Knowing Right From Wrong: Quality Control of Ribosome Biogenesis in Eubacteria
Keywords:
Quality Control; Biogenesis; Bacteria
Abstract
Ribosomes are amongst the largest molecular machines in any living cell, consist three ribosomal RNA (rRNA) over 50 ribosomal proteins (r-proteins). In bacteria they have a small subunit (30S) and a large subunit (50S) which together form a functional 70S ribosome, which translates the information in a messenger RNA (mRNA) into a polypeptide sequence. Translation occurs in multiple steps such as initiation, elongation, termination and recycling. The fidelity of these steps depends on the faithful assembly of the ribosome itself. The synthesis of ribosomes involves various processes such as folding and processing of rRNA, ordered loading of ribosomal proteins and modification of various critical residues in them. For accuracy of protein synthesis, a cell must ensure that the immature particles, are kept away from participating in active translation. And, once the ribosomes have been assembled, the cell must have a quality check to ensure the accuracy of the assembled particles. Defect in any of these processes will result in occurrence of the defective ribosomes in the translating pool, which in turn may lead to production of mis-translated proteins. In humans, genetic disorders of ribosomopathies occur because of deficiencies in ribosome biogenesis and quality control. Thus, it is crucial to understand the hitherto obscure mechanisms of quality control of ribosome biogenesis. This review is an attempt to provide an overview of the status of quality control mechanisms of ribosome biogenesis in prokaryotes.
References
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Asai T, Zaporojets D, Squires C and Squires C L (1999) An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria Proc Natl Acad Sci U S A 96 1971-1976
Bjorkman J, Samuelsson P, Andersson D I and Hughes D (1999) Novel ribosomal mutations affecting translational accuracy, antibiotic resistance and virulence of Salmonella typhimurium Mol Microbiol 31 53-58
Borg S, Bjorkman J, Eriksson S, Syk A, Andersson D I, et al. (1999) Novel Salmonella typhimurium properties in host--parasite interactions Immunol Lett 68 247-249
Burakovsky D E, Prokhorova I V, Sergiev P V, Milon P, Sergeeva O V, et al. (2012) Impact of methylations of m2G966/m5C967 in 16S rRNA on bacterial fitness and translation initiation Nucleic Acids Res 40 7885-7895
Champney W S (2006) The other target for ribosomal antibiotics: inhibition of bacterial ribosomal subunit formation Infect Disord Drug Targets 6 377-390
Clatterbuck Soper S F, Dator R P, Limbach P A and Woodson S A (2013) In vivo X-ray footprinting of pre-30S ribosomes reveals chaperone-dependent remodeling of late assembly intermediates Mol Cell 52 506-516
Condon C, Philips J, Fu Z Y, Squires C and Squires C L (1992) Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli EMBO J 11 4175-4185
Culver G M (2003) Assembly of the 30S ribosomal subunit Biopolymers 68 234-249
Culver G M and Noller H F (1999) Efficient reconstitution of functional Escherichia coli 30S ribosomal subunits from a complete set of recombinant small subunit ribosomal proteins RNA 5 832-843
Decatur W A and Fournier M J (2002) rRNA modifications and ribosome function Trends Biochem Sci 27 344-351
Dunn J J and Studier F W (1973) T7 early RNAs are generated by site-specific cleavages Proc Natl Acad Sci U S A 70 1559-1563
Ellis S R (2014) Nucleolar stress in Diamond Blackfan anemia pathophysiology Biochim Biophys Acta 1842 765-768
Geigenmuller U and Nierhaus K H (1986) Tetracycline can inhibit tRNA binding to the ribosomal P site as well as to the A site Eur J Biochem 161 723-726
