Identification of stress-related microRNA biomarkers in type 2 diabetes mellitus: A systematic review and meta-analysis
2型糖尿病的应激相关microRNA标志物:系统综述与meta分析
Ying-Zhi Liang
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Search for more papers by this authorJia-Jiang-Hui Li
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Search for more papers by this authorHuan-Bo Xiao
Department of Preventive Medicine, Yanjing Medical College, Capital Medical University, Beijing, China
Search for more papers by this authorYan He
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Search for more papers by this authorLing Zhang
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Search for more papers by this authorCorresponding Author
Yu-Xiang Yan
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Correspondence
Yu-Xiang Yan, Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, No. 10 Xitoutiao, You An Men, Beijing 100069, China.
Tel: +86 010 8391 1498
Fax: +86 010 8391 1498
Email: [email protected]
Search for more papers by this authorYing-Zhi Liang
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Search for more papers by this authorJia-Jiang-Hui Li
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Search for more papers by this authorHuan-Bo Xiao
Department of Preventive Medicine, Yanjing Medical College, Capital Medical University, Beijing, China
Search for more papers by this authorYan He
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Search for more papers by this authorLing Zhang
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Search for more papers by this authorCorresponding Author
Yu-Xiang Yan
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Beijing, China
Municipal Key Laboratory of Clinical Epidemiology, Beijing, China
Correspondence
Yu-Xiang Yan, Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, No. 10 Xitoutiao, You An Men, Beijing 100069, China.
Tel: +86 010 8391 1498
Fax: +86 010 8391 1498
Email: [email protected]
Search for more papers by this authorAbstract
enBackground
Many studies have investigated microRNAs (miRNAs) in the detection of type 2 diabetes mellitus (T2DM). Herein, the dysregulated direction of stress-related miRNAs used as biomarkers of T2DM are summarized and analyzed.
Methods
PubMed, EMBASE, ISI Web of Science, and three Chinese databases were searched for case–control miRNA profiling studies about T2DM. A meta-analysis under a random effect was performed. Subgroup analysis was conducted based on different tissues and species. Sensitivity analysis was conducted to confirm the robustness among studies. The effect size was pooled using ln odds ratios (ORs), 95% confidence intervals (95% CIs), and P-values.
Results
The present meta-analysis included 39 case–control studies with a total of 494 miRNAs. Only 33 miRNAs were reported in three or more studies and, of these, 18 were inconsistent in their direction of dysregulation. Two significantly dysregulated miRNAs (let-7 g and miR-155) were identified in the meta-analysis. Four miRNAs (miR-142-3p, miR-155, miR-21, and miR-34c-5p) were dysregulated in patients with T2DM, whereas five miRNAs (miR-146a, miR-199a-3p, miR-200b, miR-29b and miR-30e) were dysregulated in animal models of diabetes. In addition, two dysregulated miRNAs (miR-146a and miR-21) were highly cornea specific and heart specific. In sensitivity analysis, only miR-155 was still significantly dysregulated after removing studies with small sample sizes.
Conclusions
The present meta-analysis revealed that 16 stress-related miRNAs were significantly dysregulated in T2DM. MiR-148b, miR-223, miR-130a, miR-19a, miR-26b and miR-27b were selected as potential circulating biomarkers of T2DM. In addition, miR-146a and miR-21 were identified as potential tissue biomarkers of T2DM.
