Antibiotic treatment of Pseudomonas aeruginosa biofilms stimulates expression of the magnesium transporter gene mgtE

Microbiology (United Kingdom)

Volumn 160, Issue PART 1, 2014, Pages 165-178

  Redelman, Carly V ^a,b   Chakravarty, Shubham ^a   Anderson, Gregory G ^a  

^a INDIANA UNIVERSITY   (United States)

^b BUTLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; AZITHROMYCIN; AZTREONAM; CARBENICILLIN; CEFTAZIDIME; CHLORAMPHENICOL; CIPROFLOXACIN; GENTAMICIN; IMIPENEM; KANAMYCIN; MAGNESIUM; NALIDIXIC ACID; POLYSACCHARIDE; TETRACYCLINE; TOBRAMYCIN;

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BIOFILM; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOTOXICITY; GENE ACTIVITY; GENE DELETION; GENE EXPRESSION; HUMAN; HUMAN CELL; MGTE GENE; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TYPE III SECRETION SYSTEM;

ANTI-BACTERIAL AGENTS; ANTIPORTERS; BACTERIAL PROTEINS; BIOFILMS; CELL LINE; CELL SURVIVAL; DNA TRANSPOSABLE ELEMENTS; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; HUMANS; MUTAGENESIS, INSERTIONAL; PSEUDOMONAS AERUGINOSA; REAL-TIME POLYMERASE CHAIN REACTION; TRANS-ACTIVATORS;

EID: 84891617997     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.070144-0     Document Type: Article

References (75)

