Isolation of membrane vesicles from prokaryotes: a technical and biological comparison reveals heterogeneity

References

• Deatherage BL, Cookson BT. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun. 2012;80(6):1–14. ​​​​
   Web of Science ®Google Scholar
• Perez-Cruz C, Delgado L, Lopez-Iglesias C, et al. Outer-inner membrane vesicles naturally secreted by gram-negative pathogenic bacteria. Plos One. 2015;10(1):e0116896.
   PubMed Web of Science ®Google Scholar
• Perez-Cruz C, Carrion O, Delgado L, et al. New type of outer membrane vesicle produced by the Gram-negative bacterium Shewanella vesiculosa M7T: implications for DNA content. Appl Environ Microbiol. 2013;79(6):1874–1881.
   Web of Science ®Google Scholar
• Kulkarni HM, Jagannadham MV. Biogenesis and multifaceted roles of outer membrane vesicles from Gram-negative bacteria. Microbiology. 2014;160(Pt 10):2109–2121.
   PubMed Web of Science ®Google Scholar
• Grande R, Di Marcantonio MC, Robuffo I, et al. Helicobacter pylori ATCC 43629/NCTC 11639 outer membrane vesicles (OMVs) from biofilm and planktonic phase associated with extracellular DNA (eDNA). Front Microbiol. 2015;6:1369.
   PubMed Web of Science ®Google Scholar
• Yonezawa H, Osaki T, Kurata S, et al. Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol. 2009;9:197.
   PubMed Web of Science ®Google Scholar
• Macdonald IA, Kuehn MJ. Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa. J Bacteriol. 2013;195(13):2971–2981.
   PubMed Web of Science ®Google Scholar
• Kunsmann L, Ruter C, Bauwens A, et al. Virulence from vesicles: novel mechanisms of host cell injury by Escherichia coli O104: h4outbreak strain. Sci Rep. 2015;5:13252.
   PubMed Web of Science ®Google Scholar
• Elluri S, Enow C, Vdovikova S, et al. Outer membrane vesicles mediate transport of biologically active Vibrio cholerae cytolysin (VCC) from V. cholerae strains. Plos One. 2014;9(9):e106731.
   PubMed Web of Science ®Google Scholar
• Bielaszewska M, Ruter C, Kunsmann L, et al. Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis. Plos Pathog. 2013;9(12):e1003797.
   PubMed Web of Science ®Google Scholar
• Waller T, Kesper L, Hirschfeld J, et al. Porphyromonas gingivalis outer membrane vesicles induce selective tumor necrosis factor tolerance in a toll-like receptor 4- and mTOR-dependent manner. Infect Immun. 2016;84(4):1194–1204.
   Web of Science ®Google Scholar
• Deknuydt F, Nordstrom T, Riesbeck K. Diversion of the host humoral response: a novel virulence mechanism of Haemophilus influenzae mediated via outer membrane vesicles. J Leukoc Biol. 2014;95(6):983–991.
   Web of Science ®Google Scholar
• Manning AJ, Kuehn MJ. Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiol. 2011;11:258.
   PubMed Web of Science ®Google Scholar
• McCaig WD, Koller A, Thanassi DG. Production of outer membrane vesicles and outer membrane tubes by Francisella novicida. J Bacteriol. 2013;195(6):1120–1132.
   Web of Science ®Google Scholar
• Yuana Y, Koning RI, Kuil ME, et al. Cryo-electron microscopy of extracellular vesicles in fresh plasma. J Extracell Vesicles. 2013;2. ​​​​
   Google Scholar
• Hogan MC, Johnson KL, Zenka RM, et al. Subfractionation, characterization, and in-depth proteomic analysis of glomerular membrane vesicles in human urine. Kidney Int. 2014;85(5):1225–1237.
   PubMed Web of Science ®Google Scholar
• Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016;113(8):E968–E977.
   PubMed Web of Science ®Google Scholar
• Klimentova J, Stulik J. Methods of isolation and purification of outer membrane vesicles from gram-negative bacteria. Microbiol Res. 2015;170:1–9.
   Web of Science ®Google Scholar
• Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol. 2010;64:163–184.
   PubMed Web of Science ®Google Scholar
• Lotvall J, Hill AF, Hochberg F, et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International society for extracellular vesicles. J Extracell Vesicles. 2014;3:26913.
   PubMedGoogle Scholar
• Sidhu VK, Vorholter FJ, Niehaus K, et al. Analysis of outer membrane vesicle associated proteins isolated from the plant pathogenic bacterium Xanthomonas campestris pv. campestris. BMC Microbiol. 2008;8:87.
