Advertisement

Translation Elongation and Termination: Are They Conserved Processes?

  • Sandra Eltschinger
  • Peter Bütikofer
  • Michael AltmannEmail author
Chapter

Abstract

In this chapter, we focus on the function and evolution of translation elongation and termination mechanisms. We review the current knowledge on the properties of eukaryotic elongation and termination factors and compare them to their prokaryotic orthologues. Additionally, we describe posttranslational modifications of elongation factors and discuss their possible roles in translation. Although several features of elongation and termination factors are strictly conserved among all domains of life, notable differences occur between bacteria, archaea and eukaryotes.

Keywords

Stop Codon Release Factor Translation Termination SECIS Element Peptide Bond Formation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by Swiss National Foundation grants 31003A_146722/1 (M. Altmann) and 31003A_149353/1 (P. Bütikofer).

References

  1. 1.
    Kapp LD, Lorsch JR. The molecular mechanics of eukaryotic translation. Annu Rev Biochem. 2004;73:657–704. doi: 10.1146/annurev.biochem.73.030403.080419.CrossRefPubMedGoogle Scholar
  2. 2.
    Dever TE, Green R. The elongation, termination, and recycling phases of translation in eukaryotes. Cold Spring Harb Perspect Biol. 2012;4:a013706. doi: 10.1101/cshperspect.a013706.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Hernandez G, Proud CG, Preiss T, Parsyan A. On the Diversification of the Translation Apparatus across Eukaryotes. Comp Funct Genomics. 2012;2012:256848. doi: 10.1155/2012/256848.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Andersen GR, Nissen P, Nyborg J. Elongation factors in protein biosynthesis. Trends Biochem Sci. 2003;28:434–41. doi: 10.1016/S0968-0004(03)00162-2.CrossRefPubMedGoogle Scholar
  5. 5.
    Jackson RJ, Hellen CU, Pestova TV. Termination and post-termination events in eukaryotic translation. Adv Protein Chem Struct Biol. 2012;86:45–93. doi: 10.1016/B978-0-12-386497-0.00002-5.CrossRefPubMedGoogle Scholar
  6. 6.
    Rodnina MV, Wintermeyer W. Recent mechanistic insights into eukaryotic ribosomes. Curr Opin Cell Biol. 2009;21:435–43. doi: 10.1016/j.ceb.2009.01.023.CrossRefPubMedGoogle Scholar
  7. 7.
    Le Sourd F, Boulben S, Le Bouffant R, Cormier P, Morales J, Belle R, Mulner-Lorillon O. eEF1B: At the dawn of the 21st century. Biochim Biophys Acta. 2006;1759:13–31. doi: 10.1016/j.bbaexp.2006.02.003.CrossRefPubMedGoogle Scholar
  8. 8.
    Bec G, Kerjan P, Waller JP. Reconstitution in vitro of the valyl-tRNA synthetase-elongation factor (EF) 1 beta gamma delta complex. Essential roles of the NH2-terminal extension of valyl-tRNA synthetase and of the EF-1 delta subunit in complex formation. J Biol Chem. 1994;269:2086–92.PubMedGoogle Scholar
  9. 9.
    Belfield GP, Bauer M, Ross-Smith N, Tan P, Colthurst DR, Tuite MF. EF-3: a novel fungal elongation factor with homology to E. coli ribosomal protein S5. Biochem Soc Trans. 1993;21:331S.CrossRefPubMedGoogle Scholar
  10. 10.
    Belfield GP, Tuite MF. Translation elongation factor 3: a fungus-specific translation factor? Mol Microbiol. 1993;9:411–8.CrossRefPubMedGoogle Scholar
  11. 11.
    Triana-Alonso FJ, Chakraburtty K, Nierhaus KH. The elongation factor 3 unique in higher fungi and essential for protein biosynthesis is an E site factor. J Biol Chem. 1995;270:20473–8.CrossRefPubMedGoogle Scholar
  12. 12.
    Hericourt F, Jupin I. Molecular cloning and characterization of the Arabidopsis thaliana alpha-subunit of elongation factor 1B. FEBS Lett. 1999;464:148–52.CrossRefPubMedGoogle Scholar
  13. 13.
    Anand M, Balar B, Ulloque R, Gross SR, Kinzy TG. Domain and nucleotide dependence of the interaction between Saccharomyces cerevisiae translation elongation factors 3 and 1A. J Biol Chem. 2006;281:32318–26. doi: 10.1074/jbc.M601899200.CrossRefPubMedGoogle Scholar
  14. 14.
    Lucas-Lenard J. Protein biosynthesis. Annu Rev Biochem. 1971;40:409–48. doi: 10.1146/annurev.bi.40.070171.002205.CrossRefPubMedGoogle Scholar
  15. 15.
    Sengupta S, Higgs PG. Pathways of Genetic Code Evolution in Ancient and Modern Organisms. J Mol Evol. 2015;80:229–43. doi: 10.1007/s00239-015-9686-8.CrossRefPubMedGoogle Scholar
  16. 16.
    Graifer D, Karpova G. Interaction of tRNA with eukaryotic ribosome. Int J Mol Sci. 2015;16:7173–94. doi: 10.3390/ijms16047173.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Wilson DN, Doudna Cate JH. The structure and function of the eukaryotic ribosome. Cold Spring Harbor perspectives in biology. 2012; 4. doi: 10.1101/cshperspect.a011536.Google Scholar
  18. 18.
    Khalyfa A, Bourbeau D, Chen E, Petroulakis E, Pan J, Xu S, Wang E. Characterization of elongation factor-1A (eEF1A-1) and eEF1A-2/S1 protein expression in normal and wasted mice. J Biol Chem. 2001;276:22915–22. doi: 10.1074/jbc.M101011200.CrossRefPubMedGoogle Scholar
  19. 19.
    Janssen GM, Moller W. Kinetic studies on the role of elongation factors 1 beta and 1 gamma in protein synthesis. J Biol Chem. 1988;263:1773–8.PubMedGoogle Scholar
  20. 20.
    Minella O, Mulner-Lorillon O, Bec G, Cormier P, Belle R. Multiple phosphorylation sites and quaternary organization of guanine-nucleotide exchange complex of elongation factor-1 (EF-1betagammadelta/ValRS) control the various functions of EF-1alpha. Biosci Rep. 1998;18:119–27.CrossRefPubMedGoogle Scholar
  21. 21.
    Motoyoshi K, Iwasaki K. Resolution of the polypeptide chain elongation factor-1 beta gamma into subunits and some properties of the subunits. J Biochem. 1977;82:703–8.PubMedGoogle Scholar
  22. 22.
    Motoyoshi K, Iwasaki K, Kaziro Y. Purification and properties of polypeptide chain elongation factor-1 beta gamma from pig liver. J Biochem. 1977;82:145–55.PubMedGoogle Scholar
  23. 23.
    Janssen GM, Moller W. Elongation factor 1 beta gamma from Artemia. Purification and properties of its subunits. European J Biochem/ FEBS. 1988; 171:119–129.Google Scholar
  24. 24.
    Kawashima T, Berthet-Colominas C, Wulff M, Cusack S, Leberman R. The structure of the Escherichia coli EF-Tu.EF-Ts complex at 2.5 A resolution. Nature. 1996;379:511–8. doi: 10.1038/379511a0.CrossRefPubMedGoogle Scholar
  25. 25.
    Wang Y, Jiang Y, Meyering-Voss M, Sprinzl M, Sigler PB. Crystal structure of the EF-Tu.EF-Ts complex from Thermus thermophilus. Nat Struct Biol. 1997;4:650–6.CrossRefPubMedGoogle Scholar
  26. 26.
    Andersen GR, Pedersen L, Valente L, Chatterjee I, Kinzy TG, Kjeldgaard M, Nyborg J. Structural basis for nucleotide exchange and competition with tRNA in the yeast elongation factor complex eEF1A:eEF1Balpha. Mol Cell. 2000;6:1261–6.CrossRefPubMedGoogle Scholar
  27. 27.
    Sivan G, Aviner R, Elroy-Stein O. Mitotic modulation of translation elongation factor 1 leads to hindered tRNA delivery to ribosomes. J Biol Chem. 2011;286:27927–35. doi: 10.1074/jbc.M111.255810.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Andersen GR, Nyborg J. Structural studies of eukaryotic elongation factors. Cold Spring Harb Symp Quant Biol. 2001;66:425–37.CrossRefPubMedGoogle Scholar
  29. 29.
    Crepin T, Shalak VF, Yaremchuk AD, Vlasenko DO, McCarthy A, Negrutskii BS, Tukalo MA, El’skaya AV. Mammalian translation elongation factor eEF1A2: X-ray structure and new features of GDP/GTP exchange mechanism in higher eukaryotes. Nucleic Acids Res. 2014;42:12939–48. doi: 10.1093/nar/gku974.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Miller DL, Weissbach H. Interactions between the elongation factors: the displacement of GPD from the TU-GDP complex by factor Ts. Biochem Biophys Res Commun. 1970;38:1016–22.CrossRefPubMedGoogle Scholar
  31. 31.
    Saha SK, Chakraburtty K. Protein synthesis in yeast. Isolation of variant forms of elongation factor 1 from the yeast Saccharomyces cerevisiae. J Biol Chem. 1986;261:12599–603.PubMedGoogle Scholar
  32. 32.
    Gaucher EA, Das UK, Miyamoto MM, Benner SA. The crystal structure of eEF1A refines the functional predictions of an evolutionary analysis of rate changes among elongation factors. Mol Biol Evol. 2002;19:569–73.CrossRefPubMedGoogle Scholar
  33. 33.
    Spahn CM, Gomez-Lorenzo MG, Grassucci RA, Jorgensen R, Andersen GR, Beckmann R, Penczek PA, Ballesta JP, Frank J. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. The EMBO J. 2004;23:1008–19. doi: 10.1038/sj.emboj.7600102.CrossRefPubMedGoogle Scholar
  34. 34.