1. Anderson, G. G., Moreau-Marquis, S., Stanton, B. A. & O'Toole, G. A. (2008). In vitro analysis of tobramycin-treated Pseudomonas aeruginosa biofilms on cystic fibrosis-derived airway epithelial cells. Infect Immun 76, 1423-1433.
2. Anderson, G. G., Yahr, T. L., Lovewell, R. R. & O'Toole, G. A. (2010). The Pseudomonas aeruginosa magnesium transporter MgtE inhibits transcription of the type III secretion system. Infect Immun 78, 1239-1249.
3. Aron, L., Toth, C., Godfrey, H. P. & Cabello, F. C. (1996). Identification and mapping of a chromosomal gene cluster of Borrelia burgdorferi containing genes expressed in vivo. FEMS Microbiol Lett 145, 309-314.
4. Badia, J. R., Soy, D., Adrover, M., Ferrer, M., Sarasa, M., Alarcón, A., Codina, C. & Torres, A. (2004). Disposition of instilled versus nebulized tobramycin and imipenem in ventilated intensive care unit (ICU) patients. J Antimicrob Chemother 54, 508-514.
5. Bagge, N., Schuster, M., Hentzer, M., Ciofu, O., Givskov, M., Greenberg, E. P. & Høiby, N. (2004). Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and beta-lactamase and alginate production. Antimicrob Agents Chemother 48, 1175-1187.
6. Bleves, S., Soscia, C., Nogueira-Orlandi, P., Lazdunski, A. & Filloux, A. (2005). Quorum sensing negatively controls type III secretion regulon expression in Pseudomonas aeruginosa PAO1. J Bacteriol 187, 3898-3902.
7. Boucher, R. C. (2002). An overview of the pathogenesis of cystic fibrosis lung disease. Adv Drug Deliv Rev 54, 1359-1371.
8. Bruscia, E., Sangiuolo, F., Sinibaldi, P., Goncz, K. K., Novelli, G. & Gruenert, D. C. (2002). Isolation of CF cell lines corrected at DF508-CFTR locus by SFHR-mediated targeting. Gene Ther 9, 683-685.
9. Caiazza, N. C. & O'Toole, G. A. (2004). SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J Bacteriol 186, 4476-4485.
10. Caiazza, N. C., Shanks, R. M. & O'Toole, G. A. (2005). Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187, 7351-7361.
11. Campodónico, V. L., Gadjeva, M., Paradis-Bleau, C., Uluer, A. & Pier, G. B. (2008). Airway epithelial control of Pseudomonas aeruginosa infection in cystic fibrosis. Trends Mol Med 14, 120-133.
12. Coggan, K. A. & Wolfgang, M. C. (2012). Global regulatory pathways and cross-talk control Pseudomonas aeruginosa environmental lifestyle and virulence phenotype. Curr Issues Mol Biol 14, 47-70.
13. Cozens, A. L., Yezzi, M. J., Kunzelmann, K., Ohrui, T., Chin, L., Eng, K., Finkbeiner, W. E., Widdicombe, J. H. & Gruenert, D. C. (1994). CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 10, 38-47.
14. 2+ and host cell contact proceeds through two distinct signaling pathways. Infect Immun 74, 3334-3341.
15. Diaz, M. R., King, J. M. & Yahr, T. L. (2011). Intrinsic and extrinsic regulation of type III secretion gene expression in Pseudomonas aeruginosa. Front Microbiol 2, 89.
16. Emerson, J., Rosenfeld, M., McNamara, S., Ramsey, B. & Gibson, R. L. (2002). Pseudomonas aeruginosa and other predictors of mortality and morbidity in young children with cystic fibrosis. Pediatr Pulmonol 34, 91-100.
17. Gangell, C., Gard, S., Douglas, T., Park, J., de Klerk, N., Keil, T., Brennan, S., Ranganathan, S., Robins-Browne, R. & other authors (2011). Inflammatory responses to individual microorganisms in the lungs of children with cystic fibrosis. Clin Infect Dis 53, 425-432.
18. Geller, D. E., Pitlick, W. H., Nardella, P. A., Tracewell, W. G. & Ramsey, B. W. (2002). Pharmacokinetics and bioavailability of aerosolized tobramycin in cystic fibrosis. Chest 122, 219-226.
19. Gibson, R. L., Burns, J. L. & Ramsey, B. W. (2003). Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med 168, 918-951.
20. Gooderham, W. J. & Hancock, R. E. (2009). Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol Rev 33, 279-294.
21. Goodman, A. L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R. S. & Lory, S. (2004). A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7, 745-754.
22. Goodman, A. L., Merighi, M., Hyodo, M., Ventre, I., Filloux, A. & Lory, S. (2009). Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23, 249-259.
23. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2, 95-108.
24. Hoboth, C., Hoffmann, R., Eichner, A., Henke, C., Schmoldt, S., Imhof, A., Heesemann, J. & Hogardt, M. (2009). Dynamics of adaptive microevolution of hypermutable Pseudomonas aeruginosa during chronic pulmonary infection in patients with cystic fibrosis. J Infect Dis 200, 118-130.
25. Hoffman, L. R., D'Argenio, D. A., MacCoss, M. J., Zhang, Z., Jones, R. A. & Miller, S. I. (2005). Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436, 1171-1175.
