Antimicrobial targets localize to the extracellular vesicle-associated proteome of Pseudomonas aeruginosa grown in a biofilm

Frontiers in Microbiology

Volumn 5, Issue SEP, 2014, Pages

  Park, Amber J ^a   Surette, Matthew D ^a   Khursigara, Cezar M ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Antimicrobial resistance; Bacterial biofilms; Outer membrane vesicles; Proteomics; Pseudomonas aeruginosa

Indexed keywords

DRUG BINDING PROTEIN; PROTEOME;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL SURVIVAL; BIOFILM; CELL COMMUNICATION; LIQUID CHROMATOGRAPHY; MEMBRANE VESICLE; NONHUMAN; PSEUDOMONAS AERUGINOSA; SCANNING ELECTRON MICROSCOPY; TANDEM MASS SPECTROMETRY; TRANSMISSION ELECTRON MICROSCOPY; WHOLE CELL;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 84928339747     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00464     Document Type: Article

References (91)

1. Aendekerk, S. (2005). The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology 151, 1113-1125. doi: 10.1099/mic.0.27631-0
2. Aendekerk, S., Ghysels, B., Cornelis, P., and Baysse, C. (2002). Characterization of a new efflux pump, MexGHI-OpmD, from Pseudomonas aeruginosa that confers resistance to vanadium. Microbiology 148, 2371-2381.
3. Afessa, B., and Green, B. (2000). Bacterial pneumonia in hospitalized patients with HIV infection: the pulmonary complications, ICU support, and prognostic factors of hospitalized patients with HIV (PIP) study. Chest 117, 1017-1022. doi: 10.1378/chest.117.4.1017
4. Alvarez-Ortega, C., Wiegand, I., Olivares, J., Hancock, R. E. W., and Martinez, J. L. (2010). Genetic determinants involved in the susceptibility of Pseudomonas aeruginosa to beta-lactam antibiotics. Antimicrob. Agents Chemother. 54, 4159-4167. doi: 10.1128/AAC.00257-10
5. Anderl, J. N., Franklin, M. J., and Stewart, P. S. (2000). Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 44, 1818-1824. doi: 10.1128/AAC.44.7.1818-1824.2000
6. Anderl, J. N., Zahller, J., Roe, F., and Stewart, P. S. (2003). Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 47, 1251-1256. doi: 10.1128/AAC.47.4.1251-1256.2003
7. Angus, B. L., Carey, A. M., Caron, D. A., Kropinski, A. M., and Hancock, R. E. (1982). Outer membrane permeability in Pseudomonas aeruginosa: comparison of a wild-type with an antibiotic-supersusceptible mutant. Antimicrob. Agents Chemother. 21, 299-309. doi: 10.1128/AAC.21.2.299
8. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M.,et al. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29. doi: 10.1038/75556
9. Baer, M., Sawa, T., Flynn, P., Luehrsen, K., Martinez, D., Wiener-Kronish, J. P.,et al. (2009). An engineered human antibody fab fragment specific for Pseudomonas aeruginosa PcrV antigen has potent antibacterial activity. Infect. Immun. 77, 1083-1090. doi: 10.1128/IAI.00815-08
10. Bagge, N., Hentzer, M., Andersen, J. B., Ciofu, O., Givskov, M., and Hoiby, N. (2004). Dynamics and spatial distribution of beta-lactamase expression in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 48, 1168-1174. doi: 10.1128/AAC.48.4.1168-1174.2004
11. Bauman, S. J., and Kuehn, M. J. (2006). Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect. 8, 2400-2408. doi: 10.1016/j.micinf.2006.05.001
12. Bauman, S. J., and Kuehn, M. J. (2009). Pseudomonas aeruginosa vesicles associate with and are internalized by human lung epithelial cells. BMC Microbiol. 9:26. doi: 10.1186/1471-2180-9-26
13. Baysse, C., De Vos, D., Naudet, Y., Vandermonde, A., Ochsner, U., Meyer, J.-M.,et al. (2000). Vanadium interferes with siderophore-mediated iron uptake in Pseudomonas aeruginosa. Microbiology 146, 2425-2434.
