNGUS GROWTH; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN METHYLATION; QUANTITATIVE ANALYSIS; RIBOSOME;

GROWTH CONDITIONS; MASS SPECTROMETRY; POST-TRANSLATIONAL MODIFICATIONS; PROTEOMICS; RIBOSOME; STATIONARY PHASE;

AMINO ACID SEQUENCE; METHYLATION; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; RIBOSOMAL PROTEINS; RIBOSOMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84896317532     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2014.01.040     Document Type: Article

References (48)

1. Zaman S., Lippman S.I., Zhao X., Broach J.R. How Saccharomyces responds to nutrients. Annu. Rev. Genet. 2008, 42:27-81.
2. Warner J.R., Vilardell J., Sohn J.H. Economics of ribosome biosynthesis. Cold Spring Harbor. Symp. Quant. Biol. 2001, 66:567-574.
3. Zwietering M.H., Jongenburger I., Rombouts F.M., Vantriet K. Modeling of the bacterial-growth curve. Appl. Environ. Microbiol. 1990, 56:1875-1881.
4. Gray J.V., Petsko G.A., Johnston G.C., Ringe D., Singer R.A., Werner-Washburne M. "Sleeping beauty": quiescence in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2004, 68:187-206.
5. Dennis P.P., Nomura M. Stringent control of ribosomal-protein gene-expression in Escherichia-coli. Proc. Natl. Acad. Sci. U.S.A. 1974, 71:3819-3823.
6. Gasch A.P., Spellman P.T., Kao C.M., Carmel-Harel O., Eisen M.B., Storz G., Botstein D., Brown P.O. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 2000, 11:4241-4257.
7. Chen D.R., Toone W.M., Mata J., Lyne R., Burns G., Kivinen K., Brazma A., Jones N., Bahler J. Global transcriptional responses of fission yeast to environmental stress. Mol. Biol. Cell 2003, 14:214-229.
8. Causton H.C., Ren B., Koh S.S., Harbison C.T., Kanin E., Jennings E.G., Lee T.I., True H.L., Lander E.S., Young R.A. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 2001, 12:323-337.
9. Geyer P.K., Meyuhas O., Perry R.P., Johnson L.F. Regulation of ribosomal-protein messenger-RNA content and translation in growth-stimulated mouse fibroblasts. Mol. Cell Biol. 1982, 2:685-693.
10. Wendrich T.M., Blaha G., Wilson D.N., Marahiel M.A., Nierhaus K.H. Dissection of the mechanism for the stringent factor ReIA. Mol. Cell 2002, 10:779-788.
11. Ueta M., Yoshida H., Wada C., Baba T., Mori H., Wada A. Ribosome binding proteins YhbH and YfiA have opposite functions during 100S formation in the stationary phase of Escherichia coli. Genes Cells 2005, 10:1103-1112.
12. Thomas G., Siegmann M., Gordon J. Multiple phosphorylation of ribosomal protein-S6 during transition of quiescent 3t3 cells into early G1, and cellular compartmentalization of the phosphate donor. Proc. Natl. Acad. Sci. U.S.A. 1979, 76:3952-3956.
13. Cameron D.M., Gregory S.T., Thompson J., Suh M.J., Limbach P.A., Dahlberg A.E. Thermus thermophilus L11 methyltransferase, PrmA, is dispensable for growth and preferentially modifies free ribosomal protein L11 prior to ribosome assembly. J. Bacteriol. 2004, 186:5819-5825.
14. Mazumder B., Sampath P., Seshadri V., Maitra R.K., DiCorleto P.E., Fox P.L. Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcript-specific translational control. Cell 2003, 115:187-198.
15. Porras-Yakushi T.R., Whitelegge J.P., Clarke S. Yeast ribosomal/cytochrome C SET domain methyltransferase subfamily - identification of Rpl23ab methylation sites and recognition motifs. J. Biol. Chem. 2007, 282:12368-12376.
