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Interaction of bacterial extracellular microvesicles with eukaryotic cells.

https://doi.org/10.15789/1563-0625-IOB-2079

Abstract

Bacterial extracellular microvesicles (BMV) are formed by nonpathogenic, pathogenic and opportunistic bacteria. BMV are spherical bilayer-membrane organelles containing different cargoes: lipopolysaccharides, pathogen associated molecular patterns (PUMP), DNA, RNA, signal molecules, proteins, antibiotic resistance factors, virulence factors, toxins providing various immune response options and conducive to the survival and pathogen dissemination in the human body. BMVs secretion play an important role in the ability of microorganisms to cause various diseases. BMV are involved in biofilms formation, help bacteria to obtain nutrition in a nutrient-poor conditions, to evade the host's immune response, provide communication and surviving in a stressful environment during infection inside the host. The heterogeneity of the biogenesis mechanisms causes differences in the BMV and their characteristics including virulence rate. BMVs host cells entering is mediated by several mechanisms and helps to activate innate and adaptive immune reactions. This review focuses on interaction study of BMV with various eukaryotic cells types including neutrophils, dendritic cells, macrophages, epithelial, endothelial cells. This interaction depends on bacteria species, type of target cell and number of vesicles and can lead to different responses: non-immunogenic, pro-inflammatory, cytotoxic. Subcellular and molecular mechanisms related to the involvement of extracellular microvesicles in host's immune response modulation are presented. Stimulation of immune response is provided by increased secretion of proinflammatory cytokines and chemokines. In some cases BMV use mechanisms to evade immune surveillance: anti-inflammatory cytokines secretion, alterations of phagocytosis and chemotaxis of macrophages, increasing the proteolytic cleavage of CD14 on the macrophage surface, alterations of antigen-presenting function of dendritic cells, T-cell proliferation suppression, reducing the pro-inflammatory cytokines secretion, evasion of host-immune cells direct interactions, destruction of neutrophilic traps. These features allow bacterial cells to survive in the human body, increase their invasive potential, and reduce the excessive inflammatory reactions leading to death of the pathogen itself and life-threatening damage of tissues and organs of the host. Further studies of these mechanisms will improve existing therapeutic approaches to the infectious diseases treatment.

About the Authors

D. S. Shlykova
V.A. Negovsky Research Institute of General Reanimatology of Federal Research and Clinical Center of Intensive Care Medicine and Rehabilitology
Russian Federation

 Shlykova Darya S., Research Associate, Laboratory of Molecular Mechanisms of Critical Illness

107031, Moscow, Petrovka str., 25, bldg 2



V. M. Pisarev
V.A. Negovsky Research Institute of General Reanimatology of Federal Research and Clinical Center of Intensive Care Medicine and Rehabilitology; D. Rogachev Federal Research Clinical Center of Pediatric Hematology, Oncology and Immunology

Pisarev Vladimir M., PhD, MD (Medicine), Professor, Head, Laboratory of Molecular Mechanisms of Critical Illness V.A. Negovsky Research Institute of General Reanimatology of Federal Research and Clinical Center of Intensive Care Medicine and Rehabilitology; Leading Research Associate, D. Rogachev Medical Research Center of Pediatric Hematology, Oncology and Immunology

 



A. M. Gaponov
V.A. Negovsky Research Institute of General Reanimatology of Federal Research and Clinical Center of Intensive Care Medicine and Rehabilitology; D. Rogachev Federal Research Clinical Center of Pediatric Hematology, Oncology and Immunology

Gaponov Andrey M., PhD (Medicine), Head, Laboratory of Infection Immunology, D. Rogachev Federal Research Clinical Center of Pediatric Hematology, Oncology and Immunology; Leading Research Associate , Federal Research and Clinical Center of Intensive Care Medicine and Rehabilitology

 



A. V. Tutelyan
Central Research Institute of Epidemiology

Tutelyan Alexey V., PhD, MD (Medicine), Corresponding Member, Russian Academy of Sciences, Head, Laboratory of Healthcare-Associated Infections

 



References

1. Beloborodova N.B., Ostrova I.V. Sepsis-associated encephalopathy (Review). Obshchaya reanimatologiya = General Reanimatology, 2017, Vol. 13, no. 5, pp. 121-139. (In Russ.)

2. Kopitsyna M.N., Morozov A.S., Bessonov I.V., Pisarev V.M. Methods for Detection of Bacterial Endotoxin in Critical Care Medicine. Obshchaya reanimatologiya = General Reanimatology, 2017, Vol. 13, no. 5, pp. 109-120. (In Russ.)

3. Lusta K.A. Bacterial outer membrane nanovesicles: structure, biogenesis, functions, and application in biotechnology and medicine (Review). Prikladnaya biokhimiya i mikrobiologiya = Applied Biochemistry and Microbiology, 2015, Vol. 51, no. 5, pp. 485-493. (In Russ.)

4. Lusta K.A., Kozlovsky Yu.E. Outer membrane nanovesicles of gram-negative bacteria Aeromonas hydrophila and Aeromonas salmonicida. Mikrobiologiya = Microbiology, 2011, Vol. 80, no. 4, pp. 513-518. (In Russ.)

5. Lusta K.A., Kondashevskaya M.V. Bacterial outer membrane nanovesicles: involvement in pathogenesis. Vestnik novykh meditsinskikh tekhnologiy = Journal of New Medical Technologies, 2019, no. 2, pp. 148-157. (In Russ.)

6. Medvedeva E.S., Malygina T.Yu., Baranova N.B., Mouzykantov A.A., Davydova M.N., Chernova O.A., Chernov V.M. Adaptation of mycoplasmas to fluoroquinolones: modulation of proteome and genotoxicity of extracellular vesicles of acholeplasma laidlawii. Uchenye zapiski Kazanskogo universiteta = Uchenye Zapiski Kazanskogo Universiteta, 2017, Vol. 159, no. 2, pp. 248-261. (In Russ.)