14. Berleman, J., and Auer, M. (2012). The role of bacterial outer membrane vesicles for intra- and interspecies delivery. Environ. Microbiol. 15, 347-354. doi: 10.1111/1462-2920.12048
15. Binz, P. A., Barkovich, R., Beavis, R. C., Creasy, D., Horn, D. M., Julian, R. K. J.,et al. (2008). Guidelines for reporting the use of mass spectrometry informatics in proteomics. Nat. Biotechnol. 26:862. doi: 10.1038/nbt0808-862
16. Bomberger, J. M., MacEachran, D. P., Coutermarsh, B. A., Ye, S., O'Toole, G. A., and Stanton, B. A. (2009). Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 5:e1000382. doi: 10.1371/journal.ppat.1000382.s004
17. Borriello, G., Werner, E., Roe, F., Kim, A. M., Ehrlich, G. D., and Stewart, P. S. (2004). Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 48, 2659-2664. doi: 10.1128/AAC.48.7.2659-2664.2004
18. Breidenstein, E. B. M., Khaira, B. K., Wiegand, I., Overhage, J., and Hancock, R. E. W. (2008). Complex ciprofloxacin resistome revealed by screening a Pseudomonas aeruginosa mutant library for altered susceptibility. Antimicrob. Agents Chemother. 52, 4486-4491. doi: 10.1128/AAC.00222-08
19. Ceri, H., Olson, M. E., Stremick, C., Read, R. R., Morck, D., and Buret, A. (1999). The calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J. Clin. Microbiol. 37, 1771-1776.
20. Chatterjee, D., and Chaudhuri, K. (2013). Vibrio cholerae O395 outer membrane vesicles modulate intestinal epithelial cells in a NOD1 protein-dependent manner and induce dendritic cell-mediated Th2/Th17 cell responses. J. Biol. Chem. 288, 4299-4309. doi: 10.1074/jbc. M112.408302
21. Chatterjee, S., Maiti, P., Dey, R., Kundu, A., and Dey, R. (2014). Biofilms on indwelling urologic devices: microbes and antimicrobial management prospect. Ann. Med. Health Sci. Res. 4, 100-104. doi: 10.4103/2141-9248.126612
22. Chiang, W. C., Nilsson, M., Jensen, P. O., Hoiby, N., Nielsen, T. E., Givskov, M.,et al. (2013). Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 57, 2352-2361. doi: 10.1128/AAC.00001-13
23. Chuanchuen, R., Narasaki, C. T., and Schweizer, H. P. (2002). The MexJK efflux pump of Pseudomonas aeruginosa requires OprM for antibiotic efflux but not for efflux of triclosan. J. Bacteriol. 184, 5036-5044. doi: 10.1128/JB.184.18.5036-5044.2002
24. Cigana, C., Curcurù, L., Leone, M. R., Ieranò, T., Lorè, N. I., Bianconi, I.,et al. (2009). Pseudomonas aeruginosa exploits lipid A and muropeptides modification as a strategy to lower innate immunity during cystic fibrosis lung infection. PLoS ONE 4:e8439. doi: 10.1371/journal.pone.0008439.s005
25. Ciornei, C. D., Novikov, A., Beloin, C., Fitting, C., Caroff, M., Ghigo, J. M.,et al. (2010). Biofilm-forming Pseudomonas aeruginosa bacteria undergo lipopolysaccharide structural modifications and induce enhanced inflammatory cytokine response in human monocytes. Innate Immun. 16, 288-301. doi: 10.1177/1753425909341807
26. Cox, J., and Mann, M. (2008). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372. doi: 10.1038/nbt.1511
27. De Kievit, T. R. (2009). Quorum sensing in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 11, 279-288. doi: 10.1111/j.1462-2920.2008.01792.x
