A cis-acting antitoxin domain within the chromosomal toxin-antitoxin module EzeT of Escherichia coli quenches toxin activity

Molecular Microbiology

Volumn 97, Issue 3, 2015, Pages 589-604

  Rocker, Andrea ^a   Meinhart, Anton ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITOXIN; BACTERIAL TOXIN; CIS ACTING ELEMENT; PHOSPHOTRANSFERASE; PROTEIN EZET; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE; ESCHERICHIA COLI PROTEIN; EZET PROTEIN, E COLI;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CHROMOSOME; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; IN VIVO STUDY; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TOXICITY; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; BACTERIOLYSIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; POSIBACTERIA;

AMINO ACID SEQUENCE; BACTERIAL TOXINS; BACTERIOLYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84937953165     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13051     Document Type: Article

References (65)

1. Aakre, C.D., Phung, T.N., Huang, D., and Laub, M.T. (2013) A bacterial toxin inhibits DNA replication elongation through a direct interaction with the beta sliding clamp. Mol Cell 52: 617-628.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
4. Amitai, S., Yassin, Y., and Engelberg-Kulka, H. (2004) MazF-mediated cell death in Escherichia coli: a point of no return. J Bacteriol 186: 8295-8300.
5. Archer, C.T., Kim, J.F., Jeong, H., Park, J.H., Vickers, C.E., Lee, S.Y., and Nielsen, L.K. (2011) The genome sequence of E.coli W (ATCC 9637): comparative genome analysis and an improved genome-scale reconstruction of E.coli. BMC Genomics 12: 9.
6. Baker, D., Silen, J.L., and Agard, D.A. (1992) Protease pro region required for folding is a potent inhibitor of the mature enzyme. Proteins 12: 339-344.
7. Barton, G.J. (1993) ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng 6: 37-40.
8. Berthe, T., Ratajczak, M., Clermont, O., Denamur, E., and Petit, F. (2013) Evidence for coexistence of distinct Escherichia coli populations in various aquatic environments and their survival in estuary water. Appl Environ Microbiol 79: 4684-4693.
9. Blower, T.R., Short, F.L., Rao, F., Mizuguchi, K., Pei, X.Y., Fineran, P.C., etal. (2012) Identification and classification of bacterial type III toxin-antitoxin systems encoded in chromosomal and plasmid genomes. Nucleic Acids Res 40: 6158-6173.
10. Browning, D.F., Grainger, D.C., and Busby, S.J. (2010) Effects of nucleoid-associated proteins on bacterial chromosome structure and gene expression. Curr Opin Microbiol 13: 773-780.
11. Camacho, A.G., Misselwitz, R., Behlke, J., Ayora, S., Welfle, K., Meinhart, A., etal. (2002) In vitro and in vivo stability of the epsilon2zeta2 protein complex of the broad host-range Streptococcus pyogenes pSM19035 addiction system. Biol Chem 383: 1701-1713.
12. Ceglowski, P., Boitsov, A., Karamyan, N., Chai, S., and Alonso, J.C. (1993) Characterization of the effectors required for stable inheritance of Streptococcus pyogenes pSM19035-derived plasmids in Bacillus subtilis. Mol Gen Genet 241: 579-585.
13. Chan, W.T., Yeo, C.C., Sadowy, E., and Espinosa, M. (2014) Functional validation of putative toxin-antitoxin genes from the Gram-positive pathogen Streptococcus pneumoniae: phd-doc is the fourth bona-fide operon. Front Microbiol 5: 677.
14. Christensen-Dalsgaard, M., Jorgensen, M.G., and Gerdes, K. (2010) Three new RelE-homologous mRNA interferases of Escherichia coli differentially induced by environmental stresses. Mol Microbiol 75: 333-348.
15. Consalvi, V., Chiaraluce, R., Giangiacomo, L., Scandurra, R., Christova, P., Karshikoff, A., etal. (2000) Thermal unfolding and conformational stability of the recombinant domain II of glutamate dehydrogenase from the hyperthermophile Thermotoga maritima. Protein Eng 13: 501-507.
16. Correia, F.F., D'Onofrio, A., Rejtar, T., Li, L., Karger, B.L., Makarova, K., etal. (2006) Kinase activity of overexpressed HipA is required for growth arrest and multidrug tolerance in Escherichia coli. J Bacteriol 188: 8360-8367.
17. De la Cruz, M.A., Zhao, W., Farenc, C., Gimenez, G., Raoult, D., Cambillau, C., etal. (2013) A toxin-antitoxin module of Salmonella promotes virulence in mice. PLoS Pathog 9: e1003827.
