Type II Toxin-Antitoxins Loci: The relBE Family

Chapter

Abstract

relBE of Escherichia coli K-12 is a paradigm TA locus. Here, I describe the discovery of relBE and review the genetic, physiological, biochemical and structural analyses that have led to important insights into TA biology. Five relBE homologues of K-12 are also described while the 6th (mqsRA) is treated in a separate Chapter. Finally, a discussion of the possible biological functions of relBE and other type II TA loci sets the stage for future work on prokaryotic type II TA loci.

Keywords

Plasmid Stabilization RelE Homolog Persister Cell Brucella Abortus Conditional Cooperativity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by the Wellcome Trust. I thank members of the Gerdes group and of the Centre for Bacterial Cell Biology for friendly and stimulating discussions.

References

  1. Afif, H., Allali, N., Couturier, M., & Van Melderen, L. (2001). The ratio between CcdA and CcdB modulates the transcriptional repression of the ccd poison-antidote system. Molecular Microbiology, 41, 73–82.PubMedCrossRefGoogle Scholar
  2. Anantharaman, V., & Aravind, L. (2003). New connections in the prokaryotic toxin–antitoxin network: Relationship with the eukaryotic nonsense-mediated RNA decay system. Genome Biology, 4, R81.PubMedCrossRefGoogle Scholar
  3. Andreev, D., Hauryliuk, V., Terenin, I., Dmitriev, S., Ehrenberg, M., & Shatsky, I. (2008). The bacterial toxin RelE induces specific mRNA cleavage in the A site of the eukaryote ribosome. RNA, 14, 233–239.PubMedCrossRefGoogle Scholar
  4. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L., & Leibler, S. (2004). Bacterial persistence as a phenotypic switch. Science, 305, 1622–1625.PubMedCrossRefGoogle Scholar
  5. Barbosa, L. C., Garrido, S. S., Garcia, A., Delfino, D. B., & Marchetto, R. (2010). Function inferences from a molecular structural model of bacterial ParE toxin. Bioinformation, 4, 438–440.PubMedCrossRefGoogle Scholar
  6. Bech, F. W., Jorgensen, S. T., Diderichsen, B., & Karlstrom, O. H. (1985). Sequence of the Relb Transcription Unit from Escherichia-Coli and Identification of the RelB Gene. EMBO Journal, 4, 1059–1066.PubMedGoogle Scholar
  7. Bigger, J. W. (1944). Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet, ii, 497–500.CrossRefGoogle Scholar
  8. Blower, T. R., Pei, X. Y., Short, F. L., Fineran, P. C., Humphreys, D. P., Luisi, B. F., et al. (2011). A processed noncoding RNA regulates an altruistic bacterial antiviral system. Nature Structural and Molecular Biology, 18, 185–190.PubMedCrossRefGoogle Scholar
  9. Boe, L., Gerdes, K., & Molin, S. (1987). Effects of genes exerting growth inhibition and plasmid stability on plasmid maintenance. Journal of Bacteriology, 169, 4646–4650.PubMedGoogle Scholar
  10. Bordes, P., Cirinesi, A. M., Ummels, R., Sala, A., Sakr, S., Bitter, W., et al. (2011). SecB-like chaperone controls a toxin–antitoxin stress-responsive system in mycobacterium tuberculosis. Proceedings of the National Academy of Sciences of the U S A, 108, 8438–8443.CrossRefGoogle Scholar
  11. Brown, J. M., & Shaw, K. J. (2003). A novel family of Escherichia coli toxin–antitoxin gene pairs. Journal of Bacteriology, 185, 6600–6608.PubMedCrossRefGoogle Scholar
