Advancing vaccines with extracellular vesicles

References for ‘Advancing vaccines with extracellular vesicles’, in Drug Target Review Issue 3 2022.


  1. Xie J, Li Q, Haesebrouck F, et al. The tremendous biomedical potential of bacterial extracellular vesicles. Trends Biotechnol. 2022 May 14:S0167-7799(22)00073-7. doi: 10.1016/j.tibtech.2022.03.005. Epub ahead of print. PMID: 35581020.
  2. Chatterjee SN, Das J. Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. J Gen Microbiol. 1967 Oct;49(1):1-11. doi: 10.1099/00221287-49-1-1. PMID: 4168882.
  3. Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol. 2010;64:163-84. doi: 10.1146/annurev.micro.091208.073413. PMID: 20825345; PMCID: PMC3525469.
  4. Laughlin RC, Alaniz RC. Outer membrane vesicles in service as protein shuttles, biotic defenders, and immunological doppelgängers. Gut Microbes. 2016 Sep 2;7(5):450-4. doi: 10.1080/19490976.2016.1222345. Epub 2016 Aug 15. PMID: 27600586; PMCID: PMC5046169.
  5. Brameyer S, Plener L, Müller A, et al. Outer Membrane Vesicles Facilitate Trafficking of the Hydrophobic Signaling Molecule CAI-1 between Vibrio harveyi Cells. J Bacteriol. 2018 Jul 10;200(15):e00740-17. doi: 10.1128/JB.00740-17. PMID: 29555694; PMCID: PMC6040191.
  6. McMillan HM, Kuehn MJ. The extracellular vesicle generation paradox: a bacterial point of view. EMBO J. 2021 Nov 2;40(21):e108174. doi: 10.15252/embj.2021108174. Epub 2021 Oct 11. PMID: 34636061; PMCID: PMC8561641.
  7. Rudnicka M, Noszczyńska M, Malicka M, et al. Outer Membrane Vesicles as Mediators of Plant-Bacterial Interactions. Front Microbiol. 2022 Jun 1;13:902181. doi: 10.3389/fmicb.2022.902181. PMID: 35722319; PMCID: PMC9198584.
  8. Ionescu M, Zaini PA, Baccari C, et al. Xylella fastidiosa outer membrane vesicles modulate plant colonization by blocking attachment to surfaces. Proc Natl Acad Sci USA. 2014 Sep 16;111(37):E3910-8. doi: 10.1073/pnas.1414944111. Epub 2014 Sep 2. PMID: 25197068; PMCID: PMC4169949.
  9. Biller SJ, Schubotz F, Roggensack SE, et al. Bacterial vesicles in marine ecosystems. Science. 2014 Jan 10;343(6167):183-6. doi: 10.1126/science.1243457. PMID: 24408433.
  10. Tulkens J, Vergauwen G, Van Deun J, et al. Increased levels of systemic LPS-positive bacterial extracellular vesicles in patients with intestinal barrier dysfunction. Gut. 2020 Jan;69(1):191-193. doi: 10.1136/gutjnl-2018-317726. Epub 2018 Dec 5. PMID: 30518529; PMCID: PMC6943244.
  11. Gabarrini G, Grasso S, van Winkelhoff AJ, van Dijl JM. Gingimaps: Protein Localization in the Oral Pathogen Porphyromonas gingivalis. Microbiol Mol Biol Rev. 2020 Jan 2;84(1):e00032-19. doi: 10.1128/MMBR.00032-19. PMID: 31896547; PMCID: PMC6941882.
  12. Dhital S, Deo P, Stuart I, Naderer T. Bacterial outer membrane vesicles and host cell death signaling. Trends Microbiol. 2021 Dec;29(12):1106-1116. doi: 10.1016/j.tim.2021.04.003. Epub 2021 May 14. PMID: 34001418.
  13. Nonaka S, Kadowaki T, Nakanishi H. Secreted gingipains from Porphyromonas gingivalis increase permeability in human cerebral microvascular endothelial cells through intracellular degradation of tight junction proteins. Neurochem Int. 2022 Mar;154:105282. doi: 10.1016/j.neuint.2022.105282. Epub 2022 Jan 13. PMID: 35032577.
  14. Pritchard AB, Fabian Z, Lawrence CL, et al. An Investigation into the Effects of Outer Membrane Vesicles and Lipopolysaccharide of Porphyromonas gingivalis on Blood-Brain Barrier Integrity, Permeability, and Disruption of Scaffolding Proteins in a Human in vitro Model. J Alzheimers Dis. 2022;86(1):343-364. doi: 10.3233/JAD-215054. PMID: 35034897.
  15. Gerritzen MJH, Martens DE, Wijffels RH, et al. Bioengineering bacterial outer membrane vesicles as vaccine platform. Biotechnol Adv. 2017 Sep;35(5):565-574. doi: 10.1016/j.biotechadv.2017.05.003. Epub 2017 May 15. PMID: 28522212.
  16. Micoli F, Alfini R, Di Benedetto R, et al. GMMA Is a Versatile Platform to Design Effective Multivalent Combination Vaccines. Vaccines (Basel). 2020 Sep 17;8(3):540. doi: 10.3390/vaccines8030540. PMID: 32957610; PMCID: PMC7564227.
