SpringerLink
Log in

Delivery of Virulence Factors by Bacterial Membrane Vesicles to Mammalian Host Cells

  • Chapter
  • First Online:
Bacterial Membrane Vesicles

Abstract

Bacterial membrane vesicles represent a universal secretion mechanism enabling both Gram-negative and Gram-positive organisms to transfer cargo to eukaryotic cells, as well as to other bacterial cells. Bacterial vesicles can deliver to target cells an extremely wide range of virulence factors, including exotoxins, lipids, nucleic acids, and small molecules. Although there has been extensive research to decipher the mechanisms regulating cellular uptake of Gram-negative bacterial outer membrane vesicles (OMVs), much less is known about the cellular uptake of Gram-positive bacterial membrane vesicles (MVs). This chapter focuses on a selection of major bacterial pathogens and summarizes the present knowledge of OMV and MV-mediated virulence factor delivery, as well as mechanisms of bacterial vesicle–host cell interaction and uptake by mammalian cells.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmad I, Karah N, Nadeem A, Wai SN, Uhlin BE (2019) Analysis of colony phase variation switch in Acinetobacter baumannii clinical isolates. PLoS One 14:e0210082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aldick T, Bielaszewska M, Uhlin BE, Humpf HU, Wai SN, Karch H (2009) Vesicular stabilization and activity augmentation of enterohaemorrhagic Escherichia coli haemolysin. Mol Microbiol 71:1496–1508

    Article  CAS  PubMed  Google Scholar 

  • Alvarez CS, Badia J, Bosch M, Gimenez R, Baldoma L (2016) Outer membrane vesicles and soluble factors released by probiotic Escherichia coli Nissle 1917 and commensal ECOR63 enhance barrier function by regulating expression of tight junction proteins in intestinal epithelial cells. Front Microbiol 7:1981

    PubMed  PubMed Central  Google Scholar 

  • Amano A, Takeuchi H, Furuta N (2010) Outer membrane vesicles function as offensive weapons in host-parasite interactions. Microbes Infect 12:791–798

    Article  CAS  PubMed  Google Scholar 

  • Askarian F, Lapek JD Jr, Dongre M, Tsai CM, Kumaraswamy M, Kousha A, Valderrama JA, Ludviksen JA, Cavanagh JP, Uchiyama S, Mollnes TE, Gonzalez DJ, Wai SN, Nizet V, Johannessen M (2018) Staphylococcus aureus membrane-derived vesicles promote bacterial virulence and confer protective immunity in murine infection models. Front Microbiol 9:262

    Article  PubMed  PubMed Central  Google Scholar 

  • Balsalobre C, Silvan JM, Berglund S, Mizunoe Y, Uhlin BE, Wai SN (2006) Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli. Mol Microbiol 59:99–112

    Article  CAS  PubMed  Google Scholar 

  • Bauman SJ, Kuehn MJ (2006) Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect 8:2400–2408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bauman SJ, Kuehn MJ (2009) Pseudomonas aeruginosa vesicles associate with and are internalized by human lung epithelial cells. BMC Microbiol 9:26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behrouzi A, Vaziri F, Riazi Rad F, Amanzadeh A, Fateh A, Moshiri A, Khatami S, Siadat SD (2018) Comparative study of pathogenic and non-pathogenic Escherichia coli outer membrane vesicles and prediction of host-interactions with TLR signaling pathways. BMC Res Notes 11:539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belanger M, Kozarov E, Song H, Whitlock J, Progulske-Fox A (2012) Both the unique and repeat regions of the Porphyromonas gingivalis hemagglutin A are involved in adhesion and invasion of host cells. Anaerobe 18:128–134

    Article  CAS  PubMed  Google Scholar 

  • Berlanda Scorza F, Doro F, Rodriguez-Ortega MJ, Stella M, Liberatori S, Taddei AR, Serino L, Gomes Moriel D, Nesta B, Fontana MR, Spagnuolo A, Pizza M, Norais N, Grandi G (2008) Proteomics characterization of outer membrane vesicles from the extraintestinal pathogenic Escherichia coli DeltatolR IHE3034 mutant. Mol Cell Proteomics 7:473–485

    Article  CAS  PubMed  Google Scholar 

  • Berleman J, Auer M (2013) The role of bacterial outer membrane vesicles for intra- and interspecies delivery. Environ Microbiol 15:347–354

    Article  CAS  PubMed  Google Scholar 

  • Berube BJ, Bubeck Wardenburg J (2013) Staphylococcus aureus alpha-toxin: nearly a century of intrigue. Toxins (Basel) 5:1140–1166

    Article  Google Scholar 

  • Beveridge TJ, Makin SA, Kadurugamuwa JL, Li Z (1997) Interactions between biofilms and the environment. FEMS Microbiol Rev 20(3–4):291–303

