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Virulence Factors of Periodontal Pathogens: Secretion, Function and Interaction with...
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Virulence Factors of Periodontal Pathogens: Secretion, Function and Interaction with Host Immune Responses

A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Immunological Responses and Immune Defense Mechanisms".

Deadline for manuscript submissions: closed (30 September 2022) | Viewed by 17623

Special Issue Editors

Prof. Dr. Jan Potempa

E-Mail Website
Guest Editor
1. Department of Oral Immunity and Infectious Diseases, University of Louisville School of Dentistry, Louisville, KY, USA
2. Department of Microbiology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland
Interests: proteolytic enzymes and their inhibitors in homeostasis and disease and molecular bases of virulence of periodontal pathogens and their relation to systemic diseases
Dr. Anna Maria Łasica

E-Mail Website
Guest Editor
Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, Poland
Interests: enteropathogens; oral pathogens; molecular microbiology; T9SS; virulence

Special Issue Information

Dear Colleagues,

Recent methodological advances have accelerated research on periodontitis and the role of the dysbiotic microbiota on the tooth surface below the gum line in the development and maintenance of chronic inflammation of the periodontium. Concurrently, we have learned a lot about communication between bacteria recently in the dental plaque community and how they can corrupt host immune responses. Additionally, our knowledge of mechanisms causing erosion of the periodontium has increased exponentially. In all respects, Porphyromonas gingivalis, together with established and emerging periodontal pathogens, is at the center of the pathobiology of periodontitis. Therefore, the purpose of this Special Issue is to present major recent advances in investigations of different host and bacterial aspects of the disease emanating from several ground-braking findings in periodontal pathogens research in the last few years.

Potential topics include but are not limited to:

 (i) Structural and functional characterization of the novel type IX secretion system (T9SS) used by periodontal pathogens to secrete their proteinaceous virulence factors;

(ii) Advances in characterization of virulence factors structure on the atomic structure level; 

(iii) Understanding molecular mechanisms of dysbiotic community development on the tooth surface;

(iv) Elucidation of host signaling pathways manipulated by P. gingivalis and other periodontal pathogens;

(v) Implication of P. gingivalis as a potentially causative factor in diseases such as esophageal cancer, rheumatoid arthritis, Alzheimer’s disease, and other systemic diseases associated with periodontitis; 

(vi) Identification and characterization of new targets for development of novel strategies to prevent/treat periodontitis.

Such assembly of articles in one issue would be unique among the existing literature on oral pathogens and their role in pathogenesis of periodontitis and associated systemic diseases.

Prof. Dr. Jan Potempa
Dr. Anna Maria Łasica
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Pathogens is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • periodontitis
  • T9SS
  • secretion
  • gingipains
  • therapy
  • cargo proteins
  • proteases
  • virulence factors
  • Porphyromonas gingivalis
  • Tannerella forsythia
  • Filifactor alocis
  • pathogenesis
  • host–pathogen interactions
  • innate immune system
  • complement
  • antigen
  • biofilm
  • dental plaque
  • oral pathogens

Published Papers (6 papers)