摘要
zh背景
已有多个研究发现microRNAs(miRNAs)可以作为2型糖尿病的生物标志物, 本文对其中表达失调的应激相关miRNAs进行了归纳和分析。
方法
按检索策略, 系统检索PubMed、EMBASE、ISI Web of Science以及三个中文文献数据库中2型糖尿病相关miRNAs的病例-对照研究。采用随机效应模型进行meta分析, 并根据样本来自的物种和组织进行亚组分析。通过敏感性分析以确认研究结果的稳定性。使用lnORs、95% CI以及P值估计总效应量。
结果
最终研究纳入了39篇文献包括494个应激相关miRNAs。在3个及以上研究中均被报道的仅有33个miRNAs, 其中18个表达变化方向不一致, 通过meta分析, 确定其中let-7g和 miR-155与2型糖尿病显著关联。亚组分析显示, miR-142-3p、miR-155、miR-21和miR-34c-5p在2型糖尿病患者中的表达有显著性差异, miR-146a、miR-199a-3p、miR-200b、miR-29b和miR-30e在2型糖尿病动物模型中的表达有显著性差异。此外, miR-146a和miR-21分别具有角膜及心脏组织特异性。敏感性分析结果显示仅miR-155与总体分析结果一致。
结论
本研究发现16个应激相关miRNAs在2型糖尿病中存在显著表达失调。其中miR-148b、miR-223、miR-130a、miR-19a、miR-26b和miR-27b可作为潜在的循环标志物, miR-146a和miR-21则可作为潜在的组织生物标志物。
Supporting Information
Filename | Description |
---|---|
jdb12643-sup-0001-AppendixS1.docxWord 2007 document , 70.3 KB | Table S1. Characteristics of human miRNA expression profiling studies. Table S2. Characteristics of animal miRNA expression profiling studies. Table S3. Quality assessment according to the MIAME guidelines for microarray data. Table S4. Quality assessment according to the MIQE guidelines for quantitative real-time PCR experiments. Table S5. Subgroup meta-analysis of 11 miRNAs in human profiling studies. Table S6. Subgroup meta-analysis of 13 miRNAs in animal profiling studies. Table S7. Direction dysregulation of six miRNAs reported in both human and animal profiling studies. Table S8. Subgroup meta-analysis of 10 miRNAs in circulating blood. Table S9. Subgroup meta-analysis of 10 miRNAs in heart tissue. Table S10. Statistically significant dysregulation of miRNAs in different tissues. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1Winer N, Sowers JR. Epidemiology of diabetes. J Clin Pharmacol. 2004; 44: 397–405.
- 2Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract. 2014; 105: 141–150.
- 3Cumbie BC, Hermayer KL. Current concepts in targeted therapies for the pathophysiology of diabetic microvascular complications. Vasc Health Risk Manag. 2007; 3: 823–832.
- 4Gnudi L. Cellular and molecular mechanisms of diabetic glomerulopathy. Nephrol Dial Transplant. 2012; 27: 2642–2649.
- 5Donath MY. Targeting inflammation in the treatment of type 2 diabetes: Time to start. Nat Rev Drug Discov. 2014; 13: 465–476.
- 6Kultz D. Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol. 2005; 67: 225–257.
- 7Milisav I, Poljšak B, Ribarič S. Reduced risk of apoptosis: Mechanisms of stress responses. Apoptosis. 2017; 22: 265–283.
- 8Anthony KL, Phillip AS. MicroRNA functions in stress responses. Mol Cell. 2010; 40: 205–215.
- 9Pickering TG. Mental stress as a causal factor in the development of hypertension and cardiovascular disease. Curr Hypertens Rep. 2001; 3: 249–254.
- 10Black PH. The inflammatory consequences of psychologic stress: Relationship to insulin resistance, obesity, atherosclerosis and diabetes mellitus, type II. Med Hypotheses. 2006; 67: 879–891.
- 11Dhabhar FS, Saul AN, Holmes TH et al. Highanxious individuals show increased chronic stress burden, decreased protective immunity, and increased cancer progression in a mouse model of squamous cell carcinoma. PLoS One. 2012; 7: e33069.
- 12Arnett MG, Muglia LM, Laryea G, Muglia LJ. Genetic approaches to hypothalamic–pituitary-adrenal axis regulation. Neuropsychopharmacology. 2016; 41: 245–260.
- 13Collares CV, Evangelista AF, Xavier DJ et al. Identifying common and specific microRNAs expressed in peripheral blood mononuclear cell of type 1, type 2, and gestational diabetes mellitus patients. BMC Res Notes. 2013; 6: 491–505.
- 14Honda M, Kuwano Y, Katsuura-Kamano S et al. Chronic academic stress increases a group of microRNAs in peripheral blood. PLoS One. 2013; 8: e75960.
- 15Blaze J, Roth TL. Evidence from clinical and animal model studies of the long-term and transgenerational impact of stress on DNA methylation. Semin Cell Dev Biol. 2015; 43: 76–84.
