3,286
Views
40
CrossRef citations to date
0
Altmetric
Special Focus Review

The toxin-antitoxin system tisB-istR1

Expression, regulation, and biological role in persister phenotypes

&
Pages 1513-1519 | Received 19 Sep 2012, Accepted 17 Oct 2012, Published online: 23 Oct 2012

References

  • Ogura T, Hiraga S. Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc Natl Acad Sci U S A 1983; 80:4784 - 8; http://dx.doi.org/10.1073/pnas.80.15.4784; PMID: 6308648
  • Gerdes K, Bech FW, Jørgensen ST, Løbner-Olesen A, Rasmussen PB, Atlung T, et al. Mechanism of postsegregational killing by the hok gene product of the parB system of plasmid R1 and its homology with the relF gene product of the E. coli relB operon. EMBO J 1986; 5:2023 - 9; PMID: 3019679
  • Gerdes K, Wagner EG. RNA antitoxins. Curr Opin Microbiol 2007; 10:117 - 24; http://dx.doi.org/10.1016/j.mib.2007.03.003; PMID: 17376733
  • Pedersen K, Gerdes K. Multiple hok genes on the chromosome of Escherichia coli. Mol Microbiol 1999; 32:1090 - 102; http://dx.doi.org/10.1046/j.1365-2958.1999.01431.x; PMID: 10361310
  • Pandey DP, Gerdes K. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 2005; 33:966 - 76; http://dx.doi.org/10.1093/nar/gki201; PMID: 15718296
  • Ramage HR, Connolly LE, Cox JS. Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLoS Genet 2009; 5:e1000767; http://dx.doi.org/10.1371/journal.pgen.1000767; PMID: 20011113
  • Lewis K. Persister cells. Annu Rev Microbiol 2010; 64:357 - 72; http://dx.doi.org/10.1146/annurev.micro.112408.134306; PMID: 20528688
  • Yamaguchi Y, Inouye M. Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat Rev Microbiol 2011; 9:779 - 90; http://dx.doi.org/10.1038/nrmicro2651; PMID: 21927020
  • Gerdes K, Wagner EGH. RNA antitoxins. Curr Opin Microbiol 2007; 10:117 - 24; http://dx.doi.org/10.1016/j.mib.2007.03.003; PMID: 17376733
  • Fozo EM, Makarova KS, Shabalina SA, Yutin N, Koonin EV, Storz G. Abundance of type I toxin-antitoxin systems in bacteria: searches for new candidates and discovery of novel families. Nucleic Acids Res 2010; 38:3743 - 59; http://dx.doi.org/10.1093/nar/gkq054; PMID: 20156992
  • Gerdes K, Christensen SK, Løbner-Olesen A. Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 2005; 3:371 - 82; http://dx.doi.org/10.1038/nrmicro1147; PMID: 15864262
  • 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; http://dx.doi.org/10.1073/pnas.251327898; PMID: 11717402
  • Blower TR, Pei XY, Short FL, Fineran PC, Humphreys DP, Luisi BF, et al. A processed noncoding RNA regulates an altruistic bacterial antiviral system. Nat Struct Mol Biol 2011; 18:185 - 90; http://dx.doi.org/10.1038/nsmb.1981; PMID: 21240270
  • Blower TR, Short FL, Rao F, Mizuguchi K, Pei XY, Fineran PC, et al. Identification and classification of bacterial Type III toxin-antitoxin systems encoded in chromosomal and plasmid genomes. Nucleic Acids Res 2012; 40:6158 - 73; http://dx.doi.org/10.1093/nar/gks231; PMID: 22434880
  • Blower TR, Salmond GP, Luisi BF. Balancing at survival’s edge: the structure and adaptive benefits of prokaryotic toxin-antitoxin partners. Curr Opin Struct Biol 2011; 21:109 - 18; http://dx.doi.org/10.1016/j.sbi.2010.10.009; PMID: 21315267
  • Modell JW, Hopkins AC, Laub MT. A DNA damage checkpoint in Caulobacter crescentus inhibits cell division through a direct interaction with FtsW. Genes Dev 2011; 25:1328 - 43; http://dx.doi.org/10.1101/gad.2038911; PMID: 21685367
