Abstract

Extracellular vesicles constitute a heterogeneous group of nanoparticles, released by both prokaryotic and eukaryotic cells, which perform various biological functions and participate in cell-cell communication. Bacterial extracellular vesicles are made of lipids, proteins and nucleic acids. There are a number of hypotheses for the formation of extracellular vesicles, but the mechanisms of biogenesis of these structures remain unclear. Hardly soluble metabolites or signaling molecules, DNA and RNA are vesicles cargo. Extracellular vesicles have a protective function, they can eliminate other bacterial cells and participate in horizontal gene transfer. The enzymes contained inside the vesicles facilitate the acquisition of nutrients and help colonize various ecological niches. Signal molecules carried in the vesicles enable biofilm formation. In the secreted extracellular vesicles pathogenic microorganisms carry virulence factors, including toxins, into the host cells. Via vesicles, bacteria can also modulate the host immune system. Bacterial extracellular vesicles are promising vaccine candidates and can be used as drug carriers. The review discusses the current knowledge concerning biogenesis, composition, preparation methods, physiological functions and potential applications of extracellular vesicles secreted by prokaryotic cells.

References

• 1. Agrawal A., Ramachandran R.: Exploring the links between lipidgeometry and mitochondrial fission: Emerging concepts. Mitochondrion,2019; 49: 305–313
  Google Scholar
• 2. Ahmadi Badi S., Bruno S.P., Moshiri A., Tarashi S., Siadat S.D.,Masotti A.: Small RNAs in outer membrane vesicles and their functionin host-microbe interactions. Front. Microbiol., 2020; 11: 1209
  Google Scholar
• 3. Alaniz R.C., Deatherage B.L., Lara J.C., Cookson B.T.: Membranevesicles are immunogenic facsimiles of Salmonella typhimuriumthat potently activate dendritic cells, prime B and T cell responses,and stimulate protective immunity in vivo. J. Immunol., 2007;179: 7692–7701
  Google Scholar
• 4. Allesen-Holm M., Barken K.B., Yang L., Klausen M., Webb J.S.,Kjelleberg S., Molin S., Givskov M., Tolker-Nielsen T.: A characterizationof DNA release in Pseudomonas aeruginosa cultures andbiofilms. Mol. Microbiol., 2006; 59: 1114–1128
  Google Scholar
• 5. Alvarez C.S., Badia J., Bosch M., Giménez R., Baldomà L.: Outermembrane vesicles and soluble factors released by probiotic Escherichiacoli Nissle 1917 and commensal ECOR63 enhance barrierfunction by regulating expression of tight junction proteins in intestinalepithelial cells. Front. Microbiol., 2016; 7: 1981
  Google Scholar
• 6. Alves N.J., Turner K.B., Daniele M.A., Oh E., Medintz I.L., WalperS.A.: Bacterial nanobioreactors-directing enzyme packaging intobacterial outer membrane vesicles. ACS Appl. Mater. Interfaces,2015; 7: 24963–24972
  Google Scholar
• 7. Alves N.J., Turner K.B., DiVito K.A., Daniele M.A., Walper S.A.:Affinity purification of bacterial outer membrane vesicles (OMVs)utilizing a His-tag mutant. Res. Microbiol., 2017; 168: 139–146
  Google Scholar
• 8. Alves N.J., Turner K.B., Medintz I.L., Walper S.A.: Protecting enzymaticfunction through directed packaging into bacterial outermembrane vesicles. Sci. Rep., 2016; 6: 24866
  Google Scholar
• 9. Araiza-Villanueva M., Avila-Calderón E.D., Flores-Romo L.,Calderón-Amador J., Sriranganathan N., Qublan H.A., Witonsky S.,Aguilera-Arreola M.G., Ruiz-Palma M.D., Ruiz E.A., Suárez-GüemesF., Gómez-Lunar Z., Contreras-Rodríguez A.: Proteomic analysis ofmembrane blebs of Brucella abortus 2308 and RB51 and their evaluationas an acellular vaccine. Front. Microbiol., 2019; 10: 2714
