Suppression of interleukin-10 release from human periodontal ligament cells by interleukin-1β in vitro

doi:10.1016/S0003-9969(99)00120-X

Archives of Oral Biology

Volume 45, Issue 2, 1 February 2000, Pages 179-183

https://doi.org/10.1016/S0003-9969(99)00120-X Get rights and content

Abstract

Periodontitis is characterized by an inflammatory process induced by periodontopathogenic bacteria in the subgingival plaque. Periodontal inflammation can be enhanced by both an increase of inflammatory stimulators, e.g. interleukin (IL)-6, and a decrease of inflammatory inhibitors, e.g. IL-10. The amount of IL-1β is known to be increased in gingival tissues and in the gingival crevicular fluid from inflamed sites compared to healthy sites. This in vitro study sought to clarify whether IL-1β (1 ng/ml) has a regulatory effect on the release of these two cytokines from human periodontal ligament (PDL) cells. PDL cells derived from healthy premolars were grown in the presence and absence (control) of IL-1β. The concentration of IL-6 and IL-10 in the supernatants was assessed by enzyme-linked immunosorbent assay after 48 h of culture. PDL cells incubated with IL-1β released significantly (p<0.05) higher amounts of IL-6 and significantly (p<0.01) smaller amounts of IL-10 compared to control. These results give further support to the observation that IL-1β can increase the IL-6 secretion from PDL cells. Moreover, they provide original evidence that PDL cells secrete IL-10, which can be suppressed by IL-1β. It is concluded that PDL cells can function as accessory immunoinflammatory cells amplifying the inflammatory process in periodontitis and, thereby, contributing to periodontal breakdown.

References (28)

G. Hillmann et al.
Immunohistological determination of interleukin-1 beta in inflamed human gingival epithelium
Archs oral Biol.
(1995)
T. Hirano et al.
Biological and clinical aspects of interleukin 6
Immunol. Today
(1990)
U.H. Lerner
Bradykinin synergistically potentiates interleukin-1 induced bone resorption and prostanoid biosynthesis in neonatal mouse calvarial bones
Biochem. biophys. Res. Commun.
(1991)
N. Shimizu et al.
Stimulation by interleukin-1 of interleukin-6 production by human periodontal ligament cells
Archs oral Biol.
(1992)
O. Takeichi et al.
Human polymorphonuclear leukocytes derived from chronically inflamed tissue express inflammatory cytokines in vivo
Cell Immun.
(1994)
P. Wang et al.
Interleukin-10 inhibits interleukin-8 production in human neutrophils
Blood
(1994)
M.C. Wolvekamp et al.
Interleukin-6: historical background, genetics and biological significance
Immunol. Lett.
(1990)
S. Agarwal et al.
Synthesis of proinflammatory cytokines by human gingival fibroblasts in response to lipopolysaccharides and interleukin-1 beta
J. periodont. Res.
(1995)
N. Berkman et al.
Inhibition of macrophage inflammatory protein-1 alpha expression by IL-10. Differential sensitivities in human blood monocytes and alveolar macrophages
J. Immun.
(1995)
H. Birkedal-Hansen
Role of cytokines and inflammatory mediators in tissue destruction
J. periodont. Res.
(1993)

G. Del-Prete et al.

Human IL-10 is produced by both type 1 helper (Th1) and type 2 helper (Th2) T cell clones and inhibits their antigen-specific proliferation and cytokine production

J. Immun.

(1993)

R. De-Waal-Malefyt et al.

Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression

J. exp. Med.

(1991)

R. De-Waal-Malefyt et al.

Direct effects of IL-10 on subsets of human CD4+ T cell clones and resting T cells. Specific inhibition of IL-2 production and proliferation

J. Immun.

(1993)

H.L. Dickensheets et al.