Gibbs M R, Moon K M, Chen M, Balakrishnan R, Foster L J and 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
Gourse R L, Takebe Y, Sharrock R A and Nomura M (1985) Feedback regulation of rRNA and tRNA synthesis and accumulation of free ribosomes after conditional expression of rRNA genes Proc Natl Acad Sci U S A 82 1069-1073
Gyorfy Z, Draskovits G, Vernyik V, Blattner F F, Gaal T and Posfai G (2015) Engineered ribosomal RNA operon copy-number variants of E. coli reveal the evolutionary trade-offs shaping rRNA operon number Nucleic Acids Res 43 1783-1794
Heilbronn L K and Ravussin E (2003) Calorie restriction and aging: review of the literature and implications for studies in humans Am J Clin Nutr 78 361-369
Held W A and Nomura M (1973) Rate determining step in the reconstitution of Escherichia coli 30S ribosomal subunits Biochemistry 12 3273-3281
Hillebrand A, Wurm R, Menzel A and Wagner R (2005) The seven E. coli ribosomal RNA operon upstream regulatory regions differ in structure and transcription factor binding efficiencies Biol Chem 386 523-534
Hinnebusch A G and Lorsch J R (2012) The mechanism of eukaryotic translation initiation: new insights and challenges Cold Spring Harb Perspect Biol 4 a011544
Hoang L, Fredrick K and Noller H F (2004) Creating ribosomes with an all-RNA 30S subunit P site Proc Natl Acad Sci U S A 101 12439-12443
Hwang J and Inouye M (2006) The tandem GTPase, Der, is essential for the biogenesis of 50S ribosomal subunits in Escherichia coli Mol Microbiol 61 1660-1672
Ikemura T and Nomura M (1977) Expression of spacer tRNA genes in ribosomal RNA transcription units carried by hybrid Col E1 plasmids in E. coli Cell 11 779-793
Ilina E N, Malakhova M V, Bodoev I N, Oparina N Y, Filimonova A V and Govorun V M (2013) Mutation in ribosomal protein S5 leads to spectinomycin resistance in Neisseria gonorrhoeae Front Microbiol 4 186
Jacob A I, Kohrer C, Davies B W, RajBhandary U L and Walker G C (2013) Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation Mol Cell 49 427-438
Jiang M, Datta K, Walker A, Strahler J, Bagamasbad P, Andrews P C and Maddock J R (2006) The Escherichia coli GTPase CgtAE is involved in late steps of large ribosome assembly J Bacteriol 188 6757-6770
Jinks-Robertson S, Gourse R L and Nomura M (1983) Expression of rRNA and tRNA genes in Escherichia coli: evidence for feedback regulation by products of rRNA operons Cell 33 865-876
Kaczanowska M and Ryden-Aulin M (2007) Ribosome biogenesis and the translation process in Escherichia coli Microbiol Mol Biol Rev 71 477-494
Kapoor S, Das G and Varshney U (2011) 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 39 202-212
Klappenbach J A, Dunbar J M and Schmidt T M (2000) rRNA operon copy number reflects ecological strategies of bacteria Appl Environ Microbiol 66 1328-1333
Korostelev A, Trakhanov S, Asahara H, Laurberg M, Lancaster L and Noller H F (2007) Interactions and dynamics of the Shine Dalgarno helix in the 70S ribosome Proc Natl Acad Sci U S A 104 16840-16843
Lancaster L and Noller H F (2005) Involvement of 16S rRNA nucleotides G1338 and A1339 in discrimination of initiator tRNA Mol Cell 20 623-632
Lin S J, Ford E, Haigis M, Liszt G and Guarente L (2004) Calorie restriction extends yeast life span by lowering the level of NADH Genes Dev 18 12-16
Maeda M, Shimada T and Ishihama A (2015) Strength and Regulation of Seven rRNA Promoters in Escherichia coli PLoS One 10 e0144697
Mangroo D and RajBhandary U L (1995) Mutants of Escherichia coli initiator tRNA defective in initiation. Effects of overproduction of methionyl-tRNA transformylase and the initiation factors IF2 and IF3 J Biol Chem 270 12203-12209
