Outer membrane vesicles as platform vaccine technology

Biotechnology Journal

Volumn 10, Issue 11, 2015, Pages 1689-1706

  van der Pol, Leo ^a   Stork, Michiel ^b   van der Ley, Peter ^a  

^a Research   (Netherlands)

^b Product Development Intravacc   (Netherlands)

Author keywords

Lipopolysaccharide; Neisseria; Outer membrane vesicle; Pertussis; Vaccine

Indexed keywords

ANTIGENS; BACTERIA; GENETIC ENGINEERING;

GRAM-NEGATIVE BACTERIA; LIPOPOLYSACCHARIDES; MULTIPLE APPLICATIONS; NEISSERIA; NEISSERIA MENINGITIDIS; OUTER MEMBRANE VESICLES; PATHOGENIC BACTERIUM; PERTUSSIS;

VACCINES;

BACTERIAL VACCINE; CHOLERA TOXIN; CYTOLETHAL DISTENDING TOXIN; CYTOLYSIN; LIPID; MENINGITIS VACCINE; MENINGOCOCCUS VACCINE; OUTER MEMBRANE VESICLE VACCINE; PERTUSSIS VACCINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL; PHOSPHOLIPASE A; PHOSPHOLIPID; PROTEINASE; UNCLASSIFIED DRUG; UREASE; VACUOLATING TOXIN; ARTIFICIAL MEMBRANE; LIPOPOLYSACCHARIDE; NANOPARTICLE; OUTER MEMBRANE PROTEIN; VACCINE;

ANTIBODY RESPONSE; ANTIGEN PRESENTING CELL; BACTERIAL MENINGITIS; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; BIOGENESIS; BORDETELLA PERTUSSIS; CLINICAL EFFECTIVENESS; CLINICAL TRIAL (TOPIC); DNA MODIFICATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ENGINEERING; HELICOBACTER PYLORI; HETEROLOGOUS EXPRESSION; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; INNATE IMMUNITY; LYSOBACTER; MEMBRANE VESICLE; NEISSERIA MENINGITIDIS; NONHUMAN; OUTER MEMBRANE VESICLE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROCESS CONTROL; PROCESS DEVELOPMENT; PROTEIN ANALYSIS; PROTEIN FUNCTION; REVIEW; UPSTREAM PROCESS; ANIMAL; ARTIFICIAL MEMBRANE; BIOTECHNOLOGY; MOUSE;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BIOTECHNOLOGY; HUMANS; LIPOPOLYSACCHARIDES; MEMBRANES, ARTIFICIAL; MENINGOCOCCAL VACCINES; MICE; NANOPARTICLES; NEISSERIA MENINGITIDIS; VACCINES;

EID: 84946913090     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201400395     Document Type: Review

References (183)

