Interconnection of post-transcriptional regulation: The RNA-binding protein Hfq is a novel target of the Lon protease in Pseudomonas aeruginosa

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Fernandez, Lucia ^a,b   Breidenstein, Elena B M ^a,c   Taylor, Patrick K ^a,d   Bains, Manjeet ^a   De La Fuente Nunez, Cesar ^a,e   Fang, Yuan ^a   Foster, Leonard J ^a   Hancock, Robert E W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^c SUMMIT PLC   (United Kingdom)

^d UNIVERSITY OF OTTAWA   (Canada)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ENDOPEPTIDASE LA; HOST FACTOR 1;

GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN PROCESSING; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOST FACTOR 1 PROTEIN; PHENOTYPE; PROTEASE LA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; PSEUDOMONAS AERUGINOSA;

EID: 84971265090     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep26811     Document Type: Article

References (50)

1. Gottesman, S. Proteases and their targets in Escherichia coli. Annu. Rev. Genet. 30, 465-506 (1996).
2. Butler, S. M., Festa, R. A., Pearce, M. J., Darwin, K. H. Self-compartmentalized bacterial proteases and pathogenesis. Mol. Microbiol. 60, 553-562 (2006).
3. Maurizi, M. R. Proteases and protein degradation in Escherichia coli. Experimentia 48, 178-201 (1992).
4. Kobiler, O., Oppenheim, A. B., Herman, C. Recruitment of host ATP-dependent proteases by bacteriophage lambda. J. Struct. Biol. 146, 72-78 (2004).
5. Maurizi, M. R. Degradation in vitro of bacteriophage lambda N protein by Lon protease from Escherichia coli. J. Biol. Chem. 262, 2696-2703 (1987).
6. Mizusawa, S., Gottesman, S. Protein degradation in Escherichia coli: the lon gene controls the stability of SulA protein. Proc. Natl. Acad. Sci. USA 80, 358-362 (1983).
7. Torres-Cabassa, A. S., Gottesman, S. Capsule synthesis in Escherichia coli K-12 is regulated by proteolysis. J. Bacteriol. 169, 981-989 (1987).
8. Gibson, R. L., Burns, J. L., Ramsey, B. W. Pathophysiology and management of pulmonary infections in cystic fibrosis. Am. J. Respir. Crit. Care Med. 168, 918-951 (2003).
9. Hutchison, M. L., Govan, J. R. Pathogenicity of microbes associated with cystic fibrosis. Microbes Infect. 1, 1005-1014 (1999).
10. Kindrachuk, K. N., Fernández, L., Bains, M., Hancock, R. E. W. Involvement of an ATP-dependent protease, PA0779/AsrA, in inducing heat shock in response to tobramycin in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 55, 1874-1882 (2011).
11. Fernández, L., Breidenstein, E. B. M., Song, D., Hancock, R. E. W. Role of intracellular proteases in the antibiotic resistance, motility, and biofilm formation of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 56, 1128-1132 (2012).
12. Brazas, M. D., Breidenstein, E. B. M., Overhage, J., Hancock, R. E. W. Role of Lon, an ATP-dependent protease homolog, in resistance of Pseudomonas aeruginosa to ciprofloxacin. Antimicrob. Agents Chemother. 51, 4276-4283 (2007).
13. Breidenstein, E. B. M., Khaira, B. K., Wiegand, I., Overhage, J., Hancock, R. E. W. Complex ciprofloxacin resistome revealed by screening a Pseudomonas aeruginosa mutant library for altered susceptibility. Antimicrob. Agents Chemother. 52, 4486-4491 (2008).
14. Breidenstein, E. B. M., Bains, M., Hancock, R. E. W. Involvement of the Lon protease in the SOS response triggered by ciprofloxacin in Pseudomonas aeruginosa PAO1. Antimicrob. Agents Chemother. 56, 2879-2887 (2012).
15. Marr, A. K., Overhage, J., Bains, M., Hancock, R. E. W. The Lon protease of Pseudomonas aeruginosa is induced by aminoglycosides and is involved in biofilm formation and motility. Microbiology 153, 474-482 (2007).
16. Breidenstein, E. B. M. et al. The Lon protease is essential for full virulence in Pseudomonas aeruginosa. PLoS One 7, e49123 (2012).
17. Neher, S. B. et al. Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol. Cell 22, 193-204 (2006).
18. Tsui, H. C., Leung, H. C., Winkler, M. E. Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol. Microbiol. 13, 35-49 (1994).
19. Sonnleitner, E., Schuster, M., Sorger-Domenigg, T., Greenberg, E. P., Bläsi, U. Hfq-dependent alterations of the transcriptome profile and effects on quorum sensing in Pseudomonas aeruginosa. Mol. Microbiol. 59, 1542-1558 (2006).
20. Sonnleitner, E. et al. Reduced virulence of a hfq mutant of Pseudomonas aeruginosa O1. Microb. Pathog. 35, 217-228 (2003).
21. Takaya, A., Tabuchi, F., Tsuchiya, H., Isogai, E., Yamamoto, T. Negative regulation of quorum-sensing systems in Pseudomonas aeruginosa by ATP-dependent Lon protease. J. Bacteriol. 190, 4181-418 (2008).