Mattison J A, Colman R J, Beasley T M, Allison D B, Kemnitz J W, et al. (2017) Caloric restriction improves health and survival of rhesus monkeys Nat Commun 8 14063
Morgan E A, Ikemura T, Lindahl L, Fallon A M and Nomura M (1978) Some rRNA operons in E. coli have tRNA genes at their distal ends Cell 13 335-344
Mulder A M, Yoshioka C, Beck A H, Bunner A E, Milligan R A, et al. (2010) Visualizing ribosome biogenesis: parallel assembly pathways for the 30S subunit Science 330 673-677
Nesterchuk M V, Sergiev P V and Dontsova O A (2011) Posttranslational Modifications of Ribosomal Proteins in Escherichia coli Acta Naturae 3 22-33
Nikolaev N, Silengo L and Schlessinger D (1973) A role for ribonuclease 3 in processing of ribosomal ribonucleic acid and messenger ribonucleic acid precursors in Escherichia coli J Biol Chem 248 7967-7969
Nilsson A I, Zorzet A, Kanth A, Dahlstrom S, Berg O G and Andersson D I (2006) Reducing the fitness cost of antibiotic resistance by amplification of initiator tRNA genes Proc Natl Acad Sci U S A 103 6976-6981
Nomura M and Erdmann V A (1970) Reconstitution of 50S ribosomal subunits from dissociated molecular components Nature 228 744-748
Phunpruch S, Warit S, Suksamran R, Billamas P, Jaitrong S, Palittapongarnpim P and Prammananan T (2013) A role for 16S rRNA dimethyltransferase (ksgA) in intrinsic clarithromycin resistance in Mycobacterium tuberculosis Int J Antimicrob Agents 41 548-551
RajBhandary U L (1994) Initiator transfer RNAs J Bacteriol 176 547-552
Ramakrishnan V (2002) Ribosome structure and the mechanism of translation Cell 108 557-572
Roy-Chaudhuri B, Kirthi N and Culver G M (2010) Appropriate maturation and folding of 16S rRNA during 30S subunit biogenesis are critical for translational fidelity Proc Natl Acad Sci U S A 107 4567-4572
Samhita L, Nanjundiah V and Varshney U (2014) How many initiator tRNA genes does Escherichia coli need? J Bacteriol 196 2607-2615
Samhita L, Shetty S and Varshney U (2012) Unconventional initiator tRNAs sustain Escherichia coli Proc Natl Acad Sci U S A 109 13058-13063
Samhita L, Virumae K, Remme J and Varshney U (2013) Initiation with elongator tRNAs J Bacteriol 195 4202-4209
Schmeing T M and Ramakrishnan V (2009) What recent ribosome structures have revealed about the mechanism of translation Nature 461 1234-1242
Selmer M, Dunham C M, Murphy F V t, Weixlbaumer A, Petry S, et al. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA Science 313 1935-1942
Sergeeva O V, Sergiev P V, Bogdanov A A and Dontsova O A (2014) [Ribosome: lessons of a molecular factory construction] Mol Biol (Mosk) 48 543-560
Seshadri A, Dubey B, Weber M H and Varshney U (2009) Impact of rRNA methylations on ribosome recycling and fidelity of initiation in Escherichia coli Mol Microbiol 72 795-808
Shajani Z, Sykes M T and Williamson J R (2011) Assembly of bacterial ribosomes Annu Rev Biochem 80 501-526
Shetty S, Bhattacharyya S and Varshney U (2015) Is the cellular initiation of translation an exclusive property of the initiator tRNAs? RNA Biol 12 675-680
Shetty S, Nadimpalli H, Shah R A, Arora S, Das G and Varshney U (2014) An extended Shine-Dalgarno sequence in mRNA functionally bypasses a vital defect in initiator tRNA Proc Natl Acad Sci U S A 111 E4224-4233
Shetty S, Shah R A, Chembazhi U V, Sah S and Varshney U (2017) Two highly conserved features of bacterial initiator tRNAs license them to pass through distinct checkpoints in translation initiation Nucleic Acids Res 45 2040-2050
Shetty S and Varshney U (2016) An evolutionarily conserved element in initiator tRNAs prompts ultimate steps in ribosome maturation Proc Natl Acad Sci U S A 113 E6126-E6134
Shi Z and Barna M (2015) Translating the Genome in Time and Space: Specialized Ribosomes, RNA Regulons, and RNA-Binding Proteins Annu Rev Cell Dev Biol 31 31-54
