1932

Abstract

Elongation factor P (EF-P) binds to ribosomes requiring assistance with the formation of oligo-prolines. In order for EF-P to associate with paused ribosomes, certain tRNAs with specific -arm residues must be present in the peptidyl site, e.g., tRNAPro. Once EF-P is accommodated into the ribosome and bound to Pro-tRNAPro, productive synthesis of the peptide bond occurs. The underlying mechanism by which EF-P facilitates this reaction seems to have entropic origins. Maximal activity of EF-P requires a posttranslational modification in , , and . Each of these modifications is distinct and ligated onto its respective EF-P through entirely convergent means. Here we review the facets of translation elongation that are controlled by EF-P, with a particular focus on the purpose behind the many different modifications of EF-P.

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2017-09-08
2024-06-21
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Literature Cited

  1. Aoki H, Adams SL, Chung DG, Yaguchi M, Chuang SE, Ganoza MC. 1.  1991. Cloning, sequencing and overexpression of the gene for prokaryotic factor EF-P involved in peptide bond synthesis. Nucleic Acids Res 19:6215–20 [Google Scholar]
  2. Aoki H, Dekany K, Adams S-L, Ganoza MC. 2.  1997. The gene encoding the elongation factor P protein is essential for viability and is required for protein synthesis. J. Biol. Chem. 272:32254–59 [Google Scholar]
  3. Bailly M, de Crécy-Lagard V. 3.  2010. Predicting the pathway involved in post-translational modification of elongation factor P in a subset of bacterial species. Biol. Direct 5:3 [Google Scholar]
  4. Balibar CJ, Iwanowicz D, Dean CR. 4.  2013. Elongation factor P is dispensable in Escherichia coli. Pseudomonas aeruginosa. Curr. Microbiol. 67:293–99 [Google Scholar]
  5. Blaha G, Stanley RE, Steitz TA. 5.  2009. Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science 325:966–70 [Google Scholar]
  6. Blattner FR, 3rd Plunkett G, Bloch CA, Perna NT, Burland V. 6.  et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453–62 [Google Scholar]
  7. Bullwinkle TJ, Ibba M. 7.  2016. Translation quality control is critical for bacterial responses to amino acid stress. PNAS 113:2252–57 [Google Scholar]
  8. Bullwinkle TJ, Zou SB, Rajkovic A, Hersch SJ, Elgamal S. 8.  et al. 2013. (R)-β-lysine-modified elongation factor P functions in translation elongation. J. Biol. Chem. 288:4416–23 [Google Scholar]
  9. Chan PP, Lowe TM. 9.  2009. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res 37:D93–97 [Google Scholar]
  10. Choi S, Choe J. 10.  2011. Crystal structure of elongation factor P from Pseudomonas aeruginosa at 1.75 Å resolution. Proteins 79:1688–93 [Google Scholar]
  11. Dana A, Tuller T. 11.  2014. The effect of tRNA levels on decoding times of mRNA codons. Nucleic Acids Res 42:9171–81 [Google Scholar]
  12. Dever TE, Gutierrez E, Shin BS. 12.  2014. The hypusine-containing translation factor eIF5A. Crit. Rev. Biochem. Mol. Biol. 49:413–25 [Google Scholar]
  13. Doerfel LK, Wohlgemuth I, Kothe C, Peske F, Urlaub H, Rodnina MV. 13.  2012. EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339:85–88 [Google Scholar]
