Generic placeholder image

Current Diabetes Reviews

Editor-in-Chief

ISSN (Print): 1573-3998
ISSN (Online): 1875-6417

Mini-Review Article

MicroRNAs and Diabetes Mellitus Type 1

Author(s): Farbod Bahreini, Elham Rayzan and Nima Rezaei *

Volume 18, Issue 2, 2022

Published on: 15 February, 2021

Article ID: e021421191398 Pages: 8

DOI: 10.2174/1573399817666210215111201

Price: $65

Abstract

Type 1 diabetes mellitus is a multifactorial, progressive, autoimmune disease with a strong genetic feature that can affect multiple organs, including the kidney, eyes, and nerves. Early detection of type 1 diabetes can help critically to avoid serious damages to these organs. MicroRNAs are small RNA molecules that act in post-transcriptional gene regulation by attaching to the complementary sequence in the 3'-untranslated region of their target genes. Alterations in the expression of microRNA coding genes are extensively reported in several diseases, such as type 1 diabetes. Presenting non-invasive biomarkers for early detection of type 1 diabetes by quantifying microRNAs gene expression level can be a significant step in biotechnology and medicine. This review discusses the area of microRNAs dysregulation in type 1 diabetes and affected molecular mechanisms involved in pancreatic islet cell formation and dysregulation in the expression of inflammatory elements as well as pro-inflammatory cytokines.

Keywords: Type 1 diabetes mellitus, microRNAs, biomarkers, autoimmune disease, cytokines, biotechnology.

