Toxins MazF and MqsR cleave Escherichia coli rRNA precursors at multiple sites

References

• Yamaguchi Y, Park JH, Inouye M. Toxin-antitoxin systems in bacteria and archaea. Ann Rev Genet 2011; 45:61-79; PMID:22060041; http://dx.doi.org/10.1146/annurev-genet-110410-132412
   PubMed Web of Science ®Google Scholar
• Magnuson RD. Hypothetical functions of toxin-antitoxin systems. J Bacteriol 2007; 189:6089-92; PMID:17616596; http://dx.doi.org/10.1128/JB.00958-07
   PubMed Web of Science ®Google Scholar
• Gerdes K, Christensen SK, Lobner-Olesen A. Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 2005; 3:371-82; PMID:15864262; http://dx.doi.org/10.1038/nrmicro1147
   PubMed Web of Science ®Google Scholar
• Tsilibaris V, Maenhaut-Michel G, Mine N, Van Melderen L. What is the benefit to Escherichia coli of having multiple toxin-antitoxin systems in its genome? J Bacteriol 2007; 189:6101-8; PMID:17513477; http://dx.doi.org/10.1128/JB.00527-07
   PubMed Web of Science ®Google Scholar
• Keren I, Shah D, Spoering A, Kaldalu N, Lewis K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 2004; 186:8172-80; PMID:15576765; http://dx.doi.org/10.1128/JB.186.24.8172-8180.2004
   PubMed Web of Science ®Google Scholar
• Maisonneuve E, Castro-Camargo M, Gerdes K. (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 2013; 154:1140-50; PMID:23993101; http://dx.doi.org/10.1016/j.cell.2013.07.048
   PubMed Web of Science ®Google Scholar
• Maisonneuve E, Shakespeare LJ, Jorgensen MG, Gerdes K. Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci U S A 2011; 108:13206-11; PMID:21788497; http://dx.doi.org/10.1073/pnas.1100186108
   PubMed Web of Science ®Google Scholar
• Tuomanen E, Cozens R, Tosch W, Zak O, Tomasz A. The rate of killing of Escherichia coli by beta-lactam antibiotics is strictly proportional to the rate of bacterial growth. J Gen Microbiol 1986; 132:1297-304; PMID:3534137; http://dx.doi.org/10.1099/00221287-132-5-1297
   PubMedGoogle Scholar
• Rotem E, Loinger A, Ronin I, Levin-Reisman I, Gabay C, Shoresh N, Biham O, Balaban NQ. Regulation of phenotypic variability by a threshold-based mechanism underlies bacterial persistence. Proc Natl Acad Sci U S A 2010; 107:12541-6; PMID:20616060; http://dx.doi.org/10.1073/pnas.1004333107
   PubMed Web of Science ®Google Scholar
• Balaban NQ. Persistence: mechanisms for triggering and enhancing phenotypic variability. Curr Opin Genet Dev 2011; 21:768-75; PMID:22051606; http://dx.doi.org/10.1016/j.gde.2011.10.001
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang J, Hoeflich KP, Ikura M, Qing G, Inouye M. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol Cell 2003; 12:913-23; PMID:14580342; http://dx.doi.org/10.1016/S1097-2765(03)00402-7
   PubMed Web of Science ®Google Scholar
• Yamaguchi Y, Park JH, Inouye M. MqsR, a crucial regulator for quorum sensing and biofilm formation, is a GCU-specific mRNA interferase in Escherichia coli. J Biol Chem 2009; 284:28746-53; PMID:19690171; http://dx.doi.org/10.1074/jbc.M109.032904
   PubMed Web of Science ®Google Scholar
• Christensen-Dalsgaard M, Jorgensen MG, Gerdes K. Three new RelE-homologous mRNA interferases of Escherichia coli differentially induced by environmental stresses. Mol Microbiol 2010; 75:333-48; PMID:19943910; http://dx.doi.org/10.1111/j.1365-2958.2009.06969.x
   PubMed Web of Science ®Google Scholar
• Cook GM, Robson JR, Frampton RA, McKenzie J, Przybilski R, Fineran PC, Arcus VL. Ribonucleases in bacterial toxin-antitoxin systems. Biochim Biophys Acta 2013; 1829:523-31; PMID:23454553; http://dx.doi.org/10.1016/j.bbagrm.2013.02.007