7. Miller G.G., Mukhachev A.Ya., Bykovsky A.F. interconnection between cell microvesicular transport and pathogens persistence in vitro and in vivo. Mikrobiologiya = Microbiology, 2015, no. 4, pp. 63-70. (In Russ.)

8. Moroz V.V., Marchenko D.N., Skripkin Yu.V., Zabelina T.S., Ovezov A.M., Likhvantsev V.V. Perioperative predictors of unfavorable outcome of vascular surgery. Obshchaya reanimatologiya = General Reanimatology, 2017, Vol. 13, no. 3, pp. 6-12. (In Russ.)

9. Samoylova E.M., Kalsin V.A., Bespalova V.A., Devichensky V.M., Baklaushev V.P. Exosomes: from biology to clinics. Geny i kletki = Genes and Cells, 2107, Vol. 12, no. 4, pp. 7-19. (In Russ.)

10. Tyurin I.N., Avdeikin S.N., Protsenko D.N., Cherpakov R.A., Mullakaeva G.M., Kozlov I.A. Epidemiology of sepsis in patients admitted to the intensive care unit of a multi-specialty hospital (Experimental study). Obshchaya reanimatologiya = General Reanimatology, 2019, Vol. 15, no. 4, pp. 42-57. (In Russ.)

11. Chernov V.M., Chernova O.A., Sanchez-Vega C.T., Kolpakov A.I., Ilyinskaya O.N. Mycoplasma contamination of cell cultures: vesicular traffic in bacteria and infectogens control problems. Acta naturae, 2014, Vol. 6, no. 3 (22), pp. 43-54. (In Russ.)

12. Acevedo R., Fernández S., Zayas C., Acosta A., Sarmiento M.E., Ferro V.A., Rosenqvist E., Campa C., Cardoso D., Garcia L., Perez J.L. Bacterial outer membrane vesicles and vaccine applications. Front. Immunol., 2014, Vol. 5, 121. doi: 10.3389/fimmu.2014.00121.

13. Aldick T., Martina Bielaszewska M., Zhang W., Brockmeyer J., Schmidt H., Friedrich A.W., Kim K.S., Schmidt M.A., Karch H. Hemolysin from shiga toxin-negative Escherichia coli O26 strains injures microvascular endothelium. Microbes Infect., 2007, Vol. 9, no. 3, pp. 282-290.

14. Alvarez-Jiménez V.D., Leyva-Paredes K., Martínez M.G., Vázquez-Flores L., García-Paredes V.G., CampilloNavarro M., Romo-Cruz I., Rosales-García V.H., Castañeda-Casimiro J., González-Pozos S., Hernández J.M., Wong-Baeza C., García-Pérez B.E., Ortiz-Navarrete V., Estrada-Parra S., Serafín-López J., Wong-Baeza I., ChacónSalinas R., Estrada-García I.. Extracellular vesicles released from Mycobacterium tuberculosis-infected neutrophils promote macrophage autophagy and decrease intracellular mycobacterial survival. Front. Immunol., 2018, Vol. 9, 272. doi: 10.3389/fimmu.2018.00272.

15. Anand P.K., Anand E., Bleck C.K.E., Anes E., Griffiths G. Exosomal Hsp70 induces a pro-inflammatory response to foreign particles including mycobacteria. PLoS ONE, 2010, Vol. 5, no. 4, e10136. doi: 10.1371/journal.pone.0010136.

16. Askarian F., LapekJr J.D., Dongre M., Tsai C.M., Kumaraswamy M., Kousha A., Valderrama J.A., Ludviksen J.A., Cavanagh J.P., Uchiyama S., Mollnes T.E., Gonzalez D.J., Wai S.N., Nizet V., Johannessen M. Staphylococcus aureus membrane-derived vesicles promote bacterial virulence and confer protective immunity in murine infection models. Front. Microbiol., 2018, Vol. 9, 262. doi: 10.3389/fmicb.2018.0026.

17. Augustyniak D., Roszkowiak J., Wiśniewska I., Skała J., Gorczyca D., Drulis-Kawa Z. Neuropeptides SP and CGRP diminish the moraxella catarrhalis outer membrane vesicle-(OMV-) triggered inflammatory response of human A549 epithelial cells and neutrophils. Mediators Inflamm., 2018, Vol. 2018, pp. 4847205. doi: 10.1155/2018/4847205.

18. Avila-Calderón E.D., Araiza-Villanueva, M.G., Cancino-Diaz J.C., López-Villegas E.O., Sriranganathan N., Boyle S.M., Contreras-Rodríguez A. Roles of bacterial membrane vesicles. Arch. Microbiol., 2015, Vol. 197, no. 1, pp. 1-10.

19. Badi S.A., Khatami S., Irani S., Siadat S.D. Induction effects of bacteroides fragilis derived outer membrane vesicles on Toll like receptor 2, Toll like receptor 4 genes expression and cytokines concentration in human intestinal epithelial cells. Cell J., 2019, Vol. 21, no. 1, pp. 57-61.

20. Bauman S.J., Kuehn M.J. Pseudomonas aeruginosa vesicles associate with and are internalized by human lung epithelial cells. BMC Microbiol., 2009, Vol. 9, 26. doi: 10.1186/1471-2180-9-26.

21. Ben-Hur S., Biton M., Regev-Rudzki N. Extracellular vesicles: a prevalent tool for microbial gene delivery? Proteomics, 2019, Vol. 19, no. 1-2, e1800170. doi: 10.1002/pmic.201800170.

22. Bhatnagar S., Schorey J.S. Exosomes released from infected macrophages contain mycobacterium avium glycopeptidolipids and are proinflammatory. J. Biol. Chem., 2007, Vol. 282, no. 35, pp. 25779-25789.

