Antibiotic resistance in Pseudomonas aeruginosa biofilms: Towards the development of novel anti-biofilm therapies

Journal of Biotechnology

Volumn 191, Issue , 2014, Pages 121-130

  Taylor, Patrick K ^a   Yeung, Amy T Y ^a   Hancock, Robert E W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Anti biofilm therapeutics; Antibiotic resistance; Biofilm infections; Cationic peptides; Hospital acquired infections

Indexed keywords

ANTIBIOTICS; BACTERIA; HOSPITALS;

ANTI-BIOFILM; ANTIBIOTIC RESISTANCE; BIOFILM INFECTIONS; CATIONIC PEPTIDES; HOSPITAL ACQUIRED INFECTION;

BIOFILMS;

ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIOPHAGE; BIOFILM; EXTRACELLULAR MATRIX; HEALTH CARE SYSTEM; NONHUMAN; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SURFACE PROPERTY; TREATMENT PLANNING; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN;

PSEUDOMONAS AERUGINOSA;

ANTI-BACTERIAL AGENTS; BIOFILMS; DRUG RESISTANCE, MICROBIAL; HUMANS; PSEUDOMONAS AERUGINOSA; QUORUM SENSING;

EID: 84911933813     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.09.003     Document Type: Article

References (131)

1. Achtman A.H., Pilat S., Law C.W., Lynn D.J., Janot L., Mayer M., Ma S., Kindrachuk J., Finlay B.B., Brinkman F.S.L., Smyth G.K., Hancock R.E.W., Schofield L. Effective adjunctive therapy by an innate defense regulatory peptide in a pre-clinical model of severe malaria. Science Transl. Med. 2012, 4:135ra64.
2. Ahiwale S., Tamboli N., Thorat K., Kulkarni R., Ackermann H., Kapadnis B. In vitro management of hospital Pseudomonas aeruginosa biofilm using indigenous T7-like lytic phage. Curr. Microbiol. 2011, 62:335-340.
3. Allesen-Holm M., Barken K.B., Yang L., Klausen M., Webb J.S., Kjelleberg S., Molin S., Givskov M., Tolker-Nielsen T. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol. 2006, 59:1114-1128.
4. Alvarez-Ortega C., Wiegand I., Olivares J., Hancock R.E.W., Martinez J.L. Genetic determinants involved in the susceptibility of Pseudomonas aeruginosa to beta-lactam antibiotics. Antimicrob. Agents Chemother. 2010, 54:415941-415967.
5. Amini S., Hottes A.K., Smith L.E., Tavazoie S. Fitness landscape of antibiotic tolerance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 2011, 7:e1002298.
6. Anderl J.N., Franklin M.J., Stewart P.S. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 2000, 44:1818-1824.
7. Balaban N.Q., Merrin J., Chait R., Kowalik L., Leibler S. Bacterial persistence as a phenotypic switch. Science 2004, 305:1622-1625.
8. Bagge N., Hentzer M., Andersen J.B., Ciofu O., Givskov M., Høiby N. Dynamics and spatial distribution of beta-lactamase expression in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 2004, 48:1168-1174.
9. Barken K.B., Pamp S.J., Yang L., Gjermansen M., Bertrand J.J., Klausen M., Givskov M., Whitchurch C.B., Engel J.N., Tolker-Nielsen T. Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 2008, 10:2331-2343.
10. Barraud N., Schleheck D., Klebensberger J., Webb J.S., Hassett D., Rice S.A., Kjelleberg S. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J. Bacteriol. 2009, 191:7333-7342.
11. Barraud N., Storey M.V., Moore Z.P., Webb J.S., Rice S.A., Kjelleberg S. Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms. Microb. Biotechnol. 2009, 2:370-378.
12. Beaudoin T., Zhang L., Hinz A.J., Parr C.J., Mah T.F. The biofilm-specific resistance gene ndvB is important for the expression of ethanol oxidation genes in Pseudomonas aeruginosa biofilms. J. Bacteriol. 2012, 194:3128-3136.
13. Bjarnsholt T., Jensen P.Ø., Fiandaca M.J., Pedersen J., Hansen C.R., Andersen C.B., Pressler T., Givskov M., Høiby N. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr. Pulmonol. 2009, 44:547-558.
