epidemiologyЭпидемиология и ВакцинопрофилактикаEpidemiology and Vaccinal Prevention2073-30462619-0494«Numicom» LLC10.31631/2073-3046-2023-22-2-117-123epidemiology-1787Research ArticleОБЗОРREVIEWОсобенности биогенеза везикул наружных мембран микроорганизмов, их иммуногенная, протективная и адьювантная способностьFeatures of Biogenesis of Vesicles of External Membranes of Microorganisms, theirImmunogenic, Protective and Adjuvant Abilityhttps://orcid.org/0000-0001-5208-7724ОмельченкоН. Д.OmelchenkoN. D.

Наталья Дмитриевна Омельченко – кандидат медицинских наук, старший научный сотрудник лаборатории иммунологии ООИ.

344002, Ростов-на-Дону, ул. Максима Горького,117/40. +7 (918) 545-54-12,  +7 (863) 240-91-22, факс: +7 (863) 267-02-23

Omelchenko Natalia D. - Cand. Sci. (Med.), Senior Researcher Laboratory of Immunology Particularly Dangerous Infections.

117/40, Maxim Gorky str., Rostov-on-don, 344002, +7 (918) 545-54-12, +7 (863) 240-91-22, fax: +7 (863) 267-02-23

natalya.omelchenko@yandex.ruhttps://orcid.org/0000-0001-7068-4071ИвановаИ. А.IvanovaI. A.

Инна Александровна Иванова – кандидат биологических наук, ведущий научный сотрудник с врио зав. лабораторией иммунологии ООИ.

Ростов-на-Дону

Inna A. Ivanova – Cand. Sci. (Biol.), Leading Researcher with Acting Head of the Immunology Laboratory Particularly Dangerous Infections.

Rostov-on-Don

ivanova_ia@antiplague.ruhttps://orcid.org/0000-0002-1702-1620ДувановаО. В.DuvanovaO. V.

Ольга Викторовна Дуванова – кандидат биологических наук, старший научный сотрудник лаборатории диагностики ООИ.

Ростов-на-Дону

Olga V. Duvanova – Cand. Sci. (Biol.), Senior Researcher Laboratory of Diagnostic Laboratory Particularly Dangerous Infections.

Rostov-on-Don

olga_duvanova@mail.ruhttps://orcid.org/0000-0002-8517-2789ШипкоЕ. В.ShipkoE. V.

Елена Сергеевна Шипко – младший научный сотрудник лаборатории диагностики ООИ.

Ростов-на-Дону

Elena S. Shipko – Junior Researcher, Laboratory of Diagnostic Laboratory Particularly Dangerous Infections.

Rostov-on-Don

helena.shipman@gmail.comhttps://orcid.org/0000-0002-1103-4244ФилиппенкоА. В.FilippenkoA. V.

Анна Владимировна Филиппенко – младший научный сотрудник лаборатории иммунологии ООИ.

Ростов-на-Дону

Anna V. Filippenko – Junior Researcher, Laboratory of Immunology Particularly Dangerous Infections.

Rostov-on-Don

filippenko.annushka@mail.ruhttps://orcid.org/0000-0002-4770-5994ТруфановаА. А.TrufanovaA. A.

Анастасия Александровна Труфанова – младший научный сотрудник лаборатории иммунологии ООИ.

Ростов-на-Дону

Anastasia A. Trufanova – Junior Researcher, Laboratory of Immunology Particularly Dangerous Infections.

Rostov-onDon

nastyasia61@mail.ruФКУЗ Ростовский-на-Дону противочумный институт РоспотребнадзораРоссияRostov-on-Don Anti-Plague Institute of RospotrebnadzorRussian Federation202310052023222117123Copyright © Омельченко Н.Д., Иванова И.А., Дуванова О.В., Шипко Е.В., Филиппенко А.В., Труфанова А.А., 20232023Омельченко Н.Д., Иванова И.А., Дуванова О.В., Шипко Е.В., Филиппенко А.В., Труфанова А.А.Omelchenko N.D., Ivanova I.A., Duvanova O.V., Shipko E.V., Filippenko A.V., Trufanova A.A.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.epidemvac.ru/jour/article/view/1787Актуальность

Актуальность. Процесс продукции бактериями внешнемембранных везикул (outer membrane vesicles – OMVs) является основным механизмом в межклеточной коммуникации и посредником во взаимоотношениях самого разного характера (симбиоза, комменсализма и паразитизма), поэтому изучение роли везикул в пато- и иммуногенезе бактерий является важной и своевременной задачей.

