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Review

Extracellular vesicles of bacteria as potential targets for immune interventions

ORCID Icon, &
Pages 897-903 | Received 22 Mar 2020, Accepted 19 Jul 2020, Published online: 01 Sep 2020

References

  • Kegelman TP, Das SK, Emdad L, Hu B, Menezes ME, Bhoopathi P, Wang X-Y, Pellecchia M, Sarkar D, Fisher PB. Targeting tumor invasion: the roles of MDA-9/Syntenin. Expert Opin Ther Targets PMID:25219541. 2015;19(1):97–112. doi:10.1517/14728222.2014.959495.
  • van der Pol E, Boing AN, Harrison P, Sturk A, Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev PMID:22722893. 2012;64:676–705. doi:10.1124/pr.112.005983..
  • Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol PMID:19144520. 2009;19:43–51. doi:10.1016/j.tcb.2008.11.003.
  • Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol PMID:23420871. 2013;200:373–83. doi:10.1083/jcb.201211138..
  • Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic MM, Molina H, Kohsaka S, Di Giannatale A, Ceder S, et al. Tumour exosome integrins determine organotropic metastasis. Nature PMID:26524530. 2015;527:329–35. doi:10.1038/nature15756..
  • Wieckowski EU, Visus C, Szajnik M, Szczepanski MJ, Storkus WJ, Whiteside TL. Tumor-derived microvesicles promote regulatory T cell expansion and induce apoptosis in tumor-reactive activated CD8+ T lymphocytes. J Immunol PMID:19692638. 2009;183:3720–30. doi:10.94049/jimmunol.0900970.
  • Yang L, Wu XH, Wang D, Luo CL, Chen LX. Bladder cancer cell-derived exosomes inhibit tumor cell apoptosis and induce cell proliferation in vitro. Mol Med Rep PMID:23969721. 2013;8:1272–78. doi:10.3892/mmr.2013.1634.
  • Lécrivain AL, Beckmann BM. Bacterial RNA in extracellular vesicles: A new regulator of host-pathogen interactions? Biochim Biophys Acta Gene Regul Mech PMID:32142907. 2020;1863:194–519. doi:10.1016/j.bbagrm.2020.194519.
  • Cai Q, He B, Weiberg A, Buck AH, Jin H. Small RNAs and extracellular vesicles: new mechanisms of cross-species communication and innovative tools for disease control. PLoS Pathog PMID:31887135. 2019;15:e1008090. doi:10.1371/journal.ppat.1008090.
  • Ma J, Zhao Y, Sun L, Sun X, Zhao X, Sun X, Qian H, Xu W, Zhu W. Exosomes Derived from Akt -Modified Human Umbilical Cord Mesenchymal Stem Cells Improve Cardiac Regeneration and Promote Angiogenesis via Activating Platelet-Derived Growth Factor D. Stem Cells Transl Med PMID:28170176. 2017;6(1):51–59. doi:10.5966/sctm.2016-0038.
  • Brown L, Wolf JM, Prados-Rosales R, Casadevall A. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat Rev Microbiol PMID:26324094. 2015;13:620–30. doi:10.1038/nrmicro3480..
  • Kim JH, Lee J, Park J, Gho YS. Gram-negative and Gram-positive bacterial extracellular vesicles. Semin Cell Dev Biol PMID:25704309. 2015;40:97–104. doi:10.1016/j.semcdb.2015.02.006.
  • Simons M, Raposo G. Exosomes–vesicular carriers for intercellular communication. Curr Opin Cell Biol PMID:19442504. 2009;21:575–81. doi:10.1016/j.ceb.2009.03.007.
  • Tkach M, Théry C. Communication by Extracellular Vesicles: where We Are and Where We Need to Go. Cell PMID:26967288. 2016;164:1226–32. doi:10.1016/j.cell.2016.01.043..
  • Szatanek R, Baj-Krzyworzeka M, Zimoch J, Lekka M, Siedlar M, Baran J. The Methods of Choice for Extracellular Vesicles (EVs) Characterization. Int J Mol Sci. 2017. doi:18.doi:10.3390/ijms18061153. PMID:28555055.
  • Piotrowska M, Ciura K, Zalewska M, Dawid M, Correia B, Sawicka P, Lewczuk B, Kasprzyk J, Sola L, Piekoszewski W, et al. Capillary zone electrophoresis of bacterial extracellular vesicles: A proof of concept. J Chromatogr A. 2020. PMID:32197757. doi:1621:461047.doi:10.1016/j.chroma.2020.461047
  • Gould SJ, Raposo G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. J Extracell Vesicles. 2013. doi:2.doi:10.3402/jev.v2i0.20389. PMID:24009890.
