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 Table of Contents  
ORIGINAL ARTICLE
Year : 2014  |  Volume : 34  |  Issue : 2  |  Page : 120-125

Role of interleukin-23 in the immunopathogenesis of systemic lupus erythematosus


1 Department of Dermatology and Venereology, Faculty of Medicine, Tanta University, Tanta, Egypt
2 Department of Dermatology and Venereology, Faculty of Medicine, Miser University for Science and Technology (MUST University), El-Giza, Egypt
3 Department of Clinical Pathology, Faculty of Medicine, Tanta University, Tanta, Egypt
4 Department of Internal Medicine, Faculty of Medicine, Tanta University, Tanta, Egypt
5 Department of Dermatology and Venereology, Ministry of Health, Tanta, Egypt

Date of Submission01-Oct-2014
Date of Acceptance24-Nov-2014
Date of Web Publication29-Jan-2015

Correspondence Address:
Doaa Salah Hegab
MD, Department of Dermatology and Venereology, Faculty of Medicine, Tanta University Hospitals, El Geish Street, Tanta 31111
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-6530.150269

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  Abstract 

Background
Systemic lupus erythematosus (SLE) is a complex and multifactorial autoimmune disease. T-helper 17 (Th17) cells are essential modulators for propagation of immune response in several autoimmune diseases. Interleukin-23 (IL-23) is a proinflammatory mediator that is necessary for the development of T-cell-dependent inflammation. IL-23 is essential to expand and maintain Th17 cells. Increased amounts of IL-23 have been associated with several autoimmune diseases.
Aims
This work aimed to study the alteration in the serum level of IL-23 in patients with SLE in comparison with healthy individuals, and to correlate its serum level with disease activity to speculate on its possible role in the pathogenesis of SLE.
Participants and methods
Thirty-four adult patients with SLE (31 women and three men) and 30 healthy age and sex-matched controls were included. SLE patients were divided according to SLE disease activity index (SLEDAI) into active and inactive groups. IL-23 serum level was determined for all patients and controls using a quantitative enzyme-linked immunosorbent assay.
Results
Serum IL-23 concentration was significantly elevated in SLE patients than in the healthy controls (P = 0.001), and it correlated significantly with disease activity (P = 0.001). The median serum IL-23 concentrations were significantly higher in active SLE patients with renal involvement.
Conclusion
Findings support the presence of an important role of IL-23 in the pathogenesis of SLE. Our results indicate a possible relationship between the elevated serum levels of IL-23 and SLE activity. Marked elevation might be a predictor of renal insult in active cases.

Keywords: Immunopathogenesis, interleukin-23, systemic lupus erythematosus


How to cite this article:
Hegab DS, Gamei MM, Saudi WM, Ammo DE, El Bedewy MM, Elhabian NF. Role of interleukin-23 in the immunopathogenesis of systemic lupus erythematosus. Egypt J Dermatol Venerol 2014;34:120-5

How to cite this URL:
Hegab DS, Gamei MM, Saudi WM, Ammo DE, El Bedewy MM, Elhabian NF. Role of interleukin-23 in the immunopathogenesis of systemic lupus erythematosus. Egypt J Dermatol Venerol [serial online] 2014 [cited 2020 May 28];34:120-5. Available from: http://www.ejdv.eg.net/text.asp?2014/34/2/120/150269


  Introduction Top


Systemic lupus erythematosus (SLE) is an autoimmune disorder characterized by the production of pathogenic autoantibodies and immune complex deposition in various organs [1]. At present, the etiology and pathogenetic mechanisms of SLE are still unclear. Epidemiological data suggest that SLE may be a result of a combination of genetic and environmental factors, with a prominent autoimmune component. It has been confirmed that cytokines play a pleiotropic role in the pathogenesis of SLE [2].

Interleukin-23 (IL-23) is a heterodimeric cytokine comprising IL-12p40 and IL-23p19 subunits and is a member of the IL-12 cytokine family. The p19 subunit of IL-23 is produced by antigen-presenting cells as well as T cells and endothelial cells. The p40 subunit is primarily restricted to antigen-presenting cells such as monocytes, macrophages, and dendritic cells [3],[4]. IL-23 exerts its biological activities through interaction with a heterodimeric receptor complex composed of IL-12Rb1 and IL-23R [4],[5].

