Pseudomonas Aeruginosa diversification during infection development in cystic fibrosis Lungs-A review

Pathogens

Volumn 3, Issue 3, 2014, Pages 680-703

  Sousa, Ana Margarida ^a   Pereira, Maria Olívia ^a  

^a UNIVERSITY OF MINHO   (Portugal)

Author keywords

Clonal diversification; Cystic fibrosis; Mucoid phenotype; Phenotypic variation; Pseudomonas aeruginosa

Indexed keywords

N ACYLHOMOSERINE LACTONE;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL THERAPY; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM DETECTION; BACTERIUM ISOLATE; BIOFILM; CYSTIC FIBROSIS; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE MUTATION; GENETIC HETEROGENEITY; GENOTYPE ENVIRONMENT INTERACTION; GENOTYPE PHENOTYPE CORRELATION; HOST PATHOGEN INTERACTION; MICROBIAL DIVERSITY; NONHUMAN; PHENOTYPIC VARIATION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; REVIEW; TRANSCRIPTION REGULATION;

EID: 84929049801     PISSN: None     EISSN: 20760817     Source Type: Journal    
DOI: 10.3390/pathogens3030680     Document Type: Review

References (136)

1. Kreda, S.M.; Davis, C.W.; Rose, M.C. CFTR, mucins, and mucus obstruction in cystic fibrosis. Cold Spring Harb. Perspect. Med. 2012, 2, a009589.
2. Folkesson, A.; Jelsbak, L.; Yang, L.; Johansen, H.K.; Ciofu, O.; Hoiby, N.; Molin, S. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: An evolutionary perspective. Nat. Rev. Microbiol. 2012, 10, 841-851.
3. Ratjen, F.A. Cystic fibrosis: Pathogenesis and future treatment strategies. Respir. Care 2009, 54, 595-605.
4. Lubamba, B.; Dhooghe, B.; Noel, S.; Leal, T. Cystic fibrosis: Insight into CFTR pathophysiology and pharmacotherapy. Clin. Biochem. 2012, 45, 1132-1144.
5. Rubenstein, R.C. Targeted therapy for cystic fibrosis: Cystic fibrosis transmembrane conductance regulator mutation-specific pharmacologic strategies. Mol. Diagn. Ther. 2006, 10, 293-301.
6. Gomez, M.I.; Prince, A. Opportunistic infections in lung disease: Pseudomonas infections in cystic fibrosis. Curr. Opin. Pharmacol. 2007, 7, 244-251.
7. Palmer, K.L.; Mashburn, L.M.; Singh, P.K.; Whiteley, M. Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J. Bacteriol. 2005, 187, 5267-5277.
8. Sriramulu, D.D.; Lunsdorf, H.; Lam, J.S.; Romling, U. Microcolony formation: A novel biofilm model of Pseudomonas aeruginosa for the cystic fibrosis lung. J. Med. Microbiol. 2005, 54, 667-676.
9. Schobert, M.; Jahn, D. Anaerobic physiology of Pseudomonas aeruginosa in the cystic fibrosis lung. Int. J. Med. Microbiol. IJMM 2010, 300, 549-556.
10. Bittar, F.; Richet, H.; Dubus, J.C.; Reynaud-Gaubert, M.; Stremler, N.; Sarles, J.; Raoult, D.; Rolain, J.M. Molecular detection of multiple emerging pathogens in sputa from cystic fibrosis patients. PLoS One 2008, 3, e2908.
11. Cystic Fibrosis Foundation. Patient Registry 2011 Annual Report; Cystic Fibrosis Foundation: Bethesda, MD, USA, 2011.
12. Narasimhan, M.; Cohen, R. New and investigational treatments in cystic fibrosis. Ther. Adv. Respir. Dis. 2011, 5, 275-282.
13. Jain, K.; Smyth, A.R. Current dilemmas in antimicrobial therapy in cystic fibrosis. Exp. Rev. Respir. Med. 2012, 6, 407-422.
14. Döring, G.; Flume, P.; Heijerman, H.; Elborn, J.S. Treatment of lung infection in patients with cystic fibrosis: Current and future strategies. J. Cyst. Fibros. 2012, 11, 461-479.
15. Ryan, G.; Singh, M.; Dwan, K. Inhaled antibiotics for long-term therapy in cystic fibrosis. Cochrane Database Syst. Rev. 2011, 16, CD001021.
