Recent advancements in toxin and antitoxin systems involved in bacterial programmed cell death

International Journal of Microbiology

Volumn , Issue , 2010, Pages

  Hu, Ming Xi ^a   Zhang, Xiao ^a   Li, Er Li ^a   Feng, Yong Jun ^a  

^a BEIJING INSTITUTE OF TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 80052486933     PISSN: 1687918X     EISSN: 16879198     Source Type: Journal    
DOI: 10.1155/2010/781430     Document Type: Article

References (112)

1. H. Engelberg-Kulka, S. Amitai, I. Kolodkin-Gal, and R. Hazan, "Bacterial programmed cell death and multicellular behavior in bacteria, " PLoS Genetics, vol. 2, no. 10, pp. 1518- 1526, 2006. (Pubitemid 44656527)
2. M. D. Jacobson, M.Weil, andM. C. Raff, "Programmed cell death in animal development, " Cell, vol. 88, no. 3, pp. 347- 354, 1997. (Pubitemid 27131376)
3. S. K. Christensen, G. Maenhaut-Michel, N. Mine, S. Gottesman, K. Gerdes, and L. Van Melderen, "Overproduction of the Lon protease triggers inhibition of translation in Escherichia coli: involvement of the yefM-yoeB toxinantitoxin system, " Molecular Microbiology, vol. 51, no. 6, pp. 1705-1717, 2004. (Pubitemid 38406543)
4. R. B. Jensen and K. Gerdes, "Programmed cell death in bacteria: proteic plasmid stabilization systems, " Molecular Microbiology, vol. 17, no. 2, pp. 205-210, 1995.
5. E.M. Fozo, M. R.Hemm, andG. Storz, "Small toxic proteins and the antisense RNAs that repress them, " Microbiology and Molecular Biology Reviews, vol. 72, no. 4, pp. 579-589, 2008.
6. K. S. Makarova, Y. I. Wolf, and E. V. Koonin, "Comprehensive comparative-genomic analysis of type 2 toxinantitoxin systems and related mobile stress response systems in prokaryotes, " Biology Direct, vol. 4, article 19, 2009.
7. P. C. Fineran, T. R. Blower, I. J. Foulds, D. P.Humphreys, K. S. Lilley, andG. P. C. Salmond, "The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair, " Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 3, pp. 894-899, 2009.
8. E. W. Sevin and F. Barloy-Hubler, "RASTA-Bacteria: a webbased tool for identifying toxin-antitoxin loci in prokaryotes, " Genome Biology, vol. 8, no. 8, article R155, 2007.
9. E. M. Fozo, K. S. Makarova, S. A. Shabalina, N. Yutin, E. V. Koonin, and G. Storz, "Abundance of type I toxinantitoxin systems in bacteria: searches for new candidates and discovery of novel families, " Nucleic Acids Research, vol. 38, no. 11, pp. 3743-3759, 2010.
10. Y. Masuda, K. Miyakawa, Y. Nishimura, and E. Ohtsubo, "chpA and chpB, Escherichia coli chromosomal homologs of the pem locus responsible for stable maintenance of plasmid R100, " Journal of Bacteriology, vol. 175, no. 21, pp. 6850- 6856, 1993. (Pubitemid 23322434)
11. T. Ogura and S. Hiraga, "Mini-F plasmid genes that couple host cell division to plasmid proliferation, " Proceedings of the National Academy of Sciences of the United States of America, vol. 80, no. 15, pp. 4784-4788, 1983.
12. R. Loris, M. H. Dao-Thi, E. M. Bahassi et al., "Crystal structure of CcdB, a topoisomerase poison from E. coli, " Journal of Molecular Biology, vol. 285, no. 4, pp. 1667-1677, 1999. (Pubitemid 29060463)
13. L. Van Melderen, M. H. D. Thi, P. Lecchi, S. Gottesman, M. Couturier, and M. R. Maurizi, "ATP-dependent degradation of CcdA by Lon protease. Effects of secondary structure and heterologous subunit interactions, " Journal of Biological Chemistry, vol. 271, no. 44, pp. 27730-27738, 1996. (Pubitemid 26367344)
14. T. Madl, L. Van Melderen, N. Mine et al., "Structural basis for nucleic acid and toxin recognition of the bacterial antitoxin CcdA, " Journal of Molecular Biology, vol. 364, no. 2, pp. 170- 185, 2006. (Pubitemid 44647253)
15. P. Bernard and M. Couturier, "Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes, " Journal of Molecular Biology, vol. 226, no. 3, pp. 735-745, 1992.