    Article  CAS  PubMed  Google Scholar 

  • Biagini M, Garibaldi M, Aprea S, Pezzicoli A, Doro F, Becherelli M, Taddei AR, Tani C, Tavarini S, Mora M, Teti G, D’Oro U, Nuti S, Soriani M, Margarit I, Rappuoli R, Grandi G, Norais N (2015) The human pathogen Streptococcus pyogenes releases lipoproteins as lipoprotein-rich membrane vesicles. Mol Cell Proteomics 14:2138–2149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bielaszewska M, Ruter C, Kunsmann L, Greune L, Bauwens A, Zhang W, Kuczius T, Kim KS, Mellmann A, Schmidt MA, Karch H (2013) Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis. PLoS Pathog 9:e1003797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bielaszewska M, Ruter C, Bauwens A, Greune L, Jarosch KA, Steil D, Zhang W, He X, Lloubes R, Fruth A, Kim KS, Schmidt MA, Dobrindt U, Mellmann A, Karch H (2017) Host cell interactions of outer membrane vesicle-associated virulence factors of enterohemorrhagic Escherichia coli O157: intracellular delivery, trafficking and mechanisms of cell injury. PLoS Pathog 13:e1006159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bielaszewska M, Marejkova M, Bauwens A, Kunsmann-Prokscha L, Mellmann A, Karch H (2018) Enterohemorrhagic Escherichia coli O157 outer membrane vesicles induce interleukin 8 production in human intestinal epithelial cells by signaling via toll-like receptors TLR4 and TLR5 and activation of the nuclear factor NF-kappaB. Int J Med Microbiol 308:882–889

    Article  CAS  PubMed  Google Scholar 

  • Bielig H, Dongre M, Zurek B, Wai SN, Kufer TA (2011a) A role for quorum sensing in regulating innate immune responses mediated by Vibrio cholerae outer membrane vesicles (OMVs). Gut Microbes 2:274–279

    Article  PubMed  Google Scholar 

  • Bielig H, Rompikuntal PK, Dongre M, Zurek B, Lindmark B, Ramstedt M, Wai SN, Kufer TA (2011b) NOD-like receptor activation by outer membrane vesicles from Vibrio cholerae non-O1 non-O139 strains is modulated by the quorum-sensing regulator HapR. Infect Immun 79:1418–1427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biller SJ, Schubotz F, Roggensack SE, Thompson AW, Summons RE, Chisholm SW (2014) Bacterial vesicles in marine ecosystems. Science 343:183–186

    Article  CAS  PubMed  Google Scholar 

  • Bitto NJ, Kaparakis-Liaskos M (2017) The therapeutic benefit of bacterial membrane vesicles. Int J Mol Sci 18:E1287

    Article  CAS  PubMed  Google Scholar 

  • Bitto NJ, Chapman R, Pidot S, Costin A, Lo C, Choi J, D’Cruze T, Reynolds EC, Dashper SG, Turnbull L, Whitchurch CB, Stinear TP, Stacey KJ, Ferrero RL (2017) Bacterial membrane vesicles transport their DNA cargo into host cells. Sci Rep 7:7072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blenkiron C, Simonov D, Muthukaruppan A, Tsai P, Dauros P, Green S, Hong J, Print CG, Swift S, Phillips AR (2016) Uropathogenic Escherichia coli releases extracellular vesicles that are associated with RNA. PLoS One 11:e0160440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bomberger JM, Maceachran DP, Coutermarsh BA, Ye S, O'Toole GA, Stanton BA (2009) Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 5:e1000382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bourgeau G, Mayrand D (1990) Aggregation of Actinomyces strains by extracellular vesicles produced by Bacteroides gingivalis. Can J Microbiol 36:362–365

    Article  CAS  PubMed  Google Scholar 

  • Brown EA, Hardwidge PR (2007) Biochemical characterization of the enterotoxigenic Escherichia coli LeoA protein. Microbiology 153:3776–3784

    Article  CAS  PubMed  Google Scholar 

  • Canas MA, Gimenez R, Fabrega MJ, Toloza L, Baldoma L, Badia J (2016) Outer membrane vesicles from the probiotic Escherichia coli Nissle 1917 and the commensal ECOR12 enter intestinal epithelial cells via clathrin-dependent endocytosis and elicit differential effects on DNA damage. PLoS One 11:e0160374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canas MA, Fabrega MJ, Gimenez R, Badia J, Baldoma L (2018) Outer membrane vesicles from probiotic and commensal Escherichia coli activate NOD1-mediated immune responses in intestinal epithelial cells. Front Microbiol 9:498

    Article  PubMed  PubMed Central  Google Scholar 

  • Cavanagh JP, Pain M, Askarian F, Bruun JA, Urbarova I, Wai SN, Schmidt F, Johannessen M (2018) Comparative exoproteome profiling of an invasive and a commensal Staphylococcus haemolyticus isolate. J Proteomics 195:33–40

    Google Scholar 

  • Chatterjee D, Chaudhuri K (2011) Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Lett 585:1357–1362

    Article  CAS  PubMed  Google Scholar 

  • Choi JW, Kim SC, Hong SH, Lee HJ (2017a) Secretable Small RNAs via outer membrane vesicles in periodontal pathogens. J Dent Res 96:458–466

    Article  CAS  PubMed  Google Scholar 

  • Choi JW, Um JH, Cho JH, Lee HJ (2017b) Tiny RNAs and their voyage via extracellular vesicles: secretion of bacterial small RNA and eukaryotic microRNA. Exp Biol Med (Maywood) 242:1475–1481

    Article  CAS  Google Scholar 

  • Ciofu O, Beveridge TJ, Kadurugamuwa J, Walther-Rasmussen J, Hoiby N (2000) Chromosomal beta-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa. J Antimicrob Chemother 45:9–13

    Article  CAS  PubMed  Google Scholar 

  • Codemo M, Muschiol S, Iovino F, Nannapaneni P, Plant L, Wai SN, Henriques-Normark B (2018) Immunomodulatory effects of pneumococcal extracellular vesicles on cellular and humoral host defenses. MBio 9:e00559–e00518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dallo SF, Zhang B, Denno J, Hong S, Tsai A, Haskins W, Ye JY, Weitao T (2012) Association of Acinetobacter baumannii EF-Tu with cell surface, outer membrane vesicles, and fibronectin. Sci World J 2012:128705

