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Chapter 17 : Outer Membrane Vesicle-Host Cell Interactions

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Abstract:

Outer membrane vesicles (OMVs) are nanosized, spherical proteoliposomes. They are secreted via vesiculation of the outer membrane by Gram-negative bacteria as part of the normal growth process ( ). OMVs play diverse roles in intracellular communication, microbial virulence, and modulation of the host immune response ( ).

Citation: Cecil J, Sirisaengtaksin N, O’Brien-Simpson N, Krachler A. 2019. Outer Membrane Vesicle-Host Cell Interactions, p 201-214. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0001-2018
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Figures

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Figure 1

Structure and composition of bacterial OMVs. Examples of purified OMVs isolated from , , and . OMVs were purified using an optiprep gradient and visualized using cryo-transmission electron microscopy as previously described ( ). Scale bars, 200 nm. Typical composition of bacterial OMVs.

Citation: Cecil J, Sirisaengtaksin N, O’Brien-Simpson N, Krachler A. 2019. Outer Membrane Vesicle-Host Cell Interactions, p 201-214. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0001-2018
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Image of Figure 2
Figure 2

A summary of OMV interactions within gingival tissues. Bacteria accrete on the tooth’s surface and form a bacterial (plaque) biofilm that is adjacent to the epithelial cells in the gingival (gum) tissue. OMVs secreted from bacteria in this plaque biofilm bind to and penetrate into the mucosal tissue and generate host cell interactions and responses. These responses culminate in a chronic inflammatory response resulting in osteoclast activation which, in turn, promotes bone resorption and eventual tooth loss.

Citation: Cecil J, Sirisaengtaksin N, O’Brien-Simpson N, Krachler A. 2019. Outer Membrane Vesicle-Host Cell Interactions, p 201-214. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0001-2018
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Figure 3

Summary of OMV interactions with the gastrointestinal tract. Environmental pressures, such as low pH, mucin, or peptides or overgrowth of certain bacteria, result in the release of OMVs in the gastric lumen. These OMVs are able to penetrate the mucosal barrier and via different mechanisms adhere to and interact with the underlying epithelial cell and immune cells, inducing homeostasis or pathology.

Citation: Cecil J, Sirisaengtaksin N, O’Brien-Simpson N, Krachler A. 2019. Outer Membrane Vesicle-Host Cell Interactions, p 201-214. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0001-2018
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References

/content/book/10.1128/9781683670285.chap17
1. Beveridge TJ . 1999. Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181 : 4725 4733.[PubMed]
2. Kuehn MJ,, Kesty NC . 2005. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19 : 2645 2655.[CrossRef][PubMed]
3. Nakao R,, Hasegawa H,, Ochiai K,, Takashiba S,, Ainai A,, Ohnishi M,, Watanabe H,, Senpuku H . 2011. Outer membrane vesicles of Porphyromonas gingivalis elicit a mucosal immune response. PLoS One 6 : e26163.[CrossRef][PubMed]
4. Grenier D,, Mayrand D . 1987. Functional characterization of extracellular vesicles produced by Bacteroides gingivalis. Infect Immun 55 : 111 117.[PubMed]
5. Haurat MF,, Aduse-Opoku J,, Rangarajan M,, Dorobantu L,, Gray MR,, Curtis MA,, Feldman MF . 2011. Selective sorting of cargo proteins into bacterial membrane vesicles. J Biol Chem 286 : 1269 1276.[CrossRef][PubMed]
6. Veith PD,, Chen Y-Y,, Gorasia DG,, Chen D,, Glew MD,, O’Brien-Simpson NM,, Cecil JD,, Holden JA,, Reynolds EC . 2014. Porphyromonas gingivalis outer membrane vesicles exclusively contain outer membrane and periplasmic proteins and carry a cargo enriched with virulence factors. J Proteome Res 13 : 2420 2432.[CrossRef][PubMed]