   PubMed Web of Science ®Google Scholar
• Cruz JW, Sharp JD, Hoffer ED, Maehigashi T, Vvedenskaya IO, Konkimalla A, Husson RN, Nickels BE, Dunham CM, Woychik NA. Growth-regulating Mycobacterium tuberculosis VapC-mt4 toxin is an isoacceptor-specific tRNase. Nat Commun 2015; 6:7480; PMID:26158745; http://dx.doi.org/10.1038/ncomms8480
   PubMed Web of Science ®Google Scholar
• Lopes AP, Lopes LM, Fraga TR, Chura-Chambi RM, Sanson AL, Cheng E, Nakajima E, Morganti L, Martins EA. VapC from the leptospiral VapBC toxin-antitoxin module displays ribonuclease activity on the initiator tRNA. PloS One 2014; 9:e101678; PMID:25047537; http://dx.doi.org/10.1371/journal.pone.0101678
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Winther K, Tree JJ, Tollervey D, Gerdes K. VapCs of Mycobacterium tuberculosis cleave RNAs essential for translation. Nucleic Acids Res 2016; 44:9860-71; PMID:27599842; http://dx.doi.org/10.1093/nar/gkw781
   Google Scholar
• Winther KS, Brodersen DE, Brown AK, Gerdes K. VapC20 of Mycobacterium tuberculosis cleaves the sarcin-ricin loop of 23S rRNA. Nat Commun 2013; 4:2796; PMID:24225902; http://dx.doi.org/10.1038/ncomms3796
   PubMed Web of Science ®Google Scholar
• Voorhees RM, Schmeing TM, Kelley AC, Ramakrishnan V. The mechanism for activation of GTP hydrolysis on the ribosome. Science 2010; 330:835-8; PMID:21051640; http://dx.doi.org/10.1126/science.1194460
   PubMed Web of Science ®Google Scholar
• Wallin G, Kamerlin SC, Aqvist J. Energetics of activation of GTP hydrolysis on the ribosome. Nat Commun 2013; 4:1733; PMID:23591900; http://dx.doi.org/10.1038/ncomms2741
   PubMed Web of Science ®Google Scholar
• Shi X, Khade PK, Sanbonmatsu KY, Joseph S. Functional role of the sarcin-ricin loop of the 23S rRNA in the elongation cycle of protein synthesis. J Mol Biol 2012; 419:125-38; PMID:22459262; http://dx.doi.org/10.1016/j.jmb.2012.03.016
   PubMed Web of Science ®Google Scholar
• Schifano JM, Cruz JW, Vvedenskaya IO, Edifor R, Ouyang M, Husson RN, Nickels BE, Woychik NA. tRNA is a new target for cleavage by a MazF toxin. Nucleic Acids Res 2016; 44:1256-70; PMID:26740583; http://dx.doi.org/10.1093/nar/gkv1370
   PubMed Web of Science ®Google Scholar
• Schifano JM, Vvedenskaya IO, Knoblauch JG, Ouyang M, Nickels BE, Woychik NA. An RNA-seq method for defining endoribonuclease cleavage specificity identifies dual rRNA substrates for toxin MazF-mt3. Nat Commun 2014; 5:3538; PMID:24709835; http://dx.doi.org/10.1038/ncomms4538
   PubMed Web of Science ®Google Scholar
• Schifano JM, Edifor R, Sharp JD, Ouyang M, Konkimalla A, Husson RN, Woychik NA. Mycobacterial toxin MazF-mt6 inhibits translation through cleavage of 23S rRNA at the ribosomal A site. Proc Natl Acad Sci U S A 2013; 110:8501-6; PMID:23650345; http://dx.doi.org/10.1073/pnas.1222031110
   PubMed Web of Science ®Google Scholar
• Simanshu DK, Yamaguchi Y, Park JH, Inouye M, Patel DJ. Structural basis of mRNA recognition and cleavage by toxin MazF and its regulation by antitoxin MazE in Bacillus subtilis. Mol Cell 2013; 52:447-58; PMID:24120662; http://dx.doi.org/10.1016/j.molcel.2013.09.006
   PubMed Web of Science ®Google Scholar
• Zorzini V, Mernik A, Lah J, Sterckx YG, De Jonge N, Garcia-Pino A, De Greve H, Versées W, Loris R. Substrate Recognition and Activity Regulation of the Escherichia coli mRNA Endonuclease MazF. J Biol Chem 2016; 291:10950-60; PMID:27026704; http://dx.doi.org/10.1074/jbc.M116.715912
