Membrane vesicle release in bacteria, eukaryotes, and archaea: A conserved yet underappreciated aspect of microbial life

Infection and Immunity

Volumn 80, Issue 6, 2012, Pages 1948-1957

  Deatheragea, Brooke L ^a,b   Cooksona, Brad T ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIAL TOXIN; ESCRT PROTEIN;

ADAPTIVE IMMUNITY; ARCHAEON; BACTERIAL INFECTION; BACTERIAL MEMBRANE; BIOGENESIS; CELL CYCLE; CELL DIVISION; CELL FUNCTION; CELL GROWTH; CELL ORGANELLE; CELL STRESS; CELL STRUCTURE; CELL SURFACE; EUKARYOTE; FUNGUS; GRAM POSITIVE BACTERIUM; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LEISHMANIA DONOVANI; MEMBRANE VESICLE; MOLECULAR DYNAMICS; MYCOSIS; NONHUMAN; OUTER MEMBRANE; PARASITE; PATHOGENESIS; PRIORITY JOURNAL; PROTEOBACTERIA; PSEUDOMONAS AERUGINOSA; SHORT SURVEY; ANIMAL; BACTERIUM; CELL MEMBRANE; CYTOLOGY; EXOSOME; METABOLISM; PHYSIOLOGY; REVIEW;

ANIMALS; ARCHAEA; BACTERIA; CELL MEMBRANE; EUKARYOTA; EXOSOMES; FUNGI; HOST-PATHOGEN INTERACTIONS; PARASITES;

EID: 84863838790     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.06014-11     Document Type: Short Survey

References (100)