    Article  CAS  Google Scholar 

  • Dean SN, Leary DH, Sullivan CJ, Oh E, Walper SA (2019) Isolation and characterization of lactobacillus-derived membrane vesicles. Sci Rep 9:877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902

    Article  CAS  PubMed  Google Scholar 

  • Donato GM, Goldsmith CS, Paddock CD, Eby JC, Gray MC, Hewlett EL (2012) Delivery of Bordetella pertussis adenylate cyclase toxin to target cells via outer membrane vesicles. FEBS Lett 586:459–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorward DW, Garon CF (1989) DNA-binding proteins in cells and membrane blebs of Neisseria gonorrhoeae. J Bacteriol 171:4196–4201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorward DW, Garon CF, Judd RC (1989) Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J Bacteriol 171:2499–2505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duchesne P, Grenier D, Mayrand D (1995) Demonstration of adherence properties of Porphyromonas gingivalis outer membrane vesicles using a new microassay. Oral Microbiol Immunol 10:76–80

    Article  CAS  PubMed  Google Scholar 

  • Ellen RP, Grove DA (1989) Bacteroides gingivalis vesicles bind to and aggregate Actinomyces viscosus. Infect Immun 57:1618–1620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis TN, Leiman SA, Kuehn MJ (2010) 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 78:3822–3831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elluri S, Enow C, Vdovikova S, Rompikuntal PK, Dongre M, Carlsson S, Pal A, Uhlin BE, Wai SN (2014) Outer membrane vesicles mediate transport of biologically active Vibrio cholerae cytolysin (VCC) from V. cholerae strains. PLoS One 9:e106731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elmi A, Watson E, Sandu P, Gundogdu O, Mills DC, Inglis NF, Manson E, Imrie L, Bajaj-Elliott M, Wren BW, Smith DG, Dorrell N (2012) Campylobacter jejuni outer membrane vesicles play an important role in bacterial interactions with human intestinal epithelial cells. Infect Immun 80:4089–4098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elmi A, Nasher F, Jagatia H, Gundogdu O, Bajaj-Elliott M, Wren B, Dorrell N (2016) Campylobacter jejuni outer membrane vesicle-associated proteolytic activity promotes bacterial invasion by mediating cleavage of intestinal epithelial cell E-cadherin and occludin. Cell Microbiol 18:561–572

    Article  CAS  PubMed  Google Scholar 

  • Evans AG, Davey HM, Cookson A, Currinn H, Cooke-Fox G, Stanczyk PJ, Whitworth DE (2012) Predatory activity of Myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo. Microbiology 158:2742–2752

    Article  CAS  PubMed  Google Scholar 

  • Fabrega MJ, Rodriguez-Nogales A, Garrido-Mesa J, Algieri F, Badia J, Gimenez R, Galvez J, Baldoma L (2017) Intestinal anti-inflammatory effects of outer membrane vesicles from Escherichia coli Nissle 1917 in DSS-experimental colitis in mice. Front Microbiol 8:1274

    Article  PubMed  PubMed Central  Google Scholar 

  • Fulsundar S, Harms K, Flaten GE, Johnsen PJ, Chopade BA, Nielsen KM (2014) Gene transfer potential of outer membrane vesicles of Acinetobacter baylyi and effects of stress on vesiculation. Appl Environ Microbiol 80:3469–3483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furuta N, Tsuda K, Omori H, Yoshimori T, Yoshimura F, Amano A (2009) Porphyromonas gingivalis outer membrane vesicles enter human epithelial cells via an endocytic pathway and are sorted to lysosomal compartments. Infect Immun 77:4187–4196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galka F, Wai SN, Kusch H, Engelmann S, Hecker M, Schmeck B, Hippenstiel S, Uhlin BE, Steinert M (2008) Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun 76(5):1825–1836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gankema H, Wensink J, Guinee PA, Jansen WH, Witholt B (1980) Some characteristics of the outer membrane material released by growing enterotoxigenic Escherichia coli. Infect Immun 29:704–713

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao W, Howden BP, Stinear TP (2018) Evolution of virulence in Enterococcus faecium, a hospital-adapted opportunistic pathogen. Curr Opin Microbiol 41:76–82

    Article  PubMed  Google Scholar 

  • George KM, Chatterjee D, Gunawardana G, Welty D, Hayman J, Lee R, Small PL (1999) Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283:854–857

    Article  CAS  PubMed  Google Scholar 

  • Ghosh A, Saha DR, Hoque KM, Asakuna M, Yamasaki S, Koley H, Das SS, Chakrabarti MK, Pal A (2006) Enterotoxigenicity of mature 45-kilodalton and processed 35-kilodalton forms of hemagglutinin protease purified from a cholera toxin gene-negative Vibrio cholerae non-O1, non-O139 strain. Infect Immun 74:2937–2946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green ER, Mecsas J (2016) Bacterial secretion systems: an overview. Microbiol Spectr 4

    Google Scholar 

  • Gurung M, Moon DC, Choi CW, Lee JH, Bae YC, Kim J, Lee YC, Seol SY, Cho DT, Kim SI, Lee JC (2011) Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLoS One 6:e27958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hase CC, Finkelstein RA (1991) Cloning and nucleotide sequence of the Vibrio cholerae hemagglutinin/protease (HA/protease) gene and construction of an HA/protease-negative strain. J Bacteriol 173:3311–3317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haurat MF, Aduse-Opoku J, Rangarajan M, Dorobantu L, Gray MR, Curtis MA, Feldman MF (2011) Selective sorting of cargo proteins into bacterial membrane vesicles. J Biol Chem 286:1269–1276

