TY - JOUR

T1 - B-cell cytokine responses to Porphyromonas gingivalis in patients with periodontitis and healthy controls

AU - Danielsen, Anne Katrine

AU - Damgaard, Christian

AU - Massarenti, Laura

AU - Østrup, Peter

AU - Hansen, Peter Riis

AU - Holmstrup, Palle

AU - Nielsen, Claus H.

N1 - Publisher Copyright: © 2023 The Authors. Journal of Periodontology published by Wiley Periodicals LLC on behalf of American Academy of Periodontology.

PY - 2023

Y1 - 2023

N2 - 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+ memory cells, while the IL-10‒producing B cells were mainly CD27−CD5−. 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.

AB - 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+ memory cells, while the IL-10‒producing B cells were mainly CD27−CD5−. 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.

KW - B cells

KW - cytokines

KW - periodontitis

KW - Porphyromonas gingivalis

U2 - 10.1002/JPER.22-0438

DO - 10.1002/JPER.22-0438

M3 - Journal article

C2 - 36715211

AN - SCOPUS:85149679987

VL - 94

SP - 997

EP - 1007

JO - Journal of Periodontology

JF - Journal of Periodontology

SN - 0022-3492

IS - 8

ER -