22. Breidenstein, E. B. M. Global regulation of the Lon protease of Pseudomonas aeruginosa and its influence on ciprofloxacin resistance and virulence. PhD Thesis. University of British Columbia, Vancouver, Canada (2012).
23. Hassett, D. J., Charniga, L., Bean, K., Ohman, D. E., Cohen, M. S. Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase. Infect. Immun. 60, 328-336 (1992).
24. Sonnleitner, E. et al. Detection of small RNAs in Pseudomonas aeruginosa by RNomics and structure-based bioinformatic tools. Microbiology 154, 3175-3187 (2008).
25. Osborne, J., Djapgne, L., Tran, B. Q., Goo, Y. A., Oglesby-Sherrouse, A. G. A method for in vivo identification of bacterial small RNA-binding proteins. Microbiology open 3, 950-960 (2014).
26. Yeung, A. T. et al. Swarming of Pseudomonas aeruginosa is controlled by a broad spectrum of transcriptional regulators, including MetR. J. Bacteriol. 191, 5592-602 (2009).
27. Sonnleitner, E. et al. The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal. Mol. Microbiol. 80, 868-885 (2011).
28. Déziel, E. et al. The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol. Microbiol. 55, 998-1014 (2005).
29. Pesci, E. C. et al. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96, 11229-11234 (1999).
30. Yang, L., Nilsson, M., Gjermansen, M., Givskov, M., Tolker-Nielsen, T. Pyoverdine and PQS mediated subpopulation interactions involved in Pseudomonas aeruginosa biofilm formation. Mol. Microbiol. 74, 1380-1392 (2009).
31. Petrova, O. E., Sauer, K. SagS contributes to the motile-sessile switch and acts in concert with BfiSR to enable Pseudomonas aeruginosa biofilm formation. J. Bacteriol. 193, 6614-6628 (2011).
32. Yeung, A. T., Bains, M., Hancock, R. E. W. The sensor kinase CbrA is a global regulator that modulates metabolism, virulence, and antibiotic resistance in Pseudomonas aeruginosa. J. Bacteriol. 193, 918-31 (2011).
33. Kuwayama, H. et al. PCR-mediated generation of a gene disruption construct without the use of DNA ligase and plasmid vectors. Nucleic Acids Res. 30, E2 (2002).
34. Rogers, L. D., Fang, Y., Foster, L. J. An integrated global strategy for cell lysis, fractionation, enrichment and mass spectrometric analysis of phosphorylated peptides. Mol. Biosyst. 6, 822-829 (2010).
35. Cox, J. et al. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Prot. 4, 698-705 (2009).
36. Perkins, D. N., Pappin, D. J. C., Creasy, D. M., Cottrell, J. S. Probability-based protein identification by searching sequence database using mass spectrometry data. Electrophoresis 20, 3551-3567 (1999).
37. Hansen, S. et al. Regulation of the Escherichia coli HipBA toxin-antitoxin system by proteolysis. PLoS One 7, e39185 (2012).
38. Rozen, S., Skaletsky, H. J. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz, S., Misener, S. (eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, NJ, pp 365-386 (2000).
39. Choi, K. H., Kumar, A., Schweizer, H. P. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J. Microbiol. Methods 64, 391-397 (2006).
40. Overhage, J., Lewenza, S., Marr, A. K., Hancock, R. E. W. Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J. Bacteriol. 189, 2164-2169 (2007).
41. McPhee, J. B. et al. Contribution of the PhoP-PhoQ and PmrA-PmrB two-component regulatory systems to Mg2+induced gene regulation in Pseudomonas aeruginosa. J. Bacteriol. 188, 3995-4006 (2006).
42. de la Fuente-Núñez, C. et al. Inhibition of bacterial biofilm formation and swarming motility by a small synthetic cationic peptide. Antimicrob. Agents Chemother. 56, 2696-2704 (2012).
43. de la Fuente-Núñez, C., Reffuveille, F., Haney, E. F., Straus, S. K., Hancock, R. E. W. Broad-spectrum anti-biofilm peptide that targets a cellular stress response. PLoS Pathog. 10, e1004152 (2014).
44. Winsor, G. L. et al. Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39, D596-600 (2011).
45. Mylroie, J. R., Friello, D. A., Chakrabarty, A. M. Transformation of Pseudomonas putida with chromosomal DNA. Biochem. Biophys. Res. Commun. 82, 281-288 (1978).
46. Lewenza, S. et al. Construction of a mini-Tn5-luxCDABE mutant library in Pseudomonas aeruginosa PAO1: a tool for identifying differentially regulated genes. Genome Res. 15, 583-589 (2005).
47. Liberati, N. T. et al. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl. Acad. Sci. USA 103, 2833-2838 (2006).
48. Simon, R., Priefer, U., Pühler, A. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1, 784-791 (1983).
49. Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J., Schweizer, H. P. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212, 77-86 (1998).
50. Schweizer, H. P. Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene 97, 109-121 (1991).