  • Van Melderen L, Saavedra De Bast M. Bacterial toxin-antitoxin systems: more than selfish entities?. PLoS Genet 2009; 5:e1000437; http://dx.doi.org/10.1371/journal.pgen.1000437; PMID: 19325885
  • Hayes F. Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 2003; 301:1496 - 9; http://dx.doi.org/10.1126/science.1088157; PMID: 12970556
  • Amitai S, Yassin Y, Engelberg-Kulka H. MazF-mediated cell death in Escherichia coli: a point of no return. J Bacteriol 2004; 186:8295 - 300; http://dx.doi.org/10.1128/JB.186.24.8295-8300.2004; PMID: 15576778
  • Engelberg-Kulka H, Yelin I, Kolodkin-Gal I. Activation of a built-in bacterial programmed cell death system as a novel mechanism of action of some antibiotics. Commun Integr Biol 2009; 2:211 - 2; http://dx.doi.org/10.4161/cib.2.3.7876; PMID: 19641731
  • 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; http://dx.doi.org/10.1128/JB.00527-07; PMID: 17513477
  • Dörr T, Vulić M, Lewis K. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 2010; 8:e1000317; http://dx.doi.org/10.1371/journal.pbio.1000317; PMID: 20186264
  • Maisonneuve E, Shakespeare LJ, Jørgensen MG, Gerdes K. Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci U S A 2011; 108:13206 - 11; http://dx.doi.org/10.1073/pnas.1100186108; PMID: 21788497
  • Losick R, Desplan C. Stochasticity and cell fate. Science 2008; 320:65 - 8; http://dx.doi.org/10.1126/science.1147888; PMID: 18388284
  • Lewis K. Persister cells, dormancy and infectious disease. Nat Rev Microbiol 2007; 5:48 - 56; http://dx.doi.org/10.1038/nrmicro1557; PMID: 17143318
  • Rotem E, Loinger A, Ronin I, Levin-Reisman I, Gabay C, Shoresh N, et al. Regulation of phenotypic variability by a threshold-based mechanism underlies bacterial persistence. Proc Natl Acad Sci U S A 2010; 107:12541 - 6; http://dx.doi.org/10.1073/pnas.1004333107; PMID: 20616060
  • Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EGH, Margalit H, et al. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 2001; 11:941 - 50; http://dx.doi.org/10.1016/S0960-9822(01)00270-6; PMID: 11448770
  • Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S. Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev 2001; 15:1637 - 51; http://dx.doi.org/10.1101/gad.901001; PMID: 11445539
  • Vogel J, Argaman L, Wagner EGH, Altuvia S. The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 2004; 14:2271 - 6; http://dx.doi.org/10.1016/j.cub.2004.12.003; PMID: 15620655
  • Darfeuille F, Unoson C, Vogel J, Wagner EGH. An antisense RNA inhibits translation by competing with standby ribosomes. Mol Cell 2007; 26:381 - 92; http://dx.doi.org/10.1016/j.molcel.2007.04.003; PMID: 17499044
  • Unoson C, Wagner EGH. A small SOS-induced toxin is targeted against the inner membrane in Escherichia coli. Mol Microbiol 2008; 70:258 - 70; http://dx.doi.org/10.1111/j.1365-2958.2008.06416.x; PMID: 18761622
  • Fender A, Elf J, Hampel K, Zimmermann B, Wagner EGH. RNAs actively cycle on the Sm-like protein Hfq. Genes Dev 2010; 24:2621 - 6; http://dx.doi.org/10.1101/gad.591310; PMID: 21123649
  • Wagner EGH, Altuvia S, Romby P. Antisense RNAs in bacteria and their genetic elements. Adv Genet 2002; 46:361 - 98; http://dx.doi.org/10.1016/S0065-2660(02)46013-0; PMID: 11931231