   Web of Science ®Google Scholar
• Avila-Calderon ED, Lopez-Merino A, Jain N, et al. Characterization of outer membrane vesicles from Brucella melitensis and protection induced in mice. Clin Dev Immunol. 2012;2012:352493.
   PubMedGoogle Scholar
• Berleman JE, Allen S, Danielewicz MA, et al. The lethal cargo of Myxococcus xanthus outer membrane vesicles. Front Microbiol. 2014;5:474.
   PubMed Web of Science ®Google Scholar
• Horstman AL, Kuehn MJ. Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J Biol Chem. 2000;275(17):12489–12496.
   PubMed Web of Science ®Google Scholar
• Roier S, Zingl FG, Cakar F, et al. A novel mechanism for the biogenesis of outer membrane vesicles in Gram-negative bacteria. Nat Commun. 2016;7:10515.
   PubMed Web of Science ®Google Scholar
• Blenkiron C, Simonov D, Muthukaruppan A, et al. Uropathogenic escherichia coli releases extracellular vesicles that are associated with RNA. Plos One. 2016;11(8):e0160440.
   PubMed Web of Science ®Google Scholar
• Biller SJ, Schubotz F, Roggensack SE, et al. Bacterial vesicles in marine ecosystems. Science. 2014;343(6167):183–186.
   PubMed Web of Science ®Google Scholar
• Sjostrom AE, Sandblad L, Uhlin BE, et al. Membrane vesicle-mediated release of bacterial RNA. Sci Rep. 2015;5:15329.
   PubMed Web of Science ®Google Scholar
• Ghosal A, Upadhyaya BB, Fritz JV, et al. The extracellular RNA complement of Escherichia coli. Microbiologyopen. 2015;4:252–266.
   PubMed Web of Science ®Google Scholar
• Post DM, Zhang D, Eastvold JS, et al. Biochemical and functional characterization of membrane blebs purified from Neisseria meningitidis serogroup B. J Biol Chem. 2005;280(46):38383–38394.
   PubMed Web of Science ®Google Scholar
• Kataoka M, Yamaoka A, Kawasaki K, et al. Extraordinary denaturant tolerance of keratinolytic protease complex assemblies produced by Meiothermus ruber H328. Appl Microbiol Biotechnol. 2014;98(7):2973–2980.
   PubMed Web of Science ®Google Scholar
• Boing AN, Van Der Pol E, Grootemaat AE, et al. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles. 2014;3. ​​​​
   Google Scholar
• Lobb RJ, Becker M, Wen SW, et al. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J Extracell Vesicles. 2015;4:27031.
   PubMed Web of Science ®Google Scholar
• De Menezes-Neto A, Sáez MJF, Lozano-Ramos I, et al. Size-exclusion chromatography as a stand-alone methodology identifies novel markers in mass spectrometry analyses of plasma-derived vesicles from healthy individuals. J Extracell Vesicles. 2015;4:27378.
   PubMed Web of Science ®Google Scholar
• Lozano-Ramos I, Bancu I, Oliveira-Tercero A, et al. Size-exclusion chromatography-based enrichment of extracellular vesicles from urine samples. J Extracell Vesicles. 2015;4:27369.
   PubMed Web of Science ®Google Scholar
• Knapp S, Hacker J, Jarchau T, et al. Large, unstable inserts in the chromosome affect virulence properties of uropathogenic Escherichia coli O6 strain 536. J Bacteriol. 1986;168(1):22–30.
   Web of Science ®Google Scholar
• Nissle A. Die antagonistische behandlung chronischer darmstörungen mit colibakterien. Med Klin (Munich). 1918;2:29–33.
   Google Scholar
• Snapper SB, Melton RE, Mustafa S, et al. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol. 1990;4(11):1911–1919.
   Web of Science ®Google Scholar
• Allen BW. Mycobacteria. General culture methodology and safety considerations. Methods Mol Biol. 1998;101:15–30.
   PubMedGoogle Scholar
• Dauros-Singorenko P, Swift S. The transition from iron starvation to iron sufficiency as an important step in the progression of infection. Sci Prog. 2014;97(Pt 4):371–382.
   Google Scholar
• Rowe MC, Withers HL, Uropathogenic SS. Escherichia coli forms biofilm aggregates under iron restriction that disperse upon the supply of iron. FEMS Microbiol Lett. 2010;307(1):102–109.
   Web of Science ®Google Scholar
• Van Der Pol E, Coumans FA, Grootemaat AE, et al. Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing. J Thromb Haemost. 2014;12(7):1182–1192.