Цель

Цель. Целью настоящего исследования явился анализ научных публикаций российских и зарубежных журналов за период с 2002 по 2021 гг. из библиографических баз eLibrary.Ru, PubMed®, MEDLINE, посвящённых везикулам наружных мембран, формирующимся у различных видов патогенных и непатогенных бактерий.

Заключение

Заключение. Изучение структуры, факторов образования, функциональной значимости механизмов действия бактериальных везикул, а также роли этих структур в пато- и иммуногенезе различных заболеваний, в том числе и особо опасных, даёт возможность создания на их основе новых профилактических препаратов. Использование везикул в качестве средств доставки биологических препаратов и различных антигенов открывает новые возможности для совершенствования терапии и профилактики инфекций.

Relevance

Relevance. The process of production of outer membrane vesicles by bacteria is the main mechanism in intercellular communication and an intermediary in relationships of a very different nature (symbiosis, commensalism and parasitism), therefore, the study of the role of vesicles in the pathogenesis and immunogenesis of bacteria is an important and timely task.

Aims

Aims. The purpose of this research was the analysis of scientific publications Russian and foreign journals for the period from 2002 to 2021 from the bibliographic databases of eLibrary.Ru, PubMed®, MEDLINE, dedicated to vesicles of outer membranes formed in various types of pathogenic and non-pathogenic bacteria.

Conclusion

Conclusion. The study of the structure, factors of formation, functional significance of the mechanisms of action of bacterial vesicles, as well as the role of these structures in the pathogenesis and immunogenesis of various diseases, including especially dangerous ones, makes it possible to create new preventive drugs based on them. The use of vesicles as means of delivery of biological drugs and various antigens opens up new opportunities for improving the therapy and prevention of infections.