7. Friedrich V,, Gruber C,, Nimeth I,, Pabinger S,, Sekot G,, Posch G,, Altmann F,, Messner P,, Andrukhov O,, Schäffer C . 2015. Outer membrane vesicles of Tannerella forsythia: biogenesis, composition, and virulence. Mol Oral Microbiol 30 : 451 473.[CrossRef][PubMed]
8. Zhou L,, Srisatjaluk R,, Justus DE,, Doyle RJ . 1998. On the origin of membrane vesicles in gram-negative bacteria. FEMS Microbiol Lett 163 : 223 228.[CrossRef][PubMed]
9. Grenier D . 2013. Porphyromonas gingivalis outer membrane vesicles mediate coaggregation and piggybacking of Treponema denticola and Lachnoanaerobaculum saburreum. Int J Dent 2013 : 305476.[CrossRef][PubMed]
10. McBroom AJ,, Kuehn MJ . 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Microbiol 63 : 545 558.[CrossRef][PubMed]
11. Roier S,, Zingl FG,, Cakar F,, Durakovic S,, Kohl P,, Eichmann TO,, Klug L,, Gadermaier B,, Weinzerl K,, Prassl R,, Lass A,, Daum G,, Reidl J,, Feldman MF,, Schild S . 2016. A novel mechanism for the biogenesis of outer membrane vesicles in Gram-negative bacteria. Nat Commun 7 : 10515.[CrossRef][PubMed]
12. Turnbull L,, Toyofuku M,, Hynen AL,, Kurosawa M,, Pessi G,, Petty NK,, Osvath SR,, Cárcamo-Oyarce G,, Gloag ES,, Shimoni R,, Omasits U,, Ito S,, Yap X,, Monahan LG,, Cavaliere R,, Ahrens CH,, Charles IG,, Nomura N,, Eberl L,, Whitchurch CB . 2016. Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat Commun 7 : 11220.[CrossRef][PubMed]
13. Schooling SR,, Beveridge TJ . 2006. Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188 : 5945 5957.[CrossRef][PubMed]
14. Yonezawa H,, Osaki T,, Kurata S,, Fukuda M,, Kawakami H,, Ochiai K,, Hanawa T,, Kamiya S . 2009. Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol 9 : 197.[CrossRef][PubMed]
15. Tashiro Y,, Ichikawa S,, Shimizu M,, Toyofuku M,, Takaya N,, Nakajima-Kambe T,, Uchiyama H,, Nomura N . 2010. Variation of physiochemical properties and cell association activity of membrane vesicles with growth phase in Pseudomonas aeruginosa. Appl Environ Microbiol 76 : 3732 3739.[CrossRef]
16. McCaig WD,, Koller A,, Thanassi DG . 2013. Production of outer membrane vesicles and outer membrane tubes by Francisella novicida. J Bacteriol 195 : 1120 1132.[CrossRef][PubMed]
17. Ellis TN,, Kuehn MJ . 2010. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 74 : 81 94.[CrossRef][PubMed]
18. McKee AS,, McDermid AS,, Baskerville A,, Dowsett AB,, Ellwood DC,, Marsh PD . 1986. Effect of hemin on the physiology and virulence of Bacteroides gingivalis W50. Infect Immun 52 : 349 355.[PubMed]
19. Smalley JW,, Birss AJ,, McKee AS,, Marsh PD . 1991. Haemin-restriction influences haemin-binding, haemagglutination and protease activity of cells and extracellular membrane vesicles of Porphyromonas gingivalis W50. FEMS Microbiol Lett 69 : 63 67.[CrossRef][PubMed]
20. Bauwens A,, Kunsmann L,, Marejková M,, Zhang W,, Karch H,, Bielaszewska M,, Mellmann A . 2017. Intrahost milieu modulates production of outer membrane vesicles, vesicle-associated Shiga toxin 2a and cytotoxicity in Escherichia coli O157:H7 and O104:H4. Environ Microbiol Rep 9 : 626 634.[CrossRef][PubMed]
21. Macdonald IA,, Kuehn MJ . 2013. Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa. J Bacteriol 195 : 2971 2981.[CrossRef][PubMed]
22. Marisa Heredia R,, Sabrina Boeris P,, Sebastián Liffourrena A,, Fernanda Bergero M,, Alberto López G,, Inés Lucchesi G . 2016. Release of outer membrane vesicles in Pseudomonas putida as a response to stress caused by cationic surfactants. Microbiology 162 : 813 822.[CrossRef][PubMed]
23. Kulp A,, Kuehn MJ . 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64 : 163 184.[CrossRef][PubMed]