23. Bhatnagar S., Shinagawa K., Castellino F.J., Schorey J.S. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood, 2007, Vol. 110, no. 9, pp. 3234-3244.

24. Bielaszewska M., Aldick T., Bauwens A., Karch H. Hemolysin of enterohemorrhagic Escherichia coli: Structure, transport, biological activity and putative role in virulence. Int. J. Med. Microb., 2014, Vol. 304, no. 5-6, pp. 521-529.

25. Bielaszewska M., Rüter C., Bauwens A., Greune L., Jarosch K.A., Steil D., ZhangW., He X., Lloubes R., Fruth A., Kim K.S., Schmidt A., Dobrindt U., Mellmann A., Karch H. 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., 2017, Vol. 13, no. 2, e1006159. doi: 10.1371/journal.ppat.1006159.

26. Bielaszewska M., Rüter C., Kunsmann L., Greune L., Bauwens A., Zhang W., Kuczius T., Kim K.S., Mellmann A., Schmidt M.A., Karch H. Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis. PLoS Pathog., 2013, Vol. 9, no. 12, e1003797. doi: 10.1371/journal.ppat.1003797.

27. Bishop D.G., Work E. An extracellular glycolipid produced by Escherichia coli grown under lysinelimiting conditions. Biochem. J., 1965, Vol. 96, pp. 567-576.

28. Bitto N.J., Baker P.J., Dowling J.K., Wray-McCann G., De Paoli A., Tran L.S., Leung P.L., Stacey K.J., Mansell A., Masters S.L., Ferrero R.L. Membrane vesicles from Pseudomonas aeruginosa activate the noncanonical inflammasome through caspase-5 in human monocytes. Immunol. Cell Biol., 2018, Vol. 96, no. 10, pp. 1120-1130.

29. Bonnington K.E., Kuehn M.J. Protein selection and export via outer membrane vesicles. Biochim. Biophys. Acta, 2014, Vol. 1843, no. 8, pp. 1612-1619.

30. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science, 2004, Vol. 303, no. 5663, pp. 1532-1535.

31. Caruana J.C., Scott A., Walper S.A. Bacterial membrane vesicles as mediators of microbe – microbe and microbe – host community interactions. Front. Microbiol., 2020, Vol. 11, 432. doi: 10.3389/fmicb.2020.00432.

32. Cecil J.D., Sirisaengtaksin N., O’Brien-Simpson N.M., Krachler A.M. Outer membrane vesicle – host cell interactions. Microbiol. Spectr., 2019, Vol. 7, no. 1, PSIB-0001-2018. doi: 10.1128/microbiolspec.PSIB-0001-2018.

33. Chatterjee D., Chaudhuri K. Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Lett., 2011, Vol. 585, pp. 1357-1362.

34. Choi J.W., Kim S.C., Hong S.H., Lee. H.J. Secretable small RNAs via outer membrane vesicles in periodontal pathogens. J. Dent. Res., 2017, Vol. 96, no. 4, pp. 458-466.

35. Codemo M., Muschiol S., Iovino F., Nannapaneni P., Plant L., Wai S.N., Henriques-Normark B. Immunomodulatory effects of pneumococcal extracellular vesicles on cellular and humoral host defenses. mBio, 2018, Vol. 9, no. 2, e00559-18. doi: 10.1128/mBio.00559-18.

36. Cooke A.C., Nello A.V., Ernst R.K., Schertzer J.W. Analysis of Pseudomonas aeruginosa biofilm membrane vesicles supports multiple mechanisms of biogenesis. PLoS ONE, 2019, Vol. 14, no. 2, e0212275. doi: 10.1371/journal.pone.0212275.

37. Dagnelie M.A., Corvec S., Khammari A., Dréno B. Bacterial extracellular vesicles: a new way to decipher host-microbiota communications in inflammatory dermatoses. Exp. Dermatol., 2020, Vol. 29, no. 1, pp. 22-28.

38. Davis J.M., Carvalho H.V., Rasmussen S.B., O’Brien A.D. Cytotoxic necrotizing factor type 1 delivered by outer membrane vesicles of uropathogenic Escherichia coli attenuates polymorphonuclear leukocyte antimicrobial activity and chemotaxis. Infect. Immun., 2006, Vol. 74, no. 8, pp. 4401-4408.

39. Deatherage B.L., Cookson B.T. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun., 2012, Vol. 80, no. 6, pp. 1948-1957.

40. Domingues S., Nielsen K.M. Membrane vesicles and horizontal gene transfer in prokaryotes. Curr. Opin. Microbiol., 2017, Vol. 38, pp. 16-21.

41. Dunn K.L., Virji M., Moxon E.R. Investigations into the molecular basis of meningococcal toxicity for human endothelial and epithelial cells: the synergistic effect of LPS and Pili. Microb. Pathog., 1995, Vol. 18, no. 2, pp. 81-96.

42. Duncan L., Yoshioka M., Chandad F., Grenier D. Loss of lipopolysaccharide receptor CD14 from the surface of human macrophage-like cells mediated by porphyromonas gingivalis outer membrane vesicles. Microb. Pathog., 2004, Vol. 36, no. 6, pp. 319-325.

43. Ellis T.N., Kuehn M.J. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev., 2010, Vol. 74, no. 1, pp. 81-94.

44. Ellis T.N., Leiman S.A., Kuehn. M.J. 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., 2010, Vol. 78, no. 9, pp. 3822-3831.

45. Finethy R., Luoma S., Orench-Rivera N., Feeley E.M., Haldar A.K., Yamamoto M., Kanneganti T.D., Kuehn M.J., Coers J. Inflammasome activation by bacterial outer membrane vesicles requires guanylate binding proteins. mBio, 2017, Vol. 8, no. 5, e01188-17. doi: 10.1128/mBio.01188-17.