везикулы наружных мембранпатогенезиммуногенезадьювантиммунный ответвакциныouter membrane vesiclespathogenesisimmunogenesisadjuvantimmune responsevaccinesReferencesThéry S., Witwer K.W., Aikawa E., et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV 2014 guidelines // J of Extracellular Vesicles. 2018 Vol.8. Р. 1–43.Théry S, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV 2014 guidelines. J of Extracellular Vesicles. 2018; 8:1–43. doi: ORG/10.1080/20013078.2018.15357502.Шендеров Б.А., Синица А.В., Захарченко М.М., Ткаченко Е.И. Внеклеточные везикулы (экзосомы) и их роль в биологии бактерий и реализации их патогенного потенциала // Экспериментальная и клиническая гастроэнтерология. 2020 Т.179, № 7. С. 118–130.Shenderov BA, Sinica AV, Zaharchenko MM, Tkachenko EI. Vnekletochnye vezikuly (ekzosomy) i ih rol’ v biologii bakterij i realizacii ih patogennogo potenciala. Eksperimental’naya i klinicheskaya gastroenterologiya. 2020; 179 (7):118–130. (In Russ). doi: 10.31146/1682-8658-ecg179-7-118-130Луста К.А., Кондашевская М.В. Участие внеклеточных мембранных нановезикул бактерий в патологических процессах (обзор литературы) // Вестник новых мед. технологий. Электронное издание. 2019, № 2. С. 148–157.Lusta KA, Kondashevskaya MV. Uchastie vnekletochnyh membrannyh nanovezikul bakterij v patologicheskih processah (obzor literatury). Vestnik novyh med. tekhnologij. 2019; 2:148–157. (In Russ). doi: 10.24411/2075-4094-2019-16306Луста К.А. Бактериальные мембранные внеклеточные нановезикулы: строение, биогенез, функции, использование в биотехнологии и медицине (обзор) // Прикладная биохим. и микробиол. 2015 Т.51, № 5. С. 443–452.Lusta KA. Bakterial’nye membrannye vnekletochnye nanovezikuly: stroenie, biogenez, funkcii, ispol’zovanie v biotekhnologii i medicine (obzor). Prikladnaya biohim. i mikrobiol. 2015;51(5):443–452. (In Russ). doi:10.7868/S0555109915040091Schooling S.R., Beveridge T.J. Membrane vesicles: an overlooked component of the matrices of biofilms // J Bacteriol. 2006 Vol.188, №16. Р. 5945–5957.Schooling SR, Beveridge TJ. Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol. 2006;188(16):5945–5957. doi: 10.1128/jb.00257-06Perez-Cruz C., Delgado L., López-Iglesias C., Mercade E. Outer-inner membrane vesicles naturally secreted by gram-negative pathogenic bacteria // PLoS ONE. 2015 Vol.10, № 1. e0116896.Perez-Cruz C, Delgado L, López-Iglesias C, Mercade E. Outer-inner membrane vesicles naturally secreted by gram-negative pathogenic bacteria. PLoS ONE. 2015;10(1):e0116896. doi: 10.1101/gad.1299905Horstman A.L., Kuehn M.J. Bacterial surface association of heat-labile enterotoxin through lipopolysaccharide after secretion via the general secretory pathway // J Biol Chem. 2002 Vol.277, № 36. P. 32538–32545.Horstman AL, Kuehn MJ. Bacterial surface association of heat-labile enterotoxin through lipopolysaccharide after secretion via the general secretory pathway. Biol Chem. 2002; 277(36): 32538–32545. doi:10.1074/jbc.m203740200Lai C.H., Listgarten M.A, Hammond B.F. Comparative ultrastructure of leukotoxic and non-leukotoxic strains of Actinobacillus actinomycetemcomitans // J Periodontal Res. 1981 Vol.16. Р. 379–389.Lai CH, Listgarten MA, Hammond BF. Comparative ultrastructure of leukotoxic and non-leukotoxic strains of Actinobacillus actinomycetemcomitans. J Periodontal Res. 1981;16:379–389. doi: 10.1111/j.1600-0765.1981.tb00989.x.Baumgarten T., Sperling S., Seifert J., von Bergen M., et al. Membrane vesicle formation as a multiple-stress response mechanism enhances Pseudomonas putida DOT.T1E cell surface hydrophobicity and biofilm formation // Appl Environ Microbiol. 