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Review Articles

Identifying the differentially expressed microRNAs in autoimmunity: A systemic review and meta-analysis

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Pages 122-136 | Received 16 Oct 2019, Accepted 26 Dec 2019, Published online: 06 Jan 2020

Reference

  • Panousis NI, Bertsias GK, Ongen H, et al. Combined genetic and transcriptome analysis of patients with SLE: distinct, targetable signatures for susceptibility and severity. Ann Rheum Dis. 2019;78(8):1079–1089.
  • Saito Y, Saito H, Liang G, et al. Epigenetic alterations and microRNA misexpression in cancer and autoimmune diseases: a critical review. Clinic Rev Allerg Immunol. 2014;47(2):128–135.
  • Canas CA, et al. Epigenetics changes associated to environmental triggers in autoimmunity. Autoimmunity. 2016;49(1):1–11.
  • Doria A, Iaccarino L, Ghirardello A, et al. Long-term prognosis and causes of death in systemic lupus erythematosus. Am J Med. 2006;119(8):700–706.
  • Yen EY, Singh RR. Brief report: lupus-an unrecognized leading cause of death in young females: a population-based study using Nationwide Death Certificates, 2000–2015. Arthritis Rheumatol. 2018;70(8):1251–1255.
  • Jorge AM, Lu N, Zhang Y, et al. Unchanging premature mortality trends in systemic lupus erythematosus: a general population-based study (1999–2014). Rheumatology (Oxford). 2018;57(2):337–344.
  • Long H, Yin H, Wang L, et al. The critical role of epigenetics in systemic lupus erythematosus and autoimmunity. J Autoimmun. 2016;74:118–138.
  • Chang S-H, Kim T-J, Kim Y, et al. Impacts of GFP-FoxP3(+) regulatory T cells on lupus hallmarks differ by genetic background and type of GFP knock-in. Autoimmunity. 2019;52(5–6):199–207.
  • de la Rica L, Urquiza JM, Gómez-Cabrero D, et al. Identification of novel markers in rheumatoid arthritis through integrated analysis of DNA methylation and microRNA expression. J Autoimmun. 2013;41:6–16.
  • Miao C, et al. DNA hypermethylation of SFRP2 influences the pathology of rheumatoid arthritis through the canonical Wnt signaling in model rats. Autoimmunity. 2018;51(7):1–14.
  • Xie Z, Chang C, Zhou Z. Molecular mechanisms in autoimmune type 1 diabetes: a critical review. Clinic Rev Allerg Immunol. 2014;47(2):174–192.
  • Parackova Z, Kayserova J, Danova K, et al. T regulatory lymphocytes in type 1 diabetes: Impaired CD25 expression and IL-2 induced STAT5 phosphorylation in pediatric patients. Autoimmunity. 2016;49(8):523–531.
  • Grolleau-Julius A, Ray D, Yung RL. The role of epigenetics in aging and autoimmunity. Clinic Rev Allerg Immunol. 2010;39(1):42–50.
  • Zhao M, Liu S, Luo S, et al. DNA methylation and mRNA and microRNA expression of SLE CD4+ T cells correlate with disease phenotype. J Autoimmun. 2014;54:127–136.
  • Lu Q. Unmet needs in autoimmunity and potential new tools. Clinic Rev Allerg Immunol. 2014;47(2):111–118.
  • Correa Freitas E, Evelyn Karnopp T, de Souza Silva JM, et al. Vitamin D supplementation ameliorates arthritis but does not alleviates renal injury in pristane-induced lupus model. Autoimmunity. 2019;52(2):69–77.
  • Wei J-W, Huang K, Yang C, et al. Non-coding RNAs as regulators in epigenetics (Review). Oncol Rep. 2017;37(1):3–9.
  • Aslani S, Mahmoudi M, Karami J, et al. Epigenetic alterations underlying autoimmune diseases. Autoimmunity. 2016;49(2):69–83.