Shine J and Dalgarno L (1975) Determinant of cistron specificity in bacterial ribosomes Nature 254 34-38
Siibak T, Peil L, Donhofer A, Tats A, Remm M, et al. (2011) Antibiotic-induced ribosomal assembly defects result from changes in the synthesis of ribosomal proteins Mol Microbiol 80 54-67
Siibak T, Peil L, Xiong L, Mankin A, Remme J and Tenson T (2009) Erythromycin- and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition Antimicrob Agents Chemother 53 563-571
Singh N S, Ahmad R, Sangeetha R and Varshney U (2008) Recycling of ribosomal complexes stalled at the step of elongation in Escherichia coli J Mol Biol 380 451-464
Steitz J A (1973) Specific recognition of non-initiator regions in RNA bacteriophage messengers by ribosomes of Bacillus stearothermophilus J Mol Biol 73 1-16
Steitz J A and Jakes K (1975) How ribosomes select initiator regions in mRNA: base pair formation between the 3' terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli Proc Natl Acad Sci U S A 72 4734-4738
Stokes J M, Davis J H, Mangat C S, Williamson J R and Brown E D (2014) Discovery of a small molecule that inhibits bacterial ribosome biogenesis Elife 3 e03574
Strunk B S, Novak M N, Young C L and Karbstein K (2012) A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits Cell 150 111-121
Sulthana S and Deutscher M P (2013) Multiple exoribonucleases catalyze maturation of the 3' terminus of 16S ribosomal RNA (rRNA) J Biol Chem 288 12574-12579
Tissieres A and Watson J D (1958) Ribonucleoprotein particles from Escherichia coli Nature 182 778-780
Trainor P A and Merrill A E (2014) Ribosome biogenesis in skeletal development and the pathogenesis of skeletal disorders Biochim Biophys Acta 1842 769-778
Traub P and Nomura M (1969) Structure and function of Escherichia coli ribosomes. VI. Mechanism of assembly of 30 s ribosomes studied in vitro J Mol Biol 40 391-413
Traub P and Nomura M (1969) Studies on the assembly of ribosomes in vitro Cold Spring Harb Symp Quant Biol 34 63-67
Varshney U, Lee C P and RajBhandary U L (1993) From elongator tRNA to initiator tRNA Proc Natl Acad Sci U S A 90 2305-2309
Varshney U and RajBhandary U L (1992) Role of methionine and formylation of initiator tRNA in initiation of protein synthesis in Escherichia coli J Bacteriol 174 7819-7826
Williamson J R (2003) After the ribosome structures: how are the subunits assembled? RNA 9 165-167
Xue S and Barna M (2012) Specialized ribosomes: a new frontier in gene regulation and organismal biology Nat Rev Mol Cell Biol 13 355-369
Yap W H, Zhang Z and Wang Y (1999) Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon J Bacteriol 181 5201-5209
Asai T, Zaporojets D, Squires C and Squires C L (1999) An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria Proc Natl Acad Sci U S A 96 1971-1976
Bjorkman J, Samuelsson P, Andersson D I and Hughes D (1999) Novel ribosomal mutations affecting translational accuracy, antibiotic resistance and virulence of Salmonella typhimurium Mol Microbiol 31 53-58
Borg S, Bjorkman J, Eriksson S, Syk A, Andersson D I, et al. (1999) Novel Salmonella typhimurium properties in host--parasite interactions Immunol Lett 68 247-249
Burakovsky D E, Prokhorova I V, Sergiev P V, Milon P, Sergeeva O V, et al. (2012) Impact of methylations of m2G966/m5C967 in 16S rRNA on bacterial fitness and translation initiation Nucleic Acids Res 40 7885-7895
Champney W S (2006) The other target for ribosomal antibiotics: inhibition of bacterial ribosomal subunit formation Infect Disord Drug Targets 6 377-390
Clatterbuck Soper S F, Dator R P, Limbach P A and Woodson S A (2013) In vivo X-ray footprinting of pre-30S ribosomes reveals chaperone-dependent remodeling of late assembly intermediates Mol Cell 52 506-516