  Google Scholar
• 10. Behzadi E., Mahmoodzadeh Hosseini H., Imani Fooladi A.A.:The inhibitory impacts of Lactobacillus rhamnosus GG-derived extracellularvesicles on the growth of hepatic cancer cells. Microb.Pathog., 2017; 110: 1–6
  Google Scholar
• 11. Berleman J.E., Allen S., Danielewicz M.A., Remis J.P., Gorur A.,Cunha J., Hadi M.Z., Zusman D.R., Northen T.R., Witkowska H.E., AuerM.: The lethal cargo of Myxococcus xanthus outer membrane vesicles.Front. Microbiol., 2014; 5: 474
  Google Scholar
• 12. Bitto N.J., Chapman R., Pidot S., Costin A., Lo C., Choi J., D’CruzeT., Reynolds E.C., Dashper S.G., Turnbull L., Whitchurch C.B., StinearT.P., Stacey K.J., Ferrero R.L.: Bacterial membrane vesicles transporttheir DNA cargo into host cells. Sci. Rep., 2017; 7: 7072
  Google Scholar
• 13. Bonnington K.E., Kuehn M.J.: Protein selection and export viaouter membrane vesicles. Biochim. Biophys. Acta, 2014; 1843: 1612–1619
  Google Scholar
• 14. Brown L., Wolf J.M., Prados-Rosales R., Casadevall A.: Throughthe wall: Extracellular vesicles in Gram-positive bacteria, mycobacteriaand fungi. Nat. Rev. Microbiol., 2015; 13: 620–630
  Google Scholar
• 15. Caruana J.C., Walper S.A.: Bacterial membrane vesicles as mediatorsof microbe – microbe and microbe – host community interactions.Front. Microbiol., 2020; 11: 432
  Google Scholar
• 16. Chatterjee S.N., Das J.: Electron microscopic observations onthe excretion of cell-wall material by Vibrio cholerae. J. Gen. Microbiol.,1967; 49: 1–11
  Google Scholar
• 17. Chatterjee S., Mondal A., Mitra S., Basu S.: Acinetobacter baumanniitransfers the blaNDM-1 gene via outer membrane vesicles.J. Antimicrob. Chemother., 2017; 72: 2201–2207
  Google Scholar
• 18. Choi E.J., Lee H.G., Bae I.H., Kim W., Park J., Lee T.R., Cho E.G.:Propionibacterium acnes-derived extracellular vesicles promote acne-like phenotypes in human epidermis. J. Invest. Dermatol. 2018;138: 1371–1379
  Google Scholar
• 19. Chutkan H., Kuehn M.J.: Context-dependent activation kineticselicited by soluble versus outer membrane vesicle-associated heatlabileenterotoxin. Infect. Immun., 2011; 79: 3760–3769
  Google Scholar
• 20. Clarke A.J.: The “hole” story of predatory outer-membrane vesicles.Can. J. Microbiol., 2018; 64: 589–599
  Google Scholar
• 21. Daffé M.: The cell envelope of tubercle bacilli. Tuberculosis,2015; 95: S155–S158
  Google Scholar
• 22. Daniele L., Sapino A.: Anti-HER2 treatment and breast cancer:State of the art, recent patents, and new strategies. Recent Pat. AnticancerDrug Discov., 2009; 4: 9–18
  Google Scholar
• 23. Dauros-Singorenko P., Blenkiron C., Phillips A., Swift S.: Thefunctional RNA cargo of bacterial membrane vesicles. FEMS Microbiol.Lett., 2018; 365: fny023
  Google Scholar
• 24. Dean S.N., Rimmer M.A., Turner K.B., Phillips D.A., CaruanaJ.C., Hervey W.J.4th, Leary D.H., Walper S.A.: Lactobacillus acidophilusmembrane vesicles as a vehicle of bacteriocin delivery. Front.Microbiol., 2020; 11: 710
  Google Scholar
• 25. Devos S., Van Putte W., Vitse J., Van Driessche G., StremerschS., Van Den Broek W., Raemdonck K., Braeckmans K., StahlbergH., Kudryashev M., Savvides S.N., Devreese B.: Membranevesicle secretion and prophage induction in multidrug-resistantStenotrophomonas maltophilia in response to ciprofloxacin stress. Environ.Microbiol., 2017; 19: 3930–3937
  Google Scholar
• 26. Elhenawy W., Debelyy M.O., Feldman M.F.: Preferential packingof acidic glycosidases and proteases into Bacteroides outer membranevesicles. mBio, 2014; 5: e00909–14
  Google Scholar
• 27. Ellis T.N., Leiman S.A., Kuehn M.J.: Naturally produced outermembrane vesicles from Pseudomonas aeruginosa elicit a potentinnate immune response via combined sensing of both lipopolysaccharideand protein components. Infect. Immun., 2010; 78:3822–3831