1. Deatherage, B. L., Cookson, B. T., Membrane vesicle release in bacteria, eukaryotes, and archea: A conserved yet underappreciated aspect of microbial life. Infect. Immun. 2012, 80, 1948-1957.
2. Dorward, D. W., Garon, C. F., DNA is packaged within membrane derived vesicles of gram-negative but not gram-positive bacteria. Appl. Environ. Microbiol. 1990, 56, 1960-1962.
3. Rivera, J., Cordero, R. J., Nakouzi, A. S., Frases, S. et al., Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 19002-19007.
4. Lee, E. Y., Choi, D. Y., Kim, D. K., Kim, J. W. et al., Gram-positive bacteria produce membrane vesicles: Proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 2009, 9, 5425-5436.
5. Prados-Rosales, R., Baena, A., Martinez, L. R., Luque-Garcia, J. et al., Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J. Clin. Invest. 2011, 121, 1471-1483.
6. Ellen, A. F., Albers, S-V., Huibers, W., Pitcher, A. et al., Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles 2009, 13, 67-79.
7. Hopkins, A. L., Groom, C. R., The druggable genome. Nat. Rev. Drug. Discov. 2002, 1, 727-730.
8. O'Ryan, M., Stoddard, J., Toneatto, D., Wassil, J., Dull, P. M., A multi-component meningococcal serogroup B vaccine (4CMenB): The clinical development program. Drugs 2014, 74, 15-30.
9. Bachmann, M. F., Jennings, G. T., Vaccine delivery: A matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol. 2010, 10, 787-796.
10. Zepp, F., Principles of vaccine design - lessons from nature. Vaccine 2010, C14-C24.
11. Singh, M., Chakrapani, A., O'Hagan, D., Nanoparticles and microparticles as vaccine-delivery systems. Expert Rev. Vaccines 2007, 6, 797-808.
12. Scheerlinck, J. P., Greenwood, D. L., Virus-sized vaccine delivery systems. Drug Discov. Today 2008, 882-887.
13. Ellis, T. N., Kuehn, M. J., Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 2010, 74, 81-94.
14. Kuehn, M. J., Kesty, N. C., Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005, 19, 2645-2655.
15. Kulp, A., Kuehn, M. J., Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 2010, 64, 163-184.
16. Beveridge, T. J., Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 1999, 181, 4725-4733.
17. Mashburn-Warren, L. M., Whiteley, M., Special delivery: Vesicle trafficking in prokaryotes. Mol. Microbiol. 2006, 61, 839-846.
18. Bonnington, K. E., Kuehn, M. J., Protein selection and export via outer membrane vesicles. Biochim. Biophys. Acta 2014, 1843, 1612-1619.
19. Fulsundar, S., Harms, K., Flaten, G. E., Johnsen, P. J. et al., Gene transfer potential of outer membrane vesicles of Acinetobacter baylyi and effects of stress on vesiculation. Appl. Environ. Microbiol. 2014, 80, 3469-3483.
20. Kaparakis, M., Turnbull, L., Carneiro, L., Firth, S. et al., Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol. 2010, 12, 372-385.
21. Wensink, J., Witholt, B., Outer-membrane vesicles released by normally growing Escherichia coli contain very little lipoprotein. Eur. J. Biochem. 1981, 116, 331-335.
22. Olofsson, A., Vallström, A., Petzold, K., Tegtmeyer, N. et al., Biochemical and functional characterization of Helicobacter pylori vesicles. Mol. Microbiol. 2010, 77, 1539-1555.
23. Lappann, M., Otto, A., Becher, D., Ulrich Vogel, U., Comparative Proteome Analysis of Spontaneous Outer Membrane Vesicles and Purified Outer Membranes of Neisseria meningitidis. J. Bacteriol. 2013, 195, 4425-4435.
24. Berlanda Scorza, F., Doro, F., Rodriguez-Ortega, M. J., Stella, M. et al., Proteomics characterization of outer membrane vesicles from the extraintestinal pathogenic Escherichia coli DeltatolR IHE3034 mutant. Mol. Cell. Proteomics 2008, 7, 473-485.
25. Tsolakos, N., Lie, K., Bolstad, K., Maslend, S. et al., Characterization of meningococcal serogroup B outer membrane vesicle vaccines from strain 44/76 after growth in different media. Vaccine 2010, 28, 3211-3218.
26. Baumgarten, T., Sperling, S., Seifert, J., von Bergen, M. 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. 2012, 78, 6217-6224.
27. Ferrari, G., Garaguso, I., Adu-Bobie, J., Doro, F. et al., Outer membrane vesicles from group B Neisseria meningitidis delta gna33 mutant: Proteomic and immunological comparison with detergent-derived outer membrane vesicles. Proteomics 2006, 6, 1856-1866.
28. Mullaney, E., Brown, P. A., Smith, S. M., Botting, C. H. et al., Proteomic and functional characterization of the outer membrane vesicles from the gastric pathogen Helicobacter pylori. Proteomics Clin. Appl. 2009, 3, 785-796.
29. Choi, D. S., Kim, D. K., Choi, S. J., Lee, J. et al., Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa. Proteomics 2011, 11, 3424-3429.
30. van de Waterbeemd, B., Mommen, G. P. M., Pennink, J. L. A., Eppink, M. H. et. al., Quantitative proteomics reveals distinct differences in the protein content of outer membrane vesicle vaccines. J. Proteome Res. 2013, 12, 1898-1908.
