Bacterial membrane vesicles, an overlooked environmental colloid: Biology, environmental perspectives and applications

Advances in Colloid and Interface Science

Volumn 226, Issue , 2015, Pages 65-77

  Toyofuku, Masanori ^a   Tashiro, Yosuke ^b   Hasegawa, Yusuke ^b   Kurosawa, Masaharu ^a   Nomura, Nobuhiko ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b SHIZUOKA UNIVERSITY   (Japan)

Author keywords

Bacteria; Biotechnology; Membrane vesicle; Nanobiocatalysts; Nanotechnology

Indexed keywords

BIOLOGICAL SYSTEMS; BIOTECHNOLOGY; COLLOIDS; CONTROLLED DRUG DELIVERY; CYTOLOGY; GENE TRANSFER; LIPOSOMES; NANOTECHNOLOGY; PHOSPHOLIPIDS; TARGETED DRUG DELIVERY;

BACTERIAL MEMBRANES; BIOLOGICAL FUNCTIONS; DRUG DELIVERY SYSTEM; ENVIRONMENTAL COLLOIDS; MEMBRANE VESICLES; NANOBIOCATALYSTS; PHOSPHOLIPID VESICLES; PHYSICOCHEMICAL FEATURES;

BACTERIA;

COLLOID;

ANIMAL; BACTERIUM; CELL MEMBRANE; COLLOID; CYTOLOGY; ENVIRONMENT; HUMAN; METABOLISM;

ANIMALS; BACTERIA; CELL MEMBRANE; COLLOIDS; ENVIRONMENT; HUMANS;

EID: 84958770778     PISSN: 00018686     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cis.2015.08.013     Document Type: Review

References (202)