  • Waters LS, Storz G. Regulatory RNAs in bacteria. Cell 2009; 136:615 - 28; http://dx.doi.org/10.1016/j.cell.2009.01.043; PMID: 19239884
  • Unoson C, Wagner EGH. Dealing with stable structures at ribosome binding sites: bacterial translation and ribosome standby. RNA Biol 2007; 4:113 - 7; http://dx.doi.org/10.4161/rna.4.3.5350; PMID: 18094628
  • de Smit MH, van Duin J. Control of translation by mRNA secondary structure in Escherichia coli. A quantitative analysis of literature data. J Mol Biol 1994; 244:144 - 50; http://dx.doi.org/10.1006/jmbi.1994.1714; PMID: 7966326
  • de Smit MH, van Duin J. Translational standby sites: how ribosomes may deal with the rapid folding kinetics of mRNA. J Mol Biol 2003; 331:737 - 43; http://dx.doi.org/10.1016/S0022-2836(03)00809-X; PMID: 12909006
  • de Smit MH, van Duin J. Secondary structure of the ribosome binding site determines translational efficiency: a quantitative analysis. Proc Natl Acad Sci U S A 1990; 87:7668 - 72; http://dx.doi.org/10.1073/pnas.87.19.7668; PMID: 2217199
  • Studer SM, Joseph S. Unfolding of mRNA secondary structure by the bacterial translation initiation complex. Mol Cell 2006; 22:105 - 15; http://dx.doi.org/10.1016/j.molcel.2006.02.014; PMID: 16600874
  • Fozo EM, Hemm MR, Storz G. Small toxic proteins and the antisense RNAs that repress them. Microbiol Mol Biol Rev 2008; 72:579 - 89; http://dx.doi.org/10.1128/MMBR.00025-08; PMID: 19052321
  • Fozo EM, Kawano M, Fontaine F, Kaya Y, Mendieta KS, Jones KL, et al. Repression of small toxic protein synthesis by the Sib and OhsC small RNAs. Mol Microbiol 2008; 70:1076 - 93; http://dx.doi.org/10.1111/j.1365-2958.2008.06394.x; PMID: 18710431
  • Kawano M, Oshima T, Kasai H, Mori H. Molecular characterization of long direct repeat (LDR) sequences expressing a stable mRNA encoding for a 35-amino-acid cell-killing peptide and a cis-encoded small antisense RNA in Escherichia coli. Mol Microbiol 2002; 45:333 - 49; http://dx.doi.org/10.1046/j.1365-2958.2002.03042.x; PMID: 12123448
  • Yamaguchi Y, Inouye M. mRNA interferases, sequence-specific endoribonucleases from the toxin-antitoxin systems. Prog Mol Biol Transl Sci 2009; 85:467 - 500; http://dx.doi.org/10.1016/S0079-6603(08)00812-X; PMID: 19215780
  • Kawano M, Aravind L, Storz G. An antisense RNA controls synthesis of an SOS-induced toxin evolved from an antitoxin. Mol Microbiol 2007; 64:738 - 54; http://dx.doi.org/10.1111/j.1365-2958.2007.05688.x; PMID: 17462020
  • Christensen-Dalsgaard M, Gerdes K. Two higBA loci in the Vibrio cholerae superintegron encode mRNA cleaving enzymes and can stabilize plasmids. Mol Microbiol 2006; 62:397 - 411; http://dx.doi.org/10.1111/j.1365-2958.2006.05385.x; PMID: 17020579
  • Fineran PC, Blower TR, Foulds IJ, Humphreys DP, Lilley KS, Salmond GP. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc Natl Acad Sci U S A 2009; 106:894 - 9; http://dx.doi.org/10.1073/pnas.0808832106; PMID: 19124776
  • 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; http://dx.doi.org/10.1016/S1097-2765(03)00402-7; PMID: 14580342
  • Pedersen K, Zavialov AV, Pavlov MY, Elf J, Gerdes K, Ehrenberg M. The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 2003; 112:131 - 40; http://dx.doi.org/10.1016/S0092-8674(02)01248-5; PMID: 12526800
  • 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; http://dx.doi.org/10.1016/S0022-2836(03)00922-7; PMID: 12972253