31. Veith, P. D., Chen, Y. Y., Gorasia, D. G., Chen, D. et al., Porphyromonas gingivalis outer membrane vesicles exclusively contain outer membrane and periplasmic proteins and carry cargo enriched with virulence factors. J. Proteome Res. 2014, 13, 2420-2432.
32. Eddy, J. L., Gielda, L. M., Caulfield, A. J., Rangel, S. M., Lathem, W. W., Production of outer membrane vesicles by the plague pathogen Yersinia pestis. PLoS One 2014, 9, e107002.
33. Manabe, T., Kato, M., Ueno, T., Kawasaki, K., Flagella proteins contribute to the production of outer membrane vesicles from Escherichia coli W3110. Biochem. Biophys. Res. Commun. 2013, 441, 151-156.
34. Parker, H., Keenan, J. I., Composition and function of Helicobacter pylori outer membrane vesicles. Microbes Infect. 2012, 14, 9-16.
35. Horstman, A. L., Kuehn, M. J., Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J. Biol. Chem. 2000, 275, 12489-12496.
36. Wai, S. N., Lindmark, B., Soderblom, T., Takade, A. et al., Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 2003, 115, 25-35.
37. Chatterjee, D., Chaudhuri, K., Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Lett. 2011, 585, 1357-1362.
38. Fiocca, R., Necchi, V., Sommi, P., Ricci, V. 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. 1999, 188, 220-226.
39. Lindmark, B., Rompikuntal, P. K., Vaitkevicius, K., Song, T. et al., Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni. BMC Microbiol. 2009, 9, 220.
40. Lee, E. Y., Bang, J. Y., Park, G. W., Choi, D. S. et al., Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 2007, 7, 3143-3153.
41. Lee, E. Y., Choi, D. S., Kim, K. P., Gho, Y. S., Proteomics in gram-negative bacterial outer membrane vesicles. Mass Spectrom. Rev. 2008, 27, 535-555.
42. Dennehy, R., McClean, S., Immunoproteomics: The key to discovery of new vaccine antigens against bacterial respiratory infections. Curr. Protein Pept. Sci. 2012, 13, 807-815.
43. Henderson, B., Martin, A., Bacterial virulence in the moonlight: Multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect. Immun. 2011, 79, 3476-3491.
44. Toledo, A., Coleman, J. L., Kuhlow, C. J., Crowley, J. T., Benach, J. L., The enolase of Borrelia burgdorferi is a plasminogen receptor released in outer membrane vesicles. Infect. Immun. 2012, 80, 359-368.
45. Molloy, M. P., Herbert, B. R., Slade, M. B., Rabilloud, T. et al., Proteomic analysis of the Escherichia coli outer membrane. Eur. J. Biochem. 2000, 267, 2871-2881.
46. Hoekstra, D., van der Laan, J. W., de Leij, L., Witholt, B., Release of outer membrane fragments from normally growing Escherichia coli. Biochim. Biophys. Acta 1976, 455, 889-899.
47. Post, D. M., Zhang, D., Eastvold, J. S., Teghanemt, A. et al., Biochemical and functional characterization of membrane blebs purified from Neisseria meningitidis serogroup B. J. Biol. Chem. 2005, 80, 38383-38394.
48. Tashiro, Y., Inagaki, A., Shimizu, M., Ichikawa, S. et al., Characterization of phospholipids in membrane vesicles derived from Pseudomonas aeruginosa. Biosci. Biotechnol. Biochem. 2011, 75, 605-607.
49. Shimomura, H., Hayashi, S., Yokota, K., Oguma, K., Hirai, Y., Alteration in the composition of cholesteryl glucosides and other lipids in Helicobacter pylori undergoing morphological change from spiral to coccoid form. FEMS Microbiol. Lett. 2004, 237, 407-413.
50. LaRocca, T. J., Crowley, J. T., Cusack, B. J., Pathak, P. et al., Cholesterol lipids of Borrelia burgdorferi form lipid rafts and are required for the bactericidal activity of a complement-independent antibody. Cell Host Microbe 2010, 8, 331-342.
51. Kadurugamuwa, J. L., Beveridge, T. J., Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: A novel mechanism ofenzyme secretion. J. Bacteriol. 1995, 177, 3998-4008.
52. Unal, C. M., Schaar, V., Riesbeck, K., Bacterial outer membrane vesicles in disease and preventive medicine. Semin. Immunopathol. 2011, 33, 395-408.
53. Pettit, R. K., Judd, R. C., The interaction of naturally elaborated blebs from serum-susceptible and serum-resistant strains of Neisseria gonorrhoeae with normal human serum. Mol. Microbiol. 1992, 6, 729-734.
54. Schooling, S. R., Beveridge, T. J., Membrane vesicles: An overlooked component of the matrices of biofilms J. Bacteriol. 2006, 188, 5945-5957.
55. Palsdottir, H., Remis, J. P., Schaudinn, C., O'Toole, E. et al., Three-dimensional macromolecular organization of cryofixed Myxococcus xanthus biofilms as revealed by electron microscopic tomography. J. Bacteriol. 2009, 191, 2077-2082.
56. Manning, A. J., Kuehn, M. J., Contribution of bacterial outer membrane vesicles to innate bacterial defence. BMC Microbiol. 2011, 11, 258.
57. Renelli, M., Matias, V., Lo, R. Y., Beveridge, T. J., DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 2004, 150, 2161-2169.
58. Schwechheimer, C., Sullivan, C. J., Kuehn, M. J., Envelope control of outer membrane vesicle production in Gram-negative bacteria. Biochemistry 2013, 52, 3031-3040.
59. Scherzer, J. W., Whiteley, M., A bilayer-couple model of outer membrane vesicle biosynthesis. mBio 2012, 3, e00297-11.