24. Song T,, Mika F,, Lindmark B,, Liu Z,, Schild S,, Bishop A,, Zhu J,, Camilli A,, Johansson J,, Vogel J,, Wai SN . 2008. A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles. Mol Microbiol 70 : 100 111.[CrossRef][PubMed]
25. Collins BS . 2011. Gram-negative outer membrane vesicles in vaccine development. Discov Med 12 : 7 15.[PubMed]
26. Cecil JD,, O’Brien-Simpson NM,, Lenzo JC,, Holden JA,, Chen YY,, Singleton W,, Gause KT,, Yan Y,, Caruso F,, Reynolds EC . 2016. Differential responses of pattern recognition receptors to outer membrane vesicles of three periodontal pathogens. PLoS One 11 : e0151967.[CrossRef][PubMed]
27. Wieser A,, Storz E,, Liegl G,, Peter A,, Pritsch M,, Shock J,, Wai SN,, Schubert S . 2014. Efficient quantification and characterization of bacterial outer membrane derived nano-particles with flow cytometric analysis. Int J Med Microbiol 304 : 1032 1037.[CrossRef][PubMed]
28. O’Donoghue EJ,, Sirisaengtaksin N,, Browning DF,, Bielska E,, Hadis M,, Fernandez-Trillo F,, Alderwick L,, Jabbari S,, Krachler AM . 2017. Lipopolysaccharide structure impacts the entry kinetics of bacterial outer membrane vesicles into host cells. PLoS Pathog 13 : e1006760.[CrossRef][PubMed]
29. O’Donoghue EJ,, Krachler AM . 2016. Mechanisms of outer membrane vesicle entry into host cells. Cell Microbiol 18 : 1508 1517.[CrossRef][PubMed]
30. Oliver RC,, Brown LJ . 1993. Periodontal diseases and tooth loss. Periodontol 2000 2 : 117 127.[CrossRef][PubMed]
31. Shaddox LM,, Walker CB . 2010. Treating chronic periodontitis: current status, challenges, and future directions. Clin Cosmet Investig Dent 2 : 79 91.[CrossRef][PubMed]
32. Kim J,, Amar S . 2006. Periodontal disease and systemic conditions: a bidirectional relationship. Odontology 94 : 10 21.[CrossRef][PubMed]
33. Linden GJ,, Lyons A,, Scannapieco FA . 2013. Periodontal systemic associations: review of the evidence. J Periodontol 84( Suppl) : S8 S19.[CrossRef][PubMed]
34. Aas JA,, Paster BJ,, Stokes LN,, Olsen I,, Dewhirst FE . 2005. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43 : 5721 5732.[CrossRef][PubMed]
35. Paster BJ,, Olsen I,, Aas JA,, Dewhirst FE . 2006. The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol 2000 42 : 80 87.[CrossRef][PubMed]
36. Socransky SS,, Haffajee AD,, Cugini MA,, Smith C,, Kent RL Jr . 1998. Microbial complexes in subgingival plaque. J Clin Periodontol 25 : 134 144.[CrossRef][PubMed]
37. Haffajee AD,, Cugini MA,, Tanner A,, Pollack RP,, Smith C,, Kent RL Jr,, Socransky SS . 1998. Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J Clin Periodontol 25 : 346 353.[CrossRef][PubMed]
38. Byrne SJ,, Dashper SG,, Darby IB,, Adams GG,, Hoffmann B,, Reynolds EC . 2009. Progression of chronic periodontitis can be predicted by the levels of Porphyromonas gingivalis and Treponema denticola in subgingival plaque. Oral Microbiol Immunol 24 : 469 477.[CrossRef][PubMed]
39. Holt SC,, Ebersole J,, Felton J,, Brunsvold M,, Kornman KS . 1988. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science 239 : 55 57.[CrossRef][PubMed]
40. Ho M-H,, Chen C-H,, Goodwin JS,, Wang B-Y,, Xie H . 2015. Functional advantages of Porphyromonas gingivalis vesicles. PLoS One 10 : e0123448.[CrossRef][PubMed]
41. Sheets SM,, Robles-Price AG,, McKenzie RM,, Casiano CA,, Fletcher HM . 2008. Gingipain-dependent interactions with the host are important for survival of Porphyromonas gingivalis. Front Biosci 13 : 3215 3238.[CrossRef][PubMed]
42. O’Brien-Simpson NM,, Veith PD,, Dashper SG,, Reynolds EC . 2003. Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr Protein Pept Sci 4 : 409 426.[CrossRef]
43. Li N,, Collyer CA . 2011. Gingipains from Porphyromonas gingivalis—complex domain structures confer diverse functions. Eur J Microbiol Immunol 1 : 41 58.[CrossRef][PubMed]
44. Pathirana RD,, O’Brien-Simpson NM,, Brammar GC,, Slakeski N,, Reynolds EC . 2007. Kgp and RgpB, but not RgpA, are important for Porphyromonas gingivalis virulence in the murine periodontitis model. Infect Immun 75 : 1436 1442.[CrossRef][PubMed]