- 16Guil S, Esteller M. DNA methylomes, histone codes and miRNAs: Tying it all together. Int J Biochem Cell Biol. 2009; 41: 87–95.
- 17Yan YX, Wu LJ, Zhang J et al. Let-7 related genetic variation and risk of metabolic syndrome in a Chinese population. Endocr J. 2015; 62: 887–896.
- 18Wang SS, Li YQ, Liang YZ et al. Expression of miR-18a and miR-34c in circulating monocytes associated with vulnerability to type 2 diabetes mellitus and insulin resistance. J Cell Mol Med. 2017; 21: 3372–3380.
- 19Guay C, Roggli E, Nesca V, Jacovetti C, Regazzi R. Diabetes mellitus, a microRNA-related disease? Transl Res. 2011; 157: 253–264.
- 20Hamar P. Role of regulatory microRNAs in type 2 diabetes mellitus related inflammation. Nucleic Acid Ther. 2012; 22: 289–294.
- 21McClelland AD, Kantharidis P. MicroRNA in the development of diabetic complications. Clin Sci (Lond). 2014; 126: 95–110.
- 22Zhu HM, Leung SW. Identification of microRNA biomarkers in type 2 diabetes: A meta-analysis of controlled profiling studies. Diabetologia. 2015; 58: 900–911.
- 23Brazma A, Hingamp P, Quackenbush J et al. Minimum information about a microarray experiment (MIAME) toward standards for microarray data. Nat Genet. 2001; 29: 365–371.
- 24Bustin SA, Benes V, Garson JA et al. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009; 55: 611–622.
- 25Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010; 36: 1–48.
- 26Baldeón RL, Weigelt K, de Wit H et al. Type 2 diabetes monocyte microRNA and mRNA expression: Dyslipidemia associates with increased differentiation-related genes but not inflammatory activation. PLoS One. 2015; 10: e0129421.
- 27Dangwal S, Stratmann B, Bang C et al. Impairment of wound healing in patients with type 2 diabetes mellitus influences circulating microRNA patterns via inflammatory cytokines. Arterioscler Thromb Vasc Biol. 2015; 35: 1480–1488.
- 28Xavier DJ, Takahashi P, Evangelista AF et al. Assessment of DNA damage and mRNA/miRNA transcriptional expression profiles in hyperglycemic versus non-hyperglycemic patients with type 2 diabetes mellitus. Mutat Res. 2015; 776: 98–110.
- 29Wang JM, Tao J, Chen DD et al. MicroRNA miR-27b rescues bone marrow-derived angiogenic cell function and accelerates wound healing in type 2 diabetes mellitus. Arterioscler Thromb Vasc Biol. 2014; 34: 99–109.
- 30Jiang LQ, Franck N, Egan B et al. Autocrine role of interleukin-13 on skeletal muscle glucose metabolism in type 2 diabetic patients involves microRNA let-7. Am J Physiol Endocrinol Metab. 2013; 305: E1359–E1366.
- 31Jansen F, Wang H, Przybilla D et al. Vascular endothelial microparticles-incorporated microRNAs are altered in patients with diabetes mellitus. Cardiovasc Diabetol. 2016; 15: 49–58.
- 32Winkler MA, Dib C, Ljubimov AV, Saghizadeh M. Targeting miR-146a to treat delayed wound healing in human diabetic organ-cultured corneas. PLoS One. 2014; 9: e114692.
- 33Baldeón Rojas L, Weigelt K, de Wit H et al. Study on inflammation-related genes and microRNAs, with special emphasis on the vascular repair factor HGF and miR-574–3p, in monocytes and serum of patients with T2D. Diabetol Metab Syndr. 2016; 8: 6–17.
- 34Zeng J, Xiong Y, Li G et al. MiR-21 is overexpressed in response to high glucose and protects endothelial cells from apoptosis. Exp Clin Endocrinol Diabetes. 2013; 121: 425–430.
- 35Fulzele S, El-Sherbini A, Ahmad S et al. MicroRNA-146b-3p regulates retinal inflammation by suppressing adenosine deaminase-2 in diabetes. Biomed Res Int. 2015; 2015: 846501–846508.
- 36Wang HW, Su SH, Wang YL et al. MicroRNA-134 contributes to glucose-induced endothelial cell dysfunction and this effect can be reversed by far-infrared irradiation. PLoS One. 2016; 11: e0147067.
