The ζ toxin induces a set of protective responses and dormancy

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Lioy, Virginia S ^a,d   Machon, Cristina ^a   Tabone, Mariangela ^a   Gonzalez Pastor, José E ^b   Daugelavicius, Rimantas ^c   Ayora, Silvia ^a   Alonso, Juan C ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b CENTRO DE ASTROBIOLOGÍA CSIC INTA   (Spain)

^c VYTAUTAS MAGNUS UNIVERSITY   (Lithuania)

^d INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTITOXIN; BACTERIAL TOXIN; EPSILON 2 ANTITOXIN; PROPIDIUM IODIDE; UNCLASSIFIED DRUG; ZETA TOXIN; BACTERIAL PROTEIN; GUANOSINE TRIPHOSPHATE; PYROPHOSPHATE; TOXIN;

ARTICLE; CELL DEATH; CELL SUBPOPULATION; CONTROLLED STUDY; DORMANCY; ENZYME ACTIVITY; ENZYME INHIBITION; NONHUMAN; PERMEABILITY; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; STRESS; BACILLUS SUBTILIS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRACELLULAR SPACE; METABOLISM;

BACILLUS SUBTILIS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL DEATH; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; DIPHOSPHATES; GENE EXPRESSION REGULATION, BACTERIAL; GUANOSINE TRIPHOSPHATE; INTRACELLULAR SPACE; PROPIDIUM; TOXINS, BIOLOGICAL;

EID: 84856259348     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030282     Document Type: Article

References (64)

