Interleukin-1β is internalised by viable Aggregatibacter actinomycetemcomitans biofilm and locates to the outer edges of nucleoids

Paino, Annamari; Lohermaa, Elina; Sormunen, Raija; Tuominen, Heidi; Korhonen, Jari; Pöllänen, Marja; Ihalin, Riikka

doi:10.1016/j.cyto.2012.07.024

Cited by 24 publications

(29 citation statements)

References 52 publications

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“…However, due to inter-sample variance, the difference was not statistically significant. In similar organotypic gingival tissue – biofilm co-cultures with a slightly thinner keratinocyte layer 28 A. actinomycetemcomitans cells efficiently internalized IL-1β (Fig. 3C).…”

Section: Resultsmentioning

confidence: 85%

“…3A). However, when the co-culture was performed in the presence of antibiotics, which decreased the viability of the biofilm, 28 the immunohistological staining of the biofilm with anti-IL-8 and anti-IL-6 was faint (Fig. 3A).…”

Section: Resultsmentioning

confidence: 99%

“…N = 3. C) In the organotypic gingival tissue culture model, which produced approximately 200 pg of IL-1β to the culture medium during a 24-h incubation with viable A. actinomycetemcomitans wild-type biofilm, 28 the uptake efficiency of IL-1β was estimated by counting the number of gold particles in anti-IL-1β-stained immuno-EM samples. …”

Section: Resultsmentioning

confidence: 99%

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A novel intrinsically disordered outer membrane lipoprotein ofAggregatibacter actinomycetemcomitansbinds various cytokines and plays a role in biofilm response to interleukin-1β and interleukin-8

et al. 2016

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Intrinsically disordered proteins (IDPs) do not have a well-defined and stable 3-dimensional fold. Some IDPs can function as either transient or permanent binders of other proteins and may interact with an array of ligands by adopting different conformations. A novel outer membrane lipoprotein, bacterial interleukin receptor I (BilRI) of the opportunistic oral pathogen Aggregatibacter actinomycetemcomitans binds a key gatekeeper proinflammatory cytokine interleukin (IL)-1β. Because the amino acid sequence of the novel lipoprotein resembles that of fibrinogen binder A of Haemophilus ducreyi, BilRI could have the potential to bind other proteins, such as host matrix proteins. However, from the tested host matrix proteins, BilRI interacted with neither collagen nor fibrinogen. Instead, the recombinant non-lipidated BilRI, which was intrinsically disordered, bound various pro/anti-inflammatory cytokines, such as IL-8, tumor necrosis factor (TNF)-α, interferon (IFN)-γ and IL-10. Moreover, BilRI played a role in the in vitro sensing of IL-1β and IL-8 because low concentrations of cytokines did not decrease the amount of extracellular DNA in the matrix of bilRI− mutant biofilm as they did in the matrix of wild-type biofilm when the biofilms were exposed to recombinant cytokines for 22 hours. BilRI played a role in the internalization of IL-1β in the gingival model system but did not affect either IL-8 or IL-6 uptake. However, bilRI deletion did not entirely prevent IL-1β internalization, and the binding of cytokines to BilRI was relatively weak. Thus, BilRI might sequester cytokines on the surface of A. actinomycetemcomitans to facilitate the internalization process in low local cytokine concentrations.

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Section: Resultsmentioning

confidence: 85%

Section: Resultsmentioning

confidence: 99%

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A novel intrinsically disordered outer membrane lipoprotein ofAggregatibacter actinomycetemcomitansbinds various cytokines and plays a role in biofilm response to interleukin-1β and interleukin-8

et al. 2016

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“…Previous experimental models have already used single bacteria species, including A. actinomycetemcomitans, F. nucleatum, to challenge an epithelialfibroblasts co-cultured model. [55][56][57] Earlier works in our group have used this subgingival biofilm model in static coculture either with gingival fibroblasts 36 or with multilayer gingival organotypic epithelium, in order to study various aspects of host tissue-oral biofilm interaction. 58,59 As most subgingival species are strict anaerobes, 6 they were grown separately under anaerobic conditions, prior to being introduced into the bioreactor environment along with the organotypic tissue.…”

