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Vol. 28. Núm. S2.
Systemic Lupus Erythematosus II
Páginas 116-122 (Noviembre 2021)
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Vol. 28. Núm. S2.
Systemic Lupus Erythematosus II
Páginas 116-122 (Noviembre 2021)
Original Article
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MicroRNA-146a and its target gene IRAK1 polymorphisms confer susceptibility to systemic lupus erythematosus
El microARN-146a y sus polimorfismos del gen diana IRAK1 confieren susceptibilidad al lupus eritematoso sistémico
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1089
Zulvikar Syambani Ulhaqa,
Autor para correspondencia
, Evi Harwiati Ningrumb, Leonel Eslatkin Aguilar Zambranoc, Alvi Millianaa, Christian Peinado Garciad
a Department of Biomedical Science, Faculty of Medicine and Health Sciences, Maulana Malik Ibrahim State Islamic University of Malang, Malang, Indonesia
b School of Nursing, Faculty of Medicine, University of Brawijaya, Malang, Indonesia
c Medical School, Technical University of Manabi, Portoviejo, Ecuador
d Department of General Surgery, Weston General Hospital, Weston-super Mare, Somerset, United Kingdom
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Vol. 28. Núm S2

Systemic Lupus Erythematosus II

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Abstract
Objective

To clarify the association between miR-146a, miR-499, and IRAK1 polymorphism and systemic lupus erythematosus (SLE) predisposition.

Methods

A literature search was conducted until 12 September 2020 in accordance with the PRISMA guidelines. The keywords “miRNA-146a”, “miRNA-499”, “IRAK1” and “SLE” were used in combination to obtain case-control studies evaluating the abovementioned gene polymorphism and the risk of SLE.

Results

Patients harbouring C allele of miRNA-146a rs2431697 exhibited low SLE risk (CC vs. TC+TT, OR=.77, 95% CI=.62–.95, p=.019; TC vs. CC+TT, OR=.84, 95% CI=.71–.98, p=.027; and TC vs. TT, OR=.73, 95% CI=.61–.86, p=.000), whereas patients carrying the A allele and AA genotype of rs3027898 in IRAK1 had significantly decreased SLE susceptibility (A vs. C, OR=.73, 95% CI=.60–.87, p=.001; AA vs. CA+CC, OR=.64, 95% CI=.42–.97, p=.037; AA+CA vs. CC, OR=.71, 95% CI=.56–.88, p=.003, and AA vs. CC, OR=.49, 95% CI=.31–.77, p=.002). No association was observed between miRNA-146a rs2910164 and miRNA-499 rs3746444 with SLE risk.

Conclusion

This study demonstrates associations between miRNA-146a and IRAK1 polymorphisms with SLE risk. Larger studies on these associations are needed in the future to support our results.

Keywords:
miRNA-146a
miRNA-499
IRAK1
Lupus erythematosus
Systemic
predisposition
Disease susceptibility
Resumen
Objetivo

Aclarar la asociación entre el polimorfismo de miR-146a, miR-499 e IRAK1 y la predisposición al lupus eritematoso sistémico (LES).

Métodos

Se realizó una búsqueda bibliográfica hasta el 12 de septiembre del 2020, de acuerdo con las guías PRISMA. Las palabras clave «miRNA-146ª», «miRNA-499», «IRAK1» y «LES» se utilizaron en combinación para obtener estudios de casos y controles que evaluaran el polimorfismo de los genes antes mencionados y el riesgo de LES.

Resultados

Los pacientes que albergan el alelo C del miRNA-146a rs2431697 mostraron un bajo riesgo de LES (CC frente a TC+TT; OR=0,77; IC 95%=0,62-0,95; p=0,019; TC frente a CC+TT; OR=0,84; IC 95%=0,71-0,98; p=0,027; y TC vs. TT; OR=0,73; IC 95%=0,61-0,86; p=0,000), mientras que los pacientes portadores del alelo A y el genotipo AA de rs3027898 en IRAK1 redujeron significativamente la susceptibilidad al LES (A vs. C; OR=0,73; IC 95%=0,60-0,87; p=0,001; AA vs. CA+CC; OR=0,64; IC 95%=0,42-0,97; p=0,037; AA+CA vs. CC; OR=0,71; IC 95%=0,56-0,88; p=0,003 y AA vs. CC; OR=0,49; IC 95%=0,31-0,77; p=0,002). No se observó asociación entre miRNA-146a rs2910164 o miRNA-499 rs3746444 con riesgo de LES.