- 37Ye M, Li D, Yang J et al. MicroRNA-130a targets MAP3K12 to modulate diabetic endothelial progenitor cell function. Cell Physiol Biochem. 2015; 36: 712–726.
- 38Xu Q, Meng S, Liu B et al. MicroRNA-130a regulates autophagy of endothelial progenitor cells through Runx3. Clin Exp Pharmacol Physiol. 2014; 41: 351–357.
- 39Mao G, Liu L. MicroRNA-18a is a genetic marker for the early diagnosis of cerebral injury induced by type 2 diabetes. Exp Ther Med. 2014; 8: 1901–1905.
- 40Balasubramanyam M, Aravind S, Gokulakrishnan K et al. Impaired miR-146a expression links subclinical inflammation and insulin resistance in Type 2 diabetes. Mol Cell Biochem. 2011; 351: 197–205.
- 41Latouche C, Natoli A, Reddy-Luthmoodoo M, Heywood SE, Armitage JA, Kingwell BA. MicroRNA-194 modulates glucose metabolism and its skeletal muscle expression is reduced in diabetes. PLoS One. 2016; 11: e0155108.
- 42Corral-Fernández NE, Salgado-Bustamante M, Martínez-Leija ME et al. Dysregulated miR-155 expression in peripheral blood mononuclear cells from patients with type 2 diabetes. Exp Clin Endocrinol Diabetes. 2013; 121: 347–353.
- 43Mazloom H, Alizadeh S, Pasalar P, Esfahani EN, Meshkani R. Downregulated microRNA-155 expression in peripheral blood mononuclear cells of type 2 diabetic patients is not correlated with increased inflammatory cytokine production. Cytokine. 2015; 76: 403–408.
- 44Al-Kafaji G, Al-Mahroos G, Al-Muhtaresh HA, Skrypnyk C, Sabry MA, Ramadan AR. Decreased expression of circulating microRNA-126 in patients with type 2 diabetic nephropathy: A potential blood-based biomarker. Exp Ther Med. 2016; 12: 815–822.
- 45Ramirez HA, Liang L, Pastar I et al. Comparative genomic, microRNA, and tissue analyses reveal subtle differences between non-diabetic and diabetic foot skin. PLoS One. 2015; 10: e0137133.
- 46Funari VA, Winkler M, Brown J, Dimitrijevich SD, Ljubimov AV, Saghizadeh M. Differentially expressed wound healing-related microRNAs in the human diabetic cornea. PLoS One. 2013; 8: e84425.
- 47Zampetaki A, Kiechl S, Drozdov I et al. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res. 2010; 107: 810–817.
- 48Wu H, Kong L, Tan Y et al. C66 ameliorates diabetic nephropathy in mice by both upregulating NRF2 function via increase in miR-200a and inhibiting miR-21. Diabetologia. 2016; 59: 1558–1568.
- 49Alipour MR, Khamaneh AM, Yousefzadeh N, Mohammad-Nejad D, Soufi FG. Upregulation of microRNA-146a was not accompanied by downregulation of pro-inflammatory markers in diabetic kidney. Mol Biol Rep. 2013; 40: 6477–6483.
- 50Reddy MA, Jin W, Villeneuve L et al. Pro-inflammatory role of microRNA-200 in vascular smooth muscle cells from diabetic mice. Arterioscler Thromb Vasc Biol. 2012; 32: 721–729.
- 51Xu J, Wu W, Zhang L et al. The role of microRNA-146a in the pathogenesis of the diabetic wound-healing impairment. Diabetes. 2012; 61: 2906–2912.
- 52Khamaneh AM, Alipour MR, Sheikhzadeh Hesari F, Ghadiri Soufi F. A signature of microRNA-155 in the pathogenesis of diabetic complications. J Physiol Biochem. 2015; 71: 301–309.
- 53Belgardt BF, Ahmed K, Spranger M et al. The microRNA-200 family regulates pancreatic beta cell survival in type 2 diabetes. Nat Med. 2015; 21: 619–630.
- 54Feng B, Cao Y, Chen S, Ruiz M, Chakrabarti S. MiRNA-1 regulates endothelin-1 in diabetes. Life Sci. 2014; 118: 275–280.