  • Macia L, Nanan R, Hosseini-Beheshti E, Grau GE. Host- and Microbiota-Derived Extracellular Vesicles, Immune Function, and Disease Development. Int J Mol Sci. 2019. doi:21.doi:10.3390/ijms21010107. PMID:31877909.
  • Dagnelie MA, Corvec S, Khammari A, Dréno B. Bacterial extracellular vesicles: A new way to decipher host-microbiota communications in inflammatory dermatoses. Exp Dermatol PMID:31633842. 2020;29:22–28. doi:10.1111/exd.14050..
  • Roier S, Zingl FG, Cakar F, Schild S. Bacterial outer membrane vesicle biogenesis: a new mechanism and its implications. Microb Cell PMID:28357362. 2016;3:257–59. doi:10.15698/mic2016.06.508.
  • Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol PMID:12524386. 2003;21:335–76. doi:10.1146/annurev.immunol.21.120601.141126.
  • Kulkarni HM, Nagaraj R, Jagannadham MV. Protective role of E. coli outer membrane vesicles against antibiotics. Microbiol Res PMID:26640046. 2015;181:1–7. doi:10.1016/j.micres.2015.07.008.
  • Thay B, Damm A, Kufer TA, Wai SN, Oscarsson J. Aggregatibacter actinomycetemcomitans outer membrane vesicles are internalized in human host cells and trigger NOD1- and NOD2-dependent NF-kappaB activation. Infect Immun PMID:25024364. 2014;82:4034–46. doi:10.1128/IAI.01980-14.
  • Bitto NJ, Baker PJ, Dowling JK, Wray-McCann G, De Paoli A, Tran LS, Leung PL, Stacey KJ, Mansell A, Masters SL, et al. Membrane vesicles from Pseudomonas aeruginosa activate the noncanonical inflammasome through caspase-5 in human monocytes. Immunology and Cell Biology PMID:30003588. 2018;96:1120–30. doi:10.1111/imcb.12190.
  • Bartolini E, Ianni E, Frigimelica E, Petracca R, Galli G, Berlanda SF, Norais N, Laera D, Giusti F, Pierleoni A, et al. Recombinant outer membrane vesicles carrying Chlamydia muridarum HtrA induce antibodies that neutralize chlamydial infection in vitro. J Extracell Vesicles. 2013. PMID:24009891. doi:2.doi:10.3402/jev.v2i0.20181
  • Gujrati V, Kim S, Kim S-H, Min JJ, Choy HE, Kim SC, Jon S. Bioengineered bacterial outer membrane vesicles as cell-specific drug-delivery vehicles for cancer therapy. ACS Nano PMID:24410085. 2014;8:1525–37. doi:10.1021/nn405724x.
  • Bobat S, Flores-Langarica A, Hitchcock J, Marshall JL, Kingsley RA, Goodall M, Gil-Cruz C, Serre K, Leyton DL, Letran SE, et al. Soluble flagellin, FliC, induces an Ag-specific Th2 response, yet promotes T-bet-regulated Th1 clearance of Salmonella typhimurium infection. Eur J Immunol PMID:21469112. 2011;41:1606–18. doi:10.1002/eji.201041089.
  • Turner KL, Cahill BK, Dilello SK, Gutel D, Brunson DN, Alberti S, Ellis TN. Porin Loss Impacts the Host Inflammatory Response to Outer Membrane Vesicles of Klebsiella pneumoniae. Antimicrob Agents Chemother PMID:26666932. 2015;60:1360–69. doi:10.1128/AAC.01627-15.
  • Ellis TN, Kuehn MJ. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev PMID:20197500. 2010;74:81–94. doi:10.1128/MMBR.00031-09.
  • Yang J, Kim EK, Park HJ, McDowell A, Kim YK. The impact of bacteria-derived ultrafine dust particles on pulmonary diseases. Exp Mol Med PMID:32203101. 2020;52:338–47. doi:10.1038/s12276-019-0367-3.
  • Kim YS, Lee WH, Choi EJ, Choi JP, Heo YJ, Gho YS, Jee YK, Oh YM, Kim YK. Extracellular vesicles derived from Gram-negative bacteria, such as Escherichia coli, induce emphysema mainly via IL-17A-mediated neutrophilic inflammation. J Immunol PMID:25716999. 2015;194:3361–68. doi:10.4049/jimmunol.1402268.