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Sauert M, Wolfinger MT, Vesper O, Muller C, Byrgazov K, Moll I. The MazF-regulon: a toolbox for the post-transcriptional stress response in Escherichia coli. Nucleic Acids Res 2016; 44:6660-75; PMID:26908653; http://dx.doi.org/10.1093/nar/gkw115
   PubMed Web of Science ®Google Scholar
• Amitai S, Kolodkin-Gal I, Hananya-Meltabashi M, Sacher A, Engelberg-Kulka H. Escherichia coli MazF leads to the simultaneous selective synthesis of both “death proteins” and “survival proteins.” PLoS Genet 2009; 5:e1000390; PMID:19282968; http://dx.doi.org/10.1371/journal.pgen.1000390
   PubMedGoogle Scholar
• Kasari V, Mets T, Tenson T, Kaldalu N. Transcriptional cross-activation between toxin-antitoxin systems of Escherichia coli. BMC Microbiol 2013; 13:45; PMID:23432955; http://dx.doi.org/10.1186/1471-2180-13-45
   PubMed Web of Science ®Google Scholar
• Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, Chabas S, Reiche K, Hackermüller J, Reinhardt R, et al. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 2010; 464:250-5; PMID:20164839; http://dx.doi.org/10.1038/nature08756
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang J, Hara H, Kato I, Inouye M. Insights into the mRNA cleavage mechanism by MazF, an mRNA interferase. J Biol Chem 2005; 280:3143-50; PMID:15537630; http://dx.doi.org/10.1074/jbc.M411811200
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhu L, Zhang J, Inouye M. Characterization of ChpBK, an mRNA interferase from Escherichia coli. J Biol Chem 2005; 280:26080-8; PMID:15901733; http://dx.doi.org/10.1074/jbc.M502050200
   PubMed Web of Science ®Google Scholar
• Pellegrini O, Mathy N, Gogos A, Shapiro L, Condon C. The Bacillus subtilis ydcDE operon encodes an endoribonuclease of the MazF/PemK family and its inhibitor. Mol Microbiol 2005; 56:1139-48; PMID:15882409; http://dx.doi.org/10.1111/j.1365-2958.2005.04606.x
   PubMed Web of Science ®Google Scholar
• Kamphuis MB, Bonvin AM, Monti MC, Lemonnier M, Munoz-Gomez A, van den Heuvel RH, Díaz-Orejas R, Boelens R. Model for RNA binding and the catalytic site of the RNase Kid of the bacterial parD toxin-antitoxin system. J Mol Biol 2006; 357:115-26; PMID:16413033; http://dx.doi.org/10.1016/j.jmb.2005.12.033
   PubMed Web of Science ®Google Scholar
• Cannistraro VJ, Kennell D. The 5′ ends of RNA oligonucleotides in Escherichia coli and mRNA degradation. Eur J Biochem 1993; 213:285-93; PMID:7682943; http://dx.doi.org/10.1111/j.1432-1033.1993.tb17761.x
   PubMedGoogle Scholar
• Basturea GN, Zundel MA, Deutscher MP. Degradation of ribosomal RNA during starvation: comparison to quality control during steady-state growth and a role for RNase PH. Rna 2011; 17:338-45; PMID:21135037; http://dx.doi.org/10.1261/rna.2448911
   PubMed Web of Science ®Google Scholar
• Maivali U, Paier A, Tenson T. When stable RNA becomes unstable: the degradation of ribosomes in bacteria and beyond. Biol Chem 2013; 394:845-55; PMID:23612597; http://dx.doi.org/10.1515/hsz-2013-0133
   PubMed Web of Science ®Google Scholar
• Piir K, Paier A, Liiv A, Tenson T, Maivali U. Ribosome degradation in growing bacteria. EMBO Rep 2011; 12:458-62; PMID:21460796; http://dx.doi.org/10.1038/embor.2011.47
   PubMed Web of Science ®Google Scholar
• Deutscher MP. Maturation and degradation of ribosomal RNA in bacteria. Prog Mol Biol Transl Sci 2009; 85:369-91; PMID:19215777; http://dx.doi.org/10.1016/S0079-6603(08)00809-X
   PubMed Web of Science ®Google Scholar
• Das U, Shuman S. Mechanism of RNA 2′,3′-cyclic phosphate end healing by T4 polynucleotide kinase-phosphatase. Nucleic Acids Res 2013; 41:355-65; PMID:23118482; http://dx.doi.org/10.1093/nar/gks977