45. Pathirana RD,, O’Brien-Simpson NM,, Reynolds EC . 2010. Host immune responses to Porphyromonas gingivalis antigens. Periodontol 2000 52 : 218 237.[CrossRef][PubMed]
46. Inagaki S,, Onishi S,, Kuramitsu HK,, Sharma A . 2006. Porphyromonas gingivalis vesicles enhance attachment, and the leucine-rich repeat BspA protein is required for invasion of epithelial cells by “ Tannerella forsythia.” Infect Immun 74 : 5023 5028.[CrossRef][PubMed]
47. Yoshimura M,, Ohara N,, Kondo Y,, Shoji M,, Okano S,, Nakano Y,, Abiko Y,, Nakayama K . 2008. Proteome analysis of Porphyromonas gingivalis cells placed in a subcutaneous chamber of mice. Oral Microbiol Immunol 23 : 413 418.[CrossRef][PubMed]
48. Veith PD,, Chen YY,, Chen D,, O’Brien-Simpson NM,, Cecil JD,, Holden JA,, Lenzo JC,, Reynolds EC . 2015. Tannerella forsythia outer membrane vesicles are enriched with substrates of the type IX secretion system and TonB-dependent receptors. J Proteome Res 14 : 5355 5366.[CrossRef][PubMed]
49. Dane KY,, Nembrini C,, Tomei AA,, Eby JK,, O’Neil CP,, Velluto D,, Swartz MA,, Inverardi L,, Hubbell JA . 2011. Nano-sized drug-loaded micelles deliver payload to lymph node immune cells and prolong allograft survival. J Control Release 156 : 154 160.[CrossRef][PubMed]
50. Chi B,, Qi M,, Kuramitsu HK . 2003. Role of dentilisin in Treponema denticola epithelial cell layer penetration. Res Microbiol 154 : 637 643.[CrossRef][PubMed]
51. Galka F,, Wai SN,, Kusch H,, Engelmann S,, Hecker M,, Schmeck B,, Hippenstiel S,, Uhlin BE,, Steinert M . 2008. Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun 76 : 1825 1836.[CrossRef][PubMed]
52. Bomberger JM,, Maceachran DP,, Coutermarsh BA,, Ye S,, O’Toole GA,, Stanton BA . 2009. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 5 : e1000382.[CrossRef][PubMed]
53. Furuta N,, Tsuda K,, Omori H,, Yoshimori T,, Yoshimura F,, Amano A . 2009. Porphyromonas gingivalis outer membrane vesicles enter human epithelial cells via an endocytic pathway and are sorted to lysosomal compartments. Infect Immun 77 : 4187 4196.[CrossRef][PubMed]
54. Srisatjaluk R,, Kotwal GJ,, Hunt LA,, Justus DE . 2002. Modulation of gamma interferon-induced major histocompatibility complex class II gene expression by Porphyromonas gingivalis membrane vesicles. Infect Immun 70 : 1185 1192.[CrossRef][PubMed]
55. Tsuda K,, Amano A,, Umebayashi K,, Inaba H,, Nakagawa I,, Nakanishi Y,, Yoshimori T . 2005. Molecular dissection of internalization of Porphyromonas gingivalis by cells using fluorescent beads coated with bacterial membrane vesicle. Cell Struct Funct 30 : 81 91.[CrossRef][PubMed]
56. Gui MJ,, Dashper SG,, Slakeski N,, Chen YY,, Reynolds EC . 2016. Spheres of influence: Porphyromonas gingivalis outer membrane vesicles. Mol Oral Microbiol 31 : 365 378.[CrossRef][PubMed]
57. Amano A,, Kuboniwa M,, Takeuchi H . 2014. Transcellular invasive mechanisms of Porphyromonas gingivalis in host-parasite interactions. J Oral Biosci 56 : 58 62.[CrossRef]
58. Furuta N,, Takeuchi H,, Amano A . 2009. Entry of Porphyromonas gingivalis outer membrane vesicles into epithelial cells causes cellular functional impairment. Infect Immun 77 : 4761 4770.[CrossRef][PubMed]
59. Nakao R,, Takashiba S,, Kosono S,, Yoshida M,, Watanabe H,, Ohnishi M,, Senpuku H . 2014. Effect of Porphyromonas gingivalis outer membrane vesicles on gingipain-mediated detachment of cultured oral epithelial cells and immune responses. Microbes Infect 16 : 6 16.[CrossRef][PubMed]
60. Jarnbring F,, Somogyi E,, Dalton J,, Gustafsson A,, Klinge B . 2002. Quantitative assessment of apoptotic and proliferative gingival keratinocytes in oral and sulcular epithelium in patients with gingivitis and periodontitis. J Clin Periodontol 29 : 1065 1071.[CrossRef][PubMed]