16. Sawicki, G.S.; Signorovitch, J.E.; Zhang, J.; Latremouille-Viau, D.; von Wartburg, M.; Wu, E.Q.; Shi, L. Reduced mortality in cystic fibrosis patients treated with tobramycin inhalation solution. Pediatr. Pulmonol. 2012, 47, 44-52.
17. Ratjen, F.; Munck, A.; Kho, P.; Angyalosi, G. Treatment of early Pseudomonas aeruginosa infection in patients with cystic fibrosis: The ELITE trial. Thorax 2010, 65, 286-291.
18. Zobell, J.T.; Waters, C.D.; Young, D.C.; Stockmann, C.; Ampofo, K.; Sherwin, C.M.; Spigarelli, M.G. Optimization of anti-pseudomonal antibiotics for cystic fibrosis pulmonary exacerbations: I.I. cephalosporins and penicillins. Pediatr. Pulmonol. 2013, 48, 107-122.
19. Coutinho, H.D.; Falcao-Silva, V.S.; Goncalves, G.F. Pulmonary bacterial pathogens in cystic fibrosis patients and antibiotic therapy: A tool for the health workers. Int. Arch. Med. 2008, 1, 24.
20. Silby, M.W.; Winstanley, C.; Godfrey, S.A.; Levy, S.B.; Jackson, R.W. Pseudomonas genomes: Diverse and adaptable. FEMS Microbiol. Rev. 2011, 35, 652-680.
21. Rau, M.H.; Hansen, S.K.; Johansen, H.K.; Thomsen, L.E.; Workman, C.T.; Nielsen, K.F.; Jelsbak, L.; Hoiby, N.; Yang, L.; Molin, S. 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. 2010, 12, 1643-1658.
22. Hoiby, N.; Ciofu, O.; Bjarnsholt, T. Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol. 2010, 5, 1663-1674.
23. Hogardt, M.; Heesemann, J. Adaptation of Pseudomonas aeruginosa during persistence in the cystic fibrosis lung. Int. J. Med. Microbiol. 2010, 300, 557-562.
24. Schelstraete, P.; Haerynck, F.; van Daele, S.; Deseyne, S.; de Baets, F. Eradication therapy for Pseudomonas aeruginosa colonization episodes in cystic fibrosis patients not chronically colonized by P. aeruginosa. J. Cyst. Fibros. 2013, 12, 1-8.
25. Bragonzi, A.; Paroni, M.; Nonis, A.; Cramer, N.; Montanari, S.; Rejman, J.; di Serio, C.; Doring, G.; Tummler, B. Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am. J. Respir. Crit. Care Med. 2009, 180, 138-145.
26. Wright, E.A.; Fothergill, J.L.; Paterson, S.; Brockhurst, M.A.; Winstanley, C. Sub-inhibitory concentrations of some antibiotics can drive diversification of Pseudomonas aeruginosa populations in artificial sputum medium. BMC Microbiol. 2013, 13, 170.
27. Ciofu, O.; Mandsberg, L.F.; Wang, H.; Hoiby, N. Phenotypes selected during chronic lung infection in cystic fibrosis patients: Implications for the treatment of Pseudomonas aeruginosa biofilm infections. FEMS Immunol. Med. Microbiol. 2012, 65, 215-225.
28. Huse, H.K.; Kwon, T.; Zlosnik, J.E.; Speert, D.P.; Marcotte, E.M.; Whiteley, M. Parallel evolution in Pseudomonas aeruginosa over 39,000 generations in vivo. mBio 2010, doi:10.1128/mBio.00199-10.
29. Lieberman, T.D.; Michel, J.B.; Aingaran, M.; Potter-Bynoe, G.; Roux, D.; Davis, M.R.J.; Skurnik, D.; Leiby, N.; LiPuma, J.J.; Goldberg, J.J., et.al. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat. Genet. 2011, 43, 1275-1280.
30. Hassett, D.J.; Sutton, M.D.; Schurr, M.J.; Herr, A.B.; Caldwell, C.C.; Matu, J.O. Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol. 2009, 17, 130-138.
31. Bjarnsholt, T.; Jensen, P.O.; Fiandaca, M.J.; Pedersen, J.; Hansen, C.R.; Andersen, C.B.; Pressler, T.; Givskov, M.; Hoiby, N. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr. Pulmonol. 2009, 44, 547-558.