46. Fischer S. Pattern recognition receptors and control of innate immunity: role of nucleic acids. Curr. Pharm. Biotechnol., 2018, Vol. 19, no. 15, pp. 1203-1209.

47. Fleming A., Sampey G., Chung M.C., Bailey C., van Hoek M.L., Kashanchi F., Hakami R.M. The carrying pigeons of the cell: exosomes and their role in infectious diseases caused by human pathogens. Pathog Dis., 2014, Vol. 71, no. 2, pp. 109-120.

48. Garcia K.C. Dual arms of adaptive immunity: division of labor and collaboration between B and T cells. Cell, 2019, Vol. 179, no. 1, pp. 3-7.

49. Gill S., Ryan Catchpole R., Forterre P. Extracellular membrane vesicles in the three domains of life and beyond. FEMS Microbiol Rev., 2019, Vol. 43, no. 3, pp. 273-303.

50. Giordano N.P., Cian M.B., Dalebroux Z.D. Outermembrane lipid secretion and the innate immune response to Gram-negative bacteria. Infect. Immun., 2020, IAI.00920-19. doi: 10.1128/iai.00920-19.

51. Giri P.K., Schorey J.S. Exosomes derived from M. Bovis BCG infected macrophages activate antigen-specific CD4+ and CD8+ T cells in vitro and in vivo. PLoS ONE, 2008, Vol. 3, no. 6, e2461. doi: 10.1371/journal.pone.0002461.

52. Go G., Lee J., Choi D.S., Kim S.S., Gho Y.S. Extracellular vesicle-mimetic ghost nanovesicles for delivering anti-inflammatory drugs to mitigate gram-negative bacterial outer membrane vesicle-induced systemic inflammatory response syndrome. Adv. Heaithc. Mater., 2019, Vol. 8, no. 4, e1801082. doi: 10.1002/adhm.201801082.

53. Guerrero-Mandujano A., Hernández-Cortez C.H., Ibarra J.A., Castro-Escarpulli G. The outer membrane vesicles: secretion system type zero. Traffic., 2017, Vol. 18, no. 7, pp. 425-432.

54. Guidi R., Levi L., Rouf S. F., Puiac S., Rhen M., Frisan T. Salmonella enterica delivers its genotoxin through outer membrane vesicles secreted from infected cells. Cell. Microbiol., 2013, Vol. 15, pp. 2034-2050.

55. Halász H., Ghadaksaz A.R., Madarász T., Huber K., Harami G., Tóth E.A., Osteikoetxea-Molnár A., Kovács M., Balogi Z., Nyitrai M., Matkó J., Szabó-Meleg E. Live cell superresolution-SIM imaging analysis of the intercellular transport of microvesicles and costimulatory proteins via nanotubes between immune cells. Methods Appl. Fluoresc., 2018, Vol. 6, no. 4, 045005. doi: 10.1088/2050-6120/aad57d.

56. Han E.C., Choi S.Y., Lee Y., Park J.W., Hong S.H., Lee H.J. Extracellular RNAs in periodontopathogenic outer membrane vesicles promote TNF-α production in human macrophages and cross the blood-brain barrier in mice. FASEB J., 2019, Vol. 33, no. 12, pp. 13412-13422.

57. Haurat M.F.,Aduse-Opoku J., Rangarajan M., Dorobantu L., Gray M.R.,Curtis M.A., Feldman M.F. Selective sorting of cargo proteins into bacterial membrane vesicles. J. Biol. Chem., 2011, Vol. 286, no. 2, pp. 1269-1276.

58. Hellenbrand K.M., Forsythe K.M., Rivera-Rivas J.J., Czuprynski C.J., Aulik N.A. Histophilus somni causes extracellular trap formation by bovine neutrophils and macrophages. Microb. Pathog., 2013, Vol. 54, pp. 67-75.

59. Ho M.H., Chen C.H., Goodwin J.S., Wang B.Y., Xie H. Functional advantages of porphyromonas gingivalis vesicles. PLoS ONE, 2015, Vol. 10, no. 4, e0123448. doi: 10.1371/journal.pone.0123448.

60. Ho M.H., Guo Z.M., Chunga J., Goodwin J.S., Xie H. Characterization of innate immune responses of human endothelial cells induced by porphyromonas gingivalis and their derived outer membrane vesicles. Front. Cell. Infect. Microbiol., 2016, Vol. 6, 139. doi: 10.3389/fcimb.2016.00139.

61. Hock B.D., McKenzie J., Keenan J.I. Helicobacter pylori outer membrane vesicles inhibit human T cell responses via induction of monocyte COX-2 expression. Pathog Dis., 2017, Vol. 75, no. 4. doi: 10.1093/femspd/ftx034.

62. Jan A.T. Outer membrane vesicles (OMVs) of gram-negative bacteria: a perspective update. Front. Microbiol., 2017, Vol. 8, 1053. doi: 10.3389/fmicb.2017.01053.

63. Jash E., Prasad P., Kumar N., Sharma T., Goldman A., Seema Sehrawat S. Perspective on nanochannels as cellular mediators in different disease conditions. Cell Commun. Signal., 2018, Vol. 16, 76. doi: 10.1186/s12964-018-0281-7.

64. Jensen P.E. Mechanisms of antigen presentation. Clin. Chem. Lab. Med., 1999, Vol. 37, no. 3, pp. 179-186.

65. Jun S.H., Lee J.H., Kim B.R., Kim S.I., Park T.I., Lee J.C., Lee Y.C. Acinetobacter baumannii outer membrane vesicles elicit a potent innate immune response via membrane proteins. PLoS ONE, 2013, Vol. 8, no. 8, e71751. doi: 10.1371/journal.pone.0071751.

66. Kadurugamuwa J.L., Beveridge T.J. Natural release of virulence factors in membrane vesicles byPseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release. J. Antimicrob. Chemother., 1997, Vol. 40, pp. 615-621.