61. Arce RM,, Tamayo O,, Cortés A . 2007. Apoptosis of gingival fibroblasts in periodontitis. Colomb Med 38 : 197 209.
62. Fenno JC,, Hannam PM,, Leung WK,, Tamura M,, Uitto VJ,, McBride BC . 1998. Cytopathic effects of the major surface protein and the chymotrypsinlike protease of Treponema denticola. Infect Immun 66 : 1869 1877.[PubMed]
63. Tanabe S,, Bodet C,, Grenier D . 2008. Treponema denticola lipooligosaccharide activates gingival fibroblasts and upregulates inflammatory mediator production. J Cell Physiol 216 : 727 731.[CrossRef][PubMed]
64. Bartruff JB,, Yukna RA,, Layman DL . 2005. Outer membrane vesicles from Porphyromonas gingivalis affect the growth and function of cultured human gingival fibroblasts and umbilical vein endothelial cells. J Periodontol 76 : 972 979.[CrossRef][PubMed]
65. Jia Y,, Guo B,, Yang W,, Zhao Q,, Jia W,, Wu Y . 2015. Rho kinase mediates Porphyromonas gingivalis outer membrane vesicle-induced suppression of endothelial nitric oxide synthase through ERK1/2 and p38 MAPK. Arch Oral Biol 60 : 488 495.[CrossRef][PubMed]
66. Levine B,, Mizushima N,, Virgin HW . 2011. Autophagy in immunity and inflammation. Nature 469 : 323 335.[CrossRef][PubMed]
67. Kroemer G,, Mariño G,, Levine B . 2010. Autophagy and the integrated stress response. Mol Cell 40 : 280 293.[CrossRef][PubMed]
68. Bullon P,, Cordero MD,, Quiles JL,, Ramirez-Tortosa MC,, Gonzalez-Alonso A,, Alfonsi S,, García-Marín R,, de Miguel M,, Battino M . 2012. Autophagy in periodontitis patients and gingival fibroblasts: unraveling the link between chronic diseases and inflammation. BMC Med 10 : 122.[CrossRef][PubMed]
69. Irving AT,, Mimuro H,, Kufer TA,, Lo C,, Wheeler R,, Turner LJ,, Thomas BJ,, Malosse C,, Gantier MP,, Casillas LN,, Votta BJ,, Bertin J,, Boneca IG,, Sasakawa C,, Philpott DJ,, Ferrero RL,, Kaparakis-Liaskos M . 2014. The immune receptor NOD1 and kinase RIP2 interact with bacterial peptidoglycan on early endosomes to promote autophagy and inflammatory signaling. Cell Host Microbe 15 : 623 635.[CrossRef][PubMed]
70. Cecil JD,, O’Brien-Simpson NM,, Lenzo JC,, Holden JA,, Singleton W,, Perez-Gonzalez A,, Mansell A,, Reynolds EC . 2017. Outer membrane vesicles prime and activate macrophage inflammasomes and cytokine secretion in vitro and in vivo. Front Immunol 8 : 1017.[CrossRef][PubMed]
71. Silva TA,, Garlet GP,, Fukada SY,, Silva JS,, Cunha FQ . 2007. Chemokines in oral inflammatory diseases: apical periodontitis and periodontal disease. J Dent Res 86 : 306 319.[CrossRef][PubMed]
72. Stashenko P,, Teles R,, D’Souza R . 1998. Periapical inflammatory responses and their modulation. Crit Rev Oral Biol Med 9 : 498 521.[CrossRef][PubMed]
73. Graunaite I,, Lodiene G,, Maciulskiene V . 2011. Pathogenesis of apical periodontitis: a literature review. J Oral Maxillofac Res 2( 4) : e1.[PubMed]
74. Waller T,, Kesper L,, Hirschfeld J,, Dommisch H,, Kölpin J,, Oldenburg J,, Uebele J,, Hoerauf A,, Deschner J,, Jepsen S,, Bekeredjian-Ding I . 2016. Porphyromonas gingivalis outer membrane vesicles induce selective tumor necrosis factor tolerance in a Toll-like receptor 4 and mTOR-dependent manner. Infect Immun 84 : 1194 1204.[CrossRef][PubMed]
75. Qi M,, Miyakawa H,, Kuramitsu HK . 2003. Porphyromonas gingivalis induces murine macrophage foam cell formation. Microb Pathog 35 : 259 267.[CrossRef][PubMed]
76. Imayoshi R,, Cho T,, Kaminishi H . 2011. NO production in RAW264 cells stimulated with Porphyromonas gingivalis extracellular vesicles. Oral Dis 17 : 83 89.[CrossRef][PubMed]
77. Hijiya T,, Shibata Y,, Hayakawa M,, Abiko Y . 2010. A monoclonal antibody against fimA type II Porphyromonas gingivalis inhibits IL-8 production in human gingival fibroblasts. Hybridoma (Larchmt) 29 : 201 204.[CrossRef][PubMed]