  Google Scholar
• 28. Elmi A., Watson E., Sandu P., Gundogdu O., Mills D.C., InglisN.F., Manson E., Imrie L., Bajaj-Elliott M., Wren B.W., Smith D.G.,Dorrell N.: Campylobacter jejuni outer membrane vesicles play animportant role in bacterial interactions with human intestinalepithelial cells. Infect. Immun., 2012; 80: 4089–4098
  Google Scholar
• 29. Flemming H.C., Wingender J., Szewzyk U., Steinberg P., RiceS.A., Kjelleberg S.: Biofilms: An emergent form of bacterial life.Nat. Rev. Microbiol., 2016; 14: 563–575
  Google Scholar
• 30. Gao W., Fang R.H., Thamphiwatana S., Luk B.T., Li J., AngsantikulP., Zhang Q., Hu C.M., Zhang L.: Modulating antibacterialimmunity via bacterial membrane-coated nanoparticles. NanoLett., 2015; 15: 1403–1409
  Google Scholar
• 31. Gatkowska J., Długońska H.: Rola zewnątrzkomórkowychpęcherzyków błonowych w interakcji pasożyt-żywiciel. PostępyHig. Med. Dośw., 2016; 70: 951–958
  Google Scholar
• 32. Gołoś A., Lutyńska A.: Adiuwanty glinowe w szczepionkach –aktualny stan wiedzy. Przegl. Epidemiol., 2015; 69: 871–874
  Google Scholar
• 33. Grande R., Celia C., Mincione G., Stringaro A., Di Marzio L.,Colone M., Di Marcantonio M.C., Savino L., Puca V., SantoliquidoR., Locatelli M., Muraro R., Hall-Stoodley L., Stoodley P.: Detectionand physicochemical characterization of membrane vesicles (MVs)of Lactobacillus reuteri DSM 17938. Front. Microbiol., 2017; 8: 1040
  Google Scholar
• 34. Gujrati V., Kim S., Kim S.H., Min J.J., Choy H.E., Kim S.C., JonS.: Bioengineered bacterial outer membrane vesicles as cell-specificdrug-delivery vehicles for cancer therapy. ACS Nano, 2014;8: 1525–1537
  Google Scholar
• 35. Gupta S., Rodriguez G.M.: Mycobacterial extracellular vesiclesand host pathogen interactions. Pathog. Dis., 2018; 76: fty031
  Google Scholar
• 36. Hashimoto M., Matsumoto T., Tamura-Nakano M., Ozono M.,Hashiguchi S., Suda Y.: Characterization of outer membrane vesiclesof Acetobacter pasteurianus NBRC3283. J. Biosci. Bioeng., 2018;125: 425–431
  Google Scholar
• 37. Haurat M.F., Aduse-Opoku J., Rangarajan M., Dorobantu L.,Gray M.R., Curtis M.A., Feldman M.F.: Selective sorting of cargoproteins into bacterial membrane vesicles. J. Biol. Chem., 2011;286: 1269–1276
  Google Scholar
• 38. Haurat M.F., Elhenawy W., Feldman M.F.: Prokaryotic membranevesicles: New insights on biogenesis and biological roles.Biol. Chem., 2015; 396: 95–109
  Google Scholar
• 39. Hoekstra D., van der Laan J.W., de Leij L., Witholt B.: Releaseof outer membrane fragments from normally growing Escherichiacoli. Biochim. Biophys. Acta, 1976; 455: 889–899
  Google Scholar
• 40. Holst J., Oster P., Arnold R., Tatley M.V., Næss L.M., AabergeI.S., Galloway Y., McNicholas A., O’Hallahan J., Rosenqvist E., BlackS.: Vaccines against meningococcal serogroup B disease containing outer membrane vesicles (OMV): Lessons from past programsand implications for the future. Hum. Vaccin. Immunother, 2013;9: 1241–1253
  Google Scholar
• 41. Horstman A.L., Bauman S.J., Kuehn M.J.: Lipopolysaccharide3-deoxy-D-manno-octulosonic acid (Kdo) core determinesbacterial association of secreted toxins. J. Biol. Chem., 2004; 279:8070–8075
  Google Scholar
• 42. Jäger J., Marwitz S., Tiefenau J., Rasch J., Shevchuk O., KuglerC., Goldmann T., Steinert M.: Human lung tissue explants revealnovel interactions during Legionella pneumophila infections. Infect.Immun., 2013; 82: 275–285
  Google Scholar
• 43. Jeon J., Park S.C., Her J., Lee J.W., Han J.K., Kim Y.K., Kim K.P.,Ban C.: Comparative lipidomic profiling of the human commensalbacterium Propionibacterium acnes and its extracellular vesicles.RSC Adv., 2018; 8: 15241–15247