60. Sonntag, I., Schwarz, H., Hirota, Y., Henning, U., Escherichia coli: Multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins. J. Bacteriol. 1978, 136, 280.
61. Bernadac, A., Gavioli, M., Lazzaroni, J. C., Raina, S., Lloubès, R., Escherichia coli tol-pal mutants form outer membrane vesicles. J. Bacteriol. 1998, 180, 4872-4878.
62. Steeghs, L., Berns, M., ten Hove, J., de Jong, A. et al., Expression of foreign LpxA acyltransferases in Neisseria meningitidis results in modified lipid A with reduced toxicity and retained adjuvant activity. Cell. Microbiol. 2002, 4, 599-611.
63. van de Waterbeemd, B., Streefland, M., van der Ley, P., Zomer, B. et al., Improved OMV vaccine against Neisseria meningitidis using genetically engineered strains and a detergent-free purification process. Vaccine 2010, 28, 4810-4816.
64. Vollmer, W., Bertsche, U., Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim. Biophys. Acta 2008, 1778, 1714-1734.
65. Hayashi, J., Hamada, N., Kuramitsu, H. K., The autolysin of Porphyromonas gingivalis is involved in outer membrane vesicle release. FEMS Microbiol. Lett. 2002, 216, 217-222.
66. Adu-Bobie, J., Lupetti, P., Brunelli, B., Granoff, D. et al., GNA33 of Neisseria meningitidis is a lipoprotein required for cell separation, membrane architecture, and virulence. Infect. Immun. 2004, 72, 1914-1919.
67. Schwechheimer, C., Kulp, A., Kuehn, M. J., Modulation of bacterial outer membrane vesicle production by envelope structure and content. BMC Microbiol. 2014, 14, 324.
68. Bos, M. P., Tefsen, B., Voet, P., Weynants, V. et al., Function of neisserial outer membrane phospholipase A in autolysis and assessment of its vaccine potential. Infect. Immun. 2005, 73, 2222-2231.
69. Tannaes, T., Grav, H. J., and Bukholm, G., Lipid profiles of Helicobacter pylori colony variants. APMIS 2000, 349-356.
70. McBroom, A. J., Johnson, A. P., Vemulapalli, S., Kuehn, M. J., Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J. Bacteriol. 2006, 188, 5385-5392.
71. Mashburn-Warren, L., Howe, J., Garidel, P., Richter, W. et al., Interaction of quorum signals with outer membrane lipids: Insights into prokaryotic membrane vesicle formation. Mol. Microbiol. 2008, 69, 491-502.
72. Kadurugamuwa, J. L., Beveridge, T. J., Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: Conceptually new antibiotics. J. Bacteriol. 1996, 178, 2767-2774.
73. Deatherage, B. L., Cano Lara, J., Bergsbaken, T., Rassoulian Barrett, S. L. et al., Biogenesis of bacterial membrane vesicles. Mol. Microbiol. 2009, 72, 1395-1407.
74. Moon, D. C., Choi, C. H., Lee, J. H., Choi, C. W. et al., Acinetobacter baumannii outer membrane protein A modulates the biogenesis of outer membrane vesicles. J. Microbiol. 2012, 50, 155-160.
75. Song, T., Mika, F., Lindmark, B., Liu, Z. et al., "A new Vibrio cholera sRNA modulates colonization and affects release of outer membrane vesicles, "Mol. Microbiol. 2008, 70, 100-111.
76. Valeru, S. P., Shanan, S., Alossimi, H., Saeed, A. et al., Lack of outer membrane protein A enhances the release of outer membrane vesicles and survival of Vibrio cholerae and suppresses viability of Acanthamoeba castellanii. Int. J. Microbiol. 2014, 610190.
77. McBroom, A. J., Kuehn, M. J., Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 2007, 63, 545-558.
78. Hagemann, S., Stöger, L., Kappelmann, M., Hassl, I. et al., DNA-bearing membrane vesicles produced by Ahrensia kielensis and Pseudoalteromonas marina. J. Basic Microbiol. 2013, 53, 1-11.
79. Katsui, N., Tsuchido, T., Hiramatsu, R., Fujikawa, S. et al., Heat-induced blebbing and vesiculation of the outer membrane of Escherichia coli. J. Bacteriol. 1982, 151, 1523-1531.
80. Knox, K. W., Vesk, M., Work, E., Relation between excreted lipopolysaccharide complexes and surface structures of a lysine-limited culture of Escherichia coli. J. Bacteriol. 1966, 92, 1206-1217.
81. van de Waterbeemd, B., Zomer, G., van den IJssel, J., van Keulen, L. et al., Cysteine depletion causes oxidative stress and triggers outer membrane vesicle release by Neisseria meningitidis; Implications for vaccine development. PLoS One 2013, 8, e54314.
82. Loeb, M. R., Kilner, J., Release of a special fraction of the outer membrane from both growing and phage T4-infected Escherichia coli B. Biochim. Biophys. Acta 1978, 514, 117-127.
83. Borneleit, P., Hermsdorf, T., Claus, R., Walther, P., Kleber, H. P., Effect of hexadecane-induced vesiculation on the outer membrane of Acinetobacter calcoaceticus. Gen. Microbiol. 1988, 134, 1983-1992.
84. Kolodziejek, A. M., Caplan, A. B., Bohach, G. A., Paszczynski, A. J. et al., Physiological levels of glucose induce membrane vesicle secretion and affect the lipid and protein composition of Yersinia pestis cell surfaces. Appl. Environ. Microbiol. 2013, 79, 4509-4514.
85. Altindis, E., Fu, Y., Mekalanos, J. J., Proteomic analysis of Vibiro cholerae outer membrane vesicles. Proc. Natl. Acad. Sci. U.S.A. 2014, E1546-E1556.