28. De Kievit, T. R., Parkins, M. D., Gillis, R. J., Srikumar, R., Ceri, H., Poole, K.,et al. (2001). Multidrug efflux pumps: expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 45, 1761-1770. doi: 10.1128/AAC.45.6.1761-1770.2001
29. Dötsch, A., Eckweiler, D., Schniederjans, M., Zimmermann, A., Jensen, V., Scharfe, M.,et al. (2012). The Pseudomonas aeruginosa transcriptome in planktonic cultures and static biofilms using RNA sequencing. PLoS ONE 7:e31092. doi: 10.1371/journal.pone.0031092.s006
30. Drenkard, E. (2003). Antimicrobial resistance of Pseudomonas aeruginosa biofilms. Microbes Infect. 5, 1213-1219. doi: 10.1016/j.micinf.2003.08.009
31. El'Garch, F., Jeannot, K., Hocquet, D., Llanes-Barakat, C., and Plesiat, P. (2007). Cumulative effects of several nonenzymatic mechanisms on the resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob. Agents Chemother. 51, 1016-1021. doi: 10.1128/AAC.00704-06
32. Ernst, R. K. (1999). Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286, 1561-1565. doi: 10.1126/science.286.5444.1561
33. Ernst, R. K., Adams, K. N., Moskowitz, S. M., Kraig, G. M., Kawasaki, K., Stead, C. M.,et al. (2005). The Pseudomonas aeruginosa lipid A deacylase: selection for expression and loss within the cystic fibrosis airway. J. Bacteriol. 188, 191-201. doi: 10.1128/JB.188.1.191-201.2006
34. Fernandez, L., Breidenstein, E. B. M., Song, D., and Hancock, R. E. W. (2012). Role of intracellular proteases in the antibiotic resistance, motility, and biofilm formation of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 56, 1128-1132. doi: 10.1128/AAC.05336-11
35. Fernandez, L., and Hancock, R. E. W. (2012). Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance. Clin. Microbiol. Rev. 25, 661-681. doi: 10.1128/CMR.00043-12
36. Folsom, J. P., Richards, L., Pitts, B., Roe, F., Ehrlich, G. D., Parker, A.,et al. (2010). Physiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis. BMC Microbiol. 10:294. doi: 10.1186/1471-2180-10-294
37. Foster, L. J., De Hoog, C. L., and Mann, M. (2003). Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. U.S.A. 100, 5813-5818. doi: 10.1073/pnas.0631608100
38. Gordon, C. A., Hodges, N. A., and Marriott, C. (1988). Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. J Antimicrob. Chemother. 22, 667-674. doi: 10.1093/jac/22.5.667
39. Haurat, M. F., Aduse-Opoku, J., Rangarajan, M., Dorobantu, L., Gray, M. R., Curtis, M. A.,et al. (2011). Selective sorting of cargo proteins into bacterial membrane vesicles. J. Biol. Chem. 286, 1269-1276. doi: 10.1074/jbc. M110.185744
40. Hooper, D. C., and Wolfson, J. S. (1989). Bacterial resistance to the quinolone antimicrobial agents. Am. J. Med. 87, 17S-23S.
41. Jefferson, K. K., Goldmann, D. A., and Pier, G. B. (2005). Use of confocal microscopy to analyze the rate of vancomycin penetration through Staphylococcus aureus biofilms. Antimicrob. Agents Chemother. 49, 2467-2473. doi: 10.1128/AAC.49.6.2467-2473.2005
42. Jun, S. H., Lee, J. H., Kim, B. R., Kim, S. I., Park, T. I., Lee, J. C.,et al. (2013). Acinetobacter baumannii outer membrane vesicles elicit a potent innate immune response via membrane proteins. PLoS ONE 8:e71751. doi: 10.1371/journal.pone.0071751.g006
43. Kadurugamuwa, J. L., Clarke, A. J., and Beveridge, T. J. (1993). Surface action of gentamicin on Pseudomonas aeruginosa. J. Bacteriol. 175, 5798-5805.
