Multiple toxin-antitoxin systems in Mycobacterium tuberculosis

Toxins

Volumn 6, Issue 3, 2014, Pages 1002-1020

  Sala, Ambre ^a   Bordes, Patricia ^a   Genevaux, Pierre ^a  

^a UMR   (France)

Author keywords

Molecular chaperones; Persistence; Proteases; Toxin antitoxins

Indexed keywords

ANTITOXIN; MAZF4 TOXIN; PROTEINASE; TOXIN; UNCLASSIFIED DRUG; VAP B TOXIN; VAP C TOXIN;

BACTERIAL GENOME; BACTERIAL GROWTH; CHROMOSOME MAP; GENE; GENE EXPRESSION; GENE MUTATION; GROWTH INHIBITION; MYCOBACTERIUM TUBERCULOSIS; OPERON; PATHOGENESIS; PROTEUS VULGARIS; RELB GENE; RELE1 GENE; RELE2 GENE; REVIEW; VIBRIO CHOLERAE; YOEB GENE;

ANTITOXINS; BACTERIAL PROTEINS; BACTERIAL TOXINS; DNA-BINDING PROTEINS; MYCOBACTERIUM TUBERCULOSIS; PEPTIDE HYDROLASES;

EID: 84897904160     PISSN: 20726651     EISSN: None     Source Type: Journal    
DOI: 10.3390/toxins6031002     Document Type: Review

References (98)