   PubMed Web of Science ®Google Scholar
• Filipe V, Hawe A, Jiskoot W. Critical evaluation of nanoparticle tracking analysis (NTA) by NanoSight for the measurement of nanoparticles and protein aggregates. Pharm Res. 2010;27(5):796–810.
   PubMed Web of Science ®Google Scholar
• Grozdanov L, Raasch C, Schulze J, et al. Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol. 2004;186(16):5432–5441.
   PubMed Web of Science ®Google Scholar
• Baranyai T, Herczeg K, Onodi Z, et al. Isolation of exosomes from blood plasma: qualitative and quantitative comparison of ultracentrifugation and size exclusion chromatography methods. Plos One. 2015;10(12):e0145686.
   PubMed Web of Science ®Google Scholar
• Raetz CR, Whitfield C. Lipopolysaccharide endotoxins. Annu Rev Biochem. 2002;71:635–700.
   PubMed Web of Science ®Google Scholar
• Molinaro A, Holst O, Di Lorenzo F, et al. Chemistry of lipid A: at the heart of innate immunity. Chemistry. 2015;21(2):500–519.
   PubMed Web of Science ®Google Scholar
• Schwechheimer C, Kuehn MJ. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol. 2015;13(10):605–619.
   PubMed Web of Science ®Google Scholar
• Witwer KW, Buzas EI, Bemis LT, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013;2. ​​​​
   PubMedGoogle Scholar
• Roy K, Hamilton DJ, Munson GP, et al. Outer membrane vesicles induce immune responses to virulence proteins and protect against colonization by enterotoxigenic Escherichia coli. Clin Vaccine Immunol. 2011;18(11):1803–1808.
   Web of Science ®Google Scholar
• Bauman SJ, Kuehn MJ. Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect. 2006;8(9–10):2400–2408.
   PubMed Web of Science ®Google Scholar
• Ellis TN, Leiman SA, Kuehn MJ. 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(9):3822–3831.
   PubMed Web of Science ®Google Scholar
• Prados-Rosales R, Weinrick BC, Pique DG, et al. Role for Mycobacterium tuberculosis membrane vesicles in iron acquisition. J Bacteriol. 2014;196(6):1250–1256.
   PubMed Web of Science ®Google Scholar
• Keenan JI, Allardyce RA. Iron influences the expression of Helicobacter pylori outer membrane vesicle-associated virulence factors. Eur J Gastroenterol Hepatol. 2000;12(12):1267–1273.
   Web of Science ®Google Scholar
• Lappann M, Otto A, Becher D, et al. Comparative proteome analysis of spontaneous outer membrane vesicles and purified outer membranes of Neisseria meningitidis. J Bacteriol. 2013;195(19):4425–4435.
   PubMed Web of Science ®Google Scholar
• Olczak T, Wojtowicz H, Ciuraszkiewicz J, et al. Species specificity, surface exposure, protein expression, immunogenicity, and participation in biofilm formation of Porphyromonas gingivalis HmuY. BMC Microbiol. 2010;10:134.
   PubMed Web of Science ®Google Scholar
• Gorringe A, Halliwell D, Matheson M, et al. The development of a meningococcal disease vaccine based on Neisseria lactamica outer membrane vesicles. Vaccine. 2005;23(17–18):2210–2213.
   Web of Science ®Google Scholar
• Lai RC, Tan SS, Yeo RW, et al. MSC secretes at least 3 EV types each with a unique permutation of membrane lipid, protein and RNA. J Extracell Vesicles. 2016;5:29828.
   PubMed Web of Science ®Google Scholar
• Kulp AJ, Sun B, Ai T, et al. Genome-wide assessment of outer membrane vesicle production in escherichia coli. Plos One. 2015;10(9):e0139200.
   PubMed Web of Science ®Google Scholar
• Duperthuy M, Sjostrom AE, Sabharwal D, et al. Role of the Vibrio cholerae matrix protein Bap1 in cross-resistance to antimicrobial peptides. Plos Pathog. 2013;9(10):e1003620.
   Web of Science ®Google Scholar
• Bobrie A, Colombo M, Krumeich S, et al. Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation. J Extracell Vesicles. 2012;1. ​​​​
   PubMedGoogle Scholar
• Clark DJ, Fondrie WE, Liao Z, et al. Redefining the breast cancer exosome proteome by tandem mass tag quantitative proteomics and multivariate cluster analysis. Anal Chem. 2015;87(20):10462–10469.
   PubMed Web of Science ®Google Scholar