26. Ilowite, J. S., Gorvoy, J. D. & Smaldone, G. C. (1987). Quantitative deposition of aerosolized gentamicin in cystic fibrosis. Am Rev Respir Dis 136, 1445-1449.
27. Kakuda, T. & DiRita, V. J. (2006). Cj1496c encodes a Campylobacter jejuni glycoprotein that influences invasion of human epithelial cells and colonization of the chick gastrointestinal tract. Infect Immun 74, 4715-4723.
28. Khan, W., Bernier, S. P., Kuchma, S. L., Hammond, J. H., Hasan, F. & O'Toole, G. A. (2010). Aminoglycoside resistance of Pseudomonas aeruginosa biofilms modulated by extracellular polysaccharide. Int Microbiol 13, 207-212.
29. Kobayashi, H. (1995). Biofilm disease: its clinical manifestation and therapeutic possibilities of macrolides. Am J Med 99, 26S-30S.
30. Kuchma, S. L., Connolly, J. P. & O'Toole, G. A. (2005). A threecomponent regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa. J Bacteriol 187, 1441-1454.
31. Kulasekara, H. D., Ventre, I., Kulasekara, B. R., Lazdunski, A., Filloux, A. & Lory, S. (2005). A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol 55, 368-380.
32. Laskowski, M. A., Osborn, E. & 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.
33. Liberati, N. T., Urbach, J. M., Miyata, S., Lee, D. G., Drenkard, E., Wu, G., Villanueva, J., Wei, T. & Ausubel, F. M. (2006). An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci U S A 103, 2833-2838.
34. Linares, J. F., Gustafsson, I., Baquero, F. & Martinez, J. L. (2006). Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci U S A 103, 19484-19489.
35. Lizewski, S. E., Lundberg, D. S. & Schurr, M. J. (2002). The transcriptional regulator AlgR is essential for Pseudomonas aeruginosa pathogenesis. Infect Immun 70, 6083-6093.
36. Lizewski, S. E., Schurr, J. R., Jackson, D. W., Frisk, A., Carterson, A. J. & Schurr, M. J. (2004). Identification of AlgR-regulated genes in Pseudomonas aeruginosa by use of microarray analysis. J Bacteriol 186, 5672-5684.
37. MacGregor, R. R., Gibson, G. A. & Bland, J. A. (1986). Imipenem pharmacokinetics and body fluid concentrations in patients receiving high-dose treatment for serious infections. Antimicrob Agents Chemother 29, 188-192.
38. Mah, T. F. & O'Toole, G. A. (2001). Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9, 34-39.
39. 22 for expression of the alginate regulon in Pseudomonas aeruginosa and localization of its antagonist proteins MucA and MucB (AlgN). J Bacteriol 179, 3711-3720.
40. McCaw, M. L., Lykken, G. L., Singh, P. K. & Yahr, T. L. (2002). ExsD is a negative regulator of the Pseudomonas aeruginosa type III secretion regulon. Mol Microbiol 46, 1123-1133.
41. McCoy, K. S., Quittner, A. L., Oermann, C. M., Gibson, R. L., Retsch-Bogart, G. Z. & Montgomery, A. B. (2008). Inhaled aztreonam lysine for chronic airway Pseudomonas aeruginosa in cystic fibrosis. Am J Respir Crit Care Med 178, 921-928.
42. McPhee, J. B., Lewenza, S. & Hancock, R. E. (2003). Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol Microbiol 50, 205-217.
43. 2+-induced gene regulation in Pseudomonas aeruginosa. J Bacteriol 188, 3995-4006.
44. 2+ transport protein is involved in Aeromonas hydrophila adherence. FEMS Microbiol Lett 198, 189-195.
45. Miao, E. A., Freeman, J. A. & Miller, S. I. (2002). Transcription of the SsrAB regulon is repressed by alkaline pH and is independent of PhoPQ and magnesium concentration. J Bacteriol 184, 1493-1497.
46. Moreau-Marquis, S., O'Toole, G. A. & Stanton, B. A. (2009). Tobramycin and FDA-approved iron chelators eliminate Pseudomonas aeruginosa biofilms on cystic fibrosis cells. Am J Respir Cell Mol Biol 41, 305-313.
47. Moreau-Marquis, S., Redelman, C. V., Stanton, B. A. & Anderson, G. G. (2010). Co-culture models of Pseudomonas aeruginosa biofilms grown on live human airway cells. J Vis Exp 44, 2186.
48. Morici, L. A., Carterson, A. J., Wagner, V. E., Frisk, A., Schurr, J. R., Höner zu Bentrup, K., Hassett, D. J., Iglewski, B. H., Sauer, K. & Schurr, M. J. (2007). Pseudomonas aeruginosa AlgR represses the Rhl quorum-sensing system in a biofilm-specific manner. J Bacteriol 189, 7752-7764.
49. Mueller, R. S., McDougald, D., Cusumano, D., Sodhi, N., Kjelleberg, S., Azam, F. & Bartlett, D. H. (2007). Vibrio cholerae strains possess multiple strategies for abiotic and biotic surface colonization. J Bacteriol 189, 5348-5360.
50. Rahme, L. G., Stevens, E. J., Wolfort, S. F., Shao, J., Tompkins, R. G. & Ausubel, F. M. (1995). Common virulence factors for bacterial pathogenicity in plants and animals. Science 268, 1899-1902.