  Google Scholar
• 44. Jiang Y., Kong Q., Roland K.L., Curtiss R.3rd: Membrane vesiclesof Clostridium perfringens type A strains induce innate and adaptiveimmunity. Int. J. Med. Microbiol., 2014; 304: 431–443
  Google Scholar
• 45. Kadurugamuwa J.L., Beveridge T.J.: Virulence factors are releasedfrom Pseudomonas aeruginosa in association with membranevesicles during normal growth and exposure to gentamicin:A novel mechanism of enzyme secretion. J. Bacteriol., 1995; 177:3998–4008
  Google Scholar
• 46. Kadurugamuwa J.L., Beveridge T.J.: Bacteriolytic effect of membranevesicles from Pseudomonas aeruginosa on other bacteriaincluding pathogens: conceptually new antibiotics. J. Bacteriol.,1996; 178: 2767–2774
  Google Scholar
• 47. Kadurugamuwa J.L., Mayer A., Messner P., Sára M., Sleytr U.B.,Beveridge T.J.: S-layered Aneurinibacillus and Bacillus spp. are susceptibleto the lytic action of Pseudomonas aeruginosa membranevesicles. J. Bacteriol., 1998; 180: 2306–2311
  Google Scholar
• 48. Kamaguchi A., Nakayama K., Ichiyama S., Nakamura R., WatanabeT., Ohta M., Baba H., Ohyama T.: Effect of Porphyromonasgingivalis vesicles on coaggregation of Staphylococcus aureus to oralmicroorganisms. Curr. Microbiol., 2003; 47: 485–491
  Google Scholar
• 49. Kesty N.C., Kuehn M.J.: Incorporation of heterologous outermembrane and periplasmic proteins into Escherichia coli outermembrane vesicles. J. Biol. Chem., 2004; 279: 2069–2076
  Google Scholar
• 50. Kim J.H., Jeun E.J., Hong C.P., Kim S.H., Jang M.S., Lee E.J., MoonS.J., Yun C.H., Im S.H., Jeong S.G., Park B.Y., Kim K.T., Seoh J.Y., KimY.K., Oh S.J., i wsp.: Extracellular vesicle–derived protein from Bifidobacteriumlongum alleviates food allergy through mast cell suppression.J. Allergy Clin. Immunol., 2016; 137: 507–516
  Google Scholar
• 51. Kim J.H., Yoon Y.J., Lee J., Choi E.J., Yi N., Park K.S., Park J., LötvallJ., Kim Y.K., Gho Y.S.: Outer membrane vesicles derived fromEscherichia coli up-regulate expression of endothelial cell adhesionmolecules in vitro and in vivo. PLoS One, 2013; 8: e59276
  Google Scholar
• 52. Kim O.Y., Hong B.S., Park K.S., Yoon Y.J., Choi S.J., Lee W.H., RohT.Y., Lötvall J., Kim Y.K., Gho Y.S.: Immunization with Escherichiacoli outer membrane vesicles protects bacteria induced lethalityvia Th1 and Th17 cell responses. J. Immunol., 2013; 190: 4092–4102
  Google Scholar
• 53. Kim O.Y., Park H.T., Dinh N.T.H., Choi S.J., Lee J., Kim J.H.,Lee S.W., Gho Y.S.: Bacterial outer membrane vesicles suppresstumor by interferon-γ-mediated antitumor response. Nat. Commun.,2017; 8: 626
  Google Scholar
• 54. Knox K.W., Vesk M., Work E.: Relation between excreted lipopolysaccharidecomplexes and surface structures of a lysinelimitedculture of Escherichia coli. J. Bacteriol., 1966; 92: 1206–1217
  Google Scholar
• 55. Ko S.H., Jeon J.I., Kim Y.J., Yoon H.J., Kim H., Kim N., Kim J.S.,Kim J.M.: Helicobacter pylori outer membrane vesicle proteinsinduce human eosinophil degranulation via a β2 integrin CD11/CD18- and ICAM-1-dependent mechanism. Mediators Inflammation,2015; 2015: 301716
  Google Scholar
• 56. Kulkarni H.M., Jagannadham M.V.: Biogenesis and multifacetedroles of outer membrane vesicles from Gram-negative bacteria.Microbiology, 2014; 160: 2109–2121
  Google Scholar
• 57. Kulkarni H.M., Swamy C.V., Jagannadham M.V.: Molecular characterizationand functional analysis of outer membrane vesiclesfrom the antarctic bacterium Pseudomonas syringae suggest apossible response to environmental conditions. J. Proteome Res.,2014; 13: 1345–1358
  Google Scholar