14. Blanc D.S., Petignat C., Janin B., Bille J., Francioli P. Frequency and molecular diversity of Pseudomonas aeruginosa upon admission and during hospitalization: a prospective epidemiologic study. Clin. Microbiol. Infect. 1998, 4:242-247.
15. Bomchil N., Watnick P., Kolter R. Identification and characterization of a Vibrio cholerae gene, mbaA, involved in maintenance of biofilm architecture. J. Bacteriol. 2003, 185:1384-1390.
16. 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.
17. Boucher J.C., Yu H., Mudd M.H., Deretic V. Mucoid Pseudomonas aeruginosa in cystic fibrosis: characterization of muc mutations in clinical isolates and analysis of clearance in a mouse model of respiratory infection. Infect. Immun. 1997, 65:3838-3846.
18. Brazas, M.D., Hancock, R.E.W., 2005. Ciprofloxacin induction of a susceptibility determinant in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 49, 3222-3227.
19. Breidenstein E.B.M., de la Fuente-Núñez C., Hancock R.E.W. Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol. 2011, 19:419-426.
20. Breidenstein, E.B.M., Bains, M., Hancock, R.E.W., 2012a. Involvement of the lon protease in the SOS response triggered by ciprofloxacin in Pseudomonas aeruginosa PAO1. Antimicrob. Agents Chemother. 56, 2879-2887.
21. Breidenstein E.B.M., Janot L., Strehmel J., Fernández L., Taylor P.K., Kukavica-Ibrulj I., Gellatly S.L., Levesque R.C., Overhage J., Hancock R.E.W. The lon protease is essential for full virulence in Pseudomonas aeruginosa. PLoS ONE 2012, 7:e49123.
22. 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. 2008, 52:4486-4491.
23. Brouqui P., Rousseau M.C., Stein A., Drancourt M., Raoult D. Treatment of Pseudomonas aeruginosa-infected orthopedic prostheses with ceftazidime-ciprofloxacin antibiotic combination. Antimicrob. Agents Chemother. 1995, 39:2423-2425.
24. Burns J.L., Gibson R.L., McNamara S., Yim D., Emerson J., Rosenfeld M., Hiatt P., McCoy K., Castile R., Smith A.L., Ramsey B.W. Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J. Infect. Dis. 2001, 183:444-452.
25. Caiazza N.C., Merritt J.H., Brothers K.M., O'Toole G.A. Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 2007, 189:3603-3612.
26. Camins B.C. Prevention and treatment of hemodialysis-related bloodstream infections. Semin. Dial. 2013, 26:476-481.
27. Chenoweth C., Saint S. Preventing catheter-associated urinary tract infections in the intensive care unit. Crit. Care Clin. 2013, 29:19-32.
28. Chorell E., Pinkner J.S., Bengtsson C., Edvinsson S., Cusumano C.K., Rosenbaum E., Johansson L.B.Å., Hultgren S.J., Almqvist F. Design and synthesis of fluorescent pilicides and curlicides: bioactive tools to study bacterial virulence mechanisms. Chem. Eur. J. 2012, 18:4522-4532.
29. D'Argenio D.A., Calfee M.W., Rainey P.B., Pesci E.C. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 2002, 184:6481-6489.
30. Davies D. Understanding biofilm resistance to antimicrobial agents. Nat. Rev. Drug Discov. 2003, 2:114-122.
31. 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.
32. Davis E.M., Li D., Irvin R.T. A peptide-stainless steel reaction that yields a bioorganic-metal state of matter. Biomaterials 2011, 32:5311-5319.
33. Davis E.M., Li D., Shahrooei M., Yu B., Muruve D., Irvin R.T. Evidence of extensive diversity in bacterial adherence mechanisms that exploit unanticipated stainless steel structural complexity for biofilm formation. Acta Biomater. 2013, 9:6236-6244.
34. De Kievit T.R., Gillis R., Marx S., Brown C., Iglewski B.H. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 2001, 67:1865-1873.