2012 Vol.78, №17. P. 6217–6224.Baumgarten T, Sperling S, Seifert J, et al. Membrane vesicle formation as a multiple.stress response mechanism enhances Pseudomonas putida DOT.T1E cell surface hydrophobicity and biofilm formation. Appl Environ Microbiol. 2012;78(17):6217–6224. doi:10.1128/AEM.01525-12Kamaguchi A., Nakayama K., Ichiyama S., et al. Effect of Porphyromonas gingivalis vesicles on coaggregation of Staphylococcus aureus to oral microorganisms // Curr Microbiol. 2003 Vol.l47, №6. P. 485–491.Kamaguchi A, Nakayama K, Ichiyama S, et al. Effect of Porphyromonas gingivalis vesicles on coaggregation of Staphylococcus aureus to oral microorganisms. Curr Microbiol. 2003;l47(6):485–491. doi: 10.1007/s00284-003-4069-6Kuehn M.J., Kesty N.C. Bacterial outer membrane vesicles and the host-pathogen interaction // Genes Dev. 2005 Vol.19, №22. P. 2645–2655.Kuehn MJ, Kesty NC. Bacterial outer membrane vesicles and the host.pathogen interaction. Genes Dev. 2005;19(22):2645–2655. doi: 10.1101/gad.1299905Stentz R., Carvalho A.L., Jones E.J., Carding S.R. Fantastic voyage: The journey of intestinal microbiota-derived microvesicles through the body // Biochem Soc Trans. 2018 Vol.46. P. 1021–1027.Stentz R, Carvalho AL, Jones EJ, Carding SR. Fantastic voyage: The journey of intestinal microbiota-derived microvesicles through the body. Biochem Soc Trans. 2018;46:1021– 1027. doi: 10.1042/BST20180114Bose S., Aggarwal S., Singh D. V, Acharya N. Extracellular vesicles: An emerging platform in gram-positive bacteria // Microb Cell. 2020 Vol.7, №12. P.312–322.Bose S, Aggarwal S, Singh DV, Acharya N. Extracellular vesicles: An emerging platform in gram-positive bacteria. Microb Cell. 2020;7(12):312–322. doi: 10.15698/mic2020.12.737Ellis T.N., Kuehn M.J. Virulence and immunomodulatory roles of bacterial outer membrane vesicles // Microbiol Mol Biol Rev. 2010 Vol.74, №1. P.81–94.Ellis TN, Kuehn MJ. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev. 2010;74(1):81–94. doi: 10.1128/MMBR.00031-09O’Donoghue E.J., Krachler A.M. Mechanisms of outer membrane vesicle entry into host cells // Cell Microbiol. 2016 Vol.18, №11. P. 1508–1517.O’Donoghue EJ, Krachler AM. Mechanisms of outer membrane vesicle entry into host cells. Cell Microbiol. 2016;18(11):1508–1517. doi: 10.1111/cmi.12655Zakharzhevskaya N.B., Vanyushkina A.A., Altukhov I.A., et al. Outer membrane vesicles secreted by pathogenic and nonpathogenic Bacteroides fragilis represent different metabolic activities // Sci. Rep. 2017 Vol.7. P. 5008.Zakharzhevskaya NB, Vanyushkina AA, Altukhov IA, et al. Outer membrane vesicles secreted by pathogenic and nonpathogenic Bacteroides fragilis represent different metabolic activities. Sci. Rep. 2017;7:5008. doi: 10.1038/s41598-017-05264-6Ellen A.F., Albers S.-V., Huibers W., et al. Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components // Extremophiles. 2009 Vol.13, №1. P. 67–79.Ellen AF, Albers S-V, Huibers W, et al. Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles. 2009;13(1):67–79. doi: 10.1007/s00792-008-0199-xKunsmann L., Ruter C., Bauwens A., et al. Virulence from vesicles: novel mechanisms of host cell injury by Escherichia coli O104:H4 outbreak strain // Sci Rep. 2015 Vol.5. P. 13252.Kunsmann L, Ruter C, Bauwens A, et al. Virulence from vesicles: novel mechanisms of host cell injury by Escherichia coli O104:H4 outbreak strain. Sci Rep. 2015;5:13252. doi: 10.1038/srep13252Olofsson A., Vallstrom A., Petzold K., et al. Biochemical and functional characterization of Helicobacter pylori vesicles // Mol Microbiol. 2010 Vol.77, №6. P.1539–1555.Olofsson A, Vallstrom A, Petzold K, et al. Biochemical and functional characterization of Helicobacter pylori vesicles. Mol Microbiol. 2010;77(6):1539–1555. doi: 10.1111/j.1365-2958.2010.07307.xZingl F.G., Kohl P., Cakar F., et al. Outer membrane vesiculation facilitates surface exchange and in vivo adaptation of Vibrio cholerae // Cell Host Microbe. 