1. Yamaguchi, Y.; Park, J.H.; Inouye, M. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 2011, 45, 61-79.
2. Pandey, D.P.; Gerdes, K. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acid Res. 2005, 33, 966-976.
3. Gerdes, K.; Maisonneuve, E. Bacterial persistence and toxin-antitoxin loci. Annu. Rev. Microbiol. 2012, 66, 103-123.
4. Masuda, H.; Tan, Q.; Awano, N.; Wu, K.P.; Inouye, M. Yeeu enhances the bundling of cytoskeletal polymers of Mreb and Ftsz, antagonizing the Cbta (Yeev) toxicity in Escherichia coli. Mol. Microbiol. 2012, 84, 979-989.
5. Wang, X.; Lord, D.M.; Cheng, H.Y.; Osbourne, D.O.; Hong, S.H.; Sanchez-Torres, V.; Quiroga, C.; Zheng, K.; Herrmann, T.; Peti, W.; et al. A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat. Chem. Biol. 2012, 8, 855-861.
6. Van Melderen, L. Toxin-antitoxin systems: Why so many, what for? Curr. Opin. Microbiol. 2010, 13, 781-785.
7. Lewis, K. Persister cells. Ann. Rev. Microbiol. 2010, 64, 357-372.
8. Maisonneuve, E.; Castro-Camargo, M.; Gerdes, K. (p)ppgpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 2013, 154, 1140-1150.
9. Barry, C.E., 3rd.; Boshoff, H.I.; Dartois, V.; Dick, T.; Ehrt, S.; Flynn, J.; Schnappinger, D.; Wilkinson, R.J.; Young, D. The spectrum of latent tuberculosis: Rethinking the biology and intervention strategies. Nat. Rev. Microbiol. 2009, 7, 845-855.
10. Georgiades, K.; Raoult, D. Genomes of the most dangerous epidemic bacteria have a virulence repertoire characterized by fewer genes but more toxin-antitoxin modules. PLoS ONE 2011, 6, e17962.
11. Sala, A.; Bordes, P.; Fichant, G.; Genevaux, P. Toxin-antitoxin loci in Mycobacterium tuberculosis. In Prokaryotic Toxin-Antitoxin; Gerdes, K., Ed.; Springer: Berlin, Heidelberg, Germany, 2013; pp. 295-314.
12. Keren, I.; Minami, S.; Rubin, E.; Lewis, K. Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. mBio 2011, 2, e00100-e00111.
13. Fozo, E.M.; Makarova, K.S.; Shabalina, S.A.; Yutin, N.; Koonin, E.V.; Storz, G. Abundance of type I toxin-antitoxin systems in bacteria: Searches for new candidates and discovery of novel families. Nucleic Acid Res. 2010, 38, 3743-3759.
14. Blower, T.R.; Short, F.L.; Rao, F.; Mizuguchi, K.; Pei, X.Y.; Fineran, P.C.; Luisi, B.F.; Salmond, G.P. Identification and classification of bacterial type III toxin-antitoxin systems encoded in chromosomal and plasmid genomes. Nucleic Acids Res. 2012, 40, 6158-6173.
15. Gupta, A. Killing activity and rescue function of genome-wide toxin-antitoxin loci of Mycobacterium tuberculosis. FEMS Microbiol. Lett. 2009, 290, 45-53.
16. Ramage, H.R.; Connolly, L.E.; Cox, J.S. Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: Implications for pathogenesis, stress responses, and evolution. PLoS Genet. 2009, 5, e1000767.
17. Huang, F.; He, Z.G. Characterization of an interplay between a Mycobacterium tuberculosis MazF homolog, Rv1495 and its sole DNA topoisomerase I. Nucleic Acids Res. 2010, 38, 8219-8230.
18. Singh, R.; Barry, C.E., 3rd.; Boshoff, H.I. The three RelE homologs of Mycobacterium tuberculosis have individual, drug-specific effects on bacterial antibiotic tolerance. J. Bacteriol. 2010, 192, 1279-1291.
19. Zhu, L.; Sharp, J.D.; Kobayashi, H.; Woychik, N.A.; Inouye, M. Noncognate Mycobacterium tuberculosis toxin-antitoxins can physically and functionally interact. J. Biol. Chem. 2010, 285, 39732-39738.
20. Ahidjo, B.A.; Kuhnert, D.; McKenzie, J.L.; Machowski, E.E.; Gordhan, B.G.; Arcus, V.; Abrahams, G.L.; Mizrahi, V. VapC toxins from Mycobacterium tuberculosis are ribonucleases that differentially inhibit growth and are neutralized by cognate VapB antitoxins. PLoS ONE 2011, 6, e21738.
21. Pullinger, G.D.; Lax, A.J. A Salmonella dublin virulence plasmid locus that affects bacterial growth under nutrient-limited conditions. Mol. Microbiol. 1992, 6, 1631-1643.