[1]
Pang H, Luo S, Huang G, Xia Y, Xie Z, Zhou Z. Advances in knowledge of candidate genes acting at the beta-cell level in the pathogenesis of T1DM. Front Endocrinol (Lausanne) 2020; 11: 119.
[http://dx.doi.org/10.3389/fendo.2020.00119] [PMID: 32226409]
[2]
Klak M, Urban S, Gomółka M, et al. Changes in gene expression of selected genes in patients with type 1 diabetes and pancreas transplant in peripheral blood. Transplant Proc 2019; 51(8): 2787-92.
[http://dx.doi.org/10.1016/j.transproceed.2019.04.086] [PMID: 31445766]
[3]
Forouhi NG, Wareham NJ. Epidemiology of diabetes. Medicine (Baltimore) 2019; 47(1): 22-7.
[http://dx.doi.org/10.1016/j.mpmed.2018.10.004]
[4]
Huang DD, Shi G, Jiang Y, Yao C, Zhu C. A review on the potential of Resveratrol in prevention and therapy of diabetes and diabetic complications. Biomed Pharmacother 2020; 125: 109767.
[http://dx.doi.org/10.1016/j.biopha.2019.109767] [PMID: 32058210]
[5]
Dai C, Zhang Y, Xu Z, Jin M. MicroRNA-122-5p inhibits cell proliferation, migration and invasion by targeting CCNG1 in pancreatic ductal adenocarcinoma. Cancer Cell Int 2020; 20(1): 98.
[http://dx.doi.org/10.1186/s12935-020-01185-z] [PMID: 32256207]
[6]
Wang P, Liu Q, Zhao H, et al. miR-216a-targeting theranostic nanoparticles promote proliferation of insulin-secreting cells in type 1 diabetes animal model. Sci Rep 2020; 10(1): 5302.
[http://dx.doi.org/10.1038/s41598-020-62269-4] [PMID: 32210316]
[7]
Mohr AM, Mott JL. Overview of microRNA biology. Semin Liver Dis 2015; 35(1): 3-11.
[http://dx.doi.org/10.1055/s-0034-1397344] [PMID: 25632930]
[8]
Guay C, Jacovetti C, Nesca V, Motterle A, Tugay K, Regazzi R. Emerging roles of non-coding RNAs in pancreatic β-cell function and dysfunction. Diabetes Obes Metab 2012; 14(Suppl. 3): 12-21.
[http://dx.doi.org/10.1111/j.1463-1326.2012.01654.x] [PMID: 22928560]
[9]
Jacovetti C, Matkovich SJ, Rodriguez-Trejo A, Guay C, Regazzi R. Postnatal β-cell maturation is associated with islet-specific microRNA changes induced by nutrient shifts at weaning. Nat Commun 2015; 6: 8084.
[http://dx.doi.org/10.1038/ncomms9084] [PMID: 26330140]
[10]
Nik Mohamed Kamal NNSB, Shahidan WNS. Non-exosomal and exosomal circulatory micrornas: Which are more valid as biomarkers? Front Pharmacol 2020; 10: 1500.
[http://dx.doi.org/10.3389/fphar.2019.01500] [PMID: 32038230]
[11]
Wang J, Chen J, Sen S. MicroRNA as biomarkers and diagnostics. J Cell Physiol 2016; 231(1): 25-30.
[http://dx.doi.org/10.1002/jcp.25056] [PMID: 26031493]
[12]
Josefsson A, Larsson K, Freyhult E, Damber J-E, Welén K. Gene expression alterations during development of castration-resistant prostate cancer are detected in circulating tumor cells. Cancers (Basel) 2019; 12(1): 39.
[http://dx.doi.org/10.3390/cancers12010039] [PMID: 31877738]
[13]
Cieślik M, Czapski GA, Wójtowicz S, et al. Alterations of transcription of genes coding anti-oxidative and mitochondria-related proteins in amyloid β toxicity: Relevance to alzheimer’s disease. Mol Neurobiol 2020; 57(3): 1374-88.
[http://dx.doi.org/10.1007/s12035-019-01819-y] [PMID: 31734880]
[14]
Wapinski O, Chang HY. Long noncoding RNAs and human disease. Trends Cell Biol 2011; 21(6): 354-61.
[http://dx.doi.org/10.1016/j.tcb.2011.04.001] [PMID: 21550244]
[15]
Gunton JE, Kulkarni RN, Yim S, et al. Loss of ARNT/HIF1β mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes. Cell 2005; 122(3): 337-49.
[http://dx.doi.org/10.1016/j.cell.2005.05.027] [PMID: 16096055]
[16]
Guay C, Roggli E, Nesca V, Jacovetti C, Regazzi R. Diabetes mellitus, a microRNA-related disease? Transl Res 2011; 157(4): 253-64.