  • Zan H, Tat C, Casali P. MicroRNAs in lupus. Autoimmunity. 2014;47(4):272–285.
  • O'Reilly S. miRNA-29a in systemic sclerosis: a valid target. Autoimmunity. 2015;48(8):511–512.
  • Jafarinejad-Farsangi S, Gharibdoost F, Farazmand A, et al. MicroRNA-21 and microRNA-29a modulate the expression of collagen in dermal fibroblasts of patients with systemic sclerosis. Autoimmunity. 2019;52(3):108–116.
  • Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat Rev Genet. 2008;9(2):102–114.
  • Iborra M, Bernuzzi F, Invernizzi P, et al. MicroRNAs in autoimmunity and inflammatory bowel disease: crucial regulators in immune response. Autoimmun Rev. 2012;11(5):305–314.
  • Ando Y, Yang G-X, Kenny TP, et al. Overexpression of microRNA-21 is associated with elevated pro-inflammatory cytokines in dominant-negative TGF-beta receptor type II mouse. J Autoimmun. 2013;41:111–119.
  • Miao C, Yu H, Chang J, et al. miR-148b-3p affects the pathogenesis of adjuvant-induced arthritis rats through the direct target DNMT1. Autoimmunity. 2018;51(2):43–52.
  • Liu A, La Cava A. Epigenetic dysregulation in systemic lupus erythematosus. Autoimmunity. 2014;47(4):215–219.
  • Eleftheriadis T, Pissas G, Zarogiannis S, et al. Crystalline silica activates the T-cell and the B-cell antigen receptor complexes and induces T-cell and B-cell proliferation. Autoimmunity. 2019;52(3):136–143.
  • Podolska MJ, Mahajan A, Knopf J, et al. Autoimmune, rheumatic, chronic inflammatory diseases: neutrophil extracellular traps on parade. Autoimmunity. 2018;51(6):281–287.
  • Divekar AA, Dubey S, Gangalum PR, et al. Dicer insufficiency and microRNA-155 overexpression in lupus regulatory T cells: an apparent paradox in the setting of an inflammatory milieu. J Immunol. 2011;186(2):924–930.
  • Kim J, Inoue K, Ishii J, et al. A MicroRNA feedback circuit in midbrain dopamine neurons. Science. 2007;317(5842):1220–1224.
  • Ren D, Liu F, Dong G, et al. Activation of TLR7 increases CCND3 expression via the downregulation of miR-15b in B cells of systemic lupus erythematosus. Cell Mol Immunol. 2016;13(6):764–775.
  • Nagalakshmi VK, Ren Q, Pugh MM, et al. Dicer regulates the development of nephrogenic and ureteric compartments in the mammalian kidney. Kidney Int. 2011;79(3):317–330.
  • Saeki M, Watanabe M, Inoue N, et al. DICER and DROSHA gene expression and polymorphisms in autoimmune thyroid diseases. Autoimmunity. 2016;49(8):514–522.
  • O'Reilly S. MicroRNAs in fibrosis: opportunities and challenges. Arthritis Res Ther. 2016;18:11.
  • Chung ACK, Huang XR, Meng X, et al. miR-192 mediates TGF-beta/Smad3-driven renal fibrosis. JASN. 2010;21(8):1317–1325.
  • Sun HY, Lv AK, Yao H. Relationship of miRNA-146a to primary Sjogren's syndrome and to systemic lupus erythematosus: a meta-analysis. Rheumatol Int. 2017;37(8):1311–1316.
  • Schulz J, Takousis P, Wohlers I, et al. Meta-analyses identify differentially expressed microRNAs in Parkinson's disease. Ann Neurol. 2019;85(6):835–851.
  • Jeong DY, Lee SW, Park YH, et al. Genetic variation and systemic lupus erythematosus: a field synopsis and systematic meta-analysis. Autoimmun Rev. 2018;17(6):553–566.