16. H. Grønlund and K. Gerdes, "Toxin-antitoxin systems homologous with relBE of Escherichia coli plasmid P307 are ubiquitous in prokaryotes, " Journal of Molecular Biology, vol. 285, no. 4, pp. 1401-1415, 1999. (Pubitemid 29060444)
17. A. J. Muñoz-Gómez, M. Lemonnier, S. Santos-Sierra, A. Berzal-Herranz, and R. Díaz-Orejas, "RNase/anti-RNase activities of the bacterial parD toxin-antitoxin system, " Journal of Bacteriology, vol. 187, no. 9, pp. 3151-3157, 2005. (Pubitemid 40571608)
18. S. Santos-Sierra, M. Lemonnier, B. Nuñez et al., "Noncytotoxic variants of the Kid protein that retain their autoregulatory activity, " Plasmid, vol. 50, no. 2, pp. 120-130, 2003. (Pubitemid 37025644)
19. D. Hargreaves, S. Santos-Sierra, R. Giraldo et al., "Structural and functional analysis of the kid toxin protein from E. coli plasmid R1, " Structure, vol. 10, no. 10, pp. 1425-1433, 2002. (Pubitemid 35238039)
20. S. Santos-Sierra, C. Pardo-Abarrio, R. Giraldo, and R. Díaz- Orejas, "Genetic identification of two functional regions in the antitoxin of the parD killer system of plasmid R1, " FEMS Microbiology Letters, vol. 206, no. 1, pp. 115-119, 2002. (Pubitemid 34084947)
21. F. Hayes, "Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest, " Science, vol. 301, no. 5639, pp. 1496-1499, 2003. (Pubitemid 37128533)
22. C. S. Hayes and R. T. Sauer, "Toxin-antitoxin pairs in bacteria: killers or stress regulators?" Cell, vol. 112, no. 1, pp. 2-4, 2003. (Pubitemid 36106411)
23. R. Hazan and H. Engelberg-Kulka, "Escherichia coli mazEFmediated cell death as a defense mechanism that inhibits the spread of phage P1, " Molecular Genetics and Genomics, vol. 272, no. 2, pp. 227-234, 2004. (Pubitemid 39371524)
24. R. Hazan, B. Sat, and H. Engelberg-Kulka, "Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions, " Journal of Bacteriology, vol. 186, no. 11, pp. 3663-3669, 2004. (Pubitemid 38661567)
25. Y. Zhang, L. Zhu, J. Zhang, and M. Inouye, "Characterization of ChpBK, an mRNA interferase from Escherichia coli, " Journal of Biological Chemistry, vol. 280, no. 28, pp. 26080- 26088, 2005. (Pubitemid 41022200)
26. M. Gotfredsen and K. Gerdes, "The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family, " Molecular Microbiology, vol. 29, no. 4, pp. 1065-1076, 1998. (Pubitemid 28389446)
27. G. Y. Li, Y. Zhang, M. Inouye, and M. Ikura, "Structural mechanism of transcriptional autorepression of the Escherichia coli RelB/RelE antitoxin/toxin module, " Journal of Molecular Biology, vol. 380, no. 1, pp. 107-119, 2008.
28. C. Nieto, T. Pellicer, D. Balsa, S. K. Christensen, K. Gerdes, and M. Espinosa, "The chromosomal relBE2 toxin-antitoxin locus of Streptococcus pneumoniae: characterization and use of a bioluminescence resonance energy transfer assay to detect toxin-antitoxin interaction, " Molecular Microbiology, vol. 59, no. 4, pp. 1280-1296, 2006.
29. S. E. S. Bailey and F. Hayes, "Influence of operator site geometry on transcriptional control by the yefM-yoeB toxinantitoxin complex, " Journal of Bacteriology, vol. 191, no. 3, pp. 762-772, 2009.