Condon C, Philips J, Fu Z Y, Squires C and Squires C L (1992) Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli EMBO J 11 4175-4185
Culver G M (2003) Assembly of the 30S ribosomal subunit Biopolymers 68 234-249
Culver G M and Noller H F (1999) Efficient reconstitution of functional Escherichia coli 30S ribosomal subunits from a complete set of recombinant small subunit ribosomal proteins RNA 5 832-843
Decatur W A and Fournier M J (2002) rRNA modifications and ribosome function Trends Biochem Sci 27 344-351
Dunn J J and Studier F W (1973) T7 early RNAs are generated by site-specific cleavages Proc Natl Acad Sci U S A 70 1559-1563
Ellis S R (2014) Nucleolar stress in Diamond Blackfan anemia pathophysiology Biochim Biophys Acta 1842 765-768
Geigenmuller U and Nierhaus K H (1986) Tetracycline can inhibit tRNA binding to the ribosomal P site as well as to the A site Eur J Biochem 161 723-726
Gibbs M R, Moon K M, Chen M, Balakrishnan R, Foster L J and 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
Gourse R L, Takebe Y, Sharrock R A and Nomura M (1985) Feedback regulation of rRNA and tRNA synthesis and accumulation of free ribosomes after conditional expression of rRNA genes Proc Natl Acad Sci U S A 82 1069-1073
Gyorfy Z, Draskovits G, Vernyik V, Blattner F F, Gaal T and Posfai G (2015) Engineered ribosomal RNA operon copy-number variants of E. coli reveal the evolutionary trade-offs shaping rRNA operon number Nucleic Acids Res 43 1783-1794
Heilbronn L K and Ravussin E (2003) Calorie restriction and aging: review of the literature and implications for studies in humans Am J Clin Nutr 78 361-369
Held W A and Nomura M (1973) Rate determining step in the reconstitution of Escherichia coli 30S ribosomal subunits Biochemistry 12 3273-3281
Hillebrand A, Wurm R, Menzel A and Wagner R (2005) The seven E. coli ribosomal RNA operon upstream regulatory regions differ in structure and transcription factor binding efficiencies Biol Chem 386 523-534
Hinnebusch A G and Lorsch J R (2012) The mechanism of eukaryotic translation initiation: new insights and challenges Cold Spring Harb Perspect Biol 4 a011544
Hoang L, Fredrick K and Noller H F (2004) Creating ribosomes with an all-RNA 30S subunit P site Proc Natl Acad Sci U S A 101 12439-12443
Hwang J and Inouye M (2006) The tandem GTPase, Der, is essential for the biogenesis of 50S ribosomal subunits in Escherichia coli Mol Microbiol 61 1660-1672
Ikemura T and Nomura M (1977) Expression of spacer tRNA genes in ribosomal RNA transcription units carried by hybrid Col E1 plasmids in E. coli Cell 11 779-793
Ilina E N, Malakhova M V, Bodoev I N, Oparina N Y, Filimonova A V and Govorun V M (2013) Mutation in ribosomal protein S5 leads to spectinomycin resistance in Neisseria gonorrhoeae Front Microbiol 4 186
Jacob A I, Kohrer C, Davies B W, RajBhandary U L and Walker G C (2013) Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation Mol Cell 49 427-438
Jiang M, Datta K, Walker A, Strahler J, Bagamasbad P, Andrews P C and Maddock J R (2006) The Escherichia coli GTPase CgtAE is involved in late steps of large ribosome assembly J Bacteriol 188 6757-6770
Jinks-Robertson S, Gourse R L and Nomura M (1983) Expression of rRNA and tRNA genes in Escherichia coli: evidence for feedback regulation by products of rRNA operons Cell 33 865-876
Kaczanowska M and Ryden-Aulin M (2007) Ribosome biogenesis and the translation process in Escherichia coli Microbiol Mol Biol Rev 71 477-494
Kapoor S, Das G and Varshney U (2011) 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 39 202-212
Klappenbach J A, Dunbar J M and Schmidt T M (2000) rRNA operon copy number reflects ecological strategies of bacteria Appl Environ Microbiol 66 1328-1333