- 55Qiao Y, Zhao Y, Liu Y et al. MiR-483-3p regulates hyperglycaemia-induced cardiomyocyte apoptosis in transgenic mice. Biochem Biophys Res Commun. 2016; 477: 541–547.
- 56Shen E, Diao X, Wang X, Chen R, Hu B. MicroRNAs involved in the mitogen-activated protein kinase cascades pathway during glucose-induced cardiomyocyte hypertrophy. Am J Pathol. 2011; 179: 639–650.
- 57Costantino S, Paneni F, Lüscher TF, Cosentino F. MicroRNA profiling unveils hyperglycaemic memory in the diabetic heart. Eur Heart J. 2016; 37: 572–576.
- 58Chen HY, Zhong X, Huang XR et al. MicroRNA-29b inhibits diabetic nephropathy in db/db mice. Mol Ther. 2014; 22: 842–853.
- 59Villeneuve LM, Kato M, Reddy MA, Wang M, Lanting L, Natarajan R. Enhanced levels of microRNA-125b in vascular smooth muscle cells of diabetic db/db mice lead to increased inflammatory gene expression by targeting the histone methyltransferase Suv39h1. Diabetes. 2010; 59: 2904–2915.
- 60Chavali V, Tyagi SC, Mishra PK. Differential expression of Dicer, miRNAs, and inflammatory markers in diabetic Ins2+/2 Akita hearts. Cell Biochem Biophys. 2014; 68: 25–35.
- 61Yousefzadeh N, Alipour MR, Soufi FG. Deregulation of NF-κB–miR-146a negative feedback loop may be involved in the pathogenesis of diabetic neuropathy. J Physiol Biochem. 2015; 71: 51–58.
- 62Gong Q, Lu Z, Huang Q et al. Altered microRNAs expression profiling in mice with diabetic neuropathic pain. Biochem Biophys Res Commun. 2015; 456: 615–620.
- 63Zeng LQ, Wei SB, Sun YM et al. Systematic profiling of mRNA and miRNA expression in the pancreatic islets of spontaneously diabetic Goto–Kakizaki rats. Mol Med Rep. 2015; 11: 67–74.
- 64Zhong X, Chung AC, Chen HY et al. MiR-21 is a key therapeutic target for renal injury in a mouse model of type 2 diabetes. Diabetologia. 2013; 56: 663–674.
- 65Gilad S, Meiri E, Yogev Y et al. Serum microRNAs are promising novel biomarkers. PLoS One. 2008; 3: e3148.
- 66Laterza OF, Lim L, Garrett-Engele PW et al. Plasma microRNAs as sensitive and specific biomarkers of tissue injury. Clin Chem. 2009; 55: 1977–1983.
- 67Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010; 285: 17442–17452.
- 68Cho WC. Circulating microRNAs as minimally invasive biomarkers for cancer theragnosis and prognosis. Front Genet. 2011; 2: 1–6.
- 69Chen X, Ba Y, Ma L et al. Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008; 18: 997–1006.
- 70Quinn SR, O’Neill LA. A trio of microRNAs that control Toll-like receptor signalling. Int Immunol. 2011; 23: 421–425.
- 71Boldin MP, Baltimore D. MicroRNAs, new effectors and regulators of NF-kB. Immunol Rev. 2012; 246: 205–220.
- 72Hofmann MA, Schiekofer S, Kanitz M et al. Insufficient glycemic control increases nuclear factor-kappa B binding activity in peripheral blood mononuclear cells isolated from patients with type 1 diabetes. Diabetes Care. 1998; 21: 1310–1316.
- 73Adaikalakoteswari A, Rema M, Mohan V, Balasubramanyam M. Oxidative DNA damage and augmentation of poly(ADP-ribose) polymerase/nuclear factor-kappa B signaling in patients with type 2 diabetes and microangiopathy. Int J Biochem Cell Biol. 2007; 39: 1673–1684.
- 74Prattichizzo F, Giuliani A, Ceka A et al. Epigenetic mechanisms of endothelial dysfunction in type 2 diabetes. Clin Epigenetics. 2015; 7: 56–66.