44. Kesty, N. C., Mason, K. M., Reedy, M., Miller, S. E., and Kuehn, M. J. (2004). Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23, 4538-4549. doi: 10.1038/sj.emboj.7600471
45. Kim, J. H., Yoon, Y. J., Lee, J., Choi, E.-J., Yi, N., Park, K.-S.,et al. (2013). Outer membrane vesicles derived from Escherichia coli up-regulate expression of endothelial cell adhesion molecules in vitro and in vivo. PLoS ONE 8:e59276. doi: 10.1371/journal.pone.0059276.s001
46. King, J. D., Kocincova, D., Westman, E. L., and Lam, J. S. (2009). Review: lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Innate Immun. 15, 261-312. doi: 10.1177/1753425909106436
47. Köhler, T., Michéa-Hamzehpour, M., Henze, U., Gotoh, N., Curty, L. K., and Pechère, J. C. (1997). Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa. Mol. Microbiol. 23, 345-354. doi: 10.1046/j.1365-2958.1997.2281594.x
48. Lam, J., Chan, R., Lam, K., and Costerton, J. W. (1980). Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect. Immun. 28, 546-556.
49. Li, X. Z., Nikaido, H., and Poole, K. (1995). Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 39, 1948-1953. doi: 10.1128/AAC.39.9.1948
50. Li, Y., Mima, T., Komori, Y., Morita, Y., Kuroda, T., Mizushima, T.,et al. (2003). A new member of the tripartite multidrug efflux pumps, MexVW-OprM, in Pseudomonas aeruginosa. J. Antimicrob. Chemother. 52, 572-575. doi: 10.1093/jac/dkg390
51. Maier, T., Schmidt, A., Guell, M., Kühner, S., Gavin, A.-C., Aebersold, R.,et al. (2011). Quantification of mRNA and protein and integration with protein turnover in a bacterium. Mol. Syst. Biol. 7, 1-12. doi: 10.1038/msb.2011.38
52. Manning, A. J., and Kuehn, M. J. (2011). Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiol. 11:258. doi: 10.1186/1471-2180-11-258
53. Mima, T., Joshi, S., Gomez-Escalada, M., and Schweizer, H. P. (2007). Identification and characterization of TriABC-OpmH, a triclosan efflux pump of Pseudomonas aeruginosa requiring two membrane fusion proteins. J. Bacteriol. 189, 7600-7609. doi: 10.1128/JB.00850-07
54. Mima, T., Kohira, N., Li, Y., Sekiya, H., Ogawa, W., Kuroda, T.,et al. (2009). Gene cloning and characteristics of the RND-type multidrug efflux pump MuxABC-OpmB possessing two RND components in Pseudomonas aeruginosa. Microbiology 155, 3509-3517. doi: 10.1099/mic.0.031260-0
55. Mima, T., Sekiya, H., Mizushima, T., Kuroda, T., and Tsuchiya, T. (2005). Gene cloning and properties of the RND-type multidrug efflux pumps MexPQ-OpmE and MexMN-OprM from Pseudomonas aeruginosa. Microbiol. Immunol. 49, 999-1002. doi: 10.1111/j.1348-0421.2005.tb03696.x
56. Morita, Y., Kimura, N., Mima, T., Mizushima, T., and Tsuchiya, T. (2001). Roles of MexXY- and MexAB-multidrug efflux pumps in intrinsic multidrug resistance of Pseudomonas aeruginosa PAO1. J. Gen. Appl. Microbiol. 47, 27-32. doi: 10.2323/jgam.47.27
57. Mulet, X., Moya, B., Juan, C., Macia, M. D., Perez, J. L., Blazquez, J.,et al. (2011). Antagonistic interactions of Pseudomonas aeruginosa antibiotic resistance mechanisms in planktonic but not biofilm growth. Antimicrob. Agents Chemother. 55, 4560-4568. doi: 10.1128/AAC.00519-11
58. Murphy, K., Park, A. J., Hao, Y., Brewer, D., Lam, J. S., and Khursigara, C. M. (2014). Influence of O polysaccharides on biofilm development and outer membrane vesicle biogenesis in Pseudomonas aeruginosa PAO1. J. Bacteriol. 196, 1306-1317. doi: 10.1128/JB.01463-13