Conclusión

Este estudio demuestra asociaciones entre los polimorfismos de miRNA-146a e IRAK1 y el riesgo de LES. En el futuro se necesitan estudios más amplios sobre estas asociaciones para garantizar nuestros resultados.

Palabras clave:
miRNA-146a
miRNA-499
IRAK1
Lupus eritematoso sistémico
Predisposición
Susceptibilidad
Texto completo
Introduction

Systemic lupus erythematosus (SLE) is a typical chronic autoimmune disease with a wide range of clinical manifestations and is characterized by the production of autoantibodies against nuclear self-antigens.1,2 Although various autoantibodies production may be observed in SLE individuals, the antinuclear antibody (ANA)3 is commonly used as a serological marker to diagnose SLE. The etiopathogenesis of SLE is incompletely known. Nonetheless, genetic factors seem to play a pivotal part in disease susceptibility.

MicroRNAs (miRNAs) are highly conserved endogenous non-coding small RNA molecules and regulate the expression of protein-coding genes by either translational repression or messenger RNA degradation.4 Among these, miR-146a and miR-499, are two widely reported genes that significantly contribute to autoimmune diseases through their functional roles in modulating both innate and adaptive immune responses.5–8 Therefore, both miRNAs could potentially responsible to the development and progression of SLE.

Interleukin (IL)-1 receptor-associated kinase (IRAK1) and tumour necrosis factor (TNF) receptor-associated factor 6 (TRAF6) have been reported as targets of miRNA-146a,9 whereas miRNA-499 targets several factors including IL-17 receptor B (IL-17RB),10,11 IL-23a,12 IL-2R,12 IL-6,12,13 IL-2,12 IL-18R,12 and peptidyl arginine deiminase type 4 (PADI4),14 in which all of these inflammatory mediators play crucial role in progressing the pathogenesis of autoimmune diseases, including SLE.

Sequence variations observed in miRNAs have been implicated to influence the disease outcome.3 This is possibly because single nucleotide polymorphisms (SNPs) within miRNAs region may alter their expression and functions,3,12 which then resulting in differential regulation of its target protein. Functional SNPs in both miR-146a and miR-499 genes have been evaluated in SLE patients from different populations.12,15,16 However, the results remain inconclusive. Therefore, this study aims to assess the relationship between miR-146a, miR-499 and IRAK1 polymorphism and the risk of SLE.

Methods

Meta-analysis was performed in accordance to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines. Records were identified through electronic databases dated up to September 2020 with search terms such as “miRNA-146a”, “miRNA-499”, “IRAK1” and “SLE”. Studies were included on the basis of the following criteria: (1) aims to evaluate the association between gene polymorphism with predisposition to SLE; (2) conducted with a case-control design.

Meta-analysis for each gene polymorphism was performed for two or more studies. Genotypic frequency was tested for deviation from the Hardy–Weinberg equilibrium (HWE) in the control subjects. The association between gene polymorphism with predisposition to SLE was calculated by pooled odds ratio (OR) and 95% confidence interval (CI). The Z test was used to evaluate the significance of the pooled effect size. Study heterogeneity was evaluated using Q test and I2 statistic. A significant Q-statistic (p<0.10) indicated heterogeneity across studies, with substantial heterogeneity indicated by an I2 value over 50%. The fixed-effect model (FEM) was used in the absence of heterogeneity, while the random-effect model (REM) was implemented if heterogeneity was present. A funnel plot and Begg's test were used to investigate the publication bias if the pooled effect size consisted of 10 or more studies. The value of 0.05 was indicative of the statistical significance. The Newcastle–Ottawa scale (NOS) was used to assess the study quality, in which a score ≥7 is considered a good study.17–34