Korostelev A, Trakhanov S, Asahara H, Laurberg M, Lancaster L and Noller H F (2007) Interactions and dynamics of the Shine Dalgarno helix in the 70S ribosome Proc Natl Acad Sci U S A 104 16840-16843
Lancaster L and Noller H F (2005) Involvement of 16S rRNA nucleotides G1338 and A1339 in discrimination of initiator tRNA Mol Cell 20 623-632
Lin S J, Ford E, Haigis M, Liszt G and Guarente L (2004) Calorie restriction extends yeast life span by lowering the level of NADH Genes Dev 18 12-16
Maeda M, Shimada T and Ishihama A (2015) Strength and Regulation of Seven rRNA Promoters in Escherichia coli PLoS One 10 e0144697
Mangroo D and RajBhandary U L (1995) Mutants of Escherichia coli initiator tRNA defective in initiation. Effects of overproduction of methionyl-tRNA transformylase and the initiation factors IF2 and IF3 J Biol Chem 270 12203-12209
Mattison J A, Colman R J, Beasley T M, Allison D B, Kemnitz J W, et al. (2017) Caloric restriction improves health and survival of rhesus monkeys Nat Commun 8 14063
Morgan E A, Ikemura T, Lindahl L, Fallon A M and Nomura M (1978) Some rRNA operons in E. coli have tRNA genes at their distal ends Cell 13 335-344
Mulder A M, Yoshioka C, Beck A H, Bunner A E, Milligan R A, et al. (2010) Visualizing ribosome biogenesis: parallel assembly pathways for the 30S subunit Science 330 673-677
Nesterchuk M V, Sergiev P V and Dontsova O A (2011) Posttranslational Modifications of Ribosomal Proteins in Escherichia coli Acta Naturae 3 22-33
Nikolaev N, Silengo L and Schlessinger D (1973) A role for ribonuclease 3 in processing of ribosomal ribonucleic acid and messenger ribonucleic acid precursors in Escherichia coli J Biol Chem 248 7967-7969
Nilsson A I, Zorzet A, Kanth A, Dahlstrom S, Berg O G and Andersson D I (2006) Reducing the fitness cost of antibiotic resistance by amplification of initiator tRNA genes Proc Natl Acad Sci U S A 103 6976-6981
Nomura M and Erdmann V A (1970) Reconstitution of 50S ribosomal subunits from dissociated molecular components Nature 228 744-748
Phunpruch S, Warit S, Suksamran R, Billamas P, Jaitrong S, Palittapongarnpim P and Prammananan T (2013) A role for 16S rRNA dimethyltransferase (ksgA) in intrinsic clarithromycin resistance in Mycobacterium tuberculosis Int J Antimicrob Agents 41 548-551
RajBhandary U L (1994) Initiator transfer RNAs J Bacteriol 176 547-552
Ramakrishnan V (2002) Ribosome structure and the mechanism of translation Cell 108 557-572
Roy-Chaudhuri B, Kirthi N and Culver G M (2010) Appropriate maturation and folding of 16S rRNA during 30S subunit biogenesis are critical for translational fidelity Proc Natl Acad Sci U S A 107 4567-4572
Samhita L, Nanjundiah V and Varshney U (2014) How many initiator tRNA genes does Escherichia coli need? J Bacteriol 196 2607-2615
Samhita L, Shetty S and Varshney U (2012) Unconventional initiator tRNAs sustain Escherichia coli Proc Natl Acad Sci U S A 109 13058-13063
Samhita L, Virumae K, Remme J and Varshney U (2013) Initiation with elongator tRNAs J Bacteriol 195 4202-4209
Schmeing T M and Ramakrishnan V (2009) What recent ribosome structures have revealed about the mechanism of translation Nature 461 1234-1242
Selmer M, Dunham C M, Murphy F V t, Weixlbaumer A, Petry S, et al. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA Science 313 1935-1942
Sergeeva O V, Sergiev P V, Bogdanov A A and Dontsova O A (2014) [Ribosome: lessons of a molecular factory construction] Mol Biol (Mosk) 48 543-560
Seshadri A, Dubey B, Weber M H and Varshney U (2009) Impact of rRNA methylations on ribosome recycling and fidelity of initiation in Escherichia coli Mol Microbiol 72 795-808
Shajani Z, Sykes M T and Williamson J R (2011) Assembly of bacterial ribosomes Annu Rev Biochem 80 501-526