    Article  CAS  PubMed  Google Scholar 

  • Ho MH, Chen CH, Goodwin JS, Wang BY, **e H (2015) Functional advantages of Porphyromonas gingivalis vesicles. PLoS One 10:e0123448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hornung V (2014) SnapShot: nucleic acid immune sensors, part 1. Immunity 41:868, 868 e1

    PubMed  Google Scholar 

  • Horstman AL, Kuehn MJ (2000) Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J Biol Chem 275:12489–12496

    Article  CAS  PubMed  Google Scholar 

  • Horstman AL, Kuehn MJ (2002) Bacterial surface association of heat-labile enterotoxin through lipopolysaccharide after secretion via the general secretory pathway. J Biol Chem 277:32538–32545

    Article  CAS  PubMed  Google Scholar 

  • Hozbor D, Rodriguez ME, Fernandez J, Lagares A, Guiso N, Yantorno O (1999) Release of outer membrane vesicles from Bordetella pertussis. Curr Microbiol 38:273–278

    Article  CAS  PubMed  Google Scholar 

  • Imagawa T, Sonoda S, Kanoh M, Utsumi S (1979) Polymorphonuclear leukocyte-inhibitory factor of Bordetella pertussis. II. Localization in the outer membrane. Biken J 22:1–10

    CAS  PubMed  Google Scholar 

  • Irving AT, Mimuro H, Kufer TA, Lo C, Wheeler R, Turner LJ, Thomas BJ, Malosse C, Gantier MP, Casillas LN, Votta BJ, Bertin J, Boneca IG, Sasakawa C, Philpott DJ, Ferrero RL, Kaparakis-Liaskos M (2014) The immune receptor NOD1 and kinase RIP2 interact with bacterial peptidoglycan on early endosomes to promote autophagy and inflammatory signaling. Cell Host Microbe 15:623–635

    Article  CAS  PubMed  Google Scholar 

  • Jager J, Keese S, Roessle M, Steinert M, Schromm AB (2015) Fusion of Legionella pneumophila outer membrane vesicles with eukaryotic membrane systems is a mechanism to deliver pathogen factors to host cell membranes. Cell Microbiol 17:607–620

    Article  CAS  PubMed  Google Scholar 

  • Jeon H, Oh MH, Jun SH, Kim SI, Choi CW, Kwon HI, Na SH, Kim YJ, Nicholas A, Selasi GN, Lee JC (2016) Variation among Staphylococcus aureus membrane vesicle proteomes affects cytotoxicity of host cells. Microb Pathog 93:185–193

    Article  CAS  PubMed  Google Scholar 

  • Jha C, Ghosh S, Gautam V, Malhotra P, Ray P (2017) In vitro study of virulence potential of Acinetobacter baumannii outer membrane vesicles. Microb Pathog 111:218–224

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Kong Q, Roland KL, Curtiss R 3rd (2014) Membrane vesicles of Clostridium perfringens type a strains induce innate and adaptive immunity. Int J Med Microbiol 304:431–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson AM, Kaushik RS, Francis DH, Fleckenstein JM, Hardwidge PR (2009) Heat-labile enterotoxin promotes Escherichia coli adherence to intestinal epithelial cells. J Bacteriol 191:178–186

    Article  CAS  PubMed  Google Scholar 

  • Jun SH, Lee JH, Kim BR, Kim SI, Park TI, Lee JC, Lee YC (2013) Acinetobacter baumannii outer membrane vesicles elicit a potent innate immune response via membrane proteins. PLoS One 8:e71751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadurugamuwa JL, Beveridge TJ (1995) Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177:3998–4008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kadurugamuwa JL, Beveridge TJ (1998) Delivery of the non-membrane-permeative antibiotic gentamicin into mammalian cells by using Shigella flexneri membrane vesicles. Antimicrob Agents Chemother 42:1476–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadurugamuwa JL, Beveridge TJ (1999) Membrane vesicles derived from Pseudomonas aeruginosa and Shigella flexneri can be integrated into the surfaces of other gram-negative bacteria. Microbiology 145(Pt 8):2051–2060

    Article  CAS  PubMed  Google Scholar 

  • Kamaguchi A, Nakayama K, Ichiyama S, Nakamura R, Watanabe T, Ohta M, Baba H, Ohyama T (2003) Effect of Porphyromonas gingivalis vesicles on coaggregation of Staphylococcus aureus to oral microorganisms. Curr Microbiol 47:485–491

    Article  CAS  PubMed  Google Scholar 

  • Kaparakis M, Turnbull L, Carneiro L, Firth S, Coleman HA, Parkington HC, Le Bourhis L, Karrar A, Viala J, Mak J, Hutton ML, Davies JK, Crack PJ, Hertzog PJ, Philpott DJ, Girardin SE, Whitchurch CB, Ferrero RL (2010) Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol 12:372–385

    Article  CAS  PubMed  Google Scholar 

  • Kaparakis-Liaskos M, Ferrero RL (2015) Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol 15:375–387

    Article  CAS  PubMed  Google Scholar 

  • Kaper JB, Morris JG Jr, Levine MM (1995) Cholera. Clin Microbiol Rev 8:48–86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kieselbach T, Zijnge V, Granstrom E, Oscarsson J (2015) Proteomics of Aggregatibacter actinomycetemcomitans outer membrane vesicles. PLoS One 10:e0138591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YR, Kim BU, Kim SY, Kim CM, Na HS, Koh JT, Choy HE, Rhee JH, Lee SE (2010) Outer membrane vesicles of Vibrio vulnificus deliver cytolysin-hemolysin VvhA into epithelial cells to induce cytotoxicity. Biochem Biophys Res Commun 399:607–612