Section: Discussionmentioning

confidence: 99%

Establishment of an oral infection model resembling the periodontal pocket in a perfusion bioreactor system

et al. 2015

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Periodontal infection involves a complex interplay between oral biofilms, gingival tissues and cells of the immune system in a dynamic microenvironment. A humanized in vitro model that reduces the need for experimental animal models, while recapitulating key biological events in a periodontal pocket, would constitute a technical advancement in the study of periodontal disease. The aim of this study was to use a dynamic perfusion bioreactor in order to develop a gingival epithelial-fibroblast-monocyte organotypic co-culture on collagen sponges. An 11 species subgingival biofilm was used to challenge the generated tissue in the bioreactor for a period of 24 h. The histological and scanning electron microscopy analysis displayed an epithelial-like layer on the surface of the collagen sponge, supported by the underlying ingrowth of gingival fibroblasts, while monocytic cells were also found within the sponge mass. Bacterial quantification of the biofilm showed that in the presence of the organotypic tissue, the growth of selected biofilm species, especially Campylobacter rectus, Actinomyces oris, Streptococcus anginosus, Veillonella dispar, and Porphyromonas gingivalis, was suppressed, indicating a potential antimicrobial effect by the tissue. Multiplex immunoassay analysis of cytokine secretion showed that interleukin (IL)-1 β, IL-2, IL-4, and tumor necrosis factor (TNF)-α levels in cell culture supernatants were significantly up-regulated in presence of the biofilm, indicating a positive inflammatory response of the organotypic tissue to the biofilm challenge. In conclusion, this novel host-biofilm interaction organotypic model might resemble the periodontal pocket and have an important impact on the study of periodontal infections, by minimizing the need for the use of experimental animal models.

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“…In this context, Tuuli Ahlstrand (University of Turku, Finland) showed that biofilms formed by the opportunistic pathogen A. actinomycetemcomitans could disrupt the host inflammation response by binding and internalizing the proiflammatory cytokine interleukin-1b [12], which is enhanced by a specific bacterial sensor named the bacterial interleukin receptor I (BilRI) [13,14]. In the same vein, James Connolly (University of Glasgow, UK) demonstrated how pathogenic E. coli integrates host signals in order to regulate its ability to colonize the urinary tract.…”

Section: Symbiosis Pathogenesis and Mechanisms Of Host Interactionmentioning

confidence: 99%

Interaction and signalling networks: a report from the fourth ‘Young Microbiologists Symposium on Microbe Signalling, Organisation and Pathogenesis’

et al. 2017

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At the end of June, over 120 microbiologists from 18 countries gathered in Dundee, Scotland for the fourth edition of the Young Microbiologists Symposium on 'Microbe Signalling, Organisation and Pathogenesis'. The aim of the symposium was to give early career microbiologists the opportunity to present their work in a convivial environment and to interact with senior world-renowned scientists in exciting fields of microbiology research. The meeting was

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Interleukin-1β is internalised by viable Aggregatibacter actinomycetemcomitans biofilm and locates to the outer edges of nucleoids

Cited by 24 publications

References 52 publications

A novel intrinsically disordered outer membrane lipoprotein ofAggregatibacter actinomycetemcomitansbinds various cytokines and plays a role in biofilm response to interleukin-1β and interleukin-8

A novel intrinsically disordered outer membrane lipoprotein ofAggregatibacter actinomycetemcomitansbinds various cytokines and plays a role in biofilm response to interleukin-1β and interleukin-8

Establishment of an oral infection model resembling the periodontal pocket in a perfusion bioreactor system

Interaction and signalling networks: a report from the fourth ‘Young Microbiologists Symposium on Microbe Signalling, Organisation and Pathogenesis’

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