59. Needham, B. D., and Trent, M. S. (2013). Fortifying the barrier: the impact of lipid A remodelling on bacterial pathogenesis. Nat. Rev. Microbiol. 11, 467-481. doi: 10.1038/nrmicro3047
60. Neu, H. C. (1988). Bacterial resistance to fluoroquinolones. Rev. Infect. Dis. 10(Suppl. 1), S57-S63. doi: 10.1093/clinids/10.Supplement_1.S57
61. Nichols, W. W., Dorrington, S. M., Slack, M. P., and Walmsley, H. L. (1988). Inhibition of tobramycin diffusion by binding to alginate. Antimicrob. Agents Chemother. 32, 518-523. doi: 10.1128/AAC.32.4.518
62. Nie, L., Wu, G., and Zhang, W. (2006). Correlation between mRNA and protein abundance in Desulfovibrio vulgaris: a multiple regression to identify sources of variations. Biochem. Biophys. Res. Commun. 339, 603-610. doi: 10.1016/j.bbrc.2005.11.055
63. Öncül, O., Öksüz, S., Acar, A., Ülkür, E., Turhan, V., Uygur, F.,et al. (2013). Noscomial infections characteristics in a burn intensive care unit: analysis of an eleven-year active surveillance. Burns 40, 835-841. doi: 10.1016/j.burns.2013.11.003
64. Park, A. J., Murphy, K., Krieger, J. R., Brewer, D., Taylor, P., Habash, M.,et al. (2014). A temporal examination of the planktonic and biofilm proteome of whole cell Pseudomonas aeruginosa PAO1 using quantitative mass spectrometry. Mol. Cell. Proteomics 13, 1095-1105. doi: 10.1074/mcp. M113.033985.
65. Park, K.-S., Lee, J., Jang, S. C., Kim, S. R., Jang, M. H., Lötvall, J.,et al. (2013). Pulmonary inflammation induced by bacteria-free outer membrane vesicles from Pseudomonas aeruginosa. Am. J. Respir. Cell Mol. Biol. 49, 637-645. doi: 10.1165/rcmb.2012-0370OC
66. Piddock, L. J. (1999). Mechanisms of fluoroquinolone resistance: an update 1994-1998. Drugs 58(Suppl. 2), 11-18. doi: 10.1165/rcmb.2012-0370OC
67. Poole, K., Gotoh, N., Tsujimoto, H., Zhao, Q., Wada, A., Yamasaki, T.,et al. (1996). Overexpression of the mexC-mexD-oprJ efflux operon in nfxB-type multidrug-resistant strains of Pseudomonas aeruginosa. Mol. Microbiol. 21, 713-724. doi: 10.2165/00003495-199958002-00003
68. Pritt, B., O'Brien, L., and Winn, W. (2007). Mucoid Pseudomonas in cystic fibrosis. Am. J. Clin. Pathol. 128, 32-34. doi: 10.1309/KJRPC7DD5TR9NTDM
69. Rajan, S., and Saiman, L. (2002). Pulmonary infections in patients with cystic fibrosis. Semin. Respir. Infect. 17, 47-56. doi: 10.1309/KJRPC7DD5TR9NTDM
70. Rudkjobing, V. B., Thomsen, T. R., Alhede, M., Kragh, K. N., Nielsen, P. H., Johansen, U. R.,et al. (2012). The microorganisms in chronically infected end-stage and non-end-stage cystic fibrosis patients. FEMS Immunol. Med. Microbiol. 65, 236-244. doi: 10.1053/srin.2002.31690
71. Ruiz, J. (2003). Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J. Antimicrob. Chemother. 51, 1109-1117. doi: 10.1093/jac/dkg222
72. Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W., and Davies, D. G. (2002). Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184, 1140-1154. doi: 10.1128/jb.184.4.1140-1154.2002
73. Schooling, S. R., and Beveridge, T. J. (2006). Membrane vesicles: an overlooked component of the matrices of biofilms. J. Bacteriol. 188, 5945-5957. doi: 10.1128/JB.00257-06
74. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J.,et al. (2011). Global quantification of mammalian gene expression control. Nature 473, 337-342. doi: 10.1038/nature10098
75. Southey-Pillig, C. J., Davies, D. G., and Sauer, K. (2005). Characterization of temporal protein production in Pseudomonas aeruginosa biofilms. J. Bacteriol. 187, 8114-8126. doi: 10.1128/JB.187.23.8114-8126.2005
