Distinct type i and type II toxin-antitoxin modules control Salmonella lifestyle inside eukaryotic cells

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Lobato Márquez, Damián ^a,b   Moreno Córdoba, Inmaculada ^b   Figueroa, Virginia ^a   Diáz Orejas, Ramón ^b   Garciá Del Portillo, Francisco ^a  

^a CSIC   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITOXIN; BACTERIAL TOXIN;

BACTERIAL GENOME; BIOLOGY; CLUSTER ANALYSIS; EPITHELIUM CELL; EUKARYOTIC CELL; FIBROBLAST; GENE LOCUS; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES; SALMONELLA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

ANTITOXINS; BACTERIAL TOXINS; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; EPITHELIAL CELLS; EUKARYOTIC CELLS; FIBROBLASTS; GENETIC LOCI; GENOME, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 84925235038     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09374     Document Type: Article

References (69)

1. Ogura, T., Hiraga, S. Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc. Natl. Acad. Sci. USA 80, 4784-4788 (1983).
2. Bravo, A., de Torrontegui, G., Diaz, R. Identification of components of a new stability system of plasmid R1, ParD, that is close to the origin of replication of this plasmid. Mol. Gen. Genet. 210, 101-110 (1987).
3. Gerdes, K., Rasmussen, P. B., Molin, S. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc. Natl. Acad. Sci. USA 83, 3116-3120 (1986).
4. Gerdes, K. in Prokaryotic toxin-antitoxins (Springer, 2013).
5. Hayes, F. &Van Melderen, L. Toxins-antitoxins: diversity, evolution and function. Crit. Rev. Biochem. Mol. Biol. 46, 386-408 (2011).
6. Wang, X. et al. A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat. Chem. Biol. 8, 855-861 (2012).
7. Fozo, E. M. et al. Abundance of type I toxin-antitoxin systems in bacteria: searches for new candidates and discovery of novel families. Nucleic Acids Res. 38, 3743-3759 (2010).
8. 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. 5, e1000767 (2009).
9. Shao, Y. et al. TADB: a web-based resource for Type 2 toxin-antitoxin loci in bacteria and archaea. Nucleic Acids Res. 39, D606-611 (2011).
10. Sberro, H. et al. Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning. Mol. Cell 50, 136-148 (2013).
11. Yamaguchi, Y., Park, J. H., Inouye, M. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45, 61-79 (2011).
12. Yamaguchi, Y., Inouye, M. Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat. Rev. Microbiol. 9, 779-790 (2011).
13. Jensen, R. B., Gerdes, K. Programmed cell death in bacteria: proteic plasmid stabilization systems. Mol. Microbiol. 17, 205-210 (1995).
14. Maisonneuve, E., Gerdes, K. Molecular mechanisms underlying bacterial persisters. Cell 157, 539-548 (2014).
15. Fineran, P. C. et al. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc. Natl. Acad. Sci. USA 106, 894-899 (2009).
16. Hazan, R., Engelberg-Kulka, H. Escherichia coli mazEF-mediated cell death as a defense mechanism that inhibits the spread of phage P1. Mol. Genet. Genomics 272, 227-234 (2004).
17. Hazan, R., Sat, B., Engelberg-Kulka, H. Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions. J. Bacteriol. 186, 3663-3669 (2004).
18. Buts, L., Lah, J., Dao-Thi, M. H., Wyns, L., Loris, R. Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem. Sci. 30, 672-679 (2005).
19. Aguirre-Ramirez, M., Ramirez-Santos, J., Van Melderen, L., Gomez-Eichelmann, M. C. Expression of the F plasmid ccd toxin-antitoxin systemin Escherichia coli cells under nutritional stress. Can. J. Microbiol. 52, 24-30 (2006).
20. Gerdes, K., Christensen, S. K., Lobner-Olesen, A. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3, 371-382 (2005).
21. Kim, Y. et al. Escherichia coli toxin/antitoxin pair MqsR/MqsA regulate toxin CspD. Environ. Microbiol. 12, 1105-1121 (2010).
22. Frampton, R., Aggio, R. B., Villas-Boas, S. G., Arcus, V. L., Cook, G. M. Toxinantitoxin systems of Mycobacterium smegmatis are essential for cell survival. J. Biol. Chem. 287, 5340-5356 (2012).