IFN-gamma and IL-10 inhibit induction of IL-1 receptor type I and type II gene expression by IL-4 and IL-13 in human monocytes

J. Immun.

(1997)

Cited by (14)

A review of T helper 17 cell-related cytokines in serum and saliva in periodontitis
2021, Cytokine
Citation Excerpt :
In addition, IL-1β increases IL-8 and intercellular adhesion molecule (ICAM)-1 expression on endothelial cells, facilitating neutrophil infiltration into affected tissues [26,214]. IL-1β regulates extracellular matrix turnover by inducing the gene expression of several matrix metalloproteinases including collagenases (MMP-1, MMP-8), gelatinases (MMP-9, MMP-2) and stromelysin-1 (MMP-3) [215–219], and upregulating IL-6 and downregulating IL-10 from resident PDL cells [220]. IL-1β also plays a role in bone remodelling by upregulating RANKL [221], inhibiting OPG expression by osteoblasts resulting in osteoclastogenesis and subsequent bone destruction [222,223].
Periodontitis is a chronic inflammatory disease with a complex underlying immunopathology. Cytokines, as molecular mediators of inflammation, play a role in all stages of disease progression. T helper 17 (Th17) cells are thought to play a role in periodontitis. Th17 cell development and maintenance requires a pro-inflammatory cytokine milieu, with many of the cytokines implicated in the pathogenesis of periodontitis. Serum and saliva are easily accessible biofluids which can represent the systemic and local environment to promote the development of Th17 cells. Here we review human clinical studies that investigate IL-1β, IL-4, IL-6, IL-10, IL-17A, IL-17F, IL-21, IL-22, IL-23, IL-25, IL-31, IL-33, IFN-γ, sCD40L and TNF-α in serum and saliva in periodontitis. We highlight their putative role in the pathogenesis of periodontitis and place them within a wider context of animal and other clinical studies.
Interaction of Candida albicans with periodontal ligament fibroblasts limits biofilm formation over elastomer silicone disks
2016, Archives of Oral Biology
Citation Excerpt :
It should be noted that Th17 cells are known to play a protective role against C. albicans infection in the oral cavity (Conti & Gaffen, 2010). PDL cells also secrete cytokines such as IL-10 and transforming growth factor-β (TGF-β), which are anti-inflammatory and necessary for tissue repair during the healing process (Colic et al., 2009; Deschner et al., 2000; Pinkerton et al., 2008). Therefore PDL cells may play an integral role in the resistance to C. albicans infection.
Candida albicans is the most numerous commensal and potentially pathological yeast in the human oral cavity. The purpose herein is to investigate the ability of C. albicans to form a biofilm in the presence of periodontal ligament (PDL) fibroblasts.
Silicone elastomer disks (SE) were transferred to wells containing PDL cells. C. albicans suspension was added to each well. The whole mixed culture was then allowed to form a biofilm for 48 h. Biofilms were quantified by tetrazolium-salt-based (2,3-bis(2-methoxy-4-nitro-5-sulfophenyl)-5-[(phenyl amino) carbonyl]- 2H-tetrazolium hydroxide (XTT). Furthermore, biofilm was visualized by confocal scanning laser and scanning electron microscopy. Migration of C. albicans and its ability to form biofilms in presence of PDL cells was determined by using a transwell system. Last, elutes obtained from co-culturing C. albicans and PDL cells were added to SE disks and covered with C. albicans. The culture plate was then incubated to allow biofilm formation. Biofilms formed over SE disks were quantified using XTT.
PDL cells significantly limited the biofilm formation at incubation interval of 48 h. PDL cells induced less biofilm compared to mature and thick hyphae in the absence of PDL cells as seen in confocal scanning laser and scanning electron microscopy. The presence of PDL cells limited the migration and formation of biofilm by C. albicans. Elutes obtained from co-culturing PDL cells with C. albicans for one hour induced significantly less biofilm.
This is the first study to report that PDL cells exhibit antifungal activity. While the exact mechanism of how PDL cells limited biofilm formation is yet unknown, it was clear that competent PDL cells promote resistance to C. albicans biofilm formation.
Effect of periodontal therapy on crevicular fluid interleukin-1β and interleukin-10 levels in chronic periodontitis
2004, Journal of Dentistry
Objectives. This study aimed to analyse the levels of the proinflammatory cytokine IL-1β and the anti-inflammatory cytokine IL-10 in gingival crevicular fluid (GCF) of patients with chronic periodontitis prior to, and following, periodontal therapy for a period of 32 weeks.
Material and methods. GCF samples were obtained from 24 non-diseased and 72 diseased sites of 12 periodontal patients prior to as well as at 6, 16 and 32 weeks post-periodontal therapy. All sites received conventional periodontal treatment and IL-1β and IL-10 levels (concentration and total amount) were determined by enzyme linked immunosorbent assay (ELISA). Additionally, probing pocket depth (PD), clinical attachment loss (CAL), gingival (GI) and plaque (PII) indices were evaluated pre-and post-therapy.
Results. IL-1β was detected in 382 out of 384 samples, while IL-10 was detected in 337 out of 384 samples. The total amount of IL-1β was significantly higher at diseased compared to non-diseased sites (p<0.01). Following therapy, IL-1β total amounts were reduced, while IL-1β concentration gradually increased. IL-10 total amounts (per 30 s sample) were similar in diseased and non-diseased sites, and following therapy they remained almost unchanged. By contrast, IL-10 concentration was significantly higher in non-diseased sites (p<0.01) and displayed a significant increase post-therapy. Moreover, IL-1β concentration and total amount were significantly greater in smokers following therapy, while IL-10 total amount was significantly higher in non-smokers both prior to and following therapy. Total IL-1β amounts were positively correlated with GI and Pll. A weak negative corretation between IL-1β and IL-10 levels was noted (p>0.05).
Conclusions. The data suggest that the total amount rather than the concentration of IL-1β in GCF seemed to be closely associated with periodontal disease severity. Moreover, smoking status influenced IL-1β and IL-10 levels. An inverse relationship between IL-1β and IL-10 was evident.
Immunohistological study of interferon-γ- and interleukin-4-bearing cells in human periodontitis gingiva
2001, Archives of Oral Biology
Citation Excerpt :
It is surprising that IL-4-bearing cells did not increase with the increase in inflammatory cells infiltrating the gingiva. While a single cytokine itself may regulate an immune or inflammatory reaction, many cytokines together may co-regulate the reaction with a balance of effect (Deschner et al., 2000). McGee et al. (1998) examined the concentrations of IL-1β, IL-6 and IL-8 within gingival tissue biopsies and suggested that the characteristics of the gingival cytokine network are affected by the adjacent sulcular depth.
The purpose was to investigate the balance between interferon (IFN)-ϒ- and interleukin (IL)-4-bearing cells in various human inflamed gingiva by immunohistochemistry. Gingival tissues obtained from patients with gingivitis or periodontitis were divided into three groups based on the degree of histopathological inflammation, mild, moderate and severe. The tissues were also divided into four groups according to the clinical probing depth (PD). IFN-ϒ- and IL-4-bearing cells in gingival tissues were stained immunohistologically and counted. The ratio of IL-4-bearing cells to IFN-ϒ-bearing cells was calculated for each section. IFN-ϒ-bearing cells were widespread in the connective tissue and their number increased significantly with the severity of inflammation and an increase of PD. IL-4-bearing cells were located beneath the pocket epithelium and their number showed no significant differences among the inflammation or PD groups. The ratios of IL-4-bearing cells to IFN-ϒ-bearing cells in the severe inflammation or deep PD groups were significantly lower than those in the moderate inflammation or shallow PD groups. These results suggest that a low ratio of IL-4-bearing cells to IFN-ϒ-bearing cells might be involved in the destruction of periodontal tissue.
Antimicrobial Peptides and Interleukins in Cleft Soft Palate
2023, Children
Dec2 attenuates autophagy in inflamed periodontal tissues
2021, Immunity, Inflammation and Disease