86. Toyofuku, M., Zhou, S., Sawada, I., Takaya, N. et al., Membrane vesicle formation is associated with pyocin production under denitrifying conditions in Pseudomonas aeruginosa PAO1. Environ. Microbiol. 2013, 16, 2927-2938.
87. Chatterjee, S. N., Das, J., Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. J. Gen. Microbiol. 1967, 49, 1-11.
88. Devoe, I. W., Gilchrist, J. E., Release of endotoxin in the form of cell wall blebs during in vitro growth of Neisseria meningitidis. J. Exp. Med. 1973, 138, 1156-1167.
89. Mug-Opstelten, D., Witholt, B., Preferential release of new outer membrane fragments by exponentially growing Escherichia coli. Biochim. Biophys. Acta 1978, 508, 287-295.
90. Santos, S., Arauz, L. J., Baruque-Ramos, J., Lebrun, I. et al., Outer membrane vesicles (OMV) production of Neisseria meningitidis serogroup B in batch process. Vaccine 2012, 30, 6064-6069.
91. McCaig, W. D., Koller, A., Thanassi, D. G., Production of outer membrane vesicles and outer membrane tubes by Francisella novicida. J. Bacteriol. 2013, 195, 1120-1132.
92. Alaniz, R. C., Deatherage, B. L., Lara, J. C., Cookson, B. T., Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J. Immunol. 2007, 179, 7692-7701.
93. Charon, N. W., Goldstein, S. F., Marko, M., Hsieh, C. et al., The flat-ribbon configuration of the periplasmic flagella of Borrelia burgdorferi and its relationship to motility and morphology. J. Bacteriol. 2009, 191, 600-607.
94. Bager, R. J., Persson, G., Nesta, B., Soriani, M. et al., Outer membrane vesicles reflect environmental cues in Gallibacterium anatis. Veter. Microbiol. 2013, 167, 565-572.
95. Galka, F., Wai, S. N., Kusch, H., Engelmann, S. et al., Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect. Immun. 2008, 76, 1825-1836.
96. Manning, A. J., Kuehn, M. J., Functional advantages conferred by extracellular prokaryotic membrane vesicles. J. Mol. Microbiol. Biotechnol. 2013, 23, 131-141.
97. Kadurugamuwa, J. L., Beveridge, T. J., Natural release of virulence factors in membrane vesicles by Pseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release. J. Antimicrob. Chemother. 1997, 40, 615-621.
98. Aguilera, L., Toloza, L., Gimenez, R., Odena, A. et al., Proteomic analysis of outer membrane vesicles from the probiotic strain Escherichia coli Nissle 1917. Proteomics 2014, 14, 222-229.
99. Elhenawy, W., Debelyy, M. O., Feldman, M. F., Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles. Mbio 2014, 5, e00909-e00914.
100. Kesty, N. C., Kuehn, M. J., Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J. Biol. Chem. 2004, 279, 2069-2076.
101. Vasilyeva, N. V., Tsfasman, I. M., Kudryakova, I. V., Suzina, N. E. et al., The role of membrane vesicles in secretion of Lysobacter sp. bacteriolytic enzymes. J. Mol. Microbiol. Biotechnol. 2013, 23, 142-151.
102. Haurat, M. F., Aduse-Opoku, J., Rangarajan, M., Dorobantu, L. et al., Selective sorting of cargo proteins into bacterial membrane vesicles. J. Biol. Chem. 2011, 286, 1269-1276.
103. Jaroslawski, S., Duquesne, K., Sturgis, J. N., Scheuring, S., High resolution architecture of the outer membrane of the Gram-negative bacteria Roseobacter denitrificans. Mol. Microbiol. 2009, 74, 1211-1222.
104. Bielig, H., Dongre, M., Zurek, B., Wai, S. N., Kufer, T. A., A role for quorum sensing in regulating innate immune responses mediated by Vibrio cholerae outer membrane vesicles (OMVs). Gut Microbes 2011, 2, 274-279.
105. Chatterjee, D., Chaudhuri, K., 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. 2013, 288, 4299-4309.
106. Yaron, S., Kolling, G. L., Simon, L., Matthews, K. R., Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl. Environ. Microbiol. 2000, 66, 4414-4420.
107. Dorward, D. W., Garon, C. F., Judd, R. C., Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J. Bacteriol. 1989, 171, 2499-2505.
108. Sharpe, S. W., Kuehn, M. J., Mason, K. M., Elicitation of epithelial cell-derived immune effectors by outer membrane vesicles of nontypeable Haemophilus influenzae. Infect. Immun. 2011, 79, 4361-4369.
109. Dorward, D. W., Garon, C. F., Judd, R. C., Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J. Bacteriol. 1989, 171, 2499-2505.
110. Ghosal, A., Upadhyaya, B. B., Fritz, J. V., Heintz-Buschart, A. et al., The extracellular RNA complement of Escherichia coli. Microbiology Open 2015, DOI: 10.1002/mbo3.235.
111. Holst, J., Oster, P., Arnold, R., Tatley, M. V. et al., Vaccines against meningococcal serogroup B disease containing outer membrane vesicles (OMV): Lessons from past programs and implications for the future. Hum. Vaccin. Immunother. 2013, 9, 1241-1253.
112. Saunders, N. B., Shoemaker, D. R., Brandt, B. L., Moran, E. E. et al., Immunogenicity of intranasally administered meningococcal native outer membrane vesicles in mice. Infect. Immun. 1999, 67, 113-119.
113. Finne, J., Leinonen, M., Makela, P. H., Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet 1983, 2, 355-357.