1. Abadi J, Pirofski L. 1999. Antibodies reactive with the cryptococcal capsular polysaccharide glucuronoxylomannan are present in sera from children with and without human immunodeficiency virus infection. J. Infect. Dis. 180:915-919.
2. Alaniz RC, Deatherage BL, Lara JC, Cookson BT. 2007. 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. 179:7692-7701.
3. Albuquerque PC, et al. 2008. Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell. Microbiol. 10:1695-1710.
4. Bergman MA, et al. 2005. CD4_ T cells and toll-like receptors recognize Salmonella antigens expressed in bacterial surface organelles. Infect. Immun. 73:1350 -1356.
5. Bernadac A, Gavioli M, Lazzaroni JC, Raina S, Lloubes R. 1998. Escherichia coli tol-pal mutants form outer membrane vesicles. J. Bacteriol. 180:4872- 4878.
6. Beveridge TJ, Makin SA, Kadurugamuwa JL, Li Z. 1997. Interactions between biofilms and the environment. FEMS Microbiol. Rev. 20:291- 303.
7. Birdsell DC, Cota-Robles EH. 1967. Production and ultrastructure of lysozyme and ethylenediaminetetraacetate-lysozyme spheroplasts of Escherichia coli. J. Bacteriol. 93:427- 437.
8. Brandtzaeg P, et al. 2001. Neisseria meningitidis lipopolysaccharides in human pathology. J. Endotoxin Res. 7:401- 420.
9. Brandtzaeg P, et al. 1992. Meningococcal endotoxin in lethal septic shock plasma studied by gas chromatography, mass-spectrometry, ultracentrifugation, and electron microscopy. J. Clin. Invest. 89:816-823.
10. Brodsky IE, Ghori N, Falkow S, Monack D. 2005. Mig-14 is an inner membrane-associated protein that promotes Salmonella typhimurium resistance to CRAMP, survival within activated macrophages and persistent infection. Mol. Microbiol. 55:954 -972.
11. Brown A, Hormaeche CE. 1989. The antibody response to salmonellae in mice and humans studied by immunoblots and ELISA. Microb. Pathog. 6:445- 454.
12. Chutkan H, Kuehn MJ. 2011. Context-dependent activation kinetics elicited by soluble versus outer membrane vesicle-associated heat-labile enterotoxin. Infect. Immun. 79:3760 -3769.
13. Cocucci E, Racchetti G, Meldolesi J. 2009. Shedding microvesicles: artefacts no more. Trends Cell Biol. 19:43-51.
14. Cummings LA, Deatherage BL, Cookson BT. 17 September 2009, posting date. Chapter 8.8.11, Adaptive immune responses during Salmonella infection. In Fang F, Kagnoff MF (ed), EcoSal-Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, DC. http://www.ecosal.org.
15. Deatherage BL, et al. 2009. Biogenesis of bacterial membrane vesicles. Mol. Microbiol. 72:1395-1407.
16. Dorward DW, Garon CF. 1990. DNA is packaged within membranederived vesicles of gram-negative but not gram-positive bacteria. Appl. Environ. Microbiol. 56:1960 -1962.
17. Ellen AF, et al. 2009. Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles 13:67-79.
18. Ellen AF, Zolghadr B, Driessen AM, Albers SV. 2010. Shaping the archaeal cell envelope. Archaea 2010:608243.
19. Engelhardt H, Gerbl-Rieger S, Krezmar D, Schneider-Voss S, Engel A, Baumeister W. 1990. Structural properties of the outer membrane and the regular surface protein of Comamonas acidovorans. J. Struct. Biol. 105:92-102.
20. Feldmesser M, Kress Y, Casadevall A. 2001. Dynamic changes in the morphology of Cryptococcus neoformans during murine pulmonary infection. Microbiology 147:2355-2365.
21. Feldmesser M, Kress Y, Novikoff P, Casadevall A. 2000. Cryptococcus neoformans is a facultative intracellular pathogen in murine pulmonary infection. Infect. Immun. 68:4225- 4237.
22. Fernandez-Moreira E, Helbig JH, Swanson MS. 2006. Membrane vesicles shed by Legionella pneumophila inhibit fusion of phagosomes with lysosomes. Infect. Immun. 74:3285-3295.
23. Fiocca R, et al. 1999. 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. 188:220 -226.
24. Garcia-del Portillo F, Stein MA, Finlay BB. 1997. Release of lipopolysaccharide from intracellular compartments containing Salmo-nella typhimurium to vesicles of the host epithelial cell. Infect. Immun. 65:24 -34.
25. Gyorgy B, et al. 2011. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell. Mol. Life Sci. 68:2667-2688.
26. Hanson PI, Shim S, Merrill SA. 2009. Cell biology of the ESCRT machinery. Curr. Opin. Cell Biol. 21:568 -574.
27. Haurat MF, et al. 2011. Selective sorting of cargo proteins into bacterial membrane vesicles. J. Biol. Chem. 286:1269 -1276.
28. Hellman J, et al. 2000. Release of gram-negative outer-membrane proteins into human serum and septic rat blood and their interactions with immunoglobulin in antiserum to Escherichia coli J5. J. Infect. Dis. 181: 1034-1043.
29. Hoekstra D, van der Laan JW, de Leij L, Witholt B. 1976. Release of outer membrane fragments from normally growing Escherichia coli. Biochim. Biophys. Acta 455:889-899.
30. Horstman AL, Kuehn MJ. 2000. Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J. Biol. Chem. 275:12489 -12496.
31. Hozbor D, et al. 1999. Release of outer membrane vesicles from Bordetella pertussis. Curr. Microbiol. 38:273-278.
32. Hurley JH, Hanson PI. 2010. Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat. Rev. Mol. Cell Biol. 11:556- 566.