  14. Doerfel LK, Wohlgemuth I, Kubyshkin V, Starosta AL, Wilson DN. 14.  et al. 2015. Entropic contribution of elongation factor P to proline positioning at the catalytic center of the ribosome. J. Am. Chem. Soc. 137:12997–3006 [Google Scholar]
  15. Elgamal S, Artsimovitch I, Ibba M. 15.  2016. Maintenance of transcription-translation coupling by elongation factor P. mBio 7:e01373–16 [Google Scholar]
  16. Elgamal S, Katz A, Hersch SJ, Newsom D, White P. 16.  et al. 2014. EF-P dependent pauses integrate proximal and distal signals during translation. PLOS Genet 10:e1004553 [Google Scholar]
  17. Fox GE. 17.  2010. Origin and evolution of the ribosome. Cold Spring Harb. Perspect. Biol. 2:a003483 [Google Scholar]
  18. Gamper HB, Masuda I, Frenkel-Morgenstern M, Hou YM. 18.  2015. Maintenance of protein synthesis reading frame by EF-P and m1G37-tRNA. Nat. Commun. 6:7226 [Google Scholar]
  19. Glick BR, Ganoza MC. 19.  1975. Identification of a soluble protein that stimulates peptide bond synthesis. PNAS 72:4257–60 [Google Scholar]
  20. Golyshin PN, Werner J, Chernikova TN, Tran H, Ferrer M. 20.  et al. 2013. Genome sequence of Thalassolituus oleivorans MIL-1 (DSM 14913T). Genome Announc 1:e0014113 [Google Scholar]
  21. Green R, Noller HF. 21.  1997. Ribosomes and translation. Annu. Rev. Biochem. 66:679–716 [Google Scholar]
  22. Gutierrez E, Shin BS, Woolstenhulme CJ, Kim JR, Saini P. 22.  et al. 2013. eIF5A promotes translation of polyproline motifs. Mol. Cell 51:35–45 [Google Scholar]
  23. Hanawa-Suetsugu K, Sekine S-i, Sakai H, Hori-Takemoto C, Terada T. 23.  et al. 2004. Crystal structure of elongation factor P from Thermus thermophilus HB8. PNAS 101:9595–600 [Google Scholar]
  24. Hersch SJ, Elgamal S, Katz A, Ibba M, Navarre WW. 24.  2014. Translation initiation rate determines the impact of ribosome stalling on bacterial protein synthesis. J. Biol. Chem. 289:28160–71 [Google Scholar]
  25. Hersch SJ, Wang M, Zou SB, Moon K-M, Foster LJ. 25.  et al. 2013. Divergent protein motifs direct elongation factor P-mediated translational regulation in Salmonella enterica and Escherichia coli. mBio 4:e00180–13 [Google Scholar]
  26. Hovmoller S, Zhou T, Ohlson T. 26.  2002. Conformations of amino acids in proteins. Acta Crystallogr. Sect. D Biol. Crystallogr. 58:768–76 [Google Scholar]
  27. Juhling F, Morl M, Hartmann RK, Sprinzl M, Stadler PF, Putz J. 27.  2009. tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res 37:D159–62 [Google Scholar]
  28. Karlyshev AV, Nadarajah S, Abramov VM. 28.  2013. Draft genome sequence of Lactobacillus jensenii strain MD IIE-70(2). Genome Announc 1:e01005–13 [Google Scholar]
  29. Katoh T, Tajima K, Suga H. 29.  2017. Consecutive elongation of d-amino acids in translation. Cell Chem. Biol. 24:46–54 [Google Scholar]
  30. Katoh T, Wohlgemuth I, Nagano M, Rodnina MV, Suga H. 30.  2016. Essential structural elements in tRNA(Pro) for EF-P-mediated alleviation of translation stalling. Nat. Commun. 7:11657 [Google Scholar]
  31. Katz A, Solden L, Zou SB, Navarre WW, Ibba M. 31.  2014. Molecular evolution of protein-RNA mimicry as a mechanism for translational control. Nucleic Acids Res 42:3261–71 [Google Scholar]
  32. Kobayashi K, Katz A, Rajkovic A, Ishii R, Branson OE. 32.  et al. 2014. The non-canonical hydroxylase structure of YfcM reveals a metal ion-coordination motif required for EF-P hydroxylation. Nucleic Acids Res 42:12295–305 [Google Scholar]