78. Potempa J,, Mikolajczyk-Pawlinska J,, Brassell D,, Nelson D,, Thøgersen IB,, Enghild JJ,, Travis J . 1998. Comparative properties of two cysteine proteinases (gingipains R), the products of two related but individual genes of Porphyromonas gingivalis. J Biol Chem 273 : 21648 21657.[CrossRef][PubMed]
79. Grenier D . 1992. Inactivation of human serum bactericidal activity by a trypsinlike protease isolated from Porphyromonas gingivalis. Infect Immun 60 : 1854 1857.[PubMed]
80. Duncan L,, Yoshioka M,, Chandad F,, Grenier D . 2004. Loss of lipopolysaccharide receptor CD14 from the surface of human macrophage-like cells mediated by Porphyromonas gingivalis outer membrane vesicles. Microb Pathog 36 : 319 325.[CrossRef][PubMed]
81. Nussbaum G,, Ben-Adi S,, Genzler T,, Sela M,, Rosen G . 2009. Involvement of Toll-like receptors 2 and 4 in the innate immune response to Treponema denticola and its outer sheath components. Infect Immun 77 : 3939 3947.[CrossRef][PubMed]
82. Kesavalu L,, Ebersole JL,, Machen RL,, Holt SC . 1992. Porphyromonas gingivalis virulence in mice: induction of immunity to bacterial components. Infect Immun 60 : 1455 1464.[PubMed]
83. Nakao R,, Hasegawa H,, Dongying B,, Ohnishi M,, Senpuku H . 2016. Assessment of outer membrane vesicles of periodontopathic bacterium Porphyromonas gingivalis as possible mucosal immunogen. Vaccine 34 : 4626 4634.[CrossRef][PubMed]
84. Human Microbiome Project Consortium . 2012. Structure, function and diversity of the healthy human microbiome. Nature 486 : 207214.[CrossRef][PubMed]
85. Faust K,, Sathirapongsasuti JF,, Izard J,, Segata N,, Gevers D,, Raes J,, Huttenhower C . 2012. Microbial co-occurrence relationships in the human microbiome. PLOS Comput Biol 8 : e1002606.[CrossRef][PubMed]
86. O’Hara AM,, Shanahan F . 2006. The gut flora as a forgotten organ. EMBO Rep 7 : 688 693.[CrossRef][PubMed]
87. Davenport AP,, Nunez DJ,, Hall JA,, Kaumann AJ,, Brown MJ . 1989. Autoradiographical localization of binding sites for porcine [125I]endothelin-1 in humans, pigs, and rats: functional relevance in humans. J Cardiovasc Pharmacol 13( Suppl 5) : S166 S170.[CrossRef][PubMed]
88. Zeng MY,, Inohara N,, Nuñez G . 2017. Mechanisms of inflammation-driven bacterial dysbiosis in the gut. Mucosal Immunol 10 : 18 26.[CrossRef][PubMed]
89. Manichanh C,, Borruel N,, Casellas F,, Guarner F . 2012. The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol 9 : 599 608.[CrossRef][PubMed]
90. Turnbaugh PJ,, Ley RE,, Mahowald MA,, Magrini V,, Mardis ER,, Gordon JI . 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 : 1027 1031.[CrossRef][PubMed]
91. Brennan CA,, Garrett WS . 2016. Gut microbiota, inflammation, and colorectal cancer. Annu Rev Microbiol 70 : 395 411.[CrossRef][PubMed]
92. Naseer MI,, Bibi F,, Alqahtani MH,, Chaudhary AG,, Azhar EI,, Kamal MA,, Yasir M . 2014. Role of gut microbiota in obesity, type 2 diabetes and Alzheimer’s disease. CNS Neurol Disord Drug Targets 13 : 305 311.[CrossRef][PubMed]
93. Johansson ME,, Phillipson M,, Petersson J,, Velcich A,, Holm L,, Hansson GC . 2008. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 105 : 15064 15069.[CrossRef][PubMed]
94. Kolling GL,, Matthews KR . 1999. Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl Environ Microbiol 65 : 1843 1848.[PubMed]
95. Kunsmann L,, Rüter C,, Bauwens A,, Greune L,, Glüder M,, Kemper B,, Fruth A,, Wai SN,, He X,, Lloubes R,, Schmidt MA,, Dobrindt U,, Mellmann A,, Karch H,, Bielaszewska M . 2015. Virulence from vesicles: novel mechanisms of host cell injury by Escherichia coli O104:H4 outbreak strain. Sci Rep 5 : 13252.[CrossRef][PubMed]
