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Taking a Step Back from Back-Translocation: an Integrative View of LepA/EF4's Cellular Function

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Article: e00653-16 | Published online: 17 Mar 2023

REFERENCES

  • Bourne HR, Sanders DA, McCormick F. 1990. The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348:125–132. https://doi.org/10.1038/348125a0.
  • Margus T, Remm M, Tenson T. 2007. Phylogenetic distribution of translational GTPases in bacteria. BMC Genomics 8:15. https://doi.org/10.1186/1471-2164-8-15.
  • Canonaco MA, Calogero RA, Gualerzi CO. 1986. Mechanism of translational initiation in prokaryotes. Evidence for a direct effect of IF2 on the activity of the 30 S ribosomal subunit. FEBS Lett 207:198–204.
  • Milon P, Carotti M, Konevega AL, Wintermeyer W, Rodnina MV, Gualerzi CO. 2010. The ribosome-bound initiation factor 2 recruits initiator tRNA to the 30S initiation complex. EMBO Rep 11:312–316. https://doi.org/10.1038/embor.2010.12.
  • March PE, Inouye M. 1985. 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 260:7206–7213.
  • March PE, Inouye M. 1985. GTP-binding membrane protein of Escherichia coli with sequence homology to initiation factor 2 and elongation factors Tu and G. Proc Natl Acad Sci U S A 82:7500–7504. https://doi.org/10.1073/pnas.82.22.7500.
  • Dibb NJ, Wolfe PB. 1986. lep operon proximal gene is not required for growth or secretion by Escherichia coli. J Bacteriol 166:83–87. https://doi.org/10.1128/jb.166.1.83-87.1986.
  • Qin Y, Polacek N, Vesper O, Staub E, Einfeldt E, Wilson DN, Nierhaus KH. 2006. The highly conserved LepA is a ribosomal elongation factor that back-translocates the ribosome. Cell 127:721–733. https://doi.org/10.1016/j.cell.2006.09.037.
  • Bauerschmitt H, Funes S, Herrmann JM. 2008. The membrane-bound GTPase Guf1 promotes mitochondrial protein synthesis under suboptimal conditions. J Biol Chem 283:17139–17146. https://doi.org/10.1074/jbc.M710037200.
  • Bijlsma JJ, Lie ALM, Nootenboom IC, Vandenbroucke-Grauls CM, Kusters JG. 2000. Identification of loci essential for the growth of Helicobacter pylori under acidic conditions. J Infect Dis 182:1566–1569. https://doi.org/10.1086/315855.
  • Pech M, Karim Z, Yamamoto H, Kitakawa M, Qin Y, Nierhaus KH. 2011. Elongation factor 4 (EF4/LepA) accelerates protein synthesis at increased Mg2+ concentrations. Proc Natl Acad Sci U S A 108:3199–3203. https://doi.org/10.1073/pnas.1012994108.
  • Yang F, Gao Y, Li Z, Chen L, Xia Z, Xu T, Qin Y. 2014. Mitochondrial EF4 links respiratory dysfunction and cytoplasmic translation in Caenorhabditis elegans. Biochim Biophys Acta 1837:1674–1683. https://doi.org/10.1016/j.bbabio.2014.05.353.
  • Yang F, Li Z, Hao J, Qin Y. 2014. EF4 knockout E. coli cells exhibit lower levels of cellular biosynthesis under acidic stress. Protein Cell 5:563–567. https://doi.org/10.1007/s13238-014-0050-3.
  • Balakrishnan R, Oman K, Shoji S, Bundschuh R, Fredrick K. 2014. The conserved GTPase LepA contributes mainly to translation initiation in Escherichia coli. Nucleic Acids Res 42:13370–13383. https://doi.org/10.1093/nar/gku1098.
  • Gagnon MG, Lin J, Steitz TA. 2016. Elongation factor 4 remodels the A-site tRNA on the ribosome. Proc Natl Acad Sci U S A 113:4994–4999. https://doi.org/10.1073/pnas.1522932113.
  • Liu H, Chen C, Zhang H, Kaur J, Goldman YE, Cooperman BS. 2011. The conserved protein EF4 (LepA) modulates the elongation cycle of protein synthesis. Proc Natl Acad Sci U S A 108:16223–16228. https://doi.org/10.1073/pnas.1103820108.
  • Evans RN, Blaha G, Bailey S, Steitz TA. 2008. The structure of LepA, the ribosomal back translocase. Proc Natl Acad Sci U S A 105:4673–4678. https://doi.org/10.1073/pnas.0801308105.