    Venema RC, Peters HI, Traugh JA. Phosphorylation of elongation factor 1 (EF-1) and valyl-tRNA synthetase by protein kinase C and stimulation of EF-1 activity. J Biol Chem. 1991;266:12574–80.PubMedGoogle Scholar
  35. 35.
    Dever TE, Costello CE, Owens CL, Rosenberry TL, Merrick WC. Location of seven post-translational modifications in rabbit elongation factor 1 alpha including dimethyllysine, trimethyllysine, and glycerylphosphorylethanolamine. J Biol Chem. 1989;264:20518–25.PubMedGoogle Scholar
  36. 36.
    Zobel-Thropp P, Yang MC, Machado L, Clarke S. A novel post-translational modification of yeast elongation factor 1A. Methylesterification at the C terminus. J Biol Chem. 2000; 275:37150–37158. doi: 10.1074/jbc.M001005200.Google Scholar
  37. 37.
    Rosenberry TL, Krall JA, Dever TE, Haas R, Louvard D, Merrick WC. Biosynthetic incorporation of [3H]ethanolamine into protein synthesis elongation factor 1 alpha reveals a new post-translational protein modification. J Biol Chem. 1989;264:7096–9.PubMedGoogle Scholar
  38. 38.
    Whiteheart SW, Shenbagamurthi P, Chen L, Cotter RJ, Hart GW. Murine elongation factor 1 alpha (EF-1 alpha) is posttranslationally modified by novel amide-linked ethanolamine-phosphoglycerol moieties. Addition of ethanolamine-phosphoglycerol to specific glutamic acid residues on EF-1 alpha. J Biol Chem. 1989;264:14334–41.PubMedGoogle Scholar
  39. 39.
    Hamey JJ, Winter DL, Yagoub D, Overall CM, Hart-Smith G, Wilkins MR. Novel N-terminal and lysine methyltransferases that target translation elongation factor 1A in yeast and human. Mol Cell Proteomics: MCP. 2015;. doi: 10.1074/mcp.M115.052449.PubMedGoogle Scholar
  40. 40.
    Uhlen M, Bjorling E, Agaton C, Szigyarto CA, Amini B, Andersen E, Andersson AC, Angelidou P, Asplund A, Asplund C, Berglund L, Bergstrom K, Brumer H, Cerjan D, Ekstrom M, Elobeid A, Eriksson C, Fagerberg L, Falk R, Fall J, Forsberg M, Bjorklund MG, Gumbel K, Halimi A, Hallin I, Hamsten C, Hansson M, Hedhammar M, Hercules G, Kampf C, Larsson K, Lindskog M, Lodewyckx W, Lund J, Lundeberg J, Magnusson K, Malm E, Nilsson P, Odling J, Oksvold P, Olsson I, Oster E, Ottosson J, Paavilainen L, Persson A, Rimini R, Rockberg J, Runeson M, Sivertsson A, Skollermo A, Steen J, Stenvall M, Sterky F, Stromberg S, Sundberg M, Tegel H, Tourle S, Wahlund E, Walden A, Wan J, Wernerus H, Westberg J, Wester K, Wrethagen U, Xu LL, Hober S, Ponten F. A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol Cell Proteomics: MCP. 2005;4:1920–32. doi: 10.1074/mcp.M500279-MCP200.CrossRefPubMedGoogle Scholar
  41. 41.
    Ransom WD, Lao PC, Gage DA, Boss WF. Phosphoglycerylethanolamine posttranslational modification of plant eukaryotic elongation factor 1alpha. Plant Physiol. 1998;117:949–60.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Signorell A, Jelk J, Rauch M, Bütikofer P. Phosphatidylethanolamine is the precursor of the ethanolamine phosphoglycerol moiety bound to eukaryotic elongation factor 1A. J Biol Chem. 2008;283:20320–9. doi: 10.1074/jbc.M802430200.CrossRefPubMedGoogle Scholar
  43. 43.
    Greganova E, Heller M, Bütikofer P. A structural domain mediates attachment of ethanolamine phosphoglycerol to eukaryotic elongation factor 1A in Trypanosoma brucei. PLoS ONE. 2010;5:e9486. doi: 10.1371/journal.pone.0009486.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Cavallius J, Zoll W, Chakraburtty K, Merrick WC. Characterization of yeast EF-1 alpha: non-conservation of post-translational modifications. Biochim Biophys Acta. 1993;1163:75–80.CrossRefPubMedGoogle Scholar
  45. 45.
    Eltschinger S, Greganova E, Heller M, Bütikofer P, Altmann M. Eukaryotic translation elongation factor 1A (eEF1A) domain I from S. cerevisiae is required but not sufficient for inter-species complementation. PLoS ONE. 2012;7:e42338. doi: 10.1371/journal.pone.0042338.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Greganova E, Altmann M, Bütikofer P. Unique modifications of translation elongation factors. The FEBS J. 2011;278:2613–24. doi: 10.1111/j.1742-4658.2011.08199.x.CrossRefPubMedGoogle Scholar
  47. 47.
    Greganova E, Bütikofer P. Ethanolamine phosphoglycerol attachment to eEF1A is not essential for normal growth of Trypanosoma brucei. Scientific reports. 2012;2:254. doi: 10.1038/srep00254.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Burk RF, Hill KE. Orphan selenoproteins. BioEssays: News Rev Mol Cell Dev Biol. 1999;21:231–7. doi: 10.1002/(SICI)1521-1878(199903)21:3<231:AID-BIES7>3.0.CO;2-D.CrossRefGoogle Scholar
  49. 49.
    Huttenhofer A, Bock A. Selenocysteine inserting RNA elements modulate GTP hydrolysis of elongation factor SelB. Biochemistry. 1998;37:885–90. doi: 10.1021/bi972298k.CrossRefPubMedGoogle Scholar
  50. 50.
    Berry MJ, Banu L, Harney JW, Larsen PR. Functional characterization of the eukaryotic SECIS elements which direct selenocysteine insertion at UGA codons. The EMBO J. 1993;12:3315–22.PubMedGoogle Scholar
  51. 51.
    Shen Q, Chu FF, Newburger PE. Sequences in the 3′-untranslated region of the human cellular glutathione peroxidase gene are necessary and sufficient for selenocysteine incorporation at the UGA codon. J Biol Chem. 1993;268:11463–9.PubMedGoogle Scholar
  52. 52.
    Berry MJ, Banu L, Chen YY, Mandel SJ, Kieffer JD, Harney JW, Larsen PR. Recognition of UGA as a selenocysteine codon in type I deiodinase requires sequences in the 3′ untranslated region. Nature. 1991;353:273–6. doi: 10.1038/353273a0.CrossRefPubMedGoogle Scholar
  53. 53.
    Shetty SP, Copeland PR. Selenocysteine incorporation: A trump card in the game of mRNA decay. Biochimie. 2015;114:97–101. doi: 10.1016/j.biochi.2015.01.007.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Forchhammer K, Leinfelder W, Boesmiller K, Veprek B, Bock A. Selenocysteine synthase from Escherichia coli. Nucleotide sequence of the gene (selA) and purification of the protein. J Biol Chem. 1991;266:6318–23.PubMedGoogle Scholar
  55. 55.
    Leinfelder W, Zehelein E, Mandrand-Berthelot MA, Bock A. Gene for a novel tRNA species that accepts L-serine and cotranslationally inserts selenocysteine. Nature. 1988;331:723–5. doi: 10.1038/331723a0.CrossRefPubMedGoogle Scholar
  56. 56.
    Ehrenreich A, Forchhammer K, Tormay P, Veprek B, Bock A. Selenoprotein synthesis in E. coli. Purification and characterisation of the enzyme catalysing selenium activation. European J Biochem/FEBS. 1992; 206:767–773.Google Scholar
  57. 57.
    Fagegaltier D, Hubert N, Yamada K, Mizutani T, Carbon P, Krol A. Characterization of mSelB, a novel mammalian elongation factor for selenoprotein translation. The EMBO J. 2000;19:4796–805. doi: 10.1093/emboj/19.17.4796.CrossRefPubMedGoogle Scholar
  58. 58.
    Rother M, Wilting R, Commans S, Bock A. Identification and characterisation of the selenocysteine-specific translation factor SelB from the archaeon Methanococcus jannaschii. J Mol Biol. 2000;299:351–8. doi: 10.1006/jmbi.2000.3756.CrossRefPubMedGoogle Scholar
  59. 59.
    Forchhammer K, Leinfelder W, Bock A. Identification of a novel translation factor necessary for the incorporation of selenocysteine into protein. Nature. 1989;342:453–6. doi: 10.1038/342453a0.CrossRefPubMedGoogle Scholar
  60. 60.
    Zinoni F, Heider J, Bock A. Features of the formate dehydrogenase mRNA necessary for decoding of the UGA codon as selenocysteine. Proc Natl Acad Sci USA. 1990;87:4660–4.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Heider J, Bock A. Targeted insertion of selenocysteine into the alpha subunit of formate dehydrogenase from Methanobacterium formicicum. J Bacteriol. 1992;174:659–63.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Baron C, Westhof E, Bock A, Giege R. Solution structure of selenocysteine-inserting tRNA(Sec) from Escherichia coli. Comparison with canonical tRNA(Ser). J Mol Biol. 1993;231:274–92. doi: 10.1006/jmbi.1993.1282.CrossRefPubMedGoogle Scholar
  63. 63.
    Chen GF, Fang L, Inouye M. Effect of the relative position of the UGA codon to the unique secondary structure in the fdhF mRNA on its decoding by selenocysteinyl tRNA in Escherichia coli. J Biol Chem. 1993;268:23128–31.PubMedGoogle Scholar
  64. 64.
