Gram-negative and Gram-positive bacterial extracellular vesicles

Seminars in Cell and Developmental Biology

Volumn 40, Issue , 2015, Pages 97-104

  Kim, Ji Hyun ^a   Lee, Jaewook ^a   Park, Jaesung ^a   Gho, Yong Song ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

Bacteria; Communicasomes; Diagnosis; Extracellular vesicles; Outer membrane vesicles; Vaccines

Indexed keywords

DNA; LIPID; PROTEIN; RNA;

BIOGENESIS; CELL COMMUNICATION; EXOSOME; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HOST; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE VESICLE; NONHUMAN; OUTER MEMBRANE; REVIEW; STAPHYLOCOCCUS AUREUS; ANIMAL; BACTERIAL INFECTION; CYTOLOGY; METABOLISM; MICROBIOLOGY; ORGANISMAL INTERACTION;

BACTERIA (MICROORGANISMS); MAMMALIA; NEGIBACTERIA; POSIBACTERIA;

ANIMALS; BACTERIAL INFECTIONS; EXTRACELLULAR VESICLES; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HUMANS; MICROBIAL INTERACTIONS;

EID: 84929289365     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.02.006     Document Type: Review

References (97)

1. 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.
2. Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967, 13:269-288.
3. Lee E.Y., Choi D.Y., Kim D.K., Kim J.W., Park J.O., Kim S., et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 2009, 9:5425-5436.
4. Soler N., Marguet E., Verbavatz J.M., Forterre P. Virus-like vesicles and extracellular DNA produced by hyperthermophilic archaea of the order Thermococcales. Res Microbiol 2008, 159:390-399.
5. 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.
6. Skog J., Wurdinger T., van Rijn S., Meijer D.H., Gainche L., Sena-Esteves M., et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell biol 2008, 10:1470-1476.
7. Choi D.S., Kim D.K., Kim Y.K., Gho Y.S. Proteomics of extracellular vesicles: exosomes and ectosomes. Mass Spectrom Rev 2014, 10.1002/mas.21420.
8. Kim D.K., Kang B., Kim O.Y., Choi D.S., Lee J., Kim S.R., et al. EVpedia: an integrated database of high-throughput data for systemic analyses of extracellular vesicles. J Extracell Vesicles 2013, 2:20384.
9. Deatherage B.L., Cookson B.T. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun 2012, 80:1948-1957.
10. Choi D.S., Yang J.S., Choi E.J., Jang S.C., Park S., Kim O.Y., et al. The protein interaction network of extracellular vesicles derived from human colorectal cancer cells. J Proteome Res 2012, 11:1144-1151.
11. MacDonald I.A., Kuehn M.J. Offense and defense: microbial membrane vesicles play both ways. Res Microbiol 2012, 163:607-618.
12. Kulp A., Kuehn M.J. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Ann Rev Microbiol 2010, 64:163-184.
13. Bladen H.A., Waters J.F. Electron microscopic study of some strains of Bacteroides. J Bacteriol 1963, 86:1339-1344.
14. Lee E.Y., Bang J.Y., Park G.W., Choi D.S., Kang J.S., Kim H.J., et al. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 2007, 7:3143-3153.
15. Kadurugamuwa J.L., Beveridge T.J. Membrane vesicles derived from Pseudomonas aeruginosa and Shigella flexneri can be integrated into the surfaces of other Gram-negative bacteria. Microbiology 1999, 145:2051-2060.
16. Choi D.S., Kim D.K., Choi S.J., Lee J., Choi J.P., Rho S., et al. Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa. Proteomics 2011, 11:3424-3429.
17. Post D.M., Zhang D., Eastvold J.S., Teghanemt A., Gibson B.W., Weiss J.P. Biochemical and functional characterization of membrane blebs purified from Neisseria meningitidis serogroup B. J Biol Chem 2005, 280:38383-38394.
18. Fiocca R., Necchi V., Sommi P., Ricci V., Telford J., Cover T.L., 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.
19. Wai S.N., Lindmark B., Soderblom T., Takade A., Westermark M., Oscarsson J., et al. Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 2003, 115:25-35.
20. Kwon S.O., Gho Y.S., Lee J.C., Kim S.I. Proteome analysis of outer membrane vesicles from a clinical Acinetobacter baumannii isolate. FEMS Microbiol Lett 2009, 297:150-156.
21. Schooling S.R., Beveridge T.J. Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 2006, 188:5945-5957.
22. Toyofuku M., Roschitzki B., Riedel K., Eberl L. Identification of proteins associated with the Pseudomonas aeruginosa biofilm extracellular matrix. J Proteome Res 2012, 11:4906-4915.