96. Mayer CL,, Leibowitz CS,, Kurosawa S,, Stearns-Kurosawa DJ . 2012. Shiga toxins and the pathophysiology of hemolytic uremic syndrome in humans and animals. Toxins (Basel) 4 : 1261 1287.[CrossRef][PubMed]
97. Kim SH,, Lee YH,, Lee SH,, Lee SR,, Huh JW,, Kim SU,, Chang KT . 2011. Mouse model for hemolytic uremic syndrome induced by outer membrane vesicles of Escherichia coli O157:H7. FEMS Immunol Med Microbiol 63 : 427 434.[CrossRef][PubMed]
98. Bielaszewska M,, Rüter C,, Kunsmann L,, Greune L,, Bauwens A,, Zhang W,, Kuczius T,, Kim KS,, Mellmann A,, Schmidt MA,, Karch H . 2013. Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis. PLoS Pathog 9 : e1003797.[CrossRef][PubMed]
99. Bielaszewska M,, Rüter C,, Bauwens A,, Greune L,, Jarosch KA,, Steil D,, Zhang W,, He X,, Lloubes R,, Fruth A,, Kim KS,, Schmidt MA,, Dobrindt U,, Mellmann A,, Karch H . 2017. 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 13 : e1006159.[CrossRef][PubMed]
100. Elmi A,, Dorey A,, Watson E,, Jagatia H,, Inglis NF,, Gundogdu O,, Bajaj-Elliott M,, Wren BW,, Smith DGE,, Dorrell N . 2018. The bile salt sodium taurocholate induces Campylobacter jejuni outer membrane vesicle production and increases OMV-associated proteolytic activity. Cell Microbiol 20 : e12814.[CrossRef][PubMed]
101. Chatterjee D,, Chaudhuri K . 2011. Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Lett 585 : 1357 1362.[CrossRef][PubMed]
102. Cervin J,, Wands AM,, Casselbrant A,, Wu H,, Krishnamurthy S,, Cvjetkovic A,, Estelius J,, Dedic B,, Sethi A,, Wallom KL,, Riise R,, Bäckström M,, Wallenius V,, Platt FM,, Lebens M,, Teneberg S,, Fändriks L,, Kohler JJ,, Yrlid U . 2018. GM1 ganglioside-independent intoxication by cholera toxin. PLoS Pathog 14 : e1006862.[CrossRef]
103. Rasti ES,, Schappert ML,, Brown AC . 2018. Association of Vibrio cholerae 569B outer membrane vesicles with host cells occurs in a GM1-independent manner. Cell Microbiol 20 : e12828.[CrossRef]
104. Vanaja SK,, Russo AJ,, Behl B,, Banerjee I,, Yankova M,, Deshmukh SD,, Rathinam VAK . 2016. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation. Cell 165 : 1106 1119.[CrossRef]
105. Amieva M,, Peek RM Jr . 2016. Pathobiology of Helicobacter pylori-induced gastric cancer. Gastroenterology 150 : 64 78.[CrossRef]
106. Fiocca R,, Necchi V,, Sommi P,, Ricci V,, Telford J,, Cover TL,, Solcia E . 1999. Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J Pathol 188 : 220 226.[CrossRef]
107. Keenan J,, Day T,, Neal S,, Cook B,, Perez-Perez G,, Allardyce R,, Bagshaw P . 2000. A role for the bacterial outer membrane in the pathogenesis of Helicobacter pylori infection. FEMS Microbiol Lett 182 : 259 264.[CrossRef]
108. Chitcholtan K,, Hampton MB,, Keenan JI . 2008. Outer membrane vesicles enhance the carcinogenic potential of Helicobacter pylori. Carcinogenesis 29 : 2400 2405.[CrossRef]
109. Winter J,, Letley D,, Rhead J,, Atherton J,, Robinson K . 2014. Helicobacter pylori membrane vesicles stimulate innate pro- and anti-inflammatory responses and induce apoptosis in Jurkat T cells. Infect Immun 82 : 1372 1381.[CrossRef]
110. Hock BD,, McKenzie JL,, Keenan JI . 2017. Helicobacter pylori outer membrane vesicles inhibit human T cell responses via induction of monocyte COX-2 expression. Pathog Dis 75 : ftx034.[CrossRef]
111. Ko SH,, Rho DJ,, Jeon JI,, Kim YJ,, Woo HA,, Kim N,, Kim JM . 2016. Crude preparations of Helicobacter pylori outer membrane vesicles induce upregulation of heme oxygenase-1 via activating Akt-Nrf2 and mTOR–IκB kinase–NF-κB pathways in dendritic cells. Infect Immun 84 : 2162 2174.[CrossRef]
112. Cañas MA,, Fábrega MJ,, Giménez R,, Badia J,, Baldomà L . 2018. Outer membrane vesicles from probiotic and commensal Escherichia coli activate NOD1-mediated immune responses in intestinal epithelial cells. Front Microbiol 9 : 498.[CrossRef]