IL-23 plays a key role in the development of pathogenic Th17 cells that produce the cytokine IL-17 [6],[7]. IL-17 induces the production of several proinflammatory cytokines such as tumor necrosis factor-α, IL-6, chemokines, and metalloproteinases from various tissues and cell types and recruits neutrophils to tissues, which are implicated in the pathogenesis of SLE and other autoimmune diseases [8],[9],[10].

In humans, IL-23 was found to be overexpressed in clinical samples of several immune-mediated diseases, including Crohn's disease, rheumatoid arthritis, and multiple sclerosis [11]. As cytokine-mediated immunity plays a crucial role in the pathogenesis of SLE, a possible role of IL-23 in the pathogenesis of SLE is highly suspected [12].

The present study was designed to examine the alteration in the serum level of IL-23 in patients with SLE in comparison with healthy individuals, and to correlate its serum level with SLE disease activity using the SLE Disease Activity Index (SLEDAI) score to speculate on its possible role in disease pathogenesis.


  Participants and methods Top


This study was carried out on 34 adult patients with SLE (31 women and 3 men) diagnosed according to the American College of Rheumatology (ACR) diagnostic criteria for SLE [13], and these patients were either recently diagnosed cases before starting large doses of systemic steroids or immunosuppressive drugs, or patients on maintenance therapy experiencing disease exacerbation, before reinitiation of large doses of systemic therapy. In addition, 30 healthy age- and sex-matched individuals with no history of any systemic or skin disease that may affect serum IL-23 levels were included as a control group.

All the participants studied were recruited from the outpatient clinic of the Dermatology and Venereology Department and the inpatient unit and clinics of the Department of Internal Medicine (Rheumatology Unit), Tanta University Hospitals. Patients who agreed to participate in the study signed a written consent and this work was approved by the ethical committee of the Faculty of Medicine, Tanta University.

The participants studied were divided into the following groups: group I included 14 patients with inactive SLE, group II included 20 patients with active SLE, and group III included 30 healthy individuals as controls. Patients included in this study were subjected to complete history taking, and a thorough general and dermatological examination. Laboratory investigations were performed in the form of urine analysis, 24 h protein in urine, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), complete blood picture, fasting, and post-prandial blood glucose levels, liver and kidney function tests, antinuclear antibodies (ANA), anti-ds DNA, C3, C4, and ultrasound of the abdomen and pelvis. In addition, renal biopsy data (if any) were collected from the most recent data in the patients' files and they were repeated when necessary. Renal involvement in SLE cases was defined by persistence of proteinuria (>0.5 g/24 h) or the presence of cellular casts, persistent hematuria, or renal biopsy showing glomerulonephritis (mesangial, focal proliferative, diffuse proliferative, or membranous). SLE disease activity was calculated for the patients according to the SLEDAI score [14], where patients with SLEDAI score of at least 6 were considered to have active disease and patients with SLEDAI score less than 6 were considered to have inactive disease. Patients with other associated dermatological or autoimmune diseases (e.g. rheumatoid arthritis), pregnant, lactating women, and those who were receiving hormonal contraception were excluded.

The serum level of IL-23 was measured for all patients and controls by a quantitative enzyme-linked immunosorbent assay technique using the RayBio Human IL-23 ELISA Kit Protocol (RayBiotech Inc., Austria) according to the manufacturer's instructions, and the results were expressed in pg/ml.

Statistical analysis

Statistical presentation and analysis of numerical data were carried out using the mean, SD, and the χ2 -test using the Statistical Package for Social Sciences (SPSS) version 17. Differences in plasma concentration among groups were compared using an F-test of equality of variances and Scheffé's method. The Mann-Whitney U-test was used to compare the difference in the plasma concentration among the patients in group II. Correlations were assessed using Spearman's rank test. A P value less than 0.05 was considered statistically significant.