Results

A total of 37 articles were screened, among which 27 were reviewed. Sixteen studies were excluded due to their absent relation to miRNA-146a, miRNA-499, and IRAK1 polymorphisms or the inability to extract the data. Eight studies were then included in this meta-analysis3,5,12,15,16,35–37 (Fig. 1). A total of 5237 (SLE: 2226, control 3011), 2642 (SLE: 1174, control: 1468), 709 (SLE: 263; control: 446), and 1534 (SLE: 747; control: 787) subjects for miRNA-146a rs2910164, miRNA-146a rs2431697, miRNA-499 rs3746444, and IRAK1 rs3027898 polymorphisms, respectively, were further analyzed. All studies complied with the HWE (Table 1). Details of the retrieved studies are depicted in Table 1.

Fig. 1.

PRISMA flow diagram of study selection process for the association between miR-146a, miR-499 and IRAK1 polymorphism and the risk of SLE.

(0,17MB).
Table 1.

Characteristics of the studies included in the meta-analysis.

Study  Country  Ethnicity  NumbersGenotype frequencyNOS  p-HWE 
      SLE  Control  SLEControl   
miRNA-146a rs2910164    GG  GC  CC  GG  GC  CC     
Zhang et al.  China  Asian  213  209  33  101  79  23  104  82  0.239 
Löfgren et al.  Sweden  European  1109  1428  623  422  64  819  531  78  0.502 
Jimenez-Morales et al.  Mexico  Mexican  367  531  163  167  37  236  229  66  0.369 
Labib et al.  Egypt  Egyptian  80  120  32  40  26  56  38  0.530 
Aleman-Avilla et al.  Mexico  Mexican  407  486  168  179  60  218  222  46  0.327 
Ahmadi et al.  Iran  Asian  50  237  28  18  113  98  28  0.344 
miRNA-146a rs2431697    TT  TC  CC  TT  TC  CC     
Löfgren et al.  Sweden  European  1109  1428  423  524  157  434  718  240  0.052 
Fouda et al.  Egypt  Egyptian  65  40  25  29  11  22  12  0.428 
miRNA-499 rs3746444    TT  TC  CC  TT  TC  CC     
Zhang et al.  China  Asian  213  209  157  50  158  45  0.214 
Ahmadi et al.  Iran  Asian  50  237  27  23  145  83  0.495 
IRAK1 rs3027898    CC  CA  AA  CC  CA  AA     
Labib et al.  Egypt  Egyptian  80  120  28  24  28  14  32  30  0.300 
Zhai et al.  China  Asian  667  667  437  167  21  421  202  40  0.040 

Pooled results on the associations between miRNA-146a, miRNA-499, and IRAK1 polymorphisms with SLE are shown in Table 2. We failed to show any significant association between miRNA-146a rs2910164 and miRNA-499 rs3746444 in any inheritance models (Table 2). However, we found that patients harbouring C allele of miRNA-146a rs2431697 were significantly lowered SLE predisposition (CC vs. TC+TT, OR=0.77, 95% CI=0.62–0.95, p=0.019; TC vs. CC+TT, OR=0.84, 95% CI=0.71–0.98, p=0.027; and TC vs. TT, OR=0.73, 95% CI=0.61–0.86, p=0.000, Table 2). In addition, IRAK1, target of miRNA-146a, was also examined. Patients with the A allele and AA genotype of rs3027898 were significantly decreased SLE susceptibility compare to the C allele and CC genotype, respectively (A vs. C, OR=0.73, 95% CI=0.60–0.87, p=0.001; AA vs. CA+CC, OR=0.64, 95% CI=0.42–0.97, p=0.037; AA+CA vs. CC, OR=0.71, 95% CI=0.56–0.88, p=0.003, and AA vs. CC, OR=0.49, 95% CI=0.31–0.77, p=0.002, Table 2). Whereas no significant difference between the AC and AA genotype (Table 2). No evidence of publication bias was observed in any models in each gene polymorphisms (Table 2). Because we failed to show any association between miRNA-499 with SLE risk, genetic polymorphism of miRNA-499 target was not further evaluated.