  • Belbasis L, Dosis V, Evangelou E. Elucidating the environmental risk factors for rheumatic diseases: an umbrella review of meta-analyses. Int J Rheum Dis. 2018;21(8):1514–1524.
  • Whiting PF. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–536.
  • Dinnes J, Deeks J, Kirby J, et al. A methodological review of how heterogeneity has been examined in systematic reviews of diagnostic test accuracy. Health Technol Assess. 2005;9(12):1–113.
  • DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–188.
  • Friedrich M, Pracht K, Mashreghi M-F, et al. The role of the miR-148/-152 family in physiology and disease. Eur J Immunol. 2017;47(12):2026–2038.
  • Gonzalez-Martin A, Adams BD, Lai M, et al. The microRNA miR-148a functions as a critical regulator of B cell tolerance and autoimmunity. Nat Immunol. 2016;17(4):433–440.
  • Wei B, Pei G. microRNAs: critical regulators in Th17 cells and players in diseases. Cell Mol Immunol. 2010;7(3):175–181.
  • Zhang P, Lu Q. Genetic and epigenetic influences on the loss of tolerance in autoimmunity. Cell Mol Immunol. 2018;15(6):575–585.
  • Qiu R, et al. Regulatory T Cell Plasticity and Stability and Autoimmune Diseases. Clin Rev Allergy Immunol. 2018.
  • Ruan Q, Wang T, Kameswaran V, et al. The microRNA-21-PDCD4 axis prevents type 1 diabetes by blocking pancreatic beta cell death. Proc Natl Acad Sci USA. 2011;108(29):12030–12035.
  • Stagakis E, Bertsias G, Verginis P, et al. Identification of novel microRNA signatures linked to human lupus disease activity and pathogenesis: miR-21 regulates aberrant T cell responses through regulation of PDCD4 expression. Ann Rheum Dis. 2011;70(8):1496–1506.
  • Sheedy FJ, Palsson-McDermott E, Hennessy EJ, et al. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol. 2010;11(2):141–147.
  • Dong L, Wang X, Tan J, et al. Decreased expression of microRNA-21 correlates with the imbalance of Th17 and Treg cells in patients with rheumatoid arthritis. J Cell Mol Med. 2014;18(11):2213–2224.
  • Lu L-F, Thai T-H, Calado DP, et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity. 2009;30(1):80–91.
  • Wu H, Deng Y, Feng Y, et al. Epigenetic regulation in B-cell maturation and its dysregulation in autoimmunity. Cell Mol Immunol. 2018;15(7):676–684.
  • Zheng Y, Wang Z, Zhou Z. miRNAs: novel regulators of autoimmunity-mediated pancreatic beta-cell destruction in type 1 diabetes. Cell Mol Immunol. 2017;14(6):488–496.
  • Metzinger-Le Meuth V, Metzinger L. miR-223 and other miRNA's evaluation in chronic kidney disease: innovative biomarkers and therapeutic tools. Noncoding RNA Res. 2019;4(1):30–35.
  • Moran-Moguel MC, Petarra-del Rio S, Mayorquin-Galvan EE, et al. Rheumatoid Arthritis and miRNAs: a Critical Review through a Functional View. J Immunol Res. 2018;2018:1–16.
  • Luo X, Zhang L, Li M, et al. The role of miR-125b in T lymphocytes in the pathogenesis of systemic lupus erythematosus. Clin Exp Rheumatol. 2013;31(2):263–271.
  • Rogatsky I, Chandrasekaran U, Manni M, et al. Epigenetics and the IRFs: a complex interplay in the control of immunity and autoimmunity. Autoimmunity. 2014;47(4):242–255.
  • Murata K, Furu M, Yoshitomi H, et al. Comprehensive microRNA analysis identifies miR-24 and miR-125a-5p as plasma biomarkers for rheumatoid arthritis. PLoS One. 2013;8(7):e69118.
  • Ofori JK, Salunkhe VA, Bagge A, et al. Elevated miR-130a/miR130b/miR-152 expression reduces intracellular ATP levels in the pancreatic beta cell. Sci Rep. 2017;7:44986.
