956
Views
5
CrossRef citations to date
0
Altmetric
Point-of-View

Is the cellular initiation of translation an exclusive property of the initiator tRNAs?

, &
Pages 675-680 | Received 12 Mar 2015, Accepted 17 Apr 2015, Published online: 25 Jul 2015

References

  • Nierhaus KH. The assembly of prokaryotic ribosomes. Biochimie 1991; 73:739-55; PMID:1764520; http://dx.doi.org/10.1016/0300-9084(91)90054-5
  • Neidhardt FC, Umbarger HE. in Escherichia coli and Salmonella. ASM Press, Washington, DC.; 1996; 13-16
  • Gold L. Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem 1988; 57:199-233; PMID:3052271; http://dx.doi.org/10.1146/annurev.bi.57.070188.001215
  • Julian P, Milon P, Agirrezabala X, Lasso G, Gil D, Rodnina MV, Valle M. The Cryo-EM structure of a complete 30S translation initiation complex from Escherichia coli. PLoS Biol 2011; 9:e1001095; PMID:21750663; http://dx.doi.org/10.1371/journal.pbio.1001095
  • Marshall RA, Aitken CE, Puglisi JD. GTP hydrolysis by IF2 guides progression of the ribosome into elongation. Mol Cell 2009; 35:37-47; PMID:19595714; http://dx.doi.org/10.1016/j.molcel.2009.06.008
  • Hartz D, McPheeters DS, Gold L. Selection of the initiator tRNA by Escherichia coli initiation factors. Genes Dev 1989; 3:1899-912; PMID:2695390; http://dx.doi.org/10.1101/gad.3.12a.1899
  • Antoun A, Pavlov MY, Lovmar M, Ehrenberg M. How initiation factors maximize the accuracy of tRNA selection in initiation of bacterial protein synthesis. Mol Cell 2006; 23:183-93; PMID:16857585; http://dx.doi.org/10.1016/j.molcel.2006.05.030
  • Antoun A, Pavlov MY, Lovmar M, Ehrenberg M. How initiation factors tune the rate of initiation of protein synthesis in bacteria. EMBO J 2006; 25:2539-50; PMID:16724118; http://dx.doi.org/10.1038/sj.emboj.7601140
  • Canonaco MA, Calogero RA, Gualerzi CO. Mechanism of translational initiation in prokaryotes. Evidence for a direct effect of IF2 on the activity of the 30 S ribosomal subunit. FEBS Lett 1986; 207:198-204; PMID:3533628; http://dx.doi.org/10.1016/0014-5793(86)81488-0
  • Gualerzi CO, Brandi L, Caserta E, Garofalo C, Lammi M, La Teana A, Petrelli D, Spurio R, Tomsic J, Pon CL. Initiation factors in the early events of mRNA translation in bacteria. Cold Spring Harb Symp Quant Biol 2001; 66:363-76; PMID:12762039; http://dx.doi.org/10.1101/sqb.2001.66.363
  • Gualerzi CO, Pon CL. Initiation of mRNA translation in prokaryotes. Biochemistry 1990; 29:5881-89; PMID:2200518; http://dx.doi.org/10.1021/bi00477a001
  • La Teana A, Pon CL, Gualerzi CO. Late events in translation initiation. Adjustment of fMet-tRNA in the ribosomal P-site. J Mol Biol 1996; 256:667-75; PMID:8642589; http://dx.doi.org/10.1006/jmbi.1996.0116
  • Milon P, Konevega AL, Gualerzi CO, Rodnina MV. Kinetic checkpoint at a late step in translation initiation. Mol Cell 2008; 30:712-20; PMID:18570874; http://dx.doi.org/10.1016/j.molcel.2008.04.014
  • Tomsic J, Vitali LA, Daviter T, Savelsbergh A, Spurio R, Striebeck P, Wintermeyer W, Rodnina MV, Gualerzi CO. Late events of translation initiation in bacteria: a kinetic analysis. EMBO J 2000; 19:2127-36; PMID:10790378; http://dx.doi.org/10.1093/emboj/19.9.2127
  • Dyson MR, Mandal N, RajBhandary UL. Relationship between the structure and function of Escherichia coli initiator tRNA. Biochimie 1993; 75:1051-60; PMID:7515283; http://dx.doi.org/10.1016/0300-9084(93)90004-C
  • Mayer C, Stortchevoi A, Kohrer C, Varshney U, RajBhandary UL. Initiator tRNA and its role in initiation of protein synthesis. Cold Spring Harb Symp Quant Biol 2001; 66:195-206; PMID:12762022; http://dx.doi.org/10.1101/sqb.2001.66.195
  • RajBhandary UL. Initiator transfer RNAs. J Bacteriol 1994; 176:547-52; PMID:7507918