23. Yonezawa H., Osaki T., Kurata S., Fukuda M., Kawakami H., Ochiai K., et al. Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol 2009, 9:197.
24. Beveridge T.J. Structures of Gram-negative cell walls and their derived membrane vesicles. J Bacteriol 1999, 181:4725-4733.
25. Imamura T., Potempa J., Pike R.N., Moore J.N., Barton M.H., Travis J. Effect of free and vesicle-bound cysteine proteinases of Porphyromonas gingivalis on plasma clot formation: implications for bleeding tendency at periodontitis sites. Infect Immun 1995, 63:4877-4882.
26. Namork E., Brandtzaeg P. Fatal meningococcal septicaemia with blebbing meningococcus. Lancet 2002, 360:1741.
27. Kim Y.S., Choi E.J., Lee W.H., Choi S.J., Roh T.Y., Park J., 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 2013, 43:443-454.
28. Unal C.M., Schaar V., Riesbeck K. Bacterial outer membrane vesicles in disease and preventive medicine. Semin Immunopathol 2011, 33:395-408.
29. 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.
30. Berleman J., Auer M. The role of bacterial outer membrane vesicles for intra- and interspecies delivery. Environ Microbiol 2013, 15:347-354.
31. Mashburn L.M., Whiteley M. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 2005, 437:422-425.
32. Mashburn-Warren L., Howe J., Brandenburg K., Whiteley M. Structural requirements of the Pseudomonas quinolone signal for membrane vesicle stimulation. J Bacteriol 2009, 191:3411-3414.
33. Haurat M.F., Elhenawy W., Feldman M.F. Prokaryotic membrane vesicles: new insights on biogenesis and biological roles. Biol Chem 2015, 396:95-109.
34. Bonnington K.E., Kuehn M.J. Protein selection and export via outer membrane vesicles. Biochim Biophys Acta 2014, 1843:1612-1619.
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. Ferrari G., Garaguso I., Adu-Bobie J., Doro F., Taddei A.R., Biolchi A., 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.
37. Kuehn M.J., Kesty N.C. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 2005, 19:2645-2655.
38. 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.
39. Kesty N.C., Mason K.M., Reedy M., Miller S.E., Kuehn M.J. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J 2004, 23:4538-4549.
40. Chowdhury C., Jagannadham M.V. Virulence factors are released in association with outer membrane vesicles of Pseudomonas syringae pv. tomato T1 during normal growth. Biochim Biophys Acta 2013, 1834:231-239.
41. 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.
42. Kolling G.L., Matthews K.R. Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl Environ Microbiol 1999, 65:1843-1848.
43. Mashburn-Warren L.M., Whiteley M. Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 2006, 61:839-846.
44. Ellis T.N., Kuehn M.J. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 2010, 74:81-94.
45. Sahu P.K., Iyer P.S., Oak A.M., Pardesi K.R., Chopade B.A. Characterization of eDNA from the clinical strain Acinetobacter baumannii AIIMS 7 and its role in biofilm formation. Sci World J 2012, 2012:973436.
46. 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.
47. Vasilyeva N.V., Tsfasman I.M., Suzina N.E., Stepnaya O.A., Kulaev I.S. Secretion of bacteriolytic endopeptidase L5 of Lysobacter sp. XL1 into the medium by means of outer membrane vesicles. FEBS J 2008, 275:3827-3835.
48. Ciofu O., Beveridge T.J., Kadurugamuwa J., Walther-Rasmussen J., Hoiby N. Chromosomal beta-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa. J Antimicrob Chemother 2000, 45:9-13.
49. Nevot M., Deroncele V., Messner P., Guinea J., Mercade E. Characterization of outer membrane vesicles released by the psychrotolerant bacterium Pseudoalteromonas antarctica NF3. Environ Microbiol 2006, 8:1523-1533.
50. Roden J.A., Wells D.H., Chomel B.B., Kasten R.W., Koehler J.E. Hemin binding protein C is found in outer membrane vesicles and protects Bartonella henselae against toxic concentrations of hemin. Infect Immun 2012, 80:929-942.
51. Tan T.T., Morgelin M., Forsgren A., Riesbeck K. Haemophilus influenzae survival during complement-mediated attacks is promoted by Moraxella catarrhalis outer membrane vesicles. J Infect Dis 2007, 195:1661-1670.
52. 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.