  17. Piccioli D, Bartolini E, Micoli F. GMMA as a ‘plug and play’ technology to tackle infectious disease to improve global health: context and perspectives for the future. Expert Rev Vaccines. 2022 Feb;21(2):163-172. doi: 10.1080/14760584.2022.2009803. Epub 2021 Dec 16. PMID: 34913415.
  18. Rappuoli R, Pizza M, Masignani V, Vadivelu K. Meningococcal B vaccine (4CMenB): the journey from research to real world experience. Expert Rev Vaccines. 2018 Dec;17(12):1111-1121. doi: 10.1080/14760584.2018.1547637. Epub 2018 Dec 5. PMID: 30457407.
  19. Perrett KP et al. Immune responses to a recombinant, four-component, meningococcal serogroup B vaccine (4CMenB) in adolescents: a phase III, randomized, multicentre, lot-to-lot consistency study. Vaccine, 2015, 33(39), 5217-24.
  20. Launay O. et al., Safety Profile and Immunologic Responses of a Novel Vaccine Against Shigella sonnei Administered Intramuscularly,Intradermally and Intranasally: Results From Two Parallel Randomized Phase 1 Clinical Studies in Healthy Adult Volunteers in Europe. EBioMedicine. 2017 Aug 22, 164-172.
  21. Rossi O, et al. Toll-Like Receptor Activation by Generalized Modules for Membrane Antigens from Lipid A Mutants of Salmonella enterica Serovars Typhimurium and Enteritidis. Clin Vaccine Immunol 2016, 23(4), 304-14.
  22. Curley SM, Putnam D. Biological Nanoparticles in Vaccine Development. Front Bioeng Biotechnol. 2022 Mar 23;10:867119. doi: 10.3389/fbioe.2022.867119. PMID: 35402394; PMCID: PMC8984165.
  23. Zhang Y, Fang Z, Li R, et al. Design of Outer Membrane Vesicles as Cancer Vaccines: A New Toolkit for Cancer Therapy. Cancers (Basel). 2019 Sep 6;11(9):1314. doi: 10.3390/cancers11091314. PMID: 31500086; PMCID: PMC6769604.
  24. Cheng K, Zhao R, Li Y, et al. Bioengineered bacteria-derived outer membrane vesicles as a versatile antigen display platform for tumor vaccination via Plug-and-Display technology. Nat Commun. 2021 Apr 6;12(1):2041. doi: 10.1038/s41467-021-22308-8. PMID: 33824314; PMCID: PMC8024398.
  25. Zhao X, Zhao R, Nie G. Nanocarriers based on bacterial membrane materials for cancer vaccine delivery. Nat Protoc. 2022 Jul 25. doi: 10.1038/s41596-022-00713-7. Epub ahead of print. PMID: 35879454.
  26. Chen L, Valentine JL, Chung-Jr H, et al. Outer membrane vesicles displaying engineered glycotopes elicit protective antibodies. Nat’l Acad Sci (2016) E3609-E3618.
  27. Valentine JL, Chen L, Perregaux EC, et al. Immunization with Outer Membrane Vesicles Displaying Designer Glycotopes Yields Class-Switched, Glycan-Specific Antibodies. Cell Chem Biol. (2016) Jun 23;23(6):655-65. doi:10.1016/j.chembiol.2016.05.014.
  28. Stevenson TC, Cywes-Bentley C, Moeller TD, et al. Immunization with outer membrane vesicles displaying conserved surface polysaccharide antigen elicits broadly antimicrobial mantibodies. Proc Natl Acad Sci USA. 2018 pii: 201718341.
  29. J-Y Kim, A.M. Doody, D.J. Chen, G.H. et al. Engineered bacterial outer membrane vesicles with enhanced functionality. Journal of Molecular Biology (2008) 380:51-66
  30. Rappazzo CG, Watkins HC, Guarino CM, et al. Recombinant M2e outer membrane vesicle vaccines protect against lethal influenza A challenge in BALB/c mice. Vaccine (2016) 34:1252-1258.
  31. Watkins HC, Rappazzo CG, Higgins JS, et al. Safe Recombinant Outer Membrane Vesicles that Display M2e Elicit Heterologous Influenza Protection. Mol Therapy (2017) 25:1-14.
  32. Watkins, HC, Pagan, CL, Childs, HR, et al. A single dose and long-lasting vaccine against pandemic influenza through the controlled release of a heterospecies tandem M2 sequence embedded within detoxified bacterial outer membrane vesicles. Vaccine (2017) 35(40):5373-5380.
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  34. Wang L, Chang TZ, He Y, et al. Coated protein nanoclusters from influenza H7N9 HA are highly immunogenic and induce robust protective immunity. Nanomedicine. 2017. 13(1):253-262.
  35. Deng L, Mohan T, Chang TZ, et al. Double-layered protein nanoparticles induce broad protection against divergent influenza A viruses. Nat Commun. 2018. 24;9(1):359.

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