  12. Brown, B. L., Grigoriu, S., Kim, Y., Arruda, J. M., Davenport, A., Wood, T. K., et al. (2009). Three dimensional structure of the MqsR:MqsA complex: A novel TA pair comprised of a toxin homologous to RelE and an antitoxin with unique properties. PLoS Pathogens, 5, e1000706.PubMedCrossRefGoogle Scholar
  13. Chadani, Y., Ono, K., Ozawa, S., Takahashi, Y., Takai, K., Nanamiya, H., et al. (2010). Ribosome rescue by Escherichia coli ArfA (YhdL) in the absence of trans-translation system. Molecular Microbiology, 78, 796–808.PubMedCrossRefGoogle Scholar
  14. Cherny, I., & Gazit, E. (2004). The YefM antitoxin defines a family of natively unfolded proteins—implications as a novel antibacterial target. Journal of Biological Chemistry, 279, 8252–8261.PubMedCrossRefGoogle Scholar
  15. Cherny, I., Overgaard, M., Borch, J., Bram, Y., Gerdes, K., & Gazit, E. (2007). Structural and thermodynamic characterization of the Escherichia coli RelBE toxin–antitoxin system: Indication for a functional role of differential stability. Biochemistry, 46, 12152–12163.PubMedCrossRefGoogle Scholar
  16. Christensen, S. K., & Gerdes, K. (2003). RelE toxins from bacteria and Archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Molecular Microbiology, 48, 1389–1400.PubMedCrossRefGoogle Scholar
  17. Christensen, S. K., & Gerdes, K. (2004). Delayed-relaxed response explained by hyperactivation of RelE. Molecular Microbiology, 53, 587–597.PubMedCrossRefGoogle Scholar
  18. Christensen, S. K., Mikkelsen, M., Pedersen, K., & Gerdes, K. (2001). RelE, a global inhibitor of translation, is activated during nutritional stress. Proceedings of the National Academy of Sciences of the U S A, 98, 14328–14333.CrossRefGoogle Scholar
  19. Christensen, S. K., Maenhaut-Michel, G., Mine, N., Gottesman, S., Gerdes, K., & Van Melderen, L. (2004). Overproduction of the lon protease triggers inhibition of translation in Escherichia coli: Involvement of the yefM-yoeB toxin–antitoxin system. Molecular Microbiology, 51, 1705–1717.PubMedCrossRefGoogle Scholar
  20. Christensen, S. K., Pedersen, K., Hansen, F. G., & Gerdes, K. (2003). Toxin–antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. Journal of Molecular Biology, 332, 809–819.PubMedCrossRefGoogle Scholar
  21. Christensen-Dalsgaard, M., & Gerdes, K. (2006). Two higBA loci in the Vibrio cholerae superintegron encode mRNA cleaving enzymes and can stabilize plasmids. Molecular Microbiology, 62, 397–411.PubMedCrossRefGoogle Scholar
  22. Christensen-Dalsgaard, M., & Gerdes, K. (2008). Translation affects YoeB and MazF messenger RNA interferase activities by different mechanisms. Nucleic Acids Research, 36, 6472–6481.PubMedCrossRefGoogle Scholar
  23. Christensen-Dalsgaard, M., Jørgensen, M. G., & Gerdes, K. (2010). Three new RelE-homologous mRNA interferases of Escherichia coli differentially induced by environmental stresses. Molecular Microbiology, 75, 333–348.PubMedCrossRefGoogle Scholar
  24. Coles, M., Djuranovic, S., Soding, J., Frickey, T., Koretke, K., Truffault, V., et al. (2005). AbrB-like transcription factors assume a swapped hairpin fold that is evolutionarily related to double-psi beta barrels. Structure, 13, 919–928.PubMedCrossRefGoogle Scholar