    Article  CAS  PubMed  Google Scholar 

  • Kim OY, Park HT, Dinh NTH, Choi SJ, Lee J, Kim JH, Lee SW, Gho YS (2017) Bacterial outer membrane vesicles suppress tumor by interferon-gamma-mediated antitumor response. Nat Commun 8:626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi H, Uematsu K, Hirayama H, Horikoshi K (2000) Novel toluene elimination system in a toluene-tolerant microorganism. J Bacteriol 182:6451–6455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koeppen K, Hampton TH, Jarek M, Scharfe M, Gerber SA, Mielcarz DW, Demers EG, Dolben EL, Hammond JH, Hogan DA, Stanton BA (2016) A novel mechanism of host-pathogen interaction through sRNA in bacterial outer membrane vesicles. PLoS Pathog 12:e1005672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koeppen K, Barnaby R, Jackson AA, Gerber SA, Hogan DA, Stanton BA (2019) Tobramycin reduces key virulence determinants in the proteome of Pseudomonas aeruginosa outer membrane vesicles. PLoS One 14:e0211290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolling GL, Matthews KR (1999) Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl Environ Microbiol 65:1843–1848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kondo K, Takade A, Amako K (1993) Release of the outer membrane vesicles from Vibrio cholerae and Vibrio parahaemolyticus. Microbiol Immunol 37:149–152

    Article  CAS  PubMed  Google Scholar 

  • Kouokam JC, Wai SN, Fallman M, Dobrindt U, Hacker J, Uhlin BE (2006) Active cytotoxic necrotizing factor 1 associated with outer membrane vesicles from uropathogenic Escherichia coli. Infect Immun 74:2022–2030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kunsmann L, Ruter C, Bauwens A, Greune L, Gluder M, Kemper B, Fruth A, Wai SN, He X, Lloubes R, Schmidt MA, Dobrindt U, Mellmann A, Karch H, Bielaszewska M (2015) Virulence from vesicles: novel mechanisms of host cell injury by Escherichia coli O104:H4 outbreak strain. Sci Rep 5:13252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee EY, Bang JY, Park GW, Choi DS, Kang JS, Kim HJ, Park KS, Lee JO, Kim YK, Kwon KH, Kim KP, Gho YS (2007) Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 7:3143–3153

    Article  PubMed  Google Scholar 

  • Lee EY, Choi DY, Kim DK, Kim JW, Park JO, Kim S, Kim SH, Desiderio DM, Kim YK, Kim KP, Gho YS (2009) Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 9:5425–5436

    Article  CAS  PubMed  Google Scholar 

  • Lee JH, Choi CW, Lee T, Kim SI, Lee JC, Shin JH (2013) Transcription factor sigmaB plays an important role in the production of extracellular membrane-derived vesicles in Listeria monocytogenes. PLoS One 8:e73196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Yoon YJ, Kim JH, Dinh NTH, Go G, Tae S, Park KS, Park HT, Lee C, Roh TY, Di Vizio D, Gho YS (2018) Outer membrane vesicles derived from Escherichia coli regulate neutrophil migration by induction of endothelial IL-8. Front Microbiol 9:2268

    Article  PubMed  PubMed Central  Google Scholar 

  • Lei L, Yang F, Zou J, **g H, Zhang J, Xu W, Zou Q, Zhang J (2019) Wang X (2019) DNA vaccine encoding OmpA and Pal from Acinetobacter baumannii efficiently protects mice against pulmonary infection. Mol Biol Rep 46(5):5397–5408

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Clarke AJ, Beveridge TJ (1998) Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J Bacteriol 180:5478–5483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Nation RL, Turnidge JD, Milne RW, Coulthard K, Rayner CR, Pater-son DL (2006) Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections. Lancet Infect Dis 6:589–601

    Article  CAS  PubMed  Google Scholar 

  • Liao S, Klein MI, Heim KP, Fan Y, Bitoun JP, Ahn SJ, Burne RA, Koo H, Brady LJ, Wen ZT (2014) 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 196:2355–2366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindmark B, Rompikuntal PK, Vaitkevicius K, Song T, Mizunoe Y, Uhlin BE, Guerry P, Wai SN (2009) Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni. BMC Microbiol 9:220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339:520–532

    Article  CAS  PubMed  Google Scholar 

  • MacEachran DP, Ye S, Bomberger JM, Hogan DA, Swiatecka-Urban A, Stanton BA, O'Toole GA (2007) The Pseudomonas aeruginosa secreted protein PA2934 decreases apical membrane expression of the cystic fibrosis transmembrane conductance regulator. Infect Immun 75:3902–3912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malabirade A, Habier J, Heintz-Buschart A, May P, Godet J, Halder R, Etheridge A, Galas D, Wilmes P, Fritz JV (2018) The RNA complement of outer membrane vesicles from Salmonella enterica Serovar Typhimurium under distinct culture conditions. Front Microbiol 9:2015

    Article  PubMed  PubMed Central  Google Scholar 

  • Mantri CK, Chen CH, Dong X, Goodwin JS, Pratap S, Paromov V, **e H (2015) Fimbriae-mediated outer membrane vesicle production and invasion of Porphyromonas gingivalis. Microbiology 4:53–65