[http://dx.doi.org/10.1016/j.trsl.2011.01.009] [PMID: 21420036]
[17]
Jo S, Chen J, Xu G, Grayson TB, Thielen LA, Shalev A. miR-204 controls glucagon-like peptide 1 receptor expression and agonist function. Diabetes 2018; 67(2): 256-64.
[http://dx.doi.org/10.2337/db17-0506] [PMID: 29101219]
[18]
Xu G, Chen J, Jing G, Shalev A. Thioredoxin-interacting protein regulates insulin transcription through microRNA-204. Nat Med 2013; 19(9): 1141-6.
[http://dx.doi.org/10.1038/nm.3287] [PMID: 23975026]
[19]
Xu G, Chen J, Jing G, Grayson TB, Shalev A. miR-204 targets PERK and regulates UPR signaling and β-cell apoptosis. Mol Endocrinol 2016; 30(8): 917-24.
[http://dx.doi.org/10.1210/me.2016-1056] [PMID: 27384111]
[20]
Zhu Y, Liu Q, Zhou Z, Ikeda Y. PDX1, Neurogenin-3, and MAFA: critical transcription regulators for beta cell development and regeneration. Stem Cell Res Ther 2017; 8(1): 240.
[http://dx.doi.org/10.1186/s13287-017-0694-z] [PMID: 29096722]
[21]
Sacconi A, Biagioni F, Canu V, et al. miR-204 targets Bcl-2 expression and enhances responsiveness of gastric cancer. Cell death & disease 2012; 3(11): e423.
[22]
Yang J, Liu X, Bhalla K, et al. Prevention of apoptosis by Bcl-2: Release of cytochrome C from mitochondria blocked. Science 1997; 275(5303): 1129-32.
[http://dx.doi.org/10.1126/science.275.5303.1129] [PMID: 9027314]
[23]
Hockenbery DM, Oltvai ZN, Yin X-M, Milliman CL, Korsmeyer SJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 1993; 75(2): 241-51.
[http://dx.doi.org/10.1016/0092-8674(93)80066-N] [PMID: 7503812]
[24]
Xu G, Thielen LA, Chen J, et al. Serum miR-204 is an early biomarker of type 1 diabetes-associated pancreatic beta-cell loss. Am J Physiol Endocrinol Metab 2019; 317(4): E723-30.
[http://dx.doi.org/10.1152/ajpendo.00122.2019] [PMID: 31408375]
[25]
Li T, Pan H, Li R. The dual regulatory role of miR-204 in cancer. Tumour Biol 2016; 37(9): 11667-77.
[http://dx.doi.org/10.1007/s13277-016-5144-5] [PMID: 27438705]
[26]
Assmann TS, Recamonde-Mendoza M, De Souza BM, Crispim D. MicroRNA expression profiles and type 1 diabetes mellitus: systematic review and bioinformatic analysis. Endocr Connect 2017; 6(8): 773-90.
[http://dx.doi.org/10.1530/EC-17-0248] [PMID: 28986402]
[27]
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): 1496-506.
[http://dx.doi.org/10.1136/ard.2010.139857] [PMID: 21602271]
[28]
Zhong 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(3): 663-74.
[http://dx.doi.org/10.1007/s00125-012-2804-x] [PMID: 23292313]
[29]
Fouad M, Salem I, Elhefnawy K, Raafat N, Faisal A. MicroRNA-21 as an early marker of nephropathy in patients with type 1 diabetes. Indian J Nephrol 2020; 30(1): 21-5.
[http://dx.doi.org/10.4103/ijn.IJN_80_19] [PMID: 32015595]
[30]
Mostahfezian M, Azhir Z, Dehghanian F, Hojati Z. Expression pattern of microRNAs, miR-21, miR-155 and miR-338 in patients with type 1 diabetes. Arch Med Res 2019; 50(3): 79-85.
[http://dx.doi.org/10.1016/j.arcmed.2019.07.002] [PMID: 31495393]
[31]
Backe MB, Novotny GW, Christensen DP, Grunnet LG, Mandrup-Poulsen T. Altering β-cell number through stable alteration of miR-21 and miR-34a expression. Islets 2014; 6(1): e27754.
[http://dx.doi.org/10.4161/isl.27754] [PMID: 25483877]
[32]
Jiang Y, Gao Q, Wang L, et al. Deficiency of programmed cell death 4 results in increased IL-10 expression by macrophages and thereby attenuates atherosclerosis in hyperlipidemic mice. Cell Mol Immunol 2016; 13(4): 524-34.
[http://dx.doi.org/10.1038/cmi.2015.47] [PMID: 26166769]
[33]
Mongan AE, Ramdahin S, Warrington RJ. Interleukin-10 response abnormalities in systemic lupus erythematosus. Scand J Immunol 1997; 46(4): 406-12.