  • Varshney U, RajBhandary UL. Initiation of protein synthesis from a termination codon. Proc Natl Acad Sci U S A 1990; 87:1586-90; PMID:2406724; http://dx.doi.org/10.1073/pnas.87.4.1586
  • Lee CP, Seong BL, RajBhandary UL. Structural and sequence elements important for recognition of Escherichia coli formylmethionine tRNA by methionyl-tRNA transformylase are clustered in the acceptor stem. J Biol Chem 1991; 266:18012-7; PMID:1917939
  • Thanedar S, Kumar NV, Varshney U. The fate of the initiator tRNAs is sensitive to the critical balance between interacting proteins. J Biol Chem 2000; 275:20361-7; PMID:10748005; http://dx.doi.org/10.1074/jbc.M001238200
  • Seong BL, RajBhandary UL. Escherichia coli formylmethionine tRNA: mutations in GGGCCC sequence conserved in anticodon stem of initiator tRNAs affect initiation of protein synthesis and conformation of anticodon loop. Proc Natl Acad Sci U S A 1987; 84:334-8; PMID:3540960; http://dx.doi.org/10.1073/pnas.84.2.334
  • Varshney U, Lee CP, Seong BL, RajBhandary UL. Mutants of initiator tRNA that function both as initiators and elongators. J Biol Chem 1991; 266:18018-24; PMID:1917940
  • Mandal N, Mangroo D, Dalluge JJ, McCloskey JA, Rajbhandary UL. Role of the three consecutive G:C base pairs conserved in the anticodon stem of initiator tRNAs in initiation of protein synthesis in Escherichia coli. RNA 1996; 2:473-82; PMID:8665414
  • Varshney U, Lee CP, RajBhandary UL. From elongator tRNA to initiator tRNA. Proc Natl Acad Sci U S A 1993; 90:2305-9; PMID:8460138; http://dx.doi.org/10.1073/pnas.90.6.2305
  • Seong BL, RajBhandary UL. Mutants of Escherichia coli formylmethionine tRNA: a single base change enables initiator tRNA to act as an elongator in vitro. Proc Natl Acad Sci U S A 1987; 84:8859-63; PMID:3321059; http://dx.doi.org/10.1073/pnas.84.24.8859
  • Sprinzl M, Hartmann T, Weber J, Blank J, Zeidler R. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 1989; 17 Suppl:r1-172; PMID:2470031; http://dx.doi.org/10.1093/nar/17.suppl.r1
  • Samhita L, Shetty S, Varshney U. Unconventional initiator tRNAs sustain Escherichia coli. Proc Natl Acad Sci U S A 2012; 109:13058-63; PMID:22829667; http://dx.doi.org/10.1073/pnas.1207868109
  • Dong J, Munoz A, Kolitz SE, Saini AK, Chiu WL, Rahman H, Lorsch JR, Hinnebusch AG. Conserved residues in yeast initiator tRNA calibrate initiation accuracy by regulating preinitiation complex stability at the start codon. Genes Dev 2014; 28:502-20; PMID:24589778; http://dx.doi.org/10.1101/gad.236547.113
  • Lancaster L, Noller HF. Involvement of 16S rRNA nucleotides G1338 and A1339 in discrimination of initiator tRNA. Mol Cell 2005; 20:623-32; PMID:16307925; http://dx.doi.org/10.1016/j.molcel.2005.10.006
  • Dallas A, Noller HF. Interaction of translation initiation factor 3 with the 30S ribosomal subunit. Mol Cell 2001; 8:855-64; PMID:11684020; http://dx.doi.org/10.1016/S1097-2765(01)00356-2
  • Arora S, Bhamidimarri SP, Bhattacharyya M, Govindan A, Weber MH, Vishveshwara S, Varshney U. Distinctive contributions of the ribosomal P-site elements m2G966, m5C967 and the C-terminal tail of the S9 protein in the fidelity of initiation of translation in Escherichia coli. Nucleic Acids Res 2013; 41:4963-75; PMID:23530111; http://dx.doi.org/10.1093/nar/gkt175
  • Burakovsky DE, Prokhorova IV, Sergiev PV, Milon P, Sergeeva OV, Bogdanov AA, Rodnina MV, Dontsova OA. Impact of methylations of m2G966/m5C967 in 16S rRNA on bacterial fitness and translation initiation. Nucleic Acids Res 2012; 40:7885-95; PMID:22649054; http://dx.doi.org/10.1093/nar/gks508
  • Selmer M, Dunham CM, Murphy FVt, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 2006; 313:1935-42; PMID:16959973; http://dx.doi.org/10.1126/science.1131127