    CAS  Google Scholar 

  • Marsollier L, Brodin P, Jackson M, Kordulakova J, Tafelmeyer P, Carbonnelle E, Aubry J, Milon G, Legras P, Andre JP, Leroy C, Cottin J, Guillou ML, Reysset G, Cole ST (2007) Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis. PLoS Pathog 3:e62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mashburn LM, Whiteley M (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422–425

    Article  CAS  PubMed  Google Scholar 

  • Mashburn-Warren LM, Whiteley M (2006) Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61:839–846

    Article  CAS  PubMed  Google Scholar 

  • McConnell MJ, Rumbo C, Bou G, Pachon J (2011) Outer membrane vesicles as an acellular vaccine against Acinetobacter baumannii. Vaccine 29:5705–5710

    Article  CAS  PubMed  Google Scholar 

  • Mondal A, Tapader R, Chatterjee NS, Ghosh A, Sinha R, Koley H, Saha DR, Chakrabarti MK, Wai SN, Pal A (2016) Cytotoxic and inflammatory responses induced by outer membrane vesicle-associated biologically active proteases from Vibrio cholerae. Infect Immun 84:1478–1490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulcahy LA, Pink RC, Carter DR (2014) Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles 3. https://doi.org/10.3402/jev.v3.24641.eCollection

  • Murphy K, Park AJ, Hao Y, Brewer D, Lam JS, Khursigara CM (2014) Influence of O polysaccharides on biofilm development and outer membrane vesicle biogenesis in Pseudomonas aeruginosa PAO1. J Bacteriol 196:1306–1317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakao R, Myint SL, Wai SN, Uhlin BE (2018) Enhanced biofilm formation and membrane vesicle release by Escherichia coli expressing a commonly occurring plasmid gene, kil. Front Microbiol 9:2605

    Article  PubMed  PubMed Central  Google Scholar 

  • Nevo-Dinur K, Govindarajan S, Amster-Choder O (2012) Subcellular localization of RNA and proteins in prokaryotes. Trends Genet 28:314–322

    Article  CAS  PubMed  Google Scholar 

  • O’Donoghue EJ, Krachler AM (2016) Mechanisms of outer membrane vesicle entry into host cells. Cell Microbiol 18:1508–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olier M, Marcq I, Salvador-Cartier C, Secher T, Dobrindt U, Boury M, Bacquie V, Penary M, Gaultier E, Nougayrede JP, Fioramonti J, Oswald E (2012) Genotoxicity of Escherichia coli Nissle 1917 strain cannot be dissociated from its probiotic activity. Gut Microbes 3:501–509

    Article  PubMed  PubMed Central  Google Scholar 

  • Olivier V, Haines GK 3rd, Tan Y, Satchell KJ (2007) Hemolysin and the multifunctional autoprocessing RTX toxin are virulence factors during intestinal infection of mice with Vibrio cholerae El Tor O1 strains. Infect Immun 75:5035–5042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olofsson A, Nygard Skalman L, Obi I, Lundmark R, Arnqvist A (2014) Uptake of Helicobacter pylori vesicles is facilitated by clathrin-dependent and clathrin-independent endocytic pathways. MBio 5:e00979–e00914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen I, Amano A (2015) Outer membrane vesicles - offensive weapons or good Samaritans? J Oral Microbiol 7:27468

    Article  CAS  PubMed  Google Scholar 

  • Pathirana RD, Kaparakis-Liaskos M (2016) Bacterial membrane vesicles: biogenesis, immune regulation and pathogenesis. Cell Microbiol 18:1518–1524

    Article  CAS  PubMed  Google Scholar 

  • Patrick S, McKenna JP, O'Hagan S, Dermott E (1996) A comparison of the haemagglutinating and enzymic activities of Bacteroides fragilis whole cells and outer membrane vesicles. Microb Pathog 20:191–202

    Article  CAS  PubMed  Google Scholar 

  • Perez-Cruz C, Delgado L, Lopez-Iglesias C, Mercade E (2015) Outer-inner membrane vesicles naturally secreted by gram-negative pathogenic bacteria. PLoS One 10:e0116896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pollak CN, Delpino MV, Fossati CA, Baldi PC (2012) Outer membrane vesicles from Brucella abortus promote bacterial internalization by human monocytes and modulate their innate immune response. PLoS One 7:e50214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prados-Rosales R, Baena A, Martinez LR, Luque-Garcia J, Kalscheuer R, Veeraraghavan U, Camara C, Nosanchuk JD, Besra GS, Chen B, Jimenez J, Glatman-Freedman A, Jacobs WR Jr, Porcelli SA, Casadevall A (2011) Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest 121:1471–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raeven RH, Brummelman J, Pennings JL, van der Maas L, Tilstra W, Helm K, van Riet E, Jiskoot W, van Els CA, Han WG, Kersten GF, Metz B (2016) Bordetella pertussis outer membrane vesicle vaccine confers equal efficacy in mice with milder inflammatory responses compared to a whole-cell vaccine. Sci Rep 6:38240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasti ES, Schappert ML, Brown AC (2018) Association of Vibrio cholerae 569B outer membrane vesicles with host cells occurs in a GM1-independent manner. Cell Microbiol 20:e12828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rath P, Huang C, Wang T, Wang T, Li H, Prados-Rosales R, Elemento O, Casadevall A, Nathan CF (2013) Genetic regulation of vesiculogenesis and immunomodulation in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 110:E4790–E4797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renelli M, Matias V, Lo RY, Beveridge TJ (2004) DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 150:2161–2169