    Baron C, Heider J, Bock A. Interaction of translation factor SELB with the formate dehydrogenase H selenopolypeptide mRNA. Proc Natl Acad Sci USA. 1993;90:4181–5.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Tujebajeva RM, Copeland PR, Xu XM, Carlson BA, Harney JW, Driscoll DM, Hatfield DL, Berry MJ. Decoding apparatus for eukaryotic selenocysteine insertion. EMBO Rep. 2000;1:158–63. doi: 10.1038/sj.embor.embor604.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Pittman YR, Kandl K, Lewis M, Valente L, Kinzy TG. Coordination of eukaryotic translation elongation factor 1A (eEF1A) function in actin organization and translation elongation by the guanine nucleotide exchange factor eEF1Balpha. J Biol Chem. 2009;284:4739–47. doi: 10.1074/jbc.M807945200.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Hirosawa-Takamori M, Ossipov D, Novoselov SV, Turanov AA, Zhang Y, Gladyshev VN, Krol A, Vorbruggen G, Jackle H. A novel stem loop control element-dependent UGA read-through system without translational selenocysteine incorporation in Drosophila. FASEB J: Official publication of the Federation of American Societies for Experimental Biology. 2009;23:107–13. doi: 10.1096/fj.08-116640.CrossRefGoogle Scholar
  68. 68.
    Copeland PR, Fletcher JE, Carlson BA, Hatfield DL, Driscoll DM. A novel RNA binding protein, SBP2, is required for the translation of mammalian selenoprotein mRNAs. The EMBO J. 2000;19:306–14. doi: 10.1093/emboj/19.2.306.CrossRefPubMedGoogle Scholar
  69. 69.
    Lesoon A, Mehta A, Singh R, Chisolm GM, Driscoll DM. An RNA-binding protein recognizes a mammalian selenocysteine insertion sequence element required for cotranslational incorporation of selenocysteine. Mol Cell Biol. 1997;17:1977–85.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Copeland PR, Driscoll DM. Purification, redox sensitivity, and RNA binding properties of SECIS-binding protein 2, a protein involved in selenoprotein biosynthesis. J Biol Chem. 1999;274:25447–54.CrossRefPubMedGoogle Scholar
  71. 71.
    Gonzalez-Flores JN, Shetty SP, Dubey A, Copeland PR. The molecular biology of selenocysteine. Biomolecular concepts. 2013;4:349–65. doi: 10.1515/bmc-2013-0007.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Selmer M, Su XD. Crystal structure of an mRNA-binding fragment of Moorella thermoacetica elongation factor SelB. The EMBO J. 2002;21:4145–53.CrossRefPubMedGoogle Scholar
  73. 73.
    Gonzalez-Flores JN, Gupta N, DeMong LW, Copeland PR. The selenocysteine-specific elongation factor contains a novel and multi-functional domain. J Biol Chem. 2012;287:38936–45. doi: 10.1074/jbc.M112.415463.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Leibundgut M, Frick C, Thanbichler M, Bock A, Ban N. Selenocysteine tRNA-specific elongation factor SelB is a structural chimaera of elongation and initiation factors. The EMBO J. 2005;24:11–22. doi: 10.1038/sj.emboj.7600505.CrossRefPubMedGoogle Scholar
  75. 75.
    Keeling PJ, Fast NM, McFadden GI. Evolutionary relationship between translation initiation factor eIF-2gamma and selenocysteine-specific elongation factor SELB: change of function in translation factors. J Mol Evol. 1998;47:649–55.CrossRefPubMedGoogle Scholar
  76. 76.
    Allmang C, Krol A. Selenoprotein synthesis: UGA does not end the story. Biochimie. 2006;88:1561–71. doi: 10.1016/j.biochi.2006.04.015.CrossRefPubMedGoogle Scholar
  77. 77.
    Lobanov AV, Fomenko DE, Zhang Y, Sengupta A, Hatfield DL, Gladyshev VN. Evolutionary dynamics of eukaryotic selenoproteomes: large selenoproteomes may associate with aquatic life and small with terrestrial life. Genome Biol. 2007;8:R198. doi: 10.1186/gb-2007-8-9-r198.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Lobanov AV, Hatfield DL, Gladyshev VN. Eukaryotic selenoproteins and selenoproteomes. Biochim Biophys Acta. 2009;1790:1424–8. doi: 10.1016/j.bbagen.2009.05.014.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Nauser T, Steinmann D, Koppenol WH. Why do proteins use selenocysteine instead of cysteine? Amino Acids. 2012;42:39–44. doi: 10.1007/s00726-010-0602-7.CrossRefPubMedGoogle Scholar
  80. 80.
    Yates SP, Jorgensen R, Andersen GR, Merrill AR. Stealth and mimicry by deadly bacterial toxins. Trends Biochem Sci. 2006;31:123–33. doi: 10.1016/j.tibs.2005.12.007.CrossRefPubMedGoogle Scholar
  81. 81.
    Carlberg U, Nilsson A, Nygard O. Functional properties of phosphorylated elongation factor 2. European J Biochem/FEBS. 1990;191:639–45.CrossRefGoogle Scholar
  82. 82.
    Ryazanov AG, Davydova EK. Mechanism of elongation factor 2 (EF-2) inactivation upon phosphorylation. Phosphorylated EF-2 is unable to catalyze translocation. FEBS Lett. 1989;251:187–90.CrossRefPubMedGoogle Scholar
  83. 83.
    Price NT, Redpath NT, Severinov KV, Campbell DG, Russell JM, Proud CG. Identification of the phosphorylation sites in elongation factor-2 from rabbit reticulocytes. FEBS Lett. 1991;282:253–8.CrossRefPubMedGoogle Scholar
  84. 84.
    Ortiz PA, Ulloque R, Kihara GK, Zheng H, Kinzy TG. Translation elongation factor 2 anticodon mimicry domain mutants affect fidelity and diphtheria toxin resistance. J Biol Chem. 2006;281:32639–48. doi: 10.1074/jbc.M607076200.CrossRefPubMedGoogle Scholar
  85. 85.
    Zhang Y, Liu S, Lajoie G, Merrill AR. The role of the diphthamide-containing loop within eukaryotic elongation factor 2 in ADP-ribosylation by Pseudomonas aeruginosa exotoxin A. Biochem J. 2008;413:163–74. doi: 10.1042/BJ20071083.CrossRefPubMedGoogle Scholar
  86. 86.
    Pappenheimer AM Jr. Diphtheria toxin. Annu Rev Biochem. 1977;46:69–94. doi: 10.1146/annurev.bi.46.070177.000441.CrossRefPubMedGoogle Scholar
  87. 87.
    Oppenheimer NJ, Bodley JW. Diphtheria toxin. Site and configuration of ADP-ribosylation of diphthamide in elongation factor 2. J Biol Chem. 1981;256:8579–81.PubMedGoogle Scholar
  88. 88.
    Jorgensen R, Purdy AE, Fieldhouse RJ, Kimber MS, Bartlett DH, Merrill AR. Cholix toxin, a novel ADP-ribosylating factor from Vibrio cholerae. J Biol Chem. 2008;283:10671–8. doi: 10.1074/jbc.M710008200.CrossRefPubMedGoogle Scholar
  89. 89.
    Chen JY, Bodley JW. Biosynthesis of diphthamide in Saccharomyces cerevisiae. Partial purification and characterization of a specific S-adenosylmethionine:elongation factor 2 methyltransferase. J Biol Chem. 1988;263:11692–6.PubMedGoogle Scholar
  90. 90.
    Pallen MJ, Lam AC, Loman NJ, McBride A. An abundance of bacterial ADP-ribosyltransferases–implications for the origin of exotoxins and their human homologues. Trends in microbiology. 2001; 9:302–307; discussion 308.Google Scholar
  91. 91.
    Krueger KM, Barbieri JT. The family of bacterial ADP-ribosylating exotoxins. Clin Microbiol Rev. 1995;8:34–47.PubMedPubMedCentralGoogle Scholar
  92. 92.
    Corda D, Di Girolamo M. Functional aspects of protein mono-ADP-ribosylation. The EMBO J. 2003;22:1953–8. doi: 10.1093/emboj/cdg209.CrossRefPubMedGoogle Scholar
  93. 93.
    Jorgensen R, Merrill AR, Yates SP, Marquez VE, Schwan AL, Boesen T, Andersen GR. Exotoxin A-eEF2 complex structure indicates ADP ribosylation by ribosome mimicry. Nature. 2005;436:979–84. doi: 10.1038/nature03871.CrossRefPubMedGoogle Scholar
  94. 94.
    Van Ness BG, Howard JB, Bodley JW. ADP-ribosylation of elongation factor 2 by diphtheria toxin. NMR spectra and proposed structures of ribosyl-diphthamide and its hydrolysis products. J Biol Chem. 1980;255:10710–6.PubMedGoogle Scholar
  95. 95.
    Kimata Y, Kohno K. Elongation factor 2 mutants deficient in diphthamide formation show temperature-sensitive cell growth. J Biol Chem. 1994;269:13497–501.PubMedGoogle Scholar
  96. 96.
    Phan LD, Perentesis JP, Bodley JW. Saccharomyces cerevisiae elongation factor 2. Mutagenesis of the histidine precursor of diphthamide yields a functional protein that is resistant to diphtheria toxin. J Biol Chem. 1993;268:8665–8.PubMedGoogle Scholar
  97. 97.
    Jorgensen R, Merrill AR, Andersen GR. The life and death of translation elongation factor 2. Biochem Soc Trans. 2006;34:1–6. doi: 10.1042/BST20060001.CrossRefPubMedGoogle Scholar
  98. 98.