[http://dx.doi.org/10.1046/j.1365-3083.1997.d01-140.x] [PMID: 9350293]
[34]
Houssiau FA, Lefebvre C, Vanden Berghe M, Lambert M, Devogelaer JP, Renauld JC. Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus 1995; 4(5): 393-5.
[http://dx.doi.org/10.1177/096120339500400510] [PMID: 8563734]
[35]
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): 12030-5.
[http://dx.doi.org/10.1073/pnas.1101450108] [PMID: 21730150]
[36]
Faraoni I, Antonetti FR, Cardone J, Bonmassar E. miR-155 gene: a typical multifunctional microRNA. Biochim Biophys Acta 2009; 1792(6): 497-505.
[http://dx.doi.org/10.1016/j.bbadis.2009.02.013] [PMID: 19268705]
[37]
García-Díaz DF, Pizarro C, Camacho-Guillén P, Codner E, Soto N, Pérez-Bravo F. Expression of miR-155, miR-146a, and miR-326 in T1D patients from Chile: Relationship with autoimmunity and inflammatory markers. Arch Endocrinol Metab 2018; 62(1): 34-40.
[http://dx.doi.org/10.20945/2359-3997000000006] [PMID: 29694627]
[38]
Lashine YA, Salah S, Aboelenein HR, Abdelaziz AI. Correcting the expression of miRNA-155 represses PP2Ac and enhances the release of IL-2 in PBMCs of juvenile SLE patients. Lupus 2015; 24(3): 240-7.
[http://dx.doi.org/10.1177/0961203314552117] [PMID: 25253569]
[39]
Paraboschi EM, Soldà G, Gemmati D, et al. Genetic association and altered gene expression of mir-155 in multiple sclerosis patients. Int J Mol Sci 2011; 12(12): 8695-712.
[http://dx.doi.org/10.3390/ijms12128695] [PMID: 22272099]
[40]
Chatzantoni K, Mouzaki A. Anti-TNF-alpha antibody therapies in autoimmune diseases. Curr Top Med Chem 2006; 6(16): 1707-14.
[http://dx.doi.org/10.2174/156802606778194217] [PMID: 17017952]
[41]
Grieco GE, Cataldo D, Ceccarelli E, et al. Serum levels of miR-148a and miR-21-5p are increased in type 1 diabetic patients and correlated with markers of bone strength and metabolism. Noncoding RNA 2018; 4(4): E37.
[http://dx.doi.org/10.3390/ncrna4040037] [PMID: 30486455]
[42]
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): 433-40.
[http://dx.doi.org/10.1038/ni.3385] [PMID: 26901150]
[43]
Haftmann C, Stittrich AB, Zimmermann J, et al. miR-148a is upregulated by Twist1 and T-bet and promotes Th1-cell survival by regulating the proapoptotic gene Bim. Eur J Immunol 2015; 45(4): 1192-205.
[http://dx.doi.org/10.1002/eji.201444633] [PMID: 25486906]
[44]
Zhang L, Wu H, Zhao M, Lu Q. Identifying the differentially expressed microRNAs in autoimmunity: A systemic review and meta-analysis. Autoimmunity 2020; 53(3): 122-36.
[http://dx.doi.org/10.1080/08916934.2019.1710135] [PMID: 31902241]
[45]
Azhir Z, Dehghanian F, Hojati Z. Increased expression of microRNAs, miR-20a and miR-326 in PBMCs of patients with type 1 diabetes. Mol Biol Rep 2018; 45(6): 1973-80.
[http://dx.doi.org/10.1007/s11033-018-4352-z] [PMID: 30194557]
[46]
Sebastiani G, Grieco FA, Spagnuolo I, Galleri L, Cataldo D, Dotta F. Increased expression of microRNA miR-326 in type 1 diabetic patients with ongoing islet autoimmunity. Diabetes Metab Res Rev 2011; 27(8): 862-6.
[http://dx.doi.org/10.1002/dmrr.1262] [PMID: 22069274]
[47]
Van Wynsberghe PM, Chan SP, Slack FJ, Pasquinelli AE. Analysis of microRNA expression and function. Methods Cell Biol 2011; 106: 219-52.
[http://dx.doi.org/10.1016/B978-0-12-544172-8.00008-6] [PMID: 22118279]
[48]
Hu Z, Huang Y, Liu Y, et al. β-Arrestin 1 modulates functions of autoimmune T cells from primary biliary cirrhosis patients. J Clin Immunol 2011; 31(3): 346-55.
[http://dx.doi.org/10.1007/s10875-010-9492-4] [PMID: 21243522]
[49]
Du C, Liu C, Kang J, et al. MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat Immunol 2009; 10(12): 1252-9.
