Molecular Genetics and Genomics

, Volume 278, Issue 1, pp 105–123 | Cite as

In vivo functional characterization of the Saccharomyces cerevisiae 60S biogenesis GTPase Nog1

  • Jennifer L. Fuentes
  • Kaustuv Datta
  • Susan M. Sullivan
  • Angela Walker
  • Janine R. Maddock
Original Paper

Abstract

The Saccharomyces cerevisiae Nog1 GTPase is critical for assembly of the large ribosomal subunit. Mutations in conserved residues in the GTP-binding pocket cause defects in cell growth and 60S ribosome assembly but mutant proteins retain their ability to associate with the pre-60S. Association of Nog1 with the pre-60S is independent of guanine nucleotide added to cell extracts. Thus, it appears that nucleotide occupancy does not substantially affect Nog1 association with pre-60S particles. Somewhat surprisingly, neither of the conserved threonines in the G2 motif of the GTPase domain is essential for Nog1 function. Neither the steady-state rRNA levels nor the protein composition (as determined by isobaric labeling and identification by mass spectrometry of peptides) of the pre-60S particles in the nog1P176V mutant are grossly perturbed, although levels of four proteins (Nog1, Nop2, Nop15, and Tif6) are modestly reduced in pre-60S particles isolated from the mutant. Deletion analysis revealed that the C-terminal 168 amino acids are not required for function; however, the N-terminal 126 amino acids are required. Optimal association with pre-60S particles requires sequences between amino acids 347–456. Several conserved charge-to-alanine substitutions outside the GTPase domain display modest growth phenotypes indicating that these residues are not critical for function.

Keywords

NOG1 GTPase 60S Ribosome biogenesis Obg/CgtA 

Notes

Acknowledgments

We are grateful to Drs. John Woolford, David Engelke, Robert Fuller, Dennis Thiele, Phillip Liu, and Keven Morano for strains, plasmids, helpful advice and/or critical reading of this manuscript. We also thank Drs. Philip Andrews and John Strahler (National Resource for Proteomics and Pathways) for proteomic technical expertise and to Robert Cantor, Nelly Cruz, Elisabeth Ashman, Jelena Jakovljevic, Tiffany Miles, Rebecca Haeusler, Paul Good, and Daniel Smith for technical assistance. This work was supported by the National Sciences Foundation (MCB-0316357) and a supplementary award from the National Institutes of Health (GM-55133-S1) to J.R.M, as well as from a University of Michigan Rackham Merit Fellowship to J.L.F.

Supplementary material

438_2007_233_MOESM1_ESM.doc (178 kb)
Supplemental tables (DOC 177 kb)
438_2007_233_MOESM2_ESM.ppt (15.1 mb)
Figure S1. Ribosome association of nog1GTP-binding domain mutants. Wild type cells expressing HIS6Nog1, HIS6Nog1G179A, HIS6Nog1S181N, or HIS6Nog1D220A were analyzed on 7-47% sucrose gradients. The absorbance (A254) of the sucrose gradients was monitored and fractions were collected, as indicated by vertical lines. (A) A representative polysome profile is shown. (B) Proteins in the fractions were TCA precipitated and analyzed by immunoblot with anti-Nog1 antibodies. The positions of the 40S, 60S, 80S and polysomes are indicated. The positions of the episomal HIS6Nog1 and chromosomal Nog1 are also indicated (PPT 15.1 Mb)

