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Investigating Bacterial Protein Synthesis Using Systems Biology Approaches

  • Chapter
Prokaryotic Systems Biology

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 883))

Abstract

Protein synthesis is essential for bacterial growth and survival. Its study in Escherichia coli helped uncover features conserved among bacteria as well as universally. The pattern of discovery and the identification of some of the longest-known components of the protein synthesis machinery, including the ribosome itself, tRNAs, and translation factors proceeded through many stages of successively more refined biochemical purifications, finally culminating in the isolation to homogeneity, identification, and mapping of the smallest unit required for performing the given function. These early studies produced a wealth of information. However, many unknowns remained. Systems biology approaches provide an opportunity to investigate protein synthesis from a global perspective, overcoming the limitations of earlier ad hoc methods to gain unprecedented insights. This chapter reviews innovative systems biology approaches, with an emphasis on those designed specifically for investigating the protein synthesis machinery in E. coli.

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References

  • Adams JM, Capecchi MR (1966) N-formylmethionyl-sRNA as the initiator of protein synthesis. Proc Natl Acad Sci U S A 55:147–155

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alam SL, Atkins JF, Gesteland RF (1999) Programmed ribosomal frameshifting: much ado about knotting! Proc Natl Acad Sci U S A 96:14177–14179

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Asato Y (2005) Control of ribosome synthesis during the cell division cycles of E. coli and Synechococcus. Curr Issues Mol Biol 7:109–117

    CAS  PubMed  Google Scholar 

  • Astrachan L, Volkin E (1958) Properties of ribonucleic acid turnover in T2-infected Escherichia coli. Biochim Biophys Acta 29:536–544

    Article  CAS  PubMed  Google Scholar 

  • Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2, 2006.0008

    Google Scholar 

  • Babu M, Butland G, Pogoutse O, Li J, Greenblatt JF, Emili A (2009) Sequential peptide affinity purification system for the systematic isolation and identification of protein complexes from Escherichia coli. Methods Mol Biol 564:373–400

    Article  CAS  PubMed  Google Scholar 

  • Babu M, Aoki H, Chowdhury WQ, Gagarinova A, Graham C, Phanse S, Laliberte B, Sunba N, Jessulat M, Golshani A, Emili A, Greenblatt JF, Ganoza MC (2011a) Ribosome-dependent ATPase interacts with conserved membrane protein in Escherichia coli to modulate protein synthesis and oxidative phosphorylation. PLoS One 6:e18510

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Babu M, Diaz-Mejia JJ, Vlasblom J, Gagarinova A, Phanse S, Graham C, Yousif F, Ding H, Xiong X, Nazarians-Armavil A, Alamgir M, Ali M, Pogoutse O, Pe’er A, Arnold R, Michaut M, Parkinson J, Golshani A, Whitfield C, Wodak SJ, Moreno-Hagelsieb G, Greenblatt JF, Emili A (2011b) Genetic interaction maps in Escherichia coli reveal functional crosstalk among cell envelope biogenesis pathways. PLoS Genet 7:e1002377

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Babu M, Arnold R, Bundalovic-Torma C, Gagarinova A, Wong KS, Kumar A, Stewart G, Samanfar B, Aoki H, Wagih O, Vlasblom J, Phanse S, Lad K, Yeou Hsiung Yu A, Graham C, Jin K, Brown E, Golshani A, Kim P, Moreno-Hagelsieb G, Greenblatt J, Houry WA, Parkinson J, Emili A (2014) Quantitative genome-wide genetic interaction screens reveal global epistatic relationships of protein complexes in Escherichia coli. PLoS Genet 10:e1004120

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Baranov PV, Gesteland RF, Atkins JF (2002) Recoding: translational bifurcations in gene expression. Gene 286:187–201

    Article  CAS  PubMed  Google Scholar 

  • Brenner S, Jacob F, Meselson M (1961) An unstable intermediate carrying information from genes to ribosomes for protein synthesis. Nature 190:576–581