Table 2.

Meta-analysis of the associations between the miRNA-146a, miRNA-499, IRAK1 polymorphisms and SLE.

Genetic model  Ethnicity  No. of studies  Test of associationTest of heterogeneityPublication bias (p-value) 
      OR  95% CI  p-value  Model  p-value  I2 (%)   
miRNA-146a rs2910164
C vs. GOverall  0.88  0.72–1.09  0.264  REM  0.000  77.31  0.100 
Asian  0.83  0.65–1.06  0.141  FEM  0.574  NA 
Mexican  1.07  0.84–1.37  0.557  REM  0.082  66.93  NA 
CC vs. GC+GGOverall  0.85  0.57–1.26  0.431  REM  0.001  74.07  0.188 
Asian  0.87  0.60–1.27  0.494  FEM  0.576  NA 
Mexican  1.14  0.55–2.36  0.712  REM  0.014  83.35  NA 
CC+GC vs. GGOverall  0.90  0.72–1.12  0.348  REM  0.031  59.11  0.045 
Asian  0.68  0.45–1.04  0.079  FEM  0.918  NA 
Mexican  1.07  0.89–1.30  0.442  FEM  0.452  NA 
GC vs. CC+GGOverall  1.01  0.90–1.13  0.821  FEM  0.878  0.460 
Asian  0.88  0.63–1.22  0.452  FEM  0.754  NA 
Mexican  1.01  0.83–1.22  0.892  FEM  0.390  NA 
CC vs. GGOverall  0.76  0.46–1.24  0.277  REM  0.000  78.33  0.113 
Asian  0.64  0.37–1.11  0.115  FEM  0.815  NA 
Mexican  1.17  0.57–2.41  0.660  REM  0.021  81.21  NA 
CC vs. GCOverall  0.90  0.63–1.29  0.593  REM  0.015  64.21  0.252 
Asian  0.96  0.65–1.42  0.858  FEM  0.699  NA 
Mexican  1.11  0.53–2.31  0.763  REM  0.019  81.75  NA 
GC vs. GGOverall  0.99  0.88–1.12  0.964  FEM  0.348  10.49  0.016 
Asian  0.70  0.45–1.09  0.120  FEM  0.840  NA 
Mexican  1.05  0.86–1.28  0.624  FEM  0.964  NA 
miRNA-146a rs2431697
C vs. T  Overall  0.67  0.40–1.10  0.115  REM  0.072  68.97  NA 
CC vs. TC+TT  Overall  0.77  0.62–0.95  0.019  FEM  0.293  9.28  NA 
CC+TC vs. TT  Overall  0.52  0.21–1.26  0.149  REM  0.066  70.21  NA 
TC vs. CC+TT  Overall  0.84  0.71–0.98  0.027  FEM  0.540  NA 
CC vs. TT  Overall  0.45  0.15–1.28  0.137  REM  0.076  68.16  NA 
CC vs. TC  Overall  0.88  0.70–1.10  0.285  FEM  0.623  NA 
TC vs. TT  Overall  0.73  0.61–0.86  0.000  FEM  0.112  60.32  NA 
miRNA-499 rs3746444
C vs. T  Overall  1.08  0.79–1.48  0.595  FEM  0.945  NA 
CC vs. TC+TT  Overall  0.80  0.27–2.33  0.691  FEM  0.368  NA 
CC+TC vs. TT  Overall  1.18  0.82–1.68  0.363  FEM  0.613  NA 
TC vs. CC+TT  Overall  1.26  0.87–1.82  0.211  FEM  0.376  NA 
CC vs. TT  Overall  0.84  0.28–2.45  0.752  FEM  0.415  NA 
CC vs. TC  Overall  0.71  0.23–2.16  0.550  FEM  0.323  NA 
TC vs. TT  Overall  1.23  0.85–1.78  0.256  FEM  0.466  NA 
IRAK1 rs3027898
A vs. C  Overall  0.73  0.60–0.87  0.001  FEM  0.602  NA 
AA vs. CA+CC  Overall  0.64  0.42–0.97  0.037  FEM  0.328  NA 
AA+CA vs. CC  Overall  0.71  0.56–0.88  0.003  FEM  0.143  53.32  NA 
CA vs. AA+CC  Overall  0.80  0.63–1.00  0.053  FEM  0.336  NA 
AA vs. CC  Overall  0.49  0.31–0.77  0.002  FEM  0.873  NA 
AA vs. CA  Overall  0.81  0.51–1.27  0.372  FEM  0.157  50.17  NA 
CA vs. CC  Overall  0.61  0.30–1 .23  0.170  REM  0.089  65.52  NA 