  25. Cooper, C. R., Daugherty, A. J., Tachdjian, S., Blum, P. H., & Kelly, R. M. (2009). Role of vapBC toxin–antitoxin loci in the thermal stress response of Sulfolobus solfataricus. Biochemical Society Transactions, 37, 123–126.PubMedCrossRefGoogle Scholar
  26. Dao-Thi, M. H., Van Melderen, L., De Genst, E., Afif, H., Buts, L., Wyns, L., et al. (2005). Molecular basis of gyrase poisoning by the addiction toxin CcdB. Journal of Molecular Biology, 348, 1091–1102.PubMedCrossRefGoogle Scholar
  27. De Fernandez-Henestrosa, A. R., Ogi, T., Aoyagi, S., Chafin, D., Hayes, J. J., Ohmori, H., et al. (2000). Identification of additional genes belonging to the LexA regulon in Escherichia coli. Molecular Microbiology, 35, 1560–1572.CrossRefGoogle Scholar
  28. Fineran, P. C., Blower, T. R., Foulds, I. J., Humphreys, D. P., Lilley, K. S., & Salmond, G. P. (2009). The phage abortive infection system, ToxIN, functions as a protein-RNA toxin–antitoxin pair. Proceedings of the National Academy of Sciences of the U.S.A., 106, 894–899.CrossRefGoogle Scholar
  29. Francuski, D., & Saenger, W. (2009). Crystal structure of the antitoxin–toxin protein complex RelB-RelE from Methancaldococcus jannaschii. Journal of Molecular Biology, 393, 898–908.PubMedCrossRefGoogle Scholar
  30. Garcia-Pino, A., Balasubramanian, S., Wyns, L., Gazit, E., De Greve, H., Magnuson, R. D., et al. (2010). Allostery and intrinsic disorder mediate transcription regulation by conditional cooperativity. Cell, 142, 101–111.PubMedCrossRefGoogle Scholar
  31. Garza-Sanchez, F., Schaub, R. E., Janssen, B. D., & Hayes, C. S. (2011). tmRNA regulates synthesis of the ArfA ribosome rescue factor. Molecular Microbiology, 80, 1204–1219.PubMedCrossRefGoogle Scholar
  32. Gerdes, K. (2000). Toxin–antitoxin modules may regulate synthesis of macromolecules during nutritional stress. Journal of Bacteriology, 182, 561–572.PubMedCrossRefGoogle Scholar
  33. Gerdes, K., Bech, F. W., Jorgensen, S. T., Lobnerolesen, A., Rasmussen, P. B., Atlung, T., et al. (1986a). 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 Escherichia-Coli Relb operon. EMBO Journal, 5, 2023–2029.PubMedGoogle Scholar
  34. Gerdes, K., Larsen, J. E., & Molin, S. (1985). Stable inheritance of plasmid R1 requires two different loci. Journal of Bacteriology, 161, 292–298.PubMedGoogle Scholar
  35. Gerdes, K., Rasmussen, P. B., & Molin, S. (1986b). Unique type of plasmid maintenance function—postsegregational killing of plasmid-free cells. Proceedings of the National Academy of Sciences of the U.S.A., 83, 3116–3120.CrossRefGoogle Scholar
  36. Gotfredsen, M., & Gerdes, K. (1998). The Escherichia coli relBE genes belong to a new toxin–antitoxin gene family. Molecular Microbiology, 29, 1065–1076.PubMedCrossRefGoogle Scholar
  37. Grady, R., & Hayes, F. (2003). Axe-Txe, a broad-spectrum proteic toxin–antitoxin system specified by a multidrug-resistant, clinical isolate of Enterococcus faecium. Molecular Microbiology, 47, 1419–1432.PubMedCrossRefGoogle Scholar
  38. Grønlund, H., & Gerdes, K. (1999). Toxin–antitoxin systems homologous with relBE of Escherichia coli plasmid P307 are ubiquitous in prokaryotes. Journal of Molecular Biology, 285, 1401–1415.PubMedCrossRefGoogle Scholar
  39. Hazan, R., & Engelberg-Kulka, H. (2004). Escherichia coli mazEF-mediated cell death as a defence mechanism that inhibits the spread of phage P1. Molecular Genetics and Genomics, 272, 227–234.PubMedCrossRefGoogle Scholar