1. J.H. Kim, J. Lee, J. Park, and Y.S. Gho Gram-negative and Gram-positive bacterial extracellular vesicles Semin Cell Dev Biol 2015 10.1016/j.semcdb.2015.02.006
2. H.A. Bladen, and J.F. Waters Electron microscopic study of some strains of Bacteroides J Bacteriol 86 1963 1339 1344
3. M.E. Bayer, and T.F. Anderson The surface structure of Escherichia coli Proc Natl Acad Sci U S A 54 1965 1592 1599
4. S.N. Chatterjee, and J. Das Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae J Gen Microbiol 49 1967 1 11
5. S.N. De Enterotoxicity of bacteria-free culture-filtrate of Vibrio cholerae Nature 183 1959 1533 1534
6. D.G. Bishop, and E. Work An extracellular glycolipid produced by Escherichia coli grown under lysine-limiting conditions Biochem J 96 1965 567 576
7. A.J. McBroom, A.P. Johnson, S. Vemulapalli, and M.J. Kuehn Outer membrane vesicle production by Escherichia coli is independent of membrane instability J Bacteriol 188 2006 5385 5392
8. T. Beveridge Structures of gram-negative cell walls and their derived membrane vesicles J Bacteriol 181 1999 4725 4733
9. T.J. Beveridge, S.A. Makin, J.L. Kadurugamuwa, and Z. Li Interactions between biofilms and the environment FEMS Microbiol Rev 20 1997 291 303
10. P. Giesbrecht, T. Kersten, H. Maidhof, and J. Wecke Staphylococcal cell wall: morphogenesis and fatal variations in the presence of penicillin Microbiol Mol Biol Rev 62 1998 1371 1414
11. J. Buffle, and G.G. Leppard Characterization of aquatic colloids and macromolecules. 1. Structure and behavior of colloidal material Environ Sci Technol 29 1995 2169 2175
12. S.J. Bauman, and M.J. Kuehn Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response Microbes Infect 8 2006 2400 2408
13. I.W. Devoe, and J.E. Gilchrist Release of endotoxin in the form of cell wall blebs during in vitro growth of Neisseria meningitidis J Exp Med 138 1973 1156 1167
14. H. Gankema, J. Wensink, P.A. Guinée, W.H. Jansen, and B. Witholt Some characteristics of the outer membrane material released by growing enterotoxigenic Escherichia coli Infect Immun 29 1980 704 713
15. D. Hoekstra, J.W. van der Laan, L. de Leij, and B. Witholt Release of outer membrane fragments from normally growing Escherichia coli Biochim Biophys Acta 455 1976 889 899
16. M. Renelli, V. Matias, R.Y. Lo, and T.J. Beveridge DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential Microbiology 150 2004 2161 2169
17. D.S. Choi, D.K. Kim, S.J. Choi, J. Lee, J.P. Choi, S. Rho, and et al. Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa Proteomics 11 2011 3424 3429
18. E.Y. Lee, J.Y. Bang, G.W. Park, D.S. Choi, J.S. Kang, H.J. Kim, and et al. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli Proteomics 7 2007 3143 3153
19. E.Y. Lee, D.S. Choi, K.P. Kim, and Y.S. Gho Proteomics in gram-negative bacterial outer membrane vesicles Mass Spectrom Rev 27 2008 535 555
20. F. Berlanda Scorza, F. Doro, M.J. Rodriguez-Ortega, M. Stella, S. Liberatori, A.R. Taddei, and et al. Proteomics characterization of outer membrane vesicles from the extraintestinal pathogenic Escherichia coli DeltatolR IHE3034 mutant Mol Cell Proteomics 7 2008 473 485
21. M.F. Haurat, J. Aduse-Opoku, M. Rangarajan, L. Dorobantu, M.R. Gray, M.A. Curtis, and et al. Selective sorting of cargo proteins into bacterial membrane vesicles J Biol Chem 286 2011 1269 1276
22. M. Toyofuku, B. Roschitzki, K. Riedel, and L. Eberl Identification of proteins associated with the Pseudomonas aeruginosa biofilm extracellular matrix J Proteome Res 11 2012 4906 4915
23. S.A. Makin, and T.J. Beveridge Pseudomonas aeruginosa PAO1 ceases to express serotype-specific lipopolysaccharide at 45 degrees C J Bacteriol 178 1996 3350 3352
24. J.S. Lam, V.L. Taylor, S.T. Islam, Y. Hao, and D. Kocincova Genetic and Functional Diversity of Pseudomonas aeruginosa Lipopolysaccharide Front Microbiol 2 2011 118
25. H.L. Rocchetta, L.L. Burrows, and J.S. Lam Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa Microbiol Mol Biol Rev 63 1999 523 553
26. S.A. Makin, and T.J. Beveridge The influence of A-band and B-band lipopolysaccharide on the surface characteristics and adhesion of Pseudomonas aeruginosa to surfaces Microbiology 142 Pt 2 1996 299 307
27. J.L. Kadurugamuwa, and T.J. Beveridge 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 1995 3998 4008
28. Y. Tashiro, A. Inagaki, M. Shimizu, S. Ichikawa, N. Takaya, T. Nakajima-Kambe, and et al. Characterization of phospholipids in membrane vesicles derived from Pseudomonas aeruginosa Biosci Biotechnol Biochem 75 2011 605 607
29. L.D. Renner, and D.B. Weibel Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes Proc Natl Acad Sci U S A 108 2011 6264 6269
30. S. Kato, Y. Kowashi, and D.R. Demuth Outer membrane-like vesicles secreted by Actinobacillus actinomycetemcomitans are enriched in leukotoxin Microb Pathog 32 2002 1 13
31. M. Bramkamp, and D. Lopez Exploring the existence of lipid rafts in bacteria Microbiol Mol Biol Rev 79 2015 81 100
32. A.L. Horstman, and M.J. Kuehn Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles J Biol Chem 275 2000 12489 124896
33. E. Papanikou, S. Karamanou, and A. Economou Bacterial protein secretion through the translocase nanomachine Nat Rev Microbiol 5 2007 839 851
