Hybrid sensor kinase PA1611 in Pseudomonas aeruginosa regulates transitions between acute and chronic infection through direct interaction with RetS

Molecular Microbiology

Volumn 88, Issue 4, 2013, Pages 784-797

  Kong, Weina ^a   Chen, Lin ^b   Zhao, Jieqiong ^a   Shen, Tuo ^a   Surette, Michael G ^c   Shen, Lixin ^a   Duan, Kangmin ^a,b  

^a NORTHWEST UNIVERSITY   (China)

^b UNIVERSITY OF MANITOBA   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; LACTATE DEHYDROGENASE; PROTEIN 3346; PROTEIN 3347; PROTEIN GACS; PROTEIN KINASE; PROTEIN LADS; PROTEIN PA1243; PROTEIN PA2824; PROTEIN RETS; PSEUDOMONAS AERUGINOSA 1611 PROTEIN; RNA; SMALL RNA RSMY; SMALL RNA RSMZ; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL PHENOMENA AND FUNCTIONS; BIOFILM; CONTROLLED STUDY; CYTOTOXICITY; DISEASE COURSE; ENZYME ANALYSIS; ENZYME REGULATION; ENZYME RELEASE; EXOS GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC ASSOCIATION; IN VIVO STUDY; LIGAND BINDING; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS AERUGINOSA 1611 GENE; PSEUDOMONAS INFECTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SWARMING MOTILITY; TRANSPOSON; TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LOCOMOTION; PROTEIN BINDING; PROTEIN KINASES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; VIRULENCE FACTORS;

PSEUDOMONAS AERUGINOSA;

EID: 84877795205     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12223     Document Type: Article

References (47)