• 58. Kulp A., Kuehn M.J.: Biological functions and biogenesis of secretedbacterial outer membrane vesicles. Annu. Rev. Microbiol.,2010; 64: 163–184
  Google Scholar
• 59. Kurthkoti K., Amin H., Marakalala M.J., Ghanny S., Subbian S.,Sakatos A., Livny J., Fortune S.M., Berney M., Rodriguez G.M.: Thecapacity of Mycobacterium tuberculosis to survive iron starvationmight enable it to persist in iron-deprived microenvironments ofhuman granulomas. mBio, 2017; 8: e01092–17
  Google Scholar
• 60. Langlete P., Krabberød A.K., Winther-Larsen H.C.: Vesiclesfrom Vibrio cholerae contain AT-Rich DNA and shorter mRNAs thatdo not correlate with their protein products. Front. Microbiol.,2019; 10: 2708
  Google Scholar
• 61. Lapinet J.A., Scapini P., Calzetti F., Pérez O., Cassatella M.A.:Gene expression and production of tumor necrosis factor alpha,interleukin-1β (IL-1β), IL-8, macrophage inflammatory protein 1α(MIP-1α), MIP-1β, and gamma interferon-inducible protein 10 byhuman neutrophils stimulated with group B meningococcal outermembrane vesicles. Infect. Immun., 2000; 68: 6917–6923
  Google Scholar
• 62. Lee E.Y., Choi D.Y., Kim D.K., Kim J.W., Park J.O., Kim S., KimS.H., Desiderio D.M., Kim Y.K., Kim K.P., Gho Y.S.: Gram-positivebacteria produce membrane vesicles: Proteomics-based characterizationof Staphylococcus aureus-derived membrane vesicles.Proteomics, 2009; 9: 5425–5436
  Google Scholar
• 63. Lee J.H., Choi C.W., Lee T., Kim S.I., Lee J.C., Shin J.H.: Transcriptionfactor σB plays an important role in the production of extracellularmembrane-derived vesicles in Listeria monocytogenes.PLoS One, 2013; 8: e73196
  Google Scholar
• 64. Lekmeechai S., Su Y.C., Brant M., Alvarado-Kristensson M., VallströmA., Obi I., Arnqvist A., Riesbeck K.: Helicobacter pylori outermembrane vesicles protect the pathogen from reactive oxygenspecies of the respiratory burst. Front. Microbiol., 2018; 9: 1837
  Google Scholar
• 65. Li M., Zhou H., Yang C., Wu Y., Zhou X., Liu H., Wang Y.: Bacterialouter membrane vesicles as a platform for biomedical applications:An update. J. Controlled Release, 2020; 323: 253–268
  Google Scholar
• 66. Li Z., Clarke A.J., Beveridge T.J.: A major autolysin of Pseudomonasaeruginosa: Subcellular distribution, potential role in cellgrowth and division and secretion in surface membrane vesicles.J. Bacteriol., 1996; 178: 2479–2488
  Google Scholar
• 67. Li Z., Clarke A.J., Beveridge T.J.: Gram-negative bacteria producemembrane vesicles which are capable of killing other bacteria.J. Bacteriol., 1998; 180: 5478–5483
  Google Scholar
• 68. Liao S., Klein M.I., Heim K.P., Fan Y., Bitoun J.P., Ahn S.J., BurneR.A., Koo H., Brady L.J., Wen Z.T.: Streptococcus mutans extracellularDNA is upregulated during growth in biofilms, actively released viamembrane vesicles, and influenced by components of the proteinsecretion machinery. J. Bacteriol., 2014; 196: 2355-2366
  Google Scholar
• 69. Liao Y.T., Kuo S.C., Chiang M.H., Lee Y.T., Sung W.C., Chen Y.H.,Chen T.L., Fung C.P.: Acinetobacter baumannii extracellular OXA-58is primarily and selectively released via outer membrane vesiclesafter sec-dependent periplasmic translocation. Antimicrob. AgentsChemother., 2015; 59: 7346–7354
  Google Scholar
• 70. López P., González-Rodríguez I., Sánchez B., Gueimonde M.,Margolles A., Suárez A.: Treg-inducing membrane vesicles fromBifidobacterium bifidum LMG13195 as potential adjuvants in immunotherapy.Vaccine, 2012; 30: 825–829
  Google Scholar
• 71. Mashburn L.M., Whiteley M.: Membrane vesicles traffic signalsand facilitate group activities in a prokaryote. Nature, 2005;437: 422–425
  Google Scholar