32. Worlitzsch, D.; Tarran, R.; Ulrich, M.; Schwab, U.; Cekici, A.; Meyer, K.C.; Birrer, P.; Bellon, G.; Berger, J.; Weiss, T., et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Investig. 2002, 109, 317-325.
33. Suh, J.D.; Ramakrishnan, V.; Palmer, J.N. Biofilms. Otolaryngol. Clin. N. Am. 2010, 43, 521-530.
34. Bjarnsholt, T.; Alhede, M.; Alhede, M.; Eickhardt-Sørensen, S.R.; Moser, C.; Kühl, M.; Jensen, P.Ø.; Høiby, N. The in vivo biofilm. Trends Microbiol. 2013, 21, 466-474.
35. Haussler, S. Multicellular signalling and growth of Pseudomonas aeruginosa. Int. J. Med. Microbiol. 2010, 300, 544-548.
36. Kostakioti, M.; Hadjifrangiskou, M.; Hultgren, S.J. Bacterial biofilms: Development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb. Perspect. Med. 2013, 3, a010306.
37. Davies, D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2003, 2, 114-122.
38. Høiby, N.; Bjarnsholt, T.; Givskov, M.; Molin, S.; Ciofu, O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 2010, 35, 322-332.
39. Mah, T.F. Biofilm-specific antibiotic resistance. Future Microbiol. 2012, 7, 1061-1072.
40. Nikolaev, Y.A.; Plakunov, V.K. Biofilm-City of microbes{norm of matrix} or an analogue of multicellular organisms? Microbiology 2007, 76, 125-138.
41. Hoffmann, N.; Rasmussen, T.B.; Jensen, P.O.; Stub, C.; Hentzer, M.; Molin, S.; Ciofu, O.; Givskov, M.; Johansen, H.K.; Hoiby, N. Novel mouse model of chronic Pseudomonas aeruginosa lung infection mimicking cystic fibrosis. Infect. Immun. 2005, 73, 2504-2514.
42. Harder, J.; Meyer-Hoffert, U.; Teran, L.M.; Schwichtenberg, L.; Bartels, J.; Maune, S.; Schroder, J.M. Mucoid Pseudomonas aeruginosa, TNF-alpha, and IL-1beta, but not IL-6, induce human beta-defensin-2 in respiratory epithelia. Am. J. Respirat. Cell Mol. Biol. 2000, 22, 714-721.
43. Goerke, C.; Wolz, C. Adaptation of Staphylococcus aureus to the cystic fibrosis lung. Int. J. Med. Microbiol. 2011, 300, 520-525.
44. Hassett, D.J.; Cuppoletti, J.; Trapnell, B.; Lymar, S.V.; Rowe, J.J.; Yoon, S.S.; Hilliard, G.M.; Parvatiyar, K.; Kamani, M.C.; Wozniak, D.J., et al. Anaerobic metabolism and quorum sensing by Pseudomonas aeruginosa biofilms in chronically infected cystic fibrosis airways: Rethinking antibiotic treatment strategies and drug targets. Adv. Drug Deliv. Rev. 2002, 54, 1425-1443.
45. Yoon, S.S.; Hennigan, R.F.; Hilliard, G.M.; Ochsner, U.A.; Parvatiyar, K.; Kamani, M.C.; Allen, H.L.; DeKievit, T.R.; Gardner, P.R.; Schwab, U., et al. Pseudomonas aeruginosa anaerobic respiration in biofilms: Relationships to cystic fibrosis pathogenesis. Dev. Cell 2002, 3, 593-603.
46. De la Fuente-Núñez, C.; Reffuveille, F.; Fernández, L.; Hancock, R.E.W. Bacterial biofilm development as a multicellular adaptation: Antibiotic resistance and new therapeutic strategies. Curr. Opin. Microbiol. 2013, 16, 580-589.
47. Sauer, K.; Camper, A.K.; Ehrlich, G.D.; Costerton, J.W.; Davies, D.G. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 2002, 184, 1140-1154.
48. Drenkard, E. Antimicrobial resistance of Pseudomonas aeruginosa biofilms. Microbes. infect./Inst. Pasteur. 2003, 5, 1213-1219.
49. Jouenne, T.; Vilain, S.; Cosette, P.; Junter, G.A. Proteomics of Biofilm Bacteria. Curr. Proteomics 2004, 1, 211-219.