35. de la Fuente-Núñez C., Korolik V., Bains M., Nguyen U., Breidenstein E.B.M., Horsman S., Lewenza S., Burrows L.L., Hancock R.E.W. Inhibition of bacterial biofilm formation and swarming motility by a small synthetic cationic peptide. Antimicrob. Agents Chemother. 2012, 56:2696-2704.
36. 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.
37. 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. 2014, 10:e1004152.
38. Dieppois G., Ducret V., Caille O., Perron K. The transcriptional regulator CzcR modulates antibiotic resistance and quorum sensing in Pseudomonas aeruginosa. PLoS ONE 2012, 7:e38148.
39. Diggle S.P., Winzer K., Chhabra S.R., Worrall K.E., Cámara M., Williams P. The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol. Microbiol. 2003, 50:29-43.
40. Donlan R.M. Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol. 2009, 17:66-72.
41. Dötsch A., Eckweiler D., Schniederjans M., Zimmermann A., Jensen V., Scharfe M., Geffers R., Haussler S. The Pseudomonas aeruginosa transcriptome in planktonic cultures and static biofilms using RNA sequencing. PLoS ONE 2012, 7:e31092.
42. Falagas M.E., Bliziotis I.A. Pandrug-resistant Gram-negative bacteria: the dawn of the post-antibiotic era?. Int. J. Antimicrob. Agents 2007, 29:630-636.
43. Fernández L., Breidenstein E.B.M., Hancock R.E.W. Creeping baselines and adaptive resistance to antibiotics. Drug Resist. Updat. 2011, 14:1-21.
44. Fernández L., Alvarez-Ortega C., Wiegand I., Olivares J., Kocincova D., Lam J.S., Martinez J.L., Hancock R.E.W. Characterization of the polymyxin B resistome of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2012, 57:110-119.
45. 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. 2012, 56:1128-1132.
46. Fernández L., Jenssen H., Bains M., Wiegand I., Gooderham W.J., Hancock R.E.W. The two-component system CprRS senses cationic peptides and triggers adaptive resistance in Pseudomonas aeruginosa independently of ParRS. Antimicrob. Agents Chemother. 2012, 56:6212-6222.
47. Fjell C.D., Hiss J.A., Hancock R.E.W., Schneider G. Designing antimicrobial peptides: form follows function. Nat. Rev. Drug Discov. 2012, 11:37-51.
48. Folkesson A., Jelsbak L., Yang L., Johansen H.K., Ciofu O., Høiby N., Molin S. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat. Rev. Microbiol. 2012, 10:841-851.
49. Friedman L., Kolter R. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol. Microbiol. 2004, 51:675-690.
50. Glonti T., Chanishvili N., Taylor P.W. Bacteriophage-derived enzyme that depolymerizes the alginic acid capsule associated with cystic fribrosis isolates of Pseudomonas aeruginosa. J. Appl. Microbiol. 2010, 108:695-702.
51. Gooderham W.J., Bains M., McPhee J.B., Wiegand I., Hancock R.E.W. Induction by cationic antimicrobial peptides and involvement in intrinsic polymyxin and antimicrobial peptide resistance, biofilm formation, and swarming motility of PsrA in Pseudomonas aeruginosa. J. Bacteriol. 2008, 190:5624-5634.
52. Greenwood D. The activity of polymyxins against dense populations of Escherichia coli. J. Gen. Microbiol. 1975, 91:110-118.
53. Haagensen J.A.J., Klausen M., Ernst R.K., Miller S.I., Folkesson A., Tolker-Nielsen T., Molin S. Differentiation and distribution of colistin- and sodium dodecyl sulfate-tolerant cells in Pseudomonas aeruginosa biofilms. J. Bacteriol. 2007, 189:28-37.
54. Hancock R.E.W. Aminoglycoside uptake and mode of action-with special reference to streptomycin and gentamicin. II. Effects of aminoglycosides on cells. J. Antimicrob. Chemother. 1981, 8:429-445.