  40. Heaton, B. E., Herrou, J., Blackwell, A. E., Wysocki, V. H., & Crosson, S. (2012). Molecular structure and function of the novel BrnT/BrnA toxin–antitoxin system of brucella abortus. Journal of Biological Chemistry, 287, 12098–12110.PubMedCrossRefGoogle Scholar
  41. Hiraga, S., Jaffe, A., Ogura, T., Mori, H., & Takahashi, H. (1986). F-Plasmid Ccd mechanism in Escherichia-Coli. Journal of Bacteriology, 166, 100–104.PubMedGoogle Scholar
  42. Ivanova, N., Pavlov, M. Y., & Ehrenberg, M. (2005). tmRNA-induced release of messenger RNA from stalled ribosomes. Journal of Molecular Biology, 350, 897–905.PubMedCrossRefGoogle Scholar
  43. Jensen, R. B., Grohmann, E., Schwab, H., Diazorejas, R., & Gerdes, K. (1995). Comparison of Ccd of F, Parde of Rp4, and Pard of R1 using a novel conditional replication control-system of plasmid R1. Molecular Microbiology, 17, 211–220.PubMedCrossRefGoogle Scholar
  44. Jiang, Y., Pogliano, J., Helinski, D. R., & Konieczny, I. (2002). ParE toxin encoded by the broad-host-range plasmid RK2 is an inhibitor of Escherichia coli gyrase. Molecular Microbiology, 44, 971–979.PubMedCrossRefGoogle Scholar
  45. Jørgensen, M. G., Pandey, D. P., Jaskolska, M., & Gerdes, K. (2009). HicA of Escherichia coli defines a novel family of translation-independent mRNA interferases in bacteria and archaea. Journal of Bacteriology, 191, 1191–1199.PubMedCrossRefGoogle Scholar
  46. Kamada, K., & Hanaoka, F. (2005). Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin. Molecular Cell, 19, 497–509.PubMedCrossRefGoogle Scholar
  47. Kamada, K., Hanaoka, F., & Burley, S. K. (2003). Crystal structure of the MazE/MazF complex: Molecular bases of antidote-toxin recognition. Molecular Cell, 11, 875–884.PubMedCrossRefGoogle Scholar
  48. Keiler, K. C. (2008). Biology of trans-translation. Annual Review of Microbiology, 62, 133–151.PubMedCrossRefGoogle Scholar
  49. Keren, I., Shah, D., Spoering, A., Kaldalu, N., & Lewis, K. (2004). Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. Journal of Bacteriology, 186, 8172–8180.PubMedCrossRefGoogle Scholar
  50. Khoo, S. K., Loll, B., Chan, W. T., Shoeman, R. L., Ngoo, L., Yeo, C. C., et al. (2007). Molecular and structural characterization of the PezAT chromosomal toxin–antitoxin system of the human pathogen Streptococcus pneumoniae. Journal of Biological Chemistry, 282, 19606–19618.PubMedCrossRefGoogle Scholar
  51. Kiino, D. R., Phillips, G. J., & Silhavy, T. J. (1990). Increased expression of the bifunctional protein PrlF suppresses overproduction lethality associated with exported beta-galactosidase hybrid proteins in Escherichia coli. Journal of Bacteriology, 172, 185–192.PubMedGoogle Scholar
  52. Kiino, D. R., & Silhavy, T. J. (1984). Mutation prlF1 relieves the lethality associated with export of beta-galactosidase hybrid proteins in Escherichia coli. Journal of Bacteriology, 158, 878–883.PubMedGoogle Scholar
  53. Kristoffersen, P., Jensen, G. B., Gerdes, K., & Piskur, J. (2000). Bacterial toxin–antitoxin gene system as containment control in yeast cells. Applied and Environmental Microbiology, 66, 5524–5526.PubMedCrossRefGoogle Scholar