References

  1. Barbacid M (1987) Ras genes. Annu Rev Biochem 56:779–827PubMedCrossRefGoogle Scholar
  2. Bassler J, Grandi P, Gadal O, Lessmann T, Petfalski E, Tollervey D, Lechner J, Hurt E (2001) Identification of a 60S preribosomal particle that is closely linked to nuclear export. Mol Cell 8:517–529PubMedCrossRefGoogle Scholar
  3. Basu U, Si K, Warner JR, Maitra U (2001) The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis. Mol Cell Biol 21:1453–1462PubMedCrossRefGoogle Scholar
  4. Brickner JH, Fuller RS (1997) SOI1 encodes a novel, conserved protein that promotes TGN-endosomal cycling of Kex2p and other membrane proteins by modulating the function of two TGN localization signals. J Cell Biol 139:23–36PubMedCrossRefGoogle Scholar
  5. Chen SY, Huff SY, Lai CC, Der CJ, Powers S (1994) Ras-15A protein shares highly similar dominant-negative biological properties with Ras-17N and forms a stable, guanine-nucleotide resistant complex with CDC25 exchange factor. Oncogene 9:2691–2698Google Scholar
  6. Datta K, Fuentes JL, Maddock JR (2005) The yeast GTPase Mtg2p is required for mitochondrial translation and partially suppresses an rRNA methyltransferase mutant, mrm2. Mol Biol Cell 16:954–963PubMedCrossRefGoogle Scholar
  7. Datta K, Skidmore JM, Pu K, Maddock JR (2004) The Caulobacter crescentus GTPase CgtAC is required for progression through the cell cycle and for maintaining 50S ribosomal subunit levels. Mol Microbiol 54:1379–1392PubMedCrossRefGoogle Scholar
  8. de la Cruz J, Kressler D, Linder P (2004) Ribosomal subunit assembly. In: Olson MOJ (ed) The nucleolus. Kluwer Academic/Plenum Publishers, New York, pp 258–285Google Scholar
  9. De Marchis ML, Giorgi A, Schinina ME, Bozzoni I, Fatica A (2005) Rrp15p, a novel component of pre-ribosomal particles required for 60S ribosome subunit maturation. RNA 11:495–502PubMedCrossRefGoogle Scholar
  10. Deshmukh M, Tsay YF, Paulovich AG, Woolford JL Jr (1993) Yeast ribosomal protein L1 is required for the stability of newly synthesized 5S rRNA and the assembly of 60S ribosomal subunits. Mol Cell Biol 13:2835–2845PubMedGoogle Scholar
  11. Dez C, Froment C, Noaillac-Depeyre J, Monsarrat B, Caizergues-Ferrer M, Henry Y (2004) Npa1p, a component of very early pre-60S ribosomal particles, associates with a subset of small nucleolar RNPs required for peptidyl transferase center modification. Mol Cell Biol 24:6324–6337CrossRefGoogle Scholar
  12. Du YC, Stillman B (2002) Yph1p, an ORC-interacting protein: potential links between cell proliferation control, DNA replication, and ribosome biogenesis. Cell 109:835–848PubMedCrossRefGoogle Scholar
  13. Farnsworth CL, Feig LA (1991) Dominant inhibitory mutations in the Mg(2+)-binding site of RasH prevent its activation by GTP. Mol Cell Biol 11:4822–4829PubMedGoogle Scholar
  14. Fatica A, Cronshaw AD, Dlakic M, Tollervey D (2002) Ssf1p prevents premature processing of an early pre-60S ribosomal particle. Mol Cell 9:341–351PubMedCrossRefGoogle Scholar
  15. Fatica A, Tollervey D (2002) Making ribosomes. Curr Opin Cell Biol 14:313–318PubMedCrossRefGoogle Scholar
  16. Feig LA, Cooper GM (1988) Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol Cell Biol 8:3235–3243PubMedGoogle Scholar
  17. Fromont-Racine M, Senger B, Saveanu C, Fasiolo F (2003) Ribosome assembly in eukaryotes. Gene 313:17–42PubMedCrossRefGoogle Scholar
  18. Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, Marzioch M, Rau C, Jensen LJ, Bastuck S, Dumpelfeld B, Edelmann A, Heurtier MA, Hoffman V, Hoefert C, Klein K, Hudak M, Michon AM, Schelder M, Schirle M, Remor M, Rudi T, Hooper S, Bauer A, Bouwmeester T, Casari G, Drewes G, Neubauer G, Rick JM, Kuster B, Bork P, Russell RB, Superti-Furga G (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440:631–636PubMedCrossRefGoogle Scholar