55. Hancock R.E.W., Bell A. Antibiotic uptake into Gram-negative bacteria. Eur. J. Clin. Microbiol. Infect. Dis. 1988, 7:713-720.
56. Hancock R.E.W., Sahl H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 2006, 24:1551-1557.
57. Herrmann G., Yang L., Wu H., Song Z., Wang H., Høiby N., Ulrich M., Molin S., Riethmuller J., Doring G. Colistin-tobramycin combinations are superior to monotherapy concerning the killing of biofilm Pseudomonas aeruginosa. J. Infect. Dis. 2010, 202:1585-1592.
58. Høiby N., Bjarnsholt T., Givskov Molin S., Ciofu O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 2010, 35:322-332.
59. Hoyle B.D., Costerton J.W. Bacterial resistance to antibiotics: the role of biofilms. Prog. Drug Res. 1991, 37:91-105.
60. Jackson K.D., Starkey M., Kremer S., Parsek M.R., Wozniak D.J. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J. Bacteriol. 2004, 186:4466-4475.
61. Jakobsen T.H., van Gennip M., Phipps R.K., Shanmugham M.S., Christensen L.D., Alhede M., Skindersoe M.E., Rasmussen T.B., Friedrich K., Uthe F., Jensen P.Ø., Moser C., Nielsen K.F., Eberl L., Larsen T.O., Tanner D., Høiby N., Bjarnsholt T., Givskov M. Ajoene, a sulfur-rich molecule from garlic, inhibits genes controlled by quorum sensing. Antimicrob. Agents Chemother. 2012, 56:2314-2325.
62. Jenal U., Malone J. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 2006, 40:385-407.
63. Jenssen H., Hamill P., Hancock R.E.W. Peptide antimicrobial agents. Clin. Microbiol. Rev. 2006, 19:491-511.
64. Jeukens J., Boyle B., Kukavica-Ibrulj I., Ouellet M.M., Aaron S.D., Charette S.J., Fothergill J.L., Tucker N.P., Winstanley C., Levesque R.C. Comparative genomics of isolates of a Pseudomonas aeruginosa epidemic strain associated with chronic lung infections of cystic fibrosis patients. PLoS ONE 2014, 9:e87611.
65. Juan C., Zamorano L., Perez J.L., Ge Y., Oliver A. Activity of a new antipseudomonal cephalosporin, CXA-101 (FR264205), against carbapenem-resistant and multi-drug-resistant Pseudomonas aeruginosa clinical strains. Antimicrob. Agents Chemother. 2010, 54:846-851. Spanish Group for the Study of Pseudomonas, Spanish Network for Research in Infectious Diseases.
66. Keren I., Shah D., Spoering A., Kaldalu N., Lewis K. Specialized persister cells and the mechanism of multi-drug tolerance in Escherichia coli. J. Bacteriol. 2004, 186:8172-8180.
67. 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. 2011, 55:1874-1882.
68. Klausen M., Heydorn A., Ragas P., Lambertsen L., Aaes-Jorgensen A., Molin S., Tolker-Nielsen T. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 2003, 48:1511-1524.
69. Kohler T., Epp S.F., Curty L.K., Pechere J.C. Characterization of MexT, the regulator of the MexE-MexF-OprN multi-drug efflux system of Pseudomonas aeruginosa. J. Bacteriol. 1999, 181:6300-6305.
70. Kolak M., Karpati F., Monstein H.J., Jonasson J. Molecular typing of the bacterial flora in sputum of cystic fibrosis patients. Int. J. Med. Microbiol. 2003, 293:309-317.
71. Kumon H., Tomochika K., Matunaga T., Ogawa M., Ohmori H. A sandwich cup method for the penetration assay of antimicrobial agents through Pseudomonas exopolysaccharides. Microbiol. Immunol. 1994, 38:615-619.
72. Langaee T.Y., Gagnon L., Huletsky A. Inactivation of the ampD gene in Pseudomonas aeruginosa leads to moderate-basal-level and hyperinducible AmpC beta-lactamase expression. Antimicrob. Agents Chemother. 2000, 44:583-589.
73. Li W.R., Xie X.B., Shi Q.S., Zend H.Y., Ou-Yang Y.S., Chen Y.B. Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli. Appl. Microbiol. Biotechnol. 2010, 85:1115-1122.