16. Sadaie M., Shinmyozu K., Nakayama J.I. A conserved SET domain methyltransferase, Set11, modifies ribosomal protein Rpl12 in fission yeast. J. Biol. Chem. 2008, 283:7185-7195.
17. Kamita M., Kimura Y., Ino Y., Kamp R.M., Polevoda B., Sherman F., Hirano H. N-alpha-acetylation of yeast ribosomal proteins and its effect on protein synthesis. J. Proteomics 2011, 74:431-441.
18. Shin H.S., Jang C.Y., Kim H.D., Kim T.S., Kim S., Kim J. Arginine methylation of ribosomal protein S3 affects ribosome assembly. Biochem. Biophys. Res. Commun. 2009, 385:273-278.
19. Ren J.Q., Wang Y.Q., Liang Y.H., Zhang Y.Q., Bao S.L., Xu Z.H. Methylation of ribosomal protein S10 by Protein-arginine methyltransferase 5 regulates ribosome biogenesis. J. Biol. Chem. 2010, 285:12695-12705.
20. Bachand F., Silver P.A. PRMT3 is a ribosomal protein methyltransferase that affects the cellular levels of ribosomal subunits. EMBO J. 2004, 23:2641-2650.
21. Swiercz R., Cheng D.H., Kim D., Bedford M.T. Ribosomal protein RPS2 is hypomethylated in PRMT3-deficient mice. J. Biol. Chem. 2007, 282:16917-16923.
22. Lipson R.S., Webb K.J., Clarke S.G. Rmt1 catalyzes zinc-finger independent arginine methylation of ribosomal protein Rps2 in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 2010, 391:1658-1662.
23. Young B.D., Weiss D.I., Zurita-Lopez C.I., Webb K.J., Clarke S.G., McBride A.E. Identification of methylated proteins in the yeast small ribosomal subunit: a role for SPOUT methyltransferases in protein arginine methylation. Biochem. 2012, 51:5091-5104.
24. Smith L.M., Kelleher N.L. Proteoform: a single term describing protein complexity. Nat. Methods 2013, 10:186-187.
25. Goyder M.S., Willison K.R., Klug D.R., deMello A.J., Ces O. Affinity chromatography and capillary electrophoresis for analysis of the yeast ribosomal proteins. Biochem. Mol. Biol. Rep. 2012, 45:233-238.
26. Lee S.W., Berger S.J., Martinovic S., Pasa-Tolic L., Anderson G.A., Shen Y.F., Zhao R., Smith R.D. Direct mass spectrometric analysis of intact proteins of the yeast large ribosomal subunit using capillary LC/FTICR. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:5942-5947.
27. Arnold R.J., Reilly J.P. Observation of Escherichia coli ribosomal proteins and their posttranslational modifications by mass spectrometry. Anal. Biochem. 1999, 269:105-112.
28. Running W.E., Ravipaty S., Karty J.A., Reilly J.P. A top-down/bottom-up study of the ribosomal proteins of caulobacter crescentus. J. Proteome Res. 2007, 6:337-347.
29. Strader M.B., VerBerkmoes N.C., Tabb D.L., Connelly H.M., Barton J.W., Bruce B.D., Pelletier D.A., Davison B.H., Hettich R.L., Larimer F.W., Hurst G.B. Characterization of the 70S ribosome from Rhodopseudomonas palustris using an integrated "top-down" and "bottom-up" mass spectrometric approach. J. Proteome Res. 2004, 3:965-978.
30. Lauber M.A., Running W.E., Reilly J.P. B. subtilis ribosomal proteins: structural homology and post-translational modifications. J. Proteome Res. 2009, 8:4193-4206.
31. Carroll A.J., Heazlewood J.L., Ito J., Millar A.H. Analysis of the arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol. Cell. Proteomics 2008, 7:347-369.
32. Forbes A.J., Patrie S.M., Taylor G.K., Kim Y.B., Jiang L.H., Kelleher N.L. Targeted analysis and discovery of posttranslational modifications in proteins from methanogenic archaea by top-down MS. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2678-2683.