  19. Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, Remor M, Hofert C, Schelder M, Brajenovic M, Ruffner H, Merino A, Klein K, Hudak M, Dickson D, Rudi T, Gnau V, Bauch A, Bastuck S, Huhse B, Leutwein C, Heurtier MA, Copley RR, Edelmann A, Querfurth E, Rybin V, Drewes G, Raida M, Bouwmeester T, Bork P, Seraphin B, Kuster B, Neubauer G, Superti-Furga G (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141–147PubMedCrossRefGoogle Scholar
  20. Gibbs JB, Sigal IS, Poe M, Scolnick EM (1984) Intrinsic GTPase activity distinguishes normal and oncogenic ras p21 molecules. Proc Natl Acad Sci USA 81:5704–5708PubMedCrossRefGoogle Scholar
  21. Grandi P, Rybin V, Bassler J, Petfalski E, Strauss D, Marzioch M, Schafer T, Kuster B, Tschochner H, Tollervey D, Gavin AC, Hurt E (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 10:105–115PubMedCrossRefGoogle Scholar
  22. Graindorge JS, Rousselle JC, Senger B, Lenormand P, Namane A, Lacroute F, Fasiolo F (2005) Deletion of EFL1 results in heterogeneity of the 60 S GTPase-associated rRNA conformation. J Mol Biol 352:355–369PubMedGoogle Scholar
  23. Guthrie C, Fink GR (1991) Guide to yeast genetics and molecular biology. Academic, San DiegoCrossRefGoogle Scholar
  24. Harnpicharnchai P, Jakovljevic J, Horsey E, Miles T, Roman J, Rout M, Meagher D, Imai B, Guo Y, Brame CJ, Shabanowitz J, Hunt DF, Woolford JL Jr (2001) Composition and functional characterization of yeast 66S ribosome assembly intermediates. Mol Cell 8:505–515PubMedCrossRefGoogle Scholar
  25. Helser TL, Baan RA, Dahlberg AE (1981) Characterization of a 40S ribosomal subunit complex in polyribosomes of Saccharomyces cerevisiae treated with cycloheximide. Mol Cell Biol 1:51–57PubMedGoogle Scholar
  26. Hirano Y, Ohniwa RL, Wada C, Yoshimura SH, Takeyasu K (2006) Human small G proteins, ObgH1, and ObgH2, participate in the maintenance of mitochondria and nucleolar architectures. Genes Cells 11:1295–1304PubMedCrossRefGoogle Scholar
  27. Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, Adams SL, Millar A, Taylor P, Bennett K, Boutilier K, Yang L, Wolting C, Donaldson I, Schandorff S, Shewnarane J, Vo M, Taggart J, Goudreault M, Muskat B, Alfarano C, Dewar D, Lin Z, Michalickova K, Willems AR, Sassi H, Nielsen PA, Rasmussen KJ, Andersen JR, Johansen LE, Hansen LH, Jespersen H, Podtelejnikov A, Nielsen E, Crawford J, Poulsen V, Sorensen BD, Matthiesen J, Hendrickson RC, Gleeson F, Pawson T, Moran MF, Durocher D, Mann M, Hogue CW, Figeys D, Tyers M (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180–183PubMedCrossRefGoogle Scholar
  28. Hong B, Brockenbrough JS, Wu P, Aris JP (1997) Nop2p is required for pre-rRNA processing and 60S ribosome subunit synthesis in yeast. Mol Cell Biol 17:378–388PubMedGoogle Scholar
  29. Hong B, Wu K, Brockenbrough JS, Wu P, Aris JP (2001) Temperature sensitive nop2 alleles defective in synthesis of 25S rRNA and large ribosomal subunits in Saccharomyces cerevisiae. Nucleic Acids Res 29:2927–2937PubMedCrossRefGoogle Scholar
  30. Honma Y, Kitamura A, Shioda R, Maruyama H, Ozaki K, Oda Y, Mini T, Jeno P, Maki Y, Yonezawa K, Hurt E, Ueno M, Uritani M, Hall MN, Ushimaru T (2006) TOR regulates late steps of ribosome maturation in the nucleoplasm via Nog1 in response to nutrients. EMBO J 25:3832–3842PubMedCrossRefGoogle Scholar