    Article  CAS  PubMed  Google Scholar 

  • Brenner S, Stretton AO, Kaplan S (1965) Genetic code: the ‘nonsense’ triplets for chain termination and their suppression. Nature 206:994–998

    Article  CAS  PubMed  Google Scholar 

  • Bretscher MS, Goodman HM, Menninger JR, Smith JD (1965) Polypeptide chain termination using synthetic polynucleotides. J Mol Biol 14:634–639

    Article  CAS  PubMed  Google Scholar 

  • Bunner AE, Trauger SA, Siuzdak G, Williamson JR (2008) Quantitative ESI-TOF analysis of macromolecular assembly kinetics. Anal Chem 80:9379–9386

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Butland G, Peregrin-Alvarez JM, Li J, Yang W, Yang X, Canadien V, Starostine A, Richards D, Beattie B, Krogan N, Davey M, Parkinson J, Greenblatt J, Emili A (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433:531–537

    Article  CAS  PubMed  Google Scholar 

  • Butland G, Babu M, Diaz-Mejia JJ, Bohdana F, Phanse S, Gold B, Yang W, Li J, Gagarinova AG, Pogoutse O, Mori H, Wanner BL, Lo H, Wasniewski J, Christopolous C, Ali M, Venn P, Safavi-Naini A, Sourour N, Caron S, Choi JY, Laigle L, Nazarians-Armavil A, Deshpande A, Joe S, Datsenko KA, Yamamoto N, Andrews BJ, Boone C, Ding H, Sheikh B, Moreno-Hagelseib G, Greenblatt JF, Emili A (2008) eSGA: E. coli synthetic genetic array analysis. Nat Methods 5:789–795

    Article  CAS  PubMed  Google Scholar 

  • Campbell TL, Brown ED (2008) Genetic interaction screens with ordered overexpression and deletion clone sets implicate the Escherichia coli GTPase YjeQ in late ribosome biogenesis. J Bacteriol 190:2537–2545

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Capecchi MR (1967a) Polypeptide chain termination in vitro: isolation of a release factor. Proc Natl Acad Sci U S A 58:1144–1151

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Capecchi MR (1967b) A rapid assay for polypeptide chain termination. Biochem Biophys Res Commun 28:773–778

    Article  CAS  PubMed  Google Scholar 

  • Carter AP, Clemons WM Jr, Brodersen DE, Morgan-Warren RJ, Hartsch T, Wimberly BT, Ramakrishnan V (2001) Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 291:498–501

    Article  CAS  PubMed  Google Scholar 

  • Chen SS, Williamson JR (2013) Characterization of the ribosome biogenesis landscape in E. coli using quantitative mass spectrometry. J Mol Biol 425:767–779

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen SS, Sperling E, Silverman JM, Davis JH, Williamson JR (2012) Measuring the dynamics of E-coli ribosome biogenesis using pulse-labeling and quantitative mass spectrometry. Mol Biosyst 8:3325–3334

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clark BF, Marcker KA (1966) N-formyl-methionyl-sigma-ribonucleic acid and chain initiation in protein biosynthesis. Polypeptide synthesis directed by a bacteriophage ribonucleic acid in a cell-free system. Nature 211:378–380

    Article  CAS  PubMed  Google Scholar 

  • Comartin DJ, Brown ED (2006) Non-ribosomal factors in ribosome subunit assembly are emerging targets for new antibacterial drugs. Curr Opin Pharmacol 6:453–458

    Article  CAS  PubMed  Google Scholar 

  • Cramer F, Englisch U, Freist W, Sternbach H (1991) Aminoacylation of tRNAs as critical step of protein biosynthesis. Biochimie 73:1027–1035

    Article  CAS  PubMed  Google Scholar 

  • Dammel CS, Noller HF (1995) Suppression of a cold-sensitive mutation in 16S rRNA by overexpression of a novel ribosome-binding factor, RbfA. Genes Dev 9:626–637