74. Lindsay D., von Holy A. Bacterial biofilms within the clinical setting: what healthcare professionals should know. J. Hosp. Infect. 2006, 64:313-325.
75. Livermore D.M. Of Pseudomonas, porins, pumps and carbapenems. J. Antimicrob. Chemother. 2001, 47:247-250.
76. Ly-Chatain, M.H., 2014. The factors affecting effectiveness of treatment in phages therapy. Front. Microbiol. 5, eCollection 2014.
77. Ma L., Conover M., Lu H., Parsek M.R., Bayles K., Wozniak D.J. Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog. 2009, 5:e1000354.
78. Macfarlane E.L., Kwasnicka A., Hancock R.E.W. Role of Pseudomonas aeruginosa PhoP-PhoQ in resistance to antimicrobial cationic peptides and aminoglycosides. Microbiology 2000, 146:2543-2554.
79. Macfarlane E.L., Kwasnicka A., Ochs M.M., Hancock R.E.W. PhoP-PhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer-membrane protein OprH and polymyxin B resistance. Mol. Microbiol. 1999, 34:305-316.
80. Macià M.D., Perez J.L., Molin S., Oliver A. Dynamics of mutator and antibiotic-resistant populations in a pharmacokinetic/pharmacodynamic model of Pseudomonas aeruginosa biofilm treatment. Antimicrob. Agents Chemother. 2011, 55:5230-5237.
81. O'Toole, G.A., Kolter, R., 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30, 295-304.
82. Maisonneuve E., Castro-Camargo M., Gerdes K. (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 2013, 154:1140-1150.
83. McPhee J.B., Lewenza S., Hancock R.E.W. 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. 2003, 50:205-217.
84. Mijnendonckx K., Leys N., Mahillon J., Silver S., Van Houdt R. Antimicrobial Silver: Uses, Toxicity, and Potential for Resistance 2013.
85. Molin S., Tolker-Nielsen T. Gene transfer occurs with enhanced efficiency in biofilms and induces enhance stabilisation of the biofilm structure. Curr. Opin. Biotechnol. 2003, 14:255-261.
86. Moore R.A., Bates N.C., Hancock R.E.W. Interaction of polycationic antibiotics with Pseudomonas aeruginosa lipopolysaccharide and lipid A studied by using dansyl-polymyxin. Antimicrob. Agents Chemother. 1986, 29:496-500.
87. Moya B., Zamorano L., Juan C., Perez J.L., Ge Y., Oliver A. Activity of a new cephalosporin, CXA-101 (FR264205), against beta-lactam-resistant Pseudomonas aeruginosa mutants selected in vitro and after antipseudomonal treatment of intensive care unit patients. Antimicrob. Agents Chemother. 2010, 54:1213-1217.
88. Mulcahy H., Charron-Mazenod L., Lewenza S. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 2008, 4:e1000213.
89. Mulcahy L.R., Burns J.L., Lory S., Lewis K. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J. Bacteriol. 2010, 192:6191-6199.
90. Musken M., Di Fiore S., Dötsch A., Fischer R., Haussler S. Genetic determinants of Pseudomonas aeruginosa biofilm establishment. Microbiology 2010, 156:431-441.
91. Örmälä A.M., Jalasvuori M. Phage therapy: should bacterial resistance to phages be a concern, even in the long run?. Bacteriophage 2013, 3:e24219.
92. Overhage J., Campisano A., Bains M., Torfs E.C., Rehm B.H., Hancock R.E.W. Human host defense peptide LL-37 prevents bacterial biofilm formation. Infect. Immun. 2008, 76:4176-4182.
93. Pamp S.J., Gjermansen M., Johansen H.K., Tolker-Nielsen T. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol. Microbiol. 2008, 68:223-240.
94. Pesci E.C., Pearson J.P., Seed P.C., Iglewski B.H. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 1997, 179:3127-3132.
95. Piatek R., Zalewska-Piatek B., Dzierzbicka K., Makowiec S., Pilipczuk J., Szemiako K., Cyranks-Czaja A., Wojciechowski M. Pilicides inhibit the FGL chaperone/usher assisted biogenesis of the Dr fimbrial polyadhesin from uropathogenic Escherichia coli. BMC Microbiol. 2013, 13:131-142.