  Results Top


Fourteen patients with inactive SLE, 20 patients with active SLE, and 30 age and sex-matched and control participants were studied. Their sex, age, duration of diagnosis, SLEDAI score, CRP, first hour ESR, ANA, anti-ds DNA, C3, C4 levels, and the extent of renal involvement, if present are summarized in [Table 1].
Table 1: Characteristics of SLE patients and control participants

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The serum level of IL-23 in patients with inactive SLE (group I) ranged from 20 to 48 pg/ml, mean ± SD 37.35 ± 8.75 pg/ml, the level in patients with active SLE (group II) ranged from 50 to 440 pg/ml, mean ± SD 235.05 ± 137.4 pg/ml, and the level in group III ranged from 10.0 to 14.0 pg/ml, mean ± SD 11.8 ± 1.22 pg/ml, as shown in [Table 2]. Altogether, the serum IL-23 concentration was significantly higher in all SLE patients than in the control participants and in those with active SLE than in those with inactive disease (P = 0.001) [Table 2] and [Figure 1].
Figure 1: Serum level of interleukin-23 (IL-23) in systemic lupus erythematosus patient groups and controls.

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A statistically significant positive correlation was detected between the serum levels of IL-23 and the activity of the SLE disease measured by the SLEDAI score in the SLE groups (P = 0.001 in both groups) [Table 3].
Table 2: Serum level of IL-23 in SLE patient groups and controls

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Table 3: Correlation between the serum levels of IL-23 and age (years), disease duration (months), sex, ESR, ANA, anti-ds DNA, and disease activity according to the SLEDAI score of SLE groups

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A significant positive correlation was detected between the serum levels of IL-23 and first hour reading of ESR and CRP in patients of group II with active SLE, and this correlation was not detected in patients of group I with inactive disease [Table 3].

No significant correlation could be detected between the serum levels of IL-23 and age, disease duration, sex, ANA, anti-ds DNA, C3, and C4 in both groups of SLE patients [Table 3].

None of the patients in group I had renal involvement, whereas 13 out of the 20 patients in group II had renal disease [Table 1]. The median serum level of IL-23 in SLE patients in group II with renal involvement was 290 versus 100 pg/ml in those without renal involvement as shown in [Table 4] and this difference was statistically significant (P = 0.039).{Table 4}


  Discussion Top


Study of the cytokine profiles in SLE patients showed a complex interplay between proinflammatory and anti-inflammatory cytokine networks [15]. The discovery of IL-23 led to the identification of a unique helper T-cell subset called Th17 cells, which mainly produce the proinflammatory cytokines, IL-17 (A and F) and IL-21 [16]. IL-17 induces the production of several proinflammatory cytokines that are implicated in the pathogenesis of SLE and other autoimmune diseases [16]. Evidences suggest that Th17 cells may acquire a more 'inflammatory' profile in the presence of IL-23 [17].

In the present study, which included 34 SLE patients, there were 31 (91.2%) female patients and three (8.8%) male patients, and this was in agreement with previous reports, in which SLE was found to be much more common in women than in men (9 : 1 in most reports) [18],[19],[20].

In the current study, a significant increase in the serum concentrations of IL-23 was found in SLE patients than in healthy controls, which further confirms its immunopathological role in the autoinflammatory processes of SLE as exemplified by its further parallel positive correlation with disease activity. Our results provide additional information on the possible role of IL-23 in SLE.

In agreement with our study, Wong et al. [21] found that sera IL-23 and IL-17 levels and the number of Th17 cells were elevated in SLE patients compared with healthy individuals. Huang et al. [22] found that the mRNA levels of p19 (specific subunit of IL-23), p40 (common subunit for IL-23 and IL-12), and p35 (IL-12-specific subunit) in the peripheral blood mononuclear cells (PBMC) in active SLE patients were significantly higher than those in the inactive SLE patients. Their results suggest that upregulation of IL-23 may contribute toward the pathogenesis of SLE.

However, Cheng et al. [23] reported that decreased plasma IL-22 levels, but not increased IL-17 and IL-23 levels, correlate with disease activity in SLE patients. The reasons for this discrepancy are not known, but they could be attributed to the effects of different drug regimens and dosages received by SLE patients.