  33. Kolitz SE, Takacs JE, Lorsch JR. 33.  2009. Kinetic and thermodynamic analysis of the role of start codon/anticodon base pairing during eukaryotic translation initiation. RNA 15:138–52 [Google Scholar]
  34. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G. 34.  et al. 1997. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:249–56 [Google Scholar]
  35. Lam JS, Taylor VL, Islam ST, Hao Y, Kocíncová D. 35.  2011. Genetic and functional diversity of Pseudomonas aeruginosa lipopolysaccharide. Front. Microbiol. 2:118 [Google Scholar]
  36. Lassak J, Keilhauer EC, Fürst M, Wuichet K, Gödeke J. 36.  et al. 2015. Arginine-rhamnosylation as new strategy to activate translation elongation factor P. Nat. Chem. Biol 11:266–70 2015. Corrigendum Nat. Chem. Biol. 11:299 [Google Scholar]
  37. Lassak J, Wilson DN, Jung K. 37.  2016. Stall no more at polyproline stretches with the translation elongation factors EF-P and IF-5A. Mol. Microbiol. 99:219–35 [Google Scholar]
  38. Liang ST, Xu YC, Dennis P, Bremer H. 38.  2000. mRNA composition and control of bacterial gene expression. J. Bacteriol. 182:3037–44 [Google Scholar]
  39. Lindhout T, Lau PC, Brewer D, Lam JS. 39.  2009. Truncation in the core oligosaccharide of lipopolysaccharide affects flagella-mediated motility in Pseudomonas aeruginosa PAO1 via modulation of cell surface attachment. Microbiology 155:3449–60 [Google Scholar]
  40. Maini R, Umemoto S, Suga H. 40.  2016. Ribosome-mediated synthesis of natural product-like peptides via cell-free translation. Curr. Opin. Chem. Biol. 34:44–52 [Google Scholar]
  41. Meeske AJ, Rodrigues CD, Brady J, Lim HC, Bernhardt TG, Rudner DZ. 41.  2016. High-throughput genetic screens identify a large and diverse collection of new sporulation genes in Bacillus subtilis. PLOS Biol. 14:e1002341 [Google Scholar]
  42. Moine H, Romby P, Springer M, Grunberg-Manago M, Ebel JP. 42.  et al. 1988. Messenger RNA structure and gene regulation at the translational level in Escherichia coli: the case of threonine:tRNAThr ligase. PNAS 85:7892–96 [Google Scholar]
  43. Navarre WW, Zou SB, Roy H, Xie JL, Savchenko A. 43.  et al. 2010. PoxA, YjeK, and elongation factor P coordinately modulate virulence and drug resistance in Salmonella enterica. Mol. Cell 39:209–21 [Google Scholar]
  44. Ohashi Y, Inaoka T, Kasai K, Ito Y, Okamoto S. 44.  et al. 2003. Expression profiling of translation-associated genes in sporulating Bacillus subtilis and consequence of sporulation by gene inactivation. Biosci. Biotechnol. Biochem. 67:2245–53 [Google Scholar]
  45. Park S, Jung YT, Park JM, Yoon JH. 45.  2014. Pseudohongiella acticola sp. nov., a novel gammaproteobacterium isolated from seawater, and emended description of the genus Pseudohongiella. Antonie Van Leeuwenhoek 106:809–15 [Google Scholar]
  46. Pavlov MY, Watts RE, Tan Z, Cornish VW, Ehrenberg M, Forster AC. 46.  2009. Slow peptide bond formation by proline and other N-alkylamino acids in translation. PNAS 106:50–54 [Google Scholar]
  47. Peil L, Starosta AL, Virumäe K, Atkinson GC, Tenson T. 47.  et al. 2012. Lys34 of translation elongation factor EF-P is hydroxylated by YfcM. Nat. Chem. Biol. 8:695–97 [Google Scholar]