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Research

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12 pages, 1979 KiB  
Article
Matrix Metalloproteinase 9 (MMP-9) and Interleukin-8 (IL-8) in Gingival Crevicular Fluid after Regenerative Therapy in Periodontal Intrabony Defects with and without Systemic Antibiotics—Randomized Clinical Trial
by Ewa Dolińska, Małgorzata Pietruska, Violetta Dymicka-Piekarska, Robert Milewski and Anton Sculean
Pathogens 2022, 11(10), 1184; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11101184 - 14 Oct 2022
Cited by 2 | Viewed by 1168
Abstract
The aim of our study was to assess changes in the levels of IL-8 and MMP-9 in gingival crevicular fluid (GCF) collected from the periodontal pocket before and after regenerative surgery with deproteinized bovine bone mineral (DBBM) and collagen membrane (GTR) either independently [...] Read more.
The aim of our study was to assess changes in the levels of IL-8 and MMP-9 in gingival crevicular fluid (GCF) collected from the periodontal pocket before and after regenerative surgery with deproteinized bovine bone mineral (DBBM) and collagen membrane (GTR) either independently (DBBM/GTR) or with the postoperative administration of antibiotic (DBBM/GTR+AB). The study involved 41 patients, each with one intrabony defect. IL-8 and MMP-9 were determined before therapy and after 2 weeks, 4 weeks and 6 months following the surgical procedure by means of dedicated ELISA kits. No statistical differences were observed in the levels of IL-8 and MMP-9 after 2 weeks, 4 weeks and 6 months between the groups. The changes in the level of MMP-9 over time were not statistically significant in any group. The changes in the level of IL-8 were significant for the group given antibiotic but not in the nonantibiotic group in the follow-up period. IL-8 and MMP-9 were found to correlate positively but not after 4 weeks in the test group. Current assessment of IL-8 and MMP-9 obtained from GCF samples provides evidence that collagen matrix turnover occurs actively during the early healing phase in the periodontium after regenerative procedures. We observed positive correlations of MMP-9 and IL-8 throughout the study. However, we failed to reveal any differences regard parameters studied between the two groups. Full article
(This article belongs to the Special Issue Virulence Factors of Periodontal Pathogens: Secretion, Function and Interaction with Host Immune Responses)
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13 pages, 2639 KiB  
Article
Cortisol Promotes Surface Translocation of Porphyromonas gingivalis
by Hey-Min Kim, Christina Magda Rothenberger and Mary Ellen Davey
Pathogens 2022, 11(9), 982; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11090982 - 27 Aug 2022
Cited by 1 | Viewed by 1938
Abstract
Studies are showing that the stress hormone cortisol can reach high levels in the gingival sulcus and induce shifts in the metatranscriptome of the oral microbiome. Interestingly, it has also been shown that cortisol can influence expression levels of Type IX Secretion System [...] Read more.
Studies are showing that the stress hormone cortisol can reach high levels in the gingival sulcus and induce shifts in the metatranscriptome of the oral microbiome. Interestingly, it has also been shown that cortisol can influence expression levels of Type IX Secretion System (T9SS) genes involved in gliding motility in bacteria belonging to the phylum Bacteroidota. The objective of this study was to determine if cortisol impacts gene expression and surface translocation of Porphyromonas gingivalis strain W50. To conduct these experiments, P. gingivalis was stabbed to the bottom of soft agar plates containing varying cortisol concentrations (0 μM, 0.13 μM, 1.3 μM, and 13 μM), and surface translocation on the subsurface was observed after 48 h of incubation. The results show that when grown with certain nutrients, i.e., in rich medium with the addition of sheep blood, lactate, or pyruvate, cortisol promotes migration of P. gingivalis in a concentration-dependent manner. To begin to examine the underlying mechanisms, quantitative PCR was used to evaluate differential expression of genes when P. gingivalis was exposed to cortisol. In particular, we focused on differential expression of T9SS-associated genes, including mfa5, since it was previously shown that Mfa5 is required for cell movement and cell-to-cell interactions. The data show that mfa5 is significantly up-regulated in the presence of cortisol. Moreover, an mfa5 deletion mutant showed less surface translocation compared to the wild-type P. gingivalis in the presence of cortisol, and the defects of the mfa5 deletion mutant were restored by complementation. Overall, cortisol can stimulate P. gingivalis surface translocation and this coincides with higher expression levels of T9SS-associated genes, which are known to be essential to gliding motility. Our findings support a high possibility that the stress hormone cortisol from the host can promote surface translocation and potentially virulence of P. gingivalis. Full article
(This article belongs to the Special Issue Virulence Factors of Periodontal Pathogens: Secretion, Function and Interaction with Host Immune Responses)
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13 pages, 928 KiB  
Article
Proteomic Characterization of the Oral Pathogen Filifactor alocis Reveals Key Inter-Protein Interactions of Its RTX Toxin: FtxA
by Kai Bao, Rolf Claesson, Peter Gehrig, Jonas Grossmann, Jan Oscarsson and Georgios N. Belibasakis
Pathogens 2022, 11(5), 590; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050590 - 17 May 2022
Cited by 5 | Viewed by 2065
Abstract
Filifactor alocis is a Gram-positive asaccharolytic, obligate anaerobic rod that has been isolated from a variety of oral infections including periodontitis, peri-implantitis, and odontogenic abscesses. As a newly emerging pathogen, its type strain has been investigated for pathogenic properties, yet little is known [...] Read more.