22. Arcus, V.L.; McKenzie, J.L.; Robson, J.; Cook, G.M. The PIN-domain ribonucleases and the prokaryotic VapBC toxin-antitoxin array. Protein Eng. Des. Sel. 2011, 24, 33-40.
23. Miallau, L.; Faller, M.; Chiang, J.; Arbing, M.; Guo, F.; Cascio, D.; Eisenberg, D. Structure and proposed activity of a member of the VapBC family of toxin-antitoxin systems. VapBC-5 from Mycobacterium tuberculosis. J. Biol. Chem. 2009, 284, 276-283.
24. Winther, K.S.; Gerdes, K. Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA. Proc. Natl. Acad. Sci. USA 2011, 108, 7403-7407.
25. Sharp, J.D.; Cruz, J.W.; Raman, S.; Inouye, M.; Husson, R.N.; Woychik, N.A. Growth and translation inhibition through sequence specific RNA binding by a Mycobacterium tuberculosis VapC toxin. J. Biol. Chem. 2012, doi:10.1074/jbc.M112.340109.
26. McKenzie, J.L.; Duyvestyn, J.M.; Smith, T.; Bendak, K.; Mackay, J.; Cursons, R.; Cook, G.M.; Arcus, V.L. Determination of ribonuclease sequence-specificity using pentaprobes and mass spectrometry. RNA 2012, 18, 1267-1278.
27. Winther, K.S.; Brodersen, D.E.; Brown, A.K.; Gerdes, K. VapC20 of Mycobacterium tuberculosis cleaves the sarcin-ricin loop of 23S rRNA. Nat. Commun. 2013, 4, 2796.
28. Min, A.B.; Miallau, L.; Sawaya, M.R.; Habel, J.; Cascio, D.; Eisenberg, D. The crystal structure of the Rv0301-Rv0300 VapBC-3 toxin-antitoxin complex from M. tuberculosis reveals a Mg2+ ion in the active site and a putative RNA-binding site. Protein Sci. 2012, 21, 1754-1767.
29. Makarova, K.S.; Wolf, Y.I.; Koonin, E.V. Comprehensive comparative-genomic analysis of type-2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct. 2009, 4, 19.
30. McKenzie, J.L.; Robson, J.; Berney, M.; Smith, T.C.; Ruthe, A.; Gardner, P.P.; Arcus, V.L.; Cook, G.M. A VapBC toxin-antitoxin module is a post-transcriptional regulator of metabolic flux in Mycobacteria. J. Bacteriol. 2012, doi:10.1128/JB.06790-11.
31. Albrethsen, J.; Agner, J.; Piersma, S.R.; Hojrup, P.; Pham, T.V.; Weldingh, K.; Jimenez, C.R.; Andersen, P.; Rosenkrands, I. Proteomic profiling of Mycobacterium tuberculosis identifies nutrient-starvation-responsive toxin-antitoxin systems. Mol. Cell. Proteomics 2013, 12, 1180-1191.
32. Yamaguchi, Y.; Inouye, M. Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat. Rev. Microbiol. 2011, 9, 779-790.
33. Kamada, K.; Hanaoka, F.; Burley, S.K. Crystal structure of the MazE/MazF complex: Molecular bases of antidote-toxin recognition. Mol. Cell. 2003, 11, 875-884.
34. Simanshu, D.K.; Yamaguchi, Y.; Park, J.H.; Inouye, M.; Patel, D.J. Structural basis of mRNA recognition and cleavage by toxin MazF and its regulation by antitoxin MazE in Bacillus subtilis. Mol. Cell. 2013, 52, 447-458.
35. Zhang, Y.; Zhu, L.; Zhang, J.; Inouye, M. Characterization of ChpbK, an mRNA interferase from Escherichia coli. J. Biol. Chem. 2005, 280, 26080-26088.
36. Park, J.H.; Yamaguchi, Y.; Inouye, M. Bacillus subtilis MazF-bs (EndoA) is a UACAU-specific mRNA interferase. FEBS Lett. 2011, 585, 2526-2532.
37. Zhu, L.; Zhang, Y.; Teh, J.S.; Zhang, J.; Connell, N.; Rubin, H.; Inouye, M. Characterization of mRNA interferases from Mycobacterium tuberculosis. J. Biol. Chem. 2006, 281, 18638-18643.
38. Schifano, J.M.; Edifor, R.; Sharp, J.D.; Ouyang, M.; Konkimalla, A.; Husson, R.N.; Woychik, N.A. Mycobacterial toxin MazF-mt6 inhibits translation through cleavage of 23S rRNA at the ribosomal A site. Proc. Natl. Acad. Sci. USA 2013, 110, 8501-8506.
39. Zhu, L.; Phadtare, S.; Nariya, H.; Ouyang, M.; Husson, R.N.; Inouye, M. The mRNA interferases, MazF-mt3 and MazF-mt7 from Mycobacterium tuberculosis target unique pentad sequences in single-stranded RNA. Mol. Microbiol. 2008, 69, 559-569.
40. Vesper, O.; Amitai, S.; Belitsky, M.; Byrgazov, K.; Kaberdina, A.C.; Engelberg-Kulka, H.; Moll, I. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 2011, 147, 147-157.