  • Conserva F, Pontrelli P, Accetturo M, et al. The pathogenesis of diabetic nephropathy: focus on microRNAs and proteomics. J Nephrol. 2013;26(5):811–820.
  • Dunaeva M, Blom J, Thurlings R, et al. Circulating serum miR-223-3p and miR-16-5p as possible biomarkers of early rheumatoid arthritis. Clin Exp Immunol. 2018;193(3):376–385.
  • Incorvaia E, Sicouri L, Petersen-Mahrt SK, et al. Hormones and AID: balancing immunity and autoimmunity. Autoimmunity. 2013;46(2):128–137.
  • Yan S, Yim LY, Lu L, et al. MicroRNA regulation in systemic lupus erythematosus pathogenesis. Immune Netw. 2014;14(3):138–148.
  • Wang Z, Heid B, Dai R, et al. Similar dysregulation of lupus-associated miRNAs in peripheral blood mononuclear cells and splenic lymphocytes in MRL/lpr mice. Lupus Sci Med. 2018;5(1):e000290.
  • Khoshmirsafa M, Kianmehr N, Falak R, et al. Elevated expression of miR-21 and miR-155 in peripheral blood mononuclear cells as potential biomarkers for lupus nephritis. Int J Rheum Dis. 2019;22(3):458–467.
  • D'Amico F, Skarmoutsou E, Mazzarino MC. The sex bias in systemic sclerosis: on the possible mechanisms underlying the female disease preponderance. Clinic Rev Allerg Immunol. 2014;47(3):334–343.
  • Krasselt M, Baerwald C. Sex, symptom severity, and quality of life in rheumatology. Clinic Rev Allerg Immunol. 2019;56(3):346–361.
  • Pennell LM, Galligan CL, Fish EN. Sex affects immunity. J Autoimmun. 2012;38(2–3):J282–91.
  • McDonald JS, Milosevic D, Reddi HV, et al. Analysis of circulating microRNA: preanalytical and analytical challenges. Clin Chem. 2011;57(6):833–840.
  • Motawi TK, Mohsen DA, El-Maraghy SA, et al. MicroRNA-21, microRNA-181a and microRNA-196a as potential biomarkers in adult Egyptian patients with systemic lupus erythematosus. Chem Biol Interact. 2016;260:110–116.
  • Wang W, Mou S, Wang L, et al. Up-regulation of serum MiR-130b-3p level is associated with renal damage in early lupus nephritis. Sci Rep. 2015;5(1):12644.,
  • Wang G, Tam LS, Li EKM, et al. Serum and urinary cell-free MiR-146a and MiR-155 in patients with systemic lupus erythematosus. J Rheumatol. 2010;37(12):2516–2522.
  • Cao W, Qian G, Luo W, et al. miR-125b is downregulated in systemic lupus erythematosus patients and inhibits autophagy by targeting UVRAG. Biomed Pharmacother. 2018;99:791–797.
  • Lu MC, Lai NS, Chen HC, et al. Decreased microRNA(miR)-145 and increased miR-224 expression in T cells from patients with systemic lupus erythematosus involved in lupus immunopathogenesis. Clin Exp Immunol. 2013;171(1):91–99.
  • Su YJ, Tsai NW, Kung CT, et al. Investigation of microRNA in mitochondrial apoptotic pathway in systemic lupus erythematosus. Biomed Res Int. 2018;2018:1–8.
  • Te JL, Dozmorov IM, Guthridge JM, et al. Identification of unique microRNA signature associated with lupus nephritis. PLoS One. 2010;5(5):e10344.
  • Wang H, Peng W, Ouyang X, et al. Circulating microRNAs as candidate biomarkers in patients with systemic lupus erythematosus. Transl Res. 2012;160(3):198–206.
