The HicA toxin from Burkholderia pseudomallei has a role in persister cell formation

Biochemical Journal

Volumn 459, Issue 2, 2014, Pages 333-344

  Butt, Aaron ^a   Higman, Victoria A ^b   Williams, Christopher ^b   Crump, Matthew P ^b   Hemsley, Claudia M ^a   Harmer, Nicholas ^a   Titball, Richard W ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Burkholderia pseudomallei; HicAB; Melioidosis; Persister cell; Toxin antitoxin

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; CEFTAZIDIME; CIPROFLOXACIN; DOUBLE STRANDED RNA; GLYCINE; HICA TOXIN; HICB TOXIN; HISTIDINE; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BETA SHEET; BURKHOLDERIA PSEUDOMALLEI; CELL COUNT; CONTROLLED STUDY; DRUG EXPOSURE; GENE DELETION; GENE LOCUS; GENE OVEREXPRESSION; GROWTH INHIBITION; MELIOIDOSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; SURFACE PROPERTY;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BURKHOLDERIA PSEUDOMALLEI; CEFTAZIDIME; CIPROFLOXACIN; CLONING, MOLECULAR; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL SENSITIVITY TESTS; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RNA, DOUBLE-STRANDED;

EID: 84897491331     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140073     Document Type: Article

References (56)