67. Kaparakis-Liaskos M., Ferrero R.L. Immune modulation by bacterial outer membrane vesicles. Nat. Rev. Immunol., 2015, Vol. 15, no. 6, pp. 375-387.

68. Kaparakis M., Turnbull L., Carneiro L., Firth S., Coleman H. A., Parkington H.C., le Bourhis L., Karrar A., Viala J., Mak J., Hutton M.L., Davies J.K., Crack P.J., Hertzog P.J., Philpott D.J., Girardin S.E., Whitchurch C.B., Ferrero R.L. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell. Microbiol., 2010, Vol. 12, no. 3, pp. 372-385.

69. Keyel P.A., Heid M.E., Salter R.D. Macrophage responses to bacterial toxins: a balance between activation and suppression. Immunol. Res.,2011, Vol. 50. no. 2-3, pp. 118-123.

70. Kim J.H., Jeun E.J., Hong C.P., Kim S.H., Jang M.S., Lee E.J., Moon S.J., Yun C.H., Im S.H., Jeong S.G., Park B.Y., Kim K.T., Seoh J.Y., Kim Y.K., Oh S.J., Ham J.S., Yang B.G., Jang M.H. Extracellular vesicle-derived protein from bifidobacterium longum alleviates food allergy through mast cell suppression. J. Allergy Clin. Immunol., 2016, Vol. 137, no. 2, pp. 507-516.e8.

71. Kim J.H., Lee J., Park J., Gho Y.S. Gram-negative and Gram-positive bacterial extracellular vesicles. Semin. Cell Dev. Biol., 2015, Vol. 40, pp. 97-104.

72. 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 suppress tumor by interferon-γ-mediated antitumor response. Nat. Commun., 2017, Vol. 8, 626. doi: 10.1038/s41467-017-00729-8.

73. Kim J.H., Yoon Y.J., Lee J., Choi E.J., Yi N., Park K.S., Jaesung Park J., Lötvall J., Kim Y.K., Gho Y.S. Outer membrane vesicles derived from Escherichia coli up-regulate expression of endothelial cell adhesion molecules in vitro and in vivo. PLoS ONE, 2013, Vol. 8, no. 3, e59276. doi: 10.1371/journal.pone.0059276.

74. Kimura S., Hase K., Ohno H. The molecular basis of induction and formation of tunneling nanotubes. Cell Tissue Res., 2013, Vol. 352, no. 1, pp. 67-76.

75. 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 proteins induce human eosinophil degranulation via a β2 integrin CD11/CD18-and ICAM-1-dependent mechanism. Mediators Inflamm., 2015, Vol. 2015, 301716. doi: 10.1155/2015/301716.

76. Ko S.H., Rho D.J., Jeon J.I., Kim Y.J., Woo H.A., Kim N., Kim J.M. Crude Preparations of Helicobacter pylori outer membrane vesicles induce upregulation of heme oxygenase-1 via activating Akt-Nrf2 and mTOR-IκB kinaseNF-κB pathways in dendritic cells. Infect. Immun., 2016, Vol. 84, no. 8, pp. 2162-2174.

77. Kotsias F., Cebrian I., Alloatti A.Antigen processing and presentation. Int. Rev. Cell. Mol. Biol., 2019, Vol. 348, pp. 69-121.

78. Kulkarni H.M., Jagannadham M.V. Biogenesis and multifaceted roles of outer membrane vesicles from Gram-negative bacteria. Microbiology, 2014, Vol. 160, pp. 2109-2121.

79. Kulp A., Kuehn M.J. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol., 2010, Vol. 64, pp. 163-184.

80. Kunsmann L., Rüter C., Bauwens A., Greune L., Gluder M., Kemper B., et al. Virulence from vesicles: novel mechanisms of host cell injury by Escherichia coli O104:H4 outbreak strain. Sci. Rep., 2015, Vol. 5, 13252. doi: 10.1038/srep13252.

81. Lapinet J.A., Scapini P., Calzetti F., Pérez O., Cassatella M.A. Gene expression and production of tumor necrosis factor alpha, interleukin-1beta (IL-1beta), IL-8, macrophage inflammatory protein 1alpha (MIP1alpha), MIP-1beta, and gamma interferon-inducible protein 10 by human neutrophils stimulated with group B meningococcal outer membrane vesicles. Infect. Immun., 2000, Vol. 68, no. 12, pp. 6917-6923.

82. Laughlin R.C., Mickum M., Rowin K., Adams L.G., Alaniz. R.C. Altered host immune responses to membrane vesicles from salmonella and gram-negative pathogens. Vaccine, 2015, Vol. 33, no. 38, pp. 5012-5019.

83. Lee H.J. Microbe-host communication by small RNAs in extracellular vesicles: vehicles for transkingdom RNA transportation. Int. J. Mol. Sci., 2019, Vol. 20, no. 6, 1487. doi: 10.3390/ijms20061487.

84. Lee H.S.W., Boulton I.C., Reddin K., Wong H., Halliwell D., Mandelboim O., Gorringe A.R., Gray-Owen S.D. Neisserial outer membrane vesicles bind the coinhibitory receptor carcinoembryonic antigen-related cellular adhesion molecule 1 and suppress CD4+ T lymphocyte function. Infect Immun., 2007, Vol. 75. no. 9, pp. 4449-4455.

85. MacDonald I.A., Kuehn M.J. Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa. J. Bacteriol., 2013, Vol. 195, no. 13, pp. 2971-2981.

86. Maerz J.K., Steimle A., Lange A., Bender A., Fehrenbacher B., Frick J.S. Outer membrane vesicles blebbing contributes to B. vulgatus mpk-mediated immune response silencing. Gut Microbes., 2018, Vol. 9, no. 1, pp. 1-12.

87. Maldonado R., Wei R., Kachlany S.C., Kazi M., Balashova N.V. Cytotoxic effects of kingella kingae outer membrane vesicles on human cells. Microb. Pathog., 2011, Vol. 51, no. 1-2, pp. 22-30.