113. Fábrega MJ,, Rodríguez-Nogales A,, Garrido-Mesa J,, Algieri F,, Badía J,, Giménez R,, Gálvez J,, Baldomà L . 2017. Intestinal anti-inflammatory effects of outer membrane vesicles from Escherichia coli Nissle 1917 in DSS-experimental colitis in mice. Front Microbiol 8 : 1274.[CrossRef]
114. Hickey CA,, Kuhn KA,, Donermeyer DL,, Porter NT,, Jin C,, Cameron EA,, Jung H,, Kaiko GE,, Wegorzewska M,, Malvin NP,, Glowacki RW,, Hansson GC,, Allen PM,, Martens EC,, Stappenbeck TS . 2015. Colitogenic Bacteroides thetaiotaomicron antigens access host immune cells in a sulfatase-dependent manner via outer membrane vesicles. Cell Host Microbe 17 : 672 680.[CrossRef]
115. Roy K,, Hamilton DJ,, Munson GP,, Fleckenstein JM . 2011. Outer membrane vesicles induce immune responses to virulence proteins and protect against colonization by enterotoxigenic Escherichia coli. Clin Vaccine Immunol 18 : 1803 1808.[CrossRef]
116. De Benedetto G,, Alfini R,, Cescutti P,, Caboni M,, Lanzilao L,, Necchi F,, Saul A,, MacLennan CA,, Rondini S,, Micoli F . 2017. Characterization of O-antigen delivered by generalized modules for membrane antigens (GMMA) vaccine candidates against nontyphoidal Salmonella. Vaccine 35 : 419 426.[CrossRef][PubMed]
117. Adriani R,, Mousavi Gargari SL,, Nazarian S,, Sarvary S,, Noroozi N . 2018. Immunogenicity of Vibrio cholerae outer membrane vesicles secreted at various environmental conditions. Vaccine 36 : 322 330.[CrossRef][PubMed]
118. Sinha R,, Howlader DR,, Ta A,, Mitra S,, Das S,, Koley H . 2017. Retinoic acid pre-treatment down regulates V. cholerae outer membrane vesicles induced acute inflammation and enhances mucosal immunity. Vaccine 35 : 3534 3547.[CrossRef][PubMed]
119. Leitner DR,, Lichtenegger S,, Temel P,, Zingl FG,, Ratzberger D,, Roier S,, Schild-Prüfert K,, Feichter S,, Reidl J,, Schild S . 2015. A combined vaccine approach against Vibrio cholerae and ETEC based on outer membrane vesicles. Front Microbiol 6 : 823.[CrossRef]
120. Hays MP,, Houben D,, Yang Y,, Luirink J,, Hardwidge PR . 2018. Immunization with Skp delivered on outer membrane vesicles protects mice against enterotoxigenic Escherichia coli challenge. Front Cell Infect Microbiol 8 : 132.[CrossRef]
121. Wang S,, Gao J,, Wang Z . 2018. Outer membrane vesicles for vaccination and targeted drug delivery. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2018 : e1523.[CrossRef][PubMed]
122. Schager AE,, Dominguez-Medina CC,, Necchi F,, Micoli F,, Goh YS,, Goodall M,, Flores-Langarica A,, Bobat S,, Cook CNL,, Arcuri M,, Marini A,, King LDW,, Morris FC,, Anderson G,, Toellner KM,, Henderson IR,, López-Macías C,, MacLennan CA,, Cunningham AF . 2018. IgG responses to porins and lipopolysaccharide within an outer membrane-based vaccine against nontyphoidal Salmonella develop at discordant rates. mBio 9 : e02379-17.[CrossRef]
123. Liu Q,, Yi J,, Liang K,, Zhang X,, Liu Q . 2017. Outer membrane vesicles derived from Salmonella Enteritidis protect against the virulent wild-type strain infection in a mouse model. J Microbiol Biotechnol 27 : 1519 1528.
124. Choi HI,, Kim M,, Jeon J,, Han JK,, Kim KS . 2017. Overexpression of MicA induces production of OmpC-enriched outer membrane vesicles that protect against Salmonella challenge. Biochem Biophys Res Commun 490 : 991 996.[CrossRef][PubMed]
125. Bryant WA,, Stentz R,, Le Gall G,, Sternberg MJE,, Carding SR,, Wilhelm T . 2017. In silico analysis of the small molecule content of outer membrane vesicles produced by Bacteroides thetaiotaomicron indicates an extensive metabolic link between microbe and host. Front Microbiol 8 : 2440.[CrossRef]

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