2020 Vol.27. P. 225–237.Zingl FG, Kohl P, Cakar F, et al. Outer membrane vesiculation facilitates surface exchange and in vivo adaptation of Vibrio cholerae. Cell Host Microbe. 2020;27:225–237. doi.org/10.1016/j.chom.2019.12.002Kesty N.C., Mason K.M., Reedy M., et al. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells // EMBO J. 2004 Vol.23, №23. P.4538–4549.Kesty NC, Mason KM, Reedy M, et al. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 2004;23(23):4538–4549. doi: 10.1038/sj.emboj.7600471Xie H. Biogenesis and function of Porphyromonas gingivalis outer membrane vesicles // Future Microbiol. 2015 Vol.10, №9. P. 1517–1527.Xie H. Biogenesis and function of Porphyromonas gingivalis outer membrane vesicles. Future Microbiol. 2015;10(9):1517–1527. doi: 10.2217/fmb.15.63Jin J.S., Kwon S.-O., Moon D.C., et al. Acinetobacter baumannii secretes cytotoxic outer membrane protein A via outer membrane vesicles // J Рone. 2011 Vol.6, №2. e17027.Jin JS, Kwon S-O, Moon DC, et al. Acinetobacter baumannii secretes cytotoxic outer membrane protein A via outer membrane vesicles. Journal Рone. 2011;6(2):e17027. doi: 10.1371/.0017027Соколов А.В., Костин Н.Н., Овчинникова Л.А., и др. Направленный транспорт лекарственных препаратов в липидоподобных наноконтейнерах и внеклеточных везикулах // Acta Naturae. 2019 Т.11, №2 (41). С. 28–41.Sokolov AV, Kostin NN, Ovchinnikova LA, et al. Napravlennyj transport lekarstvennyh preparatov v lipidopodobnyh nanokontejnerah i vnekletochnyh vezikulah. Acta Naturae.2019; 11(2, Suppl 41):28–41. (In Russ). doi: 10.32607/20758251-2019-11-2-28-41Lee J.C., Lee E.J., Lee J.H., et al. Klebsiella pneumoniae secretes outer membrane vesicles that induce the innate immune response // FEMS Microbiol. Lett. 2012 Vol.331, №1. P. 17–24.Lee JC, Lee EJ, Lee JH, et al. Klebsiella pneumoniae secretes outer membrane vesicles that induce the innate immune response. FEMS Microbiol. Lett. 2012;331(1):17–24. doi: 10.1111/j.1574-6968.2012.02549.xShen Y., Letizia M., Torchia, G., et al. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection // Cell Host Microbe. 2012 Vol.12. P.509–520.Shen Y, Letizia M, Torchia G, et al. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe. 2012;12:509– 520. doi: 10.1016/j.chom.2012.08.004Schetters S.T.T., Jong W.S.P., Horrevorts S.K., et al. Outer membrane vesicles engineered to express membrane-bound antigen program dendritic cells for cross-presentation to CD8+ T cells // Acta Biomater. 2019 Vol.91. P. 248–257.Schetters STT, Jong WSP, Horrevorts SK, et al. Outer membrane vesicles engineered to express membrane-bound antigen program dendritic cells for cross-presentation to CD8 + T cells. Acta Biomater. 2019;91:248–257. doi: 10.1016/j.actbio.2019.04.033Johnston E.L., Heras B., Kufer T.A., Kaparakis-Liaskos M. Detection of bacterial membrane vesicles by nod-like receptors //J Mol Sci. 2021 Vol.22, №3. P. 1005.Johnston EL, Heras B, Kufer TA, Kaparakis-Liaskos M. Detection of bacterial membrane vesicles by nod-like receptors. J Mol Sci. 2021;22(3):1005. doi:10.3390/ijms22031005Filiano A.J., Xu Y., Tustison N.J., et al. Unexpected role of interferon-γ in regulating neuronal connectivity and social behavior // Nature. 2013 Vol.535. P. 425–429.Filiano AJ, Xu Y, Tustison NJ, et al. Unexpected role of interferon-γ in regulating neuronal connectivity and social behavior. Nature. 2013;535:425–429. doi: 10.1038/nature18626Kang C.S., Ban M., Choi E.J., et al. Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodiuminduced colitis // PLoS ONE. 2013 Vol.8. e76520.Kang CS, Ban M, Choi EJ, et al. Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodiuminduced colitis. PLoS ONE. 2013;8:e76520. doi: 10.1371/journal.pone.0076520.e Collection 2013Al-Nedawi K., Mian M.F., Hossain N., et al. Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems // FASEB J. 2015 Vol.29. P. 684–695.Al-Nedawi K, Mian MF, Hossain N, et al. Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems. FASEB J. 2015;29:684– 695. doi: 10.1096/fj.14-259721Yamasaki-Yashiki S., Miyoshi Y., Nakayama T., et al. IgA-enhancing effects of membrane vesicles derived from Lactobacillus sakei subsp. sakei NBRC15893 // Biosci. Microbiota Food Health. 2019 Vol.38. P. 23–29.Yamasaki-Yashiki S, Miyoshi Y, Nakayama T, et al. IgA-enhancing effects of membrane vesicles derived from Lactobacillus sakei subsp. sakei NBRC15893. Biosci. Microbiota Food Health. 2019;38:23–29. doi:org/10.12938/bmfh.18-015Fábrega M.J., Rodríguez-Nogales A., Garrido-Mesa J., et al. Intestinal anti-inflammatory effects of outer membrane vesicles from Escherichia coli nissle 1917 in dss-experimental colitis in mice // Front. Microbiol. 2017 Vol.8. P. 1274.Fábrega MJ, Rodríguez-Nogales A, Garrido-Mesa J, et al. Intestinal anti-inflammatory effects of outer membrane vesicles from Escherichia coli nissle 1917 in dss-experimental colitis in mice. Front. Microbiol. 2017;8:1274. doi: 10.3389/fmicb.2017.01274Seo M.K., Park E.J., Ko S.Y., et al. Therapeutic effects of kefir grain Lactobacillus-derived extracellular vesicles in mice with 2,4,6-trinitrobenzene sulfonic acid-induced inflammatory bowel disease // J Dairy Sci. 2018 Vol.101. P. 8662–8671.Seo MK, Park EJ, Ko SY, et al. Therapeutic effects of kefir grain Lactobacillus-derived extracellular vesicles in mice with 2,4,6-trinitrobenzene sulfonic acid-induced inflammatory bowel disease. J Dairy Sci. 2018;101:8662–8671. doi: 10.3168/jds.2018-15014Kim J.H., Jeun E.J., Hong C.P., et al. Extracellular vesicle-derived protein from Bifidobacterium longum alleviates food allergy through mast cell suppression // J Allergy Clin. Immunol. 2016 Vol.137. P. 507–516.Kim JH, Jeun EJ, Hong CP, et al. Extracellular vesicle-derived protein from Bifidobacterium longum alleviates food allergy through mast cell suppression. J Allergy Clin. Immunol. 2016;137:507–516. doi: 10.1016/j.jaci.2015.08.016Pritsch M., Ben-Khaled N., Chaloupka M., et al. Comparison of intranasal outer membrane vesicles with cholera toxin and injected MF59C.1 as adjuvants for malaria transmission blocking antigens AnAPN1 and Pfs48/45 // J of Immunology Res. 2016. e 3576028.Pritsch M, Ben-Khaled N, Chaloupka M, et al. Comparison of intranasal outer membrane vesicles with cholera toxin and injected MF59C.1 as adjuvants for malaria transmission blocking antigens AnAPN1 and Pfs48/45. J of Immunology Res. 2016;e3576028. doi: 10.1155/2016/3576028Macia L., Nanan R., Hosseini-Beheshti E., Grau G.E. Host- and microbiota-derived extracellular vesicles immune function and disease development // Int J Mol Sci. 2020 Vol.21, №1. Р. 107.Macia L, Nanan R, Hosseini-Beheshti E, Grau G.E. Host- and microbiota-derived extracellular vesicles immune function and disease development. Int J Mol Sci. 2020;21(1):107. doi:10.3390/ijms21010107Van der Pol L., Stork M., van der Ley P. Outer membrane vesicles as platform vaccine technology // Biotechnol J. 2015 Vol.10, №11. Р.1689–1706.van der Pol L, Stork M, van der Ley P. Outer membrane vesicles as platform vaccine technology. Biotechnol J. 2015;10(11):1689–1706. doi: 10.1002/biot.201400395Sedaghat M., Siadat S. D., Mirabzadeh E., et al. Evaluation of antibody responses to outer membrane vesicles (OMVs) and killed whole cell of Vibrio cholerae O1 El-Tor in immunized mice Iran // Iran J Microbiol. 2019 Vol.11, №3. Р. 212–219.Sedaghat M, Siadat SD, Mirabzadeh E, et al. Evaluation of antibody responses to outer membrane vesicles (OMVs) and killed whole cell of Vibrio cholerae O1 El-Tor in immunized miceIran. Iran J Microbiol. 