41. Sassetti, C.M.; Boyd, D.H.; Rubin, E.J. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 2003, 48, 77-84.
42. Hazan, R.; Sat, B.; Engelberg-Kulka, H. Escherichia coli MazEF-mediated cell death is triggered by various stressful conditions. J. Bacteriol. 2004, 186, 3663-3669.
43. Betts, J.C.; Lukey, P.T.; Robb, L.C.; McAdam, R.A.; Duncan, K. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol. Microbiol. 2002, 43, 717-731.
44. Dahl, J.L.; Kraus, C.N.; Boshoff, H.I.; Doan, B.; Foley, K.; Avarbock, D.; Kaplan, G.; Mizrahi, V.; Rubin, H.; Barry, C.E., 3rd. The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc. Natl. Acad. Sci. USA 2003, 100, 10026-10031.
45. Ramirez, M.V.; Dawson, C.C.; Crew, R.; England, K.; Slayden, R.A. MazF6 toxin of Mycobacterium tuberculosis demonstrates antitoxin specificity and is coupled to regulation of cell growth by a Soj-like protein. BMC Microbiol. 2013, 13, 240.
46. Diderichsen, B.; Fiil, N.P.; Lavalle, R. Genetics of the RelB locus in Escherichia coli. J. Bacteriol. 1977, 131, 30-33.
47. Christensen, S.K.; Gerdes, K. Delayed-relaxed response explained by hyperactivation of RelE. Mol. Microbiol. 2004, 53, 587-597.
48. Grady, R.; Hayes, F. Axe-txe, a broad-spectrum proteic toxin-antitoxin system specified by a multidrug-resistant, clinical isolate of Enterococcus faecium. Mol. Microbiol. 2003, 47, 1419-1432.
49. Christensen, S.K.; Gerdes, K. RelE toxins from bacteria and archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Mol. Microbiol. 2003, 48, 1389-1400.
50. Kamada, K.; Hanaoka, F. Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin. Mol. Cell. 2005, 19, 497-509.
51. Cherny, I.; Gazit, E. The YefM antitoxin defines a family of natively unfolded proteins: Implications as a novel antibacterial target. J. Biol. Chem. 2004, 279, 8252-8261.
52. Kumar, P.; Issac, B.; Dodson, E.J.; Turkenburg, J.P.; Mande, S.C. Crystal structure of Mycobacterium tuberculosis YefM antitoxin reveals that it is not an intrinsically unstructured protein. J. Mol. Biol. 2008, 383, 482-493.
53. Miallau, L.; Jain, P.; Arbing, M.A.; Cascio, D.; Phan, T.; Ahn, C.J.; Chan, S.; Chernishof, I.; Maxson, M.; Chiang, J.; et al. Comparative proteomics identifies the cell-associated lethality of M. tuberculosis RelBE-like toxin-antitoxin complexes. Structure 2013, 21, 627-637.
54. Blower, T.R.; Salmond, G.P.; Luisi, B.F. Balancing at survival's edge: The structure and adaptive benefits of prokaryotic toxin-antitoxin partners. Curr. Opin. Struct. Biol. 2011, 21, 109-118.
55. Korch, S.B.; Contreras, H.; Clark-Curtiss, J.E. Three Mycobacterium tuberculosis Rel toxin-antitoxin modules inhibit mycobacterial growth and are expressed in infected human macrophages. J. Bacteriol. 2009, 191, 1618-1630.
56. Yang, M.; Gao, C.; Wang, Y.; Zhang, H.; He, Z.G. Characterization of the interaction and cross-regulation of three Mycobacterium tuberculosis RelBE modules. PLoS ONE 2010, 5, e10672.
57. Tian, Q.B.; Ohnishi, M.; Tabuchi, A.; Terawaki, Y. A new plasmid-encoded proteic killer gene system: Cloning, sequencing, and analyzing hig locus of plasmid rts1. Biochem. Biophys. Res. Commun. 1996, 220, 280-284.
58. Gerdes, K.; Christensen, S.K.; Lobner-Olesen, A. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 2005, 3, 371-382.
59. Hurley, J.M.; Woychik, N.A. Bacterial toxin HigB associates with ribosomes and mediates translation-dependent mRNA cleavage at A-rich sites. J. Biol. Chem. 2009, 284, 18605-18613.
60. 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.
61. Schureck, M.A.; Maehigashi, T.; Miles, S.J.; Marquez, J.; Ei Cho, S.; Erdman, R.; Dunham, C.M. Structure of the P. vulgaris HigB-(HigA)2-HigB toxin-antitoxin complex. J. Biol. Chem. 2013, doi:10.1074/jbc.M113.512095.
