<i>Porphyromonas gingivalis</i> outer membrane vesicles inhibit the invasion of <i>Fusobacterium nucleatum</i> into oral epithelial cells by downregulating FadA and FomA

Zhang, Zhiying; Liu, Sai; Zhang, Shuwei; Li, Yuchao; Shi, Xiaoting; Liu, Dongjuan; Pan, Yaping

doi:10.1002/jper.21-0144

Cited by 39 publications

(19 citation statements)

References 52 publications

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“…This ability was shown previously for several putative periodontal pathogens, including P. gingivalis, T. denticola, T. forsythia,a n dF. nucleatum (Inagaki et al, 2016;Lamont et al, 1995;Li et al, 2015;Zhang et al, 2021). Our data show that the invasion and survival capability of T.…”

Section: Discussionsupporting

confidence: 88%

Multispecies biofilm behavior and host interaction support the association of Tannerella serpentiformis with periodontal health

Kendlbacher

Bloch

Hager-Mair

et al. 2022

Molecular Oral Microbiology

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The recently identified bacterium Tannerella serpentiformis is the closest phylogenetic relative of Tannerella forsythia, whose presence in oral biofilms is associated with periodontitis. Conversely, T. serpentiformis is considered health-associated. This discrepancy was investigated in a comparative study of the two Tannerella species. The biofilm behavior was analyzed upon their addition and of Porphyromonas gingivalis-each bacterium separately or in combinations-to an in vitro five-species oral model biofilm. Biofilm composition and architecture was analyzed quantitatively using real-time PCR and qualitatively by fluorescence in situ hybridization/confocal laser scanning microscopy, and by scanning electron microscopy. The presence of T. serpentiformis led to a decrease of the total cell number of biofilm bacteria, while P. gingivalis was growth-promoting. This effect was mitigated by T. serpentiformis when added to the biofilm together with P. gingivalis. Notably, T. serpentiformis outcompeted T. forsythia numbers when the two species were simultaneously added to the biofilm compared to biofilms containing T. forsythia alone. Tannerella serpentiformis appeared evenly distributed throughout the multispecies biofilm, while T. forsythia was surface-located. Adhesion and invasion assays revealed that T. serpentiformis was significantly less effective in invading human gingival epithelial cells than T. forsythia. Furthermore, compared to T. forsythia, a higher immunostimulatory potential of human gingival fibroblasts and macrophages was revealed for T. serpentiformis, based on mRNA expression levels of the inflammatory mediators interleukin 6 (IL-6), IL-8, monocyte chemoattractant protein-1 and tumor necrosis factor , and production of the corresponding proteins. Collectively, these data support the potential of T. serpentiformis to interfere with biological processes relevant to the establishment of periodontitis.

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Section: Discussionsupporting

confidence: 88%

Multispecies biofilm behavior and host interaction support the association of Tannerella serpentiformis with periodontal health

Kendlbacher

Bloch

Hager-Mair

et al. 2022

Molecular Oral Microbiology

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“…As a periodontal pathogen, F. nucleatum plays an indispensable role in the formation and growth of oral biofilms, affects the occurrence and development of periodontitis and is the main microorganism of biofilms in periodontal pockets ( Thurnheer et al, 2019 ; Curtis et al, 2020 ). Advances in research have revealed an increasing number of virulence factors ( Ellis and Kuehn, 2010 ; Zanzoni et al, 2017 ), and known virulence factors, new functions and mechanisms are continuously being reported ( Li D. H. et al, 2021 ; Zhang Z. et al, 2021 ). In addition to its significant “bridging” characteristics, the adhesin of F. nucleatum can bind to non-immune and immune cells, leading to gingival inflammation that subsequently develops into an irreversible periodontal disease.…”

Section: Discussionmentioning

confidence: 99%

Outer Membrane Vesicles From Fusobacterium nucleatum Switch M0-Like Macrophages Toward the M1 Phenotype to Destroy Periodontal Tissues in Mice