    Article  CAS  PubMed  Google Scholar 

  • Doerfel LK, Wohlgemuth I, Kothe C, Peske F, Urlaub H, Rodnina MV (2013) EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339:85–88

    Article  CAS  PubMed  Google Scholar 

  • Elgamal S, Katz A, Hersch SJ, Newsom D, White P, Navarre WW, Ibba M (2014) EF-P dependent pauses integrate proximal and distal signals during translation. PLoS Genet 10:e1004553

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fakunding JL, Hershey JW (1973) The interaction of radioactive initiation factor IF-2 with ribosomes during initiation of protein synthesis. J Biol Chem 248:4206–4212

    CAS  PubMed  Google Scholar 

  • Farabaugh PJ (1996) Programmed translational frameshifting. Annu Rev Genet 30:507–528

    Article  CAS  PubMed  Google Scholar 

  • Fluman N, Navon S, Bibi E, Pilpel Y (2014) mRNA-programmed translation pauses in the targeting of E. coli membrane proteins. eLife 3, e03440

    Google Scholar 

  • Gagarinova A, Emili A (2012) Genome-scale genetic manipulation methods for exploring bacterial molecular biology. Mol Biosyst 8:1626–1638

    Article  CAS  PubMed  Google Scholar 

  • Gale EF, Folkes JP (1955) The assimilation of amino acids by bacteria. 21. The effect of nucleic acids on the development of certain enzymic activities in disrupted staphylococcal cells. Biochem J 59:675–684

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gallant JA, Lindsley D (1998) Ribosomes can slide over and beyond “hungry” codons, resuming protein chain elongation many nucleotides downstream. Proc Natl Acad Sci U S A 95:13771–13776

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ganoza MC, Nakamoto T (1966) Studies on the mechanism of polypeptide chain termination in cell-free extracts of E. coli. Proc Natl Acad Sci U S A 55:162–169

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, Arkin AP, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian KD, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Guldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kotter P, LaBonte D, Lamb DC, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi SL, Revuelta JL, Roberts CJ, Rose M, Ross-Macdonald P, Scherens B, Schimmack G, Shafer B, Shoemaker DD, Sookhai-Mahadeo S, Storms RK, Strathern JN, Valle G, Voet M, Volckaert G, Wang CY, Ward TR, Wilhelmy J, Winzeler EA, Yang Y, Yen G, Youngman E, Yu K, Bussey H, Boeke JD, Snyder M, Philippsen P, Davis RW, Johnston M (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391

    Article  CAS  PubMed  Google Scholar 

  • Gingold H, Pilpel Y (2011) Determinants of translation efficiency and accuracy. Mol Syst Biol 7:481

    Article  PubMed Central  PubMed  Google Scholar 

  • Golovina AY, Dzama MM, Osterman IA, Sergiev PV, Serebryakova MV, Bogdanov AA, Dontsova OA (2012) The last rRNA methyltransferase of E. coli revealed: the yhiR gene encodes adenine-N6 methyltransferase specific for modification of A2030 of 23S ribosomal RNA. RNA 18:1725–1734

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guo Q, Goto S, Chen Y, Feng B, Xu Y, Muto A, Himeno H, Deng H, Lei J, Gao N (2013) Dissecting the in vivo assembly of the 30S ribosomal subunit reveals the role of RimM and general features of the assembly process. Nucleic Acids Res 41:2609–2620

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hamacher K, Trylska J, McCammon JA (2006) Dependency map of proteins in the small ribosomal subunit. PLoS Comput Biol 2:e10

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Han MJ, Park SJ, Park TJ, Lee SY (2004) Roles and applications of small heat shock proteins in the production of recombinant proteins in Escherichia coli. Biotechnol Bioeng 88:426–436

    Article  CAS  PubMed  Google Scholar 

  • Hauser R, Pech M, Kijek J, Yamamoto H, Titz B, Naeve F, Tovchigrechko A, Yamamoto K, Szaflarski W, Takeuchi N, Stellberger T, Diefenbacher ME, Nierhaus KH, Uetz P (2012) RsfA (YbeB) proteins are conserved ribosomal silencing factors. PLoS Genet 8:e1002815