  • Diaconu M, Kothe U, Schlunzen F, Fischer N, Harms JM, Tonevitsky AG, Stark H, Rodnina MV, Wahl MC. 2005. Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell 121:991–1004. https://doi.org/10.1016/j.cell.2005.04.015.
  • Savelsbergh A, Mohr D, Wilden B, Wintermeyer W, Rodnina MV. 2000. Stimulation of the GTPase activity of translation elongation factor G by ribosomal protein L7/12. J Biol Chem 275:890–894. https://doi.org/10.1074/jbc.275.2.890.
  • Nechifor R, Murataliev M, Wilson KS. 2007. Functional interactions between the G′ subdomain of bacterial translation factor EF-G and ribosomal protein L7/L12. J Biol Chem 282:36998–37005. https://doi.org/10.1074/jbc.M707179200.
  • Laurberg M, Kristensen O, Martemyanov K, Gudkov AT, Nagaev I, Hughes D, Liljas A. 2000. Structure of a mutant EF-G reveals domain III and possibly the fusidic acid binding site. J Mol Biol 303:593–603. https://doi.org/10.1006/jmbi.2000.4168.
  • De Laurentiis EI, Wieden HJ. 2015. Identification of two structural elements important for ribosome-dependent GTPase activity of elongation factor 4 (EF4/LepA). Sci Rep 5:8573. https://doi.org/10.1038/srep08573.
  • Zhang D, Yan K, Liu G, Song G, Luo J, Shi Y, Cheng E, Wu S, Jiang T, Lou J, Gao N, Qin Y. 2016. EF4 disengages the peptidyl-tRNA CCA end and facilitates back-translocation on the 70S ribosome. Nat Struct Mol Biol 23:125–131. https://doi.org/10.1038/nsmb.3160.
  • Gao YG, Selmer M, Dunham CM, Weixlbaumer A, Kelley AC, Ramakrishnan V. 2009. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326:694–699. https://doi.org/10.1126/science.1179709.
  • Connell SR, Topf M, Qin Y, Wilson DN, Mielke T, Fucini P, Nierhaus KH, Spahn CM. 2008. A new tRNA intermediate revealed on the ribosome during EF4-mediated back-translocation. Nat Struct Mol Biol 15:910–915. https://doi.org/10.1038/nsmb.1469.
  • Kumar V, Chen Y, Ero R, Ahmed T, Tan J, Li Z, Wong AS, Bhushan S, Gao YG. 2015. Structure of BipA in GTP form bound to the ratcheted ribosome. Proc Natl Acad Sci U S A 112:10944–10949. https://doi.org/10.1073/pnas.1513216112.
  • Gagnon MG, Lin J, Bulkley D, Steitz TA. 2014. Crystal structure of elongation factor 4 bound to a clockwise ratcheted ribosome. Science 345:684–687. https://doi.org/10.1126/science.1253525.
  • Maracci C, Rodnina MV. 2016. Review: translational GTPases. Biopolymers 105:463–475. https://doi.org/10.1002/bip.22832.
  • Kiss E, Huguet T, Poinsot V, Batut J. 2004. The typA gene is required for stress adaptation as well as for symbiosis of Sinorhizobium meliloti 1021 with certain Medicago truncatula lines. Mol Plant Microbe Interact 17:235–244. https://doi.org/10.1094/MPMI.2004.17.3.235.
  • Pfennig PL, Flower AM. 2001. BipA is required for growth of Escherichia coli K12 at low temperature. Mol Genet Genomics 266:313–317. https://doi.org/10.1007/s004380100559.
  • Starosta AL, Lassak J, Jung K, Wilson DN. 2014. The bacterial translation stress response. FEMS Microbiol Rev 38:1172–1201. https://doi.org/10.1111/1574-6976.12083.
  • Choudhury P, Flower AM. 2015. Efficient assembly of ribosomes is inhibited by deletion of bipA in Escherichia coli. J Bacteriol 197:1819–1827. https://doi.org/10.1128/JB.00023-15.
  • Colca JR, McDonald WG, Waldon DJ, Thomasco LM, Gadwood RC, Lund ET, Cavey GS, Mathews WR, Adams LD, Cecil ET, Pearson JD, Bock JH, Mott JE, Shinabarger DL, Xiong L, Mankin AS. 2003. Cross-linking in the living cell locates the site of action of oxazolidinone antibiotics. J Biol Chem 278:21972–21979. https://doi.org/10.1074/jbc.M302109200.