    Gupta PK, Liu S, Batavia MP, Leppla SH. The diphthamide modification on elongation factor-2 renders mammalian cells resistant to ricin. Cell Microbiol. 2008;10:1687–94. doi: 10.1111/j.1462-5822.2008.01159.x.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Qin SL, Xie AG, Bonato MC, McLaughlin CS. Sequence analysis of the translational elongation factor 3 from Saccharomyces cerevisiae. J Biol Chem. 1990;265:1903–12.PubMedGoogle Scholar
  100. 100.
    Myers KK, Fonzi WA, Sypherd PS. Isolation and sequence analysis of the gene for translation elongation factor 3 from Candida albicans. Nucleic Acids Res. 1992;20:1705–10.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Di Domenico BJ, Lupisella J, Sandbaken M, Chakraburtty K. Isolation and sequence analysis of the gene encoding translation elongation factor 3 from Candida albicans. Yeast. 1992;8:337–52. doi: 10.1002/yea.320080502.CrossRefPubMedGoogle Scholar
  102. 102.
    Blakely G, Hekman J, Chakraburtty K, Williamson PR. Evolutionary divergence of an elongation factor 3 from Cryptococcus neoformans. J Bacteriol. 2001;183:2241–8. doi: 10.1128/JB.183.7.2241-2248.2001.CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Ypma-Wong MF, Fonzi WA, Sypherd PS. Fungus-specific translation elongation factor 3 gene present in Pneumocystis carinii. Infect Immun. 1992;60:4140–5.PubMedPubMedCentralGoogle Scholar
  104. 104.
    Jones PM, George AM. Mechanism of ABC transporters: a molecular dynamics simulation of a well characterized nucleotide-binding subunit. Proc Natl Acad Sci USA. 2002;99:12639–44. doi: 10.1073/pnas.152439599.CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Kambampati R, Pellegrino C, Paiva A, Huang L, Mende-Mueller L, Chakraburtty K. Limited proteolysis of yeast elongation factor 3. Sequence and location of the subdomains. J Biol Chem. 2000;275:16963–8. doi: 10.1074/jbc.M001157200.CrossRefPubMedGoogle Scholar
  106. 106.
    Kovalchuke O, Kambampati R, Pladies E, Chakraburtty K. Competition and cooperation amongst yeast elongation factors. European J Biochem/FEBS. 1998;258:986–93.CrossRefGoogle Scholar
  107. 107.
    Gontarek RR, Li H, Nurse K, Prescott CD. The N terminus of eukaryotic translation elongation factor 3 interacts with 18 S rRNA and 80 S ribosomes. J Biol Chem. 1998;273:10249–52.CrossRefPubMedGoogle Scholar
  108. 108.
    Kamath A, Chakraburtty K. Role of yeast elongation factor 3 in the elongation cycle. J Biol Chem. 1989;264:15423–8.PubMedGoogle Scholar
  109. 109.
    Harms J, Schluenzen F, Zarivach R, Bashan A, Gat S, Agmon I, Bartels H, Franceschi F, Yonath A. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell. 2001;107:679–88.CrossRefPubMedGoogle Scholar
  110. 110.
    Andersen CB, Becker T, Blau M, Anand M, Halic M, Balar B, Mielke T, Boesen T, Pedersen JS, Spahn CM, Kinzy TG, Andersen GR, Beckmann R. Structure of eEF3 and the mechanism of transfer RNA release from the E-site. Nature. 2006;443:663–8. doi: 10.1038/nature05126.CrossRefPubMedGoogle Scholar
  111. 111.
    Sarthy AV, McGonigal T, Capobianco JO, Schmidt M, Green SR, Moehle CM, Goldman RC. Identification and kinetic analysis of a functional homolog of elongation factor 3, YEF3 in Saccharomyces cerevisiae. Yeast. 1998;14:239–53. doi: 10.1002/(SICI)1097-0061(199802)14:3<239:AID-YEA219>3.0.CO;2-B.CrossRefPubMedGoogle Scholar
  112. 112.
    Maurice TC, Mazzucco CE, Ramanathan CS, Ryan BM, Warr GA, Puziss JW. A highly conserved intraspecies homolog of the Saccharomyces cerevisiae elongation factor-3 encoded by the HEF3 gene. Yeast. 1998;14:1105–13. doi: 10.1002/(SICI)1097-0061(19980915)14:12<1105:AID-YEA313>3.0.CO;2-Y.CrossRefPubMedGoogle Scholar
  113. 113.
    Herrera F, Martinez JA, Moreno N, Sadnik I, McLaughlin CS, Feinberg B, Moldave K. Identification of an altered elongation factor in temperature-sensitive mutant ts 7′-14 of Saccharomyces cerevisiae. J Biol Chem. 1984;259:14347–9.PubMedGoogle Scholar
  114. 114.
    Samra N, Atir-Lande A, Pnueli L, Arava Y. The elongation factor eEF3 (Yef3) interacts with mRNA in a translation independent manner. BMC Mol Biol. 2015;16:17. doi: 10.1186/s12867-015-0045-5.CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    March PE, Inouye M. Characterization of the lep operon of Escherichia coli. Identification of the promoter and the gene upstream of the signal peptidase I gene. J Biol Chem. 1985;260:7206–13.PubMedGoogle Scholar
  116. 116.
    Zwizinski C, Wickner W. Purification and characterization of leader (signal) peptidase from Escherichia coli. J Biol Chem. 1980;255:7973–7.PubMedGoogle Scholar
  117. 117.
    Qin Y, Polacek N, Vesper O, Staub E, Einfeldt E, Wilson DN, Nierhaus KH. The highly conserved LepA is a ribosomal elongation factor that back-translocates the ribosome. Cell. 2006;127:721–33. doi: 10.1016/j.cell.2006.09.037.CrossRefPubMedGoogle Scholar
  118. 118.
    Bauerschmitt H, Funes S, Herrmann JM. The membrane-bound GTPase Guf1 promotes mitochondrial protein synthesis under suboptimal conditions. J Biol Chem. 2008;283:17139–46. doi: 10.1074/jbc.M710037200.CrossRefPubMedGoogle Scholar
  119. 119.
    Ji DL, Lin H, Chi W, Zhang LX. CpLEPA is critical for chloroplast protein synthesis under suboptimal conditions in Arabidopsis thaliana. PLoS ONE. 2012;7:e49746. doi: 10.1371/journal.pone.0049746.CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Margus T, Remm M, Tenson T. Phylogenetic distribution of translational GTPases in bacteria. BMC Genom. 2007;8:15. doi: 10.1186/1471-2164-8-15.CrossRefGoogle Scholar
  121. 121.
    Yamamoto H, Qin Y, Achenbach J, Li C, Kijek J, Spahn CM, Nierhaus KH. EF-G and EF4: translocation and back-translocation on the bacterial ribosome. Nat Rev Microbiol. 2014;12:89–100. doi: 10.1038/nrmicro3176.CrossRefPubMedGoogle Scholar
  122. 122.
    Evans RN, Blaha G, Bailey S, Steitz TA. The structure of LepA, the ribosomal back translocase. Proc Natl Acad Sci USA. 2008;105:4673–8. doi: 10.1073/pnas.0801308105.CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    Gagnon MG, Lin J, Bulkley D, Steitz TA. Crystal structure of elongation factor 4 bound to a clockwise ratcheted ribosome. Science. 2014;345:684–7. doi: 10.1126/science.1253525.CrossRefPubMedGoogle Scholar
  124. 124.
    Zhang D, Qin Y. The paradox of elongation factor 4: highly conserved, yet of no physiological significance? Biochem J. 2013;452:173–81. doi: 10.1042/BJ20121792.CrossRefPubMedGoogle Scholar
  125. 125.
    Kiser GL, Weinert TA. GUF1, a gene encoding a novel evolutionarily conserved GTPase in budding yeast. Yeast. 1995;11:1311–6. doi: 10.1002/yea.320111312.CrossRefPubMedGoogle Scholar
  126. 126.
    Thomas A, Goumans H, Amesz H, Benne R, Voorma HO. A comparison of the initiation factors of eukaryotic protein synthesis from ribosomes and from the postribosomal supernatant. European J Biochem/FEBS. 1979;98:329–37.CrossRefGoogle Scholar
  127. 127.
    Gordon ED, Mora R, Meredith SC, Lee C, Lindquist SL. Eukaryotic initiation factor 4D, the hypusine-containing protein, is conserved among eukaryotes. J Biol Chem. 1987;262:16585–9.PubMedGoogle Scholar
  128. 128.
    Gordon ED, Mora R, Meredith SC, Lindquist SL. Hypusine formation in eukaryotic initiation factor 4D is not reversed when rates or specificity of protein synthesis is altered. J Biol Chem. 1987;262:16590–5.PubMedGoogle Scholar
  129. 129.
    Kemper WM, Berry KW, Merrick WC. Purification and properties of rabbit reticulocyte protein synthesis initiation factors M2Balpha and M2Bbeta. J Biol Chem. 1976;251:5551–7.PubMedGoogle Scholar
  130. 130.
    Schreier MH, Erni B, Staehelin T. Initiation of mammalian protein synthesis. I. Purification and characterization of seven initiation factors. J Mol Biol. 1977;116:727–53.CrossRefPubMedGoogle Scholar
  131. 131.
    Jao DL, Chen KY. Tandem affinity purification revealed the hypusine-dependent binding of eukaryotic initiation factor 5A to the translating 80S ribosomal complex. J Cell Biochem. 2006;97:583–98. doi: 10.1002/jcb.20658.CrossRefPubMedGoogle Scholar
  132. 132.
    Benne R, Brown-Luedi ML, Hershey JW. Purification and characterization of protein synthesis initiation factors eIF-1, eIF-4C, eIF-4D, and eIF-5 from rabbit reticulocytes. J Biol Chem. 1978;253:3070–7.PubMedGoogle Scholar
  133. 133.
