Role of Pseudomonas aeruginosa peptidoglycan-associated outer membrane proteins in vesicle formation

Journal of Bacteriology

Volumn 195, Issue 2, 2013, Pages 213-219

  Wessel, Aimee K ^a   Liew, Jean ^a   Kwon, Taejoon ^a   Marcotte, Edward M ^a   Whiteley, Marvin ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN OPRF; OUTER MEMBRANE PROTEIN OPRI; OUTER MEMBRANE PROTEIN OPRL; PEPTIDOGLYCAN; QUINOLONE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL OUTER MEMBRANE; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; EXOSOMES; LIPOPROTEINS; PEPTIDOGLYCAN; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA;

ENTEROBACTERIACEAE; EUKARYOTA; NEGIBACTERIA; OAT MOSAIC VIRUS; PROKARYOTA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 84872134823     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01253-12     Document Type: Article

References (69)

1. Dorward DW, Garon CF. 1990. DNA is packaged within membranederived vesicles of gram-negative but not gram-positive bacteria. Appl. Environ. Microbiol. 56:1960-1962.
2. Knox KW, Vesk M, Work E. 1966. Relation between excreted lipopolysaccharide complexes and surface structures of a lysine-limited culture of Escherichia coli. J. Bacteriol. 92:1206-1217.
3. Thery C, Zitvogel L, Amigorena S. 2002. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2:569-579.
4. Work E, Knox KW, Vesk M. 1966. The chemistry and electron microscopy of an extracellular lipopolysaccharide from Escherichia coli. Ann. N. Y. Acad. Sci. 133:438-449.
5. Rivera J, Cordero RJ, Nakouzi AS, Frases S, Nicola A, Casadevall A. 2010. Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc. Natl. Acad. Sci. U. S. A. 107:19002-19007.
6. Deatherage BL, Lara JC, Bergsbaken T, Rassoulian Barrett SL, Lara S, Cookson BT. 2009. Biogenesis of bacterial membrane vesicles. Mol. Microbiol. 72:1395-1407.
7. Dorward DW, Garon CF, Judd RC. 1989. Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J. Bacteriol. 171:2499-2505.
8. Hoekstra D, van der Laan JW, de Leij L, Witholt B. 1976. Release of outer membrane fragments from normally growing Escherichia coli. Biochim. Biophys. Acta 455:889-899.
9. Kulp A, Kuehn MJ. 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 64:163-184.
10. Mashburn LM, Whiteley M. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422-425.
11. Beveridge TJ, Makin SA, Kadurugamuwa JL, Li Z. 1997. Interactions between biofilms and the environment. FEMS Microbiol. Rev. 20:291-303.
12. Chatterjee SN, Das J. 1967. Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. J. Gen. Microbiol. 49:1-11.
13. Kadurugamuwa JL, Beveridge TJ. 1995. Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J. Bacteriol. 177:3998-4008.
14. Kahn ME, Maul G, Goodgal SH. 1982. Possible mechanism for donor DNA binding and transport in Haemophilus. Proc. Natl. Acad. Sci. U. S. A. 79:6370-6374.
15. Pettit RK, Judd RC. 1992. The interaction of naturally elaborated blebs from serum-susceptible and serum-resistant strains of Neisseria gonorrhoeae with normal human serum. Mol. Microbiol. 6:729-734.
16. Choi DS, Kim DK, Choi SJ, Lee J, Choi JP, Rho S, Park SH, Kim YK, Hwang D, Gho YS. 2011. Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa. Proteomics 11:3424-3429.
17. Ciofu O, Beveridge TJ, Kadurugamuwa J, Walther-Rasmussen J, Hoiby N. 2000. Chromosomal beta-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa. J. Antimicrob. Chemother. 45:9-13.
18. Kesty NC, Kuehn MJ. 2004. Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J. Biol. Chem. 279:2069-2076.
19. Kuehn MJ, Kesty NC. 2005. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 19:2645-2655.
20. Schooling SR, Beveridge TJ. 2006. Membrane vesicles: an overlooked component of the matrices of biofilms. J. Bacteriol. 188:5945-5957.
21. Schooling SR, Hubley A, Beveridge TJ. 2009. Interactions of DNA with biofilm-derived membrane vesicles. J. Bacteriol. 191:4097-4102.
22. Burdett ID, Murray RG. 1974. Electron microscope study of septum formation in Escherichia coli strains B and B-r during synchronous growth. J. Bacteriol. 119:1039-1056.