  54. Lavalle, R. (1965). New mutants for regulation of RNA synthesis. Bull Soc Chim Biol (Paris), 47, 1567–1570.Google Scholar
  55. Lewis, K. (2010). Persister cells. Annual Review of Microbiology, 64, 357–372.PubMedCrossRefGoogle Scholar
  56. Lewis, L. K., Harlow, G. R., Gregg-Jolly, L. A., & Mount, D. W. (1994). Identification of high affinity binding sites for LexA which define new DNA damage-inducible genes in Escherichia coli. Journal of Molecular Biology, 241, 507–523.PubMedCrossRefGoogle Scholar
  57. Li, G. Y., Zhang, Y., Inouye, M., & Ikura, M. (2008). Structural mechanism of transcriptional autorepression of the Escherichia coli RelB/RelE antitoxin/toxin module. Journal of Molecular Biology, 380, 107–119.PubMedCrossRefGoogle Scholar
  58. Li, G. Y., Zhang, Y., Inouye, M., & Ikura, M. (2009). Inhibitory mechanism of Escherichia coli RelE-RelB toxin–antitoxin module involves a helix displacement near an mRNA interferase active site. Journal of Biological Chemistry, 284, 14628–14636.PubMedCrossRefGoogle Scholar
  59. Magnuson, R. D. (2007). Hypothetical functions of toxin–antitoxin systems. Journal of Bacteriology, 189, 6089–6092.PubMedCrossRefGoogle Scholar
  60. Magnusson, L. U., Farewell, A., & Nyström, T. (2005). ppGpp a global regulator in Escherichia coli. Trends in Microbiology, 13, 236–242.PubMedCrossRefGoogle Scholar
  61. Maisonneuve, E., Shakespeare, L. J., Jorgensen, M. G., & Gerdes, K. (2011). Bacterial persistence by RNA endonucleases. Proceedings of the National Academy of Sciences of the U S A, 108, 13206–13211.CrossRefGoogle Scholar
  62. Motiejunaite, R., Armalyte, J., Markuckas, A., & Suziedeliene, E. (2007). Escherichia coli dinJ-yafQ genes act as a toxin–antitoxin module. FEMS Microbiology Letters, 268, 112–119.PubMedCrossRefGoogle Scholar
  63. Moyed, H. S., & Bertrand, K. P. (1983). hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. Journal of Bacteriology, 155, 768–775.PubMedGoogle Scholar
  64. Neubauer, C., Gao, Y. G., Andersen, K. R., Dunham, C. M., Kelley, A. C., Hentschel, J., et al. (2009). The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE. Cell, 139, 1084–1095.PubMedCrossRefGoogle Scholar
  65. Odaert, B., Saida, F., Aliprandi, P., Durand, S., Crechet, J. B., Guerois, R., et al. (2007). Structural and functional studies of RegB, a new member of a family of sequence-specific ribonucleases involved in mRNA inactivation on the ribosome. Journal of Biological Chemistry, 282, 2019–2028.PubMedCrossRefGoogle Scholar
  66. Ogura, T., & Hiraga, S. (1983). Mini-F plasmid genes that couple host-cell division to plasmid proliferation. Proceedings of the National Academy of Sciences of the U.S.A., 80, 4784–4788.CrossRefGoogle Scholar
  67. Overgaard, M., Borch, J., & Gerdes, K. (2009). RelB and RelE of Escherichia coli form a tight complex that represses transcription via the ribbon-helix-helix motif in RelB. Journal of Molecular Biology, 394, 183–196.PubMedCrossRefGoogle Scholar
  68. Overgaard, M., Borch, J., Jorgensen, M. G., & Gerdes, K. (2008). Messenger RNA interferase RelE controls relBE transcription by conditional cooperativity. Molecular Microbiology, 69, 841–857.PubMedCrossRefGoogle Scholar
  69. Pandey, D. P., & Gerdes, K. (2005). Toxin–antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Research, 33, 966–976.PubMedCrossRefGoogle Scholar