In the current study, the significant positive correlation detected between the serum levels of IL-23 and first hour reading of ESR and CRP in patients with active SLE was very predictable in light of the direct relation of these laboratory parameters to the severity and activity of the disease. Our results also suggest a direct relation between the markedly elevated serum IL-23 levels and the possibility of renal disease in SLE. In agreement with our results, the IL-23/IL-17 axis and IL-23R(+) T-cell subsets in particular have been linked previously to increased disease activity in SLE patients [24], and moreover to lupus nephritis [7],[25], and inflammatory manifestations including severe cutaneous involvement and serositis [26]. In a recent publication, serum IL-23 mRNA levels were found to be significantly higher in patients with SLE compared with healthy controls, and in patients with SLE and renal involvement compared with SLE alone. IL-23 mRNA levels were not different between patients with active or inactive SLE, but the IL-17/IL-23 ratio was significantly higher in patients with active disease [27].

IL-23 has been reported to increase IL-17 secretion, whereas IL-12 has been reported to inhibit IL-17 secretion by PBMC from healthy individuals [28]. However, another study showed that the mRNA levels of IL-23p19, p40, and p35 of IL-12 were significantly higher in active SLE patients, thereby suggesting that IL-23 could play a role in SLE disease exacerbation [29]. Moreover, the likely significance of IL-23 in autoinflammatory responses was further supported by a previous report that indicated that Th1 transcription factor T-bet could upregulate IL-23 receptor expression and the differentiation of Th1 and Th17 cells in autoimmunity [30].

For a better understanding of the involvement of IL-23 in the IL-23/IL-17 autoinflammatory axis and the immunopathological mechanisms of the activation of Th17 cells in SLE, a previous work had attempted to elucidate the effect of IL-23 on the ex-vivo production of IL-17 from the anti-CD3-stimulated and anti-CD28-costimulated PBMC. Upon IL-23 induction, the costimulated PBMC responded with an aberrant ex-vivo production of IL-17 and the increase was significantly higher in SLE patients than the controls (P < 0.05) [21]. It has been reported that the pathogenic Th17 subgroup expresses increased levels of the IL-23 receptor by the activation by T-bet, thereby representing a distinct inflammatory Th cell lineage for the development of organ-specific autoimmune inflammation [8],[30]. Previous data presented evidence on the direct involvement of IL-23 in the IL-23/IL-17 inflammatory axis, which acts to induce a distinct T-cell activation state that produces IL-17 as the effector cytokine that could promote the autoinflammatory responses in SLE [21]. IL-23-mediated activation of IL-17-producing Th cells in SLE patients may probably be closely influenced by IL-18 activation, which is considered to orchestrate the inflammation of SLE [21].

It should be noted that some studies have reported no association between IL-23 receptor gene polymorphisms and susceptibility to SLE in several populations including Spanish [31], Korean [32], and Chinese populations [33]. Despite this, it should be noted that the level of IL-23 was not examined directly. Furthermore, differences in ethnicity may lead to conflicting results on the association between IL-23 and SLE.

Given the complexity of cytokine interaction and their involvement in the presentation of various diseases, further experiments are perhaps required to elucidate the detailed relationship between the Th1 cytokine IL-12 and its family member IL-23 in patients with autoimmune diseases. Despite this, a previous publication has recapitulated the crucial role of IL-12 in the pathogenesis of several Th1-mediated autoimmune diseases including type I diabetes, multiple sclerosis, rheumatoid arthritis, and inflammatory graft-versus-host reaction [34]. Therefore, pharmacological control of the production of IL-12 family cytokines including IL-23 may be a key therapeutic strategy in the modulation of specific immune-mediated diseases dominated by Th1 cytokines and IL-17 responses. In fact, anti-IL-23 therapy effectively inhibited multiple inflammatory pathways that are critical for driving autoimmune inflammation in the central nervous system [35] as well as lupus nephritis [36].


  Conclusion Top


The IL-23/IL-17 axis could contribute significantly toward the pathogenesis of SLE. IL-23 (a member of the IL-12 cytokine family) can promote SLE disease severity, activity, and renal insult by activating pathogenic Th1 and Th17 cells. Targeting of IL-23 or the IL-23 receptor is a potential therapeutic approach for autoimmune diseases including SLE and particularly in cases with renal involvement.


  Acknowledgements Top


Conflicts of interest

There are no conflicts of interest.

 
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    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]


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