23. Burdett ID, Murray RG. 1974. Septum formation in Escherichia coli: characterization of septal structure and the effects of antibiotics on cell division. J. Bacteriol. 119:303-324.
24. Kadurugamuwa JL, Beveridge TJ. 1996. Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J. Bacteriol. 178:2767-2774.
25. Li Z, Clarke AJ, Beveridge TJ. 1996. A major autolysin of Pseudomonas aeruginosa: subcellular distribution, potential role in cell growth and division and secretion in surface membrane vesicles. J. Bacteriol. 178:2479-2488.
26. McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ. 2006. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J. Bacteriol. 188:5385-5392.
27. McBroom AJ, Kuehn MJ. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 63:545-558.
28. Tashiro Y, Sakai R, Toyofuku M, Sawada I, Nakajima-Kambe T, Uchiyama H, Nomura N. 2009. Outer membrane machinery and alginate synthesis regulators control membrane vesicle production in Pseudomonas aeruginosa. J. Bacteriol. 191:7509-7519.
29. Mashburn-Warren L, Howe J, Garidel P, Richter W, Steiniger F, Roessle M, Brandenburg K, Whiteley M. 2008. Interaction of quorum signals with outer membrane lipids: insights into prokaryotic membrane vesicle formation. Mol. Microbiol. 69:491-502.
30. Mashburn-Warren LM, Whiteley M. 2006. Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 61:839-846.
31. Schertzer JW, Whiteley M. 2012. A bilayer-couple model of bacterial outer membrane vesicle biogenesis. mBio 3(2):e00297-11. doi:10.1128/mBio.00297-11.
32. Mashburn-Warren L, Howe J, Brandenburg K, Whiteley M. 2009. Structural requirements of the Pseudomonas quinolone signal for membrane vesicle stimulation. J. Bacteriol. 191:3411-3414.
33. Wensink J, Witholt B. 1981. Outer-membrane vesicles released by normally growing Escherichia coli contain very little lipoprotein. Eur. J. Biochem. 116:331-335.
34. Bernadac A, Gavioli M, Lazzaroni JC, Raina S, Lloubes R. 1998. Escherichia coli tol-pal mutants form outer membrane vesicles. J. Bacteriol. 180:4872-4878.
35. Cascales E, Bernadac A, Gavioli M, Lazzaroni JC, Lloubes R. 2002. Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J. Bacteriol. 184:754-759.
36. Sonntag I, Schwarz H, Hirota Y, Henning U. 1978. Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins. J. Bacteriol. 136: 280-285.
37. Yem DW, Wu HC. 1978. Physiological characterization of an Escherichia coli mutant altered in the structure of murein lipoprotein. J. Bacteriol. 133:1419-1426.
38. Hancock RE, Siehnel R, Martin N. 1990. Outer membrane proteins of Pseudomonas. Mol. Microbiol. 4:1069-1075.
39. Hancock RE, Irvin RT, Costerton JW, Carey AM. 1981. Pseudomonas aeruginosa outer membrane: peptidoglycan-associated proteins. J. Bacteriol. 145:628-631.
40. Sugawara E, Nestorovich EM, Bezrukov SM, Nikaido H. 2006. Pseudomonas aeruginosa porin OprF exists in two different conformations. J. Biol. Chem. 281:16220-16229.
41. Koebnik R. 1995. Proposal for a peptidoglycan-associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins. Mol. Microbiol. 16:1269-1270.
42. Lim A, Jr, De Vos D, Brauns M, Mossialos D, Gaballa A, Qing D, Cornelis P. 1997. Molecular and immunological characterization of OprL, the 18 kDa outer-membrane peptidoglycan-associated lipoprotein (PAL) of Pseudomonas aeruginosa. Microbiology 143(Pt 5):1709-1716.
43. Mizuno T. 1981. A novel peptidoglycan-associated lipoprotein (PAL) found in the outer membrane of Proteus mirabilis and other Gramnegative bacteria. J. Biochem. 89:1039-1049.
44. Mizuno T. 1979. A novel peptidoglycan-associated lipoprotein found in the cell envelope of Pseudomonas aeruginosa and Escherichia coli. J. Biochem. 86:991-1000.
45. Duchene M, Barron C, Schweizer A, von Specht BU, Domdey H. 1989. Pseudomonas aeruginosa outer membrane lipoprotein I gene: molecular cloning, sequence, and expression in Escherichia coli. J. Bacteriol. 171: 4130-4137.