114. Granoff, D. M., Pelton, S., Harrison, L. H., Meningococcal vaccines, in: Plotkin, S. A., Orenstein, W. A., Offit, P. A. (Eds.), Vaccines 6th Edn., Elsevier Health Sciences 2013, pp. 388-418.
115. Holst, J., Martin, D., Arnold, R., Huergo, C. C. et al., Properties and clinical performance of vaccines containing outer membrane vesicles from Neisseria meningitidis. Vaccine 2009, B3-B12.
116. Urwin, R., Russell, J. E., Thompson, E. A., Holmes, E. C. et al., Distribution of surface protein variants among hyperinvasive meningococci: Implications for vaccine design. Infect. Immun. 2004, 72, 5955-5962.
117. Rappuoli, R., Reversevaccinology. Curr. Opin. Microbiol. 2000, 3, 445-450.
118. Acevedo, R., Fernández, S., Zayas, C., Acosta, A. et al., Bacterial outer membrane vesicles and vaccine applications. Front. Immunol. 2014, 5, 121.
119. Bjune, G., Høiby, E. A., Grønnesby, J. K., Arnesen, O. et al., Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet 1991, 338, 1093-1096.
120. Sierra, G. V., Campa, H. C., Varcacel, N. M., Garcia, I. L. et al., Vaccine against group B Neisseria meningitidis: Protection trial and mass vaccination results in Cuba. NIPH Ann. 1991, 14, 195-210.
121. Arnold, R., Galloway, Y., McNicholas, A., O'Hallahan, J., Effectiveness of a vaccination programme for an epidemic of meningococcal B in New Zealand. Vaccine 2011, 29, 7100-7106.
122. Claassen, I., Meylis, J., van der Ley, P., Peeters, C. et al., Production, characterization and control of a Neisseria meningitidis hexavalent class 1 outer membrane protein containing vesicle vaccine. Vaccine 1996, 14, 1001-1008.
123. Peeters, C. C., Rümke, H. C., Sundermann, L. C., Rouppe van der Voort, E. M. et al., Phase I clinical trial with a hexavalent PorA containing meningococcal outer membrane vesicle vaccine. Vaccine 1996, 14, 1009-1015.
124. Evans, C. M., Pratt, C. B., Matheson, M., Vaughan, T. E. et al., Nasopharyngeal colonization by Neisseria lactamica and induction of protective immunity against Neisseria meningitides. Clin. Infect. Dis. 2011, 52, 70-77.
125. van der Ley, P., Steeghs, L., Hamstra, H. J., ten Hove, J. et al., Modification of lipid A biosynthesis in Neisseria meningitidis lpxL mutants: Influence on lipopolysaccharide structure, toxicity, and adjuvant activity. Infect. Immun. 2001, 69, 5981-5990.
126. Keiser, P. B., Biggs-Cicatelli, S., Moran, E. E., Schmiel, D. H. et al., A phase 1 study of a meningococcal native outer membrane vesicle vaccine made from a group B strain with deleted lpxL1 and synX, over-expressed factor H binding protein, two PorAs and stabilized OpcA expression. Vaccine 2011, 29, 1413-1420.
127. Costa, I., Pajon, R., Granoff, D. M., Human factor H (FH) impairs protective meningococcal anti-FHbp antibody responses and the antibodies enhance FH binding. MBio 2014, 5, e01625-14.
128. Koeberling, O., Ispasanie, E., Hauser, J., Rossi, O. et al., A broadly-protective vaccine against meningococcal disease in sub-Saharan Africa based on generalized modules for membrane antigens (GMMA). Vaccine 2014, 32, 2688-2695.
129. Koeberling, O., Delany, I., Granoff, D. M., A critical threshold of meningococcal factor H binding protein expression is required for increased breadth of protective antibodies elicited by native outer membrane vesicle vaccines. Clin. Vaccine Immunol. 2011, 18, 736-742.
130. Moran, E., Burden, R., Labrie III, J. E., Wen, Z. et al., Analysis of the Bactericidal Response to an Experimental Neisseria meningitidis Vesicle Vaccine. Clin. Vaccine Immunol. 2012, 19, 659-665.
131. Beernink, P. T., Caugant, D. A., Welsch, J. A., Koeberling, O., Granoff, D. M., Meningococcal factor H-binding protein variants expressed by epidemic capsular group A, W-135, and X strains from Africa. J. Infect. Dis. 2009, 199, 1360-1368.
132. Roberts, R., Moreno, G., Bottero, D., Gaillard, M. E. et al., Outer membrane vesicles as acellular vaccine against pertussis. Vaccine 2008, 26, 4639-4646.
133. Asensio, C. J., Gaillard, M. E., Moreno, G., Bottero, D. et al., Outer membrane vesicles obtained from Bordetella pertussisTohama expressing the lipid A deacylase PagL as a novel acellular vaccine candidate. Vaccine 2011, 29, 1649-1656.
134. Bottero, D., Gaillard, M. E., Errea, A., Moreno, G. et al., Outer membrane vesicles derived from Bordetella parapertussis as an acellular vaccine against Bordetella parapertussis and Bordetella pertussis infection. Vaccine 2013, 31, 5262-5268.
135. Kesavalu, L., Ebersole, J. L., Machen, R. L., Holt, S. C., Porphyromonas gingivalis virulence in mice: Induction of immunity to bacterial components. Infect. Immun. 1992, 60, 1455-1464.
136. Schild, S., Nelson, E. J., Camilli, A., Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect. Immun. 2008, 76, 4554-4563.
137. Keenan, J. I., Allardyce, R. A., Bagshaw, P. F., Lack of protection following immunisation with H. pylori outer membrane vesicles highlights antigenic differences between H. felis and H. pylori. FEMS Microbiol. Lett. 1998, 161, 21-27.