23. Kim, Y., Wang, X., Ma, Q., Zhang, X. S., Wood, T. K. Toxin-antitoxin systems in Escherichia coli influence biofilm formation through YjgK (TabA) and fimbriae. J. Bacteriol. 191, 1258-1267 (2009).
24. Muranaka, L. S., Takita, M. A., Olivato, J. C., Kishi, L. T., de Souza, A. A. Global expression profile of biofilm resistance to antimicrobial compounds in the plantpathogenic bacterium Xylella fastidiosa reveals evidence of persister cells. J. Bacteriol. 194, 4561-4569 (2012).
25. Wang, X. &Wood, T. K. Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl. Environ. Microbiol. 77, 5577-5583 (2011).
26. Helaine, S., Kugelberg, E. Bacterial persisters: formation, eradication, and experimental systems. Trends Microbiol. 22, 417-424 (2014).
27. Schuster, C. F., Bertram, R. Toxin-antitoxin systems are ubiquitous and versatile modulators of prokaryotic cell fate. FEMS Microbiol. Lett. 340, 73-85 (2013).
28. Norton, J. P., Mulvey, M. A. Toxin-antitoxin systems are important for nichespecific colonization and stress resistance of uropathogenic Escherichia coli. PLoS Pathog. 8, e1002954 (2012).
29. Ren, D., Walker, A. N., Daines, D. A. Toxin-antitoxin loci vapBC-1 and vapXD contribute to survival and virulence in nontypeable Haemophilus influenzae. BMC Microbiol. 12, 263 (2012).
30. Ren, D., Kordis, A. A., Sonenshine, D. E., Daines, D. A. The ToxA-vapA toxinantitoxin locus contributes to the survival of nontypeable Haemophilus influenzae during infection. PLoS One 9, e91523 (2014).
31. De la Cruz, M. A. et al. A toxin-antitoxin module of Salmonella promotes virulence in mice. PLoS Pathog. 9, e1003827 (2013).
32. Helaine, S. et al. Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science 343, 204-208 (2014).
33. 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 6, e17962 (2011).
34. Sala, A., Bordes, P., Genevaux, P. Multiple toxin-antitoxin systems in Mycobacterium tuberculosis. Toxins 6, 1002-1020 (2014).
35. Ruby, T., McLaughlin, L., Gopinath, S., Monack, D. Salmonella's long-term relationship with its host. FEMS Microbiol. Rev. 36, 600-615 (2012).
36. Tsolis, R. M. et al. Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections. Adv. Exp. Med. Biol. 473, 261-274 (1999).
37. Crawford, R. W. et al. Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proc. Natl. Acad. Sci. USA 107, 4353-4358 (2010).
38. Monack, D. M., Bouley, D. M., Falkow, S. Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp11/1 mice and can be reactivated by IFNgamma neutralization. J. Exp. Med. 199, 231-241 (2004).
39. Mastroeni, P., Grant, A., Restif, O. &Maskell, D. Adynamic view of the spread and intracellular distribution of Salmonella enterica. Nat. Rev. Microbiol. 7, 73-80 (2009).
40. Garcia-del Portillo, F. Salmonella intracellular proliferation: where, when and how? Microbes Infect. 3, 1305-1311 (2001).
41. Núñez-Hernández, C. et al. Genome expression analysis of nonproliferating intracellular Salmonella enterica serovar Typhimurium unravels an acid pHdependent PhoP-PhoQ response essential for dormancy. Infect. Immun. 81, 154-165 (2013).
42. Blower, T. R. et al. Identification and classification of bacterial Type III toxinantitoxin systems encoded in chromosomal and plasmid genomes. Nucleic Acids Res. 40, 6158-6173 (2012).
43. Fookes, M. et al. Salmonella bongori provides insights into the evolution of the Salmonellae. PLoS Pathog. 7, e1002191 (2011).
44. Nuccio, S. P., Baumler, A. J. Comparative analysis of Salmonella genomes identifies a metabolic network for escalating growth in the inflamed gut. MBio 5, e00929-00914 (2014).
45. Bahassi, E. M., Salmon, M. A., Van Melderen, L., Bernard, P., Couturier, M. F plasmid CcdB killer protein: ccdB genemutants coding for non-cytotoxic proteins which retain their regulatory functions. Mol. Microbiol. 15, 1031-1037 (1995).