1. Becher, A., and Schweizer, H.P. (2000) Integration-proficient Pseudomonas aeruginosa vectors for isolation of single-copy chromosomal lacZ and lux gene fusions. Biotechniques 29: 948-950, 952.
2. Bhuwan, M., Lee, H.J., Peng, H.L., and Chang, H.Y. (2012) Histidine-containing phosphotransfer protein-B (HptB) regulates swarming motility through partner switching system in Pseudomonas aeruginosa PAO1 strain. J Biol Chem 287: 1903-1914.
3. Bordi, C., Lamy, M.C., Ventre, I., Termine, E., Hachani, A., Fillet, S., etal. (2010) Regulatory RNAs and the HptB/RetS signalling pathways fine-tune Pseudomonas aeruginosa pathogenesis. Mol Microbiol 76: 1427-1443.
4. Brencic, A., and Lory, S. (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 72: 612-632.
5. Brencic, A., McFarland, K.A., McManus, H.R., Castang, S., Mogno, I., Dove, S.L., and Lory, S. (2009) The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol Microbiol 73: 434-445.
6. Burrowes, E., Baysse, C., Adams, C., and O'Gara, F. (2006) Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152: 405-418.
7. Coburn, B., Sekirov, I., and Finlay, B.B. (2007) Type III secretion systems and disease. Clin Microbiol Rev 20: 535-549.
8. Ditta, G., Stanfield, S., Corbin, D., and Helinski, D.R. (1980) Broad host range DNA cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci USA 77: 7347-7351.
9. Duan, K., Dammel, C., Stein, J., Rabin, H., and Surette, M.G. (2003) Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50: 1477-1491.
10. Fleiszig, S.M., Wiener-Kronish, J.P., Miyazaki, H., Vallas, V., Mostov, K.E., Kanada, D., etal. (1997) Pseudomonas aeruginosa-mediated cytotoxicity and invasion correlate with distinct genotypes at the loci encoding exoenzyme S. Infect Immun 65: 579-586.
11. Frank, D.W. (1997) The exoenzyme S regulon of Pseudomonas aeruginosa. Mol Microbiol 26: 621-629.
12. Friedman, L., and Kolter, R. (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51: 675-690.
13. Goodman, A.L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R.S., and Lory, S. (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7: 745-754.
14. Goodman, A.L., Merighi, M., Hyodo, M., Ventre, I., Filloux, A., and Lory, S. (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23: 249-259.
15. Hauser, A.R. (2009) The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol 7: 654-665.
16. Heurlier, K., Williams, F., Heeb, S., Dormond, C., Pessi, G., Singer, D., etal. (2004) Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186: 2936-2945.
17. Hoang, T.T., Karkhoff-Schweizer, R.A.R., Kutchma, A.J., and Schweizer, H.P. (1998) 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.
18. Hoang, T.T., Kutchma, A.J., Becher, A., and Schweizer, H.P. (2000) Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43: 59-72.
19. Hsu, J.L., Chen, H.C., Peng, H.L., and Chang, H.Y. (2008) Characterization of the histidine-containing phosphotransfer protein B-mediated multistep phosphorelay system in Pseudomonas aeruginosa PAO1. J Biol Chem 283: 9933-9944.
20. Irie, Y., Starkey, M., Edwards, A.N., Wozniak, D.J., Romeo, T., and Parsek, M.R. (2010) Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA. Mol Microbiol 78: 158-172.
21. Kay, E., Humair, B., Dénervaud, V., Riedel, K., Spahr, S., Eberl, L., etal. (2006) Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 188: 6026-6033.
22. Kulasekara, H.D., Ventre, I., Kulasekara, B.R., Lazdunski, A., Filloux, A., and Lory, S. (2005) A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol 55: 368-380.
23. Laskowski, M.A., and Kazmierczak, B.I. (2006) Mutational analysis of RetS, an unusual sensor kinase-response regulator hybrid required for Pseudomonas aeruginosa virulence. Infect Immun 74: 4462-4473.
24. Laskowski, M.A., Osborn, E., and Kazmierczak, B.I. (2004) A novel sensor kinase-response regulator hybrid regulates type III secretion and is required for virulence in Pseudomonas aeruginosa. Mol Microbiol 54: 1090-1103.
25. Liang, H., Li, L., Dong, Z., Surette, M.G., and Duan, K. (2008) The YebC family protein PA0964 negatively regulates the Pseudomonas aeruginosa quinolone signal system and pyocyanin production. J Bacteriol 190: 6217-6227.
26. Liang, H., Duan, J., Sibley, C.D., Surette, M.G., and Duan, K. (2011) Identification of mutants with altered phenazine production in Pseudomonas aeruginosa. J Med Microbiol 60: 22-34.
27. Lin, C.T., Huang, Y.J., Chu, P.H., Hsu, J.L., Huang, C.H., and Peng, H.L. (2006) Identification of an HptB-mediated multi-step phosphorelay in Pseudomonas aeruginosa PAO1. Res Microbiol 157: 169-175.
28. Lyczak, J.B., Cannon, C.L., and Pier, G.B. (2000) Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2: 1051-1060.
29. Lyczak, J.B., Cannon, C.L., and Pier, G.B. (2002) Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15: 194-222.
30. Mern, D.S., Ha, S.W., Khodaverdi, V., Gliese, N., and Gorisch, H. (2010) A complex regulatory network controls aerobic ethanol oxidation in Pseudomonas aeruginosa: indication of four levels of sensor kinases and response regulators. Microbiology 156: 1505-1516.
31. Mulcahy, H., O'Callaghan, J., O'Grady, E.P., Adams, C., and O'Gara, F. (2006) The posttranscriptional regulator RsmA plays a role in the interaction between Pseudomonas aeruginosa and human airway epithelial cells by positively regulating the type III secretion system. Infect Immun 74: 3012-3015.
32. O'Toole, G.A., and Kolter, R. (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28: 449-461.
33. Parsek, M.R., and Singh, P.K. (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57: 677-701.
34. Pessi, G., Williams, F., Hindle, Z., Heurlier, K., Holden, M.T.G., Camara, M., etal. (2001) The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 183: 6676-6683.
35. Petrova, O.E., and Sauer, K. (2009) A novel signaling network essential for regulating Pseudomonas aeruginosa biofilm development. PLoS Pathog 5: e1000668.
36. Petrova, O.E., and Sauer, K. (2011) SagS contributes to the motile-sessile switch and acts in concert with BfiSR to enable Pseudomonas aeruginosa biofilm formation. J Bacteriol 193: 6614-6628.
37. Poole, K., Neshat, S., Krebes, K., and Heinrichs, D.E. (1993) Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J Bacteriol 175: 4597-4604.
38. Rashid, M.H., and Kornberg, A. (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97: 4885-4890.
39. Schweizer, H.P. (1993) Two plasmids, X1918 and Z1918, for easy recovery of the xylE and lacZ reporter genes. Gene 134: 89-91.
40. Sibley, C.D., Duan, K., Fischer, C., Parkins, M.D., Storey, D.G., Rabin, H.R., and Surette, M.G. (2008) Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 4: e1000184.
41. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat Biotechnol 1: 784-791.
42. Ventre, I., Goodman, A.L., Vallet-Gely, I., Vasseur, P., Soscia, C., Molin, S., etal. (2006) Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci USA 103: 171-176.
43. Vincent, F., Round, A., Reynaud, A., Bordi, C., Filloux, A., and Bourne, Y. (2010) Distinct oligomeric forms of the Pseudomonas aeruginosa RetS sensor domain modulate accessibility to the ligand binding site. Environ Microbiol 12: 1775-1786.
44. Wagner, V.E., and Iglewski, B.H. (2008) P. aeruginosa biofilms in CF infection. Clin Rev Allergy Immunol 35: 124-134.
45. Winsor, G.L., Lam, D.K.W., Fleming, L., Lo, R., Whiteside, M.D., Nancy, Y.Y., etal. (2011) Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res 39: D596-D600.
46. Wolanin, P.M., Thomason, P.A., and Stock, J.B. (2002) Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol 3: 3013.
47. Zolfaghar, I., Angus, A.A., Kang, P.J., To, A., Evans, D.J., and Fleiszig, S.M.J. (2005) Mutation of retS, encoding a putative hybrid two-component regulatory protein in Pseudomonas aeruginosa, attenuates multiple virulence mechanisms. Microbes Infect 7: 1305-1316.