Vfr directly activates exsA transcription to regulate expression of the Pseudomonas aeruginosa type III secretion system

Journal of Bacteriology

Volumn 198, Issue 9, 2016, Pages 1442-1450

  Marsden, Anne E ^a   Intile, Peter J ^a   Schulmeyer, Kayley H ^a   Simmons Patterson, Ethan R ^a   Urbanowski, Mark L ^a   Wolfgang, Matthew C ^b   Yahr, Timothy L ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRULENCE FACTOR; BACTERIAL PROTEIN; CYCLIC AMP BINDING PROTEIN; DNA BINDING PROTEIN; EXSA PROTEIN, PSEUDOMONAS AERUGINOSA; HYBRID PROTEIN; PROTEIN BINDING; TRANSACTIVATOR PROTEIN; TYPE III SECRETION SYSTEM; VFR PROTEIN, PSEUDOMONAS AERUGINOSA;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CULTURE; DNA FOOTPRINTING; EXSA GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; NONHUMAN; PHENOTYPE; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PSEUDOMONAS AERUGINOSA; TRANSCRIPTION INITIATION; TYPE III SECRETION SYSTEM; GEL MOBILITY SHIFT ASSAY; GENETICS; METABOLISM; OPERON;

BACTERIAL PROTEINS; CYCLIC AMP RECEPTOR PROTEIN; DNA FOOTPRINTING; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; OPERON; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; RECOMBINANT FUSION PROTEINS; TRANS-ACTIVATORS; TYPE III SECRETION SYSTEMS; VIRULENCE FACTORS;

EID: 84964969800     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00049-16     Document Type: Article

References (36)