76. Srikumar, R., Tsang, E., and Poole, K. (1999). Contribution of the MexAB-OprM multidrug efflux system to the β-lactam resistance of penicillin-binding protein and β-lactamase-derepressed mutants of Pseudomonas aeruginosa. J. Antimicrob. Chemother. 44, 537-540. doi: 10.1093/jac/44.4.537
77. Taniguchi, Y., Choi, P. J., Li, G. W., Chen, H., Babu, M., Hearn, J.,et al. (2010). Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329, 533-538. doi: 10.1126/science.1188308
78. Thay, B., Wai, S. N., and Oscarsson, J. (2013). Staphylococcus aureus α-toxin-dependent induction of host cell death by membrane-derived vesicles. PLoS ONE 8:e54661. doi: 10.1371/journal.pone.0054661.g007
79. Trent, M. S. (2004). Biosynthesis, transport, and modification of lipid A. Biochem. Cell Biol. 82, 71-86. doi: 10.1139/o03-070
80. Tuomanen, E., Cozens, R., Tosch, W., Zak, O., and Tomasz, A. (1986). The rate of killing of Escherichia coli by beta-lactam antibiotics is strictly proportional to the rate of bacterial growth. Microbiology 132, 1297-1304. doi: 10.1099/00221287-132-5-1297
81. Vilain, S., Cosette, P., Hubert, M., Lange, C., Junter, G.-A., and Jouenne, T. (2004). Comparative proteomic analysis of planktonic and immobilized Pseudomonas aeruginosa cells: a multivariate statistical approach. Anal. Biochem. 329, 120-130. doi: 10.1016/j.ab.2004.02.014
82. Walley, J. W., Shen, Z., Sartor, R., and Wu, K. J. (2013). Reconstruction of protein networks from an atlas of maize seed proteotypes. Proc. Natl. Acad. Sci. U.S.A. 110, E4808-E4817. doi: 10.1073/pnas.1319113110
83. Walters, M. C., Roe, F., Bugnicourt, A., Franklin, M. J., and Stewart, P. S. (2003). Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47, 317-323. doi: 10.1128/AAC.47.1.317-323.2003
84. Welch, A., Awah, C. U., Jing, S., van Veen, H. W., and Venter, H. (2010). Promiscuous partnering and independent activity of MexB, the multidrug transporter protein from Pseudomonas aeruginosa. Biochem. J. 430, 355-364. doi: 10.1128/JB.185.19.5657-5664.2003
85. Wessel, A. K., Arshad, T. A., Fitzpatrick, M., Connell, J. L., Bonnecaze, R. T., Shear, J. B.,et al. (2014). Oxygen limitation within a bacterial aggregate. MBio 5:e00992. doi: 10.1128/mBio.00992-14
86. Whiteley, M., Bangera, M. G., Bumgarner, R. E., Parsek, M. R., Teitzel, G. M., Lory, S.,et al. (2001). Gene expression in Pseudomonas aeruginosa biofilms. Nature 413, 860-864. doi: 10.1038/35101627
87. Winsor, G. L., Lam, D. K. W., Fleming, L., Lo, R., Whiteside, M. D., Yu, N. Y.,et al. (2010). Pseudomonas genome database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39, D596-D600. doi: 10.1093/nar/gkq869
88. Wishart, D. S., Knox, C., Guo, A. C., Cheng, D., Shrivastava, S., Tzur, D.,et al. (2007). DrugBank: a knowledgebase for drugs, drug actions and drug targets. Nucleic Acids Res. 36, D901-D906. doi: 10.1093/nar/gkm958
89. Yonezawa, H., Osaki, T., Kurata, S., Fukuda, M., Kawakami, H., Ochiai, K.,et al. (2009). Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol. 9:197. doi: 10.1186/1471-2180-9-197
90. Yoshimura, F., and Nikaido, H. (1982). Permeability of Pseudomonas aeruginosa outer membrane to hydrophilic solutes. J. Bacteriol. 152, 636-642.
91. Zhang, L., and Mah, T. F. (2008). Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J. Bacteriol. 190, 4447-4452. doi: 10.1128/JB.01655-07