30. R. Motiejûnaitë, J. Armalytë, A. Markuckas, and E. Sužiedeliene, "Escherichia coli dinJ-yafQ genes act as a toxinantitoxin module, " FEMS Microbiology Letters, vol. 268, no. 1, pp. 112-119, 2007. (Pubitemid 46192843)
31. O. Schmidt, V. J. Schuenemann, N. J. Hand et al., "prlF and yhaV encode a new toxin-antitoxin system in Escherichia coli, " Journal of Molecular Biology, vol. 372, no. 4, pp. 894- 905, 2007. (Pubitemid 47368350)
32. S. B. Korch, H. Contreras, and J. E. Clark-Curtiss, "Three Mycobacterium tuberculosis rel toxin-antitoxin modules inhibit mycobacterial growth and are expressed in infected humanmacrophages, " Journal of Bacteriology, vol. 191, no. 5, pp. 1618-1630, 2009.
33. H. Nariya and M. Inouye, "MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development, " Cell, vol. 132, no. 1, pp. 55-66, 2008.
34. E. M. Moritz and P. J. Hergenrother, "Toxin-antitoxin systems are ubiquitous and plasmid-encoded in vancomycinresistant enterococci, " Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 1, pp. 311-316, 2006. (Pubitemid 46068028)
35. J. A. C. Lemos, T. A. Brown Jr., J. Abranches, and R. A. Burne, "Characteristics of Streptococcus mutans strains lacking the mazEF and RelBE toxin-antitoxin modules, " FEMS Microbiology Letters, vol. 253, no. 2, pp. 251-257, 2005. (Pubitemid 41674523)
36. L. Cheng, H. Lin, X. Fan et al., "A novel toxin-antitoxin operon talA/B from the Gram-positive bacterium Leifsonia xyli subsp. cynodontis, " FEBS Letters, vol. 582, no. 21-22, pp. 3211-3216, 2008.
37. J.-S. Han, J. J. Lee, T. Anandan et al., "Characterization of a chromosomal toxin-antitoxin, Rv1102c-Rv1103c system in Mycobacterium tuberculosis, " Biochemical and Biophysical Research Communications, vol. 400, no. 3, pp. 293-298, 2010.
38. S. Amitai, Y. Yassin, and H. Engelberg-Kulka, "MazFmediated cell death in Escherichia coli: a point of no return, " Journal of Bacteriology, vol. 186, no. 24, pp. 8295-8300, 2004. (Pubitemid 39603219)
39. Y. Zhang, J. Zhang, K. P. Hoeflich, M. Ikura, G. Qing, and M. Inouye, "MazF cleaves cellularmRNAs specifically at ACA to block protein synthesis in Escherichia coli, " Molecular Cell, vol. 12, no. 4, pp. 913-923, 2003. (Pubitemid 37352784)
40. Y. Zhang, J. Zhang, H.Hara, I. Kato, and M. Inouye, "Insights into the mRNA cleavage mechanism by MazF, an mRNA interferase, " Journal of Biological Chemistry, vol. 280, no. 5, pp. 3143-3150, 2004.
41. E. Aizenman, H. Engelberg-Kulka, and G. Glaser, "An Escherichia coli chromosomal "addiction module" regulated by 3', 5'-bispyrophosphate: a model for programmed bacterial cell death, " Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 12, pp. 6059-6063, 1996.
42. K. Kamada, F. Hanaoka, and S. K. Burley, "Crystal structure of the MazE/MazF complex: molecular bases of antidotetoxin recognition, " Molecular Cell, vol. 11, no. 4, pp. 875-884, 2003. (Pubitemid 36569246)
43. I. Marianovsky, E. Aizenman, H. Engelberg-Kulka, and G. Glaser, "The regulation of the Escherichia coli mazEF promoter involves an unusual alternating palindrome, " Journal of Biological Chemistry, vol. 276, no. 8, pp. 5975-5984, 2001.
44. B. Sat, R. Hazan, T. Fisher, H. Khaner, G. Glaser, and H. Engelberg-Kulka, "Programmed cell death in Escherichia coli: some antibiotics can trigger mazEF lethality, " Journal of Bacteriology, vol. 183, no. 6, pp. 2041-2045, 2001. (Pubitemid 32226000)
45. B. Sat, M. Reches, and H. Engelberg-Kulka, "The Escherichia coli chromosomal suicidal module mazEF is involved in thymine-less death, " Journal of Bacteriology, vol. 185, no. 6, pp. 1803-1807, 2003. (Pubitemid 36297879)
46. A. Jaffe, T. Ogura, and S. Hiraga, "Effects of the ccd function of the F plasmid on bacterial growth, " Journal of Bacteriology, vol. 163, no. 3, pp. 841-849, 1985. (Pubitemid 15230711)
47. M. H. Dao-Thi, D. Charlier, R. Loris et al., "Intricate interactions within the ccd plasmid addiction system, " Journal of Biological Chemistry, vol. 277, no. 5, pp. 3733-3742, 2002. (Pubitemid 34953248)
48. R. Motiejūnaitė, J. Armalytė, V. Šeputienė, and E. Sužiedėlienė, "Escherichia coli dinJ-yafQ operon shows characteristic features of bacterial toxin-antitoxin modules, " Biologija, vol. 4, pp. 9-14, 2005.