  70. Pecota, D. C., & Wood, T. K. (1996). Exclusion of T4 phage by the hok/sok killer locus from plasmid R1. Journal of Bacteriology, 178, 2044–2050.PubMedGoogle Scholar
  71. Pedersen, K., Christensen, S. K., & Gerdes, K. (2002). Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Molecular Microbiology, 45, 501–510.PubMedCrossRefGoogle Scholar
  72. Pedersen, K., & Gerdes, K. (1999). Multiple hok genes on the chromosome of Escherichia coli. Molecular Microbiology, 32, 1090–1102.PubMedCrossRefGoogle Scholar
  73. Pedersen, K., Zavialov, A. V., Pavlov, M. Y., Elf, J., Gerdes, K., & Ehrenberg, M. (2003). The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell, 112, 131–140.PubMedCrossRefGoogle Scholar
  74. Potrykus, K., & Cashel, M. (2008). (p)ppGpp still magical? Annual Review of Microbiology, 62, 35–51.PubMedCrossRefGoogle Scholar
  75. Prysak, M. H., Mozdzierz, C. J., Cook, A. M., Zhu, L., Zhang, Y., Inouye, M., et al. (2009). Bacterial toxin YafQ is an endoribonuclease that associates with the ribosome and blocks translation elongation through sequence-specific and frame-dependent mRNA cleavage. Molecular Microbiology, 71, 1071–1087.PubMedCrossRefGoogle Scholar
  76. Roberts, R. C., & Helinski, D. R. (1992). Definition of a minimal plasmid stabilization system from the broad-host-range plasmid Rk2. Journal of Bacteriology, 174, 8119–8132.PubMedGoogle Scholar
  77. Schmidt, O., Schuenemann, V. J., Hand, N. J., Silhavy, T. J., Martin, J., Lupas, A. N., et al. (2007). prIF and yhaV encode a new toxin–antitoxin system in Escherichia coli. Journal of Molecular Biology, 372, 894–905.PubMedCrossRefGoogle Scholar
  78. Sevin, E. W., & Barloy-Hubler, F. (2007). RASTA-Bacteria: A web-based tool for identifying toxin–antitoxin loci in prokaryotes. Genome Biology, 8, R155.PubMedCrossRefGoogle Scholar
  79. Shah, D., Zhang, Z. G., Khodursky, A., Kaldalu, N., Kurg, K., & Lewis, K. (2006). Persisters: A distinct physiological state of E-coli. Bmc Microbiology, 6, 53.PubMedCrossRefGoogle Scholar
  80. Shi, Y. L., Bao, L., Shang, Z. L., & Yao, S. X. (2008). RelE toxin protein of mycobacterium tuberculosis induces growth inhibition of lung cancer A-549 cell. Sichuan Da Xue Xue Bao Yi Xue Ban, 39, 368–372.PubMedGoogle Scholar
  81. Singletary, L. A., Gibson, J. L., Tanner, E. J., McKenzie, G. J., Lee, P. L., Gonzalez, C., et al. (2009). An SOS-regulated type 2 toxin–antitoxin system. Journal of Bacteriology, 191, 7456–7465.PubMedCrossRefGoogle Scholar
  82. Snyder, W. B., & Silhavy, T. J. (1992). Enhanced export of beta-galactosidase fusion proteins in prlF mutants is Lon dependent. Journal of Bacteriology, 174, 5661–5668.PubMedGoogle Scholar
  83. Sørensen, M. A. (2001). Charging levels of four tRNA species in Escherichia coli Rel(+) and Rel(-) strains during amino acid starvation: A simple model for the effect of ppGpp on translational accuracy. Journal of Molecular Biology, 307, 785–798.PubMedCrossRefGoogle Scholar
  84. Szekeres, S., Dauti, M., Wilde, C., Mazel, D., & Rowe-Magnus, D. A. (2007). Chromosomal toxin––antitoxin loci can diminish large-scale genome reductions in the absence of selection. Molecular Microbiology, 63, 1588–1605.PubMedCrossRefGoogle Scholar