  31. Horsey EW, Jakovljevic J, Miles TD, Harnpicharnchai P, Woolford JL Jr (2004) Role of the yeast Rrp1 protein in the dynamics of pre-ribosome maturation. RNA 10:813–827PubMedCrossRefGoogle Scholar
  32. 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 425:686–691PubMedCrossRefGoogle Scholar
  33. Hwang J, Inouye M (2006) The tandem GTPase, Der, is essential for the biogenesis of 50S ribosomal subunits in Escherichia coli. Mol Microbiol 61:1660–1672PubMedCrossRefGoogle Scholar
  34. Jagtap P, Michailidis G, Zielke R, Walker AK, Patel N, Strahler JR, Driks A, Andrews PC, Maddock JR (2006) Early events of Bacillus anthracis germination identified by time-course quantitative proteomics. Proteomics 6:5199–5211PubMedCrossRefGoogle Scholar
  35. Jensen BC, Kifer CT, Brekken DL, Randall AC, Wang Q, Drees BL, Parsons M (2007) Characterization of protein kinase CK2 from Trypanosoma brucei. Mol Biochem Parasitol 151:28–40PubMedCrossRefGoogle Scholar
  36. Jensen BC, Wang Q, Kifer CT, Parsons M (2003) The NOG1 GTP-binding protein is required for biogenesis of the 60 S ribosomal subunit. J Biol Chem 278:32204–32211PubMedCrossRefGoogle Scholar
  37. Jiang M, Datta K, Walker A, Strahler J, Bagamasbad P, Andrews PC, Maddock JR (2006) The Escherichia coli GTPase CgtAE is involved in late steps of large ribosome assembly. J Bacteriol 188:6757–6770PubMedCrossRefGoogle Scholar
  38. John J, Rensland H, Schlichting I, Vetter I, Borasio GD, Goody RS, Wittinghofer A (1993) Kinetic and structural analysis of the Mg(2+)-binding site of the guanine nucleotide-binding protein p21H-ras. J Biol Chem 268:923–929PubMedGoogle Scholar
  39. Kallstrom G, Hedges J, Johnson A (2003) The putative GTPases Nog1p and Lsg1p are required for 60S ribosomal subunit biogenesis and are localized to the nucleus and cytoplasm, respectively. Mol Cell Biol 23:4344–4355PubMedCrossRefGoogle Scholar
  40. Kressler D, Linder P, de La Cruz J (1999) Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol 19:7897–7912PubMedGoogle Scholar
  41. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A, Li J, Pu S, Datta N, Tikuisis AP, Punna T, Peregrin-Alvarez JM, Shales M, Zhang X, Davey M, Robinson MD, Paccanaro A, Bray JE, Sheung A, Beattie B, Richards DP, Canadien V, Lalev A, Mena F, Wong P, Starostine A, Canete MM, Vlasblom J, Wu S, Orsi C, Collins SR, Chandran S, Haw R, Rilstone JJ, Gandi K, Thompson NJ, Musso G, St Onge P, Ghanny S, Lam MH, Butland G, Altaf-Ul AM, Kanaya S, Shilatifard A, O’Shea E, Weissman JS, Ingles CJ, Hughes TR, Parkinson J, Gerstein M, Wodak SJ, Emili A, Greenblatt JF (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440:637–643PubMedCrossRefGoogle Scholar
  42. Lebaron S, Froment C, Fromont-Racine M, Rain JC, Monsarrat B, Caizergues-Ferrer M, Henry Y (2005) The splicing ATPase prp43p is a component of multiple preribosomal particles. Mol Cell Biol 25:9269–9282PubMedCrossRefGoogle Scholar
  43. Lebreton A, Saveanu C, Decourty L, Jacquier A, Fromont-Racine M (2006) NSA2, an unstable, conserved factor required for the maturation of 27SB PRE-rRNAs. J Biol Chem 281:27099–27108PubMedCrossRefGoogle Scholar
  44. Leipe DD, Wolf YI, Koonin EV, Aravind L (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317:41–72PubMedCrossRefGoogle Scholar
  45. Lin B, Covalle KL, Maddock JR (1999) The Caulobacter crescentus CgtA protein displays unusual guanine nucleotide binding and exchange properties. J Bacteriol 181:5825–5832PubMedGoogle Scholar
  46. Lin B, Skidmore JM, Bhatt A, Pfeffer SM, Pawloski L, Maddock JR (2001) Alanine scan mutagenesis of the switch I domain of the Caulobacter crescentus CgtA protein reveals critical amino acids required for in vivo function. Mol Microbiol 39:924–934PubMedCrossRefGoogle Scholar