• 72. McBroom A.J., Johnson A.P., Vemulapalli S., Kuehn M.J.: Outermembrane vesicle production by Escherichia coli is independent ofmembrane instability. J. Bacteriol., 2006; 188: 5385–5392
  Google Scholar
• 73. Mergenhagen S.E., Bladen H.A., Hsu K.C.: Electron microscopiclocalization of endotoxic lipopolysaccharide in Gram-negativeorganisms. Ann. N. Y. Acad. Sci., 1966; 133: 279–291
  Google Scholar
• 74. Mug-Opstelten D., Witholt B.: Preferential release of newouter membrane fragments by exponentially growing Escherichiacoli. Biochim. Biophys. Acta, 1978; 508: 287–295
  Google Scholar
• 75. Nagakubo T., Nomura N., Toyofuku M.: Cracking open bacterialmembrane vesicles. Front. Microbiol., 2020; 10: 3026
  Google Scholar
• 76. Olaya-Abril A., Prados-Rosales R., McConnell M.J., Martín-Peña R., González-Reyes J.A., Jiménez-Munguía I., Gómez-GascónL., Fernández J., Luque-García J.L., García-Lidón C., Estévez H.,Pachón J., Obando I., Casadevall A., Pirofski L.A. i wsp.: Characterizationof protective extracellular membrane-derived vesicles producedby Streptococcus pneumoniae. J. Proteomics, 2014; 106: 46–60
  Google Scholar
• 77. Oliver C., Hernández M.A., Tandberg J.I., Valenzuela K.N.,Lagos L.X., Haro R.E., Sánchez P., Ruiz P.A., Sanhueza-OyarzúnC., Cortés M.A., Villar M.T., Artigues A., Winther-Larsen H.C.,Avendaño-Herrera R., Yáñez A.J.: The proteome of biologicallyactive membrane vesicles from Piscirickettsia salmonis LF-89 typestrain identifies plasmid-encoded putative toxins. Front. Cell.Infect. Microbiol., 2017; 7: 420
  Google Scholar
• 78. Orr N., Robin G., Cohen D., Arnon R., Lowell G.H.: Immunogenicityand efficacy of oral or intranasal Shigella flexneri 2a andShigella sonnei proteosome-lipopolysaccharide vaccines in animalmodels. Infect. Immun., 1993; 61: 2390–2395
  Google Scholar
• 79. Palsdottir H., Remis J.P., Schaudinn C., O’Toole E., Lux R., ShiW., McDonald K.L., Costerton J.W., Auer M.: Three-dimensionalmacromolecular organization of cryofixed Myxococcus xanthusbiofilms as revealed by electron microscopic tomography. J. Bacteriol.,2009; 191: 2077–2082
  Google Scholar
• 80. Parida S.K., Domann E., Rohde M., Müller S., Darji A., Hain T.,Wehland J., Chakraborty T.: Internalin B is essential for adhesionand mediates the invasion of Listeria monocytogenes into humanendothelial cells. Mol. Microbiol., 2002; 28: 81–93
  Google Scholar
• 81. Park J.S., Lee W.C., Yeo K.J., Ryu K.S., Kumarasiri M., HesekD., Lee M., Mobashery S., Song J.H., Kim S.I., Lee J.C., Cheong C.,Jeon Y.H., Kim H.Y.: Mechanism of anchoring of OmpA protein tothe cell wall peptidoglycan of the gram‐negative bacterial outermembrane. FASEB J., 2012; 26: 219–228
  Google Scholar
• 82. Pérez-Cruz C., Carrión O., Delgado L., Martinez G., López-Iglesias C., Mercade E.: New type of outer membrane vesicle producedby the Gram-negative bacterium Shewanella vesiculosa M7T:Implications for DNA content. Appl. Environ. Microbiol., 2013;79: 1874–1881
  Google Scholar
• 83. Prados-Rosales R., Baena A., Martinez L.R., Luque-GarciaJ., Kalscheuer R., Veeraraghavan U., Camara C., Nosanchuk J.D.,Besra G.S., Chen B., Jimenez J., Glatman-Freedman A., JacobsW.R.Jr., Porcelli S.A., Casadevall A.: Mycobacteria release activemembrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J. Clin. Invest., 2011; 121: 1471–1483
  Google Scholar
• 84. Prados-Rosales R., Weinrick B.C., Piqué D.G., Jacobs W.R. Jr.,Casadevall A., Rodriguez G.M.: Role for Mycobacterium tuberculosismembrane vesicles in iron acquisition. J. Bacteriol., 2014;196: 1250–1256
  Google Scholar
• 85. Pritsch M., Ben-Khaled N., Chaloupka M., Kobold S., Berens-Riha N., Peter A., Liegl G., Schubert S., Hoelscher M., Löscher T.,Wieser A.: Comparison of intranasal outer membrane vesicles withCholera toxin and injected MF59C.1 as adjuvants for malaria transmissionblocking antigens AnAPN1 and Pfs48/45. J. Immunol. Res.,2016; 2016: 3576028