  85. Takagi, H., Kakuta, Y., Okada, T., Yao, M., Tanaka, I., & Kimura, M. (2005). Crystal structure of archaeal toxin–antitoxin RelE-RelB complex with implications for toxin activity and antitoxin effects. Nature Structural and Molecular Biology, 12, 327–331.PubMedCrossRefGoogle Scholar
  86. Temperley, R., Richter, R., Dennerlein, S., Lightowlers, R. N., & Chrzanowska-Lightowlers, Z. M. (2010). Hungry codons promote frameshifting in human mitochondrial ribosomes. Science, 327, 301.PubMedCrossRefGoogle Scholar
  87. Tian, Q. B., Hayashi, T., Murata, T., & Terawaki, Y. (1996). Gene product identification and promoter analysis of hig locus of plasmid Rts1. Biochemical and Biophysical Research Communications, 225, 679–684.PubMedCrossRefGoogle Scholar
  88. Van Dyk, T. K., DeRose, E. J., & Gonye, G. E. (2001). LuxArray, a high-density, genomewide transcription analysis of Escherichia coli using bioluminescent reporter strains. Journal of Bacteriology, 183, 5496–5505.PubMedCrossRefGoogle Scholar
  89. Van Melderen, L. (2010). Toxin–antitoxin systems: Why so many, what for? Current Opinion in Microbiology, 13, 781–785.PubMedCrossRefGoogle Scholar
  90. Wagner, J., Gruz, P., Kim, S. R., Yamada, M., Matsui, K., Fuchs, R. P., et al. (1999). The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Molecular Cell, 4, 281–286.PubMedCrossRefGoogle Scholar
  91. Wang, X., Kim, Y., Hong, S. H., Ma, Q., Brown, B. L., Pu, M., et al. (2011). Antitoxin MqsA helps mediate the bacterial general stress response. Nature Chemical Biology, 7, 359–366.PubMedCrossRefGoogle Scholar
  92. Winther, K. S., & Gerdes, K. (2009). Ectopic production of VapCs from Enterobacteria inhibits translation and trans-activates YoeB mRNA interferase. Molecular Microbiology, 72, 918–930.PubMedCrossRefGoogle Scholar
  93. Winther, K. S., & Gerdes, K. (2012). Regulation of Enteric vapBC Transcription: Induction by VapC Toxin Dimer-Breaking. Nucleic Acids Research, 40, 4347–4357.PubMedCrossRefGoogle Scholar
  94. Wozniak, R. A., & Waldor, M. K. (2009). A toxin–antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genetics, 5, e1000439.PubMedCrossRefGoogle Scholar
  95. Yamamoto, T. A. M., Gerdes, K., & Tunnacliffe, A. (2002). Bacterial toxin RelE induces apoptosis in human cells. FEBS Letters, 519, 191–194.PubMedCrossRefGoogle Scholar
  96. Yang, M., Gao, C., Wang, Y., Zhang, H., & He, Z. G. (2010). Characterization of the interaction and cross-regulation of three mycobacterium tuberculosis RelBE modules. PLoS ONE, 5, e10672.PubMedCrossRefGoogle Scholar
  97. Yuan, J., Yamaichi, Y., & Waldor, M. K. (2011). The three vibrio cholerae chromosome II-encoded ParE toxins degrade chromosome I following loss of chromosome II. Journal of Bacteriology, 193, 611–619.PubMedCrossRefGoogle Scholar
  98. Zhang, Y., & Inouye, M. (2009). The inhibitory mechanism of protein synthesis by YoeB, an Escherichia coli toxin. Journal of Biological Chemistry, 284, 6627–6638.PubMedCrossRefGoogle Scholar
  99. Zhang, Y. L., Zhang, J. J., Hoeflich, K. P., Ikura, M., Qing, G. L., & Inouye, M. (2003). MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Molecular Cell, 12, 913–923.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Institute for Cell and Molecular Biosciences, Centre for Bacterial Cell BiologyNewcastle UniversityNewcastle upon TyneUK

Personalised recommendations