49. T. Franch and K. Gerdes, "Programmed cell death in bacteria: translational repression by mRNA end-pairing, " Molecular Microbiology, vol. 21, no. 5, pp. 1049-1060, 1996. (Pubitemid 26297770)
50. K. Wu and T. K. Wood, "Evaluation of the hok/sok killer locus for enhanced plasmid stability, " Biotechnology and Bioengineering, vol. 44, no. 8, pp. 912-921, 1994. (Pubitemid 24308539)
51. B. Pimentel, M. A. Madine, and G. De La Cueva-Méndez, "Kid cleaves specific mRNAs at UUACU sites to rescue the copy number of plasmid R1, " EMBO Journal, vol. 24, no. 19, pp. 3459-3469, 2005. (Pubitemid 41486783)
52. A. Bravo, G. de Torrontegui, and R. Díaz, "Identification of components of a new stability system of plasmid R1, parD, that is close to the origin of replication of this plasmid, "MGG Molecular & General Genetics, vol. 210, no. 1, pp. 101-110, 1987.
53. J. Zhang, Y. Zhang, L. Zhu, M. Suzuki, and M. Inouye, "Interference ofmRNA function by sequence-specific endoribonuclease PemK, " Journal of Biological Chemistry, vol. 279, no. 20, pp. 20678-20684, 2004. (Pubitemid 38656463)
54. C. Nieto, I. Cherny, K. K. Seok et al., "The yefM-yoeB toxin-antitoxin systems of Escherichia coli and Streptococcus pneumoniae: functional and structural correlation, " Journal of Bacteriology, vol. 189, no. 4, pp. 1266-1278, 2007. (Pubitemid 46239748)
55. M. Christensen-Dalsgaard and K. Gerdes, "Two higBA loci in the Vibrio cholerae superintegron encode mRNA cleaving enzymes and can stabilize plasmids, " MolecularMicrobiology, vol. 62, no. 2, pp. 397-411, 2006. (Pubitemid 44477230)
56. J. M. Hurley and N. A. Woychik, "Bacterial toxin HigB associates with ribosomes and mediates translation-dependent mRNA cleavage at A-rich sites, " Journal of Biological Chemistry, vol. 284, no. 28, pp. 18605-18613, 2009.
57. M. Liu, Y. Zhang, M. Inouye, and N. A. Woychik, "Bacterial addiction module toxin Doc inhibits translation elongation through its association with the 30S ribosomal subunit, " Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 15, pp. 5885-5890, 2008. (Pubitemid 351758467)
58. R. Grady and F. Hayes, "Axe-Txe, a broad-spectrum proteic toxin-antitoxin system specified by a multidrug-resistant, clinical isolate of Enterococcus faecium, " Molecular Microbiology, vol. 47, no. 5, pp. 1419-1432, 2003. (Pubitemid 36307861)
59. H. Sletvold, P. J. Johnsen, I. Hamre, G. S. Simonsen, A. Sundsfjord, and K. M. Nielsen, "Complete sequence of Enterococcus faecium pVEF3 and the detection of an ω-ε-ζ toxin-antitoxin module and an ABC transporter, " Plasmid, vol. 60, no. 1, pp. 75-85, 2008.
60. U. Zielenkiewicz, M. Kowalewska, C. Kaczor, and P. Cegłowski, "In vivo interactions between toxin-antitoxin proteins epsilon and zeta of streptococcal plasmid pSM19035 in Saccharomyces cerevisiae, " Journal of Bacteriology, vol. 191, no. 11, pp. 3677-3684, 2009.
61. S. Shokeen, S. Patel, T. J. Greenfield, C. Brinkman, and K. E. Weaver, "Translational regulation by an intramolecular stemloop is required for intermolecular RNA regulation of the par addiction module, " Journal of Bacteriology, vol. 190, no. 18, pp. 6076-6083, 2008.