62. Arbing, M.A.; Handelman, S.K.; Kuzin, A.P.; Verdon, G.; Wang, C.; Su, M.; Rothenbacher, F.P.; Abashidze, M.; Liu, M.; Hurley, J.M.; et al. Crystal structures of Phd-Doc, HigA, and YeeU establish multiple evolutionary links between microbial growth-regulating toxin-antitoxin systems. Structure 2010, 18, 996-1010.
63. Stinear, T.P.; Seemann, T.; Harrison, P.F.; Jenkin, G.A.; Davies, J.K.; Johnson, P.D.; Abdellah, Z.; Arrowsmith, C.; Chillingworth, T.; Churcher, C.; et al. Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res. 2008, 18, 729-741.
64. Bordes, P.; Cirinesi, A.M.; Ummels, R.; Sala, A.; Sakr, S.; Bitter, W.; Genevaux, P. SecB-like chaperone controls a toxin-antitoxin stress-responsive system in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 2011, 108, 8438-8443.
65. Fivian-Hughes, A.S.; Davis, E.O. Analyzing the regulatory role of the HigA antitoxin within Mycobacterium tuberculosis. J. Bacteriol. 2010, 192, 4348-4356.
66. Sala, A.; Calderon, V.; Bordes, P.; Genevaux, P. TAC from Mycobacterium tuberculosis: A paradigm for stress-responsive toxin-antitoxin systems controlled by SecB-like chaperones. Cell Stress Chap. 2013, 18, 129-135.
67. Schuessler, D.L.; Cortes, T.; Fivian-Hughes, A.S.; Lougheed, K.E.; Harvey, E.; Buxton, R.S.; Davis, E.O.; Young, D.B. Induced ectopic expression of HigB toxin in Mycobacterium tuberculosis results in growth inhibition, reduced abundance of a subset of mRNAs and cleavage of tmRNA. Mol. Microbiol. 2013, 90, 195-207.
68. Botella, H.; Peyron, P.; Levillain, F.; Poincloux, R.; Poquet, Y.; Brandli, I.; Wang, C.; Tailleux, L.; Tilleul, S.; Charriere, G.M.; et al. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell. Host Microbe 2011, 10, 248-259.
69. Smollett, K.L.; Fivian-Hughes, A.S.; Smith, J.E.; Chang, A.; Rao, T.; Davis, E.O. Experimental determination of translational start sites resolves uncertainties in genomic open reading frame predictions-application to Mycobacterium tuberculosis. Microbiology 2009, 155, 186-197.
70. Stewart, G.R.; Wernisch, L.; Stabler, R.; Mangan, J.A.; Hinds, J.; Laing, K.G.; Young, D.B.; Butcher, P.D. Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 2002, 148, 3129-3138.
71. Tailleux, L.; Waddell, S.J.; Pelizzola, M.; Mortellaro, A.; Withers, M.; Tanne, A.; Castagnoli, P.R.; Gicquel, B.; Stoker, N.G.; Butcher, P.D.; et al. Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS ONE 2008, 3, e1403.
72. Guo, M.; Feng, H.; Zhang, J.; Wang, W.; Wang, Y.; Li, Y.; Gao, C.; Chen, H.; Feng, Y.; He, Z.G. Dissecting transcription regulatory pathways through a new bacterial one-hybrid reporter system. Genome Res. 2009, 19, 1301-1308.
73. Driessen, A.J.; Nouwen, N. Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 2008, 77, 643-667.
74. Randall, L.L.; Hardy, S.J. SecB, one small chaperone in the complex milieu of the cell. Cell. Mol. Life Sci. 2002, 59, 1617-1623.
75. Castanie-Cornet, M.P.; Bruel, N.; Genevaux, P. Chaperone networking facilitates protein targeting to the bacterial cytoplasmic membrane. Biochim. Biophys. Acta 2013, doi:10.1016/j.bbamcr.2013.11.007.
76. Zuber, B.; Chami, M.; Houssin, C.; Dubochet, J.; Griffiths, G.; Daffe, M. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 2008, 190, 5672-5680.
77. Niederweis, M.; Danilchanka, O.; Huff, J.; Hoffmann, C.; Engelhardt, H. Mycobacterial outer membranes: In search of proteins. Trends Microbiol. 2010, 18, 109-116.
78. Sani, M.; Houben, E.N.; Geurtsen, J.; Pierson, J.; de Punder, K.; van Zon, M.; Wever, B.; Piersma, S.R.; Jimenez, C.R.; Daffe, M.; et al. Direct visualization by cryo-EM of the mycobacterial capsular layer: A labile structure containing ESX-1-secreted proteins. PLoS Path. 2010, 6, e1000794.
79. Calloni, G.; Chen, T.; Schermann, S.M.; Chang, H.C.; Genevaux, P.; Agostini, F.; Tartaglia, G.G.; Hayer-Hartl, M.; Hartl, F.U. DnaK functions as a central hub in the E. coli chaperone network. Cell. Rep. 2012, 1, 251-264.