138. Zhou, K., Deng, X., He, C., Yue, B., Wu, M., Pseudomonas aeruginosa outer membrane vesicles modulate host immune responses by targeting the Toll-like receptor 4 signaling pathway. Infect. Immun. 2013, 81, 4509-4518.
139. Bishop, A. L., Schild, S., Patimalla, B., Klein, B., Camilli, A., Mucosal immunization with Vibrio cholerae outer membrane vesicles provides maternal protection mediated by antilipopolysaccharide antibodies that inhibit bacterial motility. Infect. Immun. 2010, 78, 4402-4420.
140. Nieves, W., Asakrah, S., Qazi, O., Brown, K. A. et al., A naturally derived outer membrane vesicle vaccine protects against lethal pulmonary Burkholderia pseudomallei infection. Vaccine 2011, 29, 8381-8389.
141. Pierson, T., Matrakas, D., Taylor, Y. U., Manyam, G. 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. 2011, 10, 954-967.
142. Jong, W., Daleke-Schermerhorn, M. H., Vikström, D., Ten Hagen-Jongman, C. M. et al., An autotransporter display platform for the development of multivalent recombinant bacterial vector vaccines. Microb. Cell Fact. 2014, 13, 162.
143. Basto, A. P., Piedade, J., Ramalho, R., Alves, S. et al., A new cloning system based on the OprI lipoprotein for the production of recombinant bacterial cell wall-derived immunogenic formulations. J. Biotechnol. 2012, 157, 50-63.
144. Fantappiè, L., de Santis, M., Chiarot, E., Carboni, F. et al., Antibody-mediated immunity induced by engineered Escherichia coli OMVs carrying heterologous antigens in their lumen. J. Extracell. Vesicles 2014, 3, 24015.
145. Park, M., Sun, Q., Liu, F., DeLisa, M. P., Chen, W., Positional Assembly of enzymes on bacterial outer membrane vesicles for cascade reactions. PLoS One 2014, 9, e97103.
146. Muralinath, M., Kuehn, M. J., Immunization with Salmonella enterica serovar typhimurium-derived outer membrane vesicles delivering the pneumococcal protein PspA confers protection against challenge with Streptococcus pneumoniae. Infect. Immun. 2011, 79, 887-894.
147. Bartolini, E., Ianni, E., Frigimelica, E., Petracca, R. et al., Recombinant outer membrane vesicles carrying Chlamydia muridarum HtrA induce antibodies that neutralize chlamydial infection in vitro. J. Extracell. Vesicles 2013, 2, 20181.
148. Maisonneuve, C., Bertholet, S., Philpott, D. J., de Gregorio, E., Unleashing the potential of NOD- and Toll-like agonists as vaccine adjuvants. Proc. Natl. Acad. Sci. U.S.A. 2014, 111, 12294-12299.
149. Somerville, J. E. Jr, Cassiano, L., Bainbridge, B., Cunningham, M. D., Darveau, R. P., A novel Escherichia coli lipid A mutant that produces an antiinflammatory lipopolysaccharide. J. Clin. Invest. 1996, 97, 359-365.
150. Mata-Haro, V., Cekic, C., Martin, M., Chilton, P. M. et al., The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 2007, 316, 1628-1632.
151. Pupo, E., Hamstra, H. J., Meiring, H., van der Ley, P., Lipopolysaccharide engineering in Neisseria meningitidis: Structural analysis of different pentaacyl lipid A mutants and comparison of their modified agonist properties. J. Biol. Chem. 2014, 289, 8668-8680.
152. Jin, M. S., Kim, S. E., Heo, J. Y., Lee, M. E. et al., Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 2007, 130, 1071-1082.
153. Kovacs-Simon, A., Titball, R. W., Michell, S. L., Lipoproteins of bacterial pathogens. Infect. Immun. 2011, 79, 548-561.
154. Fransen, F., Stenger, R. M., Poelen, M. C., van Dijken, H. H. et al., Differential effect of TLR2 and TLR4 on the immune response after immunization with a vaccine against Neisseria meningitidis or Bordetella pertussis. PLoS One 2010, 5, e15692.
155. Li, J., Lee, D. S., Madrenas, J., Evolving bacterial envelopes and plasticity of TLR2-dependent responses: Basic research and translational opportunities. Front. Immunol. 2013, 4, 347.
156. Zariri, A., van Dijken, H., Hamstra, H. J., van der Flier, M. et al., Expression of human CEACAM1 in transgenic mice limits the Opa-specific immune response against meningococcal outer membrane vesicles. Vaccine 2013, 31, 5585-5593.
157. Steeghs, L., van Vliet, S. J., Uronen-Hansson, H., van Mourik, A. et al., Neisseria meningitidis expressing lgtB lipopolysaccharide targets DC-SIGN and modulates dendritic cell function. Cell. Microbiol. 2006, 8, 316-325.
158. Kim, S-H., Kim, K-S., Lee, S-R., Kim, E. et al., Structural modifications of outer membrane vesicles to refine them as vaccine delivery vesicles. Biochim. Biophys. Acta 2009, 1788, 2150-2159.
159. Chutkan, H., MacDonald, I., Manning, A., Kuehn, M. J., Quantitative and qualitative preparations of bacterial outer membrane vesicles, in: Delcour, A. H. (Ed.), Bacterial Cell Surfaces: Methods and Protocols, Methods in Molecular Biology, Springer, New York 2013, pp. 259-272.
160. Frandoloso, R., Martínez-Martínez, S., Calmettes, C., Fegan, J. et al., Nonbinding site-directed mutants of transferrin binding protein B exhibit enhanced immunogenicity and protective capabilities. Infect. Immun. 2015, 83, 1030-1038.
161. Josefsberg, J. O., Buckland, B., Vaccine process technology. Biotechnol. Bioeng. 2012, 109, 1443-1460.