1. Gaynes R, Edwards JR, National Nosocomial Infections Surveillance System. 2005. Overview of nosocomial infections caused by gramnegative bacilli. Clin Infect Dis 41:848-854. http://dx.doi.org/10.1086/432803.
2. Pendleton JN, Gorman SP, Gilmore BF. 2013. Clinical relevance of the ESKAPE pathogens. Expert Rev Anti Infect Ther 11:297-308. http://dx.doi.org/10.1586/eri.13.12.
3. Turner KH, Everett J, Trivedi U, Rumbaugh KP, Whiteley M. 2014. Requirements for Pseudomonas aeruginosa acute burn and chronic surgical wound infection. PLoS Genet 10:e1004518. http://dx.doi.org/10.1371/journal.pgen.1004518.
4. Wurtzel O, Yoder-Himes DR, Han K, Dandekar AA, Edelheit S, Greenberg EP, Sorek R, Lory S. 2012. The single-nucleotide resolution transcriptome of Pseudomonas aeruginosa grown in body temperature. PLoS Pathog 8:e1002945. http://dx.doi.org/10.1371/journal.ppat.1002945.
5. Vasil ML. 2007. How we learnt about iron acquisition in Pseudomonas aeruginosa: a series of very fortunate events. Biometals 20:587-601. http://dx.doi.org/10.1007/s10534-006-9067-2.
6. Koh AY, Mikkelsen PJ, Smith RS, Coggshall KT, Kamei A, Givskov M, Lory S, Pier GB. 2010. Utility of in vivo transcription profiling for identifying Pseudomonas aeruginosa genes needed for gastrointestinal colonization and dissemination. PLoS One 5:e15131. http://dx.doi.org/10.1371/journal.pone.0015131.
7. Chugani S, Greenberg EP. 2007. The influence of human respiratory epithelia on Pseudomonas aeruginosa gene expression. Microb Pathog 42:29-35. http://dx.doi.org/10.1016/j.micpath.2006.10.004.
8. Frisk A, Schurr JR, Wang G, Bertucci DC, Marrero L, Hwang SH, Hassett DJ, Schurr MJ. 2004. Transcriptome analysis of Pseudomonas aeruginosa after interaction with human airway epithelial cells. Infect Immun 72:5433-5438. http://dx.doi.org/10.1128/IAI.72.9.5433-5438.2004.
9. Wolfgang MC, Lee VT, Gilmore ME, Lory S. 2003. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell 4:253-263. http://dx.doi.org/10.1016/S1534-5807(03)00019-4.
10. Coggan KA, Wolfgang MC. 2012. Global regulatory pathways and crosstalk control Pseudomonas aeruginosa environmental lifestyle and virulence phenotype. Curr Issues Mol Biol 14:47-70.
11. Fuchs EL, Brutinel ED, Klem ER, Fehr AR, Yahr TL, Wolfgang MC. 2010. In vitro and in vivo characterization of the Pseudomonas aeruginosa cyclicAMP(cAMP) phosphodiesterase CpdA, required forcAMPhomeostasis and virulence factor regulation. J Bacteriol 192:2779-2790. http://dx.doi.org/10.1128/JB.00168-10.
12. West SE, Sample AK, Runyen-Janecky LJ. 1994. The Vfr gene product, required for Pseudomonas aeruginosa exotoxin A and protease production, belongs to the cyclic AMP receptor protein family. J Bacteriol 176:7532-7542.
13. Fuchs EL, Brutinel ED, Jones AK, Fulcher NB, Urbanowski ML, Yahr TL, Wolfgang MC. 2010. The Pseudomonas aeruginosa Vfr regulator controls global virulence factor expression through cyclic AMP-dependent and -independent mechanisms. J Bacteriol 192:3553-3564. http://dx.doi.org/10.1128/JB.00363-10.
14. Jones AK, Fulcher NB, Balzer GJ, Urbanowski ML, Pritchett CL, Schurr MJ, Yahr TL, Wolfgang MC. 2010. Activation of the Pseudomonas aeruginosa AlgU regulon through mucA mutation inhibits cyclic AMP/Vfr signaling. J Bacteriol 192:5709-5717. http://dx.doi.org/10.1128/JB.00526-10.
15. Hauser AR. 2009. The type III secretion system of Pseudomonas aeruginosa:infection by injection. Nat Rev Microbiol 7:654-665. http://dx.doi.org/10.1038/nrmicro2199.
16. Brutinel ED, Vakulskas CA, Brady KM, Yahr TL. 2008. Characterization of ExsA and of ExsA-dependent promoters required for expression of the Pseudomonas aeruginosa type III secretion system. Mol Microbiol 68:657-671. http://dx.doi.org/10.1111/j.1365-2958.2008.06179.x.
17. Hovey AK, Frank DW. 1995. Analyses of the DNA-binding and transcriptional activation properties of ExsA, the transcriptional activator of the Pseudomonas aeruginosa exoenzyme S regulon. J Bacteriol 177:4427-4436.
18. Diaz MR, King JM, Yahr TL. 2011. Intrinsic and extrinsic regulation of type III secretion gene expression in Pseudomonas Aeruginosa. Front Microbiol 2:89.
