Functional advantages conferred by extracellular prokaryotic membrane vesicles

Journal of Molecular Microbiology and Biotechnology

Volumn 23, Issue 1-2, 2013, Pages 131-141

  Manning, Andrew J ^a   Kuehn, Meta J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Antimicrobial protection; Biofilm; Outer membrane vesicles; Prokaryotic envelope; Transformation; Virulence factor transmission

Indexed keywords

HEAVY METAL; VIRULENCE FACTOR; ANTIINFECTIVE AGENT;

ARCHAEON; ARTICLE; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; BINDING AFFINITY; CELL FUNCTION; CELL ORGANELLE; CELL PROTECTION; GENE TARGETING; GENETIC TRANSFORMATION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; MEMBRANE VESICLE; NONHUMAN; ORGANISMAL INTERACTION; STRESS; COMMUNITY LIVING; CRYSTAL; ENERGY; EXTRACELLULAR SPACE; PROKARYOTIC CELL;

ARCHAEA; ARCHAEAL PROTEINS; BACTERIA; BACTERIAL OUTER MEMBRANE PROTEINS; BIOFILMS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CYTOPLASMIC VESICLES; EXTRACELLULAR MATRIX; ORGANELLES; VIRULENCE FACTORS;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; POSIBACTERIA; PROKARYOTA;

EID: 84876808643     PISSN: 14641801     EISSN: 16602412     Source Type: Journal    
DOI: 10.1159/000346548     Document Type: Article

References (84)