1. Wiersinga, W., van der Poll, T., White, N., Day, N. and Peacock, S. J. (2006) Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat. Rev. Microbiol. 4, 273-282
2. Wiersinga, W. J., Currie, B. J. and Peacock, S. J. (2012) Melioidosis. N. Engl. J. Med. 367, 1035-1044
3. Limmathurotsakul, D. and Peacock, S. J. (2011) Melioidosis: a clinical overview. Br. Med. Bull. 99, 125-139
4. Currie, B., Fisher, D., Anstey, N. and Jacups, S. (2000) Melioidosis: acute and chronic disease, relapse and re-activation. Trans. R. Soc. Trop. Med. Hyg. 94, 301-304 (Pubitemid 30406565)
5. Lazar Adler, N. R., Govan, B., Cullinane, M., Harper, M., Adler, B. and Boyce, J. D. (2009) The molecular and cellular basis of pathogenesis in melioidosis: how does Burkholderia pseudomallei cause disease? FEMS Microbiol. Rev. 33, 1079-1099
6. Bigger, J. (1944) Treatment of staphylococcal infections with penicillin. Lancet 244, 497-500
7. Goodyear, A., Bielefeldt-Ohmann, H., Schweizer, H. and Dow, S. (2012) Persistent gastric colonization with Burkholderia pseudomallei and dissemination from the gastrointestinal tract following mucosal inoculation of mice. PLoS ONE 7, e37324
8. Fauvart, M., De Groote, V. N. and Michiels, J. (2011) Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J. Med. Microbiol. 60, 699-709
9. Joers, A., Kaldalu, N. and Tenson, T. (2010) The frequency of persisters in Escherichia coli reflects the kinetics of awakening from dormancy. J. Bacteriol. 192, 3379-3384
10. Keren, I., Kaldalu, N., Spoering, A., Wang, Y. and Lewis, K. (2004) Persister cells and tolerance to antimicrobials. FEMS Microbiol. Lett. 230, 13-18 (Pubitemid 38091733)
11. Kint, C. I., Verstraeten, N., Fauvart, M. and Michiels, J. (2012) New-found fundamentals of bacterial persistence. Trends Microbiol. 20, 577-585
12. Leung, V. and Lévesque, C. (2012) A stress-inducible quorum-sensing peptide mediates the formation of persister cells with noninherited multidrug tolerance. J. Bacteriol. 194, 2265-2274
13. Vega, N. M., Allison, K. R., Khalil, A. S. and Collins, J. J. (2012) Signaling-mediated bacterial persister formation. Nat. Chem. Biol. 8, 431-433
14. Moker, N., Dean, C. R. and Tao, J. (2010) Pseudomonas aeruginosa increases formation of multidrug-tolerant persister cells in response to quorum-sensing signaling molecules. J. Bacteriol. 192, 1946-1955
15. Shah, D., Zhang, Z., Khodursky, A., Kaldalu, N., Kurg, K. and Lewis, K. (2006) Persisters: a distinct physiological state of E. coli. BMC Microbiol. 6, 53
16. Dörr, T., Vulić, M. and Lewis, K. (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol. 8, e1000317
17. Zhao, J., Wang, Q., Li, M., Heijstra, B. D., Wang, S., Liang, Q. and Qi, Q. (2013) Escherichia coli toxin gene hipA affects biofilm formation and DNA release. Microbiology 159, 633-640
18. Korch, S. B., Henderson, T. A. and Hill, T. M. (2003) Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol. Microbiol. 50, 1199-1213 (Pubitemid 37475853)
19. Korch, S. and Hill, T. (2006) Ectopic overexpression of wild-type and mutant hipA genes in Escherichia coli: effects on macromolecular synthesis and persister formation. J. Bacteriol. 188, 3826-3836 (Pubitemid 43825388)
20. Singh, R., Barry, 3rd, C. E. and Boshoff, H. I. (2010) The three RelE homologs of Mycobacterium tuberculosis have individual, drug-specific effects on bacterial antibiotic tolerance. J. Bacteriol. 192, 1279-1291
21. Butt, A., Muller, C., Harmer, N. and Titball, R. W. (2013) Identification of type II toxin-antitoxin modules in Burkholderia pseudomallei. FEMS Microbiol. Lett. 338, 86-94
22. 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. U.S.A. 83, 3116-3120 (Pubitemid 16042987)
23. Yamaguchi, Y., Park, J. and Inouye, M. (2011) Toxin-antitoxin systems in Bacteria and Archaea. Ann. Rev. Genet. 45, 61-79
24. 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
25. 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. (2012) A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat. Chem. Biol. 8, 855-861
26. Hayes, F. (2003) Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301, 1496-1499
27. Jorgensen, M. G., Pandey, D. P., Jaskolska, M. and Gerdes, K. (2009) HicA of Escherichia coli defines a novel family of translation-independent mRNA interferases in bacteria and archaea. J. Bacteriol. 191, 1191-1199
28. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207-234
29. Milton, D. L., O'Toole, R., Horstedt, P. and Wolf-Watz, H. (1996) Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178, 1310-1319 (Pubitemid 26073387)
30. Subramaniam, S. (1998) The Biology Workbench: a seamless database and analysis environment for the biologist. Proteins 32, 1-2
31. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biol. NMR 6, 277-293
32. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J. and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687-696 (Pubitemid 40695845)
33. Bardiaux, B., Malliavin, T. and Nilges, M. (2012) ARIA for solution and solid-state NMR. Methods Mol. Biol. 831, 453-483
34. Bhattacharya, A., Tejero, R. and Montelione, G. T. (2007) Evaluating protein structures determined by structural genomics consortia. Proteins 66, 778-795
35. Doreleijers, J. F., Sousa da Silva, A. W., Krieger, E., Nabuurs, S. B., Spronk, C. A., Stevens, T. J., Vranken, W. F., Vriend, G. and Vuister, G. W. (2012) CING: an integrated residue-based structure validation program suite. J. Biomol. NMR 54, 267-283
36. Ulrich, E. L., Akutsu, H., Doreleijers, J. F., Harano, Y., Ioannidis, Y. E., Lin, J., Livny, M., Mading, S., Maziuk, D., Miller, Z. et al. (2008) BioMagResBank. Nucleic Acids Res. 36, D402-D408 (Pubitemid 351149757)
37. Liew, F. Y., Tay, S. T. and Puthucheary, S. D. (2011) Reduced susceptibility of Malaysian clinical isolates of Burkholderia pseudomallei to ciprofloxacin. Trop. Biomed. 28, 646-650
38. Madigan, M., Martinko, J., Stahl, D. and Clark, D. (2012) Microbial growth. In Brock Biology of Microorganisms, pp. 145-177, Pearson, San Francisco
39. Knudsen, G. M., Ng, Y. and Gram, L. (2013) Survival of bactericidal antibiotic treatment by a persister subpopulation of Listeria monocytogenes. Appl. Environ. Microbiol. 79, 7390-7397
40. Lewis, K. (2010) Persister cells. Annu. Rev. Microbiol. 64, 357-372
41. Ahmad, Z., Klinkenberg, L. G., Pinn, M. L., Fraig, M. M., Peloquin, C. A., Bishai, W. R., Nuermberger, E. L., Grosset, J. H. and Karakousis, P. C. (2009) Biphasic kill curve of isoniazid reveals the presence of drug-tolerant, not drug-resistant, Mycobacterium tuberculosis in the guinea pig. J. Infect. Dis. 200, 1136-1143
42. Lewis, K. (2007) Persister cells, dormancy and infectious disease. Nat. Rev. Microbiol. 5, 48-56
43. Fiebig, A., Castro Rojas, C. M., Siegal-Gaskins, D. and Crosson, S. (2010) Interaction specificity, toxicity and regulation of a paralogous set of ParE/RelE-family toxin-antitoxin systems. Mol. Microbiol. 77, 236-251
44. Sevillano, L., Díaz, M., Yamaguchi, Y., Inouye, M. and Santamaría, R. (2012) Identification of the first functional toxin-antitoxin system in Streptomyces. PLoS ONE 7, e32977
45. Gerdes, K. and Maisonneuve, E. (2012) Bacterial persistence and toxin-antitoxin loci. Annu. Rev. Microbiol. 66, 103-123
46. Maisonneuve, E., Shakespeare, L., Jorgensen, M. and Gerdes, K. (2011) Bacterial persistence by RNA endonucleases. Proc. Natl. Acad. Sci. U.S.A. 108, 13206-13211
47. Kim, Y. and Wood, T. K. (2010) Toxins Hha and CspD and small RNA regulator Hfq are involved in persister cell formation through MqsR in Escherichia coli. Biochem. Biophys. Res. Commun. 391, 209-213
48. Keren, I., Shah, D., Spoering, A., Kaldalu, N. and Lewis, K. (2004) Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186, 8172-8180 (Pubitemid 39603206)
49. Makarova, K. S., Grishin, N. V. and Koonin, E. V. (2006) The HicAB cassette, a putative novel, RNA-targeting toxin-antitoxin system in archaea and bacteria. Bioinformatics 22, 2581-2584 (Pubitemid 44642594)
50. Blower, T. R., Salmond, G. P. and Luisi, B. F. (2011) Balancing at survival's edge: the structure and adaptive benefits of prokaryotic toxin-antitoxin partners. Curr. Opin. Struct. Biol. 21, 109-118
51. Zhu, L., Phadtare, S., Nariya, H., Ouyang, M., Husson, R. N. and Inouye, M. (2008) The mRNA interferases, MazF-mt3 and MazF-mt7 from Mycobacterium tuberculosis target unique pentad sequences in single-stranded RNA. Mol. Microbiol. 69, 559-569 (Pubitemid 351962556)
52. Goeders, N., Dreze, P. L. and Van Melderen, L. (2013) Relaxed cleavage specificity within the RelE toxin family. J. Bacteriol. 195, 2541-2549
53. Porter, C. T., Bartlett, G. J. and Thornton, J. M. (2004) The Catalytic Site Atlas: a resource of catalytic sites and residues identified in enzymes using structural data. Nucleic Acids Res. 32, D129-D133 (Pubitemid 38081621)
54. Heeb, S., Blumer, C. and Haas, D. (2002) Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J. Bacteriol. 184, 1046-1056 (Pubitemid 34113373)
55. Ichiyanagi, K., Ishino, Y., Ariyoshi, M., Komori, K. and Morikawa, K. (2000) Crystal structure of an archaeal intein-encoded homing endonuclease PI-PfuI. J. Mol. Biol. 300, 889-901
56. Murzin, A. G., Brenner, S. E., Hubbard, T. and Chothia, C. (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247, 536-540