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Helser TL, Davies JE, Dahlberg JE (1971) Change in methylation of 16S ribosomal RNA associated with mutation to kasugamycin resistance in Escherichia coli. Nat New Biol 233:12–14

    Article  CAS  PubMed  Google Scholar 

  • Helser TL, Davies JE, Dahlberg JE (1972) Mechanism of kasugamycin resistance in Escherichia coli. Nat New Biol 235:6–9

    Article  CAS  PubMed  Google Scholar 

  • Herr AJ, Gesteland RF, Atkins JF (2000) One protein from two open reading frames: mechanism of a 50 nt translational bypass. EMBO J 19:2671–2680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hersch SJ, Elgamal S, Katz A, Ibba M, Navarre WW (2014) Translation initiation rate determines the impact of ribosome stalling on bacterial protein synthesis. J Biol Chem 289:28160–28171

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hochkoeppler A (2013) Expanding the landscape of recombinant protein production in Escherichia coli. Biotechnol Lett 35:1971–1981

    Article  CAS  PubMed  Google Scholar 

  • Hu P, Janga SC, Babu M, Diaz-Mejia JJ, Butland G, Yang W, Pogoutse O, Guo X, Phanse S, Wong P, Chandran S, Christopoulos C, Nazarians-Armavil A, Nasseri NK, Musso G, Ali M, Nazemof N, Eroukova V, Golshani A, Paccanaro A, Greenblatt JF, Moreno-Hagelsieb G, Emili A (2009) Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol 7:e96

    Article  PubMed  CAS  Google Scholar 

  • Huang WM, Ao SZ, Casjens S, Orlandi R, Zeikus R, Weiss R, Winge D, Fang M (1988) A persistent untranslated sequence within bacteriophage T4 DNA topoisomerase gene 60. Science 239:1005–1012

    Article  CAS  PubMed  Google Scholar 

  • Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:218–223

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ingolia NT, Brar GA, Rouskin S, McGeachy AM, Weissman JS (2012) The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat Protoc 7:1534–1550

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Janssen BD, Hayes CS (2012) The tmRNA ribosome-rescue system. Adv Protein Chem Struct Biol 86:151–191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jiang M, Sullivan SM, Walker AK, Strahler JR, Andrews PC, Maddock JR (2007) Identification of novel Escherichia coli ribosome-associated proteins using isobaric tags and multidimensional protein identification techniques. J Bacteriol 189:3434–3444

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jomaa A, Stewart G, Martin-Benito J, Zielke R, Campbell TL, Maddock JR, Brown ED, Ortega J (2011) Understanding ribosome assembly: the structure of in vivo assembled immature 30S subunits revealed by cryo-electron microscopy. RNA 17:697–709

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jorgensen F, Kurland CG (1990) Processivity errors of gene expression in Escherichia coli. J Mol Biol 215:511–521

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen F, Adamski FM, Tate WP, Kurland CG (1993) Release factor-dependent false stops are infrequent in Escherichia coli. J Mol Biol 230:41–50

    Article  CAS  PubMed  Google Scholar 

  • Kaczanowska M, Ryden-Aulin M (2005) The YrdC protein—a putative ribosome maturation factor. Biochim Biophys Acta 1727:87–96

    Article  CAS  PubMed  Google Scholar 

  • Kaczanowska M, Ryden-Aulin M (2007) Ribosome biogenesis and the translation process in Escherichia coli. Microbiol Mol Biol Rev 71:477–494

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaltschmidt E, Wittmann HG (1970) Ribosomal proteins. XII. Number of proteins in small and large ribosomal subunits of Escherichia coli as determined by two-dimensional gel electrophoresis. Proc Natl Acad Sci U S A 67:1276–1282