1. Baquero F: Environmental stress and evolvability in microbial systems. Clin Microbiol Infect 2009; 15(SUPPL. 1):5-10.
2. Barrangou R, Horvath P: CRISPR: new horizons in phage resistance and strain identification. Annu Rev Food Sci Technol 2012; 3:143-162.
3. Baumgarten T, Sperling S, Seifert J., von Bergen M, Steiniger F, Wick L.Y., Heipieper HJ: Membrane vesicle formation as a multiple-stress response mechanism enhances Pseudomonas putida DOT-T1E cell surface hydrophobicity and biofilm formation. Appl Environ Micro-biol 2012; 78:6217-6224.
4. Baumgarten T, Vazquez J, Bastisch C., Veron W, Feuilloley MG, Nietzsche S, Wick L.Y., Heipieper HJ: 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 2011; 93:837-845.
5. Beveridge TJ: Structures of Gram-negative cell walls and their derived membrane vesicles. J Bacteriol 1999; 181:4725-4733. (Pubitemid 29383496)
6. Carrio MM, Villaverde A: Construction and de-construction of bacterial inclusion bodies. J Biotechnol 2002; 96:3-12. (Pubitemid 34876295)
7. Chatterjee D, Chaudhuri K: Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Letters 2011; 585:1357-1362.
8. Chen DJ, Osterrieder N, Metzger S.M., Buckles E., Doody AM, DeLisa MP, Putnam D: Delivery of foreign antigens by engineered outer membrane vesicle vaccines. Proc Natl Acad Sci USA 2010; 107:3099-3104.
9. Chutkan H, Kuehn MJ: Context-dependent activation kinetics elicited by soluble versus outer membrane vesicle-associated heat-labile en-terotoxin. Infect Immun 2011; 79:3760-3769.
10. Collins BS: Gram-negative outer membrane vesicles in vaccine development. Discov Med 2011; 12:7-15.
11. Concino MF, Goodgal SH: DNA-binding vesicles released from the surface of a competence-deficient mutant of Haemophilus influenzae. J Bacteriol 1982; 152:441-450. (Pubitemid 13198700)
12. Deatherage BL, Lara JC, Bergsbaken T, Rassoulian Barrett SL, Lara S, Cookson BT: Biogenesis of bacterial membrane vesicles. Mol Microbiol 2009; 72:1395-1407.
13. Dorward DW, Garon CF: DNA-binding proteins in cells and membrane blebs of Neisseria gon-orrhoeae. J Bacteriol 1989; 171:4196-4201. (Pubitemid 19190314)
14. Dorward DW, Garon CF: DNA is packaged within membrane-derived vesicles of Gram-negative but not Gram-positive bacteria. Appl Environ Microbiol 1990; 56:1960-1962. (Pubitemid 20202172)
15. Dorward DW, Garon CF, Judd RC: Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J Bacteriol 1989; 171:2499-2505. (Pubitemid 19125081)
16. Ellen AF, Albers SV, Huibers W, Pitcher A., Hobel CF, Schwarz H, Folea M, Schouten S., Boekema EJ, Poolman B, et al: Proteomic analysis of secreted membrane vesicles of archaeal Sul-folobus species reveals the presence of endo-some sorting complex components. Extremophiles 2009; 13:67-79.
17. Ellis TN, Kuehn MJ: Virulence and immunomod-ulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 2010; 74:81-94.
18. Ferrari G, Garaguso I, Adu-Bobie J, Doro F., Taddei AR, Biolchi A, Brunelli B, Giuliani M.M., Pizza M., Norais N, 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.
19. Gaudin M, Gauliard E, Schouten S., Houel-Renault L, Lenormand P, Marguet E, Forterre P: Hyperthermophilic archaea produce membrane vesicles that can transfer DNA. Environ Microbiol Rep 2012, E-pub ahead of print.
20. Gerlach RG, Hensel M: Protein secretion systems and adhesins: the molecular armory of Gramnegative pathogens. Int J Med Microbiol 2007; 297:401-415. (Pubitemid 47375177)
21. Gorby Y, McLean J, Korenevsky A., Rosso K, El-Naggar MY, Beveridge TJ: Redox-reactive membrane vesicles produced by Shewanella. Geobiology 2008; 6:232-241. (Pubitemid 351733133)
22. Govan JR, Deretic V: Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aerugi-nosa and Burkholderia cepacia. Microbiol Rev 1996; 60:539-574. (Pubitemid 26303478)
23. Grenier D, Belanger M: Protective effect of Por-phyromonas gingivalis outer membrane vesicles against bactericidal activity of human serum. Infect Immun 1991; 59:3004-3008.
24. Grenier D, Bertrand J, Mayrand D: Porphyromo-nas gingivalis outer membrane vesicles promote bacterial resistance to chlorhexidine. Oral Microbiol Immunol 1995; 10:319-320.
25. Gurung M, Moon DC, Choi C.W., Lee JH, Bae YC, Kim J, Lee Y.C., Seol SY, Cho DT, Kim SI, et al: Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLoS One 2011; 6:e27958.
26. Hayes CS, Aoki SK, Low DA: Bacterial contact-dependent delivery systems. Annu Rev Genet 2010; 44:71-90.
27. Henderson IR, Navarro-Garcia F, Desvaux M., Fernandez RC, Ala'Aldeen D: Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 2004; 68:692-744. (Pubitemid 39628534)
28. Horstman AL, Kuehn MJ: Enterotoxigenic Escherichia coli secretes active heat-labile entero-toxin via outer membrane vesicles. J Biol Chem 2000; 275:12489-12496. (Pubitemid 30241392)