2019;11(3): Р.212–219. doi.org/10.18502/ijm.v11i3.1317Bottero D, Zurita M.E., Gaillard M.E., et al. Outer-membrane-vesicle-associated O antigen, a crucial component for protecting against Bordetella parapertussis // Infection Frontiers in immunology. 2018 Vol.9. Р. 2501.Bottero D, Zurita ME, Gaillard ME, et al. Outer-membrane-vesicle-associated O antigen, a crucial component for protecting against Bordetella parapertussis. Infection Frontiers in immunology. 2018;9:2501. doi.org/10.3389/fimmu.2018.02501Howlader D.R., Koley H., Sinha R., et al. Development of a novel S. typhi and paratyphi A outer membrane vesicles based bivalent vaccine against enteric fever // PLoS ONE. 2018 Vol.13, №9. e0203631.Howlader DR, Koley H, Sinha R, et al. Development of a novel S. typhi and paratyphi A outer membrane vesicles based bivalent vaccine against enteric fever. PLoS ONE. 2018;13(9):e0203631. doi.org/10.1371/journal.pone.0203631Schager A.E., Dominguez-Medina C.C., Necchi F., et al. IgG responses to porins and lipopolysaccharide within an outer membrane-based vaccine against nontyphoidal Salmonella develop at discordant rates // mBio. 2018 Vol.9, №2. e 02379–17.Schager AE, Dominguez-Medina CC, Necchi F, et al. IgG responses to porins and lipopolysaccharide within an outer membrane-based vaccine against nontyphoidal Salmonella develop at discordant rates. mBio. 2018;9:e02379–17. doi: 10.1128/mBio.02379-17Mitra S., Barman S., Nag D., et al. Outer membrane vesicles of Shigella boydii type 4 induce passive immunity in neonatal mice // Fems Immunology et Medical Microbiology. 2012 Vol.66, №2. Р. 240–250.Mitra S, Barman S, Nag D, et al. Outer membrane vesicles of Shigella boydii type 4 induce passive immunity in neonatal mice. Fems Immunology et Medical Microbiology. 2012;66(2):240–250. doi: 10.1111/j.1574-695X.2012.01004.xКорнева А.В., Николаев В.Б., Половинкина В.С., и др. Получение, характеристика и вакцинный потенциал поверхностных структур бактериальных возбудителей особо опасных инфекций // Дальневосточный журнал инфекционной патологии. 2019 №37. С. 91–92.Korneva AV, Nikolaev VB, Polovinkina VS, et al. Poluchenie, harakteristika i vakcinnyj potencial poverhnostnyh struktur bakterial’nyh vozbuditelej osobo opasnyh infekcij. Dal’nevostochnyj zhurnal infekcionnoj patologii. 2019;37(Suppl 37):91–92. (In Russ). http://elib.fesmu.ru/elib/Article.aspx?id=392565Pierson T., Matrakas D., Taylor Y.U., et al. Proteomic characterization and functional analysis of outer membrane vesicles of Francisella novicida suggests possible role in virulence and use as a vaccine // J Proteome Res. 2011 Vol.10, №3. P. 954–967.Pierson T, Matrakas D, Taylor YU, et al. Proteomic characterization and functional analysis of outer membrane vesicles of Francisella novicida suggests possible role in virulence and use as a vaccine. J Proteome Res. 2011;10(3):954–967. doi: 10.1021/pr1009756McCaig W.D., Koller A., Thanassi D.G. Production of outer membrane vesicles and outer membrane tubes by Francisella novicida // J Bacteriol. 2013 Vol.195, №6. P. 1120– 1132.McCaig WD, Koller A, Thanassi DG. Production of outer membrane vesicles and outer membrane tubes by Francisella novicida. J Bacteriol. 2013;195(6):1120–1132. doi: 10.1128/JB.02007-12Avila-Calderón E.D., Lopez-Merino A, Jain N., et al. Characterization of outer membrane vesicles from Brucella melitensis and protection induced in mice // Clinical and Developmental Immunology. 2012 Vol.2. Р. 352493.Avila-Calderón ED, Lopez-Merino A, Jain N, et al. Characterization of outer membrane vesicles from Brucella melitensis and protection induced in mice. Clinical and Developmental Immunology. 