51. Rau, M. H., Hansen, S. K., Johansen, H. K., Thomsen, L. E., Workman, C. T., Nielsen, K. F., Jelsbak, L., Høiby, N., Yang, L. & Molin, S. (2010). Early adaptive developments of Pseudomonas aeruginosa after the transition from life in the environment to persistent colonization in the airways of human cystic fibrosis hosts. Environ Microbiol 12, 1643-1658.
52. Riordan, J. R., Rommens, J. M., Kerem, B., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic, N. & other authors (1989). Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245, 1066-1073.
53. Rowen, D. W. & Deretic, V. (2000). Membrane-to-cytosol redistribution of ECF sigma factor AlgU and conversion to mucoidy in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Mol Microbiol 36, 314-327.
54. Sauer, K., Cullen, M. C., Rickard, A. H., Zeef, L. A., Davies, D. G. & Gilbert, P. (2004). Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186, 7312-7326.
55. Shanks, R. M., Caiazza, N. C., Hinsa, S. M., Toutain, C. M. & O'Toole, G. A. (2006). Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl Environ Microbiol 72, 5027-5036.
56. Siegmund, I. & Wagner, F. (1991). New method for detecting rhamnolipids excreted by Pseudomonas species during growth on mineral agar. Biotechnol Tech 5, 265-268.
57. Simon, R., Priefer, U. & 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.
58. Skindersoe, M. E., Alhede, M., Phipps, R., Yang, L., Jensen, P. O., Rasmussen, T. B., Bjarnsholt, T., Tolker-Nielsen, T., Høiby, N. & Givskov, M. (2008). Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 52, 3648-3663.
59. Strandvik, B., Malmborg, A. S., Alfredson, H. & Ericsson, A. (1983). Clinical results and pharmacokinetics of ceftazidime treatment in patients with cystic fibrosis. J Antimicrob Chemother 12 (Suppl. A), 283-287.
60. Stutman, H. R., Shalit, I., Marks, M. I., Greenwood, R., Chartrand, S. A. & Hilman, B. C. (1987). Pharmacokinetics of two dosage regimens of ciprofloxacin during a two-week therapeutic trial in patients with cystic fibrosis. Am J Med 82, 142-145.
61. Swiatecka-Urban, A., Brown, A., Moreau-Marquis, S., Renuka, J., Coutermarsh, B., Barnaby, R., Karlson, K. H., Flotte, T. R., Fukuda, M. & other authors (2005). The short apical membrane half-life of rescued DF508-cystic fibrosis transmembrane conductance regulator (CFTR) results from accelerated endocytosis of DF508-CFTR in polarized human airway epithelial cells. J Biol Chem 280, 36762-36772.
62. Tolker-Nielsen, T., Brinch, U. C., Ragas, P. C., Andersen, J. B., Jacobsen, C. S. & Molin, S. (2000). Development and dynamics of Pseudomonas sp. biofilms. J Bacteriol 182, 6482-6489.
63. Trautmann, M., Lepper, P. M. & Haller, M. (2005). Ecology of Pseudomonas aeruginosa in the intensive care unit and the evolving role of water outlets as a reservoir of the organism. Am J Infect Control 33 (Suppl. 1), S41-S49.
64. Tuomanen, E., Cozens, R., Tosch, W., Zak, O. & Tomasz, A. (1986). The rate of killing of Escherichia coli by b-lactam antibiotics is strictly proportional to the rate of bacterial growth. J Gen Microbiol 132, 1297-1304.
65. Twiss, J., Byrnes, C., Johnson, R. & Holland, D. (2005). Nebulised gentamicin-suitable for childhood bronchiectasis. Int J Pharm 295, 113-119.
66. van Delden, C., Comte, R. & Bally, A. M. (2001). Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. J Bacteriol 183, 5376-5384.
67. Warwick, G. & Elston, C. (2011). Improving outcomes in patients with cystic fibrosis. Practitioner 255, 29-32, 3.
68. Whitchurch, C. B., Alm, R. A. & Mattick, J. S. (1996). The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 93, 9839-9843.
69. Wilms, E. B., Touw, D. J. & Heijerman, H. G. (2008). Pharmacokinetics and sputum penetration of azithromycin during once weekly dosing in cystic fibrosis patients. J Cyst Fibros 7, 79-84.
70. Wingender, J. & Flemming, H. C. (2011). Biofilms in drinking water and their role as reservoir for pathogens. Int J Hyg Environ Health 214, 417-423.
71. 22 (AlgT) and the AlgW and Prc proteases. Mol Microbiol 62, 412-426.
72. Worlitzsch, D., Tarran, R., Ulrich, M., Schwab, U., Cekici, A., Meyer, K. C., Birrer, P., Bellon, G., Berger, J. & other authors (2002). Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109, 317-325.
73. Wu, W., Badrane, H., Arora, S., Baker, H. V. & Jin, S. (2004). MucAmediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. J Bacteriol 186, 7575-7585.
74. Yahr, T. L. & Wolfgang, M. C. (2006). Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol Microbiol 62, 631-640.
75. Yu, H., Mudd, M., Boucher, J. C., Schurr, M. J. & Deretic, V. (1997). Identification of the algZ gene upstream of the response regulator algR and its participation in control of alginate production in Pseudomonas aeruginosa. J Bacteriol 179, 187-193.