29. Horstman AL, Kuehn MJ: Bacterial surface association of heat-labile enterotoxin through li-popolysaccharide after secretion via the general secretory pathway. J Biol Chem 2002; 277: 32538-32545. (Pubitemid 34987554)
30. Jani AJ, Cotter PA: Type VI secretion: not just for pathogenesis anymore. Cell Host and Microbe 2010; 8:2-6.
31. Johnson TL, Abendroth J, Hol W.G., Sandkvist M: Type II secretion: from structure to function. FEMS Microbiol Lett 2006; 255:175-186.
32. Juhas M, Crook DW, Hood DW: Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell Microbiol 2008; 10:2377-2386.
33. Kadurugamuwa JL, Beveridge TJ: Virulence factors are released from Pseudomonas aerugi-nosa in association with membrane vesicles during normal growth and exposure to genta-micin: a novel mechanism of enzyme secretion. J Bacteriol 1995; 177:3998-4008.
34. Kadurugamuwa JL, Beveridge TJ: Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J Bacteriol 1996; 178:2767-2774. (Pubitemid 26144032)
35. Kadurugamuwa JL, Beveridge TJ: 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. (Pubitemid 27503991)
36. Kadurugamuwa JL, Clarke AJ, Beveridge TJ: Surface action of gentamicin on Pseudomonas ae-ruginosa. J Bacteriol 1993; 175:5798-5805. (Pubitemid 23277426)
37. Kesty NC, Kuehn MJ: Incorporation of heterolo-gous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J Biol Chem 2004; 279:2069-2076. (Pubitemid 38084479)
38. Kesty NC, Mason KM, Reedy M, Miller S.E., Kuehn MJ: Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. Embo J 2004; 23:4538-4549. (Pubitemid 39657854)
39. Khandelwal P, Banerjee-Bhatnagar N: Insecticid-al activity associated with the outer membrane vesicles of Xenorhabdus nematophilus. Appl Environ Microbiol 2003; 69:2032-2037. (Pubitemid 36443616)
40. Knox KW, 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.
41. Komeili A: Molecular mechanisms of compart-mentalization and biomineralization in mag-netotactic bacteria. FEMS Microbiol Rev 2011; 36:232-255.
42. Kreft JU: Biofilms promote altruism. Microbiology 2004; 150:2751-2760.
43. Kulp A, Kuehn MJ: Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 2010; 64:163-184.
44. Lee EY, Choi DS, Kim K.P., Gho YS: Proteomics in Gram-negative bacterial outer membrane vesicles. Mass Spectrom Rev 2008; 27:535-555.
45. Li Z, Clarke AJ, Beveridge TJ: A major autolysin of Pseudomonas aeruginosa: subcellular distribution, potential role in cell growth and division and secretion in surface membrane vesicles. J Bacteriol 1996; 178:2479-2488. (Pubitemid 26134469)
46. Li Z, Clarke AJ, Beveridge TJ: Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J Bacteriol 1998; 180:5478-5483. (Pubitemid 28471550)
47. Macdonald IA, Kuehn MJ: Offense and defense: microbial membrane vesicles play both ways. Res Microbiol 2012; 163:607-618.
48. Manning AJ, Kuehn MJ: Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiol 2011; 11:258.
49. Mashburn-Warren L., Howe J, Garidel P., Richter W, Steiniger F, Roessle M., Brandenburg K, Whiteley M: Interaction of quorum signals with outer membrane lipids: insights into prokaryotic membrane vesicle formation. Mol Microbiol 2008; 69:491-502. (Pubitemid 351988019)
50. Matlakowska R, Sklodowska A: The culturable bacteria isolated from organic-rich black shale potentially useful in biometallurgical procedures. J Appl Microbiol 2009; 107:858-866.
51. Matlakowska R, Sklodowska A, Nejbert K: Bio-weathering of Kupferschiefer black shale (Fore-Sudetic Monocline, SW Poland) by indigenous bacteria: implication for dissolution and precipitation of minerals in deep underground mine. FEMS Microbiol Ecol 2012; 81: 99-110.
52. McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ: Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 2006; 188:5385-5392. (Pubitemid 44157294)
53. McBroom AJ, Kuehn MJ: Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Micro-biol 2007; 63:545-558. (Pubitemid 46058939)
54. Miller ES, Kutter E, Mosig G., Arisaka F, Kunisawa T, Ruger W: Bacteriophage T4 genome. Microbiol Mol Biol Rev 2003; 67:86-156. (Pubitemid 36314786)
55. Moshiri A, Dashtbani-Roozbehani A, Najar Peerayeh S, Davar Siadat S: Outer membrane vesicle: a macromolecule with multifunctional activity. Hum Vaccin Immunother 2012; 8: 953-955.
56. Mudrak B, Rodriguez DL, Kuehn MJ: Residues of heat-labile enterotoxin involved in bacterial cell surface binding. J Bacteriol 2009; 191: 2917-2925.
57. Mullaney E, Brown PA, Smith S.M., Botting CH, Yamaoka YY, Terres AM, Kelleher DP, Windle HJ: Proteomic and functional characterization of the outer membrane vesicles from the gastric pathogen Helicobacter pylori. Proteomics Clin Appl 2009; 3:785-796.
58. Muralinath M, Kuehn MJ, Roland K.L., Curtiss R 3rd: Immunization with Salmonella enterica serovar Typhimurium-derived outer membrane vesicles delivering the pneumococcal protein PspA confers protection against challenge with serovar Typhimurium-derived outer membrane vesicles delivering the pneumococcal protein PspA confers protection against challenge with Streptococcus pneumoniae. Infect Immun 2010; 79:887-894.