34. J. Wensink, and B. Witholt Outer-membrane vesicles released by normally growing Escherichia coli contain very little lipoprotein Eur J Biochem 116 1981 331 335
35. M. Toyofuku, S. Zhou, I. Sawada, N. Takaya, H. Uchiyama, and N. Nomura Membrane vesicle formation is associated with pyocin production under denitrifying conditions in Pseudomonas aeruginosa PAO1 Environ Microbiol 16 2014 2927 2938
36. R.K. Pettit, and R.C. Judd Characterization of naturally elaborated blebs from serum-susceptible and serum-resistant strains of Neisseria gonorrhoeae Mol Microbiol 6 1992 723 728
37. S.N. Wai, B. Lindmark, T. Soderblom, A. Takade, M. Westermark, J. Oscarsson, and et al. Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin Cell 115 2003 25 35
38. B. Lindmark, P.K. Rompikuntal, K. Vaitkevicius, T. Song, Y. Mizunoe, B.E. Uhlin, and et al. Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni BMC Microbiol 9 2009 220
39. D.W. Dorward, and C.F. Garon DNA is packaged within membrane-derived vesicles of Gram-negative but not Gram-positive bacteria Appl Environ Microbiol 56 1990 1960 1962
40. G.L. Kolling, and K.R. Matthews Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7 Appl Environ Microbiol 65 1999 1843 1848
41. L.M. Mashburn, and M. Whiteley Membrane vesicles traffic signals and facilitate group activities in a prokaryote Nature 437 2005 422 425
42. M.R. Kim, S.W. Hong, E.B. Choi, W.H. Lee, Y.S. Kim, S.G. Jeon, and et al. Staphylococcus aureus-derived extracellular vesicles induce neutrophilic pulmonary inflammation via both Th1 and Th17 cell responses Allergy 67 2012 1271 1281
43. Y.S. Kim, E.J. Choi, W.H. Lee, S.J. Choi, T.Y. Roh, J. Park, and et al. Extracellular vesicles, especially derived from Gram-negative bacteria, in indoor dust induce neutrophilic pulmonary inflammation associated with both Th1 and Th17 cell responses Clin Exp Allergy 43 2013 443 454
44. S.R. Schooling, and T.J. Beveridge Membrane vesicles: an overlooked component of the matrices of biofilms J Bacteriol 188 2006 5945 5957
45. H. Yonezawa, T. Osaki, S. Kurata, M. Fukuda, H. Kawakami, K. Ochiai, and et al. Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation BMC Microbiol 9 2009 197
46. H.C. Flemming, and J. Wingender The biofilm matrix Nat Rev Microbiol 8 2010 623 633
47. S. Shibata, and K.L. Visick Sensor kinase RscS induces the production of antigenically distinct outer membrane vesicles that depend on the symbiosis polysaccharide locus in Vibrio fischeri J Bacteriol 194 2012 185 194
48. P.P. Shao, L.R. Comolli, and R. Bernier-Latmani Membrane vesicles as a novel strategy for shedding encrusted cell surfaces Mineral 4 2014 74 88
49. H. Palsdottir, J.P. Remis, C. Schaudinn, E. O'Toole, R. Lux, W. Shi, and et al. Three-dimensional macromolecular organization of cryofixed Myxococcus xanthus biofilms as revealed by electron microscopic tomography J Bacteriol 191 2009 2077 2082
50. E. Banin, M.L. Vasil, and E.P. Greenberg Iron and Pseudomonas aeruginosa biofilm formation Proc Natl Acad Sci U S A 102 2005 11076 11081
51. S.J. Biller, F. Schubotz, S.E. Roggensack, A.W. Thompson, R.E. Summons, and S.W. Chisholm Bacterial vesicles in marine ecosystems Science 343 2014 183 186
52. N. Soler, M. Krupovic, E. Marguet, and P. Forterre Membrane vesicles in natural environments: a major challenge in viral ecology ISME J 9 2014 793 796
53. W.C. Chin, M.V. Orellana, and P. Verdugo Spontaneous assembly of marine dissolved organic matter into polymer gels Nature 391 1998 568 572
54. M. Suzumura Phospholipids in marine environments: a review Talanta 66 2005 422 434
55. A. Shibata, K. Kogure, I. Koike, and K. Ohwada Formation of submicron colloidal particles from marine bacteria by viral infection Mar Ecol Prog Ser 155 1997 303 307
56. E. Bar-Zeev, U. Passow, S.R. Castrillon, and M. Elimelech Transparent exopolymer particles: from aquatic environments and engineered systems to membrane biofouling Environ Sci Technol 49 2015 691 707
57. U. Passow Production of transparent exopolymer particles (TEP) by phyto- and bacterioplankton Mar Ecol Prog Ser 236 2002 1 12
58. E. Bar-Zeev, I. Berman-Frank, O. Girshevitz, and T. Berman Revised paradigm of aquatic biofilm formation facilitated by microgel transparent exopolymer particles Proc Natl Acad Sci U S A 109 2012 9119 9124
59. T. Berman, R. Mizrahi, and C.G. Dosoretz Transparent exopolymer particles (TEP): a critical factor in aquatic biofilm initiation and fouling on filtration membranes Desalination 276 2011 184 190
60. S. Judd A review of fouling of membrane bioreactors in sewage treatment Water Sci Technol 49 2004 229 235
61. G.X. Song, J. Wang, C.A. Chiu, and P. Westerhoff Biogenic nanoscale colloids in wastewater effluents Environ Sci Technol 44 2010 8216 8222
62. M.C. Barry, K. Hristovski, and P. Westerhoff Membrane fouling by vesicles and prevention through ozonation Environ Sci Technol 48 2014 7349 7356
63. J.H. Jorgensen, J.C. Lee, and H.R. Pahren Rapid detection of bacterial endotoxins in drinking-water and renovated wastewater Appl Environ Microbiol 32 1976 347 351
64. N.R. Di Luzio, and T.J. Friedmann Bacterial endotoxins in the environment Nature 244 1973 49 51