  47. Lin B, Thayer DA, Maddock JR (2004) The Caulobacter crescentus CgtAC protein cosediments with the free 50S ribosomal subunit. J Bacteriol 186:481–489PubMedCrossRefGoogle Scholar
  48. Liu PC, Thiele DJ (2001) Novel stress-responsive genes EMG1 and NOP14 encode conserved, interacting proteins required for 40S ribosome biogenesis. Mol Biol Cell 12:3644–3657PubMedGoogle Scholar
  49. Longtine MS, McKenzie A, 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961Google Scholar
  50. Martinez-Vicente M, Yim L, Villarroya M, Mellado M, Perez-Paya E, Bjork GR, Armengod ME (2005) Effects of mutagenesis in the switch I region and conserved arginines of Escherichia coli MnmE protein, a GTPase involved in tRNA modification. J Biol Chem 280:30660–30670PubMedCrossRefGoogle Scholar
  51. Matsuo Y, Morimoto T, Kuwano M, Loh PC, Oshima T, Ogasawara N (2006) The GTP-binding protein YlqF participates in the late step of 50 S ribosomal subunit assembly in Bacillus subtilis. J Biol Chem 281:8110–8117PubMedCrossRefGoogle Scholar
  52. Miles TD, Jakovljevic J, Horsey EW, Harnpicharnchai P, Tang L, Woolford JL Jr (2005) Ytm1, Nop7, and Erb1 form a complex necessary for maturation of yeast 66S preribosomes. Mol Cell Biol 25:10419–10432PubMedCrossRefGoogle Scholar
  53. Mumberg D, Muller R, Funk M (1994) Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res 22:5767–5768PubMedCrossRefGoogle Scholar
  54. Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E (2002) 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J 21:5539–5547PubMedCrossRefGoogle Scholar
  55. Oeffinger M, Tollervey D (2003) Yeast Nop15p is an RNA-binding protein required for pre-rRNA processing and cytokinesis. EMBO J 22:6573–6583PubMedCrossRefGoogle Scholar
  56. Park JH, Jensen BC, Kifer CT, Parsons M (2001) A novel nucleolar G-protein conserved in eukaryotes. J Cell Sci 114:173–185PubMedGoogle Scholar
  57. Planta RJ, Mager WH (1998) The list of cytoplasmic ribosomal proteins of Saccharomyces cerevisiae. Yeast 14:471–477PubMedCrossRefGoogle Scholar
  58. Powers S, O’Neill K, Wigler M (1989) Dominant yeast and mammalian RAS mutants that interfere with the CDC25-dependent activation of wild-type RAS in Saccharomyces cerevisiae. Mol Cell Biol 9:390–395PubMedGoogle Scholar
  59. Raue HA (2004) Pre-ribosomal RNA processing and assembly in Saccharomyces cerevisiae: the machine that makes the machine. In: Olson MOJ (ed) The nucleolus. Kluwer Academic/Plenum Publishers, New York, pp 199–222Google Scholar
  60. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, Seraphin B (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17:1030–1032PubMedCrossRefGoogle Scholar
  61. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3:1154–1169PubMedCrossRefGoogle Scholar
  62. Rotenberg MO, Moritz M, Woolford JL Jr (1988) Depletion of Saccharomyces cerevisiae ribosomal protein L16 causes a decrease in 60S ribosomal subunits and formation of half-mer polyribosomes. Genes Dev 2:160–172PubMedCrossRefGoogle Scholar
  63. Salamitou S, Lemaire M, Fujino T, Ohayon H, Gounon P, Beguin P, Aubert JP (1994) Subcellular localization of Clostridium thermocellum ORF3p, a protein carrying a receptor for the docking sequence borne by the catalytic components of the cellulosome. J Bacteriol 176:2828–2834PubMedGoogle Scholar
  64. Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual. Cold Spirng Harbor, Laboratory Press, Cold Spring HarborGoogle Scholar