Filifactor alocis is a Gram-positive asaccharolytic, obligate anaerobic rod that has been isolated from a variety of oral infections including periodontitis, peri-implantitis, and odontogenic abscesses. As a newly emerging pathogen, its type strain has been investigated for pathogenic properties, yet little is known about its virulence variations among strains. We previously screened the whole genome of nine clinical oral isolates and a reference strain of F. alocis, and they expressed a novel RTX toxin, FtxA. In the present study, we aimed to use label-free quantification proteomics to characterize the full proteome of those ten F. alocis strains. A total of 872 proteins were quantified, and 97 among them were differentially expressed in FtxA-positive strains compared with the negative strains. In addition, 44 of these differentially expressed proteins formed 66 pairs of associations based on their predicted functions, which included clusters of proteins with DNA repair/mediated transformation and catalytic activity-related function, indicating different biosynthetic activities among strains. FtxA displayed specific interactions with another six intracellular proteins, forming a functional cluster that could discriminate between FtxA-producing and non-producing strains. Among them were FtxB and FtxD, predicted to be encoded by the same operon as FtxA. While revealing the broader qualitative and quantitative proteomic landscape of F. alocis, this study also sheds light on the deeper functional inter-relationships of FtxA, thus placing this RTX family member into context as a major virulence factor of this species. Full article
(This article belongs to the Special Issue Virulence Factors of Periodontal Pathogens: Secretion, Function and Interaction with Host Immune Responses)
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15 pages, 2552 KiB  
Article
The Subgingival Plaque Microbiome, Systemic Antibodies against Bacteria and Citrullinated Proteins following Periodontal Therapy
by Emily Davison, William Johnston, Krystyna Piela, Bob T. Rosier, Michael Paterson, Alex Mira and Shauna Culshaw
Pathogens 2021, 10(2), 193; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10020193 - 10 Feb 2021
Cited by 13 | Viewed by 4100
Abstract
Periodontitis (PD) shows an association with rheumatoid arthritis (RA) and systemic inflammation. Periodontal pathogens, namely Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans, are proposed to be capable of inducing citrullination of peptides in the gingiva, inducing the formation of anti-citrullinated protein antibodies (ACPAs) within [...] Read more.
Periodontitis (PD) shows an association with rheumatoid arthritis (RA) and systemic inflammation. Periodontal pathogens, namely Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans, are proposed to be capable of inducing citrullination of peptides in the gingiva, inducing the formation of anti-citrullinated protein antibodies (ACPAs) within susceptible hosts. Here, we sought to investigate whether periodontal treatment influenced systemic inflammation and antibody titres to P. gingivalis, A. actinomycetemcomitans, Prevotella intermedia and ACPA in 42 systemically health patients with periodontal disease. Subgingival plaque and serum samples were collected from study participants before (baseline) and 90 days after treatment to analyse the abundance of specific bacteria and evaluate anti-bacterial antibodies, C-reactive protein (CRP), tumour necrosis factor α (TNF-α), interleukin 6 (IL-6) and ACPA in serum. Following treatment, all patients showed reduced periodontal inflammation. Despite observing a weak positive correlation between CRP and IL-6 with periodontal inflammation at baseline, we observed no significant reductions in any indicators of systemic inflammation 90 days after treatment. In contrast, anti-P. gingivalis IgG significantly reduced post-treatment (p < 0.001, Wilcoxon signed rank test), although no changes were observed for other antibody titres. Patients who had detectable P. gingivalis in subgingival plaques had significantly higher anti-P. gingivalis IgG and ACPA titres, suggesting a potential association between P. gingivalis colonisation and systemic antibody titres. Full article
(This article belongs to the Special Issue Virulence Factors of Periodontal Pathogens: Secretion, Function and Interaction with Host Immune Responses)
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13 pages, 7745 KiB  
Article
Application of the In Vitro HoxB8 Model System to Characterize the Contributions of Neutrophil–LPS Interaction to Periodontal Disease
by Maja Sochalska, Magdalena B. Stańczyk, Maria Użarowska, Natalia Zubrzycka, Susanne Kirschnek, Aleksander M. Grabiec, Tomasz Kantyka and Jan Potempa
Pathogens 2020, 9(7), 530; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens9070530 - 01 Jul 2020
Cited by 2 | Viewed by 3754
Abstract
(1) Background: Studying neutrophils in vitro is difficult since these cells are terminally differentiated and are easily activated during isolation. At the same time, most of the available model cell lines are associated with certain limitations, such as functional deficiency or a lack [...] Read more.
(1) Background: Studying neutrophils in vitro is difficult since these cells are terminally differentiated and are easily activated during isolation. At the same time, most of the available model cell lines are associated with certain limitations, such as functional deficiency or a lack of expression of surface markers characteristic of neutrophils. P. gingivalis is a periodontopathogen that causes dysbiosis in subgingival bacterial biofilm. This triggers the accumulation of functional neutrophils in the periodontium. However, until now, the specific effects of P. gingivalis-derived lipopolysaccharide on neutrophil functions have not been analyzed. (2) Methods: The impact of two variants of commercially available P. gingivalis endotoxin on neutrophil functions was tested using the HoxB8 in vitro system that is well suited to analyze neutrophil response to different stimuli in a controlled manner. (3) Results: The Standard P. gingivalis lipopolysaccharide (LPS), known to activate cells through Toll-like receptor 2 (TLR2)- and Toll-like receptor 4 (TLR4)-dependent pathways, prolonged neutrophil survival and exhibited pro-inflammatory effects. In contrast, Ultrapure LPS, binding exclusively to TLR4, neither protected neutrophils from apoptosis, nor induced an inflammatory response. (4) Conclusion: Two variants of P. gingivalis-derived LPS elicited effects on neutrophils and, based on the obtained results, we concluded that the engagement of both TLR2 and TLR4 is required for the manipulation of survival and the stimulation of immune responses of HoxB8 neutrophils. Full article
(This article belongs to the Special Issue Virulence Factors of Periodontal Pathogens: Secretion, Function and Interaction with Host Immune Responses)
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Review