50. Southey-Pillig, C.J.; Davies, D.G.; Sauer, K. Characterization of temporal protein production in Pseudomonas aeruginosa biofilms. J. Bacteriol. 2005, 187, 8114-8126.
51. Li, Y.H.; Tian, X. Quorum sensing and bacterial social interactions in biofilms. Sensors 2012, 12, 2519-2538.
52. Hassett, D.J.; Korfhagen, T.R.; Irvin, R.T.; Schurr, M.J.; Sauer, K.; Lau, G.W.; Sutton, M.D.; Yu, H.; Hoiby, N. Pseudomonas aeruginosa biofilm infections in cystic fibrosis: Insights into pathogenic processes and treatment strategies. Exp. Opin. Ther. Targets 2010, 14, 117-130.
53. Davies, D.G.; Parsek, M.R.; Pearson, J.P.; Iglewski, B.H.; Costerton, J.W.; Greenberg, E.P. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998, 280, 295-298.
54. Parkins, M.D.; Ceri, H.; Storey, D.G. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol. Microbiol. 2001, 40, 1215-1226.
55. O'Toole, G.A.; Gibbs, K.A.; Hager, P.W.; Phibbs, P.V.J.; Kolter, R. The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 2000, 182, 425-431.
56. Whitchurch, C.B.; Erova, T.E.; Emery, J.A.; Sargent, J.L.; Harris, J.M.; Semmler, A.B.; Young, M.D.; Mattick, J.S.; Wozniak, D.J. Phosphorylation of the Pseudomonas aeruginosa response regulator AlgR is essential for type IV fimbria-mediated twitching motility. J. Bacteriol. 2002, 184, 4544-4554.
57. Sousa, A.M.; Machado, I.; Nicolau, A.; Pereira, M.O. Improvements on colony morphology identification towards bacterial profiling. J. Microbiol. Methods 2013, 95, 327-335.
58. Kirov, S.M.; Webb, J.S.; O'May C.Y.; Reid, D.W.; Woo, J.K.; Rice, S.A.; Kjelleberg, S. Biofilm differentiation and dispersal in mucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 2007, 153, 3264-3274.
59. Boles, B.R.; Thoendel, M.; Singh, P.K. Self-generated diversity produces-insurance effects{norm of matrix} in biofilm communities. Proc. Natl. Acad. Sci. USA 2004, 101, 16630-16635.
60. Stewart, P.S.; Franklin, M.J. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 2008, 6, 199-210.
61. Parsek, M.R.; Greenberg, E.P. Sociomicrobiology: The connections between quorum sensing and biofilms. Trends Microbiol. 2005, 13, 27-33.
62. Sharma, G.; Rao, S.; Bansal, A.; Dang, S.; Gupta, S.; Gabrani, R. Pseudomonas aeruginosa biofilm: Potential therapeutic targets. Biologicals 2014, 42, 1-7.
63. Fux, C.A.; Costerton, J.W.; Stewart, P.S.; Stoodley, P. Survival strategies of infectious biofilms. Trends Microbiol. 2005, 13, 34-40.
64. Sauer, K.; Cullen, M.C.; Rickard, A.H.; Zeef, L.A.; Davies, D.G.; Gilbert, P. Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J. Bacteriol. 2004, 186, 7312-7326.
65. Woo, J.K.K.; Webb, J.S.; Kirov, S.M.; Kjelleberg, S.; Rice, S.A. Biofilm dispersal cells of a cystic fibrosis Pseudomonas aeruginosa isolate exhibit variability in functional traits likely to contribute to persistent infection. FEMS Immunol. Med. Microbiol. 2012, 66, 251-264.
66. Oliver, A.; Canton, R.; Campo, P.; Baquero, F.; Blazquez, J. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 2000, 288, 1251-1253.
67. Rodriguez-Rojas, A.; Oliver, A.; Blazquez, J. Intrinsic and environmental mutagenesis drive diversification and persistence of Pseudomonas aeruginosa in chronic lung infections. J. Infect. Dis. 2012, 205, 121-127.
68. Mena, A.; Smith, E.E.; Burns, J.L.; Speert, D.P.; Moskowitz, S.M.; Perez, J.L.; Oliver, A. Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J. Bacteriol. 2008, 190, 7910-7917.
69. Spiers, A.J.; Buckling, A.; Rainey, P.B. The causes of Pseudomonas diversity. Microbiology 2000, 146 Pt 10, 2345-2350.