  Google Scholar
• 86. Rakoff-Nahoum S., Coyne M.J., Comstock L.E.: An ecologicalnetwork of polysaccharide utilization among human intestinalsymbionts. Curr. Biol., 2014; 24: 40–49
  Google Scholar
• 87. Rao P.K., Rodriguez G.M., Smith I., Li Q.: Protein dynamicsin iron-starved Mycobacterium tuberculosis revealed by turnoverand abundance measurement using hybrid-linear ion trap-Fouriertransform mass spectrometry. Anal. Chem., 2008; 80: 6860–6869
  Google Scholar
• 88. Rath P., Huang C., Wang T., Wang T., Li H., Prados-RosalesR., Elemento O., Casadevall A., Nathan C.F.: Genetic regulation ofvesiculogenesis and immunomodulation in Mycobacterium tuberculosis.Proc. Natl. Acad. Sci. USA, 2013; 110: 4790–4797
  Google Scholar
• 89. Ratledge C., Patel P.V., Mundy J.: Iron transport in Mycobacteriumsmegmatis: The location of mycobactin by electron microscopy.J. Gen. Microbiol., 1982; 128: 1559–1565
  Google Scholar
• 90. Renelli M., Matias V., Lo R.Y., Beveridge T.J.: DNA-containingmembrane vesicles of Pseudomonas aeruginosa PAO1 andtheir genetic transformation potential. Microbiology, 2004; 150:2161–2169
  Google Scholar
• 91. Resch U., Tsatsaronis J.A., Le Rhun A., Stübiger G., Rohde M.,Kasvandik S., Holzmeister S., Tinnefeld P., Wai S.N., CharpentierE.: A two-component regulatory system impacts extracellularmembrane-derived vesicle production in group A Streptococcus.mBio, 2016; 7: e00207–16
  Google Scholar
• 92. Rivera J., Cordero R.J., Nakouzi A.S., Frases S., Nicola A., CasadevallA.: Bacillus anthracis produces membrane-derived vesiclescontaining biologically active toxins. Proc. Natl. Acad. Sci. USA,2010; 107: 19002–19007
  Google Scholar
• 93. Rodriguez G.M., Prados-Rosales R.: Functions and importanceof mycobacterial extracellular vesicles. Appl. Microbiol. Biotechnol.,2016; 100: 3887–3892
  Google Scholar
• 94. Rodriguez G.M., Smith I.: Mechanisms of iron regulation inmycobacteria: Role in physiology and virulence. Mol. Microbiol.,2003; 47: 1485–1494
  Google Scholar
• 95. Roier S., Zingl F.G., Cakar F., Durakovic S., Kohl P., EichmannT.O., Klug L., Gadermaier B., Weinzerl K., Prassl R., Lass A., DaumG., Reidl J., Feldman M.F., Schild S.: A novel mechanism for thebiogenesis of outer membrane vesicles in Gram-negative bacteria.Nat. Commun., 2016; 7: 10515
  Google Scholar
• 96. Rothfield L., Pearlman-Kothencz M.: Synthesis and assemblyof bacterial membrane components: A lipopolysaccharidephospholipid-protein complex excreted by living bacteria. J. Mol.Biol., 1969; 44: 477–492
  Google Scholar
• 97. Rumbo C., Fernández-Moreira E., Merino M., Poza M., MendezJ.A., Soares N.C., Mosquera A., Chaves F., Bou G.: Horizontaltransfer of the OXA-24 carbapenemase gene via outer membranevesicles: A new mechanism of dissemination of carbapenem resistancegenes in Acinetobacter baumannii. Antimicrob. AgentsChemother., 2011; 55: 3084–3090
  Google Scholar
• 98. Sander L.E., Davis M.J., Boekschoten M.V., Amsen D., DascherC.C., Ryffel B., Swanson J.A., Müller M., Blander J.M.: Detectionof prokaryotic mRNA signifies microbial viability and promotesimmunity. Nature, 2011; 474: 385–389
  Google Scholar
• 99. Schooling S.R., Beveridge T.J.: Membrane vesicles: An overlookedcomponent of the matrices of biofilms. J. Bacteriol., 2006;188: 5945–5957
  Google Scholar
• 100. Schrempf H., Koebsch I., Walter S., Engelhardt H., MeschkeH.: Extracellular Streptomyces vesicles: Amphorae for survival anddefence. Microb. Biotechnol., 2011; 4: 286–299
  Google Scholar