18. Demidyuk, I.V., Shubin, A.V., Gasanov, E.V., and Kostrov, S.V. (2010) Propeptides as modulators of functional activity of proteases. BioMol Concepts 1: 305-322.
19. de Diego, I., Veillard, F.T., Guevara, T., Potempa, B., Sztukowska, M., Potempa, J., and Gomis-Ruth, F.X. (2013) Porphyromonas gingivalis virulence factor gingipain RgpB shows a unique zymogenic mechanism for cysteine peptidases. J Biol Chem 288: 14287-14296.
20. Donegan, N.P., and Cheung, A.L. (2009) Regulation of the mazEF toxin-antitoxin module in Staphylococcus aureus and its impact on sigB expression. J Bacteriol 191: 2795-2805.
21. Fozo, E.M. (2012) New type I toxin-antitoxin families from 'wild' and laboratory strains of E.coli: Ibs-Sib, ShoB-OhsC and Zor-Orz. RNA Biol 9: 1504-1512.
22. Garcia-Pino, A., Balasubramanian, S., Wyns, L., Gazit, E., De Greve, H., Magnuson, R.D., etal. (2010) Allostery and intrinsic disorder mediate transcription regulation by conditional cooperativity. Cell 142: 101-111.
23. Gerdes, K. (2013) Introduction. In Prokaryotic Toxin-Antitoxins. Gerdes, K. (ed.). Berlin Heidelberg: Springer, pp. 1-8.
24. Gerdes, K., and Maisonneuve, E. (2012) Bacterial persistence and toxin-antitoxin loci. Annu Rev Microbiol 66: 103-123.
25. Gerdes, K., Rasmussen, P.B., and Molin, S. (1986) Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc Natl Acad Sci USA 83: 3116-3120.
26. Gerdes, K., Christensen, S.K., and Lobner-Olesen, A. (2005) Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3: 371-382.
27. Goeders, N., and Van Melderen, L. (2014) Toxin-antitoxin systems as multilevel interaction systems. Toxins (Basel) 6: 304-324.
28. Gordon, D.M., and Cowling, A. (2003) The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149: 3575-3586.
29. Harvey, R.M., Stroeher, U.H., Ogunniyi, A.D., Smith-Vaughan, H.C., Leach, A.J., and Paton, J.C. (2011) A variable region within the genome of Streptococcus pneumoniae contributes to strain-strain variation in virulence. PLoS ONE 6: e19650.
30. Jones, D.T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195-202.
31. Kasari, V., Kurg, K., Margus, T., Tenson, T., and Kaldalu, N. (2010) The Escherichia coli mqsR and ygiT genes encode a new toxin-antitoxin pair. J Bacteriol 192: 2908-2919.
32. Kawano, M., Aravind, L., and Storz, G. (2007) An antisense RNA controls synthesis of an SOS-induced toxin evolved from an antitoxin. Mol Microbiol 64: 738-754.
33. Kessler, E., and Safrin, M. (1994) The propeptide of Pseudomonas aeruginosa elastase acts an elastase inhibitor. J Biol Chem 269: 22726-22731.
34. Khoo, S.K., Loll, B., Chan, W.T., Shoeman, R.L., Ngoo, L., Yeo, C.C., and Meinhart, A. (2007) Molecular and structural characterization of the PezAT chromosomal toxin-antitoxin system of the human pathogen Streptococcus pneumoniae. J Biol Chem 282: 19606-19618.
35. Leplae, R., Geeraerts, D., Hallez, R., Guglielmini, J., Dreze, P., and Van Melderen, L. (2011) Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res 39: 5513-5525.
36. Lioy, V.S., Martin, M.T., Camacho, A.G., Lurz, R., Antelmann, H., Hecker, M., etal. (2006) pSM19035-encoded zeta toxin induces stasis followed by death in a subpopulation of cells. Microbiology 152: 2365-2379.
37. Lioy, V.S., Machon, C., Tabone, M., Gonzalez-Pastor, J.E., Daugelavicius, R., Ayora, S., and Alonso, J.C. (2012) The zeta toxin induces a set of protective responses and dormancy. PLoS ONE 7: e30282.
38. Livingstone, C.D., and Barton, G.J. (1993) Protein sequence alignments: a strategy for the hierarchical analysis of residue conservation. Comput Appl Biosci 9: 745-756.
39. Makarova, K.S., Wolf, Y.I., and Koonin, E.V. (2009) Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol Direct 4: 19.
40. Martin, H.H. (1983) Protoplasts and spheroplasts of gram-negative bacteria (with special emphasis on Proteus mirabilis). In Protoplasts 1983. Potrykus, I., Harms, C.T., Hinnen, A., Hütter, R., King, P.J., and Shillito, R.D. (eds). Basel: Springer Basel AG, pp. 213-226.