59. Murat D, Byrne M, Komeili A: Cell biology of prokaryotic organelles. Cold Spring Harb Perspect Biol 2010; 2:a000422.
60. Prangishvili D, Holz I, Stieger E., Nickell S, Kristjansson JK, Zillig W: Sulfolobicins, specific proteinaceous toxins produced by strains of the extremely thermophilic archaeal genus Sulfolobus. J Bacteriol 2000; 182:2985-2988. (Pubitemid 30246936)
61. Rachel R, Wyschkony I, Riehl S., Huber H: The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 2002; 1:9-18. (Pubitemid 38871626)
62. Records AR: The type VI secretion system: a multipurpose delivery system with a phage-like machinery. Mol Plant Microbe Interact 2011; 24:751-757.
63. Renelli M, Matias V, Lo R.Y., Beveridge TJ: DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 2004; 150: 2161-2169. (Pubitemid 39117630)
64. Ricci V, Chiozzi V, Necchi V., Oldani A, Romano M, Solcia E., Ventura U: Free-soluble and outer membrane vesicle-associated VacA from Helicobacter pylori: two forms of release, a different activity. Biochem Biophys Res Commun 2005; 337:173-178. (Pubitemid 41393775)
65. Rivera J, Cordero RJ, Nakouzi A.S., Frases S., Nicola A, Casadevall A: Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc Natl Acad Sci USA 2010; 107:19002-19007.
66. Roier S, Leitner DR, Iwashkiw J, Schild-Prufert K, Feldman M.F., Krohne G., Reidl J, Schild S: Intranasal immunization with nontypeable Haemophilus influenzae outer membrane vesicles induces cross-protective immunity in mice. PLoS One 2012; 7:e42664.
67. Rompikuntal PK, Thay B, Khan M.K., Alanko J., Penttinen AM, Asikainen S, Wai SN, Oscarsson J: Perinuclear localization of internalized outer membrane vesicles carrying active cyto-lethal distending toxin from Aggregatibacter actinomycetemcomitans. Infect Immun 2012; 80:31-42.
68. Schooling SR, Beveridge TJ: Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 2006; 188:5945-5957. (Pubitemid 44384103)
69. Schooling SR, Hubley A, Beveridge TJ: Interactions of DNA with biofilm-derived membrane vesicles. J Bacteriol 2009; 191:4097-4102.
70. Shah B, Sullivan CJ, Lonergan N.E., Stanley S., Soult MC, Britt LD: Circulating bacterial membrane vesicles cause sepsis in rats. Shock 2012; 37:621-628.
71. Soler N, Gaudin M, Marguet E., Forterre P: Plas-mids, viruses and virus-like membrane vesicles from Thermococcales. Biochem Soc Trans 2011; 39:36-44.
72. 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.
73. Song T, Wai SN: A novel sRNA that modulates virulence and environmental fitness of Vibrio cholerae. RNA Biol 2009; 6:254-258.
74. Tashiro Y, Sakai R, Toyofuku M., Sawada I, Nakajima-Kambe T, Uchiyama H, Nomura N: Outer membrane machinery and alginate synthesis regulators control membrane vesicle production in Pseudomonas aeruginosa. J Bacteriol 2009; 191:7509-7519.
75. Thompson SS, Naidu YM, Pestka JJ: Ultrastructural localization of an extracellular protease in Pseudomonas fragi by using the peroxidase- antiperoxidase reaction. Appl Environ Microbiol 1985; 50:1038-1042. (Pubitemid 16192822)
76. Toussaint A, Chandler M: Prokaryote genome fluidity: toward a system approach of the mobilome. Methods Mol Biol 2012; 804:57-80.
77. van der Ley P, van den Dobbelsteen G: Next-generation outer membrane vesicle vaccines against Neisseria meningitidis based on non-toxic LPS mutants. Hum Vaccin 2011; 7:886-890.
78. Vasilyeva NV, Tsfasman IM, Suzina N.E., Stepnaya OA, Kulaev IS: Secretion of bacteriolytic en-dopeptidase L5 of Lysobacter sp. XL1 into the medium by means of outer membrane vesicles. FEBS J 2008; 275:3827-3835. (Pubitemid 351990948)
79. Wallden K, Rivera-Calzada A, Waksman G: Type IV secretion systems: versatility and diversity in function. Cell Microbiol 2010; 12:1203-1212.
80. Waters CM, Bassler BL: Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 2005; 21:319-346. (Pubitemid 41740638)
81. Yaron S, Kolling GL, Simon L, Matthews KR: Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl Environ Microbiol 2000; 66: 4414-4420.
82. Yonezawa H, Osaki T, Kurata S., Fukuda M, Kawakami H, Ochiai K., Hanawa T, Kamiya S: Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol 2009; 9:197.
83. Yonezawa H, Osaki T, Woo T., Kurata S, Zaman C, Hojo F., Hanawa T, Kato S, Kamiya S: Analysis of outer membrane vesicle protein involved in biofilm formation of Helicobacter pylori. Anaerobe 2011; 17:388-390.
84. Yu Q, Griffin EF, Moreau-Marquis S, Schwartzman JD, Stanton BA, O'Toole GA: In vitro evaluation of tobramycin and aztreonam versus Pseudomonas aeruginosa biofilms on cystic fibrosis-derived human airway epithelial cells. J Antimicrob Chemother 2012; 67:2673-2681.