• 101. Seitz P., Pezeshgi Modarres H., Borgeaud S., Bulushev R.D.,Steinbock L.J., Radenovic A., Dal Peraro M., Blokesch M.: ComEAis essential for the transfer of external DNA into the periplasm innaturally transformable Vibrio cholerae cells. PLoS Genet., 2014;10: e1004066
  Google Scholar
• 102. Singh U., Grenier D., McBride B.C.: Bactemides gingivalis vesiclesmediate attachment of streptococci to serum‐coated hydroxyapatite.Oral Microbiol. Immunol., 1989; 4: 199–203
  Google Scholar
• 103. Smith S.G., Mahon V., Lambert M.A., Fagan R.P.: A molecularSwiss army knife: OmpA structure, function and expression. FEMSMicrobiol. Lett., 2007; 273: 1–11
  Google Scholar
• 104. Solanki K.S., Pal D., Kaur G., Kumar P., Sahoo M., ChaudhuriP.: Isolation and characterization of OMPs and OMVs of Brucellaabortus S19 and Brucella abortus S19Δper. J. Pure Appl. Microbiol.,2016; 10: 2121–2126
  Google Scholar
• 105. Tashiro Y., Inagaki A., Shimizu M., Ichikawa S., Takaya N.,Nakajima-Kambe T., Uchiyama H., Nomura N.: Characterizationof phospholipids in membrane vesicles derived from Pseudomonasaeruginosa. Biosci. Biotechnol. Biochem., 2011; 75: 605–607
  Google Scholar
• 106. Tashiro Y., Yawata Y., Toyofuku M., Uchiyama H., Nomura N.:Interspecies interaction between Pseudomonas aeruginosa and othermicroorganisms. Microbes Environ., 2013; 28: 13–24
  Google Scholar
• 107. Todorova D., Simoncini S., Lacroix R., Sabatier F., Dignat-George F.: Extracellular vesicles in angiogenesis. Circ. Res., 2017; 120: 1658–1673
  Google Scholar
• 108. Toyofuku M., Cárcamo-Oyarce G., Yamamoto T., Eisenstein F.,Hsiao C.C., Kurosawa M., Gademann K., Pilhofer M., Nomura N., EberlL.: Prophage-triggered membrane vesicle formation through peptidoglycandamage in Bacillus subtilis. Nat. Commun., 2017; 8: 481
  Google Scholar
• 109. Toyofuku M., Nomura N., Eberl L.: Types and origins of bacterialmembrane vesicles. Nat. Rev. Microbiol., 2019; 17: 13–24
  Google Scholar
• 110. Toyofuku M., Tashiro Y., Nomura N., Eberl L.: Functions ofMVs in Inter-Bacterial Communication. W: Bacterial MembraneVesicles. Biogenesis, Function and Applications, red.: M. Kaparakis-Liaskos, T.A. Kufer, Springer, Cham, Szwajcaria 2020, 101-117
  Google Scholar
• 111. Tsatsaronis J.A., Franch-Arroyo S., Resch U., Charpentier E.:Extracellular vesicle RNA: A universal mediator of microbial communication?Trends Microbiol., 2018; 26: 401-410
  Google Scholar
• 112. Tzipilevich E., Habusha M., Ben-Yehuda S.: Acquisition ofphage sensitivity by bacteria through exchange of phage receptors.Cell, 2017; 168: 186-199.e12
  Google Scholar
• 113. Valguarnera E., Scott N.E., Azimzadeh P., Feldman M.F.: Surfaceexposure and packing of lipoproteins into outer membranevesicles are coupled processes in Bacteroides. mSphere, 2018; 3:e00559-18
  Google Scholar
• 114. Vallejo M.C., Nakayasu E.S., Longo L.V.G., Ganiko L., Lopes F.G.,Matsuo A.L., Almeida I.C., Puccia R.: Correction: Lipidomic analysisof extracellular vesicles from the pathogenic phase of Paracoccidioidesbrasiliensis. PLoS One, 2012; 7: e39463
  Google Scholar
• 115. Wang S., Gao J., Wang Z.: Outer membrane vesicles for vaccinationand targeted drug delivery. Wiley Interdiscip. Rev. Nanomed.Nanobiotechnol., 2019; 11: e1523
  Google Scholar
• 116. Yaron S., Kolling G.L., Simon L., Matthews K.R.: Vesicle-mediatedtransfer of virulence genes from Escherichia coli O157:H7 toother enteric bacteria. Appl. Environ. Microbiol., 2000; 66: 4414-4420
  Google Scholar
• 117. Yonezawa H., Osaki T., Kurata S., Fukuda M., Kawakami H.,Ochiai K., Hanawa T., Kamiya S.: Outer membrane vesicles of Helicobacterpylori TK1402 are involved in biofilm formation. BMC Microbiol.,2009; 9: 197
  Google Scholar

Full text