[http://dx.doi.org/10.1038/ni.1798] [PMID: 19838199]
[50]
Abe M, Hiasa Y, Onji M. T helper 17 cells in autoimmune liver diseases. Clin Dev Immunol 2013; 2013.
[51]
Tesmer LA, Lundy SK, Sarkar S, Fox DA. Th17 cells in human disease. Immunol Rev 2008; 223: 87-113.
[http://dx.doi.org/10.1111/j.1600-065X.2008.00628.x] [PMID: 18613831]
[52]
von Essen MR, Kongsbak M, Schjerling P, Olgaard K, Odum N, Geisler C. Vitamin D controls T cell antigen receptor signaling and activation of human T cells. Nat Immunol 2010; 11(4): 344-9.
[http://dx.doi.org/10.1038/ni.1851] [PMID: 20208539]
[53]
Sun XG, Tao JH, 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): 822-9.
[http://dx.doi.org/10.1007/s10753-016-0312-8] [PMID: 26861134]
[54]
Strillacci A, Griffoni C, Sansone P, et al. MiR-101 downregulation is involved in cyclooxygenase-2 overexpression in human colon cancer cells. Exp Cell Res 2009; 315(8): 1439-47.
[http://dx.doi.org/10.1016/j.yexcr.2008.12.010] [PMID: 19133256]
[55]
Wang SS, Huang ZG, Wu HY, et al. Downregulation of miR-193a-3p is involved in the pathogenesis of hepatocellular carcinoma by targeting CCND1. PeerJ 2020; 8: e8409.
[http://dx.doi.org/10.7717/peerj.8409] [PMID: 32095323]
[56]
Ventriglia G, Mancarella F, Sebastiani G, et al. miR-409-3p is reduced in plasma and islet immune infiltrates of NOD diabetic mice and is differentially expressed in people with type 1 diabetes. Diabetologia 2020; 63(1): 124-36.
[http://dx.doi.org/10.1007/s00125-019-05026-1] [PMID: 31659408]
[57]
Sun H, Guo F, Xu L. Downregulation of microRNA-101-3p participates in systemic lupus erythematosus progression via negatively regulating HDAC9. J Cell Biochem 2020; 121(10): 4310-20.
[http://dx.doi.org/10.1002/jcb.29624] [PMID: 31904179]
[58]
Zheng Y, Wang Z, Zhou Z. miRNAs: Novel regulators of autoimmunity-mediated pancreatic β-cell destruction in type 1 diabetes. Cell Mol Immunol 2017; 14(6): 488-96.
[http://dx.doi.org/10.1038/cmi.2017.7] [PMID: 28317889]
[59]
Ibrahim AA, Ramadan A, Wahby AA, Hassan M, Soliman HM, Abdel Hamid TA. Micro-RNA 196a2 expression and miR-196a2 (rs11614913) polymorphism in T1DM: A pilot study. J Pediatr Endocrinol Metab 2019; 32(10): 1171-9.
[http://dx.doi.org/10.1515/jpem-2019-0226] [PMID: 31472066]
[60]
Fu Z, Zhang S, Wang B, Huang W, Zheng L, Cheng A. Annexin A1: A double-edged sword as novel cancer biomarker. Clin Chim Acta 2020; 504: 36-42.
[http://dx.doi.org/10.1016/j.cca.2020.01.022] [PMID: 32006544]
[61]
Ibrahim AA, Ramadan A, Wahby AA, Draz IH, El Baroudy NR, Abdel Hamid TA. Evaluation of miR-196a2 expression and annexin A1 level in children with bronchial asthmaEvaluation of miR-196a2 expression and Annexin A1 level in children. Allergol Immunopathol (Madr) 2020; 48(5): 458-64.
[http://dx.doi.org/10.1016/j.aller.2019.11.002] [PMID: 32279913]
[62]
Tedeschi A, Asero R. Asthma and autoimmunity: A complex but intriguing relation. Expert Rev Clin Immunol 2008; 4(6): 767-76.
[http://dx.doi.org/10.1586/1744666X.4.6.767] [PMID: 20477126]
[63]
Bedognetti D, Roelands J, Decock J, Wang E, Hendrickx W. The MAPK hypothesis: immune-regulatory effects of MAPK-pathway genetic dysregulations and implications for breast cancer immunotherapy. Emerging Topics in Life Sciences 2017; 1(5): 429-45.
[http://dx.doi.org/10.1042/ETLS20170142]
[64]
Avnit-Sagi T, Kantorovich L, Kredo-Russo S, Hornstein E, Walker MD. The promoter of the pri-miR-375 gene directs expression selectively to the endocrine pancreas. PLoS One 2009; 4(4): e5033.
[http://dx.doi.org/10.1371/journal.pone.0005033] [PMID: 19343226]
[65]