   PubMed Web of Science ®Google Scholar
• Romero DA, Hasan AH, Lin YF, Kime L, Ruiz-Larrabeiti O, Urem M, Bucca G, Mamanova L, Laing EE, van Wezel GP, et al. A comparison of key aspects of gene regulation in Streptomyces coelicolor and Escherichia coli using nucleotide-resolution transcription maps produced in parallel by global and differential RNA sequencing. Mol Microbiol 2014; 94:963-87; PMID:25266672; http://dx.doi.org/10.1111/mmi.12810
   Web of Science ®Google Scholar
• Sulthana S, Basturea GN, Deutscher MP. Elucidation of pathways of ribosomal RNA degradation: an essential role for RNase E. Rna; 22:1163-71; PMID:27298395; http://dx.doi.org/10.1261/rna.056275.116
   PubMed Web of Science ®Google Scholar
• Dahlberg AE, Dahlberg JE, Lund E, Tokimatsu H, Rabson AB, Calvert PC, Reynolds F, Zahalak M. Processing of the 5′ end of Escherichia coli 16S ribosomal RNA. Proc Natl Acad Sci U S A 1978; 75:3598-602; PMID:358190; http://dx.doi.org/10.1073/pnas.75.8.3598
   PubMed Web of Science ®Google Scholar
• Sirdeshmukh R, Schlessinger D. Ordered processing of Escherichia coli 23S rRNA in vitro. Nucleic Acids Res 1985; 13:5041-54; PMID:2991850; http://dx.doi.org/10.1093/nar/13.14.5041
   PubMed Web of Science ®Google Scholar
• Srivastava AK, Schlessinger D. Coregulation of processing and translation: mature 5′ termini of Escherichia coli 23S ribosomal RNA form in polysomes. Proc Natl Acad Sci U S A 1988; 85:7144-8; PMID:3050989; http://dx.doi.org/10.1073/pnas.85.19.7144
   PubMed Web of Science ®Google Scholar
• Sirdeshmukh R, Schlessinger D. Why is processing of 23 S ribosomal RNA in Escherichia coli not obligate for its function? J Mol Biol 1985; 186:669-72; PMID:3912511; http://dx.doi.org/10.1016/0022-2836(85)90139-1
   PubMed Web of Science ®Google Scholar
• Luidalepp H, Berger S, Joss O, Tenson T, Polacek N. Ribosome shut-down by 16S rRNA fragmentation in stationary phase E. coli. J Mol Biol 2016; 428:2237-47; PMID:27067112; http://dx.doi.org/10.1016/j.jmb.2016.01.033
   PubMed Web of Science ®Google Scholar
• Christensen SK, Pedersen K, Hansen FG, Gerdes K. Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. J Mol Biol 2003; 332:809-19; PMID:12972253; http://dx.doi.org/10.1016/S0022-2836(03)00922-7
   PubMed Web of Science ®Google Scholar
• Sat B, Hazan R, Fisher T, Khaner H, Glaser G, Engelberg-Kulka H. Programmed cell death in Escherichia coli: some antibiotics can trigger mazEF lethality. J Bacteriol 2001; 183:2041-5; PMID:11222603; http://dx.doi.org/10.1128/JB.183.6.2041-2045.2001
   PubMed Web of Science ®Google Scholar
• Lancaster LE, Savelsbergh A, Kleanthous C, Wintermeyer W, Rodnina MV. Colicin E3 cleavage of 16S rRNA impairs decoding and accelerates tRNA translocation on Escherichia coli ribosomes. Mol Microbiol 2008; 69:390-401; PMID:18485067; http://dx.doi.org/10.1111/j.1365-2958.2008.06283.x
   PubMed Web of Science ®Google Scholar
• Siibak T, Peil L, Donhofer A, Tats A, Remm M, Wilson DN, Tenson T, Remme J. Antibiotic-induced ribosomal assembly defects result from changes in the synthesis of ribosomal proteins. Mol Microbiol 2011; 80:54-67; PMID:21320180; http://dx.doi.org/10.1111/j.1365-2958.2011.07555.x
   PubMed Web of Science ®Google Scholar
• Siibak T, Peil L, Xiong L, Mankin A, Remme J, Tenson T. Erythromycin- and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition. Antimicrob Agents Chemother 2009; 53:563-71; PMID:19029332; http://dx.doi.org/10.1128/AAC.00870-08
   PubMed Web of Science ®Google Scholar