  • Gerdes K. Toxin-antitoxin modules may regulate synthesis of macromolecules during nutritional stress. J Bacteriol 2000; 182:561 - 72; http://dx.doi.org/10.1128/JB.182.3.561-572.2000; PMID: 10633087
  • Kolodkin-Gal I, Hazan R, Gaathon A, Carmeli S, Engelberg-Kulka H. A linear pentapeptide is a quorum-sensing factor required for mazEF-mediated cell death in Escherichia coli. Science 2007; 318:652 - 5; http://dx.doi.org/10.1126/science.1147248; PMID: 17962566
  • Vesper O, Amitai S, Belitsky M, Byrgazov K, Kaberdina AC, Engelberg-Kulka H, et al. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 2011; 147:147 - 57; http://dx.doi.org/10.1016/j.cell.2011.07.047; PMID: 21944167
  • Lafleur MD, Qi Q, Lewis K. Patients with long-term oral carriage harbor high-persister mutants of Candida albicans. Antimicrob Agents Chemother 2010; 54:39 - 44; http://dx.doi.org/10.1128/AAC.00860-09; PMID: 19841146
  • 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; http://dx.doi.org/10.1128/JB.186.24.8172-8180.2004; PMID: 15576765
  • Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K. Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 2004; 230:13 - 8; http://dx.doi.org/10.1016/S0378-1097(03)00856-5; PMID: 14734160
  • Shah D, Zhang Z, Khodursky A, Kaldalu N, Kurg K, Lewis K. Persisters: a distinct physiological state of E. coli. BMC Microbiol 2006; 6:53; http://dx.doi.org/10.1186/1471-2180-6-53; PMID: 16768798
  • Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial persistence as a phenotypic switch. Science 2004; 305:1622 - 5; http://dx.doi.org/10.1126/science.1099390; PMID: 15308767
  • LaFleur MD, Kumamoto CA, Lewis K. Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother 2006; 50:3839 - 46; http://dx.doi.org/10.1128/AAC.00684-06; PMID: 16923951
  • Girgis HS, Harris K, Tavazoie S. Large mutational target size for rapid emergence of bacterial persistence. Proc Natl Acad Sci U S A 2012; 109:12740 - 5; http://dx.doi.org/10.1073/pnas.1205124109; PMID: 22802628
  • Lewis K. Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol 2008; 322:107 - 31; http://dx.doi.org/10.1007/978-3-540-75418-3_6; PMID: 18453274
  • Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, Brennan RG. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 2009; 323:396 - 401; http://dx.doi.org/10.1126/science.1163806; PMID: 19150849
  • Dörr T, Lewis K, Vulić M. SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet 2009; 5:e1000760; http://dx.doi.org/10.1371/journal.pgen.1000760; PMID: 20011100
  • Vega NM, Allison KR, Khalil AS, Collins JJ. Signaling-mediated bacterial persister formation. Nat Chem Biol 2012; 8:431 - 3; http://dx.doi.org/10.1038/nchembio.915; PMID: 22426114
  • Pecota DC, Wood TK. Exclusion of T4 phage by the hok/sok killer locus from plasmid R1. J Bacteriol 1996; 178:2044 - 50; PMID: 8606182
  • Kim Y, Wood TK. Toxins Hha and CspD and small RNA regulator Hfq are involved in persister cell formation through MqsR in Escherichia coli. Biochem Biophys Res Commun 2010; 391:209 - 13; http://dx.doi.org/10.1016/j.bbrc.2009.11.033; PMID: 19909729
  • Fozo EM. New type I toxin-antitoxin families from “wild” and laboratory strains of E. coli: Ibs-Sib, ShoB-OhsC and Zor-Orz. RNA Biol 2012; 9; In press; http://dx.doi.org/10.4161/rna.22568; PMID: 23182878

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.