  48. Proshkin S, Rahmouni AR, Mironov A, Nudler E. 48.  2010. Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328:504–8 [Google Scholar]
  49. Prunetti L, Graf M, Blaby IK, Peil L, Makkay AM. 49.  et al. 2016. Deciphering the translation initiation factor 5a modification pathway in halophilic Archaea. Archaea 2016:7316725 [Google Scholar]
  50. Rahim R, Ochsner UA, Olvera C, Graninger M, Messner P. 50.  et al. 2001. Cloning and functional characterization of the Pseudomonas aeruginosa rhlC gene that encodes rhamnosyltransferase 2, an enzyme responsible for di-rhamnolipid biosynthesis. Mol. Microbiol. 40:708–18 [Google Scholar]
  51. Rajkovic A, Erickson S, Witzky A, Branson OE, Seo J. 51.  et al. 2015. Cyclic rhamnosylated elongation factor P establishes antibiotic resistance in Pseudomonas aeruginosa. mBio 6:e00823 [Google Scholar]
  52. Rajkovic A, Hummels KR, Witzky A, Erickson S, Gafken PR. 52.  et al. 2016. Translation control of swarming proficiency in Bacillus subtilis by 5-amino-pentanolylated elongation factor P. J. Biol. Chem. 291:10976–85 [Google Scholar]
  53. Roy H, Zou SB, Bullwinkle TJ, Wolfe BS, Gilreath MS. 53.  et al. 2011. The tRNA synthetase paralog PoxA modifies elongation factor-P with (R)-β-lysine. Nat. Chem. Biol. 7:667–69 [Google Scholar]
  54. Schirm M, Arora SK, Verma A, Vinogradov E, Thibault P. 54.  et al. 2004. Structural and genetic characterization of glycosylation of type A flagellin in Pseudomonas aeruginosa. J. Bacteriol. 186:2523–31 [Google Scholar]
  55. Singh A, Vaidya B, Tanuku NR, Pinnaka AK. 55.  2015. Nitrincola nitratireducens sp. nov. isolated from a haloalkaline crater lake. Syst. Appl. Microbiol. 38:555–62 [Google Scholar]
  56. Starosta AL, Lassak J, Peil L, Atkinson GC, Woolstenhulme CJ. 56.  et al. 2014. A conserved proline triplet in Val-tRNA synthetase and the origin of elongation factor P. Cell Rep 9:476–83 [Google Scholar]
  57. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P. 57.  et al. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–64 [Google Scholar]
  58. Ude S, Lassak J, Starosta AL, Kraxenberger T, Wilson DN, Jung K. 58.  2013. Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science 339:82–85 [Google Scholar]
  59. Woolstenhulme CJ, Guydosh NR, Green R, Buskirk AR. 59.  2015. High-precision analysis of translational pausing by ribosome profiling in bacteria lacking EFP. Cell Rep 11:13–21 [Google Scholar]
  60. Yanagisawa T, Takahashi H, Suzuki T, Masuda A, Dohmae N, Yokoyama S. 60.  2016. Neisseria meningitidis translation elongation factor P and its active-site arginine residue are essential for cell viability. PLOS ONE 11:e0147907 [Google Scholar]
  61. Yanofsky C, Horn V. 61.  1994. Role of regulatory features of the trp operon of Escherichia coli in mediating a response to a nutritional shift. J. Bacteriol. 176:6245–54 [Google Scholar]
  62. Yu H, Zhao Y, Guo C, Gan Y, Huang H. 62.  2015. The role of proline substitutions within flexible regions on thermostability of luciferase. Biochim. Biophys. Acta 1854:65–72 [Google Scholar]
  63. Zou SB, Hersch SJ, Roy H, Wiggers JB, Leung AS. 63.  et al. 2012. Loss of elongation factor P disrupts bacterial outer membrane integrity. J. Bacteriol. 194:413–25 [Google Scholar]
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