et al. 2022

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Periodontitis is a chronic inflammatory oral disease that affects nearly 50% of all adults. Fusobacterium nucleatum (F. nucleatum) is known to be involved in the formation and development of periodontitis. Outer membrane vesicles (OMVs) harboring toxic bacterial components are continuously released during F. nucleatum growth and regulate the extent of the inflammatory response by controlling the functions of immune and non-immune cells in tissues. Macrophages are important immune cells in periodontal tissue that resist pathogen invasion and play an important role in the pathophysiological process of periodontitis. However, the role of the interaction between F. nucleatum OMVs and macrophages in the occurrence and development of periodontitis has not been studied. The purpose of this study was to clarify the effect of F. nucleatum OMVs on the polarization of macrophages and the roles of this specific polarization and F. nucleatum OMVs in the pathophysiology of periodontitis. The periodontitis model was established by inducing ligation in C57BL/6 mice as previously described. Micro-CT, RT-qPCR, hematoxylin-eosin (H&E) and tartrate acid phosphatase (TRAP) staining assays were performed to analyze the periodontal tissue, alveolar bone loss, number of osteoclasts and expression of inflammatory factors in gingival tissue. The changes in the state and cytokine secretion of bone marrow-derived macrophages (BMDMs) stimulated by F. nucleatum OMVs were observed in vivo by confocal microscopy, flow cytometry, Western blot and ELISA. Mouse gingival fibroblasts (MGFs) were isolated and then cocultured with macrophages. The effects of F. nucleatum OMVs on the proliferation and apoptosis of MGFs were analyzed by flow cytometry and lactate dehydrogenase (LDH) assays. The periodontitis symptoms of mice in the F. nucleatum OMVs + ligation group were more serious than those of mice in the simple ligation group, with more osteoclasts and more inflammatory factors (IL-1β, IL-6, and TNF-α) being observed in their gingival tissues. M0 macrophages transformed into M1 macrophages after the stimulation of BMDMs with F. nucleatum OMVs, and the M1 macrophages then released more inflammatory cytokines. Analysis of the coculture model showed that the MGF apoptosis and LDH release in the inflammatory environment were increased by F. nucleatum OMV treatment. In conclusion, F. nucleatum OMVs were shown to aggravate periodontitis, alveolar bone loss and the number of osteoclasts in an animal model of periodontitis. F. nucleatum OMVs promoted the polarization of macrophages toward the proinflammatory M1 phenotype, and the inflammatory environment further aggravated the toxicity of F. nucleatum OMVs on MGFs. These results suggest that M1 macrophages and F. nucleatum OMVs play roles in the occurrence and development of periodontitis.

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“…Apart from RadD, many other outer membrane proteins in F. nucleatum also have prominent roles in bacterial coaggregation and biofilm formation. The 42-kDa F. nucleatum major outer-membrane protein (FomA), which mediates coaggregation with P. gingivalis in periodontal pockets ( Kinder and Holt, 1993 ), has been reported to be a crucial factor for fusobacterial biofilm-bridge function ( Zhang et al, 2021 ). FomA cooperates with RadD and Fap2 to achieve binding between F. nucleatum and P. gingivalis ( Brennan and Garrett, 2019 ).…”

Section: The Role Of Fusobacterium Nucleatum In Pe...mentioning

confidence: 99%

“…However, the invasive feature of P. gingivalis to host cells is dramatically inferior to that of F. nucleatum ( Jang et al, 2017 ), which is in agreement with the finding of De Andrade et al (2021) that F. nucleatum is more virulent than P. gingivalis to host cells. It has been demonstrated that mixed infection with F. nucleatum strengthens the invasion capacity of P. gingivalis in oral epithelial cells ( Zhang et al, 2021 ). The “promoter” characteristic of F. nucleatum makes it a crucial pathogen in host mixed infection.…”

Section: The Role Of Fusobacterium Nucleatum In Pe...mentioning

confidence: 99%

Fusobacterium nucleatum: The Opportunistic Pathogen of Periodontal and Peri-Implant Diseases

Chen

Shi

et al. 2022

Front. Microbiol.

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Peri-implant diseases are considered to be a chronic destructive inflammatory destruction/damage occurring in soft and hard peri-implant tissues during the patient’s perennial use after implant restoration and have attracted much attention because of their high incidence. Although most studies seem to suggest that the pathogenesis of peri-implant diseases is similar to that of periodontal diseases and that both begin with microbial infection, the specific mechanism of peri-implant diseases remains unclear. As an oral opportunistic pathogen, Fusobacterium nucleatum (F. nucleatum) has been demonstrated to be vital for the occurrence and development of many oral infectious diseases, especially periodontal diseases. More notably, the latest relevant studies suggest that F. nucleatum may contribute to the occurrence and development of peri-implant diseases. Considering the close connection between peri-implant diseases and periodontal diseases, a summary of the role of Fusobacterium nucleatum in periodontal diseases may provide more research directions and ideas for the peri-implantation mechanism. In this review, we summarize the effects of F. nucleatum on periodontal diseases by biofilm formation, host infection, and host response, and then we establish the relationship between periodontal and peri-implant diseases. Based on the above aspects, we discuss the importance and potential value of F. nucleatum in peri-implant diseases.

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Porphyromonas gingivalis outer membrane vesicles inhibit the invasion of Fusobacterium nucleatum into oral epithelial cells by downregulating FadA and FomA

Cited by 39 publications

References 52 publications

Multispecies biofilm behavior and host interaction support the association of Tannerella serpentiformis with periodontal health

Multispecies biofilm behavior and host interaction support the association of Tannerella serpentiformis with periodontal health

Outer Membrane Vesicles From Fusobacterium nucleatum Switch M0-Like Macrophages Toward the M1 Phenotype to Destroy Periodontal Tissues in Mice

Fusobacterium nucleatum: The Opportunistic Pathogen of Periodontal and Peri-Implant Diseases

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