65. A. Kulp, and M.J. Kuehn Biological functions and biogenesis of secreted bacterial outer membrane vesicles Annu Rev Microbiol 64 2010 163 184
66. R. Nakao, K. Kikushima, H. Higuchi, N. Obana, N. Nomura, D. Bai, and et al. A novel approach for purification and selective capture of membrane vesicles of the periodontopathic bacterium, Porphyromonas gingivalis: membrane vesicles bind to magnetic beads coated with epoxy groups in a noncovalent, species-specific manner PLoS One 9 2014 e95137
67. J. Wen, S. Zhou, and J. Chen Colorimetric detection of Shewanella oneidensis based on immunomagnetic capture and bacterial intrinsic peroxidase activity Sci Rep 4 2014 5191
68. Y. Tashiro, R. Sakai, M. Toyofuku, I. Sawada, T. Nakajima-Kambe, H. Uchiyama, and et al. Outer membrane machinery and alginate synthesis regulators control membrane vesicle production in Pseudomonas aeruginosa J Bacteriol 191 2009 7509 7519
69. L. Brown, A. Kessler, P. Cabezas-Sanchez, J.L. Luque-Garcia, and A. Casadevall Extracellular vesicles produced by the Gram-positive bacterium Bacillus subtilis are disrupted by the lipopeptide surfactin Mol Microbiol 93 2014 183 198
70. I.A. Macdonald, and M.J. Kuehn Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa J Bacteriol 195 2013 2971 2981
71. C. Schwechheimer, A. Kulp, and M.J. Kuehn Modulation of bacterial outer membrane vesicle production by envelope structure and content BMC Microbiol 14 2014 324
72. A.J. Manning, and M.J. Kuehn Contribution of bacterial outer membrane vesicles to innate bacterial defense BMC Microbiol 11 2011 258
73. M. Ionescu, P.A. Zaini, C. Baccari, S. Tran, A.M. da Silva, and S.E. Lindow Xylella fastidiosa outer membrane vesicles modulate plant colonization by blocking attachment to surfaces Proc Natl Acad Sci U S A 111 2014 E3910 E3918
74. A. Wieser, E. Storz, G. Liegl, A. Peter, M. Pritsch, J. Shock, and et al. Efficient quantification and characterization of bacterial outer membrane derived nano-particles with flow cytometric analysis Int J Med Microbiol 304 2014 1032 1037
75. Y. Tashiro, S. Ichikawa, M. Shimizu, M. Toyofuku, N. Takaya, T. Nakajima-Kambe, and et al. Variation of physiochemical properties and cell association activity of membrane vesicles with growth phase in Pseudomonas aeruginosa Appl Environ Microbiol 76 2010 3732 3739
76. Y. Jiang, Q. Kong, K.L. Roland, and R. Curtiss 3rd Membrane vesicles of Clostridium perfringens type A strains induce innate and adaptive immunity Int J Med Microbiol 304 2014 431 443
77. T.N. Ellis, and M.J. Kuehn Virulence and immunomodulatory roles of bacterial outer membrane vesicles Microbiol Mol Biol Rev 74 2010 81 94
78. T. Aldick, M. Bielaszewska, B.E. Uhlin, H.U. Humpf, S.N. Wai, and H. Karch Vesicular stabilization and activity augmentation of enterohaemorrhagic Escherichia coli haemolysin Mol Microbiol 71 2009 1496 1508
79. V. Gujrati, S. Kim, S.H. Kim, J.J. Min, H.E. Choy, S.C. Kim, and et al. Bioengineered bacterial outer membrane vesicles as cell-specific drug-delivery vehicles for cancer therapy ACS Nano 8 2014 1525 1537
80. J.M. Bomberger, D.P. Maceachran, B.A. Coutermarsh, S. Ye, G.A. O'Toole, and B.A. Stanton Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles PLoS Pathog 5 2009 e1000382
81. A. Yamaoka, M. Kataoka, K. Kawasaki, E. Kobayashi, Y. Shigeri, and K. Watanabe Meiothermus ruber H328 enhances the production of membrane vesicles for feather degradation Biosci Biotechnol Biochem 78 2014 1623 1625
82. T.M. Voegel, J.G. Warren, A. Matsumoto, M.M. Igo, and B.C. Kirkpatrick Localization and characterization of Xylella fastidiosa hemagglutinin adhesins Microbiology 156 2010 2172 2179
83. V. Ricci, V. Chiozzi, V. Necchi, A. Oldani, M. Romano, E. Solcia, and et al. Free-soluble and outer membrane vesicle-associated VacA from Helicobacter pylori: two forms of release, a different activity Biochem Biophys Res Commun 337 2005 173 178
84. E.Y. Furuya, and F.D. Lowy Antimicrobial-resistant bacteria in the community setting Nat Rev Microbiol 4 2006 36 45
85. S. Hagemann, L. Stoger, M. Kappelmann, I. Hassl, A. Ellinger, and B. Velimirov DNA-bearing membrane vesicles produced by Ahrensia kielensis and Pseudoalteromonas marina J Basic Microbiol 54 2014 1062 1072
86. S.R. Schooling, A. Hubley, and T.J. Beveridge Interactions of DNA with biofilm-derived membrane vesicles J Bacteriol 191 2009 4097 4102
87. S. Yaron, G.L. Kolling, L. Simon, and K.R. Matthews Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria Appl Environ Microbiol 66 2000 4414 4420
88. S. Fulsundar, K. Harms, G.E. Flaten, P.J. Johnsen, B.A. Chopade, and K.M. Nielsen Gene transfer potential of outer membrane vesicles of Acinetobacter baylyi and effects of stress on vesiculation Appl Environ Microbiol 80 2014 3469 3483
89. C. Rumbo, E. Fernandez-Moreira, M. Merino, M. Poza, J.A. Mendez, N.C. Soares, and et al. Horizontal transfer of the OXA-24 carbapenemase gene via outer membrane vesicles: a new mechanism of dissemination of carbapenem resistance genes in Acinetobacter baumannii Antimicrob Agents Chemother 55 2011 3084 3090
90. M. Gaudin, E. Gauliard, S. Schouten, L. Houel-Renault, P. Lenormand, E. Marguet, and et al. Hyperthermophilic archaea produce membrane vesicles that can transfer DNA Environ Microbiol Rep 5 2013 109 116