1. Engelberg-Kulka H, Amitai S, Kolodkin-Gal I, Hazan R, (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2: e135.
2. Gerdes K, (2000) Toxin-antitoxin modules may regulate synthesis of macromolecules during nutritional stress. J Bacteriol 182: 561-572.
3. Van Melderen L, Saavedra De Bast M, (2009) Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genet 5: e1000437.
4. Hayes F, Van Melderen L, (2011) Toxins-antitoxins: diversity, evolution and function. Crit Rev Biochem Mol Biol 46: 386-408.
5. Yamaguchi Y, Inouye M, (2011) Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat Rev Microbiol 9: 779-790.
6. Gerdes K, Christensen SK, Lobner-Olesen A, (2005) Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3: 371-382.
7. Blower TR, Salmond GP, Luisi BF, (2011) Balancing at survival's edge: the structure and adaptive benefits of prokaryotic toxin-antitoxin partners. Curr Opin Struct Biol 21: 109-118.
8. Leplae R, Geeraerts D, Hallez R, Guglielmini J, Dreze P, et al. (2011) Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res 39: 5513-5525.
9. Hargreaves D, Santos-Sierra S, Giraldo R, Sabariegos-Jareno R, de la Cueva-Mendez G, et al. (2002) Structural and functional analysis of the kid toxin protein from E. coli plasmid R1. Structure (Camb) 10: 1425-1433.
10. Kamada K, Hanaoka F, Burley SK, (2003) Crystal structure of the MazE/MazF complex: molecular bases of antidote-toxin recognition. Mol Cell 11: 875-884.
11. Takagi H, Kakuta Y, Okada T, Yao M, Tanaka I, et al. (2005) Crystal structure of archaeal toxin-antitoxin RelE-RelB complex with implications for toxin activity and antitoxin effects. Nat Struct Mol Biol 12: 327-331.
12. Kamphuis MB, Monti MC, van den Heuvel RH, Lopez-Villarejo J, Diaz-Orejas R, et al. (2007) Structure and function of bacterial kid-kis and related toxin-antitoxin systems. Protein Pept Lett 14: 113-124.
13. Miallau L, Faller M, Chiang J, Arbing M, Guo F, et al. (2009) Structure and proposed activity of a member of the VapBC family of toxin-antitoxin systems. VapBC-5 from Mycobacterium tuberculosis. J Biol Chem 284: 276-283.
14. Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, et al. (2009) Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 323: 396-401.
15. Loris R, Dao-Thi MH, Bahassi EM, Van Melderen L, Poortmans F, et al. (1999) Crystal structure of CcdB, a topoisomerase poison from E. coli. J Mol Biol 285: 1667-1677.
16. De Jonge N, Garcia-Pino A, Buts L, Haesaerts S, Charlier D, et al. (2009) Rejuvenation of CcdB-poisoned gyrase by an intrinsically disordered protein domain. Mol Cell 35: 154-163.
17. Tan Q, Awano N, Inouye M, (2011) YeeV is an Escherichia coli toxin that inhibits cell division by targeting the cytoskeleton proteins, FtsZ and MreB. Mol Microbiol 79: 109-118.
18. Meinhart A, Alonso JC, Strater N, Saenger W, (2003) Crystal structure of the plasmid maintenance system εζ: functional mechanism of toxin ζ and inactivation by ε2ζ2 complex formation. Proc Natl Acad Sci U S A 100: 1661-1666.
19. Khoo SK, Loll B, Chan WT, Shoeman RL, Ngoo L, et al. (2007) Molecular and structural characterization of the PezAT chromosomal toxin-antitoxin system of the human pathogen Streptococcus pneumoniae. J Biol Chem 282: 19606-19618.
20. Mutschler H, Gebhardt M, Shoeman RL, Meinhart A, (2011) A novel mechanism of programmed cell death in bacteria by toxin-antitoxin systems corrupts peptidoglycan synthesis. PLoS Biol 9: e1001033.
21. Unoson C, Wagner EG, (2008) A small SOS-induced toxin is targeted against the inner membrane in Escherichia coli. Mol Microbiol 70: 258-270.
22. Amitai S, Yassin Y, Engelberg-Kulka H, (2004) MazF-mediated cell death in Escherichia coli: a point of no return. J Bacteriol 186: 8295-8300.
23. Kolodkin-Gal I, Hazan R, Gaathon A, Carmeli S, Engelberg-Kulka H, (2007) A linear pentapeptide is a quorum-sensing factor required for mazEF-mediated cell death in Escherichia coli. Science 318: 652-655.
24. Belitsky M, Avshalom H, Erental A, Yelin I, Kumar S, et al. (2011) The Escherichia coli extracellular death factor EDF induces the endoribonucleolytic activities of the toxins MazF and ChpBK. Mol Cell 41: 625-635.
25. Van Melderen L, (2010) Toxin-antitoxin systems: why so many, what for? Curr Opin Microbiol 13: 781-785.
26. Lewis K, (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5: 48-56.
27. Dörr T, Vulic M, Lewis K, (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8: e1000317.
28. Tsilibaris V, Maenhaut-Michel G, Mine N, Van Melderen L, (2007) What is the benefit to Escherichia coli of having multiple toxin-antitoxin systems in its genome? J Bacteriol 189: 6101-6108.
29. Maisonneuve E, Shakespeare LJ, Jorgensen MG, Gerdes K, (2011) Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci U S A.
30. Meinhart A, Alings C, Strater N, Camacho AG, Alonso JC, et al. (2001) Crystallization and preliminary X-ray diffraction studies of the εζ addiction system encoded by Streptococcus pyogenes plasmid pSM19035. Acta Crystallogr D Biol Crystallogr 57: 745-747.
31. Lioy VS, Martin MT, Camacho AG, Lurz R, Antelmann H, et al. (2006) pSM19035-encoded ζ toxin induces stasis followed by death in a subpopulation of cells. Microbiology 152: 2365-2379.
32. Zielenkiewicz U, Ceglowski P, (2005) The Toxin-Antitoxin System of the Streptococcal Plasmid pSM19035. J Bacteriol 187: 6094-6105.
33. Pellegrini O, Mathy N, Gogos A, Shapiro L, Condon C, (2005) The Bacillus subtilis ydcDE operon encodes an endoribonuclease of the MazF/PemK family and its inhibitor. Mol Microbiol 56: 1139-1148.