    Smit-McBride Z, Schnier J, Kaufman RJ, Hershey JW. Protein synthesis initiation factor eIF-4D. Functional comparison of native and unhypusinated forms of the protein. J Biol Chem. 1989;264:18527–30.PubMedGoogle Scholar
  134. 134.
    Park MH. The essential role of hypusine in eukaryotic translation initiation factor 4D (eIF-4D). Purification of eIF-4D and its precursors and comparison of their activities. J Biol Chem. 1989;264:18531–5.PubMedGoogle Scholar
  135. 135.
    Gregio AP, Cano VP, Avaca JS, Valentini SR, Zanelli CF. eIF5A has a function in the elongation step of translation in yeast. Biochem Biophys Res Commun. 2009;380:785–90. doi: 10.1016/j.bbrc.2009.01.148.CrossRefPubMedGoogle Scholar
  136. 136.
    Saini P, Eyler DE, Green R, Dever TE. Hypusine-containing protein eIF5A promotes translation elongation. Nature. 2009;459:118–21. doi: 10.1038/nature08034.CrossRefPubMedPubMedCentralGoogle Scholar
  137. 137.
    Zanelli CF, Maragno AL, Gregio AP, Komili S, Pandolfi JR, Mestriner CA, Lustri WR, Valentini SR. eIF5A binds to translational machinery components and affects translation in yeast. Biochem Biophys Res Commun. 2006;348:1358–66. doi: 10.1016/j.bbrc.2006.07.195.CrossRefPubMedGoogle Scholar
  138. 138.
    Kang HA, Hershey JW. Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae. J Biol Chem. 1994;269:3934–40.PubMedGoogle Scholar
  139. 139.
    Doerfel LK, Rodnina MV. Elongation factor P: Function and effects on bacterial fitness. Biopolymers. 2013;99:837–45. doi: 10.1002/bip.22341.CrossRefPubMedGoogle Scholar
  140. 140.
    Doerfel LK, Wohlgemuth I, Kothe C, Peske F, Urlaub H, Rodnina MV. EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science. 2013;339:85–8. doi: 10.1126/science.1229017.CrossRefPubMedGoogle Scholar
  141. 141.
    Gutierrez E, Shin BS, Woolstenhulme CJ, Kim JR, Saini P, Buskirk AR, Dever TE. eIF5A promotes translation of polyproline motifs. Mol Cell. 2013;51:35–45. doi: 10.1016/j.molcel.2013.04.021.CrossRefPubMedPubMedCentralGoogle Scholar
  142. 142.
    Ude S, Lassak J, Starosta AL, Kraxenberger T, Wilson DN, Jung K. Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science. 2013;339:82–5. doi: 10.1126/science.1228985.CrossRefPubMedGoogle Scholar
  143. 143.
    Blaha G, Stanley RE, Steitz TA. Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science. 2009;325:966–70. doi: 10.1126/science.1175800.CrossRefPubMedPubMedCentralGoogle Scholar
  144. 144.
    Hanawa-Suetsugu K, Sekine S, Sakai H, Hori-Takemoto C, Terada T, Unzai S, Tame JR, Kuramitsu S, Shirouzu M, Yokoyama S. Crystal structure of elongation factor P from Thermus thermophilus HB8. Proc Natl Acad Sci USA. 2004;101:9595–600. doi: 10.1073/pnas.0308667101.CrossRefPubMedPubMedCentralGoogle Scholar
  145. 145.
    Kim KK, Hung LW, Yokota H, Kim R, Kim SH. Crystal structures of eukaryotic translation initiation factor 5A from Methanococcus jannaschii at 1.8 A resolution. Proc Natl Acad Sci USA. 1998;95:10419–24.CrossRefPubMedPubMedCentralGoogle Scholar
  146. 146.
    Park MH, Nishimura K, Zanelli CF, Valentini SR. Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids. 2010;38:491–500. doi: 10.1007/s00726-009-0408-7.CrossRefPubMedGoogle Scholar
  147. 147.
    Park MH, Wolff EC, Smit-McBride Z, Hershey JW, Folk JE. Comparison of the activities of variant forms of eIF-4D. The requirement for hypusine or deoxyhypusine. J Biol Chem. 1991;266:7988–94.PubMedGoogle Scholar
  148. 148.
    Lee SB, Park JH, Kaevel J, Sramkova M, Weigert R, Park MH. The effect of hypusine modification on the intracellular localization of eIF5A. Biochem Biophys Res Commun. 2009;383:497–502. doi: 10.1016/j.bbrc.2009.04.049.CrossRefPubMedPubMedCentralGoogle Scholar
  149. 149.
    Bailly M, de Crecy-Lagard V. Predicting the pathway involved in post-translational modification of elongation factor P in a subset of bacterial species. Biol Direct. 2010;5:3. doi: 10.1186/1745-6150-5-3.CrossRefPubMedPubMedCentralGoogle Scholar
  150. 150.
    Navarre WW, Zou SB, Roy H, Xie JL, Savchenko A, Singer A, Edvokimova E, Prost LR, Kumar R, Ibba M, Fang FC. PoxA, yjeK, and elongation factor P coordinately modulate virulence and drug resistance in Salmonella enterica. Mol Cell. 2010;39:209–21. doi: 10.1016/j.molcel.2010.06.021.CrossRefPubMedPubMedCentralGoogle Scholar
  151. 151.
    Yanagisawa T, Sumida T, Ishii R, Takemoto C, Yokoyama S. A paralog of lysyl-tRNA synthetase aminoacylates a conserved lysine residue in translation elongation factor P. Nat Struct Mol Biol. 2010;17:1136–43. doi: 10.1038/nsmb.1889.CrossRefPubMedGoogle Scholar
  152. 152.
    Park JH, Johansson HE, Aoki H, Huang BX, Kim HY, Ganoza MC, Park MH. Post-translational modification by beta-lysylation is required for activity of Escherichia coli elongation factor P (EF-P). J Biol Chem. 2012;287:2579–90. doi: 10.1074/jbc.M111.309633.CrossRefPubMedGoogle Scholar
  153. 153.
    Lassak J, Keilhauer EC, Furst M, Wuichet K, Godeke J, Starosta AL, Chen JM, Sogaard-Andersen L, Rohr J, Wilson DN, Haussler S, Mann M, Jung K. Corrigendum: Arginine-rhamnosylation as new strategy to activate translation elongation factor P. Nat Chem Biol. 2015;11:299. doi: 10.1038/nchembio0415-299d.CrossRefPubMedGoogle Scholar
  154. 154.
    Lassak J, Keilhauer EC, Furst M, Wuichet K, Godeke J, Starosta AL, Chen JM, Sogaard-Andersen L, Rohr J, Wilson DN, Haussler S, Mann M, Jung K. Arginine-rhamnosylation as new strategy to activate translation elongation factor P. Nat Chem Biol. 2015;11:266–70. doi: 10.1038/nchembio.1751.CrossRefPubMedPubMedCentralGoogle Scholar
  155. 155.
    Choi S, Choe J. Crystal structure of elongation factor P from Pseudomonas aeruginosa at 1.75 A resolution. Proteins. 2011;79:1688–93. doi: 10.1002/prot.22992.CrossRefPubMedGoogle Scholar
  156. 156.
    Lassak J, Wilson DN, Jung K. Stall no more at polyproline stretches with the translation elongation factors EF-P and IF-5A. Mol Microbiol. 2015;. doi: 10.1111/mmi.13233.PubMedGoogle Scholar
  157. 157.
    Jenkins ZA, Haag PG, Johansson HE. Human eIF5A2 on chromosome 3q25-q27 is a phylogenetically conserved vertebrate variant of eukaryotic translation initiation factor 5A with tissue-specific expression. Genomics. 2001;71:101–9. doi: 10.1006/geno.2000.6418.CrossRefPubMedGoogle Scholar
  158. 158.
    Ohashi Y, Inaoka T, Kasai K, Ito Y, Okamoto S, Satsu H, Tozawa Y, Kawamura F, Ochi K. Expression profiling of translation-associated genes in sporulating Bacillus subtilis and consequence of sporulation by gene inactivation. Biosci Biotechnol Biochem. 2003;67:2245–53. doi: 10.1271/bbb.67.2245.CrossRefPubMedGoogle Scholar
  159. 159.
    Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol. 2006;2006(2):0008. doi: 10.1038/msb4100050.Google Scholar
  160. 160.
    Sassetti CM, Boyd DH, Rubin EJ. Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol. 2003;48:77–84.CrossRefPubMedGoogle Scholar
  161. 161.
    Ejiri S. Moonlighting functions of polypeptide elongation factor 1: from actin bundling to zinc finger protein R1-associated nuclear localization. Biosci Biotechnol Biochem. 2002;66:1–21. doi: 10.1271/bbb.66.1.CrossRefPubMedGoogle Scholar
  162. 162.
    Altmann M, Muller PP, Pelletier J, Sonenberg N, Trachsel H. A mammalian translation initiation factor can substitute for its yeast homologue in vivo. J Biol Chem. 1989;264:12145–7.PubMedGoogle Scholar
  163. 163.
    Arcari P, Masullo M, Arcucci A, Ianniciello G, de Paola B, Bocchini V. A chimeric elongation factor containing the putative guanine nucleotide binding domain of archaeal EF-1 alpha and the M and C domains of eubacterial EF-Tu. Biochemistry. 1999;38:12288–95.CrossRefPubMedGoogle Scholar
  164. 164.
    Anand M, Chakraburtty K, Marton MJ, Hinnebusch AG, Kinzy TG. Functional interactions between yeast translation eukaryotic elongation factor (eEF) 1A and eEF3. J Biol Chem. 2003;278:6985–91. doi: 10.1074/jbc.M209224200.CrossRefPubMedGoogle Scholar
  165. 165.