62. S. Patel and K. E. Weaver, "Addiction toxin Fst has unique effects on chromosome segregation and cell division in Enterococcus faecalis and Bacillus subtilis, " Journal of Bacteriology, vol. 188, no. 15, pp. 5374-5384, 2006. (Pubitemid 44157293)
63. S. Sayeed, L. Reaves, L. Radnedge, and S. Austin, "The stability region of the large virulence plasmid of Shigella flexneri encodes an efficient postsegregational killing system, " Journal of Bacteriology, vol. 182, no. 9, pp. 2416-2421, 2000. (Pubitemid 30212897)
64. M. Wilbaux, N. Mine, A. M. Guérout, D. Mazel, and L. Van Melderen, "Functional interactions between coexisting toxin-antitoxin systems of the ccd family in Escherichia coli O157:H7, " Journal of Bacteriology, vol. 189, no. 7, pp. 2712- 2719, 2007. (Pubitemid 46556053)
65. M. H. Prysak, C. J. Mozdzierz, A. M. Cook et al., "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, vol. 71, no. 5, pp. 1071-1087, 2009.
66. F. F. Correia, A. D'Onofrio, T. Rejtar et al., "Kinase activity of overexpressed HipA is required for growth arrest and multidrug tolerance in Escherichia coli, " Journal of Bacteriology, vol. 188, no. 24, pp. 8360-8367, 2006. (Pubitemid 44894035)
67. S. K. Christensen, M. Mikkelsen, K. Pedersen, and K. Gerdes, "RelE, a global inhibitor of translation, is activated during nutritional stress, " Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 25, pp. 14328-14333, 2001. (Pubitemid 33121391)
68. C. Unoson and E. G. H. Wagner, "A small SOS-induced toxin is targeted against the inner membrane in Escherichia coli, " Molecular Microbiology, vol. 70, no. 1, pp. 258-270, 2008.
69. Y. Kim, X.Wang, X. S. Zhang et al., "Escherichia coli toxin/antitoxin pair MqsR/MqsA regulate toxin CspD, " Environmental Microbiology, vol. 12, no. 5, pp. 1105-1121, 2010.
70. M. G. Jørgensen, D. P. Pandey, M. Jaskolska, and K. Gerdes, "HicA of Escherichia coli defines a novel family of translationindependent mRNA interferases in bacteria and archaea, " Journal of Bacteriology, vol. 191, no. 4, pp. 1191-1199, 2009.
71. Y. Zhang, Y. Yamaguchi, and M. Inouye, "Characterization of YafO, an Escherichia coli toxin, " Journal of Biological Chemistry, vol. 284, no. 38, pp. 25522-25531, 2009.
72. K. K. Seok, B. Loll, T. C.Wai et al., "Molecular and structural characterization of the PezAT chromosomal toxin-antitoxin system of the human pathogen Streptococcus pneumoniae, " Journal of Biological Chemistry, vol. 282, no. 27, pp. 19606- 19618, 2007. (Pubitemid 47100079)
73. O. Pellegrini, N. Mathy, A. Gogos, L. Shapiro, and C. Condon, "The Bacillus subtilis ydcDE operon encodes an endoribonuclease of the MazF/PemK family and its inhibitor, " Molecular Microbiology, vol. 56, no. 5, pp. 1139-1148, 2005. (Pubitemid 40755999)
74. S. Agarwal, S. Agarwal, and R. Bhatnagar, "Identification and characterization of a novel toxin-antitoxin module from Bacillus anthracis, " FEBS Letters, vol. 581, no. 9, pp. 1727- 1734, 2007. (Pubitemid 46602263)
75. D. P. Pandey and K. Gerdes, "Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes, " Nucleic Acids Research, vol. 33, no. 3, pp. 966- 976, 2005. (Pubitemid 41430517)
76. L. Zhao and J. Zhang, "Biochemical characterization of a chromosomal toxin-antitoxin system in Mycobacterium tuberculosis, " FEBS Letters, vol. 582, no. 5, pp. 710-714, 2008.
77. J. Robson, J. L. McKenzie, R. Cursons, G. M. Cook, and V. L. Arcus, "The vapBC operon from Mycobacterium smegmatis is an autoregulated toxin-antitoxin module that controls growth via inhibition of translation, " Journal of Molecular Biology, vol. 390, no. 3, pp. 353-367, 2009.
78. L. Miallau, M. Faller, C. Janet et al., "Structure and proposed activity of a member of the VapBC family of toxin-antitoxin systems VapBC-5 from Mycobacterium tuberculosis, " Journal of Biological Chemistry, vol. 284, no. 1, pp. 276-283, 2009.