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13 pages, 1460 KiB  
Review
A Tale of Two Fimbriae: How Invasion of Dendritic Cells by Porphyromonas gingivalis Disrupts DC Maturation and Depolarizes the T-Cell-Mediated Immune Response
by Mohamed M. Meghil, Mira Ghaly and Christopher W. Cutler
Pathogens 2022, 11(3), 328; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11030328 - 08 Mar 2022
Cited by 11 | Viewed by 2999
Abstract
Porphyromonas gingivalis (P. gingivalis) is a unique pathogen implicated in severe forms of periodontitis (PD), a disease that affects around 50% of the US population. P. gingivalis is equipped with a plethora of virulence factors that it uses to exploit its [...] Read more.
Porphyromonas gingivalis (P. gingivalis) is a unique pathogen implicated in severe forms of periodontitis (PD), a disease that affects around 50% of the US population. P. gingivalis is equipped with a plethora of virulence factors that it uses to exploit its environment and survive. These include distinct fimbrial adhesins that enable it to bind to other microbes, colonize inflamed tissues, acquire nutrients, and invade cells of the stroma and immune system. Most notable for this review is its ability to invade dendritic cells (DCs), which bridge the innate and adaptive immune systems. This invasion process is tightly linked to the bridging functions of resultant DCs, in that it can disable (or stimulate) the maturation function of DCs and cytokines that are secreted. Maturation molecules (e.g., MHCII, CD80/CD86, CD40) and inflammatory cytokines (e.g., IL-1b, TNFa, IL-6) are essential signals for antigen presentation and for proliferation of effector T-cells such as Th17 cells. In this regard, the ability of P. gingivalis to coordinately regulate its expression of major (fimA) and minor (mfa-1) fimbriae under different environmental influences becomes highly relevant. This review will, therefore, focus on the immunoregulatory role of P. gingivalis fimbriae in the invasion of DCs, intracellular signaling, and functional outcomes such as alveolar bone loss and immune senescence. Full article
(This article belongs to the Special Issue Virulence Factors of Periodontal Pathogens: Secretion, Function and Interaction with Host Immune Responses)
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