2012;352493. doi.org/10.1155/2012/352493Byvalov A.A., Konyshev I.V., Uversky V.N., et al. Yersinia outer membrane vesicles as potential vaccine candidates in protecting against plague // Biomolecules. 2020 Vol.10, №12. e.1694.Byvalov AA, Konyshev IV, Uversky VN, et al. Yersinia outer membrane vesicles as potential vaccine candidates in protecting against plague. Biomolecules. 2020;10(12):e1694. doi: 10.3390/biom10121694Petersen H., Nieves W., Russell-Lodrigue K., et al. Evaluation of a Burkholderia pseudomallei outer membrane vesicle vaccine in nonhuman primates // Procedia Vaccinal. 2014 Vol.8. Р. 38–42.Petersen H, Nieves W, Russell-Lodrigue K, et al. Evaluation of a Burkholderia pseudomallei outer membrane vesicle vaccine in nonhuman primates. Procedia Vaccinal. 2014;8:38–42. doi: 10.1016/j.provac.2014.07.007Baker S.M., Davitt C.J.H., Motyka N., et al. A Burkholderia pseudomallei outer membrane vesicle vaccine provides cross protection against inhalational glanders in mice and non-Human primates // Vaccine. 2017 Vol.5, №4. Р. 49.Baker SM, Davitt CJ. H, Motyka N, et al. A Burkholderia pseudomallei outer membrane vesicle vaccine provides cross protection against inhalational glanders in mice and non-Human primates. Vaccine. 2017;5(4):49. doi: 10.3390/vaccines5040049Norris M.H., Khan M.S.R., Chirakul S., et al. Outer membrane vesicle vaccines from biosafe surrogates prevent acute lethal glanders in mice // Vaccine. 2018 Vol.6, №1. Р. 5.Norris MH, Khan MSR, Chirakul S, et al. Outer membrane vesicle vaccines from biosafe surrogates prevent acute lethal glanders in mice. Vaccine. 2018;6(1):5. doi: 10.3390/vaccines6010005Schild S., Nelson E.J., Camilli A. Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice // Infect Immun. 2008 Vol.76, №10. Р. 4554–4563.Schild S, Nelson EJ, Camilli A. Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect Immun. 2008;76(10):4554– 4563. doi: 10.1128/IAI.00532-08Roy N., Barman S., Ghosh A., et al. Immunogenicity and protective efficacy of Vibrio cholerae outer membrane vesicles in rabbit model // FEMS Immunol Med Microbiol. 2010 Vol 60, №1. Р.18–27.Roy N, Barman S, Ghosh A, et al. Immunogenicity and protective efficacy of Vibrio cholerae outer membrane vesicles in rabbit model. FEMS Immunol Med Microbiol. 2010;60(1):18–27. doi: 10.1111/j.1574-695X.2010.00692.xBishop A.L., Tarique A.A., Patimalla B., et al. Immunization of mice with Vibrio cholerae outer-membrane vesicles protects against hyperinfectious challenge and blocks transmission // Journal of Infectious Diseases. 2012 Vol.205, №3. Р.412–421.Bishop AL, Tarique AA, Patimalla B, et al. Immunization of mice with Vibrio cholerae outer-membrane vesicles protects against hyperinfectious challenge and blocks transmission. Journal of Infectious Diseases. 2012;205(3):412–421. doi: 10.1093/infdis/jir756Leitner D.R., Feichter S., Schild- Prüfert K., et al. Lipopolysaccharide modifications of a cholera vaccine candidate based on outer membrane vesicles reduce endotoxicity and reveal the major protective antigen // Infect Immun. 2013 Vol.81, №7. Р. 2379–2393.Leitner DR, Feichter S, Schild-Prüfert K, et al. Lipopolysaccharide modifications of a cholera vaccine candidate based on outer membrane vesicles reduce endotoxicity and reveal the major protective antigen. Infect Immun. 2013;81(7):2379–2393. doi: 10.1128/IAI.01382-12Leitner D.R., Lichtenegger S., Temel P., et al. A combined vaccine approach against Vibrio cholerae and ETEC based on outer membrane vesicles // Front Microbiol. 2015 Vol. 6. Р. 823.Leitner DR, Lichtenegger S, Temel P, et al. A combined vaccine approach against Vibrio cholerae and ETEC based on outer membrane vesicles. Front Microbiol. 2015;6:823. doi: 10.3389/fmicb.2015.00823

The authors declare that there are no conflicts of interest present.