96. Pinkner J.S., Remaut H., Buelens F., Miller E., Åberg V., Pemberton N., Hedenström M., Larsson A., Seed P., Waksman G., Hultgren S.J., Almqvist F. Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17897-17902.
97. Potrykus K., Cashel M. (p)ppGpp: still magical?. Annu. Rev. Microbiol. 2008, 62:35-51.
98. Rampioni G., Leoni L., Williams P. The art of antibacterial warfare: deception through interference with quorum sensing-mediated communication. Bioorg. Chem. 2014, 55:60-68.
99. Reffuveille, F., de la Fuente-Núñez, C., Mansour, S., Hancock, R.E.W., 2014. A broad-spectrum anti-biofilm peptide enhances antibiotic action against bacterial biofilms. Antimicrob. Agents Chemother., 58, 5363-5371.
100. Riera E., Macià M.D., Mena A., Mulet X., Perez J.L., Ge Y., Oliver A. Anti-biofilm and resistance suppression activities of CXA-101 against chronic respiratory infection phenotypes of Pseudomonas aeruginosa strain PAO1. J. Antimicrob. Chemother. 2010, 65:1399-1404.
101. Rivas-Santiago B., Castañeda-Delgado J.E., Rivas Santiago C.E., Waldbrook M., González-Curiel I., León-Contreras J.C., Enciso-Moreno A., del Villar V., Méndez-Ramos J., Hancock R.E.W., Hernandez-Pando R. Ability of innate defence regulator peptides IDR-1002, IDR-HH2 and IDR-1018 to protect against Mycobacterium tuberculosis infections in animal models. PLoS ONE 2013, 8:e59119.
102. Rudkjøbing V.B., Thomsen T.R., Alhebe M., Kragh K.N., Nielsen P.H., Johansen U.R., Givskov M., Høiby N., Bjarnsholt T. The microorganisms in chronically infected end-stage and non-end-stage cystic fibrosis patients. FEMS Immunol. Med. Microbiol. 2012, 65:236-244.
103. Ryan E.M., Gorman S.P., Donnelly R.F., Gilmore B.F. Recent advances in bacteriophage therapy: how delivery routes, formulation, concentration and timing influence the success of phage therapy. J. Pharm. Pharmacol. 2011, 63:1253-1264.
104. Ryjenkov D.A., Tarutina M., Moskvin O.V., Gomelsky M. Cyclic diguanylate is a ubiquitous signaling molecule in Bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 2005, 187:1792-1798.
105. Schurek K.N., Marr A.K., Taylor P.K., Wiegand I., Semenec L., Khaira B.K., Hancock R.E.W. Novel genetic determinants of low-level aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2008, 52:4213-4419.
106. Schurek K.N., Sampaio J.L., Kiffer C.R., Sinto S., Mendes C.M., Hancock R.E.W. Involvement of pmrAB and phoPQ in polymyxin B adaptation and inducible resistance in non-cystic fibrosis clinical isolates of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2009, 53:4345-4351.
107. Scutera S., Zucca M., Savoia D. Novel approaches for the design and discovery of quorum-sensing inhibitors. Expert Opin. Drug Discov. 2014, 9:353-366.
108. Shah D., Zhang Z., Khodursky A.B., Kaldalu N., Kurg K., Lewis K. Persisters: a distinct physiological state of E. coli. BMC Microbiol. 2006, 6:53.
109. Shakir A., El Badaway M.R., Shields C.R., Jakubovics N.S., Burgess J.G. Removal of biofilms from tracheoesophageal speech valves using novel marine microbial deoxyribonuclease. Otolaryngol. Head Neck Surg. 2012, 147:509-514.
110. 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.
111. Sulakvelidze A., Alavidze Z., Morris J.G. Bacteriophage therapy. Antimicrob. Agents Chemother. 2001, 45:649-659.
112. Thomas C.M., Nielsen K.M. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. Microbiol. 2005, 3:711-721.
113. Toutain C.M., Caizza N.C., Zegans M.E., O'Toole G.A. Roles for flagellar stators in biofilm formation by Pseudomonas aeruginosa. Res. Microbiol. 2007, 158:471-477.