88. Mirlashari M.R., Hagberg I.A., Lyberg T. Platelet-platelet and platelet-leukocyte interactions induced by outer membrane vesicles from N. meningitidis. Platelets., 2002, Vol. 13, no. 2, pp. 91-99.

89. Mondal A., Tapader R., Chatterjee N.S., Ghosh A., Ritam Sinha R., Koley H., Saha D.R., Chakrabarti M.K., Wai S.N., Pal A. Cytotoxic and inflammatory responses induced by outer membrane vesicle-associated biologically active proteases from vibrio cholerae. Infect. Immun., 2016, Vol. 84, no. 5, pp. 1478-1490.

90. Nho J.S., Jun S.H., Oh M.H., Park T.I., Choi C.W., Kim S.I., Choi C.H., Lee J.C. Acinetobacter nosocomialis secretes outer membrane vesicles that induce epithelial cell death and host inflammatory responses. Microb. Pathog., 2015, Vol. 81, pp. 39-45.

91. Németh A., Orgovan N., Sódar B.W., Osteikoetxea X., Pálóczi K., Szabó-Taylor K.E., Vukman K., Kittel A., Turiák L., Wiener Z., Tóth S., Drahos L., Vékey K., Horvath R., Buzás I. Antibiotic-induced release of small extracellular vesicles (exosomes) with surface-associated DNA. Sci. Rep., 2017, Vol. 7, 8202. doi: 10.1038/s41598-017-08392-1.

92. Olsen I., Taubman M.A., Singhrao S.K. Porphyromonas gingivalis suppresses adaptive immunity in periodontitis, atherosclerosis, and Alzheimer’s disease. J. Oral Microbiol., 2016, Vol. 8, no. 1. doi: 10.3402/jom.v8.33029.

93. Önfelt B., Nedvetzki S., Benninger R.K.P., Purbhoo M.A., Sowinski S.,Hume A.N., Seabra M.C., Neil M.A.A., French P.M.W., Davis D.M. Structurally Distinct membrane nanotubes between human macrophages support longdistance vesicular traffic or surfing of bacteria. J. Immunol., 2006, Vol. 177, no. 12, pp. 8476-8483.

94. Osteikoetxea-Molnár A., Szabó-Meleg E., Tóth E.A., Oszvald A., Izsépi E., Kremlitzka M., Biri B., Nyitray L., Bozó T., Németh P., Kellermayer M., Nyitrai M., Matko J. The growth determinants and transport properties of tunneling nanotube networks between B lymphocytes. Cell Mol Life Sci., 2016, Vol. 73, no. 23, pp. 4531-4545.

95. Orench-Rivera N., Kuehn M.J. Environmentally controlled bacterial vesicle-mediated export. Cell. Microbiol., 2016, Vol. 18, no. 11, pp. 1525-1536.

96. Park K.S., Lee J., Lee C., Park H.T., Kim J.W., Kim O.Y., Kim S.R., Rådinger M., Jung H.Y., Park J., Lötvall J., Gho Y.S. Sepsis-like systemic inflammation induced by nano-sized extracellular vesicles from feces. Front. Microbiol., 2018, Vol. 9, 1735. doi: 10.3389/fmicb.2018.01735.

97. Paust S., Senman B., von Andrian U.H. Adaptive immune responses mediated by natural killer cells. Immunol. Rev., 2010, Vol. 235, no. 1, pp. 286-296.

98. Pathirana R., Kaparakis-Liaskos M. Bacterial membrane vesicles: biogenesis, immune regulation and pathogenesis. Cell. Microbiol., 2016, Vol. 18, no. 11, pp. 1518-1524.

99. Perez Vidakovics M.L., Jendholm J., Mörgelin M., Månsson A., Larsson C., Cardell L.O., Riesbeck K. B Cell activation by outer membrane vesicles – a novel virulence mechanism. PLoS Pathog., 2010, Vol. 6, no. 1, e1000724. doi: 10.1371/journal.ppat.1000724.

100. Pham K., Feik D., Hammond B.F., Rams T.E., Whitaker E.J. Aggregation of human platelets by gingipain-R from porphyromonas gingivalis cells and membrane vesicles. Platelets, 2002, Vol. 13, no. 1, pp. 21-30.

101. Plotnikov E.Y., Silachev D.N., Popkov V.A., Zorova L.D., Pevzner I.B., Zorov S.D., Jankauskas S.S., Babenko V.A., Sukhikh G.T., Zorov D.B. Intercellular signalling cross-talk: to kill, to heal and to rejuvenate. Heart Lung Circ., 2017, Vol. 26, no. 7, pp. 648-659.

102. Pollak C.N., Delpino M.V., Fossati C.A., Baldi P.C. Outer membrane vesicles from brucella abortus promote bacterial internalization by human monocytes and modulate their innate immune response. PLoS ONE, 2012, Vol. 7, no. 11, e50214. doi: 10.1371/journal.pone.0050214.

103. Qigui Y., Chow E.C., McCaw S.E., Hu N., Byrd D., Amet T., Hu S., Ostrowski M.A., Gray-Owen S.D. Association of neisseria gonorrhoeae opa(CEA) with dendritic cells suppresses their ability to elicit an HIV-1- specific T cell memory response. PLoS ONE, 2013, Vol. 8, no. 2, e56705. doi: 10.1371/journal.pone.0056705.

104. Rada B. Neutrophil extracellular traps. Meth. Mol. Biol., 2019, Vol. 1982, pp. 517-528.

105. Raposo G., Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell. Biol., 2013, Vol. 200, no. 4, pp. 373-383.

106. Resch U., Tsatsaronis J.A., Le Rhun A., Stübiger G., Rohde M., Kasvandik S. A two-component regulatory system impacts extracellular membrane-derived vesicle production in group A streptococcus. MBio, 2016, Vol. 7, e00207-16. doi: 10.1128/mBio.00207-16.