80. Bruel, N.; Castanie-Cornet, M.P.; Cirinesi, A.M.; Koningstein, G.; Georgopoulos, C.; Luirink, J.; Genevaux, P. Hsp33 controls elongation factor-Tu stability and allows Escherichia coli growth in the absence of the major DnaK and trigger factor chaperones. J. Biol Chem 2012, 287, 44435-44446.
81. Roberts, R.C.; Helinski, D.R. Definition of a minimal plasmid stabilization system from the broad-host-range plasmid rk2. J. Bacteriol. 1992, 174, 8119-8132.
82. Jiang, Y.; Pogliano, J.; Helinski, D.R.; Konieczny, I. ParE toxin encoded by the broad-host-range plasmid rk2 is an inhibitor of Escherichia coli gyrase. Mol. Microbiol. 2002, 44, 971-979.
83. Sberro, H.; Leavitt, A.; Kiro, R.; Koh, E.; Peleg, Y.; Qimron, U.; Sorek, R. Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning. Mol. Cell. 2013, 50, 136-148.
84. Dy, R.L.; Przybilski, R.; Semeijn, K.; Salmond, G.P.; Fineran, P.C. A widespread bacteriophage abortive infection system functions through a type IV toxin-antitoxin mechanism. Nucleic Acid Res. 2014, doi: 10.1093/nar/gkt1419.
85. Wozniak, R.A.; Waldor, M.K. A toxin-antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genet. 2009, 5, e1000439.
86. Christensen, S.K.; Mikkelsen, M.; Pedersen, K.; Gerdes, K. RelE, a global inhibitor of translation, is activated during nutritional stress. Proc. Natl. Acad. Sci. USA 2001, 98, 14328-14333.
87. Aizenman, E.; Engelberg-Kulka, H.; Glaser, G. An Escherichia coli chromosomal "addiction module" regulated by guanosine [corrected] 3',5'-bispyrophosphate: A model for programmed bacterial cell death. Proc. Natl. Acad. Sci. USA 1996, 93, 6059-6063.
88. Christensen-Dalsgaard, M.; Jorgensen, M.G.; Gerdes, K. Three new RelE-homologous mRNA interferases of Escherichia coli differentially induced by environmental stresses. Mol. Microbiol. 2010, 75, 333-348.
89. Ning, D.; Liu, S.; Xu, W.; Zhuang, Q.; Wen, C.; Tang, X. Transcriptional and proteolytic regulation of the toxin-antitoxin locus VapBC10 (ssr2962/slr1767) on the chromosome of Synechocystis sp. Pcc 6803. PLoS ONE 2013, 8, e80716.
90. Donegan, N.P.; Thompson, E.T.; Fu, Z.; Cheung, A.L. Proteolytic regulation of toxin-antitoxin systems by ClpPC in Staphylococcus aureus. J. Bacteriol. 2010, 192, 1416-1422.
91. Van Melderen, L.; Bernard, P.; Couturier, M. Lon-dependent proteolysis of CcdA is the key control for activation of CcdB in plasmid-free segregant bacteria. Mol. Microbiol. 1994, 11, 1151-1157.
92. Van Melderen, L.; Thi, M.H.; Lecchi, P.; Gottesman, S.; Couturier, M.; Maurizi, M.R. ATP-dependent degradation of CcdA by Lon protease. Effects of secondary structure and heterologous subunit interactions. J. Biol. Chem. 1996, 271, 27730-27738.
93. Loris, R.; Marianovsky, I.; Lah, J.; Laeremans, T.; Engelberg-Kulka, H.; Glaser, G.; Muyldermans, S.; Wyns, L. Crystal structure of the intrinsically flexible addiction antidote MazE. J. Biol. Chem. 2003, 278, 28252-28257.
94. Hansen, S.; Vulic, M.; Min, J.; Yen, T.J.; Schumacher, M.A.; Brennan, R.G.; Lewis, K. Regulation of the Escherichia coli HipBA toxin-antitoxin system by proteolysis. PLoS ONE 2012, 7, e39185.
95. Boutte, C.C.; Crosson, S. Bacterial lifestyle shapes stringent response activation. Trends Microbiol. 2013, 21, 174-180.
96. Ribeiro-Guimaraes, M.L.; Pessolani, M.C. Comparative genomics of mycobacterial proteases. Microb. Pathogen. 2007, 43, 173-178.
97. Pearce, M.J.; Mintseris, J.; Ferreyra, J.; Gygi, S.P.; Darwin, K.H. Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 2008, 322, 1104-1107.
98. Festa, R.A.; McAllister, F.; Pearce, M.J.; Mintseris, J.; Burns, K.E.; Gygi, S.P.; Darwin, K.H. Prokaryotic ubiquitin-like protein (Pup) proteome of Mycobacterium tuberculosis [corrected]. PLoS ONE 2010, 5, e8589.