33. Louie D.F., Resing K.A., Lewis T.S., Ahn N.G. Mass spectrometric analysis of 40 S ribosomal proteins from Rat-1 fibroblasts. J. Biol. Chem. 1996, 271:28189-28198.
34. Inada T., Winstall E., Tarun S.Z., Yates J.R., Schieltz D., Sachs A.B. One-step affinity purification of the yeast ribosome and its associated proteins and mRNAs. RNA 2002, 8:948-958.
35. Simons S.P., McLellan T.J., Aeed P.A., Zaniewski R.P., Desbonnet C.R., Wondrack L.M., Marr E.S., Subashi T.A., Dougherty T.J., Xu Z.Y., Wang I.K., LeMotte P.K., Maguire B.A. Purification of the large ribosomal subunit via its association with the small subunit. Anal. Biochem. 2009, 395:77-85.
36. Hardy S.J.S., Kurland C.G., Voynow P., Mora G. Ribosomal proteins of Escherichia Coli. I. Purification of 30s ribosomal proteins. Biochem. 1969, 8:2897-2905.
37. Benjamini Y., Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. R. Statist. Soc. B 1995, 57:289-300.
38. Shen Y.F., Tolic N., Xie F., Zhao R., Purvine S.O., Schepmoes A.A., Ronald J.M., Anderson G.A., Smith R.D. Effectiveness of CID, HCD, and ETD with FT MS/MS for degradomic-peptidomic analysis: comparison of peptide identification methods. J. Proteome Res. 2011, 10:3929-3943.
39. Yishai L., Schwarz E., Wang L., Leweke F.M., Bahn S. Label-Free LC-MS/MS Quantitative Proteomics for Large-Scale Biomarker Discovery in Complex Samples. J. Sep. Sci. 2007, 30:2198-2203.
40. Zhang B., VerBerkmoes N.C., Langston M.A., Uberbacher E., Hettich R.L., Samatova N.F. Detecting differential and correlated protein expression in label-free shotgun proteomics. J. Proteome Res. 2006, 5:2909-2918.
41. Bachand F., Lackner D.H., Bahler J., Silver P.A. Autoregulation of ribosome biosynthesis by a translational response in fission yeast. Mol. Cell Biol. 2006, 26:1731-1742.
42. Perreault A., Bellemer C., Bachand F. Nuclear export competence of pre-40S subunits in fission yeast requires the ribosomal protein Rps2. Nucleic Acids Res. 2008, 36:6132-6142.
43. Perreault A., Lemieux C., Bachand F. Regulation of the nuclear poly(A)-binding protein by arginine methylation in fission yeast. J. Biol. Chem. 2007, 282:7552-7562.
44. Choi S., Jung C.R., Kim J.Y., Im D.S. PRMT3 inhibits ubiquitination of ribosomal protein S2 and together forms an active enzyme complex. Biochim. Biophys. Acta, Gen. Subj. 2008, 1780:1062-1069.
45. Ferreira-Cerca S., Pöll G., Gleizes P.-E., Tschochner H., Milkereit P. Roles of eukaryotic ribosomal proteins in maturation and transport of Pre-18S rRNA and ribosome function. Mol. Cell 2005, 20:263-275.
46. Shen E.C., Henry M.F., Weiss V.H., Valentini S.R., Silver P.A., Lee M.S. Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes Dev. 1998, 12:679-691.
47. Green D.M., Marfatia K.A., Crafton E.B., Zhang X., Cheng X.D., Corbett A.H. Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p. J. Biol. Chem. 2002, 277:7752-7760.
48. McBride A.E., Cook J.T., Stemmler E.A., Rutledge K.L., McGrath K.A., Rubens J.A. Arginine methylation of yeast mRNA-binding protein Npl3 directly affects its function, nuclear export, and intranuclear protein interactions. J. Biol. Chem. 2005, 280:30888-30898.