33. Kadurugamuwa JL, Beveridge TJ. 1997. Natural release of virulence factors in membrane vesicles by Pseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release. J. Antimicrob. Chemother. 40:615- 621.
34. Kahn ME, Barany F, Smith HO. 1983. Transformasomes: specialized membranous structures that protect DNA during Haemophilus transformation. Proc. Natl. Acad. Sci. U. S. A. 80:6927- 6931.
35. Kaparakis M, et al. 2010. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell. Microbiol. 12:372-385.
36. Kawai T, Akira S. 2009. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol. 21:317-337.
37. Keller S, Sanderson MP, Stoeck A, Altevogt P. 2006. Exosomes: from biogenesis and secretion to biological function. Immunol. Lett. 107:102- 108.
38. Kesty NC, Mason KM, Reedy M, Miller SE, Kuehn MJ. 2004. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23:4538-4549.
39. Kitagawa R, et al. 2010. Biogenesis of Salmonella enterica serovar Typhimurium membrane vesicles provoked by induction of PagC. J. Bacteriol. 192:5645-5656.
40. Knox KW, Vesk M, Work E. 1966. Relation between excreted lipopolysaccharide complexes and surface structures of a lysine-limited culture of Escherichia coli. J. Bacteriol. 92:1206 -1217.
41. Kouokam JC, et al. 2006. Active cytotoxic necrotizing factor 1 associated with outer membrane vesicles from uropathogenic Escherichia coli. Infect. Immun. 74:2022-2030.
42. Kuehn MJ, Kesty NC. 2005. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 19:2645-2655.
43. Kulp A, Kuehn MJ. 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 64:163-184.
44. Lam MY, et al. 1989. Occurrence of a common lipopolysaccharide antigen in standard and clinical strains of Pseudomonas aeruginosa. J. Clin. Microbiol. 27:962-967.
45. Lee EY, et al. 2007. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 7:3143-3153.
46. Lee EY, Choi DS, Kim KP, Gho YS. 2008. Proteomics in gram-negative bacterial outer membrane vesicles. Mass Spectrom. Rev. 27:535-555.
47. Lee EY, et al. 2009. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 9:5425-5436.
48. Leung KF, Dacks JB, Field MC. 2008. Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9:1698 -1716.
49. Lindmark B, et al. 2009. Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni.BMCMicrobiol. 9:220.
50. Loeb MR. 1974. Bacteriophage T4-mediated release of envelope components from Escherichia coli. J. Virol. 13:631- 641.
51. Makarova KS, Yutin N, Bell SD, Koonin EV. 2010. Evolution of diverse cell division and vesicle formation systems in Archaea. Nat. Rev. Microbiol. 8:731-741.
52. Marsollier L, et al. 2007. Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis. PLoS Pathog. 3:e62.
53. Mashburn-Warren L, et al. 2008. Interaction of quorum signals with outer membrane lipids: insights into prokaryotic membrane vesicle formation. Mol. Microbiol. 69:491-502.
54. Mashburn LM, Whiteley M. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422- 425.
55. Mathivanan S, Ji H, Simpson RJ. 2010. Exosomes: extracellular organelles important in intercellular communication. J. Proteomics 73:1907- 1920.
56. Mayer F, Gottschalk G. 2003. The bacterial cytoskeleton and its putative role in membrane vesicle formation observed in a Gram-positive bacterium producing starch-degrading enzymes. J. Mol. Microbiol. Biotechnol. 6:127-132.
57. McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ. 2006. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J. Bacteriol. 188:5385-5392.
58. McBroom AJ, Kuehn MJ. 12 May 2005, posting date. Chapter 2.2.4, Outer membrane vesicles. In Finlay BB (ed), EcoSal-Escherichia coli and Salmonella: cellular and molecular biology.ASMPress, Washington, DC. http://www.ecosal.org.
59. McBroom AJ, Kuehn MJ. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 63:545-558.
60. Mug-Opstelten D, Witholt B. 1978. Preferential release of new outer membrane fragments by exponentially growing Escherichia coli. Biochim. Biophys. Acta 508:287-295.
61. Munford RS, Varley AW. 2006. Shield as signal: lipopolysaccharides and the evolution of immunity to gram-negative bacteria. PLoS Pathog. 2:e67.
62. Namork E, Brandtzaeg P. 2002. Fatal meningococcal septicaemia with " blebbing" meningococcus. Lancet 360:1741.
63. Necchi V, et al. 2007. Intracellular, intercellular, and stromal invasion of gastric mucosa, preneoplastic lesions, and cancer by Helicobacter pylori. Gastroenterology 132:1009 -1023.
64. Nguyen TT, Saxena A, Beveridge TJ. 2003. Effect of surface lipopolysaccharide on the nature of membrane vesicles liberated from the Gramnegative bacterium Pseudomonas aeruginosa. J. Electron Microsc. (Tokyo) 52:465- 469.
65. Nosanchuk JD, Nimrichter L, Casadevall A, Rodrigues ML. 2008. A role for vesicular transport of macromolecules across cell walls in fungal pathogenesis. Commun. Integr. Biol. 1:37-39.
66. Oliveira DL, et al. 2010. Biogenesis of extracellular vesicles in yeast: many questions with few answers. Commun. Integr. Biol. 3:533-535.
67. Oliveira DL, et al. 2010. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One 5:e11113.
68. Piccin A, Murphy WG, Smith OP. 2007. Circulating microparticles: pathophysiology and clinical implications. Blood Rev. 21:157-171.