  • Park K-S, Lee J, Jang SC, Kim SR, Jang MH, Lötvall J, Kim Y-K, Gho YS. Pulmonary inflammation induced by bacteria-free outer membrane vesicles from Pseudomonas aeruginosa. American Journal of Respiratory Cell and Molecular Biology PMID:23713467. 2013;49:637–45. doi:10.1165/rcmb.2012-0370OC.
  • Nahui PRA, Vanpouille C, Laghi L, Parolin C, Melikov K, Backlund P, Vitali B, Margolis L. Extracellular vesicles from symbiotic vaginal lactobacilli inhibit HIV-1 infection of human tissues. Nat Commun. 2019. doi:10:5656.doi:10.1038/s41467-019-13468-9. PMID:31827089.
  • Lee WH, Choi HI, Hong SW, Kim KS, Gho YS, Jeon SG. Vaccination with Klebsiella pneumoniae-derived extracellular vesicles protects against bacteria-induced lethality via both humoral and cellular immunity. Exp Mol Med PMID:26358222. 2015;47:e183. doi:10.1038/emm.2015.59.
  • Unal CM, Schaar V, Riesbeck K. Bacterial outer membrane vesicles in disease and preventive medicine. Seminars in Immunopathology PMID:21153593. 2011;33:395–408. doi:10.1007/s00281-010-0231-y.
  • Di Pasquale A, Bonanni P, Garçon N, Stanberry LR, El-Hodhod M, Tavares Da Silva F. Vaccine safety evaluation: practical aspects in assessing benefits and risks. Vaccine PMID:27836435. 2016;34:6672–80. doi:10.1016/j.vaccine.2016.10.039.
  • McConnell MJ, Rumbo C, Bou G, Pachón J. Outer membrane vesicles as an acellular vaccine against Acinetobacter baumannii. Vaccine PMID:21679737. 2011;29:5705–10. doi:10.1016/j.vaccine.2011.06.001.
  • Nieves W, Petersen H, Judy BM, Blumentritt CA, Russell-Lodrigue K, Roy CJ, Torres AG, Morici LA. A Burkholderia pseudomallei outer membrane vesicle vaccine provides protection against lethal sepsis. Clin Vaccine Immunol PMID:24671550. 2014;21:747–54. doi:10.1128/cvi.00119-14.
  • Mitra S, Chakrabarti MK, Koley H. Multi-serotype outer membrane vesicles of Shigellae confer passive protection to the neonatal mice against shigellosis. Vaccine PMID:23684822. 2013;31:3163–73. doi:10.1016/j.vaccine.2013.05.001.
  • Hirahara K, Nakayama T. CD4+ T-cell subsets in inflammatory diseases: beyond the Th1/Th2 paradigm. Int Immunol PMID:26874355. 2016;28:163–71. doi:10.1093/intimm/dxw006.
  • Yasuda K, Takeuchi Y, Hirota K. The pathogenicity of Th17 cells in autoimmune diseases. Semin Immunopathol PMID:30891627. 2019;41:283–97. doi:10.1007/s00281-019-00733-8.
  • Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D, Jenney A, Connor TR, Hsu LY, Severin J, et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci U S A PMID:26100894. 2015;112:E3574–3581. doi:10.1073/pnas.1501049112.
  • Camilo V, Sugiyama T, Touati E. Pathogenesis of Helicobacter pylori infection. Helicobacter. 2017;22(Suppl). doi:1.doi:10.1111/hel.12405. PMID:28891130.
  • Liu Q, Li X, Zhang Y, Song Z, Li R, Ruan H, Huang X. Orally-administered outer-membrane vesicles from Helicobacter pylori reduce H. pylori infection via Th2-biased immune responses in mice. Pathogens and Disease. 2019;77: PMID:31504509. doi:10.1093/femspd/ftz050.
  • Hegerle N, Guiso N. Bordetella pertussis and pertactin-deficient clinical isolates: lessons for pertussis vaccines. Expert Rev Vaccines PMID:24953157. 2014;13:1135–46. doi:10.1586/14760584.2014.932254.
  • Zurita ME, Wilk MM, Carriquiriborde F, Bartel E, Moreno G, Misiak A, Mills KHG, Hozbor D. A Pertussis Outer Membrane Vesicle-Based Vaccine Induces Lung-Resident Memory CD4 T Cells and Protection Against, Including Pertactin Deficient Strains. Frontiers in Cellular and Infection Microbiology PMID:31106160. 2019;9:125. doi:10.3389/fcimb.2019.00125.
