Activation of bone marrow-derived dendritic cells and CD4⁺ T cell differentiation by outer membrane vesicles of periodontal pathogens

References

• Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases. Nat Rev Dis Primers. 2017;3(1):17038.
   PubMed Web of Science ®Google Scholar
• Darveau RP. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol. 2010;8:481–11.
   PubMed Web of Science ®Google Scholar
• Bui FQ, Almeida-da-Silva CLC, Huynh B, et al. Association between periodontal pathogens and systemic disease. Biomed J. 2019;42:27–35.
   PubMed Web of Science ®Google Scholar
• Hajishengallis G, Chavakis T. Local and systemic mechanisms linking periodontal disease and inflammatory comorbidities. Nat Rev Immunol. 2021;21:426–440.
   PubMed Web of Science ®Google Scholar
• Yoon YJ, Kim OY, Gho YS. Extracellular vesicles as emerging intercellular communicasomes. BMB Rep. 2014;47:531–539.
   PubMed Web of Science ®Google Scholar
• Toyofuku M, Nomura N, Eberl L. Types and origins of bacterial membrane vesicles. Nat Rev Microbiol. 2019;17:13–24.
   PubMed Web of Science ®Google Scholar
• Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009;9:581–593.
   PubMed Web of Science ®Google Scholar
• Cecil JD, O’Brien-Simpson NM, Lenzo JC, et al. Differential responses of pattern recognition receptors to outer membrane vesicles of three periodontal pathogens. PLoS One. 2016;11:e0151967.
   PubMed Web of Science ®Google Scholar
• Cecil JD, O’Brien-Simpson NM, Lenzo JC, et al. Outer membrane vesicles prime and activate macrophage inflammasomes and cytokine secretion in vitro and in vivo. Front Immunol. 2017;8:1017.
   Web of Science ®Google Scholar
• Villard A, Boursier J, Andriantsitohaina R. Microbiota-derived extracellular vesicles and metabolic syndrome. Acta Physiol (Oxf). 2021;231(4):e13600.
   Web of Science ®Google Scholar
• Zhang Z, Liu D, Liu S, et al. The role of Porphyromonas gingivalis outer membrane vesicles in periodontal disease and related systemic diseases. Front Cell Infect Microbiol. 2021;10:585917.
   PubMed Web of Science ®Google Scholar
• Okamura H, Hirota K, Yoshida K, et al. Outer membrane vesicles of Porphyromonas gingivalis: novel communication tool and strategy. Japanese Dental Sci Review. 2021;57:138–146.
   Web of Science ®Google Scholar
• Kim HY, Song M-K, Gho YS, et al. Extracellular vesicles derived from the periodontal pathogen Filifactor alocis induce systemic bone loss through Toll-like receptor 2. J Extracell Vesicles. 2021;10(12):e12157.
   Web of Science ®Google Scholar
• Cabeza-Cabrerizo M, Cardoso A, Minutti CM, et al. Dendritic cells revisited. Annu Rev Immunol. 2021;39:131–166.
   Web of Science ®Google Scholar
• Zhou L, Chong MM, Littman DR. Plasticity of CD4+ T cell lineage differentiation. Immunity. 2009;30:646–655.
   PubMed Web of Science ®Google Scholar
• Wu RQ, Zhang DF, Tu E, et al. The mucosal immune system in the oral cavity-an orchestra of T cell diversity. Int J Oral Sci. 2014;6:125–132.
   PubMed Web of Science ®Google Scholar
• Dutzan N, Abusleme L, Bridgeman H, et al. On-going mechanical damage from mastication drives homeostatic Th17 cell responses at the oral barrier. Immunity. 2017;46:133–147.
   Web of Science ®Google Scholar
• Xiao E, Mattos M, Vieira GHA, et al. Diabetes enhances IL-17 expression and alters the oral microbiome to increase its pathogenicity. Cell Host Microbe. 2017;22:120–128 e124.
   PubMed Web of Science ®Google Scholar
• Dutzan N, Kajikawa T, Abusleme L, et al. A dysbiotic microbiome triggers Th17 cells to mediate oral mucosal immunopathology in mice and humans. Sci Transl Med. 2018;10(463):eaat0797.