91. E. Marguet, M. Gaudin, E. Gauliard, I. Fourquaux, S. le Blond du Plouy, I. Matsui, and et al. Membrane vesicles, nanopods and/or nanotubes produced by hyperthermophilic archaea of the genus Thermococcus Biochem Soc Trans 41 2013 436 442
92. J.W. Schertzer, M.L. Boulette, and M. Whiteley More than a signal: non-signaling properties of quorum sensing molecules Trends Microbiol 17 2009 189 195
93. J.W. Schertzer, and M. Whiteley Bacterial outer membrane vesicles in trafficking, communication and the host-pathogen interaction J Mol Microbiol Biotechnol 23 2013 118 130
94. R. Prados-Rosales, B.C. Weinrick, D.G. Pique, W.R. Jacobs Jr., A. Casadevall, and G.M. Rodriguez Role for Mycobacterium tuberculosis membrane vesicles in iron acquisition J Bacteriol 196 2014 1250 1256
95. S. Rakoff-Nahoum, M.J. Coyne, and L.E. Comstock An ecological network of polysaccharide utilization among human intestinal symbionts Curr Biol 24 2014 40 49
96. C.R. Myers, and K.H. Nealson Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor Science 240 1988 1319 1321
97. K. Rabaey, and R.A. Rozendal Microbial electrosynthesis - revisiting the electrical route for microbial production Nat Rev Microbiol 8 2010 706 716
98. S. Pirbadian, S.E. Barchinger, K.M. Leung, H.S. Byun, Y. Jangir, R.A. Bouhenni, and et al. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components Proc Natl Acad Sci U S A 111 2014 12883 12888
99. A. Shetty, S. Chen, E.I. Tocheva, G.J. Jensen, and W.J. Hickey Nanopods: a new bacterial structure and mechanism for deployment of outer membrane vesicles PLoS One 6 2011 e20725
100. Y. Gorby, J. McLean, A. Korenevsky, K. Rosso, M.Y. El-Naggar, and T.J. Beveridge Redox-reactive membrane vesicles produced by Shewanella Geobiology 6 2008 232 241
101. H. Kobayashi, K. Uematsu, H. Hirayama, and K. Horikoshi Novel toluene elimination system in a toluene-tolerant microorganism J Bacteriol 182 2000 6451 6455
102. T. Baumgarten, J. Vazquez, C. Bastisch, W. Veron, M.G. Feuilloley, S. Nietzsche, and et al. Alkanols and chlorophenols cause different physiological adaptive responses on the level of cell surface properties and membrane vesicle formation in Pseudomonas putida DOT-T1E Appl Microbiol Biotechnol 93 2012 837 845
103. B. van de Waterbeemd, G. Zomer, P. Kaaijk, N. Ruiterkamp, R.H. Wijffels, G.P. van den Dobbelsteen, and et al. Improved production process for native outer membrane vesicle vaccine against Neisseria meningitidis PLoS One 8 2013 e65157
104. S.C. Jang, S.R. Kim, Y.J. Yoon, K.S. Park, J.H. Kim, J. Lee, and et al. In vivo kinetic biodistribution of nano-sized outer membrane vesicles derived from bacteria Small 11 2015 456 461
105. V.A. Ray, A. Driks, and K.L. Visick Identification of a novel matrix protein that promotes biofilm maturation in Vibrio fischeri J Bacteriol 197 2015 518 528
106. W. Hashimoto, Y. Miyamoto, M. Yamamoto, F. Yoneyama, and K. Murata A novel bleb-dependent polysaccharide export system in nitrogen-fixing Azotobacter vinelandii subjected to low nitrogen gas levels Int Microbiol 16 2013 35 44
107. C.B. Whitchurch, T. Tolker-Nielsen, P.C. Ragas, and J.S. Mattick Extracellular DNA required for bacterial biofilm formation Science 295 2002 1487
108. N. Kesty, K. Mason, M. Reedy, S. Miller, and M. Kuehn Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells EMBO J 23 2004 4538 4549
109. S.J. Bauman, and M.J. Kuehn Pseudomonas aeruginosa vesicles associate with and are internalized by human lung epithelial cells BMC Microbiol 9 2009 26
110. H. Parker, K. Chitcholtan, M.B. Hampton, and J.I. Keenan Uptake of Helicobacter pylori outer membrane vesicles by gastric epithelial cells Infect Immun 78 2010 5054 5061
111. T. Gutsmann, M. Müller, S.F. Carroll, R.C. MacKenzie, A. Wiese, and U. Seydel Dual role of lipopolysaccharide (LPS)-binding protein in neutralization of LPS and enhancement of LPS-induced activation of mononuclear cells Infect Immun 69 2001 6942 6950
112. J. Jäger, S. Keese, M. Roessle, M. Steinert, and A.B. Schromm Fusion of Legionella pneumophila outer membrane vesicles with eukaryotic membrane systems is a mechanism to deliver pathogen factors to host cell membranes Cell Microbiol 17 2014 607 620
113. J.L. Kadurugamuwa, and T.J. Beveridge Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics J Bacteriol 178 1996 2767 2774
114. Z. Li, A.J. Clarke, and T.J. Beveridge Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria J Bacteriol 180 1998 5478 5483
115. J.L. Kadurugamuwa, A. Mayer, P. Messner, M. Sára, U.B. Sleytr, and T.J. Beveridge S-layered Aneurinibacillus and Bacillus spp. are susceptible to the lytic action of Pseudomonas aeruginosa membrane vesicles J Bacteriol 180 1998 2306 2311
116. Y. Tashiro, H. Uchiyama, and N. Nomura Multifunctional membrane vesicles in Pseudomonas aeruginosa Environ Microbiol 14 2012 1349 1362
117. T. Baumgarten, S. Sperling, J. Seifert, M. von Bergen, F. Steiniger, L.Y. Wick, and et al. Membrane vesicle formation as a multiple-stress response mechanism enhances Pseudomonas putida DOT-T1E cell surface hydrophobicity and biofilm formation Appl Environ Microbiol 78 2012 6217 6224