  65. Saveanu C, Bienvenu D, Namane A, Gleizes PE, Gas N, Jacquier A, Fromont-Racine M (2001) Nog2p, a putative GTPase associated with pre-60S subunits and required for late 60S maturation steps. EMBO J 20:6475–6484PubMedCrossRefGoogle Scholar
  66. Saveanu C, Namane A, Gleizes PE, Lebreton A, Rousselle JC, Noaillac-Depeyre J, Gas N, Jacquier A, Fromont-Racine M (2003) Sequential protein association with nascent 60S ribosomal particles. Mol Cell Biol 23:4449–4460PubMedCrossRefGoogle Scholar
  67. Schafer T, Strauss D, Petfalski E, Tollervey D, Hurt E (2003) The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J 22:1370–1380PubMedCrossRefGoogle Scholar
  68. Seeburg PH, Colby WW, Capon DJ, Goeddel DV, Levinson AD (1984) Biological properties of human c-Ha-ras1 genes mutated at codon 12. Nature 312:71–75PubMedCrossRefGoogle Scholar
  69. Shimamoto T, Inouye M (1996) Mutational analysis of Era, an essential GTP-binding protein of Escherichia coli. FEMS Microbiol Lett 136:57–62PubMedCrossRefGoogle Scholar
  70. Si K, Maitra U (1999) The Saccharomyces cerevisiae homologue of mammalian translation initiation factor 6 does not function as a translation initiation factor. Mol Cell Biol 19:1416–1426Google Scholar
  71. Sikora AE, Datta K, Maddock JR (2006) Biochemical properties of the Vibrio harveyi CgtAV GTPase. Biochem Biophys Res Commun 339:1165–1170PubMedCrossRefGoogle Scholar
  72. Spoerner M, Herrmann C, Vetter IR, Kalbitzer HR, Wittinghofer A (2001) Dynamic properties of the Ras switch I region and its importance for binding to effectors. Proc Natl Acad Sci USA 98:4944–4949PubMedCrossRefGoogle Scholar
  73. Tschochner H, Hurt E (2003) Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol 13:255–263PubMedCrossRefGoogle Scholar
  74. Venema J, Tollervey D (1999) Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet 33:261–311PubMedCrossRefGoogle Scholar
  75. Vetter IR, Wittinghofer A (2001) The guanine nucleotide-binding switch in three dimensions. Science 294:1299–1304PubMedCrossRefGoogle Scholar
  76. Volta V, Ceci M, Emery B, Bachi A, Petfalski E, Tollervey D, Linder P, Marchisio PC, Piatti S, Biffo S (2005) Sen34p depletion blocks tRNA splicing in vivo and delays rRNA processing. Biochem Biophys Res Commun 337:89–94PubMedCrossRefGoogle Scholar
  77. Washburn MP, Wolters D, Yates JR III (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19:242–247PubMedCrossRefGoogle Scholar
  78. Welsh KM, Trach KA, Folger C, Hoch JA (1994) Biochemical characterization of the essential GTP-binding protein Obg of Bacillus subtilis. J Bacteriol 176:7161–7168PubMedGoogle Scholar
  79. Wittinghofer A, Franken SM, Scheidig AJ, Rensland H, Lautwein A, Pai EF, Goody RS (1993) Three-dimensional structure and properties of wild-type and mutant H-ras-encoded p21. Ciba Found Symp 176:6–21; discussion 21–27Google Scholar
  80. Wood LC, Ashby MN, Grunfeld C, Feingold KR (1999) Cloning of murine translation initiation factor 6 and functional analysis of the homologous sequence YPR016c in Saccharomyces cerevisiae. J Biol Chem 274:11653–11659PubMedCrossRefGoogle Scholar
  81. Wout P, Pu K, Sullivan SM, Reese V, Zhou S, Lin B, Maddock JR (2004) The Escherichia coli GTPase CgtAE cofractionates with the 50S ribosomal subunit and interacts with SpoT, a ppGpp synthetase/hydrolase. J Bacteriol 186:5249–5257PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Jennifer L. Fuentes
    • 1
  • Kaustuv Datta
    • 1
  • Susan M. Sullivan
    • 1
  • Angela Walker
    • 2
  • Janine R. Maddock
    • 1
  1. 1.Department of Molecular, Cellular and Developmental BiologyUniversity of MichiganAnn ArborUSA
  2. 2.Department of Biological ChemistryUniversity of MichiganAnn ArborUSA

Personalised recommendations