   Web of Science ®Google Scholar
• Srisatjaluk R, Doyle RJ, Justus DE. Outer membrane vesicles of Porphyromonas gingivalis inhibit IFN-gamma-mediated MHC class II expression by human vascular endothelial cells. Microb Pathog. 1999;27:81–91.
   Web of Science ®Google Scholar
• Qi M, Miyakawa H, Kuramitsu HK. Porphyromonas gingivalis induces murine macrophage foam cell formation. Microb Pathog. 2003;35:259–267.
   PubMed Web of Science ®Google Scholar
• Ha JY, Choi SY, Lee JH, et al. Delivery of periodontopathogenic extracellular vesicles to brain monocytes and microglial IL-6 promotion by RNA cargo. Front Mol Biosci. 2020;7:596366.
   PubMed Web of Science ®Google Scholar
• Lim H, Kim YU, Sun H, et al. Proatherogenic conditions promote autoimmune T helper 17 cell responses in vivo. Immunity. 2014;40:153–165.
   Web of Science ®Google Scholar
• Gardiner C, Ferreira YJ, Dragovic RA, et al. Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. J Extracell Vesicles. 2013;2:19671.
   PubMedGoogle Scholar
• Huang G, Wang Y, Chi H. Regulation of Th17 cell differentiation by innate immune signals. Cell Mol Immunol. 2012;9:287–295.
   Web of Science ®Google Scholar
• Zenobia C, Herpoldt KL, Freire M. Is the oral microbiome a source to enhance mucosal immunity against infectious diseases?. NPJ Vaccines. 2021;6:80.
   Web of Science ®Google Scholar
• Nussbaum G, Ben-Adi S, Genzler T, et al. Involvement of Toll-like receptors 2 and 4 in the innate immune response to Treponema denticola and its outer sheath components. Infect Immun. 2009;77:3939–3947.
   PubMed Web of Science ®Google Scholar
• Myneni SR, Settem RP, Connell TD, et al. TLR2 signaling and Th2 responses drive Tannerella forsythia-induced periodontal bone loss. J Immunol. 2011;187:501–509.
   Web of Science ®Google Scholar
• Lin M, Hu Y, Wang Y, et al. Different engagement of TLR2 and TLR4 in Porphyromonas gingivalis vs. ligature-induced periodontal bone loss. Braz Oral Res. 2017;31:e63.
   Web of Science ®Google Scholar
• Alaniz RC, Deatherage BL, Lara JC, et al. Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J Immunol. 2007;179:7692–7701.
   PubMed Web of Science ®Google Scholar
• Durand V, Mackenzie J, de Leon J, et al. Role of lipopolysaccharide in the induction of type I interferon-dependent cross-priming and IL-10 production in mice by meningococcal outer membrane vesicles. Vaccine. 2009;27:1912–1922.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Zhu Z, Antenucci F, Villumsen KR, et al. Bacterial outer membrane vesicles as a versatile tool in vaccine research and the fight against antimicrobial resistance. mBio. 2021;12:e0170721.
   Web of Science ®Google Scholar
• Moutsopoulos NM, Kling HM, Angelov N, et al. Porphyromonas gingivalis promotes Th17 inducing pathways in chronic periodontitis. J Autoimmun. 2012;39:294–303.
   PubMed Web of Science ®Google Scholar
• Cheng WC, van Asten SD, Burns LA, et al. Periodontitis-associated pathogens P. gingivalis and A. actinomycetemcomitans activate human CD14+ monocytes leading to enhanced Th17/IL-17 responses. Eur J Immunol. 2016;46:2211–2221.
   PubMed Web of Science ®Google Scholar
• Bittner-Eddy PD, Fischer LA, Kaplan DH, et al. Mucosal langerhans cells promote differentiation of Th17 cells in a murine model of periodontitis but are not required for Porphyromonas gingivalis-driven alveolar bone destruction. J Immunol. 2016;197:1435–1446.
   Web of Science ®Google Scholar
• Bittner-Eddy PD, Fischer LA, Costalonga M. Transient expression of IL-17A in Foxp3 fate-tracked cells in Porphyromonas gingivalis-mediated oral dysbiosis. Front Immunol. 2020;11:677.