  • Wang X, Zhang C, Wu Z, et al. CircIBTK inhibits DNA demethylation and activation of AKT signaling pathway via miR-29b in peripheral blood mononuclear cells in systemic lupus erythematosus. Arthritis Res Ther. 2018;20(1):118.
  • Dominguez-Gutierrez PR, Ceribelli A, Satoh M, et al. Positive correlation of STAT1 and miR-146a with anemia in patients with systemic lupus erythematosus. J Clin Immunol. 2014;34(2):171–180.
  • Liu D, Zhang N, Zhang X, et al. MiR-410 down-regulates the expression of interleukin-10 by targeting STAT3 in the pathogenesis of systemic lupus erythematosus. Cell Physiol Biochem. 2016;39(1):303–315.
  • Tang Q, Yang Y, Zhao M, et al. Mycophenolic acid upregulates miR-142-3P/5P and miR-146a in lupus CD4 + T cells. Lupus. 2015;24(9):935–942.
  • Pan W, Zhu S, Yuan M, et al. MicroRNA-21 and microRNA-148a contribute to DNA hypomethylation in lupus CD4+ T cells by directly and indirectly targeting DNA methyltransferase 1. J Immunol. 2010;184(12):6773–6781.
  • Rasmussen TK, Andersen T, Bak RO, et al. Overexpression of microRNA-155 increases IL-21 mediated STAT3 signaling and IL-21 production in systemic lupus erythematosus. Arthritis Res Ther. 2015;17(1):154.
  • Wang Y, Liang J, Qin H, et al. Elevated expression of miR-142-3p is related to the pro-inflammatory function of monocyte-derived dendritic cells in SLE. Arthritis Res Ther. 2016;18(1):263.
  • Zhao S, Wang Y, Liang Y, et al. MicroRNA-126 regulates DNA methylation in CD4+ T cells and contributes to systemic lupus erythematosus by targeting DNA methyltransferase 1. Arthritis Rheum. 2011;63(5):1376–1386.
  • Ding S, Liang Y, Zhao M, et al. Decreased microRNA-142-3p/5p expression causes CD4+ T cell activation and B cell hyperstimulation in systemic lupus erythematosus. Arthritis Rheum. 2012;64(9):2953–2963.
  • Liu L, Liu Y, Yuan M, et al. Elevated expression of microRNA-873 facilitates Th17 differentiation by targeting forkhead box O1 (Foxo1) in the pathogenesis of systemic lupus erythematosus. Biochem Biophys Res Commun. 2017;492(3):453–460.
  • Sun X-G, Tao J-H, Xiang N, et al. Negative correlation between miR-326 and Ets-1 in regulatory t cells from new-onset SLE patients. Inflammation. 2016;39(2):822–829.
  • Luo S, Liu Y, Liang G, et al. The role of microRNA-1246 in the regulation of B cell activation and the pathogenesis of systemic lupus erythematosus. Clin Epigenetics. 2015;7:24.
  • Chen JQ, Papp G, Póliska S, et al. MicroRNA expression profiles identify disease-specific alterations in systemic lupus erythematosus and primary Sjogren's syndrome. PLoS One. 2017;12(3):e0174585.
  • Qingjuan L, Xiaojuan F, Wei Z, et al. miR-148a-3p overexpression contributes to glomerular cell proliferation by targeting PTEN in lupus nephritis. Am J Physiol Cell Physiol. 2016;310(6):C470–8.
  • Costa-Reis P, Russo PA, Zhang Z, et al. The role of microRNAs and human epidermal growth factor receptor 2 in proliferative lupus nephritis. Arthritis Rheumatol. 2015;67(9):2415–2426.
  • Krasoudaki E, Banos A, Stagakis E, et al. Micro-RNA analysis of renal biopsies in human lupus nephritis demonstrates up-regulated miR-422a driving reduction of kallikrein-related peptidase 4. Nephrol Dial Transplant. 2016;31(10):1676–1686.