79. P. P. Budde, B. M. Davis, J. Yuan, and M. K. Waldor, " Characterization of a higBA toxin-antitoxin locus in Vibrio cholerae, " Journal of Bacteriology, vol. 189, no. 2, pp. 491-500, 2007. (Pubitemid 46106381)
80. R. A. F.Wozniak and M. K.Waldor, "A toxin-antitoxin system promotes the maintenance of an integrative conjugative element, " PLoS Genetics, vol. 5, no. 3, Article ID e1000439, 2009.
81. M. Cashel and K. E. Rudd, "The stringent response, " in Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, pp. 1410-1438, American Society for Microbiology, Washington, DC, USA, 1987.
82. I. Kolodkin-Gal, R. Hazan, A. Gaathon, S. Carmeli, and H. Engelberg-Kulka, "A linear pentapeptide is a quorum-sensing factor required for mazEF-mediated cell death in Escherichia coli, " Science, vol. 318, no. 5850, pp. 652-655, 2007. (Pubitemid 350014840)
83. I. Kolodkin-Gal and H. Engelberg-Kulka, "The extracellular death factor: physiological and genetic factors influencing its production and response in Escherichia coli, " Journal of Bacteriology, vol. 190, no. 9, pp. 3169-3175, 2008. (Pubitemid 351581412)
84. H. Engelberg-Kulka, I. Yelin, and I. Kolodkin-Gal, "Activation of a built-in bacterial programmed cell death system as a novel mechanism of action of some antibiotics, " Communitative and Integrative Biology, vol. 2, no. 3, pp. 211- 212, 2009.
85. I. Kolodkin-Gal, B. Sat, A. Keshet, and H. Engelberg-Kulka, "The communication factor EDF and the toxin-antitoxin module mazEF determine the mode of action of antibiotics, " PLoS Biology, vol. 6, no. 12, pp. 2774-2785, 2008.
86. S. Amitai, I. Kolodkin-Gal, M. Hananya-Meltabashi, A. Sacher, and H. E. Kulka, "Escherichia coli MazF leads to the simultaneous selective synthesis of both "death proteins" and "survival proteins PLoS Genetics, vol. 5, no. 3, Article ID e1000390, 2009.
87. W. C. Cheng and J. M. Hardwick, "A quorum on bacterial programmed cell death, " Molecular Cell, vol. 28, no. 4, pp. 515-517, 2007. (Pubitemid 350137802)
88. A. King and E. Gottlieb, "Glucose metabolism and programmed cell death: an evolutionary and mechanistic perspective, " Current Opinion in Cell Biology, vol. 21, no. 6, pp. 885-893, 2009.
89. M. E. Davey and G. A. O'Toole, "Microbial biofilms: from ecology to molecular genetics, " Microbiology and Molecular Biology Reviews, vol. 64, no. 4, pp. 847-867, 2000. (Pubitemid 32475933)
90. C. Sternberg, B. B. Christensen, T. Johansen et al., "Distribution of bacterial growth activity in flow-chamber biofilms, " Applied and Environmental Microbiology, vol. 65, no. 9, pp. 4108-4117, 1999.
91. S. A. Rani, B. Pitts, H. Beyenal et al., "Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states, " Journal of Bacteriology, vol. 189, no. 11, pp. 4223-4233, 2007. (Pubitemid 46847371)
92. K. C. Rice, E. E. Mann, J. L. Endres et al., "The cidAmurein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus, " Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 19, pp. 8113-8118, 2007. (Pubitemid 47185884)
93. J. S. Webb, L. S. Thompson, S. James et al., "Cell death in Pseudomonas aeruginosa biofilm development, " Journal of Bacteriology, vol. 185, no. 15, pp. 4585-4592, 2003. (Pubitemid 36890507)
94. S. A. West, S. P. Diggle, A. Buckling, A. Gardner, and A. S. Griffin, "The social lives of microbes, " Annual Review of Ecology, Evolution, and Systematics, vol. 38, pp. 53-77, 2007.
95. Y. Kim, X. Wang, Q. Ma, X. S. Zhang, and T. K. Wood, "Toxin- antitoxin systems in Escherichia coli influence biofilm formation through YjgK (TabA) and fimbriae, " Journal of Bacteriology, vol. 191, no. 4, pp. 1258-1267, 2009.