69. Prangishvili D, et al. 2000. Sulfolobicins, specific proteinaceous toxins produced by strains of the extremely thermophilic archaeal genus Sulfolobus. J. Bacteriol. 182:2985-2988.
70. Puohiniemi R, et al. 1990. A strong antibody response to the periplasmic C-terminal domain of the OmpA protein of Escherichia coli is produced by immunization with purified OmpA or with whole E. coli or Salmonella typhimurium bacteria. Infect. Immun. 58:1691-1696.
71. Rachel R, Wyschkony I, Riehl S, Huber H. 2002. The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 1:9 -18.
72. Ricci V, et al. 2005. Free-soluble and outer membrane vesicle-associated VacA from Helicobacter pylori: two forms of release, a different activity. Biochem. Biophys. Res. Commun. 337:173-178.
73. Rivera J, et al. 2010. Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc. Natl. Acad. Sci. U. S. A. 107:19002-19007.
74. Rivera M, Bryan LE, Hancock RE, McGroarty EJ. 1988. Heterogeneity of lipopolysaccharides from Pseudomonas aeruginosa: analysis of lipopolysaccharide chain length. J. Bacteriol. 170:512-521.
75. Rodrigues ML, et al. 2008. Extracellular vesicles produced by Crypto-coccus neoformans contain protein components associated with virulence. Eukaryot. Cell 7:58-67.
76. Rodrigues ML, et al. 2007. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot. Cell 6:48 -59.
77. Sakaguchi N, Baba T, Fukuzawa M, Ohno S. 1993. Ultrastructural study of Cryptococcus neoformans by quick-freezing and deep-etching method. Mycopathologia 121:133-141.
78. Schooling SR, Beveridge TJ. 2006. Membrane vesicles: an overlooked component of the matrices of biofilms. J. Bacteriol. 188:5945-5957.
79. Schop J. 2007. Protective immunity against cryptococcus neoformans infection. McGill J. Med. 10:35- 43.
80. Sharma A, et al. 2000. Porphyromonas gingivalis platelet aggregation activity: outer membrane vesicles are potent activators of murine platelets. Oral Microbiol. Immunol. 15:393-396.
81. Shetty A, Chen S, Tocheva EI, Jensen GJ, Hickey WJ. 2011. Nanopods: a new bacterial structure and mechanism for deployment of outer membrane vesicles. PLoS One 6:e20725.
82. Silverman JM, et al. 2008. Proteomic analysis of the secretome of Leishmania donovani. Genome Biol. 9:R35.
83. Silverman JM, et al. 2010. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J. Cell Sci. 123:842- 852.
84. Singh SP, Williams YU, Benjamin WH, Klebba PE, Boyd D. 1996. Immunoprotection by monoclonal antibodies to the porins and lipopolysaccharide of Salmonella typhimurium. Microb. Pathog. 21:249- 263.
85. Singh SP, Williams YU, Klebba PE, Macchia P, Miller S. 2000. Immune recognition of porin and lipopolysaccharide epitopes of Salmonella typhimurium in mice. Microb. Pathog. 28:157-167.
86. Soler N, Marguet E, Verbavatz JM, Forterre P. 2008. Virus-like vesicles and extracellular DNA produced by hyperthermophilic archaea of the order Thermococcales. Res. Microbiol. 159:390 -399.
87. Sommi P, et al. 1998. Persistence of Helicobacter pylori VacA toxin and vacuolating potential in cultured gastric epithelial cells. Am. J. Physiol. 275:G681-688.
88. Stephens DS, Edwards KM, Morris F, McGee ZA. 1982. Pili and outer membrane appendages on Neisseria meningitidis in the cerebrospinal fluid of an infant. J. Infect. Dis. 146:568.
89. Tashiro Y, Ichikawa S, Nakajima-Kambe T, Uchiyama H, Nomura N. 2010. Pseudomonas quinolone signal affects membrane vesicle production in not only gram-negative but also gram-positive bacteria. Microbes Environ. 25:120 -125.
90. Tetz VV, Rybalchenko OV, Savkova GA. 1990. Ultrastructural features of microbial colony organization. J. Basic Microbiol. 30:597- 607.
91. Trajkovic K, et al. 2008. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319:1244 -1247.
92. Vaughan TE, et al. 2006. Proteomic analysis of Neisseria lactamica and Neisseria meningitidis outer membrane vesicle vaccine antigens. Vaccine 24:5277-5293.
93. Vidakovics ML, et al. 2010. B cell activation by outer membrane vesicles- a novel virulence mechanism. PLoS Pathog. 6:e1000724.
94. Vipond C, et al. 2006. Proteomic analysis of a meningococcal outer membrane vesicle vaccine prepared from the group B strain NZ98/254. Proteomics 6:3400 -3413.
95. Wai SN, et al. 2003. Vesicle-mediated export and assembly of poreforming oligomers of the enterobacterial ClyA cytotoxin. Cell 115: 25-35.
96. Wensink J, Witholt B. 1981. Outer-membrane vesicles released by normally growing Escherichia coli contain very little lipoprotein. Eur. J. Biochem. 116:331-335.
97. Winter SE, et al. 2010. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426-429.
98. Wollert T, et al. 2009. The ESCRT machinery at a glance. J. Cell Sci. 122:2163-2166.
99. Xu HR, Tan YY, Hsu HS, Moncure CW, Wang XM. 1993. Comparative antibody response to Salmonella antigens in genetically resistant and susceptible mice. Clin. Exp. Immunol. 91:73-77
100. Yoon H, Ansong C, Adkins JN, Heffron F. 2011. Discovery of Salmonella virulence factors translocated via outer membrane vesicles to murine macrophages. Infect. Immun. 79:2182-2192.