View all citing articles on Scopus

View full text

Short communicationSuppression of interleukin-10 release from human periodontal ligament cells by interleukin-1β in vitro

Abstract

Archs oral Biol.

Immunol. Today

Biochem. biophys. Res. Commun.

Archs oral Biol.

Cell Immun.

Blood

Immunol. Lett.

Synthesis of proinflammatory cytokines by human gingival fibroblasts in response to lipopolysaccharides and interleukin-1 beta

J. periodont. Res.

Inhibition of macrophage inflammatory protein-1 alpha expression by IL-10. Differential sensitivities in human blood monocytes and alveolar macrophages

J. Immun.

Role of cytokines and inflammatory mediators in tissue destruction

J. periodont. Res.

Human IL-10 is produced by both type 1 helper (Th1) and type 2 helper (Th2) T cell clones and inhibits their antigen-specific proliferation and cytokine production

J. Immun.

Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression

J. exp. Med.

Direct effects of IL-10 on subsets of human CD4+ T cell clones and resting T cells. Specific inhibition of IL-2 production and proliferation

J. Immun.

IFN-gamma and IL-10 inhibit induction of IL-1 receptor type I and type II gene expression by IL-4 and IL-13 in human monocytes

J. Immun.

Short communication
Suppression of interleukin-10 release from human periodontal ligament cells by interleukin-1β in vitro