118. I. Sonntag, H. Schwarz, Y. Hirota, and U. Henning Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins J Bacteriol 136 1978 280 285
119. H. Suzuki, Y. Nishimura, S. Yasuda, A. Nishimura, M. Yamada, and Y. Hirota Murein-lipoprotein of Escherichia coli: a protein involved in the stabilization of bacterial cell envelope Mol Gen Genet 167 1978 1 9
120. D.W. Yem, and H.C. Wu Physiological characterization of an Escherichia coli mutant altered in the structure of murein lipoprotein J Bacteriol 133 1978 1419 1426
121. A. Bernadac, M. Gavioli, J.C. Lazzaroni, S. Raina, and R. Lloubés Escherichia coli tol-pal mutants form outer membrane vesicles J Bacteriol 180 1998 4872 4878
122. B.L. Deatherage, J.C. Lara, T. Bergsbaken, S.L.R. Barrett, S. Lara, and B.T. Cookson Biogenesis of bacterial membrane vesicles Mol Microbiol 72 2009 1395 1407
123. H.T. McMahon, and J.L. Gallop Membrane curvature and mechanisms of dynamic cell membrane remodelling Nature 438 2005 590 596
124. N. Unwin Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution J Mol Biol 346 2005 967 989
125. L. Zhou, R. Srisatjaluk, D. Justus, and R. Doyle On the origin of membrane vesicles in Gram-negative bacteria FEMS Microbiol Lett 163 1998 223 228
126. M. Kaparakis, L. Turnbull, L. Carneiro, S. Firth, H.A. Coleman, H.C. Parkington, and et al. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells Cell Microbiol 12 2010 372 385
127. J.-i. Hayashi, N. Hamada, and H.K. Kuramitsu The autolysin of Porphyromonas gingivalis is involved in outer membrane vesicle release FEMS Microbiol Lett 216 2002 217 222
128. M.F. Haurat, W. Elhenawy, and F. Feldman Mario Prokaryotic membrane vesicles: new insights on biogenesis and biological roles Biol Chem 2015 95
129. A.J. McBroom, and M.J. Kuehn Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response Mol Microbiol 63 2007 545 558
130. M.C. Mansilla, L.E. Cybulski, D. Albanesi, and D. de Mendoza Control of membrane lipid fluidity by molecular thermosensors J Bacteriol 186 2004 6681 6688
131. L. Mashburn-Warren, J. Howe, P. Garidel, W. Richter, F. Steiniger, M. Roessle, and et al. Interaction of quorum signals with outer membrane lipids: insights into prokaryotic membrane vesicle formation Mol Microbiol 69 2008 491 502
132. J. Zhang, X. Li, and X. Li Stimuli-triggered structural engineering of synthetic and biological polymeric assemblies Prog Polym Sci 37 2012 1130 1176
133. C.-M. Lin, C.-S. Li, Y.-J. Sheng, D.T. Wu, and H.-K. Tsao Size-dependent properties of small unilamellar vesicles formed by model lipids Langmuir 28 2012 689 700
134. Y. Tashiro, S. Ichikawa, T. Nakajima-Kambe, H. Uchimura, and N. Nomura Pseudomonas quinolone signal affects membrane vesicle production in not only Gram-negative but also Gram-positive bacteria Microbes Environ 25 2010 120 125
135. J. Kadurugamuwa, and T. Beveridge Delivery of the non-membrane-permeative antibiotic gentamicin into mammalian cells by using Shigella flexneri membrane vesicles Antimicrob Agents Chemother 42 1998 1476 1483
136. L.M. Mashburn-Warren, and M. Whiteley Special delivery: vesicle trafficking in prokaryotes Mol Microbiol 61 2006 839 846
137. J.W. Schertzer, and M. Whiteley A bilayer-couple model of bacterial outer membrane vesicle biogenesis mBio 3 2012
138. J. Ramos, E. Duque, M. Huertas, and A. Haidour Isolation and expansion of the catabolic potential of a Pseudomonas putida strain able to grow in the presence of high concentrations of aromatic hydrocarbons J Bacteriol 177 1995 3911 3916
139. J.L. Baker, L. Chen, J.A. Rosenthal, D. Putnam, and M.P. DeLisa Microbial biosynthesis of designer outer membrane vesicles Curr Opin Biotechnol 29 2014 76 84
140. H.J. Marvin, M.B. ter Beest, and B. Witholt Release of outer membrane fragments from wild-type Escherichia coli and from several E. coli lipopolysaccharide mutants by EDTA and heat shock treatments J Bacteriol 171 1989 5262 5267
141. J.L. Kadurugamuwa, and T.J. Beveridge Natural release of virulence factors in membrane vesicles by Pseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release J Antimicrob Chemother 40 1997 615 621
142. B. van de Waterbeemd, G.P. Mommen, J.L. Pennings, M.H. Eppink, R.H. Wijffels, L.A. van der Pol, and et al. Quantitative proteomics reveals distinct differences in the protein content of outer membrane vesicle vaccines J Proteome Res 12 2013 1898 1908
143. R. Lloubés, E. Cascales, A. Walburger, E. Bouveret, C. Lazdunski, A. Bernadac, and et al. The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152 2001 523 529
144. J.Y. Kim, A.M. Doody, D.J. Chen, G.H. Cremona, M.L. Shuler, D. Putnam, and et al. Engineered bacterial outer membrane vesicles with enhanced functionality J Mol Biol 380 2008 51 66
145. T. Henry, S. Pommier, L. Journet, A. Bernadac, J.P. Gorvel, and R. Lloubès Improved methods for producing outer membrane vesicles in Gram-negative bacteria Res Microbiol 155 2004 437 446
146. N.C. Kesty, and M.J. Kuehn Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles J Biol Chem 279 2004 2069 2076
147. E. van Bloois, R.T. Winter, H. Kolmar, and M.W. Fraaije Decorating microbes: surface display of proteins on Escherichia coli Trends Biotechnol 29 2011 79 86