  • Liu J, Zhu L, Xie G-l, et al. Let-7 miRNAs modulate the activation of NF-kappaB by targeting TNFAIP3 and are involved in the pathogenesis of lupus nephritis. PLoS One. 2015;10(6):e0121256.
  • Zhu S, Pan W, Song X, et al. The microRNA miR-23b suppresses IL-17-associated autoimmune inflammation by targeting TAB2, TAB3 and IKK-alpha. Nat Med. 2012;18(7):1077–1086.
  • Abulaban KM, Fall N, Nunna R, et al. Relationship of cell-free urine MicroRNA with lupus nephritis in children. Pediatr Rheumatol. 2016;14(1):4.
  • Wang G, Tam LS, Kwan BCH, et al. Expression of miR-146a and miR-155 in the urinary sediment of systemic lupus erythematosus. Clin Rheumatol. 2012;31(3):435–440.
  • Perez-Hernandez J, Forner MJ, Pinto C, et al. Increased urinary exosomal micrornas in patients with systemic lupus erythematosus. PLoS One. 2015;10(9):e0138618.
  • Sole C, et al. miR-29c in urinary exosomes as predictor of early renal fibrosis in lupus nephritis. Nephrol Dial Transplant. 2015;30(9):1488–1496.
  • Balzano F, Deiana M, Dei Giudici S, et al. MicroRNA expression analysis of centenarians and rheumatoid arthritis patients reveals a common expression pattern. Int J Med Sci. 2017;14(7):622–628.
  • Ormseth MJ, Solus JF, Vickers KC, et al. Utility of select plasma microRNA for disease and cardiovascular risk assessment in patients with rheumatoid arthritis. J Rheumatol. 2015;42(10):1746–1751.
  • Murata K, Yoshitomi H, Tanida S, et al. Plasma and synovial fluid microRNAs as potential biomarkers of rheumatoid arthritis and osteoarthritis. Arthritis Res Ther. 2010;12(3):R86.
  • Ouboussad L, Hunt L, Hensor EMA, et al. Profiling microRNAs in individuals at risk of progression to rheumatoid arthritis. Arthritis Res Ther. 2017;19(1):288.
  • Bogunia-Kubik K, Wysoczańska B, Piątek D, et al. Significance of polymorphism and expression of mir-146a and nfkb1 genetic variants in patients with rheumatoid arthritis. Arch Immunol Ther Exp (Exp), 2016;64(S1):131–136.
  • Ciccacci C, Conigliaro P, Perricone C, et al. Polymorphisms in STAT-4, IL-10, PSORS1C1, PTPN2 and MIR146A genes are associated differently with prognostic factors in Italian patients affected by rheumatoid arthritis. Clin Exp Immunol. 2016;186(2):157–163.
  • Hruskova V, Jandova R, Vernerova L, et al. MicroRNA-125b: association with disease activity and the treatment response of patients with early rheumatoid arthritis. Arthritis Res Ther. 2016;18(1):124.
  • Pauley KM, Satoh M, Chan AL, et al. Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res Ther. 2008;10(4):R101.
  • Liu X, Ni S, Li C, et al. Circulating microRNA-23b as a new biomarker for rheumatoid arthritis. Gene. 2019;712:143911.
  • Fulci V, Scappucci G, Sebastiani GD, et al. miR-223 is overexpressed in T-lymphocytes of patients affected by rheumatoid arthritis. Hum Immunol. 2010;71(2):206–211.
  • Ayeldeen G, Nassar Y, Ahmed H, et al. Possible use of miRNAs-146a and -499 expression and their polymorphisms as diagnostic markers for rheumatoid arthritis. Mol Cell Biochem. 2018;449(1–2):145–156.
  • Abo ElAtta AS, Ali YBM, Bassyouni IH, et al. Upregulation of miR-221/222 expression in rheumatoid arthritis (RA) patients: correlation with disease activity. Clin Exp Med. 2019;19(1):47–53.