  • Gerver SM, Mihalkova M, Bion JF, Wilson APR, Chudasama D, Johnson AP, Hope R. Surveillance of Bloodstream Infections in Intensive Care Units in England, May 2016-April 2017: epidemiology and Ecology. J Hosp Infect. 2020. doi:10.1016/j.jhin.2020.05.010. PMID:32422311.
  • Lee E-Y, Choi D-Y, Kim D-K, Kim J-W, Park JO, Kim S, Kim S-H, Desiderio DM, Kim Y-K, Kim K-P, et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics PMID:19834908. 2009;9:5425–36. doi:10.1002/pmic.200900338.
  • Choi SJ, Kim M-H, Jeon J, Kim OY, Choi Y, Seo J, Hong S-W, Lee W-H, Jeon SG, Gho YS, et al. Active Immunization with Extracellular Vesicles Derived from Staphylococcus aureus Effectively Protects against Staphylococcal Lung Infections, Mainly via Th1 Cell-Mediated Immunity. PloS One PMID:26333035. 2015;10:e0136021. doi:10.1371/journal.pone.0136021.
  • Pastor Y, Camacho A, Gil AG, Ramos R, ALd C, Peñuelas I, Irache JM, Gamazo C. Effective protection of mice against Shigella flexneri with a new self-adjuvant multicomponent vaccine. Journal of Medical Microbiology PMID:28721849. 2017;66:946–58. doi:10.1099/jmm.0.000527.
  • Cho KS, Kang SA, Kim SD, Mun SJ, Yu HS, Roh HJ. Dendritic cells and M2 macrophage play an important role in suppression of Th2-mediated inflammation by adipose stem cells-derived extracellular vesicles. Stem Cell Res. 2019. doi:39:101500.doi:10.1016/j.scr.2019.101500. PMID:31344653.
  • Kim HY, Lim Y, An SJ, Choi BK. Characterization and immunostimulatory activity of extracellular vesicles from Filifactor alocis. Mol Oral Microbiol PMID:31675472. 2020;35:1–9. doi:10.1111/omi.12272.
  • Badmasti F, Ajdary S, Bouzari S, Fooladi AAI, Shahcheraghi F, Siadat SD. Immunological evaluation of OMV(PagL)+Bap(1-487aa) and AbOmpA(8-346aa)+Bap(1-487aa) as vaccine candidates against Acinetobacter baumannii sepsis infection. Molecular Immunology PMID:26277277. 2015;67:552–58. doi:10.1016/j.molimm.2015.07.031.
  • Huang W, Yao Y, Long Q, Yang X, Sun W, Liu C, Jin X, Li Y, Chu X, Chen B, et al. Immunization against multidrug-resistant Acinetobacter baumannii effectively protects mice in both pneumonia and sepsis models. PloS One. 2014;9. PMID:24956279. doi:e100727.doi:10.1371/journal.pone.0100727.
  • MacLennan CA, Riddle MS, Chen WH, Talaat KR, Jain V, Bourgeois AL, Frenck R, Kotloff K, Porter CK. Consensus Report on Shigella Controlled Human Infection Model: clinical Endpoints. Clin Infect Dis PMID:31816065. 2019;69:S591–s595. doi:10.1093/cid/ciz891.
  • Camacho AI, de Souza J, Sánchez-Gómez S, Pardo-Ros M, Irache JM, Gamazo C. Mucosal immunization with Shigella flexneri outer membrane vesicles induced protection in mice. Vaccine PMID:21911022. 2011;29:8222–29. doi:10.1016/j.vaccine.2011.08.121.
  • Chitneni P, Beksinska M, Dietrich JJ, Jaggernath M, Closson K, Smith P, Lewis DA, Matthews LT, Smit J, Ndung’u T, et al. Partner notification and treatment outcomes among South African adolescents and young adults diagnosed with a sexually transmitted infection via laboratory-based screening. Int J STD AIDS. 2020;956462420915395. PMID:32403988. doi:10.1177/0956462420915395
  • Liu Y, Hammer LA, Liu W, Hobbs MM, Zielke RA, Sikora AE, Jerse AE, Egilmez NK, Russell MW. Experimental vaccine induces Th1-driven immune responses and resistance to Neisseria gonorrhoeae infection in a murine model. Mucosal Immunology PMID:28272393. 2017;10:1594–608. doi:10.1038/mi.2017.11.
  • Choi C-W, Park EC, Yun SH, Lee S-Y, Kim SI, Kim G-H. Potential Usefulness of Extracellular Membrane Vesicles as Antibacterial Vaccines. Journal of Immunology Research PMID:28210633. 2017;2017:7931982. doi:10.1155/2017/7931982.