148. S.K. Yim, D.H. Kim, H.C. Jung, J.G. Pan, H.S. Kang, T. Ahn, and et al. Surface display of heme- and diflavin-containing cytochrome P450 BM3 in Escherichia coli: a whole cell biocatalyst for oxidation J Microbiol Biotechnol 20 2010 712 717
149. M. Park, Q. Sun, F. Liu, M.P. DeLisa, and W. Chen Positional assembly of enzymes on bacterial outer membrane vesicles for cascade reactions PLoS One 9 2014 e97103
150. R.H. Doi, and A. Kosugi Cellulosomes: plant-cell-wall-degrading enzyme complexes Nat Rev Microbiol 2 2004 541 551
151. Y. Malam, M. Loizidou, and A.M. Seifalian Liposomes and nanoparticles: nanosized vehicles for drug delivery in cancer Trends Pharmacol Sci 30 2009 592 599
152. G. Vernikos, and D. Medini Bexsero(R) chronicle Pathog Glob Health 108 2014 305 316
153. B. van de Waterbeemd, M. Streefland, P. van der Ley, B. Zomer, H. van Dijken, D. Martens, and et al. Improved OMV vaccine against Neisseria meningitidis using genetically engineered strains and a detergent-free purification process Vaccine 28 2010 4810 4816
154. P. van der Ley, and G. van den Dobbelsteen Next-generation outer membrane vesicle vaccines against Neisseria meningitidis based on nontoxic LPS mutants Hum Vaccin 7 2011 886 890
155. G.P. van den Dobbelsteen, H.H. van Dijken, S. Pillai, and L. van Alphen Immunogenicity of a combination vaccine containing pneumococcal conjugates and meningococcal PorA OMVs Vaccine 25 2007 2491 2496
156. W. Nieves, S. Asakrah, O. Qazi, K.A. Brown, J. Kurtz, D.P. Aucoin, and et al. A naturally derived outer-membrane vesicle vaccine protects against lethal pulmonary Burkholderia pseudomallei infection Vaccine 29 2011 8381 8389
157. A.I. Camacho, J. de Souza, S. Sánchez-Gómez, M. Pardo-Ros, J.M. Irache, and C. Gamazo Mucosal immunization with Shigella flexneri outer membrane vesicles induced protection in mice Vaccine 29 2011 8222 8229
158. D. Bottero, M.E. Gaillard, A. Errea, G. Moreno, E. Zurita, L. Pianciola, and et al. Outer membrane vesicles derived from Bordetella parapertussis as an acellular vaccine against Bordetella parapertussis and Bordetella pertussis infection Vaccine 31 2013 5262 5268
159. T. Pierson, D. Matrakas, Y.U. Taylor, G. Manyam, V.N. Morozov, W.D. Zhou, and et al. Proteomic characterization and functional analysis of outer membrane vesicles of Francisella novicida suggests possible role in virulence and use as a vaccine J Proteome Res 10 2011 954 967
160. S.B. Park, H. Bin Jang, S.W. Nho, I.S. Cha, J. Hikima, M. Ohtani, and et al. Outer membrane vesicles as a candidate vaccine against edwardsiellosis PLoS One 6 2011 e17629
161. M.J. McConnell, C. Rumbo, G. Bou, and J. Pachon Outer membrane vesicles as an acellular vaccine against Acinetobacter baumannii Vaccine 29 2011 5705 5710
162. R. Nakao, H. Hasegawa, K. Ochiai, S. Takashiba, A. Ainai, M. Ohnishi, and et al. Outer membrane vesicles of Porphyromonas gingivalis elicit a mucosal immune response PLoS One 6 2011 e26163
163. B.L. Deatherage, and B.T. Cookson Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life Infect Immun 80 2012 1948 1957
164. H. Ohshima Electrophoretic mobility of soft particles Electrophoresis 16 1995 1360 1363
165. C. Beloin, A. Houry, M. Froment, J.M. Ghigo, and N. Henry A short-time scale colloidal system reveals early bacterial adhesion dynamics PLoS Biol 6 2008 e167
166. T.R. Scheuerman, A.K. Camper, and M.A. Hamilton Effects of substratum topography on bacterial adhesion J Colloid Interface Sci 208 1998 23 33
167. S. Perni, E.C. Preedy, and P. Prokopovich Success and failure of colloidal approaches in adhesion of microorganisms to surfaces Adv Colloid Interface Sci 206 2014 265 274
168. R.J. Crawford, H.K. Webb, V.K. Truong, J. Hasan, and E.P. Ivanova Surface topographical factors influencing bacterial attachment Adv Colloid Interface Sci 179-182 2012 142 149
169. K.C. Marshall Adsorption and adhesion processes in microbial growth at interfaces Adv Colloid Interface Sci 25 1986 59 86
170. J.F.L. Duval, and F. Gaboriaud Progress in electrohydrodynamics of soft microbial particle interphases Curr Opin Colloid Interface Sci 15 2010 184 195
171. L. Feng, M. Kobayashi, and Y. Adachi Initial stage dynamics of bridging flocculation of polystyrene latex particles with low charge density polycation in a mixing flow near the isoelectric point Colloid Polym Sci 2015 10.1007/s00396-015-3729-y
172. C. Pérez-Cruz, L. Delgado, C. López-Iglesias, and E. Mercade Outer-inner membrane vesicles naturally secreted by gram-negative pathogenic bacteria PLoS One 10 2015 e0116896
173. R.I. Koning, A. de Breij, G.T. Oostergetel, P.H. Nibbering, A.J. Koster, and L. Dijkshoorn Cryo-electron tomography analysis of membrane vesicles from Acinetobacter baumannii ATCC19606 T Res Microbiol 164 2013 397 405
174. T. Kieselbach, V. Zijnge, E. Granström, and J. Oscarsson Proteomics of Aggregatibacter actinomycetemcomitans Outer Membrane Vesicles PLoS ONE 10 2015 e0138591
175. E. Negrete-Abascal, R.M. García, M.E. Reyes, D. Godínez, and M. de la Garza Membrane vesicles released by Actinobacillus pleuropneumoniae contain proteases and Apx toxins FEMS Microbiol Lett 191 2000 109 113
176. C.W. Forsberg, T.J. Beveridge, and A. Hellstrom Cellulase and xylanase release from Bacteroides succinogenes and its importance in the rumen environment Appl Environ Microbiol 42 1981 886 896