162. Baart, G. J. E., de Jong, G., Philippi, M., van 't Riet, K. et al., Scale-up of bulk production of vaccine against meningococcal disease. Vaccine 2007, 25, 6399-6408.
163. van de Waterbeemd, B., Streefland, M., van Keulen, L., van den IJssel, J. et al., Identification and optimization of critical process parameters for the production of nOMV vaccine against Neisseria meningitidis. Vaccine 2012, 30, 3683-3690.
164. Berlanda Scorza, F., Colucci, A. M., Maggiore, L., Sanzone, S. et al., High yield production process for Shigella outer membrane particles. PLoS One 2012, 7, e35616.
165. van de Waterbeemd, B., Zomer, B., Kaaijk, P., Ruiterkamp, N. et al., Improved production process for native outer membrane vesicle vaccine against Neisseria meningitidis. PLoS One 2013, e65157.
166. Ellis, T. N., Leiman, S. A., Kuehn, M. J., Naturally produced outer membrane vesicles from Pseudomonas aeruginosa elicit a potent innate immune response via combined sensing of both lipopolysaccharide and protein components. Infect. Immun. 2010, 78, 3822-3831.
167. Donato, G. M., Goldsmith, C. S., Paddock, C. D., Eby, J. C. et al., Delivery of Bordetella pertussis adenylate cyclase toxin to target cells via outer membrane vesicles. FEBS Lett. 2012, 586, 459-465.
168. Shang, E. S., Champion, C. I., Wu, X. Y., Skare, J. T. et al., Comparison of protection in rabbits against host-adapted and cultivated Borrelia burgdorferi following infection-derived immunity or immunization with outer membrane vesicles or outer surface protein A. Infect. Immun. 2000, 68, 4189-4199.
169. Dormitzer, P. R., Grandi, G., Rappuoli, R., Structural vaccinology starts to deliver. Nat. Rev. Microbiol. 2012, 10, 807-813.
170. Thornton, V., Lennon, D., Rasanathan, K., O'Hallahan, J. et al., Safety and immunogenicity of New Zealand strain meningococcal serogroup B OMV vaccine in healthy adults: Beginning of epidemic control. Vaccine 2006, 24, 1395-1400.
171. de Kleijn, E. D., de Groot, R., Labadie, J., Lafeber, A. B. et al., Immunogenicity and safety of a hexavalent meningococcal outer-membrane-vesicle vaccine in children of 2±3 and 7±8 years of age. Vaccine 2000, 18, 1456-1466.
172. de Kleijn, E. D., van Eijndhoven, L., Vermont, C., Kuipers, B. et al., Serum bactericidal activity and isotype distribution of antibodies in toddlers and schoolchildren after vaccination with RIVM hexavalent PorA vesicle vaccine. Vaccine 2002, 20, 352-358.
173. Martin, S., Sadler, F., Borrow, R., Dawson, M. et al., IgG antibody subclass responses determined by immunoblot in infants' sera following vaccination with a meningococcal recombinant hexavalent PorA OMV vaccine. Vaccine 2001, 19, 4404-4408.
174. Keiser, P. B., Gibbs, B. T., Coster, T. S., Moran, E. E. et al., A phase 1 study of a group B meningococcal native outer membrane vesicle vaccine made from a strain with deleted lpxL2 and synX and stable expression of opcA. Vaccine 2010, 28, 6970-6976.
175. Keiser, P. B., Biggs-Cicatelli, S., Moran, E. E., Schmiel, D. H. et al., A phase 1 study of a meningococcal native outer membrane vesicle vaccine made from a group B strain with deleted lpxL1 and synX, over-expressed factor H binding protein, two PorAs and stabilized OpcA expression. Vaccine 2011, 29, 1413-1420.
176. Gorringe, A. R., Taylor, S., Brookes, C., Matheson, M. et al., Phase I safety and immunogenicity study of a candidate meningococcal disease vaccine based on Neisseria lactamica outer membrane vesicles. Clin. Vaccine Immunol. 2009, 16, 1113-1120.
177. McConnell, M.J., Rumbo, C., Bou, G., Pachón, J., Outer membrane vesicles as an acellular vaccine against Acinetobacter baumannii. Vaccine 2011, 29, 5705-5710.
178. Avila-Calderon, E. D., Lopez-Merino, A., Jain, N., Peralta, H. et al., Characterization of outer membrane vesicles from Brucella melitensis and protection induced in mice. Clin. Dev. Immunol. 2012, 2012, 352493.
179. Nieves, W., Petersen, H., Judy, B. M., Blumentritt, C. A. et al., A Burkholderia pseudomallei outer membrane vesicle vaccine provides protection against lethal sepsis. Clin. Vaccine Immunol. 2014, 21, 747-754.
180. Keenan, J., Day, T., Neal, S., Cook, B. et al., A role for the bacterial outer membrane in the pathogenesis of Helicobacter pylori infection. FEMS Microbiol. Lett. 2000, 182, 259-264.
181. Lee, J. C., Lee, E. J., Lee, J. H., Jun, S. H. et al., Klebsiella pneumoniae secretes outer membrane vesicles that induce the innate immune response. FEMS Microbiol Lett. 2012, 331, 17-24.
182. Finney, M., Vaughan, T., Taylor, S., Hudson, M. J. et al., Characterization of the key antigenic components and pre-clinical immune responses to a meningococcal disease vaccine based on Neisseria lactamica outer membrane vesicles. Hum. Vaccin. 2008, 4, 23-30.
183. Mitra, S., Chakrabarti, M. K., Koley, H., Multi-serotype outer membrane vesicles of Shigellae confer passive protection to the neonatal mice against shigellosis. Vaccine 2013, 31, 3163-3173.