  • Leach KL, Swaney SM, Colca JR, McDonald WG, Blinn JR, Thomasco LM, Gadwood RC, Shinabarger D, Xiong L, Mankin AS. 2007. The site of action of oxazolidinone antibiotics in living bacteria and in human mitochondria. Mol Cell 26:393–402. https://doi.org/10.1016/j.molcel.2007.04.005.
  • Kumar V, Ero R, Ahmed T, Goh KJ, Zhan Y, Bhushan S, Gao YG. 2016. Structure of the GTP form of elongation factor 4 (EF4) bound to the ribosome. J Biol Chem 291:12943–12950. https://doi.org/10.1074/jbc.M116.725945.
  • Connell SR, Takemoto C, Wilson DN, Wang H, Murayama K, Terada T, Shirouzu M, Rost M, Schuler M, Giesebrecht J, Dabrowski M, Mielke T, Fucini P, Yokoyama S, Spahn CM. 2007. Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors. Mol Cell 25:751–764. https://doi.org/10.1016/j.molcel.2007.01.027.
  • Shoji S, Janssen BD, Hayes CS, Fredrick K. 2010. Translation factor LepA contributes to tellurite resistance in Escherichia coli but plays no apparent role in the fidelity of protein synthesis. Biochimie 92:157–163. https://doi.org/10.1016/j.biochi.2009.11.002.
  • Liu H, Pan D, Pech M, Cooperman BS. 2010. Interrupted catalysis: the EF4 (LepA) effect on back-translocation. J Mol Biol 396:1043–1052. https://doi.org/10.1016/j.jmb.2009.12.043.
  • Konevega AL, Fischer N, Semenkov YP, Stark H, Wintermeyer W, Rodnina MV. 2007. Spontaneous reverse movement of mRNA-bound tRNA through the ribosome. Nat Struct Mol Biol 14:318–324. https://doi.org/10.1038/nsmb1221.
  • Arenz S, Bock LV, Graf M, Innis CA, Beckmann R, Grubmuller H, Vaiana AC, Wilson DN. 2016. A combined cryo-EM and molecular dynamics approach reveals the mechanism of ErmBL-mediated translation arrest. Nat Commun 7:12026. https://doi.org/10.1038/ncomms12026.
  • Gibbs MR, Moon K-M, Chen M, Balakrishnan R, Foster LJ, Fredrick K. 2017. Conserved GTPase LepA (elongation factor 4) functions in biogenesis of the 30S subunit of the 70S ribosome. Proc Natl Acad Sci U S A 114:980–985. https://doi.org/10.1073/pnas.1613665114.
  • Kiser GL, Weinert TA. 1995. GUF1, a gene encoding a novel evolutionarily conserved GTPase in budding yeast. Yeast 11:1311–1316. https://doi.org/10.1002/yea.320111312.
  • Ji DL, Lin H, Chi W, Zhang LX. 2012. CpLEPA is critical for chloroplast protein synthesis under suboptimal conditions in Arabidopsis thaliana. PLoS One 7:e49746. https://doi.org/10.1371/journal.pone.0049746.
  • Gao Y, Bai X, Zhang D, Han C, Yuan J, Liu W, Cao X, Chen Z, Shangguan F, Zhu Z, Gao F, Qin Y. 2016. Mammalian elongation factor 4 regulates mitochondrial translation essential for spermatogenesis. Nat Struct Mol Biol 23:441–449. https://doi.org/10.1038/nsmb.3206.
  • Greber BJ, Ban N. 2016. Structure and function of the mitochondrial ribosome. Annu Rev Biochem 85:103–132. https://doi.org/10.1146/annurev-biochem-060815-014343.
  • De Laurentiis EI, Mercier E, Wieden HJ. 2016. The C-terminal helix of Pseudomonas aeruginosa elongation factor Ts tunes EF-Tu dynamics to modulate nucleotide exchange. J Biol Chem 291:23136–23148. https://doi.org/10.1074/jbc.M116.740381.
  • Grosjean H, Breton M, Sirand-Pugnet P, Tardy F, Thiaucourt F, Citti C, Barre A, Yoshizawa S, Fourmy D, de Crecy-Lagard V, Blanchard A. 2014. Predicting the minimal translation apparatus: lessons from the reductive evolution of mollicutes. PLoS Genet 10:e1004363. https://doi.org/10.1371/journal.pgen.1004363.

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