53. Bomberger J.M., Maceachran D.P., Coutermarsh B.A., Ye S., O'Toole G.A., Stanton B.A. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 2009, 5:e1000382.
54. 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.
55. Kim J.H., Yoon Y.J., Lee J., Choi E.J., Yi N., Park K.S., et al. Outer membrane vesicles derived from Escherichia coli up-regulate expression of endothelial cell adhesion molecules in vitro and in vivo. PLoS ONE 2013, 8:e59276.
56. Kato S., Kowashi Y., Demuth D.R. Outer membrane-like vesicles secreted by Actinobacillus actinomycetemcomitans are enriched in leukotoxin. Microb Pathog 2002, 32:1-13.
57. Hozbor D., Rodriguez M.E., Fernandez J., Lagares A., Guiso N., Yantorno O. Release of outer membrane vesicles from Bordetella pertussis. Curr Microbiol 1999, 38:273-278.
58. Galka F., Wai S.N., Kusch H., Engelmann S., Hecker M., Schmeck B., et al. Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun 2008, 76:1825-1836.
59. Park K.S., Choi K.H., Kim Y.S., Hong B.S., Kim O.Y., Kim J.H., et al. Outer membrane vesicles derived from Escherichia coli induce systemic inflammatory response syndrome. PLoS ONE 2010, 5:e11334.
60. Shah B., Sullivan C.J., Lonergan N.E., Stanley S., Soult M.C., Britt L.D. Circulating bacterial membrane vesicles cause sepsis in rats. Shock 2012, 37:621-628.
61. Schaar V., de Vries S.P., Perez Vidakovics M.L., Bootsma H.J., Larsson L., Hermans P.W., et al. Multicomponent Moraxella catarrhalis outer membrane vesicles induce an inflammatory response and are internalized by human epithelial cells. Cell Microbiol 2011, 13:432-449.
62. Lee J.C., Lee E.J., Lee J.H., Jun S.H., Choi C.W., Kim S.I., et al. Klebsiella pneumoniae secretes outer membrane vesicles that induce the innate immune response. FEMS Microbiol Lett 2012, 331:17-24.
63. Park K.S., Lee J., Jang S.C., Kim S.R., Jang M.H., Lötvall J., et al. Pulmonary inflammation induced by bacteria-free outer membrane vesicles from Pseudomonas aeruginosa. Am J Respir Cell Mol Biol 2013, 49:637-645.
64. Kim O.Y., Hong B.S., Park K.S., Yoon Y.J., Choi S.J., Lee W.H., et al. Immunization with Escherichia coli outer membrane vesicles protects bacteria-induced lethality via Th1 and Th17 cell responses. J Immunol 2013, 190:4092-4102.
65. Schild S., Nelson E.J., Bishop A.L., Camilli A. Characterization of Vibrio cholerae outer membrane vesicles as a candidate vaccine for cholera. Infect Immun 2009, 77:472-484.
66. 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.
67. Acevedo R., Fernandez S., Zayas C., Acosta A., Sarmiento M.E., Ferro V.A., et al. Bacterial outer membrane vesicles and vaccine applications. Front Immunol 2014, 5:121.
68. Baker J.L., Chen L., Rosenthal J.A., Putnam D., Delisa M.P. Microbial biosynthesis of designer outer membrane vesicles. Curr Opin Biotechnol 2014, 29:76-84.
69. Jang S.C., Kim S.R., Yoon Y.J., Park K.S., Kim J.H., Lee J., et al. In vivo kinetic biodistribution of nano-sized outer membrane vesicles derived from bacteria. Small 2015, 11:456-461.
70. Rivera J., Cordero R.J., Nakouzi A.S., Frases S., Nicola A., Casadevall A. Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc Natl Acad Sci U S A 2010, 107:19002-19007.
71. Schrempf H., Koebsch I., Walter S., Engelhardt H., Meschke H. Extracellular Streptomyces vesicles: amphorae for survival and defence. Microb Biotechnol 2011, 4:286-299.
72. Lee J.H., Choi C.W., Lee T., Kim S.I., Lee J.C., Shin J.H. Transcription factor σ(B) plays an important role in the production of extracellular membrane-derived vesicles in Listeria monocytogenes. PLoS ONE 2013, 8:e73196.
73. Jiang Y., Kong Q., Roland K.L., Curtiss R. Membrane vesicles of Clostridium perfringens type A strains induce innate and adaptive immunity. Int J Med Microbiol 2014, 304:431-443.
74. Liao S., Klein M.I., Heim K.P., Fan Y., Bitoun J.P., Ahn S.J., et al. Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery. J Bacteriol 2014, 196:2355-2366.
75. Olaya-Abril A., Prados-Rosales R., McConnell M.J., Martin-Pena R., Gonzalez-Reyes J.A., Jimenez-Munguia I., et al. Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae. J Proteomics 2014, 106:46-60.