70. Jolivet-Gougeon, A.; Kovacs, B.; le Gall-David, S.; le Bars, H.; Bousarghin, L.; Bonnaure-Mallet, M.; Lobel, B.; Guille, F.; Soussy, C.J.; Tenke, P. Bacterial hypermutation: Clinical implications. J. Med. Microbiol. 2011, 60, 563-573.
71. Ciofu, O.; Riis, B.; Pressler, T.; Poulsen, H.E.; Hoiby, N. Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. Antimicrob. Agents Chemother. 2005, 49, 2276-2282.
72. Kohanski, M.A.; DePristo, M.A.; Collins, J.J. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 2010, 37, 311-320.
73. Macia, M.D.; Blanquer, D.; Togores, B.; Sauleda, J.; Perez, J.L.; Oliver, A. Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob. Agents Chemother. 2005, 49, 3382-3386.
74. Ciofu, O.; Mandsberg, L.F.; Bjarnsholt, T.; Wassermann, T.; Hoiby, N. Genetic adaptation of Pseudomonas aeruginosa during chronic lung infection of patients with cystic fibrosis: Strong and weak mutators with heterogeneous genetic backgrounds emerge in mucA and/or lasR mutants. Microbiology 2010, 156, 1108-1119.
75. Driffield, K.; Miller, K.; Bostock, J.M.; O'Neill, A.J.; Chopra, I. Increased mutability of Pseudomonas aeruginosa in biofilms. J. Antimicrob. Chemother. 2008, 61, 1053-1056.
76. Lujan, A.M.; Macia, M.D.; Yang, L.; Molin, S.; Oliver, A.; Smania, A.M. Evolution and adaptation in Pseudomonas aeruginosa biofilms driven by mismatch repair system-deficient mutators. PLoS One 2011, 6, e27842.
77. Yachi, S.; Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis. Proc. Natl. Acad. Sci. USA 1999, 96, 1463-1468.
78. Hogardt, M.; Hoboth, C.; Schmoldt, S.; Henke, C.; Bader, L.; Heesemann, J. Stage-specific adaptation of hypermutable Pseudomonas aeruginosa isolates during chronic pulmonary infection in patients with cystic fibrosis. J. Infect. Dis. 2007, 195, 70-80.
79. Oliver, A.; Mena, A. Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin. Microbiol. Infect. 2010, 16, 798-808.
80. Hoboth, C.; Hoffmann, R.; Eichner, A.; Henke, C.; Schmoldt, S.; Imhof, A.; Heesemann, J.; Hogardt, M. Dynamics of adaptive microevolution of hypermutable Pseudomonas aeruginosa during chronic pulmonary infection in patients with cystic fibrosis. J. Infect. Dis. 2009, 200, 118-130.
81. Jiricny, N.; Molin, S.; Foster, K.; Diggle, S.P.; Scanlan, P.D.; Ghoul, M.; Johansen, H.K.; Santorelli, L.A.; Popat, R.; West, S.A., et al. Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis. PLoS One 2014, 9, e83124.
82. Workentine, M.L.; Sibley, C.D.; Glezerson, B.; Purighalla, S.; Norgaard-Gron, J.C.; Parkins, M.D.; Rabin, H.R.; Surette, M.G. Phenotypic heterogeneity of Pseudomonas aeruginosa populations in a cystic fibrosis patient. PLoS One 2013, 8, e60225.
83. Doring, G.; Conway, S.P.; Heijerman, H.G.; Hodson, M.E.; Hoiby, N.; Smyth, A.; Touw, D.J. Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: A European consensus. Eur. Respirat. J. 2000, 16, 749-767.
84. Manos, J.; Hu, H.; Rose, B.R.; Wainwright, C.E.; Zablotska, I.B.; Cheney, J.; Turnbull, L.; Whitchurch, C.B.; Grimwood, K., et al. Virulence factor expression patterns in Pseudomonas aeruginosa strains from infants with cystic fibrosis. Eur. J. Clin. Microbiol. Infect. Dis. 2013, 32, 1583-1592.
85. Burns, J.L.; Gibson, R.L.; McNamara, S.; Yim, D.; Emerson, J.; Rosenfeld, M.; Hiatt, P.; McCoy, K.; Castile, R.; Smith, A.L., et al. Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J. Infect. Dis. 2001, 183, 444-452.