  • Hoang L, Fredrick K, Noller HF. Creating ribosomes with an all-RNA 30S subunit P site. Proc Natl Acad Sci U S A 2004; 101:12439-43; PMID:15308780; http://dx.doi.org/10.1073/pnas.0405227101
  • Kimura S, Suzuki T. Fine-tuning of the ribosomal decoding center by conserved methyl-modifications in the Escherichia coli 16S rRNA. Nucleic Acids Res 2010; 38:1341-52; PMID:19965768; http://dx.doi.org/10.1093/nar/gkp1073
  • Das G, Thotala DK, Kapoor S, Karunanithi S, Thakur SS, Singh NS, Varshney U. Role of 16S ribosomal RNA methylations in translation initiation in Escherichia coli. EMBO J 2008; 27:840-51; PMID:18288206; http://dx.doi.org/10.1038/emboj.2008.20
  • Brimacombe R, Mitchell P, Osswald M, Stade K, Bochkariov D. Clustering of modified nucleotides at the functional center of bacterial ribosomal RNA. FASEB J 1993; 7:161-7; PMID:8422963
  • Seshadri A, Dubey B, Weber MH, Varshney U. Impact of rRNA methylations on ribosome recycling and fidelity of initiation in Escherichia coli. Mol Microbiol 2009; 72:795-808; PMID:19400784; http://dx.doi.org/10.1111/j.1365-2958.2009.06685.x
  • Das G, Dineshkumar TK, Thanedar S, Varshney U. Acquisition of a stable mutation in metY allows efficient initiation from an amber codon in Escherichia coli. Microbiology 2005; 151:1741-50; PMID:15941983; http://dx.doi.org/10.1099/mic.0.27915-0
  • Ishii S, Kuroki K, Imamoto F. tRNAMetf2 gene in the leader region of the nusA operon in Escherichia coli. Proc Natl Acad Sci U S A 1984; 81:409-413; PMID:6364142; http://dx.doi.org/10.1073/pnas.81.2.409
  • Mandal N, RajBhandary UL. Escherichia coli B lacks one of the two initiator tRNA species present in E. coli K-12. J Bacteriol 1992; 174:7827-30; PMID:1447149
  • Kapoor S, Das G, Varshney U. Crucial contribution of the multiple copies of the initiator tRNA genes in the fidelity of tRNA(fMet) selection on the ribosomal P-site in Escherichia coli. Nucleic Acids Res 2011; 39:202-12; PMID:20798174; http://dx.doi.org/10.1093/nar/gkq760
  • Samhita L, Virumae K, Remme J, Varshney U. Initiation with elongator tRNAs. J Bacteriol 2013; 195:4202-9; PMID:23852868; http://dx.doi.org/10.1128/JB.00637-13
  • Krin E, Laurent-Winter C, Bertin PN, Danchin A, Kolb A. Transcription regulation coupling of the divergent argG and metY promoters in Escherichia coli K-12. J Bacteriol 2003; 185:3139-46; PMID:12730174; http://dx.doi.org/10.1128/JB.185.10.3139-3146.2003
  • Kanduc D. Changes of tRNA population during compensatory cell proliferation: differential expression of methionine-tRNA species. Arch Biochem Biophys 1997; 342:1-5; PMID:9185607; http://dx.doi.org/10.1006/abbi.1996.9869
  • Dittmar KA, Sorensen MA, Elf J, Ehrenberg M, Pan T. Selective charging of tRNA isoacceptors induced by amino-acid starvation. EMBO Rep 2005; 6:151-7; PMID:15678157; http://dx.doi.org/10.1038/sj.embor.7400341
  • Conesa C, Ruotolo R, Soularue P, Simms TA, Donze D, Sentenac A, Dieci G. Modulation of yeast genome expression in response to defective RNA polymerase III-dependent transcription. Mol Cell Biol 2005; 25:8631-42; PMID:16166643; http://dx.doi.org/10.1128/MCB.25.19.8631-8642.2005
  • Nagase T, Ishii S, Imamoto F. Differential transcriptional control of the two tRNA(fMet) genes of Escherichia coli K-12. Gene 1988; 67:49-57; PMID:2843439; http://dx.doi.org/10.1016/0378-1119(88)90007-8
  • Guillon JM, Mechulam Y, Schmitter JM, Blanquet S, Fayat G. Disruption of the gene for Met-tRNA(fMet) formyltransferase severely impairs growth of Escherichia coli. J Bacteriol 1992; 174:4294-301; PMID:1624424
  • Ling J, So BR, Yadavalli SS, Roy H, Shoji S, Fredrick K, Musier-Forsyth K, Ibba M. Resampling and editing of mischarged tRNA prior to translation elongation. Mol Cell 2009; 33:654-60; PMID:19285947; http://dx.doi.org/10.1016/j.molcel.2009.01.031