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kannan K, Kanabar P, Schryer D, Florin T, Oh E, Bahroos N, Tenson T, Weissman JS, Mankin AS (2014) The general mode of translation inhibition by macrolide antibiotics. Proc Natl Acad Sci U S A 111:15958–15963

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Keiler K, Lee D (2010) trans-Translation. In: Atkins JF, Gesteland RF (eds) Recoding: expansion of decoding rules enriches gene expression. Springer, New York, pp 383–405

    Chapter  Google Scholar 

  • Keiler KC, Waller PR, Sauer RT (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271:990–993

    Article  CAS  PubMed  Google Scholar 

  • Khorana HG, Buchi H, Ghosh H, Gupta N, Jacob TM, Kossel H, Morgan R, Narang SA, Ohtsuka E, Wells RD (1966) Polynucleotide synthesis and the genetic code. Cold Spring Harb Symp Quant Biol 31:39–49

    Article  CAS  PubMed  Google Scholar 

  • Kim KM, Yi EC, Kim Y (2012) Mapping protein receptor–ligand interactions via in vivo chemical crosslinking, affinity purification, and differential mass spectrometry. Methods 56:161–165

    Article  CAS  PubMed  Google Scholar 

  • Kjeldgaard NO, Gausing K (1974) Regulation of Biosynthesis of Ribosomes. In Ribosomes, P. Lengyel, M. Nomura, and A. Tissières, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory), pp. 369–392

    Google Scholar 

  • Labaj PP, Leparc GG, Linggi BE, Markillie LM, Wiley HS, Kreil DP (2011) Characterization and improvement of RNA-Seq precision in quantitative transcript expression profiling. Bioinformatics 27:i383–i391

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lamborg MR, Zamecnik PC (1960) Amino acid incorporation into protein by extracts of E. coli. Biochim Biophys Acta 42:206–211

    Article  CAS  PubMed  Google Scholar 

  • Last JA, Stanley WM Jr, Salas M, Hille MB, Wahba AJ, Ochoa S (1967) Translation of the genetic message, IV. UAA as a chain termination codon. Proc Natl Acad Sci U S A 57:1062–1067

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee PS, Lee KH (2005) Engineering HlyA hypersecretion in Escherichia coli based on proteomic and microarray analyses. Biotechnol Bioeng 89:195–205

    Article  CAS  PubMed  Google Scholar 

  • Lengyel P, Speyer JF, Ochoa S (1961) Synthetic polynucleotides and the amino acid code. Proc Natl Acad Sci U S A 47:1936–1942

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leong V, Kent M, Jomaa A, Ortega J (2013) Escherichia coli rimM and yjeQ null strains accumulate immature 30S subunits of similar structure and protein complement. RNA 19:789–802

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Levin JZ, Berger MF, Adiconis X, Rogov P, Melnikov A, Fennell T, Nusbaum C, Garraway LA, Gnirke A (2009) Targeted next-generation sequencing of a cancer transcriptome enhances detection of sequence variants and novel fusion transcripts. Genome Biol 10:R115

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li GW, Oh E, Weissman JS (2012) The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484:538–541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liebman SW, Chernoff YO, Liu R (1995) The accuracy center of a eukaryotic ribosome. Biochem Cell Biol 73:1141–1149

    Article  CAS  PubMed  Google Scholar 

  • Lindahl L (1975) Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J Mol Biol 92:15–37

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Jiang H, Gu Z, Roberts JW (2013) High-resolution view of bacteriophage lambda gene expression by ribosome profiling. Proc Natl Acad Sci U S A 110:11928–11933

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mani R, St Onge RP, Hartman JL 4th, Giaever G, Roth FP (2008) Defining genetic interaction. Proc Natl Acad Sci U S A 105:3461–3466

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Menninger JR (1976) Peptidyl transfer RNA dissociates during protein synthesis from ribosomes of Escherichia coli. J Biol Chem 251:3392–3398