19. Yahr TL, Frank DW. 1994. Transcriptional organization of the transregulatory locus which controls exoenzyme S synthesis in Pseudomonas aeruginosa. J Bacteriol 176:3832-3838.
20. Brutinel ED, Yahr TL. 2008. Control of gene expression by type III secretory activity. Curr Opin Microbiol 11:128-133. http://dx.doi.org/10.1016/j.mib.2008.02.010.
21. McCaw ML, Lykken GL, Singh PK, Yahr TL. 2002. ExsD is a negative regulator of the Pseudomonas aeruginosa type III secretion regulon. Mol Microbiol 46:1123-1133. http://dx.doi.org/10.1046/j.1365-2958.2002.03228.x.
22. Dasgupta N, Lykken GL, Wolfgang MC, Yahr TL. 2004. A novel antianti-activator mechanism regulates expression of the Pseudomonas aeruginosa type III secretion system. Mol Microbiol 53:297-308. http://dx.doi.org/10.1111/j.1365-2958.2004.04128.x.
23. Rietsch A, Mekalanos JJ. 2006. Metabolic regulation of type III secretion gene expression in Pseudomonas aeruginosa. Mol Microbiol 59:807-820. http://dx.doi.org/10.1111/j.1365-2958.2005.04990.x.
24. Brutinel ED, Vakulskas CA, Yahr TL. 2010. ExsD inhibits expression of the Pseudomonas aeruginosa type III secretion system by disrupting ExsA self-association and DNA binding activity. J Bacteriol 192:1479-1486. http://dx.doi.org/10.1128/JB.01457-09.
25. Rietsch A, Vallet-Gely I, Dove SL, Mekalanos JJ. 2005. ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 102:8006-8011. http://dx.doi.org/10.1073/pnas.0503005102.
26. Urbanowski ML, Lykken GL, Yahr TL. 2005. A secreted regulatory protein couples transcription to the secretory activity of the Pseudomonas aeruginosa type III secretion system. Proc Natl Acad Sci U S A 102:9930-9935. http://dx.doi.org/10.1073/pnas.0504405102.
27. Zheng Z, Chen G, Joshi S, Brutinel ED, Yahr TL, Chen L. 2007. Biochemical characterization of a regulatory cascade controlling transcription of the Pseudomonas aeruginosa type III secretion system. J Biol Chem 282:6136-6142.
28. Urbanowski ML, Brutinel ED, Yahr TL. 2007. Translocation of ExsE into Chinese hamster ovary cells is required for transcriptional induction of the Pseudomonas aeruginosa type III secretion system. Infect Immun 75:4432-4439. http://dx.doi.org/10.1128/IAI.00664-07.
29. Hornef MW, Roggenkamp A, Geiger AM, Hogardt M, Jacobi CA, Heesemann J. 2000. Triggering the ExoS regulon of Pseudomonas aeruginosa:a GFP-reporter analysis of exoenzyme (Exo) S, ExoT, and ExoU synthesis. Microb Pathog 29:329-343. http://dx.doi.org/10.1006/mpat.2000.0398.
30. Dubnau D, Losick R. 2006. Bistability in bacteria. Mol Microbiol 61:564-572. http://dx.doi.org/10.1111/j.1365-2958.05249.x.
31. Hoang TT, Kutchma AJ, Becher A, Schweizer HP. 2000. Integrationproficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43:59-72. http://dx.doi.org/10.1006/plas.1999.1441.
32. Fulcher NB, Holliday PM, Klem E, Cann MJ, Wolfgang MC. 2010. The Pseudomonas aeruginosa Chp chemosensory system regulates intracellular cAMP levels by modulating adenylate cyclase activity. Mol Microbiol 76:889-904. http://dx.doi.org/10.1111/j.1365-2958.2010.07135.x.
33. Kanack KJ, Runyen-Janecky LJ, Ferrell EP, Suh SJ, West SE. 2006. Characterization of DNA-binding specificity and analysis of binding sites of the Pseudomonas aeruginosa global regulator, Vfr, a homologue of the Escherichia coli cAMP receptor protein. Microbiology 152:3485-3496. http://dx.doi.org/10.1099/mic.0.29008-0.
34. Liang H, Deng X, Li X, Ye Y, Wu M. 2014. Molecular mechanisms of master regulator VqsM mediating quorum-sensing and antibiotic resistance in Pseudomonas aeruginosa. Nucleic Acids Res 42:10307-10320. http://dx.doi.org/10.1093/nar/gku586.
35. Intile PJ, Balzer GJ, Wolfgang MC, Yahr TL. 2015. The RNA helicase DeaD stimulates ExsA translation to promote expression of the Pseudomonas aeruginosa type III secretion system. J Bacteriol 197:2664-2674. http://dx.doi.org/10.1128/JB.00231-15.
36. Intile PJ, Diaz MR, Urbanowski ML, Wolfgang MC, Yahr TL. 2014. The AlgZR two-component system recalibrates the RsmAYZ posttranscriptional regulatory system to inhibit expression of the Pseudomonas aeruginosa type III secretion system. J Bacteriol 196:357-366. http://dx.doi.org/10.1128/JB.01199-13.