86. Tramper-Stranders, G.A.; van der Ent, C.K.; Molin, S.; Yang, L.; Hansen, S.K.; Rau, M.H.; Ciofu, O.; Johansen, H.K.; Wolfs, T.F. Initial Pseudomonas aeruginosa infection in patients with cystic fibrosis: Characteristics of eradicated and persistent isolates. Clin. Microbiol. Infect. 2012, 18, 567-574.
87. Pacheco, G.J.; Reis, R.S.; Fernandes, A.C.; da Rocha, S.L.; Pereira, M.D.; Perales, J.; Freire, D.M. Rhamnolipid production: Effect of oxidative stress on virulence factors and proteome of Pseudomonas aeruginosa PA1. Appl. Microbiol. Biotechnol. 2012, 95, 1519-1529.
88. Abdel-Mawgoud, A.M.; Lepine, F.; Deziel, E. Rhamnolipids: Diversity of structures, microbial origins and roles. Appl. Microbiol. Biotechnol. 2010, 86, 1323-1336.
89. Montanari, S.; Oliver, A.; Salerno, P.; Mena, A.; Bertoni, G.; Tummler, B.; Cariani, L.; Conese, M.; Doring, G.; Bragonzi, A. Biological cost of hypermutation in Pseudomonas aeruginosa strains from patients with cystic fibrosis. Microbiol. Sgm 2007, 153, 1445-1454.
90. Hansen, S.K.; Rau, M.H.; Johansen, H.K.; Ciofu, O.; Jelsbak, L.; Yang, L.; Folkesson, A.; Jarmer, H.O.; Aanaes, K.; von Buchwald, C., et al. Evolution and diversification of Pseudomonas aeruginosa in the paranasal sinuses of cystic fibrosis children have implications for chronic lung infection. ISME J. 2012, 6, 31-45.
91. Berkhout, M.C.; Rijntjes, E.; el Bouazzaoui, L.H.; Fokkens, W.J.; Brimicombe, R.W.; Heijerman, H.G.M. Importance of bacteriology in upper airways of patients with Cystic Fibrosis. J. Cyst. Fibros. 2013, 12, 525-529.
92. Troxler, R.B.; Hoover, W.C.; Britton, L.J.; Gerwin, A.M.; Rowe, S.M. Clearance of initial mucoid Pseudomonas aeruginosa in patients with cystic fibrosis. Pediatr. Pulmonol. 2012, 47, 1113-1122.
93. Williams, B.J.; Dehnbostel, J.; Blackwell, T.S. Pseudomonas aeruginosa: Host defence in lung diseases. Respirology 2010, 15, 1037-1056.
94. Smith, E.E.; Buckley, D.G.; Wu, Z.; Saenphimmachak, C.; Hoffman, L.R.; D'Argenio, D.A.; Miller, S.I.; Ramsey, B.W.; Speert, D.P.; Moskowitz, S.M., et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 2006, 103, 8487-8492.
95. Döring, G.; Parameswaran, I.G.; Murphy, T.F. Differential adaptation of microbial pathogens to airways of patients with cystic fibrosis and chronic obstructive pulmonary disease. FEMS Microbiol. Rev. 2011, 35, 124-146.
96. Cramer, N.; Klockgether, J.; Wrasman, K.; Schmidt, M.; Davenport, C.F.; Tummler, B. Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ. Microbiol. 2011, 13, 1690-1704.
97. Qiu, D.; Eisinger, V.M.; Rowen, D.W.; Yu, H.D. Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 2007, 104, 8107-8112.
98. Govan, J.R.; Deretic, V. Microbial pathogenesis in cystic fibrosis: Mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 1996, 60, 539-574.
99. Deretic, V.; Schurr, M.J.; Yu, H. Pseudomonas aeruginosa, mucoidy and the chronic infection phenotype in cystic fibrosis. Trends Microbiol. 1995, 3, 351-356.
100. Ramsey, D.M.; Wozniak, D.J. Understanding the control of Pseudomonas aeruginosa alginate synthesis and the prospects for management of chronic infections in cystic fibrosis. Mol. Microbiol. 2005, 56, 309-322.
101. Martin, D.W.; Schurr, M.J.; Mudd, M.H.; Govan, J.R.; Holloway, B.W.; Deretic, V. Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 1993, 90, 8377-8381.
102. Wood, L.F.; Ohman, D.E. Identification of genes in the σ22 regulon of Pseudomonas aeruginosa required for cell envelope homeostasis in either the planktonic or the sessile mode of growth. mBio 2012, 3, e00094-12.