Bold text indicates a statistically significant difference with a p-value less than 0.05.

Discussion

Our current study addresses the possible association between the miR-146a, miRNA-499, and IRAK1 polymorphism and its susceptibility to SLE. We found that the individuals carrying the C and A allele of rs2431697 and rs3027898, respectively, displayed protection against the occurrence of SLE, thereby implying that both miR-146a and its target protein, IRAK1, are crucial in the pathogenesis of SLE. Similar to previously reported studies38–41; our updated meta-analysis strengthens the notion that the miR-146a rs2910164 was not responsible for SLE predisposition.

Functional analysis revealed that numerous SNPs within miR-146a have been shown to affect the expression level of mature miR-146a.16 For example, the T allele of rs2431697 decreases matures miR-146a expression.16 Downregulation of human-miR-146a is associated to the manifestations of SLE by deregulating the activation of the interferon (IFN) pathway.42,43 This may be due to several reason such as the decreasing expression of miR-146a and subsequent upregulation of IRAK1 and nuclear factor-κB (NF-κB) that may stimulate transcription of several genes-related inflammatory responses.44 Hence, it suggests the presence of inverse relationship between miR-146a expression level and SLE. Moreover, a study also identified that the biological axis between miR-146a and TRAF6 is closely linked to the SLE progression.45 Additionally, mutant or alternative type (T allele) carriers of rs2431697 evidently increased the coronary artery disease risk, but not the severity of the disease.46 Compiling to our findings, this implies that the rs2431697 is important in determining SLE susceptibility. Further studies investigating the effect of rs2431697 and SLE progression are required.

Although functional analysis of rs3027898 in IRAK1 is currently unavailable,47 it is possible to speculate that the C allele may contribute to the upregulation of IRAK1. Indeed, hyperactivation of IRAK1 in CD4+ T cells was observed in SLE individuals.48 While we failed to show any association between rs2910164 with SLE predisposition, other polymorphism such as rs57095329 in miR-146a is correlated with SLE.40,39 Luo et al.43 have successfully demonstrated the attenuation of miR-146 expression is partly influenced by low binding capability to Ets-1 due to conformational changes in the promoter region of rs57095329.

Association between miRNA-499 polymorphism with SLE was also evaluated, but no association was observed. Interestingly, however, patients harbouring the T allele of rs3746444 had low RA risk.39 Additionally, Lu et al.49 demonstrated that rs3746444 polymorphism is closely linked to RA susceptibility in Mediterranean populations. Nonetheless, further studies are still required to determine whether the rs3746444 polymorphisms contribute to SLE susceptibility in different ethnic groups.

The present study has some limitations. Firstly, some of the pooled studies were generated from the limited number of included studies, thus the result may not be precise. Secondly, methodological variation of SNP identification and the opposite findings between studies may influence the results obtained in this particular study. Thirdly, because SLE is a complex disease, other factors, including, genetics, hormonal, environmental, and immune response/status should be closely examined.

In conclusion, our study demonstrates the association between miRNA-146a and IRAK1 polymorphisms with SLE risk. Further investigations evaluating functional analysis of miRNA-146a and IRAK1 in individuals with SLE and controls are necessary to clarify the role of the microRNA and its target gene in the etiology of SLE.

Funding

This research received no external funding.

Conflicts of interest

None to declare.

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