Shetty S, Bhattacharyya S and Varshney U (2015) Is the cellular initiation of translation an exclusive property of the initiator tRNAs? RNA Biol 12 675-680
Shetty S, Nadimpalli H, Shah R A, Arora S, Das G and Varshney U (2014) An extended Shine-Dalgarno sequence in mRNA functionally bypasses a vital defect in initiator tRNA Proc Natl Acad Sci U S A 111 E4224-4233
Shetty S, Shah R A, Chembazhi U V, Sah S and Varshney U (2017) Two highly conserved features of bacterial initiator tRNAs license them to pass through distinct checkpoints in translation initiation Nucleic Acids Res 45 2040-2050
Shetty S and Varshney U (2016) An evolutionarily conserved element in initiator tRNAs prompts ultimate steps in ribosome maturation Proc Natl Acad Sci U S A 113 E6126-E6134
Shi Z and Barna M (2015) Translating the Genome in Time and Space: Specialized Ribosomes, RNA Regulons, and RNA-Binding Proteins Annu Rev Cell Dev Biol 31 31-54
Shine J and Dalgarno L (1975) Determinant of cistron specificity in bacterial ribosomes Nature 254 34-38
Siibak T, Peil L, Donhofer A, Tats A, Remm M, et al. (2011) Antibiotic-induced ribosomal assembly defects result from changes in the synthesis of ribosomal proteins Mol Microbiol 80 54-67
Siibak T, Peil L, Xiong L, Mankin A, Remme J and Tenson T (2009) Erythromycin- and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition Antimicrob Agents Chemother 53 563-571
Singh N S, Ahmad R, Sangeetha R and Varshney U (2008) Recycling of ribosomal complexes stalled at the step of elongation in Escherichia coli J Mol Biol 380 451-464
Steitz J A (1973) Specific recognition of non-initiator regions in RNA bacteriophage messengers by ribosomes of Bacillus stearothermophilus J Mol Biol 73 1-16
Steitz J A and Jakes K (1975) How ribosomes select initiator regions in mRNA: base pair formation between the 3' terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli Proc Natl Acad Sci U S A 72 4734-4738
Stokes J M, Davis J H, Mangat C S, Williamson J R and Brown E D (2014) Discovery of a small molecule that inhibits bacterial ribosome biogenesis Elife 3 e03574
Strunk B S, Novak M N, Young C L and Karbstein K (2012) A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits Cell 150 111-121
Sulthana S and Deutscher M P (2013) Multiple exoribonucleases catalyze maturation of the 3' terminus of 16S ribosomal RNA (rRNA) J Biol Chem 288 12574-12579
Tissieres A and Watson J D (1958) Ribonucleoprotein particles from Escherichia coli Nature 182 778-780
Trainor P A and Merrill A E (2014) Ribosome biogenesis in skeletal development and the pathogenesis of skeletal disorders Biochim Biophys Acta 1842 769-778
Traub P and Nomura M (1969) Structure and function of Escherichia coli ribosomes. VI. Mechanism of assembly of 30 s ribosomes studied in vitro J Mol Biol 40 391-413
Traub P and Nomura M (1969) Studies on the assembly of ribosomes in vitro Cold Spring Harb Symp Quant Biol 34 63-67
Varshney U, Lee C P and RajBhandary U L (1993) From elongator tRNA to initiator tRNA Proc Natl Acad Sci U S A 90 2305-2309
Varshney U and RajBhandary U L (1992) Role of methionine and formylation of initiator tRNA in initiation of protein synthesis in Escherichia coli J Bacteriol 174 7819-7826
Williamson J R (2003) After the ribosome structures: how are the subunits assembled? RNA 9 165-167
Xue S and Barna M (2012) Specialized ribosomes: a new frontier in gene regulation and organismal biology Nat Rev Mol Cell Biol 13 355-369
Yap W H, Zhang Z and Wang Y (1999) Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon J Bacteriol 181 5201-5209
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2018-05-05
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