- 75Masters SL, Mielke LA, Cornish AL et al. Regulation of interleukin-1β by interferon-γ is species specific, limited by suppressor of cytokine signalling 1 and influences interleukin-17 production. EMBO Rep. 2010; 11: 640–646.
- 76Chaudhuri AA, So AY, Sinha N et al. MicroRNA-125b potentiates macrophage activation. J Immunol. 2011; 187: 5062–5068.
- 77He J, Xu Q, Jing Y et al. Reactive oxygen species regulate ERBB2 and ERBB3 expression via miR-199a/125b and DNA methylation. EMBO Rep. 2012; 13: 1116–1122.
- 78Rudov A, Balduini W, Carloni S, Perrone S, Buonocore G, Albertini MC. Involvement of miRNAs in placental alterations mediated by oxidative stress. Oxid Med Cell Longev. 2014; 2014: 103068–103075.
- 79Hu Y, Li P, Hao S, Liu L, Zhao J, Hou Y. Differential expression of microRNAs in the placentae of Chinese patients with severe pre-eclampsia. Clin Chem Lab Med. 2009; 47: 923–929.
- 80Zhu XM, Han T, Sargent IL, Yin GW, Yao YQ. Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. Am J Obstet Gynecol. 2009; 200: 661.e1–661.e7.
- 81Kutty RK, Samuel W, Jaworski C et al. MicroRNA expression in human retinal pigment epithelial (ARPE-19) cells: Increased expression of microRNA-9 by N-(4-hydroxyphenyl) retinamide. Mol Vis. 2010; 16: 1475–1486.
- 82Lee HM, Kim JJ, Kim HJ, Shong M, Ku BJ, Jo EK. Upregulated NLRP3 inflammasome activation in patients with type 2 diabetes. Diabetes. 2013; 62: 194–204.
- 83Haneklaus M, Gerlic M, Kurowska-Stolarska M et al. Cutting edge: MiR-223 and EBV miR-BART15 regulate the NLRP3 inflammasome and IL-1beta production. J Immunol. 2012; 139: 3795–3799.
- 84Spranger J, Kroke A, Möhlig M et al. Inflammatory cytokines and the risk to develop type 2 diabetes: Results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes. 2003; 52: 812–817.
- 85Jager J, Grémeaux T, Cormont M, Le Marchand-Brustel Y, Tanti JF. Interleukin-1beta-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology. 2007; 148: 241–251.
- 86Larsen CM, Faulenbach M, Vaag A et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med. 2007; 356: 1517–1526.
- 87Mandrup-Poulsen T, Pickersgill L, Donath MY. Blockade of interleukin 1 in type 1 diabetes mellitus. Nat Rev Endocrinol. 2010; 6: 158–166.
- 88Xu G, Chen J, Jing G, Shalev A. Thioredoxin-interacting protein regulates insulin transcription through microRNA-204. Nat Med. 2013; 19: 1141–1146.
- 89Hennessy E, Clynes M, Jeppesen PB, O’Driscoll L. Identification of microRNAs with a role in glucose stimulated insulin secretion by expression profiling of MIN6 cells. Biochem Biophys Res Commun. 2010; 396: 457–462.
- 90Azizi M, Teimoori-Toolabi L, Arzanani MK, Azadmanesh K, Fard-Esfahani P, Zeinali S. MicroRNA-148b and microRNA-152 reactivate tumor suppressor genes through suppression of DNA methyltransferase-1 gene in pancreatic cancer cell lines. Cancer Biol Ther. 2014; 15: 419–427.
- 91Chen YT, Lin WD, Liao WL, Lin YJ, Chang JG, Tsai FJ. PTPRD silencing by DNA hypermethylation decreases insulin receptor signaling and leads to type 2 diabetes. Oncotarget. 2015; 6: 12 997–13 005.
10.18632/oncotarget.4092 Google Scholar
- 92Anderson RM, Bosch JA, Goll MG et al. Loss of Dnmt1 catalytic activity reveals multiple roles for DNA methylation during pancreas development and regeneration. Dev Biol. 2009; 334: 213–223.[Correction added on 17 April 2019, after first online publication: references 22 - 64 and their respective in-text citations have been renumbered accordingly.].
Citing Literature
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