41. Meinhart, A., Alonso, J.C., Strater, N., and Saenger, W. (2003) Crystal structure of the plasmid maintenance system epsilon/zeta: functional mechanism of toxin zeta and inactivation by epsilon 2 zeta 2 complex formation. Proc Natl Acad Sci USA 100: 1661-1666.
42. Meric, G., Kemsley, E.K., Falush, D., Saggers, E.J., and Lucchini, S. (2013) Phylogenetic distribution of traits associated with plant colonization in Escherichia coli. Environ Microbiol 15: 487-501.
43. Mutschler, H., Reinstein, J., and Meinhart, A. (2010) Assembly dynamics and stability of the pneumococcal epsilon zeta antitoxin toxin (PezAT) system from Streptococcus pneumoniae. J Biol Chem 85: 21797-21806.
44. Mutschler, H., and Meinhart, A. (2011) Epsilon/zeta systems: their role in resistance, virulence, and their potential for antibiotic development. J Mol Med (Berl) 12: 1183-1194.
45. Mutschler, H., Gebhardt, M., Shoeman, R.L., and Meinhart, A. (2011) A novel mechanism of programmed cell death in bacteria by toxin-antitoxin systems corrupts peptidoglycan synthesis. PLoS Biol 9: e1001033.
46. Park, J.H., Yamaguchi, Y., and Inouye, M. (2012) Intramolecular regulation of the sequence-specific mRNA interferase activity of MazF fused to a MazE fragment with a linker cleavable by specific proteases. Appl Environ Microbiol 78: 3794-3799.
47. Pedelacq, J.D., Cabantous, S., Tran, T., Terwilliger, T.C., and Waldo, G.S. (2006) Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol 24: 79-88.
48. Sberro, H., Leavitt, A., Kiro, R., Koh, E., Peleg, Y., Qimron, U., and Sorek, R. (2013) Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning. Mol Cell 50: 136-148.
49. Schuster, C.F., and Bertram, R. (2013) Toxin-antitoxin systems are ubiquitous and versatile modulators of prokaryotic cell fate. FEMS Microbiol Lett 340: 73-85.
50. Sevin, E.W., and Barloy-Hubler, F. (2007) RASTA-bacteria: a web-based tool for identifying toxin-antitoxin loci in prokaryotes. Genome Biol 8: R155.
51. Shapira, A., Shapira, S., Gal-Tanamy, M., Zemel, R., Tur-Kaspa, R., and Benhar, I. (2012) Removal of hepatitis C virus-infected cells by a zymogenized bacterial toxin. PLoS ONE 7: e32320.
52. Sievers, F., and Higgins, D.G. (2014) Clustal Omega, accurate alignment of very large numbers of sequences. Methods Mol Biol 1079: 105-116.
53. Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., etal. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539.
54. Szekeres, S., Dauti, M., Wilde, C., Mazel, D., and Rowe-Magnus, D.A. (2007) Chromosomal toxin-antitoxin loci can diminish large-scale genome reductions in the absence of selection. Mol Microbiol 63: 1588-1605.
55. Tabone, M., Ayora, S., and Alonso, J.C. (2014) Toxin zeta reversible induces dormancy and reduces the UDP-N-acetylglucosamine pool as one of the protective responses to cope with stress. Toxins (Basel) 6: 2787-2803.
56. Tamman, H., Ainelo, A., Ainsaar, K., and Horak, R. (2014) A moderate toxin, GraT, modulates growth rate and stress tolerance of Pseudomonas putida. J Bacteriol 196: 157-169.
57. Vogel, J., Argaman, L., Wagner, E.G., and Altuvia, S. (2004) The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 14: 2271-2276.
58. Walk, S.T., Alm, E.W., Calhoun, L.M., Mladonicky, J.M., and Whittam, T.S. (2007) Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environ Microbiol 9: 2274-2288.
59. Wang, X., Lord, D.M., Cheng, H.Y., Osbourne, D.O., Hong, S.H., Sanchez-Torres, V., etal. (2012) A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat Chem Biol 8: 855-861.
60. Wang, X., and Wood, T.K. (2011) Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl Environ Microbiol 77: 5577-5583.
61. Wozniak, R.A., and Waldor, M.K. (2009) A toxin-antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genet 5: e1000439.
62. Yamaguchi, Y., and Inouye, M. (2011) Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat Rev Microbiol 9: 779-790.
63. Yamaguchi, Y., Park, J.H., and Inouye, M. (2011) Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 45: 61-79.
64. Zielenkiewicz, U., and Ceglowski, P. (2001) Mechanisms of plasmid stable maintenance with special focus on plasmid addiction systems. Acta Biochim Pol 48: 1003-1023.
65. Zielenkiewicz, U., and Ceglowski, P. (2005) The toxin-antitoxin system of the streptococcal plasmid pSM19035. J Bacteriol 187: 6094-6105.