76. Hong S.W., Kim M.R., Lee E.Y., Kim J.H., Kim Y.S., Jeon S.G., et al. Extracellular vesicles derived from Staphylococcus aureus induce atopic dermatitis-like skin inflammation. Allergy 2011, 66:351-359.
77. Kim M.R., Hong S.W., Choi E.B., Lee W.H., Kim Y.S., Jeon S.G., et al. Staphylococcus aureus-derived extracellular vesicles induce neutrophilic pulmonary inflammation via both Th1 and Th17 cell responses. Allergy 2012, 67:1271-1281.
78. Lee J., Lee E.Y., Kim S.H., Kim D.K., Park K.S., Kim K.P., et al. Staphylococcus aureus extracellular vesicles carry biologically active beta-lactamase. Antimicrob Agents Chemother 2013, 57:2589-2595.
79. Hong S.W., Choi E.B., Min T.K., Kim J.H., Kim M.H., Jeon S.G., et al. An important role of alpha-hemolysin in extracellular vesicles on the development of atopic dermatitis induced by Staphylococcus aureus. PLoS ONE 2014, 9:e100499.
80. Gurung M., Moon D.C., Choi C.W., Lee J.H., Bae Y.C., Kim J., et al. Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLoS ONE 2011, 6:e27958.
81. Thay B., Wai S.N., Oscarsson J. Staphylococcus aureus alpha-toxin-dependent induction of host cell death by membrane-derived vesicles. PLoS ONE 2013, 8:e54661.
82. Lee H.M., Choi E.J., Kim J.H., Kim T.D., Kim Y.K., Kang C., et al. A membranous form of ICAM-1 on exosomes efficiently blocks leukocyte adhesion to activated endothelial cells. Biochem Biophys Res Commun 2010, 397:251-256.
83. Brown L., Kessler A., Cabezas-Sanchez P., Luque-Garcia J.L., Casadevall A. Extracellular vesicles produced by the Gram-positive bacterium Bacillus subtilis are disrupted by the lipopeptide surfactin. Mol Microbiol 2014, 93:183-198.
84. Wiedmann M., Arvik T.J., Hurley R.J., Boor K.J. General stress transcription factor sigmaB and its role in acid tolerance and virulence of Listeria monocytogenes. J Bacteriol 1998, 180:3650-3656.
85. Choi D.S., Kim D.K., Kim Y.K., Gho Y.S. Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics 2013, 13:1554-1571.
86. Lloubes R., Bernadac A., Houot L., Pommier S. Non classical secretion systems. Res Microbiol 2013, 164:655-663.
87. Lee J.C. Staphylococcus aureus membrane vesicles and its potential role in bacterial pathogenesis. J Bacteriol Virol 2012, 42:181-188.
88. Mullaney E., Brown P.A., Smith S.M., Botting C.H., Yamaoka Y.Y., Terres A.M., et al. Proteomic and functional characterization of the outer membrane vesicles from the gastric pathogen Helicobacter pylori. Proteomics Clin Appl 2009, 3:785-796.
89. Kahnt J., Aguiluz K., Koch J., Treuner-Lange A., Konovalova A., Huntley S., et al. Profiling the outer membrane proteome during growth and development of the social bacterium Myxococcus xanthus by selective biotinylation and analyses of outer membrane vesicles. J Proteome Res 2010, 9:5197-5208.
90. Jin J.S., Kwon S.O., Moon D.C., Gurung M., Lee J.H., Kim S.I., et al. Acinetobacter baumannii secretes cytotoxic outer membrane protein A via outer membrane vesicles. PLoS ONE 2011, 6:e17027.
91. Pierson T., Matrakas D., Taylor Y.U., Manyam G., Morozov V.N., Zhou W., 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.
92. Mendez J.A., Soares N.C., Mateos J., Gayoso C., Rumbo C., Aranda J., et al. Extracellular proteome of a highly invasive multidrug-resistant clinical strain of Acinetobacter baumannii. J Proteome Res 2012, 11:5678-5694.
93. van de Waterbeemd B., Mommen G.P., Pennings J.L., Eppink M.H., Wijffels R.H., van der Pol L.A., et al. Quantitative proteomics reveals distinct differences in the protein content of outer membrane vesicle vaccines. J Proteome Res 2013, 12:1898-1908.
94. Jang K.S., Sweredoski M.J., Graham R.L., Hess S., Clemons W.M. Comprehensive proteomic profiling of outer membrane vesicles from Campylobacter jejuni. J Proteomics 2014, 98:90-98.
95. Aguilera L., Toloza L., Gimenez R., Odena A., Oliveira E., Aguilar J., et al. Proteomic analysis of outer membrane vesicles from the probiotic strain Escherichia coli Nissle 1917. Proteomics 2014, 14:222-229.
96. Kulkarni H.M., Swamy Ch V., Jagannadham M.V. 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 2014, 13:1345-1358.
97. Bai J., Kim S.I., Ryu S., Yoon H. Identification and characterization of outer membrane vesicle-associated proteins in Salmonella enterica serovar Typhimurium. Infect Immun 2014, 82:4001-4010. T.