  • de Figueiredo P, Ficht TA, Rice-Ficht A, Rossetti CA, Adams LG. Pathogenesis and immunobiology of brucellosis: review of Brucella-host interactions. The American Journal of Pathology PMID:25892682. 2015;185:1505–17. doi:10.1016/j.ajpath.2015.03.003.
  • Bagheri Nejad R, Yahyaraeyat R, Es-Haghi A, Nayeri Fasaei B, Zahraei Salehi T. Induction of specific cell-mediated immune responses and protection in BALB/c mice by vaccination with outer membrane vesicles from a Brucella melitensis human isolate. APMIS: acta pathologica, microbiologica, et immunologica Scandinavica PMID:31514254. 2019;127:797–804. doi:10.1111/apm.12997.
  • Vetter V, Denizer G, Friedland LR, Krishnan J, Shapiro M. Understanding modern-day vaccines: what you need to know. Ann Med PMID:29172780. 2018;50:110–20. doi:10.1080/07853890.2017.1407035.
  • Langereis JD, de Jonge MI. Unraveling Haemophilus influenzae virulence mechanisms enable discovery of new targets for antimicrobials and vaccines. Curr Opin Infect Dis PMID:32304471. 2020;33:231–37. doi:10.1097/qco.0000000000000645.
  • Michel LV, Kaur R, Zavorin M, Pryharski K, Khan MN, LaClair C, O’Neil M, Xu Q, Pichichero ME. Intranasal coinfection model allows for assessment of protein vaccines against nontypeable Haemophilus influenzae in mice. J Med Microbiol PMID:30136923. 2018;67:1527–32. doi:10.1099/jmm.0.000827.
  • Behrouzi A, Bouzari S, Siadat SD, Oloomi M, Davari M, Mazaheri H. Evaluation of the immunogenic property of NT H. influenzae protein D with Neisseria meningitidis OMV in BALB/c. Journal of Infection in Developing Countries PMID:28036315. 2016;10:1345–51. doi:10.3855/jidc.7513.
  • Batista-Duharte A, Martínez DT, Carlos IZ. Efficacy and safety of immunological adjuvants. Where is the cut-off? Biomed Pharmacother PMID:29894962. 2018;105:616–24. doi:10.1016/j.biopha.2018.06.026.
  • Trainor EA, Nicholson TL, Merkel TJ. Bordetella pertussis transmission. Pathog Dis PMID:26374235. 2015;73:ftv068. doi:10.1093/femspd/ftv068.
  • Bottero D, Zurita ME, Gaillard ME, Carriquiriborde F, Martin Aispuro P, Elizagaray M, Bartel E, Castuma C, Hozbor D. Outer-Membrane-Vesicle-Associated O Antigen, a Crucial Component for Protecting Against Infection. Frontiers in Immunology PMID:30459769. 2018;9:2501. doi:10.3389/fimmu.2018.02501.
  • Ylinen E, Salmenlinna S, Halkilahti J, Jahnukainen T, Korhonen L, Virkkala T, Rimhanen-Finne R, Nuutinen M, Kataja J, Arikoski P, et al. Hemolytic uremic syndrome caused by Shiga toxin-producing Escherichia coli in children: incidence, risk factors, and clinical outcome. Pediatr Nephrol. 2020. PMID:32323005. doi:10.1007/s00467-020-04560-0
  • Fingermann M, Avila L, De Marco MB, Vázquez L, Di Biase DN, Müller AV, Lescano M, Dokmetjian JC, Fernández Castillo S, Pérez Quiñoy JL. OMV-based vaccine formulations against Shiga toxin producing Escherichia coli strains are both protective in mice and immunogenic in calves. Human Vaccines & Immunotherapeutics PMID:29923791. 2018;14:2208–13. doi:10.1080/21645515.2018.1490381.
  • Pulido MR, García-Quintanilla M, Pachón J, McConnell MJ. A lipopolysaccharide-free outer membrane vesicle vaccine protects against Acinetobacter baumannii infection. Vaccine PMID:31843268. 2020;38:719–24. doi:10.1016/j.vaccine.2019.11.043.
  • Ellis TN, Leiman SA, Kuehn MJ. 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 PMID:20605984. 2010;78:3822–31. doi:10.1128/iai.00433-10.
  • van der Pol L, Stork M. van der Ley P. Outer membrane vesicles as platform vaccine technology. Biotechnol J PMID:26912077. 2015;10:1689–706. doi:10.1002/biot.201400395.
  • Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol PMID:20948547. 2010;10:787–96. doi:10.1038/nri2868.

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