114. Trias J., Nikaido H. Outer membrane protein D2 catalyzes facilitated diffusion of carbapenems and penems through the outer membrane of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 1990, 34:52-57.
115. Tre-Hardy M., Nagant C., El Manssouri N., Vanderbist F., Traore H., Vaneechoutte M., Dehaye J.P. Efficacy of the combination of tobramycin and a macrolide in an in vitro Pseudomonas aeruginosa mature biofilm model. Antimicrob. Agents Chemother. 2010, 54:4409-4415.
116. Umadevi S., Joseph N.M., Kumari K., Easow J.M., Kumar S., Stephen S., Srirangarag S., Raj S. Detection of extended spectrum beta-lactamases, AmpC beta-lactamases and metallobetalactamases in clinical isolates of ceftazidime resistant Pseudomonas aeruginosa. Braz. J. Microbiol. 2011, 42:1284-1288.
117. van Belkim A., Renders N.H.M., Smith S., Overbeek S.E., Verbrugh H.A. Comparison of conventional and molecular methods for the detection of bacterial pathogens in sputum samples from cystic fibrosis patients. FEMS Immunol. Med. Microbiol. 2000, 27:51-57.
118. Vasseur P., Vallet-Gely I., Soscia C., Genin S., Filloux A. The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 2005, 151:985-997.
119. Walters M.C., Roe F., Bugnicourt A., Franklin M.J., Stewart P.S. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 2003, 47:317-323.
120. Wang J., Zhou J.Y., Qu T.T., Shen P., Wei Z.Q., Yu Y.S., Li L.J. Molecular epidemiology and mechanisms of carbapenem resistance in Pseudomonas aeruginosa isolates from Chinese hospitals. Int. J. Antimicrob. Agents 2010, 35:486-491.
121. Werner E., Roe F., Bugnicourt A., Franklin M.J., Heydorn A., Molin S., Pitts B., Stewart P.S. Stratified growth in Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 2004, 70:6188-6196.
122. Whitchurch C.B., Tolker-Nielsen T., Ragas P.C., Mattick J.S. Extracellular DNA required for bacterial biofilm formation. Science 2002, 29:1487.
123. Whiteley M., Bangera M.G., Bumgarner R.E., Parsek M.R., Teitzel G.M., Lory S., Greenberg E.P. Gene expression in Pseudomonas aeruginosa biofilms. Nature 2001, 413:860-864.
124. Worlitzsch D., Tarran R., Ulrich M., Schwab U., Cekici A., Meyer K.C., Birrer P., Bellon G., Berger J., Weiss T., Botzenhart K., Yankaskas J.R., Randell S., Boucher R.C., Döring G. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 2002, 109:317-325.
125. Xu K.D., Stewart P.S., Xia F., Huang C.T., McFeters G.A. Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl. Environ. Microbiol. 1998, 64:4035-4039.
126. Yeung A.T.Y., 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. 2011, 193:918-931.
127. Yeung A.T.Y., Torfs E.C., Jamshidi F., Bains M., Wiegand I., Hancock R.E.W., Overhage J. Swarming of Pseudomonas aeruginosa is controlled by a broad spectrum of transcriptional regulators, including MetR. J. Bacteriol. 2009, 191:5592-5602.
128. Yu Q., Griffin E.F., Moreau-Marquis S., Schwartzman J.D., Stanton B.A., O'Toole G.A. In vitro evaluation of tobramycin and aztreonam versus Pseudomonas aeruginosa biofilms on cystic fibrosis-derived human airway epithelial cells. J. Antimicrob. Chemother. 2012, 67:2673-2681.
129. Zhang L., Fritsch M., Hammond L., Landreville R., Slatculescu C., Colavita A., Mah T.F. Identification of genes involved in Pseudomonas aeruginosa biofilm-specific resistance to antibiotics. PLoS ONE 2013, 8:e61625.
130. Zhang L., Hinz A.J., Nadeau J.P., Mah T.F. Pseudomonas aeruginosa tssC1 links type VI secretion and biofilm-specific antibiotic resistance. J. Bacteriol. 2011, 193:5510-5513.
131. Zhang L., Mah T.F. Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J. Bacteriol. 2008, 190:4447-4452.