    Mateyak MK, Kinzy TG. eEF1A: thinking outside the ribosome. J Biol Chem. 2010;285:21209–13. doi: 10.1074/jbc.R110.113795.CrossRefPubMedPubMedCentralGoogle Scholar
  166. 166.
    Liu G, Grant WM, Persky D, Latham VM Jr, Singer RH, Condeelis J. Interactions of elongation factor 1alpha with F-actin and beta-actin mRNA: implications for anchoring mRNA in cell protrusions. Mol Biol Cell. 2002;13:579–92. doi: 10.1091/mbc.01-03-0140.CrossRefPubMedPubMedCentralGoogle Scholar
  167. 167.
    van den Ent F, Amos LA, Lowe J. Prokaryotic origin of the actin cytoskeleton. Nature. 2001;413:39–44. doi: 10.1038/35092500.CrossRefPubMedGoogle Scholar
  168. 168.
    Defeu Soufo HJ. Reimold C, Linne U, Knust T, Gescher J, Graumann PL. Bacterial translation elongation factor EF-Tu interacts and colocalizes with actin-like MreB protein. Proc Natl Acad Sci USA. 2010;107:3163–8. doi: 10.1073/pnas.0911979107.CrossRefPubMedPubMedCentralGoogle Scholar
  169. 169.
    Liu Z, Xing D, Su QP, Zhu Y, Zhang J, Kong X, Xue B, Wang S, Sun H, Tao Y, Sun Y. Super-resolution imaging and tracking of protein-protein interactions in sub-diffraction cellular space. Nat Commun. 2014;5:4443. doi: 10.1038/ncomms5443.PubMedPubMedCentralGoogle Scholar
  170. 170.
    Defeu Soufo HJ. Reimold C, Breddermann H, Mannherz HG, Graumann PL. Translation elongation factor EF-Tu modulates filament formation of actin-like MreB protein in vitro. J Mol Biol. 2015;427:1715–27. doi: 10.1016/j.jmb.2015.01.025.CrossRefPubMedGoogle Scholar
  171. 171.
    Anand N, Murthy S, Amann G, Wernick M, Porter LA, Cukier IH, Collins C, Gray JW, Diebold J, Demetrick DJ, Lee JM. Protein elongation factor EEF1A2 is a putative oncogene in ovarian cancer. Nat Genet. 2002;31:301–5. doi: 10.1038/ng904.PubMedGoogle Scholar
  172. 172.
    Tomlinson VA, Newbery HJ, Wray NR, Jackson J, Larionov A, Miller WR, Dixon JM, Abbott CM. Translation elongation factor eEF1A2 is a potential oncoprotein that is overexpressed in two-thirds of breast tumours. BMC Cancer. 2005;5:113. doi: 10.1186/1471-2407-5-113.CrossRefPubMedPubMedCentralGoogle Scholar
  173. 173.
    Pinke DE, Kalloger SE, Francetic T, Huntsman DG, Lee JM. The prognostic significance of elongation factor eEF1A2 in ovarian cancer. Gynecol Oncol. 2008;108:561–8. doi: 10.1016/j.ygyno.2007.11.019.CrossRefPubMedGoogle Scholar
  174. 174.
    Scaggiante B, Dapas B, Bonin S, Grassi M, Zennaro C, Farra R, Cristiano L, Siracusano S, Zanconati F, Giansante C, Grassi G. Dissecting the expression of EEF1A1/2 genes in human prostate cancer cells: the potential of EEF1A2 as a hallmark for prostate transformation and progression. Br J Cancer. 2012;106:166–73. doi: 10.1038/bjc.2011.500.CrossRefPubMedGoogle Scholar
  175. 175.
    Keeling PJ, Inagaki Y. A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1alpha. Proc Natl Acad Sci USA. 2004;101:15380–5. doi: 10.1073/pnas.0404505101.CrossRefPubMedPubMedCentralGoogle Scholar
  176. 176.
    Sakaguchi M, Takishita K, Matsumoto T, Hashimoto T, Inagaki Y. Tracing back EFL gene evolution in the cryptomonads-haptophytes assemblage: separate origins of EFL genes in haptophytes, photosynthetic cryptomonads, and goniomonads. Gene. 2009;441:126–31. doi: 10.1016/j.gene.2008.05.010.CrossRefPubMedGoogle Scholar
  177. 177.
    Noble GP, Rogers MB, Keeling PJ. Complex distribution of EFL and EF-1alpha proteins in the green algal lineage. BMC Evol Biol. 2007;7:82. doi: 10.1186/1471-2148-7-82.CrossRefPubMedPubMedCentralGoogle Scholar
  178. 178.
    Kamikawa R, Inagaki Y, Sako Y. Direct phylogenetic evidence for lateral transfer of elongation factor-like gene. Proc Natl Acad Sci USA. 2008;105:6965–9. doi: 10.1073/pnas.0711084105.CrossRefPubMedPubMedCentralGoogle Scholar
  179. 179.
    Gile GH, Faktorova D, Castlejohn CA, Burger G, Lang BF, Farmer MA, Lukes J, Keeling PJ. Distribution and phylogeny of EFL and EF-1alpha in Euglenozoa suggest ancestral co-occurrence followed by differential loss. PLoS ONE. 2009;4:e5162. doi: 10.1371/journal.pone.0005162.CrossRefPubMedPubMedCentralGoogle Scholar
  180. 180.
    Cocquyt E, Verbruggen H, Leliaert F, Zechman FW, Sabbe K, De Clerck O. Gain and loss of elongation factor genes in green algae. BMC Evol Biol. 2009;9:39. doi: 10.1186/1471-2148-9-39.CrossRefPubMedPubMedCentralGoogle Scholar
  181. 181.
    Kamikawa R, Sakaguchi M, Matsumoto T, Hashimoto T, Inagaki Y. Rooting for the root of elongation factor-like protein phylogeny. Mol Phylogenet Evol. 2010;56:1082–8. doi: 10.1016/j.ympev.2010.04.040.CrossRefPubMedGoogle Scholar
  182. 182.
    Skogerson L, Engelhardt D. Dissimilarity in protein chain elongation factor requirements between yeast and rat liver ribosomes. J Biol Chem. 1977;252:1471–5.PubMedGoogle Scholar
  183. 183.
    Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M. The structure of the eukaryotic ribosome at 3.0 A resolution. Science. 2011; 334:1524–1529. doi: 10.1126/science.1212642.Google Scholar
  184. 184.
    Van Dyke N, Pickering BF, Van Dyke MW. Stm1p alters the ribosome association of eukaryotic elongation factor 3 and affects translation elongation. Nucleic Acids Res. 2009;37:6116–25. doi: 10.1093/nar/gkp645.CrossRefPubMedPubMedCentralGoogle Scholar
  185. 185.
    Ben-Shem A, Jenner L, Yusupova G, Yusupov M. Crystal structure of the eukaryotic ribosome. Science. 2010;330:1203–9. doi: 10.1126/science.1194294.CrossRefPubMedGoogle Scholar
  186. 186.
    Van Dyke N, Chanchorn E, Van Dyke MW. The Saccharomyces cerevisiae protein Stm1p facilitates ribosome preservation during quiescence. Biochem Biophys Res Commun. 2013;430:745–50. doi: 10.1016/j.bbrc.2012.11.078.CrossRefPubMedGoogle Scholar
  187. 187.
    Bijlsma JJ, Lie ALM, Nootenboom IC, Vandenbroucke-Grauls CM, Kusters JG. Identification of loci essential for the growth of Helicobacter pylori under acidic conditions. J Infect Dis. 2000;182:1566–9. doi: 10.1086/315855.CrossRefPubMedGoogle Scholar
  188. 188.
    Song H, Mugnier P, Das AK, Webb HM, Evans DR, Tuite MF, Hemmings BA, Barford D. The crystal structure of human eukaryotic release factor eRF1–mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell. 2000;100:311–21.CrossRefPubMedGoogle Scholar
  189. 189.
    Vestergaard B, Van LB, Andersen GR, Nyborg J, Buckingham RH, Kjeldgaard M. Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol Cell. 2001;8:1375–82.CrossRefPubMedGoogle Scholar
  190. 190.
    Shin DH, Brandsen J, Jancarik J, Yokota H, Kim R, Kim SH. Structural analyses of peptide release factor 1 from Thermotoga maritima reveal domain flexibility required for its interaction with the ribosome. J Mol Biol. 2004;341:227–39. doi: 10.1016/j.jmb.2004.05.055.CrossRefPubMedGoogle Scholar
  191. 191.
    Brenner S, Stretton AO, Kaplan S. Genetic code: the ‘nonsense’ triplets for chain termination and their suppression. Nature. 1965;206:994–8.CrossRefPubMedGoogle Scholar
  192. 192.
    Nakamura Y, Ito K, Isaksson LA. Emerging understanding of translation termination. Cell. 1996;87:147–50.CrossRefPubMedGoogle Scholar
  193. 193.
    Buckingham RH, Grentzmann G, Kisselev L. Polypeptide chain release factors. Mol Microbiol. 1997;24:449–56.CrossRefPubMedGoogle Scholar
  194. 194.
    Jorgensen F, Adamski FM, Tate WP, Kurland CG. Release factor-dependent false stops are infrequent in Escherichia coli. J Mol Biol. 1993;230:41–50. doi: 10.1006/jmbi.1993.1124.CrossRefPubMedGoogle Scholar
  195. 195.
    Nakamura Y, Ito K, Ehrenberg M. Mimicry grasps reality in translation termination. Cell. 2000;101:349–52.CrossRefPubMedGoogle Scholar
  196. 196.
    Kisselev LL, Buckingham RH. Translational termination comes of age. Trends Biochem Sci. 2000;25:561–6.CrossRefPubMedGoogle Scholar
  197. 197.
    Stansfield I, Jones KM, Kushnirov VV, Dagkesamanskaya AR, Poznyakovski AI, Paushkin SV, Nierras CR, Cox BS, Ter-Avanesyan MD, Tuite MF. The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. The EMBO J. 1995;14:4365–73.PubMedGoogle Scholar
  198. 198.