  • Xia Z, Meng F, Liu Y, et al. Decreased MiR-128-3p alleviates the progression of rheumatoid arthritis by up-regulating the expression of TNFAIP3. Biosci Rep. 2018;38(4).
  • Chen Y-J, Chang W-A, Wu L-Y, et al. Systematic analysis of differential expression profile in rheumatoid arthritis chondrocytes using next-generation sequencing and bioinformatics approaches. Int J Med Sci. 2018;15(11):1129–1142.
  • Lu M-C, Yu C-L, Chen H-C, et al. Increased miR-223 expression in T cells from patients with rheumatoid arthritis leads to decreased insulin-like growth factor-1-mediated interleukin-10 production. Clin Exp Immunol. 2014;177(3):641–651.
  • Rajasekhar M, Olsson AM, Steel KJA, et al. MicroRNA-155 contributes to enhanced resistance to apoptosis in monocytes from patients with rheumatoid arthritis. J Autoimmun. 2017;79:53–62.
  • Smigielska-Czepiel K, van den Berg A, Jellema P, et al. Comprehensive analysis of miRNA expression in T-cell subsets of rheumatoid arthritis patients reveals defined signatures of naive and memory Tregs. Genes Immun. 2014;15(2):115–125.
  • Niimoto T, Nakasa T, Ishikawa M, et al. MicroRNA-146a expresses in interleukin-17 producing T cells in rheumatoid arthritis patients. BMC Musculoskelet Disord. 2010;11(1):209.
  • Zhou Q, Haupt S, Kreuzer JT, et al. Decreased expression of miR-146a and miR-155 contributes to an abnormal Treg phenotype in patients with rheumatoid arthritis. Ann Rheum Dis. 2015;74(6):1265–1274.
  • Alivernini S, Kurowska-Stolarska M, Tolusso B, et al. MicroRNA-155 influences B-cell function through PU.1 in rheumatoid arthritis. Nat Commun. 2016;7:12970.
  • Akhtar N, Singh AK, Ahmed S. MicroRNA-17 suppresses TNF-alpha signaling by interfering with TRAF2 and cIAP2 association in rheumatoid arthritis synovial fibroblasts. J Immunol. 2016;197(6):2219–2228.
  • Nakasa T, Miyaki S, Okubo A, et al. Expression of microRNA-146 in rheumatoid arthritis synovial tissue. Arthritis Rheum. 2008;58(5):1284–1292.
  • Wang Z-C, Lu H, Zhou Q, et al. MiR-451 inhibits synovial fibroblasts proliferation and inflammatory cytokines secretion in rheumatoid arthritis through mediating p38MAPK signaling pathway. Int J Clin Exp Pathol. 2015;8(11):14562–14567.
  • Guo J, Du J, Xing J, et al. miR152 inhibits rheumatoid arthritis synovial fibroblast proliferation and induces apoptosis by targeting ADAM10. Int J Mol Med. 2018;42(1):643–650.
  • Lin J, Huo R, Xiao L, et al. A novel p53/microRNA-22/Cyr61 axis in synovial cells regulates inflammation in rheumatoid arthritis. Arthritis Rheumatol. 2014;66(1):49–59.
  • Wangyang Y, Yi L, Wang T, et al. MiR-199a-3p inhibits proliferation and induces apoptosis in rheumatoid arthritis fibroblast-like synoviocytes via suppressing retinoblastoma 1. Biosci Rep. 2018;38(6):pii: BSR20180982.
  • Liu J, Fei D, Xing J, et al. MicroRNA-29a inhibits proliferation and induces apoptosis in rheumatoid arthritis fibroblast-like synoviocytes by repressing STAT3. Biomed Pharmacother. 2017;96:173–181.
  • Wu J, Fan W, Ma L, et al. miR-708-5p promotes fibroblast-like synoviocytes' cell apoptosis and ameliorates rheumatoid arthritis by the inhibition of Wnt3a/beta-catenin pathway. DDDT. 2018;12:3439–3447.