34. Moritz EM, Hergenrother PJ, (2007) Toxin-antitoxin systems are ubiquitous and plasmid-encoded in vancomycin-resistant enterococci. Proc Natl Acad Sci U S A 104: 311-316.
35. Rosvoll TC, Pedersen T, Sletvold H, Johnsen PJ, Sollid JE, et al. (2010) PCR-based plasmid typing in Enterococcus faecium strains reveals widely distributed pRE25-, pRUM-, pIP501- and pHTß-related replicons associated with glycopeptide resistance and stabilizing toxin-antitoxin systems. FEMS Immunol Med Microbiol 58: 254-268.
36. de la Hoz AB, Ayora S, Sitkiewicz I, Fernandez S, Pankiewicz R, et al. (2000) Plasmid copy-number control and better-than-random segregation genes of pSM19035 share a common regulator. Proc Natl Acad Sci U S A 97: 728-733.
37. Wendrich TM, Marahiel MA, (1997) Cloning and characterization of a relA/spoT homologue from Bacillus subtilis. Mol Microbiol 26: 65-79.
38. Britton RA, Eichenberger P, Gonzalez-Pastor JE, Fawcett P, Monson R, et al. (2002) Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis. J Bacteriol 184: 4881-4890.
39. Daugelavicius R, Gaidelyte A, Cvirkaite-Krupovic V, Bamford DH, (2007) On-line monitoring of changes in host cell physiology during the one-step growth cycle of Bacillus phage Bam35. J Microbiol Methods 69: 174-179.
40. Wang JD, Sanders GM, Grossman AD, (2007) Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128: 865-875.
41. Fu Z, Tamber S, Memmi G, Donegan NP, Cheung AL, (2009) Overexpression of MazFsa in Staphylococcus aureus induces bacteriostasis by selectively targeting mRNAs for cleavage. J Bacteriol 191: 2051-2059.
42. Nieto C, Sadowy E, de la Campa AG, Hryniewicz W, Espinosa M, (2010) The relBE2Spn toxin-antitoxin system of Streptococcus pneumoniae: role in antibiotic tolerance and functional conservation in clinical isolates. PLoS One 5: e11289.
43. Nariya H, Inouye M, (2008) MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell 132: 55-66.
44. Camacho AG, Misselwitz R, Behlke J, Ayora S, Welfle K, et al. (2002) In vitro and in vivo stability of the ε2ζ2 protein complex of the broad host-range Streptococcus pyogenes pSM19035 addiction system. Biol Chem 383: 1701-1713.
45. Dörr T, Lewis K, Vulic M, (2009) SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet 5: e1000760.
46. Kolodkin-Gal I, Sat B, Keshet A, Engelberg-Kulka H, (2008) The communication factor EDF and the toxin-antitoxin module mazEF determine the mode of action of antibiotics. PLoS Biol 6: e319.
47. Lee S, Kim MH, Kang BS, Kim JS, Kim GH, et al. (2008) Crystal structure of Escherichia coli MazG, the regulator of nutritional stress response. J Biol Chem 283: 15232-15240.
48. Gross M, Marianovsky I, Glaser G, (2006) MazG- a regulator of programmed cell death in Escherichia coli. Mol Microbiol 59: 590-601.
49. Nanamiya H, Kasai K, Nozawa A, Yun CS, Narisawa T, et al. (2008) Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol Microbiol 67: 291-304.
50. Lemos JA, Lin VK, Nascimento MM, Abranches J, Burne RA, (2007) Three gene products govern (p)ppGpp production by Streptococcus mutans. Mol Microbiol 65: 1568-1581.
51. Cashel M, Gentry DR, Hernandez VJ, Vinella D, (1996) The stringent response. In: Neidhardt FC, Curtiss R, Ingraham JL, Lin ECC, Low KB, editors. Escherichia coli and Salmonella typhimurium: cellular and molecular biology, 2nd ed Washington, DC American Society for Microbiology pp. 1458-1496.
52. Potrykus K, Cashel M, (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62: 35-51.
53. Ochi K, Kandala J, Freese E, (1982) Evidence that Bacillus subtilis sporulation induced by the stringent response is caused by the decrease in GTP or GDP. J Bacteriol 151: 1062-1065.
54. Srivatsan A, Wang JD, (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11: 100-105.
55. Samarrai W, Liu DX, White AM, Studamire B, Edelstein J, et al. (2011) Differential responses of Bacillus subtilis rRNA promoters to nutritional stress. J Bacteriol 193: 723-733.
56. Eymann C, Homuth G, Scharf C, Hecker M, (2002) Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J Bacteriol 184: 2500-2520.
57. Kostrewa D, D'Arcy A, Takacs B, Kamber M, (2001) Crystal structures of Streptococcus pneumoniae N-acetylglucosamine-1-phosphate uridyltransferase, GlmU, in apo form at 2.33 Å resolution and in complex with UDP-N-acetylglucosamine and Mg2+ at 1.96 Å resolution. J Mol Biol 305: 279-289.
58. Lopez JM, Dromerick A, Freese E, (1981) Response of guanosine 5′-triphosphate concentration to nutritional changes and its significance for Bacillus subtilis sporulation. J Bacteriol 146: 605-613.
59. Krasny L, Gourse RL, (2004) An alternative strategy for bacterial ribosome synthesis: Bacillus subtilis rRNA transcription regulation. EMBO J 23: 4473-4483.
60. Belitskii BR, Shakulov RS, (1980) [Guanosine polyphosphate concentration and stable RNA synthesis in Bacillus subtilis following suppression of protein synthesis]. Mol Biol (Mosk) 14: 1342-1353.
61. Nystrom T, (2003) Conditional senescence in bacteria: death of the immortals. Mol Microbiol 48: 17-23.
62. Stewart EJ, Madden R, Paul G, Taddei F, (2005) Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biol 3: e45.
63. Christensen SK, Mikkelsen M, Pedersen K, Gerdes K, (2001) RelE, a global inhibitor of translation, is activated during nutritional stress. Proc Natl Acad Sci U S A 98: 14328-14333.
64. Imlay JA, Chin SM, Linn S, (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240: 640-642.