46. Mizuno T, Kageyama M. 1979. Isolation of characterization of a major outer membrane protein of Pseudomonas aeruginosa. Evidence for the occurrence of a lipoprotein. J. Biochem. 85:115-122.
47. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. de Lorenzo V, Timmis KN. 1994. Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5-and Tn10-derived minitransposons. Methods Enzymol. 235:386-405.
49. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E, Wu G, Villanueva J, Wei T, Ausubel FM. 2006. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl. Acad. Sci. U. S. A. 103:2833-2838.
50. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
51. Pearson JP, Pesci EC, Iglewski BH. 1997. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J. Bacteriol. 179:5756-5767.
52. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. 1997. Short protocols in molecular biology, 3rd ed. John Wiley & Sons, Inc, New York, NY.
53. Schertzer JW, Brown SA, Whiteley M. 2010. Oxygen levels rapidly modulate Pseudomonas aeruginosa social behaviours via substrate limitation of PqsH. Mol. Microbiol. 77:1527-1538.
54. Stewart JC. 1980. Colorimetric determination of phospholipids with ammonium ferrothiocyanate. Anal. Biochem. 104:10-14.
55. Kwon T, Choi H, Vogel C, Nesvizhskii AI, Marcotte EM. 2011. MSblender: a probabilistic approach for integrating peptide identifications from multiple database search engines. J. Proteome Res. 10:2949-2958.
56. Winsor GL, Lam DK, Fleming L, Lo R, Whiteside MD, Yu NY, Hancock RE, Brinkman FS. 2011. Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39:D596-D600. doi:10.1093/nar/gkq869.
57. Park CY, Klammer AA, Kall L, MacCoss MJ, Noble WS. 2008. Rapid and accurate peptide identification from tandem mass spectra. J. Proteome Res. 7:3022-3027.
58. Craig R, Beavis RC. 2004. TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20:1466-1467.
59. Keller A, Eng J, Zhang N, Li XJ, Aebersold R. 2005. A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol. Syst. Biol. 1:2005.0017. doi:10.1038/msb4100024.
60. Tanner S, Shu H, Frank A, Wang LC, Zandi E, Mumby M, Pevzner PA, Bafna V. 2005. InsPecT: identification of posttranslationally modified peptides from tandem mass spectra. Anal. Chem. 77:4626-4639.
61. Kim S, Mischerikow N, Bandeira N, Navarro JD, Wich L, Mohammed S, Heck AJ, Pevzner PA. 2010. The generating function of CID, ETD, and CID/ETD pairs of tandem mass spectra: applications to database search. Mol. Cell. Proteomics 9:2840-2852.
62. Lu P, Vogel C, Wang R, Yao X, Marcotte EM. 2007. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 25:117-124.
63. Vogel C, Marcotte EM. 2008. Calculating absolute and relative protein abundance from mass spectrometry-based protein expression data. Nat. Protoc. 3:1444-1451.
64. Lee DG, Urbach JM, Wu G, Liberati NT, Feinbaum RL, Miyata S, Diggins LT, He J, Saucier M, Deziel E, Friedman L, Li L, Grills G, Montgomery K, Kucherlapati R, Rahme LG, Ausubel FM. 2006. Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol. 7:R90. doi:10.1186/gb-2006-7-10-r90.
65. D'Argenio DA, Calfee MW, Rainey PB, Pesci EC. 2002. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 184:6481-6489.
66. Palmer GC, Schertzer JW, Mashburn-Warren L, Whiteley M. 2011. Quantifying Pseudomonas aeruginosa quinolones and examining their interactions with lipids. Methods Mol. Biol. 692:207-217.
67. Fito-Boncompte L, Chapalain A, Bouffartigues E, Chaker H, Lesouhaitier O, Gicquel G, Bazire A, Madi A, Connil N, Veron W, Taupin L, Toussaint B, Cornelis P, Wei Q, Shioya K, Deziel E, Feuilloley MG, Orange N, Dufour A, Chevalier S. 2011. Full virulence of Pseudomonas aeruginosa requires OprF. Infect. Immun. 79:1176-1186.
68. Lepine F, Deziel E, Milot S, Rahme LG. 2003. A stable isotope dilution assay for the quantification of the Pseudomonas quinolone signal in Pseudomonas aeruginosa cultures. Biochim. Biophys. Acta 1622:36-41.
69. Niewerth H, Bergander K, Chhabra SR, Williams P, Fetzner S. 2011. Synthesis and biotransformation of 2-alkyl-4(1H)-quinolones by recombinant Pseudomonas putida KT2440. Appl. Microbiol. Biotechnol. 91: 1399-1408.