  • Satake E, Pezzolesi MG, Md Dom ZI, et al. Circulating miRNA profiles associated with hyperglycemia in patients with type 1 diabetes. Diabetes. 2018;67(5):1013–1023.
  • Nielsen LB, Wang C, Sorensen K, et al. Circulating levels of microRNA from children with newly diagnosed type 1 diabetes and healthy controls: evidence that miR-25 associates to residual beta-cell function and glycaemic control during disease progression. Exp Diabetes Res. 2012;2012:896362.
  • Marchand L, Jalabert A, Meugnier E, et al. miRNA-375 a sensor of glucotoxicity is altered in the serum of children with newly diagnosed type 1 diabetes. J Diabetes Res. 2016;2016:1869082.
  • Erener S, Marwaha A, Tan R, et al. Profiling of circulating microRNAs in children with recent onset of type 1 diabetes. JCI Insight. 2017;2(4):e89656.
  • Nabih ES, Andrawes NG. The association between circulating levels of miRNA-181a and pancreatic beta cells dysfunction via SMAD7 in type 1 diabetic children and adolescents. J Clin Lab Anal. 2016;30(5):727–731.
  • Garcia-Diaz DF, Camacho-Guillén P, Codner E, et al. miR15a and miR16 in Chilean type 1 diabetes patients: possible association with apoptosis, inflammatory, or autoimmunity markers. J Endocrinol Invest. 2018;41(9):1083–1088.
  • Takahashi P, Xavier DJ, Evangelista AF, et al. MicroRNA expression profiling and functional annotation analysis of their targets in patients with type 1 diabetes mellitus. Gene. 2014;539(2):213–223.
  • Wang G, Gu Y, Xu N, et al. Decreased expression of miR-150, miR146a and miR424 in type 1 diabetic patients: association with ongoing islet autoimmunity. Biochem Biophys Res Commun. 2018;498(3):382–387.
  • Assmann TS, Duarte GCK, Brondani LA, et al. Polymorphisms in genes encoding miR-155 and miR-146a are associated with protection to type 1 diabetes mellitus. Acta Diabetol. 2017;54(5):433–441.
  • Yang M, Ye L, Wang B, et al. Decreased miR-146 expression in peripheral blood mononuclear cells is correlated with ongoing islet autoimmunity in type 1 diabetes patients 1miR-146. J Diabetes. 2015;7(2):158–165.
  • Zhang Y, Feng Z-P, Naselli G, et al. MicroRNAs in CD4(+) T cell subsets are markers of disease risk and T cell dysfunction in individuals at risk for type 1 diabetes. J Autoimmun. 2016;68:52–61.
  • Barutta F, Tricarico M, Corbelli A, et al. Urinary exosomal microRNAs in incipient diabetic nephropathy. PLoS One. 2013;8(11):e73798.
  • Argyropoulos C, Wang K, McClarty S, et al. Urinary microRNA profiling in the nephropathy of type 1 diabetes. PLoS One. 2013;8(1):e54662.
  • Argyropoulos C, Wang K, Bernardo J, et al. Urinary microRNA profiling predicts the development of microalbuminuria in patients with type 1 diabetes. JCM. 2015;4(7):1498–1517.
  • El-Samahy MH, Adly AA, Elhenawy YI, et al. Urinary miRNA-377 and miRNA-216a as biomarkers of nephropathy and subclinical atherosclerotic risk in pediatric patients with type 1 diabetes. J Diabetes Complications. 2018;32(2):185–192.
  • Ghai V, Wu X, Bheda-Malge A, et al. Genome-wide profiling of urinary extracellular vesicle microRNAs associated with diabetic nephropathy in type 1 diabetes. Kidney Int Rep. 2018;3(3):555–572.
  • Osipova J, Fischer D-C, Dangwal S, et al. Diabetes-associated microRNAs in pediatric patients with type 1 diabetes mellitus: a cross-sectional cohort study. J Clin Endocrinol Metab. 2014;99(9):E1661–E1665.

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