46. Núñez-Hernández, C., Alonso, A., Pucciarelli, M. G., Casadesus, J., Garc?á del Portillo, F. Dormant intracellular Salmonella enterica serovar Typhimurium discriminates among Salmonella pathogenicity island 2 effectors to persist inside fibroblasts. Infect. Immun. 82, 221-232 (2014).
47. Malik-Kale, P., Winfree, S., Steele-Mortimer, O. The bimodal lifestyle of intracellular Salmonella in epithelial cells: replication in the cytosol obscures defects in vacuolar replication. PLoS One 7, e38732 (2012).
48. Slattery, A., Victorsen, A. H., Brown, A., Hillman, K., Phillips, G. J. Isolation of highly persistent mutants of Salmonella enterica serovar typhimurium reveals a new toxin-antitoxin module. J. Bacteriol. 195, 647-657 (2013).
49. Bordes, P. et al. SecB-like chaperone controls a toxin-antitoxin stress-responsive system in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 108, 8438-8443 (2011).
50. Nariya, H., Inouye, M. MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell 132, 55-66 (2008).
51. Cook, G. M. et al. Ribonucleases in bacterial toxin-antitoxin systems. Biochim. Biophys. Acta 1829, 523-531 (2013).
52. Vetting, M. W. et al. Structure and functions of the GNAT superfamily of acetyltransferases. Arch. Biochem. Biophys. 433, 212-226 (2005).
53. Spange, S., Wagner, T., Heinzel, T., Kramer, O. H. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int. J. Biochem. Cell Biol. 41, 185-198 (2009).
54. Thao, S., Escalante-Semerena, J. C. Biochemical and thermodynamic analyses of Salmonella enterica Pat, a multidomain, multimeric N(epsilon)-lysine acetyltransferase involved in carbon and energy metabolism. MBio 2, e00216-11 (2011).
55. Wagner, E. G., Unoson, C. The toxin-antitoxin system tisB-istR1: Expression, regulation, and biological role in persister phenotypes. RNA Biol. 9, 1513-1519 (2012).
56. Yamaguchi, Y., Tokunaga, N., Inouye, M., Phadtare, S. Characterization of LdrA (long direct repeat A) protein of Escherichia coli. J. Mol. Microbiol. Biotechnol. 24, 91-97 (2014).
57. Steif, A., Meyer, I. M. The hok mRNA family. RNA Biol. 9, 1399-1404 (2012).
58. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M., Hinton, J. C. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47, 103-118 (2003).
59. Kasari, V., Mets, T., Tenson, T., Kaldalu, N. Transcriptional cross-activation between toxin-antitoxin systems of Escherichia coli. BMC Microbiol. 13, 45 (2013).
60. Winther, K. S., Gerdes, K. Ectopic production of VapCs from Enterobacteria inhibits translation and trans-activates YoeB mRNA interferase. Mol. Microbiol. 72, 918-930 (2009).
61. Malik-Kale, P. et al. Salmonella-at home in the host cell. Front. Microbiol. 2, 125 (2011).
62. Leplae, R. et al. Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res. 39, 5513-5525 (2011).
63. Chang, A. C., Cohen, S. N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134, 1141-1156 (1978).
64. Lemonnier, M., Lane, D. Expression of the second lysine decarboxylase gene of Escherichia coli. Microbiology 144, 10 (1998).
65. Gotfredsen, M., Gerdes, K. The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family. Mol. Microbiol. 29, 1065-1076 (1998).
66. Nieto, C. et al. The chromosomal relBE2 toxin-antitoxin locus of Streptococcus pneumoniae: characterization and use of a bioluminescence resonance energy transfer assay to detect toxin-antitoxin interaction. Mol. Microbiol. 59, 1280-1296 (2006).
67. Maisonneuve, E., Shakespeare, L. J., Jorgensen, M. G., Gerdes, K. Bacterial persistence by RNA endonucleases. Proc. Natl. Acad. Sci. USA 108, 13206-13211 (2011).
68. Uzzau, S., Figueroa-Bossi, N., Rubino, S., Bossi, L. Epitope tagging of chromosomal genes in Salmonella. Proc. Natl. Acad. Sci. USA 98, 15264-15269 (2001).
69. Aiastui, A., Pucciarelli, M. G., Garcia-del Portillo, F. Salmonella enterica serovar typhimurium invades fibroblasts by multiple routes differing from the entry into epithelial cells. Infect. Immun. 78, 2700-2713 (2010).