    CAS  PubMed  Google Scholar 

  • Mizushima S, Nomura M (1970) Assembly mapping of 30S ribosomal proteins from E. coli. Nature 226:1214

    Article  CAS  PubMed  Google Scholar 

  • Mostafavi S, Ray D, Warde-Farley D, Grouios C, Morris Q (2008) GeneMANIA: a real-time multiple association network integration algorithm for predicting gene function. Genome Biol 9(Suppl 1):S4

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nesvizhskii AI (2012) Computational and informatics strategies for identification of specific protein interaction partners in affinity purification mass spectrometry experiments. Proteomics 12:1639–1655

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nierhaus KH, Dohme F (1974) Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc Natl Acad Sci U S A 71:4713–4717

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Noll M, Noll H (1972) Mechanism and control of initiation in the translation of R17 RNA. Nat New Biol 238:225–228

    Article  CAS  PubMed  Google Scholar 

  • O’Farrell PH (1978) The suppression of defective translation by ppGpp and its role in the stringent response. Cell 14:545–557

    Article  PubMed  Google Scholar 

  • Ogle JM, Murphy FV, Tarry MJ, Ramakrishnan V (2002) Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111:721–732

    Article  CAS  PubMed  Google Scholar 

  • Oh E, Becker AH, Sandikci A, Huber D, Chaba R, Gloge F, Nichols RJ, Typas A, Gross CA, Kramer G, Weissman JS, Bukau B (2011) Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 147:1295–1308

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roy-Chaudhuri B, Kirthi N, Kelley T, Culver GM (2008) Suppression of a cold-sensitive mutation in ribosomal protein S5 reveals a role for RimJ in ribosome biogenesis. Mol Microbiol 68:1547–1559

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sabol S, Ochoa S (1971) Ribosomal binding of labelled initiation factor F3. Nat New Biol 234:233–236

    Article  CAS  PubMed  Google Scholar 

  • Sabol S, Sillero MA, Iwasaki K, Ochoa S (1970) Purification and properties of initiation factor F3. Nature 228:1269–1273

    Article  CAS  PubMed  Google Scholar 

  • Scolnick E, Tompkins R, Caskey T, Nirenberg M (1968) Release factors differing in specificity for terminator codons. Proc Natl Acad Sci U S A 61:768–774

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sergiev PV, Golovina AY, Sergeeva OV, Osterman IA, Nesterchuk MV, Bogdanov AA, Dontsova OA (2012) How much can we learn about the function of bacterial rRNA modification by mining large-scale experimental datasets? Nucleic Acids Res 40:5694–5705

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shajani Z, Sykes MT, Williamson JR (2011) Assembly of bacterial ribosomes. Annu Rev Biochem 80:501–526

    Article  CAS  PubMed  Google Scholar 

  • Shine J, Dalgarno L (1975) Determinant of cistron specificity in bacterial ribosomes. Nature 254:34–38

    Article  CAS  PubMed  Google Scholar 

  • Spahn CM, Prescott CD (1996) Throwing a spanner in the works: antibiotics and the translation apparatus. J Mol Med (Berl) 74:423–439

    Article  CAS  Google Scholar 

  • Sparling PF (1970) Kasugamycin resistance: 30S ribosomal mutation with an unusual location on the Escherichia coli chromosome. Science 167:56–58

    Article  CAS  PubMed  Google Scholar 

  • Srivastava AK, Schlessinger D (1990) Mechanism and regulation of bacterial ribosomal RNA processing. Annu Rev Microbiol 44:105–129

    Article  CAS  PubMed  Google Scholar 

  • Stahl G, McCarty GP, Farabaugh PJ (2002) Ribosome structure: revisiting the connection between translational accuracy and unconventional decoding. Trends Biochem Sci 27:178–183

    Article  CAS  PubMed  Google Scholar 

  • Sykes MT, Shajani Z, Sperling E, Beck AH, Williamson JR (2010) Quantitative proteomic analysis of ribosome assembly and turnover in vivo. J Mol Biol 403:331–345