  • Shetty S, Nadimpalli H, Shah RA, Arora S, Das G, Varshney U. An extended Shine-Dalgarno sequence in mRNA functionally bypasses a vital defect in initiator tRNA. Proc Natl Acad Sci U S A 2014; 111:E4224-33; PMID:25246575; http://dx.doi.org/10.1073/pnas.1411637111
  • Mawn MV, Fournier MJ, Tirrell DA, Mason TL. Depletion of free 30S ribosomal subunits in Escherichia coli by expression of RNA containing Shine-Dalgarno-like sequences. J Bacteriol 2002; 184:494-502; PMID:11751827; http://dx.doi.org/10.1128/JB.184.2.494-502.2002
  • Masuda T, Petrov AN, Iizuka R, Funatsu T, Puglisi JD, Uemura S. Initiation factor 2, tRNA, and 50S subunits cooperatively stabilize mRNAs on the ribosome during initiation. Proc Natl Acad Sci U S A 2012; 109:4881-5; PMID:22411833; http://dx.doi.org/10.1073/pnas.1118452109
  • Moll I, Blasi U. Differential inhibition of 30S and 70S translation initiation complexes on leaderless mRNA by kasugamycin. Biochem Biophys Res Commun 2002; 297:1021-6; PMID:12359258; http://dx.doi.org/10.1016/S0006-291X(02)02333-1
  • Kaberdina AC, Szaflarski W, Nierhaus KH, Moll I. An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis? Mol Cell 2009; 33:227-36; PMID:19187763; http://dx.doi.org/10.1016/j.molcel.2008.12.014
  • Poldermans B, Goosen N, Van Knippenberg PH. Studies on the function of two adjacent N6,N6-dimethyladenosines near the 3' end of 16 S ribosomal RNA of Escherichia coli. I. The effect of kasugamycin on initiation of protein synthesis. J Biol Chem 1979; 254:9085-9; PMID:383710
  • Moll I, Hirokawa G, Kiel MC, Kaji A, Blasi U. Translation initiation with 70S ribosomes: an alternative pathway for leaderless mRNAs. Nucleic Acids Res 2004; 32:3354-63; PMID:15215335; http://dx.doi.org/10.1093/nar/gkh663
  • Abdi NM, Fredrick K. Contribution of 16S rRNA nucleotides forming the 30S subunit A and P sites to translation in Escherichia coli. RNA 2005; 11:1624-32; PMID:16177132; http://dx.doi.org/10.1261/rna.2118105
  • Qin D, Abdi NM, Fredrick K. Characterization of 16S rRNA mutations that decrease the fidelity of translation initiation. RNA 2007; 13:2348-55; PMID:17942743; http://dx.doi.org/10.1261/rna.715307
  • Korostelev A, Trakhanov S, Asahara H, Laurberg M, Lancaster L, Noller HF. Interactions and dynamics of the Shine Dalgarno helix in the 70S ribosome. Proc Natl Acad Sci U S A 2007; 104:16840-3; PMID:17940016; http://dx.doi.org/10.1073/pnas.0707850104
  • Hartz D, Binkley J, Hollingsworth T, Gold L. Domains of initiator tRNA and initiation codon crucial for initiator tRNA selection by Escherichia coli IF3. Genes Dev 1990; 4:1790-800; PMID:1701151; http://dx.doi.org/10.1101/gad.4.10.1790
  • Sauert M, Temmel H, Moll I. Heterogeneity of the translational machinery: Variations on a common theme. Biochimie 2014; PMID:25542647
  • Vesper O, Amitai S, Belitsky M, Byrgazov K, Kaberdina AC, Engelberg-Kulka H, Moll I. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 2011; 147:147-57; PMID:21944167; http://dx.doi.org/10.1016/j.cell.2011.07.047
  • Winther KS, Gerdes K. Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA. Proc Natl Acad Sci U S A 2011; 108:7403-7; PMID:21502523; http://dx.doi.org/10.1073/pnas.1019587108
  • Li GW, Oh E, Weissman JS. The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 2012; 484:538-41; PMID:22456704; http://dx.doi.org/10.1038/nature10965
  • Vimberg V, Tats A, Remm M, Tenson T. Translation initiation region sequence preferences in Escherichia coli. BMC Mol Biol 2007; 8:100; PMID:17973990; http://dx.doi.org/10.1186/1471-2199-8-100

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.