103. Wu, W.; Badrane, H.; Arora, S.; Baker, H.V.; Jin, S. MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. J. Bacteriol. 2004, 186, 7575-7585.
104. Bragonzi, A.; Wiehlmann, L.; Klockgether, J.; Cramer, N.; Worlitzsch, D.; Doring, G.; Tummler, B. Sequence diversity of the mucABD locus in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 2006, 152, 3261-3269.
105. Haussler, S.; Tummler, B.; Weissbrodt, H.; Rohde, M.; Steinmetz, I. Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin. Infect. Dis. 1999, 29, 621-625.
106. Haussler, S.; Ziegler, I.; Lottel, A.; von Gotz, F.; Rohde, M.; Wehmhohner, D.; Saravanamuthu, S.; Tummler, B.; Steinmetz, I. Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J. Med. Microbiol. 2003, 52, 295-301.
107. Haussler, S. Biofilm formation by the small colony variant phenotype of Pseudomonas aeruginosa. Environ. Microbiol. 2004, 6, 546-551.
108. Deziel, E.; Comeau, Y.; Villemur, R. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities 1. J. Bacteriol. 2001, 183, 1195-1204.
109. Kirisits, M.J.; Prost, L.; Starkey, M.; Parsek, M.R. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 2005, 71, 4809-4821.
110. Kahl, B.C. Small colony variants (SCVs) of Staphylococcus aureus-A bacterial survival strategy. Infect. Genet. Evol. 2014, 21, 515-522.
111. Starkey, M.; Hickman, J.H.; Ma, L.; Zhang, N.; de Long, S.; Hinz, A.; Palacios, S.; Manoil, C.; Kirisits, M.J.; Starner, T.D., et al. Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J. Bacteriol. 2009, 191, 3492-3503.
112. Tuchscherr, L.; Medina, E.; Hussain, M.; Volker, W.; Heitmann, V.; Niemann, S.; Holzinger, D.; Roth, J.; Proctor, R.A.; Becker, K., et al. Staphylococcus aureus phenotype switching: An effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol. Med. 2011, 3, 129-141.
113. Sendi, P.; Proctor, R.A. Staphylococcus aureus as an intracellular pathogen: The role of small colony variants. Trends Microbiol. 2009, 17, 54-58.
114. Proctor, R.A.; von Eiff, C.; Kahl, B.C.; Becker, K.; McNamara, P.; Herrmann, M.; Peters, G. Small colony variants: A pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat. Rev. Microbiol. 2006, 4, 295-305.
115. Willcox, M.D.; Zhu, H.; Conibear, T.C.; Hume, E.B.; Givskov, M.; Kjelleberg, S.; Rice, S.A. Role of quorum sensing by Pseudomonas aeruginosa in microbial keratitis and cystic fibrosis. Microbiology 2008, 154, 2184-2194.
116. Chang, Y.S.; Klockgether, J.; Tummler, B. An intragenic deletion in pilQ leads to nonpiliation of a Pseudomonas aeruginosa strain isolated from cystic fibrosis lung. FEMS Microbiol. Lett. 2007, 270, 201-206.
117. Kresse, A.U.; Dinesh, S.D.; Larbig, K.; Romling, U. Impact of large chromosomal inversions on the adaptation and evolution of Pseudomonas aeruginosa chronically colonizing cystic fibrosis lungs. Mol. Microbiol. 2003, 47, 145-158.
118. D'Argenio, D.A.; Wu, M.; Hoffman, L.R.; Kulasekara, H.D.; Deziel, E.; Smith, E.E.; Nguyen, H.; Ernst, R.K.; Larson Freeman, T.J.; Spencer, D.H., et al. Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol. Microbiol. 2007, 64, 512-533.
119. Schaber, J.A.; Carty, N.L.; McDonald, N.A.; Graham, E.D.; Cheluvappa, R.; Griswold, J.A.; Hamood, A.N. Analysis of quorum sensing-deficient clinical isolates of Pseudomonas aeruginosa. J. Med. Microbiol. 2004, 53, 841-853.
120. Frimmersdorf, E.; Horatzek, S.; Pelnikevich, A.; Wiehlmann, L.; Schomburg, D. How Pseudomonas aeruginosa adapts to various environments: A metabolomic approach. Environ. Microbiol. 2010, 12, 1734-1747.