    Zhouravleva G, Frolova L, Le Goff X, Le Guellec R, Inge-Vechtomov S, Kisselev L, Philippe M. Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. The EMBO J. 1995;14:4065–72.PubMedGoogle Scholar
  199. 199.
    Alkalaeva EZ, Pisarev AV, Frolova LY, Kisselev LL, Pestova TV. In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell. 2006;125:1125–36. doi: 10.1016/j.cell.2006.04.035.CrossRefPubMedGoogle Scholar
  200. 200.
    Pisareva VP, Pisarev AV, Hellen CU, Rodnina MV, Pestova TV. Kinetic analysis of interaction of eukaryotic release factor 3 with guanine nucleotides. J Biol Chem. 2006;281:40224–35. doi: 10.1074/jbc.M607461200.CrossRefPubMedGoogle Scholar
  201. 201.
    Hauryliuk V, Zavialov A, Kisselev L, Ehrenberg M. Class-1 release factor eRF1 promotes GTP binding by class-2 release factor eRF3. Biochimie. 2006;88:747–57. doi: 10.1016/j.biochi.2006.06.001.CrossRefPubMedGoogle Scholar
  202. 202.
    Nakamura Y, Ito K. tRNA mimicry in translation termination and beyond. Wiley Interdiscip Rev RNA. 2011;2:647–68. doi: 10.1002/wrna.81.CrossRefPubMedGoogle Scholar
  203. 203.
    Shoemaker CJ, Green R. Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast. Proc Natl Acad Sci USA. 2011;108:E1392–8. doi: 10.1073/pnas.1113956108.CrossRefPubMedPubMedCentralGoogle Scholar
  204. 204.
    Brown A, Shao S, Murray J, Hegde RS, Ramakrishnan V. Structural basis for stop codon recognition in eukaryotes. Nature. 2015;524:493–6. doi: 10.1038/nature14896.CrossRefPubMedPubMedCentralGoogle Scholar
  205. 205.
    Frolova LY, Tsivkovskii RY, Sivolobova GF, Oparina NY, Serpinsky OI, Blinov VM, Tatkov SI, Kisselev LL. Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis. RNA. 1999;5:1014–20.CrossRefPubMedPubMedCentralGoogle Scholar
  206. 206.
    Chavatte L, Seit-Nebi A, Dubovaya V, Favre A. The invariant uridine of stop codons contacts the conserved NIKSR loop of human eRF1 in the ribosome. The EMBO J. 2002;21:5302–11.CrossRefPubMedGoogle Scholar
  207. 207.
    Bulygin KN, Khairulina YS, Kolosov PM, Ven’yaminova AG, Graifer DM, Vorobjev YN, Frolova LY, Kisselev LL, Karpova GG. Three distinct peptides from the N domain of translation termination factor eRF1 surround stop codon in the ribosome. RNA. 2010;16:1902–14. doi: 10.1261/rna.2066910.CrossRefPubMedPubMedCentralGoogle Scholar
  208. 208.
    Shaw JJ, Green R. Two distinct components of release factor function uncovered by nucleophile partitioning analysis. Mol Cell. 2007;28:458–67. doi: 10.1016/j.molcel.2007.09.007.CrossRefPubMedPubMedCentralGoogle Scholar
  209. 209.
    Trobro S, Aqvist J. A model for how ribosomal release factors induce peptidyl-tRNA cleavage in termination of protein synthesis. Mol Cell. 2007;27:758–66. doi: 10.1016/j.molcel.2007.06.032.CrossRefPubMedGoogle Scholar
  210. 210.
    Merkulova TI, Frolova LY, Lazar M, Camonis J, Kisselev LL. C-terminal domains of human translation termination factors eRF1 and eRF3 mediate their in vivo interaction. FEBS Lett. 1999;443:41–7.CrossRefPubMedGoogle Scholar
  211. 211.
    Cheng Z, Saito K, Pisarev AV, Wada M, Pisareva VP, Pestova TV, Gajda M, Round A, Kong C, Lim M, Nakamura Y, Svergun DI, Ito K, Song H. Structural insights into eRF3 and stop codon recognition by eRF1. Genes Dev. 2009;23:1106–18. doi: 10.1101/gad.1770109.CrossRefPubMedPubMedCentralGoogle Scholar
  212. 212.
    Kononenko AV, Mitkevich VA, Dubovaya VI, Kolosov PM, Makarov AA, Kisselev LL. Role of the individual domains of translation termination factor eRF1 in GTP binding to eRF3. Proteins. 2008;70:388–93. doi: 10.1002/prot.21544.CrossRefPubMedGoogle Scholar
  213. 213.
    Saito K, Kobayashi K, Wada M, Kikuno I, Takusagawa A, Mochizuki M, Uchiumi T, Ishitani R, Nureki O, Ito K. Omnipotent role of archaeal elongation factor 1 alpha (EF1alpha in translational elongation and termination, and quality control of protein synthesis. Proc Natl Acad Sci USA. 2010;107:19242–7. doi: 10.1073/pnas.1009599107.CrossRefPubMedPubMedCentralGoogle Scholar
  214. 214.
    Ito K, Uno M, Nakamura Y. A tripeptide ‘anticodon’ deciphers stop codons in messenger RNA. Nature. 2000;403:680–4. doi: 10.1038/35001115.CrossRefPubMedGoogle Scholar
  215. 215.
    Klaholz BP, Pape T, Zavialov AV, Myasnikov AG, Orlova EV, Vestergaard B, Ehrenberg M, van Heel M. Structure of the Escherichia coli ribosomal termination complex with release factor 2. Nature. 2003;421:90–4. doi: 10.1038/nature01225.CrossRefPubMedGoogle Scholar
  216. 216.
    Petry S, Brodersen DE, Murphy FVt, Dunham CM, Selmer M, Tarry MJ, Kelley AC, Ramakrishnan V. Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon. Cell. 2005; 123:1255–1266. doi: 10.1016/j.cell.2005.09.039.Google Scholar
  217. 217.
    Rawat UB, Zavialov AV, Sengupta J, Valle M, Grassucci RA, Linde J, Vestergaard B, Ehrenberg M, Frank J. A cryo-electron microscopic study of ribosome-bound termination factor RF2. Nature. 2003;421:87–90. doi: 10.1038/nature01224.CrossRefPubMedGoogle Scholar
  218. 218.
    Rawat U, Gao H, Zavialov A, Gursky R, Ehrenberg M, Frank J. Interactions of the release factor RF1 with the ribosome as revealed by cryo-EM. J Mol Biol. 2006;357:1144–53. doi: 10.1016/j.jmb.2006.01.038.CrossRefPubMedGoogle Scholar
  219. 219.
    Bertram G, Bell HA, Ritchie DW, Fullerton G, Stansfield I. Terminating eukaryote translation: domain 1 of release factor eRF1 functions in stop codon recognition. RNA. 2000;6:1236–47.CrossRefPubMedPubMedCentralGoogle Scholar
  220. 220.
    Frolova L, Seit-Nebi A, Kisselev L. Highly conserved NIKS tetrapeptide is functionally essential in eukaryotic translation termination factor eRF1. RNA. 2002;8:129–36.CrossRefPubMedPubMedCentralGoogle Scholar
  221. 221.
    Inagaki Y, Blouin C, Doolittle WF, Roger AJ. Convergence and constraint in eukaryotic release factor 1 (eRF1) domain 1: the evolution of stop codon specificity. Nucleic Acids Res. 2002;30:532–44.CrossRefPubMedPubMedCentralGoogle Scholar
  222. 222.
    Weixlbaumer A, Jin H, Neubauer C, Voorhees RM, Petry S, Kelley AC, Ramakrishnan V. Insights into translational termination from the structure of RF2 bound to the ribosome. Science. 2008;322:953–6. doi: 10.1126/science.1164840.CrossRefPubMedPubMedCentralGoogle Scholar
  223. 223.
    Korostelev AA. Structural aspects of translation termination on the ribosome. RNA. 2011;17:1409–21. doi: 10.1261/rna.2733411.CrossRefPubMedPubMedCentralGoogle Scholar
  224. 224.
    Jin H, Kelley AC, Ramakrishnan V. Crystal structure of the hybrid state of ribosome in complex with the guanosine triphosphatase release factor 3. Proc Natl Acad Sci USA. 2011;108:15798–803. doi: 10.1073/pnas.1112185108.CrossRefPubMedPubMedCentralGoogle Scholar
  225. 225.
    Zhou J, Lancaster L, Trakhanov S, Noller HF. Crystal structure of release factor RF3 trapped in the GTP state on a rotated conformation of the ribosome. RNA. 2012;18:230–40. doi: 10.1261/rna.031187.111.CrossRefPubMedPubMedCentralGoogle Scholar
  226. 226.
    Freistroffer DV, Pavlov MY, MacDougall J, Buckingham RH, Ehrenberg M. Release factor RF3 in E.coli accelerates the dissociation of release factors RF1 and RF2 from the ribosome in a GTP-dependent manner. The EMBO J. 1997;16:4126–33. doi: 10.1093/emboj/16.13.4126.CrossRefPubMedGoogle Scholar
  227. 227.
    Gao H, Zhou Z, Rawat U, Huang C, Bouakaz L, Wang C, Cheng Z, Liu Y, Zavialov A, Gursky R, Sanyal S, Ehrenberg M, Frank J, Song H. RF3 induces ribosomal conformational changes responsible for dissociation of class I release factors. Cell. 2007;129:929–41. doi: 10.1016/j.cell.2007.03.050.CrossRefPubMedGoogle Scholar
  228. 228.
    Zavialov AV, Buckingham RH, Ehrenberg M. A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3. Cell. 2001;107:115–24.CrossRefPubMedGoogle Scholar
  229. 229.