96. A. Mai-Prochnow, F. Evans, D. Dalisay-Saludes et al., "Biofilm development and cell death in themarine bacterium Pseudoalteromonas tunicata, " Applied and Environmental Microbiology, vol. 70, no. 6, pp. 3232-3238, 2004. (Pubitemid 38745863)
97. V. Tsilibaris, G. Maenhaut-Michel, N. Mine, and L. Van Melderen, "What is the benefit to Escherichia coli of having multiple toxin-antitoxin systems in its genome?" Journal of Bacteriology, vol. 189, no. 17, pp. 6101-6108, 2007. (Pubitemid 47378616)
98. I. Kolodkin-Gal, R. Verdinger, A. Shlosberg-Fedida, and H. Engelberg-Kulka, "A differential effect of E. coli toxinantitoxin systems on cell death in liquid media and biofilm formation, " PLoS One, vol. 4, no. 8, Article ID e6785, 2009.
99. Y. Kim and T. K. Wood, "Toxins Hha and CspD and small RNA regulator Hfq are involved in persister cell formation through MqsR in Escherichia coli, " Biochemical and Biophysical Research Communications, vol. 391, no. 1, pp. 209-213, 2010.
100. I. Kolodkin-Gal and H. Engelberg-Kulka, "The stationaryphase sigma factor σ is responsible for the resistance of Escherichia coli stationary-phase cells to mazEF-mediated cell death, " Journal of Bacteriology, vol. 191, no. 9, pp. 3177-3182, 2009.
101. H. Engelberg-Kulka, B. Sat, M. Reches, S. Amitai, and R. Hazan, "Bacterial programmed cell death systems as targets for antibiotics, " Trends in Microbiology, vol. 12, no. 2, pp. 66- 71, 2004. (Pubitemid 38167340)
102. K. Pedersen, S. K. Christensen, and K. Gerdes, "Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins, " Molecular Microbiology, vol. 45, no. 2, pp. 501-510, 2002. (Pubitemid 34779839)
103. M. Christensen-Dalsgaard, M. G. Jørgensen, and K. Gerdes, "Three new RelE-homologous mRNA interferases of Escherichia coli differentially induced by environmental stresses, " Molecular Microbiology, vol. 75, no. 2, pp. 333-348, 2010.
104. I. Kolodkin-Gal and H. Engelberg-Kulka, "Induction of Escherichia coli chromosomal mazEF by stressful conditions causes an irreversible loss of viability, " Journal of Bacteriology, vol. 188, no. 9, pp. 3420-3423, 2006.
105. E. Diago-Navarro, A. M. Hernandez-Arriaga, J. López- Villarejo et al., "parD toxin-antitoxin system of plasmid R1-basic contributions, biotechnological applications and relationships with closely-related toxin-antitoxin systems, " FEBS Journal, vol. 277, no. 15, pp. 3097-3117, 2010.
106. R. Díaz-Orejas, E. Diago-Navarro, A. M. H. Arriaga et al., "Bacterial toxin-antitoxin systems targeting translation, " Journal of Applied Biomedicine, vol. 8, no. 4, pp. 179-188, 2010.
107. A. A. Prozorov and V. N. Danilenko, "Toxin-antitoxin systems in bacteria: apoptotic tools or metabolic regulators?" Microbiology, vol. 79, no. 2, pp. 129-140, 2010.
108. R. Jayaraman, "Bacterial persistence: some new insights into an old phenomenon, " Journal of Biosciences, vol. 33, no. 5, pp. 795-805, 2008.
109. R. D. Magnuson, "Hypothetical functions of toxin-antitoxin systems, " Journal of Bacteriology, vol. 189, no. 17, pp. 6089- 6092, 2007. (Pubitemid 47378614)
110. L. Van Melderen and M. S. De Bast, "Bacterial toxin-antitoxin systems: more than selfish entities?" PLoS Genetics, vol. 5, no. 3, pp. 1-6, 2009.
111. K. C. Rice and K. W. Bayles, "Molecular control of bacterial death and lysis, "Microbiology and Molecular Biology Reviews, vol. 72, no. 1, pp. 85-109, 2008. (Pubitemid 351398056)
112. S. Kornbluth and K. White, "Apoptosis in Drosophila: neither fish nor fowl (nor man, nor worm), " Journal of Cell Science, vol. 118, no. 9, pp. 1779-1787, 2005. (Pubitemid 40723823)