107. Rivera J., Cordero R.J.B., Nakouzi A.S., Frases S., Nicola A., Casadevall A. Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc. Natl. Acad. Sci. USA., 2010, Vol. 107, no. 44, pp. 19002-19007.

108. Roche P.A., Cresswell P. Antigen processing and presentation mechanisms in myeloid cells. Microbiol. Spectr., 2016, Vol. 4, no. 3. doi: 10.1128/microbiolspec.MCHD-0008-2015.

109. Rodrigues M., Fan J., Lyon C., Wan M., Hu Y. Role of extracellular vesicles in viral and bacterial infections: pathogenesis, diagnostics, and therapeutics. Theranostics, 2018, Vol. 8, no. 10, pp. 2709-2721.

110. Satarian F., Nejadsattari T., Vaziri F., Davar Siadat S.D. Comparative study of immune responses elicited by outer membrane vesicles of different pseudomonas aeruginosa strains. Comp. Immunol. Microbiol. Infect. Dis., 2019, Vol. 66, 101328. doi: 10.1016/j.cimid.2019.101328.

111. Schaar V., de Vries S.P.W., Vidakovics M., Bootsma H.J., Larsson L., Hermans P.W.M. Multicomponent Moraxella catarrhalis outer membrane vesicles induce an inflammatory response and are internalized by human epithelial cells. Cell. Microbiol., 2010, Vol. 13, pp. 432-449.

112. Schertzer J.W., Whiteley M. Bacterial outer membrane vesicles in trafficking, communication and the hostpathogen interaction. J. Mol. Microbiol. Biotechnol., 2013, Vol. 23, no. 1-2, pp. 118-130.

113. Schetters S.T.T., Jong W.S.P., Horrevorts S.K.,Kruijssen L.J.W., Engels S., Stolk D., Daleke-Schermerhorn M.H., Vallejo J.G., Houben D., Unger W.W.J., Den Haan J.M.M., Luirink J., Van Kooyk Y. Outer membrane vesicles engineered to express membrane-bound antigen program dendritic cells for cross-presentation to CD8+ T cells. Acta Biomater., 2019, Vol. 91, pp. 248-257.

114. Schwechheimer C., Kuehn M.J. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat. Rev. Microbiol., 2015, Vol. 13. no. 10, pp. 605-619.

115. Schwechheimer C., Kulp A., Kuehn M.J. Modulation of bacterial outer membrane vesicle production by envelope structure and content. BMC Microbiol., 2014, Vol. 14, 324. doi: 10.1186/s12866-014-0324-1.

116. Schorey J.S., Cheng Y., Singh P.S., Smit V.L. Exosomes and other extracellular vesicles in host-pathogen. EMBO Rep., 2015, Vol. 16, no. 1, pp. 24-43.

117. Schorey J.S., Harding C.V. Extracellular vesicles and infectious diseases: new complexity to an old story. J. Clin. Invest., 2016, Vol. 126, no. 4, pp. 1181-1189.

118. Sharma A., Novak E.K., Sojar H.T., Swank R.T., Kuramitsu H.K., Genco R.J. Porphyromonas gingivalis platelet aggregation activity: outer membrane vesicles are potent activators of murine platelets. Oral Microbiol. Immunol., 2000, Vol. 15, no. 6, pp. 393-396.

119. Sheerin D., O’Connor D., Dold C., Clutterbuck E., Attar M., Rollier C.S., Sadarangani M., Pollard A.J. Comparative transcriptomics between species attributes reactogenicity pathways induced by the capsular group B meningococcal vaccine, 4CMenB, to the membrane-bound endotoxin of its outer membrane vesicle component. Sci. Rep., 2019, Vol. 9, 13797. doi: 10.1038/s41598-019-50310-0.

120. Sheldon I.M., Owens S.E., Lloyd Turner M. Innate immunity and the sensing of infection, damage and danger in the female genital tract. J. Reprod. Immunol., 2017, Vol. 119, pp. 67-73.

121. Shen Y., Giardino Torchia M.L., Lawson G.W., Karp C.L., Ashwell J.D. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe, 2012, Vol. 12, pp. 509-520.

122. Shoberg R.J., Thomas D.D. Specific adherence of borrelia burgdorferi extracellular vesicles to human endothelial cells in culture. Infect. Immun., 1993, Vol. 61, no. 9, pp. 3892-3900.

123. Singhrao S.K., Olsen I. Are porphyromonas gingivalis outer membrane vesicles microbullets for sporadic Alzheimer’s disease manifestation? J. Alzheimers Dis. Rep., 2018, Vol. 2, no. 1, pp. 219-228.

124. Soult M.C.,Dobrydneva Y.,Wahab K.H., Britt L.D., Sullivan C.J. Outer membrane vesicles alter inflammation and coagulation mediators. J. Surg. Res., 2014, Vol. 192, no. 1, pp. 134-142.

125. Soult M.C., Lonergan N.E., Shah B., Kim W.K., Britt L.D., Sullivan C.J. Outer membrane vesicles from pathogenic bacteria initiate an inflammatory response in human endothelial cells. J. Surg. Res., 2013, Vol. 184, no. 1, pp. 458-466.

126. Srisatjaluk R., Doyle R.J., Justus D.E. Outer membrane vesicles of porphyromonas gingivalis inhibit IFNgamma-mediated MHC class II expression by human vascular endothelial cells. Microb. Pathog., 1999, Vol. 27, no. 2, pp. 81-91.

127. Thay B., Damm A., Kufer T.A., Wai S.N., Oscarsson J. Aggregatibacter actinomycetemcomitans outer membrane vesicles are internalized in human host cells and trigger NOD1-and NOD2-dependent NF-κB activation. Infect. Immun., 2014, Vol. 82, no. 10, pp. 4034-4046.