    Article  CAS  PubMed  Google Scholar 

  • Resch U, Tsatsaronis JA, Le Rhun A, Stubiger G, Rohde M, Kasvandik S, Holzmeister S, Tinnefeld P, Wai SN, Charpentier E (2016) A two-component regulatory system impacts extracellular membrane-derived vesicle production in group A Streptococcus. MBio 7:e00207–e00216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riley DR, Sieber KB, Robinson KM, White JR, Ganesan A, Nourbakhsh S, Dunning Hotopp JC (2013) Bacteria-human somatic cell lateral gene transfer is enriched in cancer samples. PLoS Comput Biol 9:e1003107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivera J, Cordero RJ, Nakouzi AS, Frases S, Nicola A, Casadevall A (2010) Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc Natl Acad Sci U S A 107:19002–19007

    Article  PubMed  PubMed Central  Google Scholar 

  • Rompikuntal PK, Thay B, Khan MK, Alanko J, Penttinen AM, Asikainen S, Wai SN, Oscarsson J (2012) Perinuclear localization of internalized outer membrane vesicles carrying active cytolethal distending toxin from Aggregatibacter actinomycetemcomitans. Infect Immun 80:31–42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rompikuntal PK, Vdovikova S, Duperthuy M, Johnson TL, Ahlund M, Lundmark R, Oscarsson J, Sandkvist M, Uhlin BE, Wai SN (2015) Outer membrane vesicle-mediated export of processed PrtV protease from Vibrio cholerae. PLoS One 10:e0134098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rumbo C, Fernandez-Moreira E, Merino M, Poza M, Mendez JA, Soares NC, Mosquera A, Chaves F, Bou G (2011) Horizontal transfer of the OXA-24 carbapenemase gene via outer membrane vesicles: a new mechanism of dissemination of carbapenem resistance genes in Acinetobacter baumannii. Antimicrob Agents Chemother 55:3084–3090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaar V, de Vries SP, Perez Vidakovics ML, Bootsma HJ, Larsson L, Hermans PW, Bjartell A, Morgelin M, Riesbeck K (2011) Multicomponent Moraxella catarrhalis outer membrane vesicles induce an inflammatory response and are internalized by human epithelial cells. Cell Microbiol 13:432–449

    Article  CAS  PubMed  Google Scholar 

  • Sharpe SW, Kuehn MJ, Mason KM (2011) Elicitation of epithelial cell-derived immune effectors by outer membrane vesicles of nontypeable Haemophilus influenzae. Infect Immun 79:4361–4369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Y, Giardino Torchia ML, Lawson GW, Karp CL, Ashwell JD, Mazmanian SK (2012) Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12:509–520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh U, Grenier D, McBride BC (1989) Bacteroides gingivalis vesicles mediate attachment of streptococci to serum-coated hydroxyapatite. Oral Microbiol Immunol 4:199–203

    Article  CAS  PubMed  Google Scholar 

  • Sjostrom AE, Sandblad L, Uhlin BE, Wai SN (2015) Membrane vesicle-mediated release of bacterial RNA. Sci Rep 5:15329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smalley JW, Birss AJ, McKee AS, Marsh PD (1991) Haemin-restriction influences haemin-binding, haemagglutination and protease activity of cells and extracellular membrane vesicles of Porphyromonas gingivalis W50. FEMS Microbiol Lett 69:63–67

    Article  CAS  PubMed  Google Scholar 

  • Svennerholm K, Park KS, Wikstrom J, Lasser C, Crescitelli R, Shelke GV, Jang SC, Suzuki S, Bandeira E, Olofsson CS, Lotvall J (2017) Escherichia coli outer membrane vesicles can contribute to sepsis induced cardiac dysfunction. Sci Rep 7:17434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Syngkon A, Elluri S, Koley H, Rompikuntal PK, Saha DR, Chakrabarti MK, Bhadra RK, Wai SN, Pal A (2010) Studies on a novel serine protease of a DeltahapADeltaprtV Vibrio cholerae O1 strain and its role in hemorrhagic response in the rabbit ileal loop model. PLoS One 5:e13122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taheri N, Mahmud A, Sandblad L, Fallman M, Wai SN, Fahlgren A (2018) Campylobacter jejuni bile exposure influences outer membrane vesicles protein content and bacterial interaction with epithelial cells. Sci Rep 8:16996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tashiro Y, Ichikawa S, Shimizu M, Toyofuku M, Takaya N, Nakajima-Kambe T, Uchiyama H, Nomura N (2010) Variation of physiochemical properties and cell association activity of membrane vesicles with growth phase in Pseudomonas aeruginosa. Appl Environ Microbiol 76:3732–3739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tashiro Y, Inagaki A, Shimizu M, Ichikawa S, Takaya N, Nakajima-Kambe T, Uchiyama H, Nomura N (2011) Characterization of phospholipids in membrane vesicles derived from Pseudomonas aeruginosa. Biosci Biotechnol Biochem 75:605–607