• Dodd J, Kolb JM, Nomura M. Lack of complete cooperativity of ribosome assembly in vitro and its possible relevance to in vivo ribosome assembly and the regulation of ribosomal gene expression. Biochimie 1991; 73:757-67; PMID:1764521; http://dx.doi.org/10.1016/0300-9084(91)90055-6
   PubMed Web of Science ®Google Scholar
• Ainelo A, Tamman H, Leppik M, Remme J, Horak R. The toxin GraT inhibits ribosome biogenesis. Mol Microbiol 2016; 100:719-34; PMID:26833678; http://dx.doi.org/10.1111/mmi.13344
   PubMed Web of Science ®Google Scholar
• Suzuki M, Zhang J, Liu M, Woychik NA, Inouye M. Single protein production in living cells facilitated by an mRNA interferase. Mol Cell 2005; 18:253-61; PMID:15837428; http://dx.doi.org/10.1016/j.molcel.2005.03.011
   PubMed Web of Science ®Google Scholar
• Christensen SK, Mikkelsen M, Pedersen K, Gerdes K. RelE, a global inhibitor of translation, is activated during nutritional stress. Proc Natl Acad Sci U S A 2001; 98:14328-33; PMID:11717402; http://dx.doi.org/10.1073/pnas.251327898
   PubMed Web of Science ®Google Scholar
• Ray AE, Connon SA, Sheridan PP, Gilbreath J, Shields M, Newby DT, Fujita Y, Magnuson TS. Intragenomic heterogeneity of the 16S rRNA gene in strain UFO1 caused by a 100-bp insertion in helix 6. FEMS Microbiol Ecol 2010; 72:343-53; PMID:20557571; http://dx.doi.org/10.1111/j.1574-6941.2010.00868.x
   PubMed Web of Science ®Google Scholar
• Evguenieva-Hackenberg E. Bacterial ribosomal RNA in pieces. Mol Microbiol 2005; 57:318-25; PMID:15978067; http://dx.doi.org/10.1111/j.1365-2958.2005.04662.x
   PubMed Web of Science ®Google Scholar
• Winkler ME. Ribosomal ribonucleic acid isolated from Salmonella typhimurium: absence of the intact 23S species. J Bacteriol 1979; 139:842-9; PMID:383696
   PubMed Web of Science ®Google Scholar
• Cochella L, Brunelle JL, Green R. Mutational analysis reveals two independent molecular requirements during transfer RNA selection on the ribosome. Nat Struct Mol Biol 2007; 14:30-6; PMID:17159993; http://dx.doi.org/10.1038/nsmb1183
   PubMed Web of Science ®Google Scholar
• Leonov AA, Sergiev PV, Bogdanov AA, Brimacombe R, Dontsova OA. Affinity purification of ribosomes with a lethal G2655C mutation in 23 S rRNA that affects the translocation. J Biol Chem 2003; 278:25664-70; PMID:12730236; http://dx.doi.org/10.1074/jbc.M302873200
   PubMed Web of Science ®Google Scholar
• Gregory ST, O'Connor M, Dahlberg AE. Functional Escherichia coli 23S rRNAs containing processed and unprocessed intervening sequences from Salmonella typhimurium. Nucleic Acids Res 1996; 24:4918-23; PMID:9016661; http://dx.doi.org/10.1093/nar/24.24.4918
   PubMed Web of Science ®Google Scholar
• Gourse RL, Gaal T, Bartlett MS, Appleman JA, Ross W. rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. Ann Rev Microbiol 1996; 50:645-77; PMID:8905094; http://dx.doi.org/10.1146/annurev.micro.50.1.645
   PubMed Web of Science ®Google Scholar
• Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10:R25; PMID:19261174; http://dx.doi.org/10.1186/gb-2009-10-3-r25
   PubMed Web of Science ®Google Scholar
• Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078-9; PMID:19505943; http://dx.doi.org/10.1093/bioinformatics/btp352
   PubMed Web of Science ®Google Scholar
• Noeske J, Huang J, Olivier NB, Giacobbe RA, Zambrowski M, Cate JH. Synergy of streptogramin antibiotics occurs independently of their effects on translation. Antimicrob Agents Chemother; 58:5269-79; PMID:24957822; http://dx.doi.org/10.1128/AAC.03389-14
   PubMed Web of Science ®Google Scholar