128. Toyofuku M., Nomura N. What will membrane vesicles (MVs) bring to bacterial communication? Microbes Environ., 2017, Vol. 32, no. 3, pp. 185-187.

129. Toyofuku M., Nomura N., Eberl L. Types and origins of bacterial membrane vesicles. Nat. Rev. Microbiol., 2019, Vol. 17, no. 1, pp. 13-24.

130. Tran F., Boedicker J.Q. Genetic cargo and bacterial species set the rate of vesicle-mediated horizontal gene transfer. Sci. Rep., 2017, Vol. 7, 8813. doi: 10.1038/s41598-017-07447-7.

131. Turnbull L., Toyofuku M., Hynen A.L., Kurosawa M., Pessi G., Petty N.K., Osvath S.R., Cárcamo-Oyarce G., Gloag E.S., Shimoni R., Omasits U., Ito S.,Yap X., Monahan L.G.,Cavaliere R.,Ahrens C.H.,Charles I.G., Nomura N., Eberl L., Whitchurch C.B. Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat. Commun., 2016, Vol. 7, 11220. doi: 10.1038/ncomms11220.

132. Turner L., Bitto N.J., Steer D.L., Lo C., D’Costa K., Ramm G., Shambrook M., Hill A.F., Ferrero R.L., Kaparakis-Liaskos M. Helicobacter pylori outer membrane vesicle size determines their mechanisms of host cell entry and protein content. Front. Immunol., 2018, Vol. 9, 1466. doi: 10.3389/fimmu.2018.01466.

133. Uhlmann J., Rohde M., Siemens N., Kreikemeyer B., Bergman P., Johansson L., Norrby-Teglund A. LL-37 triggers formation of streptococcus pyogenes extracellular vesicle-like structures with immune stimulatory properties. J. Innate Immun., 2016, Vol. 8, no. 3, pp. 243-257.

134. Vanaja S.K., Russo A.J., Behl B., Banerjee I., Yankova M., Deshmukh S.D., Rathinam V.A.K. Bacterial outer membrane vesicles mediate cytosolic localization of lps and caspase-11 activation. Cell, 2016, Vol. 165, no. 5, pp. 1106-1119.

135. van Bergenhenegouwen J., Kraneveld A.D., Rutten L., Kettelarij N., Garssen J., Vos A.P. Extracellular vesicles modulate host-microbe responses by altering TLR2 activity and phagocytosis. PLoS ONE, 2014, Vol. 9, no. 2, e89121. doi: 10.1371/journal.pone.0089121.

136. Velimirov B., Ranftler C. Unexpected aspects in the dynamics of horizontal gene transfer of prokaryotes: The impact of outer membrane vesicles. Wien Med Wochenschr., 2018, Vol. 168, no. 11, pp. 307-313.

137. Wang J., Yao Y., Chen X., Wu J., Gu T., Tang X. Host derived exosomes-pathogens interactions: potential functions of exosomes in pathogen infection. Biomed. Pharmacoter., 2018, Vol. 108, pp. 1451-1459.

138. Wang J., YaoY., Xiong J., Wu J., Tang X., Li G. Evaluation of the inflammatory response in macrophages stimulated with exosomes secreted by Mycobacterium avium-infected macrophages. Biomed. Res. Int., 2015, Vol. 2015, 658421. doi: 10.1155/2015/658421.

139. Winter J., Letley D., Rhead J., Atherton J., Robinson K. Helicobacter pylori membrane vesicles stimulate innate pro-and anti-inflammatory responses and induce apoptosis in Jurkat T cells. Infect. Immun., 2014, Vol. 82, no. 4, pp. 1372-1381.

140. Yu H., Kim K.S. YgfZ contributes to secretion of cytotoxic necrotizing factor 1 into outer-membrane vesicles in Escherichia coli. Microbiology, 2012, Vol. 158, Pt 3, pp. 612-621.

141. Yu Y.J., Wang X.H., Fan C.G. Versatile effects of bacterium-released membrane vesicles on mammalian cells and infectious/inflammatory diseases. Acta Pharmacol. Sin., 2018, Vol. 39, no. 4, pp. 514-533.

142. Yoon H. Bacterial outer membrane vesicles as a delivery system for virulence regulation. J. Microbiol. Biotechnol., 2016, Vol. 26, no. 8, pp. 1343-1347.

143. Yuana Y., Sturk A., Nieuwland R. Extracellular vesicles in physiological and pathological conditions. Blood Rev., 2013, Vol. 27, no. 1, pp. 31-39.

144. Zariri A., van Dijken H., Hamstra H.J., van der Flier M., Vidarsson G., Van Putten J.M.P., Boog C.J.P., van den Dobbelsteen G., van der Ley P. Expression of human CEACAM1 in transgenic mice limits the opa-specific immune response against meningococcal outer membrane vesicles.Vaccine, 2013, Vol. 31, no. 47, pp. 5585-5593.

145. Zhang B., Yin Y., Lai R.C., Lim S.K. Immunotherapeutic potential of extracellular vesicles. Front. Immunol., 2014, Vol. 5, 518. doi: 10.3389/fimmu.2014.00518.

146. Zhu W., Tomberg J., Knilans K.J., Anderson J.E., McKinnon K.P., Sempowski G.D., Nicholas R.A., Duncan J.A. Properly folded and functional PorB from neisseria gonorrhoeae inhibits dendritic cell stimulation of CD4+ T cell proliferation. J. Biol. Chem., 2018, Vol. 293, no. 28, pp. 11218-11229.


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Shlykova D.S., Pisarev V.M., Gaponov A.M., Tutelyan A.V. Interaction of bacterial extracellular microvesicles with eukaryotic cells. Medical Immunology (Russia). 2020;22(6):1065-1084. (In Russ.) https://doi.org/10.15789/1563-0625-IOB-2079

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