    Salas-Marco J, Bedwell DM. GTP hydrolysis by eRF3 facilitates stop codon decoding during eukaryotic translation termination. Mol Cell Biol. 2004;24:7769–78. doi: 10.1128/MCB.24.17.7769-7778.2004.CrossRefPubMedPubMedCentralGoogle Scholar
  230. 230.
    Zaher HS, Green R. Quality control by the ribosome following peptide bond formation. Nature. 2009;457:161–6. doi: 10.1038/nature07582.CrossRefPubMedGoogle Scholar
  231. 231.
    Zaher HS, Green R. A primary role for release factor 3 in quality control during translation elongation in Escherichia coli. Cell. 2011;147:396–408. doi: 10.1016/j.cell.2011.08.045.CrossRefPubMedPubMedCentralGoogle Scholar
  232. 232.
    Kushnirov VV, Ter-Avanesyan MD, Telckov MV, Surguchov AP, Smirnov VN, Inge-Vechtomov SG. Nucleotide sequence of the SUP2 (SUP35) gene of Saccharomyces cerevisiae. Gene. 1988;66:45–54.CrossRefPubMedGoogle Scholar
  233. 233.
    Wilson PG, Culbertson MR. SUF12 suppressor protein of yeast. A fusion protein related to the EF-1 family of elongation factors. J Mol Biol. 1988;199:559–73.CrossRefPubMedGoogle Scholar
  234. 234.
    Grentzmann G, Brechemier-Baey D, Heurgue V, Mora L, Buckingham RH. Localization and characterization of the gene encoding release factor RF3 in Escherichia coli. Proc Natl Acad Sci USA. 1994;91:5848–52.CrossRefPubMedPubMedCentralGoogle Scholar
  235. 235.
    Mikuni O, Ito K, Moffat J, Matsumura K, McCaughan K, Nobukuni T, Tate W, Nakamura Y. Identification of the prfC gene, which encodes peptide-chain-release factor 3 of Escherichia coli. Proc Natl Acad Sci USA. 1994;91:5798–802.CrossRefPubMedPubMedCentralGoogle Scholar
  236. 236.
    Caskey CT, Beaudet AL, Scolnick EM, Rosman M. Hydrolysis of fMet-tRNA by peptidyl transferase. Proc Natl Acad Sci USA. 1971;68:3163–7.CrossRefPubMedPubMedCentralGoogle Scholar
  237. 237.
    Zavialov AV, Mora L, Buckingham RH, Ehrenberg M. Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3. Mol Cell. 2002;10:789–98.CrossRefPubMedGoogle Scholar
  238. 238.
    Frolova L, Le Goff X, Rasmussen HH, Cheperegin S, Drugeon G, Kress M, Arman I, Haenni AL, Celis JE, Philippe M, et al. A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor. Nature. 1994;372:701–3. doi: 10.1038/372701a0.CrossRefPubMedGoogle Scholar
  239. 239.
    Stansfield I, Tuite MF. Polypeptide chain termination in Saccharomyces cerevisiae. Curr Genet. 1994;25:385–95.CrossRefPubMedGoogle Scholar
  240. 240.
    Kobayashi T, Funakoshi Y, Hoshino S, Katada T. The GTP-binding release factor eRF3 as a key mediator coupling translation termination to mRNA decay. J Biol Chem. 2004;279:45693–700. doi: 10.1074/jbc.M405163200.CrossRefPubMedGoogle Scholar
  241. 241.
    Leipe DD, Wolf YI, Koonin EV, Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol. 2002;317:41–72. doi: 10.1006/jmbi.2001.5378.CrossRefPubMedGoogle Scholar
  242. 242.
    Inagaki Y, Dacks JB, Doolittle WF, Watanabe KI, Ohama T. Evolutionary relationship between dinoflagellates bearing obligate diatom endosymbionts: insight into tertiary endosymbiosis. Int J Syst Evol Microbiol. 2000;50(Pt 6):2075–81. doi: 10.1099/00207713-50-6-2075.CrossRefPubMedGoogle Scholar
  243. 243.
    Atkinson GC, Baldauf SL, Hauryliuk V. Evolution of nonstop, no-go and nonsense-mediated mRNA decay and their termination factor-derived components. BMC Evol Biol. 2008;8:290. doi: 10.1186/1471-2148-8-290.CrossRefPubMedPubMedCentralGoogle Scholar
  244. 244.
    Inagaki Y, Blouin C, Susko E, Roger AJ. Assessing functional divergence in EF-1alpha and its paralogs in eukaryotes and archaebacteria. Nucleic Acids Res. 2003;31:4227–37.CrossRefPubMedPubMedCentralGoogle Scholar
  245. 245.
    Inagaki Y. Ford Doolittle W. Evolution of the eukaryotic translation termination system: origins of release factors. Mol Biol Evol. 2000;17:882–9.CrossRefPubMedGoogle Scholar
  246. 246.
    Dontsova M, Frolova L, Vassilieva J, Piendl W, Kisselev L, Garber M. Translation termination factor aRF1 from the archaeon Methanococcus jannaschii is active with eukaryotic ribosomes. FEBS Lett. 2000;472:213–6.CrossRefPubMedGoogle Scholar
  247. 247.
    Kisselev L. Polypeptide release factors in prokaryotes and eukaryotes: same function, different structure. Structure. 2002;10:8–9.CrossRefPubMedGoogle Scholar
  248. 248.
    Ito K, Ebihara K, Nakamura Y. The stretch of C-terminal acidic amino acids of translational release factor eRF1 is a primary binding site for eRF3 of fission yeast. RNA. 1998;4:958–72.CrossRefPubMedPubMedCentralGoogle Scholar
  249. 249.
    Mora L, Zavialov A, Ehrenberg M, Buckingham RH. Stop codon recognition and interactions with peptide release factor RF3 of truncated and chimeric RF1 and RF2 from Escherichia coli. Mol Microbiol. 2003;50:1467–76.CrossRefPubMedGoogle Scholar
  250. 250.
    Scolnick E, Tompkins R, Caskey T, Nirenberg M. Release factors differing in specificity for terminator codons. Proc Natl Acad Sci USA. 1968;61:768–74.CrossRefPubMedPubMedCentralGoogle Scholar
  251. 251.
    Mora L, Heurgue-Hamard V, Champ S, Ehrenberg M, Kisselev LL, Buckingham RH. The essential role of the invariant GGQ motif in the function and stability in vivo of bacterial release factors RF1 and RF2. Mol Microbiol. 2003;47:267–75.CrossRefPubMedGoogle Scholar
  252. 252.
    Heurgue-Hamard V, Champ S, Engstrom A, Ehrenberg M, Buckingham RH. The hemK gene in Escherichia coli encodes the N(5)-glutamine methyltransferase that modifies peptide release factors. The EMBO J. 2002;21:769–78. doi: 10.1093/emboj/21.4.769.CrossRefPubMedGoogle Scholar
  253. 253.
    Heurgue-Hamard V, Graille M, Scrima N, Ulryck N, Champ S, van Tilbeurgh H, Buckingham RH. The zinc finger protein Ynr046w is plurifunctional and a component of the eRF1 methyltransferase in yeast. J Biol Chem. 2006;281:36140–8. doi: 10.1074/jbc.M608571200.CrossRefPubMedGoogle Scholar
  254. 254.
    Graille M, Figaro S, Kervestin S, Buckingham RH, Liger D, Heurgue-Hamard V. Methylation of class I translation termination factors: structural and functional aspects. Biochimie. 2012;94:1533–43. doi: 10.1016/j.biochi.2012.01.005.CrossRefPubMedGoogle Scholar
  255. 255.
    Hoshino S, Hosoda N, Araki Y, Kobayashi T, Uchida N, Funakoshi Y, Katada T. Novel function of the eukaryotic polypeptide-chain releasing factor 3 (eRF3/GSPT) in the mRNA degradation pathway. Biochemistry Biokhimiia. 1999;64:1367–72.PubMedGoogle Scholar
  256. 256.
    Hosoda N, Kobayashi T, Uchida N, Funakoshi Y, Kikuchi Y, Hoshino S, Katada T. Translation termination factor eRF3 mediates mRNA decay through the regulation of deadenylation. J Biol Chem. 2003;278:38287–91. doi: 10.1074/jbc.C300300200.CrossRefPubMedGoogle Scholar
  257. 257.
    Graille M, Chaillet M, van Tilbeurgh H. Structure of yeast Dom34: a protein related to translation termination factor Erf1 and involved in No-Go decay. J Biol Chem. 2008;283:7145–54. doi: 10.1074/jbc.M708224200.CrossRefPubMedGoogle Scholar
  258. 258.
    Moreira D, Kervestin S, Jean-Jean O, Philippe H. Evolution of eukaryotic translation elongation and termination factors: variations of evolutionary rate and genetic code deviations. Mol Biol Evol. 2002;19:189–200.CrossRefPubMedGoogle Scholar
  259. 259.
    Drugeon G, Jean-Jean O, Frolova L, Le Goff X, Philippe M, Kisselev L, Haenni AL. Eukaryotic release factor 1 (eRF1) abolishes readthrough and competes with suppressor tRNAs at all three termination codons in messenger RNA. Nucleic Acids Res. 1997;25:2254–8.CrossRefPubMedPubMedCentralGoogle Scholar
  260. 260.
    Le Goff X, Philippe M, Jean-Jean O. Overexpression of human release factor 1 alone has an antisuppressor effect in human cells. Mol Cell Biol. 1997;17:3164–72.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Sandra Eltschinger
    • 1
  • Peter Bütikofer
    • 1
  • Michael Altmann
    • 1
    Email author
  1. 1.Institute of Biochemistry and Molecular Medicine (IBMM)BernSwitzerland

Personalised recommendations