B-cell cytokine responses to Porphyromonas gingivalis in patients with periodontitis and healthy controls.


Journal

Journal of periodontology
ISSN: 1943-3670
Titre abrégé: J Periodontol
Pays: United States
ID NLM: 8000345

Informations de publication

Date de publication:
08 2023
Historique:
revised: 24 12 2022
received: 22 07 2022
accepted: 17 01 2023
medline: 18 8 2023
pubmed: 31 1 2023
entrez: 30 1 2023
Statut: ppublish

Résumé

Cytokine-producing B cells play a well-established role in modifying immune responses in chronic inflammatory diseases. We characterized B-cell cytokine responses against periodontitis-associated bacteria in patients with periodontitis. Blood and saliva samples were collected from patients with periodontitis grade B (N = 31) or grade C (N = 25), and 25 healthy controls (HCs). Mononuclear cells were stimulated with Porphyromonas gingivalis, Fusobacterium nucleatum, Staphylococcus epidermidis, or Cutibacterium acnes, and B-cell production of tumor necrosis factor (TNF)-α, interleukin (IL)-6, interferon (IFN)-γ, IL-10 and transforming growth factor (TGF)-β by B cells was assessed by flow cytometry. HCs had higher baseline frequencies of B cells producing IFN-γ or TNF-α than grade B patients, but only B cells from grade B patients showed significant differentiation into IFN-γ-, TNF-α-, TGF-β-, or IL-10-producing cells after challenge with P. gingivalis and into IFN-γ-, TGF-β-, or IL-10-producing cells after challenge F. nucleatum. Notably, the baseline frequency of IL-10-producing B cells from grade C patients correlated inversely with clinical attachment loss (AL). The major proportion of the IFN-γ- and TGF-β-producing B cells were CD27 B cells from grade B patients, particularly those harboring P. gingivalis, showed proinflammatory B-cell responses to P. gingivalis. Moreover, the baseline frequency of IL-10-producing B cells in the grade C group correlated inversely with AL, suggesting a diminished immunoregulatory capacity of IL-10-producing B cells in these patients.

Sections du résumé

BACKGROUND
Cytokine-producing B cells play a well-established role in modifying immune responses in chronic inflammatory diseases. We characterized B-cell cytokine responses against periodontitis-associated bacteria in patients with periodontitis.
METHODS
Blood and saliva samples were collected from patients with periodontitis grade B (N = 31) or grade C (N = 25), and 25 healthy controls (HCs). Mononuclear cells were stimulated with Porphyromonas gingivalis, Fusobacterium nucleatum, Staphylococcus epidermidis, or Cutibacterium acnes, and B-cell production of tumor necrosis factor (TNF)-α, interleukin (IL)-6, interferon (IFN)-γ, IL-10 and transforming growth factor (TGF)-β by B cells was assessed by flow cytometry.
RESULTS
HCs had higher baseline frequencies of B cells producing IFN-γ or TNF-α than grade B patients, but only B cells from grade B patients showed significant differentiation into IFN-γ-, TNF-α-, TGF-β-, or IL-10-producing cells after challenge with P. gingivalis and into IFN-γ-, TGF-β-, or IL-10-producing cells after challenge F. nucleatum. Notably, the baseline frequency of IL-10-producing B cells from grade C patients correlated inversely with clinical attachment loss (AL). The major proportion of the IFN-γ- and TGF-β-producing B cells were CD27
CONCLUSIONS
B cells from grade B patients, particularly those harboring P. gingivalis, showed proinflammatory B-cell responses to P. gingivalis. Moreover, the baseline frequency of IL-10-producing B cells in the grade C group correlated inversely with AL, suggesting a diminished immunoregulatory capacity of IL-10-producing B cells in these patients.

Identifiants

pubmed: 36715211
doi: 10.1002/JPER.22-0438
doi:

Substances chimiques

Cytokines 0
Interleukin-10 130068-27-8
Tumor Necrosis Factor-alpha 0
Interleukin-6 0
Transforming Growth Factor beta 0

Banques de données

ClinicalTrials.gov
['NCT03225950']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

997-1007

Informations de copyright

© 2023 The Authors. Journal of Periodontology published by Wiley Periodicals LLC on behalf of American Academy of Periodontology.

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Auteurs

Anne Katrine Danielsen (AK)

Faculty of Health and Medical Sciences, Section for Oral, Biology and Immunopathology, Department of Odontology, University of Copenhagen, Copenhagen, Denmark.
Institute for Inflammation Research, Center for Rheumatology and Spine Diseases, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.

Christian Damgaard (C)

Faculty of Health and Medical Sciences, Section for Oral, Biology and Immunopathology, Department of Odontology, University of Copenhagen, Copenhagen, Denmark.
Institute for Inflammation Research, Center for Rheumatology and Spine Diseases, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.

Laura Massarenti (L)

Institute for Inflammation Research, Center for Rheumatology and Spine Diseases, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.

Peter Østrup (P)

Institute for Inflammation Research, Center for Rheumatology and Spine Diseases, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
Faculty of Health and Medical Sciences, Costerton Biofilm Center, Department of Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark.

Peter Riis Hansen (P)

Department of Cardiology, Herlev and Gentofte Hospital, University of Copenhagen, Hellerup, Denmark.

Palle Holmstrup (P)

Faculty of Health and Medical Sciences, Section for Oral, Biology and Immunopathology, Department of Odontology, University of Copenhagen, Copenhagen, Denmark.

Claus H Nielsen (CH)

Faculty of Health and Medical Sciences, Section for Oral, Biology and Immunopathology, Department of Odontology, University of Copenhagen, Copenhagen, Denmark.
Institute for Inflammation Research, Center for Rheumatology and Spine Diseases, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.

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