177. D. Hozbor, M.E. Rodriguez, J. Fernandez, A. Lagares, N. Guiso, and O. Yantorno Release of outer membrane vesicles from Bordetella pertussis Curr Microbiol 38 1999 273 278
178. K.S. Jang, M.J. Sweredoski, R.L. Graham, S. Hess, and W.M. Clemons Jr. Comprehensive proteomic profiling of outer membrane vesicles from Campylobacter jejuni J Proteomics 98 2014 90 98
179. S.J. Richmond, and P. Stirling Localization of chlamydial group Antigen in McCoy cell monolayers infected with Chlamydia trachomatis or Chlamydia psittaci Infect Immun 34 1981 561 570
180. R.A. Deich, and L.C. Hoyer Generation and release of DNA-binding vesicles by Haemophilus influenzae during induction and loss of competence J Bacteriol 152 1982 855 864
181. R. Fiocca, V. Necchi, P. Sommi, V. Ricci, J. Telford, T.L. Cover, and et al. Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium J Pathol 188 1999 220 226
182. U. Heczko, V.C. Smith, R. Mark Meloche, A.M. Buchan, and B.B. Finlay Characteristics of Helicobacter pylori attachment to human primary antral epithelial cells Microbes Infect 2 2000 1669 1676
183. D.W. Dorward, C.F. Garon, and R.C. Judd Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae J Bacteriol 171 1989 2499 2505
184. J. Holst, D. Martin, R. Arnold, C.C. Huergo, P. Oster, J. O'Hallahan, and et al. Properties and clinical performance of vaccines containing outer membrane vesicles from Neisseria meningitidis Vaccine 27 Suppl. 2 2009 B3 B12
185. P.D. Veith, Y.Y. Chen, D.G. Gorasia, D. Chen, M.D. Glew, N.M. O'Brien-Simpson, and et al. Porphyromonas gingivalis outer membrane vesicles exclusively contain outer membrane and periplasmic proteins and carry a cargo enriched with virulence factors J Proteome Res 13 2014 2420 2432
186. M. Nevot, V. Deroncele, P. Messner, J. Guinea, and E. Mercade Characterization of outer membrane vesicles released by the psychrotolerant bacterium Pseudoalteromonas antarctica NF3 Environ Microbiol 8 2006 1523 1533
187. C.W. Choi, E.C. Park, S.H. Yun, S.Y. Lee, Y.G. Lee, Y. Hong, and et al. Proteomic characterization of the outer membrane vesicle of Pseudomonas putida KT2440 J Proteome Res 13 2014 4298 4309
188. H.M. Kulkarni, V. Swamy Ch, and M.V. Jagannadham Molecular characterization and functional analysis of outer membrane vesicles from the antarctic bacterium Pseudomonas syringae suggest a possible response to environmental conditions J Proteome Res 13 2014 1345 1358
189. C. Chowdhury, and M.V. Jagannadham Virulence factors are released in association with outer membrane vesicles of Pseudomonas syringae pv. tomato T1 during normal growth Biochim Biophys Acta 1834 2013 231 239
190. C.J. Vesy, R.L. Kitchens, G. Wolfbauer, J.J. Albers, and R.S. Munford Lipopolysaccharide-binding protein and phospholipid transfer protein release lipopolysaccharides from gram-negative bacterial membranes Infect Immun 68 2000 2410 2417
191. S. Mitra, S. Barman, D. Nag, R. Sinha, D.R. Saha, and H. Koley Outer membrane vesicles of Shigella boydii type 4 induce passive immunity in neonatal mice FEMS Immunol Med Microbiol 66 2012 240 250
192. J.L. Kadurugamuwa, and T.J. Beveridge Membrane vesicles derived from Pseudomonas aeruginosa and Shigella flexneri can be integrated into the surfaces of other Gram-negative bacteria Microbiology 145 1999 2051 2060
193. Y. Chen, L. Liu, H. Fu, C. Wei, and Q. Jin Comparative proteomic analysis of outer membrane vesicles from Shigella flexneri under different culture conditions Biochem Biophys Res Commun 453 2014 696 702
194. V.K. Sidhu, F.J. Vorholter, K. Niehaus, and S.A. Watt Analysis of outer membrane vesicle associated proteins isolated from the plant pathogenic bacterium Xanthomonas campestris pv. campestris BMC Microbiol 8 2008 87
195. P. Khandelwal, and N. Banerjee-Bhatnagar Insecticidal activity associated with the outer membrane vesicles of Xenorhabdus nematophilus Appl Environ Microbiol 69 2003 2032 2037
196. J. Rivera, R.J. Cordero, A.S. Nakouzi, S. Frases, A. Nicola, and A. Casadevall Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins Proc Natl Acad Sci U S A 107 2010 19002 19007
197. R. Prados-Rosales, A. Baena, L.R. Martinez, J. Luque-Garcia, R. Kalscheuer, U. Veeraraghavan, and et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice J Clin Invest 121 2011 1471 1483
198. L. Marsollier, P. Brodin, M. Jackson, J. Kordulakova, P. Tafelmeyer, E. Carbonnelle, and et al. Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis PLoS Pathog 3 2007 e62
199. E.Y. Lee, D.Y. Choi, D.K. Kim, J.W. Kim, J.O. Park, S. Kim, and et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles Proteomics 9 2009 5425 5436
200. M. Gurung, D.C. Moon, C.W. Choi, J.H. Lee, Y.C. Bae, J. Kim, and et al. Staphylococcus aureus produces membrane-derived vesicles that induce host cell death PLoS One 6 2011 e27958
201. A. Olaya-Abril, R. Prados-Rosales, M.J. McConnell, R. Martín-Peña, J.A. González-Reyes, I. Jiménez-Munguía, and et al. Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae J Proteomics 106 2014 46 60
202. H. Schrempf, I. Koebsch, S. Walter, H. Engelhardt, and H. Meschke Extracellular Streptomyces vesicles: amphorae for survival and defence Microb Biotechnol 4 2011 286 299