    Article  CAS  PubMed  Google Scholar 

  • Tashiro Y, Hasegawa Y, Shintani M, Takaki K, Ohkuma M, Kimbara K, Futamata H (2017) Interaction of bacterial membrane vesicles with specific species and their potential for delivery to target cells. Front Microbiol 8:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Thay B, Wai SN, Oscarsson J (2013) Staphylococcus aureus alpha-toxin-dependent induction of host cell death by membrane-derived vesicles. PLoS One 8:e54661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thay B, Damm A, Kufer TA, Wai SN, Oscarsson J (2014) Aggregatibacter actinomycetemcomitans outer membrane vesicles are internalized in human host cells and trigger NOD1- and NOD2-dependent NF-kappaB activation. Infect Immun 82:4034–4046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turnbull L, Toyofuku M, Hynen AL, Kurosawa M, Pessi G, Petty NK, Osvath SR, Carcamo-Oyarce G, Gloag ES, Shimoni R, Omasits U, Ito S, Yap X, Monahan LG, Cavaliere R, Ahrens CH, Charles IG, Nomura N, Eberl L, Whitchurch CB (2016) Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat Commun 7:11220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner L, Bitto NJ, Steer DL, Lo C, D'Costa K, Ramm G, Shambrook M, Hill AF, Ferrero RL, Kaparakis-Liaskos M (2018) Helicobacter pylori outer membrane vesicle size determines their mechanisms of host cell entry and protein content. Front Immunol 9:1466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyrer PC, Frizelle FA, Keenan JI (2014) Escherichia coli-derived outer membrane vesicles are genotoxic to human enterocyte-like cells. Infect Agent Cancer 9:2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaitkevicius K, Lindmark B, Ou G, Song T, Toma C, Iwanaga M, Zhu J, Andersson A, Hammarstrom ML, Tuck S, Wai SN (2006) A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing. Proc Natl Acad Sci U S A 103:9280–9285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659

    Article  CAS  PubMed  Google Scholar 

  • Vanaja SK, Russo AJ, Behl B, Banerjee I, Yankova M, Deshmukh SD, Rathinam VAK (2016) Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation. Cell 165:1106–1119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vdovikova S, Luhr M, Szalai P, Nygard Skalman L, Francis MK, Lundmark R, Engedal N, Johansson J, Wai SN (2017) A novel role of Listeria monocytogenes membrane vesicles in inhibition of autophagy and cell death. Front Cell Infect Microbiol 7:154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vdovikova S, Gilfillan S, Wang S, Dongre M, Wai SN, Hurtado A (2018) Modulation of gene transcription and epigenetics of colon carcinoma cells by bacterial membrane vesicles. Sci Rep 8:7434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veith PD, Chen YY, Gorasia DG, Chen D, Glew MD, O’Brien-Simpson NM, Cecil JD, Holden JA, Reynolds EC (2014) Porphyromonas gingivalis outer membrane vesicles exclusively contain outer membrane and periplasmic proteins and carry a cargo enriched with virulence factors. J Proteome Res 13:2420–2432

    Article  CAS  PubMed  Google Scholar 

  • Vidakovics ML, Jendholm J, Morgelin M, Mansson A, Larsson C, Cardell LO, Riesbeck K (2010) B cell activation by outer membrane vesicles-a novel virulence mechanism. PLoS Pathog 6:e1000724

    Article  CAS  PubMed  Google Scholar 

  • Wagner T, Joshi B, Janice J, Askarian F, Skalko-Basnet N, Hagestad OC, Mekhlif A, Wai SN, Hegstad K, Johannessen M (2018) Enterococcus faecium produces membrane vesicles containing virulence factors and antimicrobial resistance related proteins. J Proteome 187:28–38

    Article  CAS  Google Scholar 

  • Wai SN, Lindmark B, Soderblom T, Takade A, Westermark M, Oscarsson J, Jass J, Richter-Dahlfors A, Mizunoe Y, Uhlin BE (2003) Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115:25–35

    Article  CAS  PubMed  Google Scholar 

  • **e H (2015) Biogenesis and function of Porphyromonas gingivalis outer membrane vesicles. Future Microbiol 10:1517–1527

    Article  CAS  PubMed  Google Scholar 

  • Yaron S, Kolling GL, Simon L, Matthews KR (2000) Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl Environ Microbiol 66:4414–4420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Ju J, Rigney T, Tribble GD (2011) Fimbriae of Porphyromonas gingivalis are important for initial invasion of osteoblasts, but not for inhibition of their differentiation and mineralization. J Periodontol 82:909–916

    Article  CAS  PubMed  Google Scholar 

  • Zhong H, Yang Y, Ma S, **u F, Cai Z, Zhao H, Du L (2011) Induction of a tumour-specific CTL response by exosomes isolated from heat-treated malignant ascites of gastric cancer patients. Int J Hyperth 27:604–611

    Article  CAS  Google Scholar 

  • Zomer A, Vendrig T, Hopmans ES, van Eijndhoven M, Middeldorp JM, Pegtel DM (2010) Exosomes: fit to deliver small RNA. Commun Integr Biol 3:447–450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Biology, Umeå University, Umeå, Sweden

    Aftab Nadeem & Sun Nyunt Wai

  2. The Umeå Centre for Microbial Research (UCMR), Umeå University, Umeå, Sweden

    Aftab Nadeem & Sun Nyunt Wai

  3. Oral Microbiology, Department of Odontology, Umeå University, Umeå, Sweden

    Jan Oscarsson

Authors
  1. Aftab Nadeem
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jan Oscarsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sun Nyunt Wai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sun Nyunt Wai .

Editor information

Editors and Affiliations

  1. Department of Physiology, Anatomy and Microbiology, La Trobe University, Melbourne, VIC, Australia

    Maria Kaparakis-Liaskos

  2. Department of Immunology, Institute of Nutritional Medicine, University of Hohenheim, Stuttgart, Baden-Württemberg, Germany

    Thomas A. Kufer

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Nadeem, A., Oscarsson, J., Wai, S.N. (2020). Delivery of Virulence Factors by Bacterial Membrane Vesicles to Mammalian Host Cells. In: Kaparakis-Liaskos, M., Kufer, T. (eds) Bacterial Membrane Vesicles. Springer, Cham. https://doi.org/10.1007/978-3-030-36331-4_7

Download citation

Publish with us

Policies and ethics

Search

Navigation