   Web of Science ®Google Scholar
• Zhang L, Gao L, Xu C, et al. Porphyromonas gingivalis lipopolysaccharide promotes T- helper 17 cell differentiation from human CD4+ naive T cells via Toll-like receptor-2 in vitro. Arch Oral Biol. 2019;107:104483.
   Web of Science ®Google Scholar
• Perricone C, Ceccarelli F, Saccucci M, et al. Porphyromonas gingivalis and rheumatoid arthritis. Curr Opin Rheumatol. 2019;31:517–524.
   PubMed Web of Science ®Google Scholar
• Marchesan JT, Gerow EA, Schaff R, et al. Porphyromonas gingivalis oral infection exacerbates the development and severity of collagen-induced arthritis. Arthritis Res Ther. 2013;15:R186.
   Web of Science ®Google Scholar
• Zhou N, Zou F, Cheng X, et al. Porphyromonas gingivalis induces periodontitis, causes immune imbalance, and promotes rheumatoid arthritis. J Leukoc Biol. 2021;110:461–473.
   Web of Science ®Google Scholar
• Nishihara M, Ogura H, Ueda N, et al. IL-6-gp130-STAT3 in T cells directs the development of IL-17+ Th with a minimum effect on that of Treg in the steady state. Int Immunol. 2007;19:695–702.
   PubMed Web of Science ®Google Scholar
• Tripathi SK, Chen Z, Larjo A, et al. Genome-wide analysis of STAT3-mediated transcription during early human Th17 cell differentiation. Cell Rep. 2017;19:1888–1901.
   Web of Science ®Google Scholar
• Diehl S, Anguita J, Hoffmeyer A, et al. Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity. 2000;13:805–815.
   PubMed Web of Science ®Google Scholar
• Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol. 2003;3:133–146.
   PubMed Web of Science ®Google Scholar
• Settem RP, Honma K, Nakajima T, et al. A bacterial glycan core linked to surface (S)-layer proteins modulates host immunity through Th17 suppression. Mucosal Immunol. 2013;6:415–426.
   PubMed Web of Science ®Google Scholar
• Tomek MB, Maresch D, Windwarder M, et al. A general protein O-glycosylation gene cluster encodes the species-specific glycan of the oral pathogen Tannerella forsythia: o-glycan biosynthesis and immunological implications. Front Microbiol. 2018;9:2008.
   Web of Science ®Google Scholar
• Godovikova V, Goetting-Minesky MP, Fenno JC. Composition and localization of Treponema denticola outer membrane complexes. Infect Immun. 2011;79:4868–4875.
   Web of Science ®Google Scholar
• Veith PD, Glew MD, Gorasia DG, et al. Localization of outer membrane proteins in Treponema denticola by quantitative proteome analyses of outer membrane vesicles and cellular fractions. J Proteome Res. 2019;18:1567–1581.
   Web of Science ®Google Scholar
• Miyamoto M, Ishihara K, Okuda K. The Treponema denticola surface protease dentilisin degrades interleukin-1 beta (IL-1 beta), IL-6, and tumor necrosis factor alpha. Infect Immun. 2006;74:2462–2467.
   Web of Science ®Google Scholar
• Jia L, Han N, Du J, et al. Pathogenesis of important virulence factors of Porphyromonas gingivalis via Toll-like receptors. Front Cell Infect Microbiol. 2019;9:262.
   PubMed Web of Science ®Google Scholar
• O’Brien-Simpson NM, Veith PD, Dashper SG, et al. Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr Protein Pept Sci. 2003;4:409–426.
   PubMed Web of Science ®Google Scholar
• Veith PD, Chen YY, Gorasia DG, et al. Porphyromonas gingivalis outer membrane vesicles exclusively contain outer membrane and periplasmic proteins and carry a cargo enriched with virulence factors. J Proteome Res. 2014;13:2420–2432.
   PubMed Web of Science ®Google Scholar
• Hajishengallis G. Immune evasion strategies of Porphyromonas gingivalis. J Oral Biosci. 2011;53:233–240.
   PubMedGoogle Scholar