121. Thomas, S.R.; Ray, A.; Hodson, M.E.; Pitt, T.L. Increased sputum amino acid concentrations and auxotrophy of Pseudomonas aeruginosa in severe cystic fibrosis lung disease. Thorax 2000, 55, 795-797.
122. Barth, A.L.; Pitt, T.L. Auxotrophic variants of Pseudomonas aeruginosa are selected from prototrophic wild-type strains in respiratory infections in patients with cystic fibrosis. J. Clin. Microbiol. 1995, 33, 37-40.
123. Mowat, E.; Paterson, S.; Fothergill, J.L.; Wright, E.A.; Ledson, M.J.; Walshaw, M.J.; Brockhurst, M.A.; Winstanley, C. Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am. J. Respir. Crit. Care Med. 2011, 183, 1674-1679.
124. Agarwal, G.; Kapil, A.; Kabra, S.K.; Das, B.K.; Dwivedi, S.N. Characterization of Pseudomonas aeruginosa isolated from chronically infected children with cystic fibrosis in India. BMC Microbiol. 2005, 5, 43.
125. Borriello, G.; Werner, E.; Roe, F.; Kim, A.M.; Ehrlich, G.D.; Stewart, P.S. Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 2004, 48, 2659-2664.
126. Field, T.R.; White, A.; Elborn, J.S.; Tunney, M.M. Effect of oxygen limitation on the in vitro antimicrobial susceptibility of clinical isolates of Pseudomonas aeruginosa grown planktonically and as biofilms. Eur.J. Clin. Microbiol. Infect. Dis. 2005, 24, 677-687.
127. Bragonzi, A.; Worlitzsch, D.; Pier, G.B.; Timpert, P.; Ulrich, M.; Hentzer, M.; Andersen, J.B.; Givskov, M.; Conese, M.; Doring, G. Nonmucoid Pseudomonas aeruginosa expresses alginate in the lungs of patients with cystic fibrosis and in a mouse model. J. Infect. Dis. 2005, 192, 410-419.
128. Boles, B.R.; Singh, P.K. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc. Natl. Acad. Sci. USA 2008, 105, 12503-12508.
129. Giwercman, B.; Meyer, C.; Lambert, P.A.; Reinert, C.; Hoiby, N. High-level beta-lactamase activity in sputum samples from cystic-fibrosis patients during antipseudomonal treatment. Antimicrob. Agents Chemother. 1992, 36, 71-76.
130. Jalal, S.; Ciofu, O.; Hoiby, N.; Gotoh, N.; Wretlind, B. Molecular mechanisms of fluoroquinolone resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob. Agents Chemother. 2000, 44, 710-712.
131. Johansen, H.K.; Moskowitz, S.M.; Ciofu, O.; Pressler, T.; Høiby, N. Spread of colistin resistant non-mucoid Pseudomonas aeruginosa among chronically infected Danish cystic fibrosis patients. J. Cyst. Fibros. 2008, 7, 391-397.
132. Islam, S.; Oh, H.; Jalal, S.; Karpati, F.; Ciofu, O.; Hoiby, N.; Wretlind, B. Chromosomal mechanisms of aminoglycoside resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Clin. Microbiol. Infect. 2009, 15, 60-66.
133. Giwercman, B.; Jensen, E.T.; Hoiby, N.; Kharazmi, A.; Costerton, J.W. Induction of beta-lactamase production in Pseudomonas aeruginosa biofilm. Antimicrob. Agents Chemother. 1991, 35, 1008-1010.
134. Bagge, N.; Hentzer, M.; Andersen, J.B.; Ciofu, O.; Givskov, M.; Hoiby, N. Dynamics and spatial distribution of beta-lactamase expression in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 2004, 48, 1168-1174.
135. Hengzhuang, W.; Ciofu, O.; Yang, L.; Wu, H.; Song, Z.; Oliver, A.; Hoiby, N. High beta-lactamase levels change the pharmacodynamics of beta-lactam antibiotics in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 2013, 57, 196-204.
136. Plasencia, V.; Borrell, N.; Macia, M.D.; Moya, B.; Perez, J.L.; Oliver, A. Influence of high mutation rates on the mechanisms and dynamics of in vitro and in vivo resistance development to single or combined antipseudomonal agents. Antimicrob. Agents Chemother. 2007, 51, 2574-2581.