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, Hearn J, Emili A, Xie XS (2010) Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329:533–538

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tissieres A, Watson JD (1958) Ribonucleoprotein particles from Escherichia coli. Nature 182:778–780

    Article  CAS  PubMed  Google Scholar 

  • Ude S, Lassak J, Starosta AL, Kraxenberger T, Wilson DN, Jung K (2013) Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science 339:82–85

    Article  CAS  PubMed  Google Scholar 

  • Vlasblom J, Zuberi K, Rodriguez H, Arnold R, Gagarinova A, Deineko V, Kumar A, Leung E, Rizzolo K, Samanfar B, Chang L, Phanse S, Golshani A, Greenblatt JF, Houry WA, Emili A, Morris Q, Bader G, Babu M (2015) Novel function discovery with GeneMANIA: a new integrated resource for gene function prediction in Escherichia coli. Bioinformatics 31:306–310

    Google Scholar 

  • Waegeman H, Soetaert W (2011) Increasing recombinant protein production in Escherichia coli through metabolic and genetic engineering. J Ind Microbiol Biotechnol 38:1891–1910

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K (2010) Unique features of animal mitochondrial translation systems. The non-universal genetic code, unusual features of the translational apparatus and their relevance to human mitochondrial diseases. Proc Jpn Acad Ser B 86:11–39

    Article  CAS  Google Scholar 

  • Weigert MG, Garen A (1965) Base composition of nonsense codons in E. coli. Evidence from amino-acid substitutions at a tryptophan site in alkaline phosphatase. Nature 206:992–994

    Article  CAS  PubMed  Google Scholar 

  • Weiss RB, Huang WM, Dunn DM (1990) A nascent peptide is required for ribosomal bypass of the coding gap in bacteriophage T4 gene 60. Cell 62:117–126

    Article  CAS  PubMed  Google Scholar 

  • Wilson DN (2009) The A–Z of bacterial translation inhibitors. Crit Rev Biochem Mol Biol 44:393–433

    Article  CAS  PubMed  Google Scholar 

  • Woolstenhulme CJ, Guydosh NR, Green R, Buskirk AR (2015) High-precision analysis of translational pausing by ribosome profiling in bacteria lacking EFP. Cell Rep 11:13–21

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Culver GM (2010) Differential assembly of 16S rRNA domains during 30S subunit formation. RNA 16:1990–2001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zeghouf M, Li J, Butland G, Borkowska A, Canadien V, Richards D, Beattie B, Emili A, Greenblatt JF (2004) Sequential Peptide Affinity (SPA) system for the identification of mammalian and bacterial protein complexes. J Proteome Res 3:463–468

    Article  CAS  PubMed  Google Scholar 

  • Zou SB, Hersch SJ, Roy H, Wiggers JB, Leung AS, Buranyi S, Xie JL, Dare K, Ibba M, Navarre WW (2012) Loss of elongation factor P disrupts bacterial outer membrane integrity. J Bacteriol 194:413–425

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada, M5S 1A8

    Alla Gagarinova & Andrew Emili

  2. Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, ON, Canada, M5S 3E1

    Alla Gagarinova & Andrew Emili

Authors
  1. Alla Gagarinova
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  2. Andrew Emili
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Correspondence to Alla Gagarinova .

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Editors and Affiliations

  1. Cellular and Molecular Pharmacology, Univ of California, San Francisco, SAN FRANCISCO, California, USA

    Nevan J. Krogan, PhD

  2. Department of Biochemistry, University of Regina, Regina, Saskatchewan, Canada

    Mohan Babu, PhD

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Gagarinova, A., Emili, A. (2015). Investigating Bacterial Protein Synthesis Using Systems Biology Approaches. In: Krogan, PhD, N., Babu, PhD, M. (eds) Prokaryotic Systems Biology. Advances in Experimental Medicine and Biology, vol 883. Springer, Cham. https://doi.org/10.1007/978-3-319-23603-2_2

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