Poy MN, Eliasson L, Krutzfeldt J, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004; 432(7014): 226-30.
[http://dx.doi.org/10.1038/nature03076] [PMID: 15538371]
[66]
Bai C, Gao Y, Li X, et al. MicroRNAs can effectively induce formation of insulin-producing cells from mesenchymal stem cells. J Tissue Eng Regen Med 2017; 11(12): 3457-68.
[http://dx.doi.org/10.1002/term.2259] [PMID: 28397402]
[67]
Dumortier O, Van Obberghen E. MicroRNAs in pancreas development. Diabetes Obes Metab 2012; 14(Suppl. 3): 22-8.
[http://dx.doi.org/10.1111/j.1463-1326.2012.01656.x] [PMID: 22928561]
[68]
Lahmy R, Soleimani M, Sanati MH, Behmanesh M, Kouhkan F, Mobarra N. MiRNA-375 promotes beta pancreatic differentiation in human induced pluripotent stem (hiPS) cells. Mol Biol Rep 2014; 41(4): 2055-66.
[http://dx.doi.org/10.1007/s11033-014-3054-4] [PMID: 24469711]
[69]
Poy MN, Hausser J, Trajkovski M, et al. miR-375 maintains normal pancreatic alpha- and beta-cell mass. Proc Natl Acad Sci USA 2009; 106(14): 5813-8.
[http://dx.doi.org/10.1073/pnas.0810550106] [PMID: 19289822]
[70]
Li X. MiR-375, a microRNA related to diabetes. Gene 2014; 533(1): 1-4.
[http://dx.doi.org/10.1016/j.gene.2013.09.105] [PMID: 24120394]
[71]
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
[72]
Gao Y, Zhang R, Dai S, Zhang X, Li X, Bai C. Role of TGF-β/Smad Pathway in the Transcription of Pancreas-Specific Genes During Beta Cell Differentiation. Front Cell Dev Biol 2019; 7: 351.
[http://dx.doi.org/10.3389/fcell.2019.00351] [PMID: 31921861]
[73]
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): 158-65.
[http://dx.doi.org/10.1111/1753-0407.12163] [PMID: 24796653]
[74]
Li JY, Huang WX, Zhou X, Chen J, Li Z. Numb inhibits epithelial-mesenchymal transition via RBP-Jκ-dependent Notch1/PTEN/FAK signaling pathway in tongue cancer. BMC Cancer 2019; 19(1): 391.
[http://dx.doi.org/10.1186/s12885-019-5605-5] [PMID: 31023264]
[75]
Namjou B, Choi CB, Harley IT, et al. Evaluation of TRAF6 in a large multiancestral lupus cohort. Arthritis Rheum 2012; 64(6): 1960-9.
[http://dx.doi.org/10.1002/art.34361] [PMID: 22231568]
[76]
Tang Y, Luo X, Cui H, et al. MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum 2009; 60(4): 1065-75.
[http://dx.doi.org/10.1002/art.24436] [PMID: 19333922]
[77]
Ferrandi C, Richard F, Tavano P, et al. Characterization of immune cell subsets during the active phase of multiple sclerosis reveals disease and c-Jun N-terminal kinase pathway biomarkers. Mult Scler 2011; 17(1): 43-56.
[http://dx.doi.org/10.1177/1352458510381258] [PMID: 20855355]
[78]
Wang G, Gu Y, Xu N, Zhang M, Yang T. 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): 382-7.
[http://dx.doi.org/10.1016/j.bbrc.2017.06.196] [PMID: 28733034]
[79]
Liu Y, Ma M, Yu J, et al. Decreased serum microRNA-21, microRNA-25, microRNA-146a, and microRNA-181a in autoimmune diabetes: Potential biomarkers for diagnosis and possible involvement in pathogenesis. Int J Endocrinol 2019; 2019: 8406438.
[http://dx.doi.org/10.1155/2019/8406438] [PMID: 31582977]
[80]
Guled M, Lahti L, Lindholm PM, et al. CDKN2A, NF2, and JUN are dysregulated among other genes by miRNAs in malignant mesothelioma -A miRNA microarray analysis. Genes Chromosomes Cancer 2009; 48(7): 615-23.
[http://dx.doi.org/10.1002/gcc.20669] [PMID: 19396864]
[81]
Xiao F, Qiu H, Cui H, et al. MicroRNA-885-3p inhibits the growth of HT-29 colon cancer cell xenografts by disrupting angiogenesis via targeting BMPR1A and blocking BMP/Smad/Id1 signaling. Oncogene 2015; 34(15): 1968-78.
[http://dx.doi.org/10.1038/onc.2014.134] [PMID: 24882581]
[82]
Hunsberger JG, Fessler EB, Wang Z, Elkahloun AG, Chuang DM. Post-insult valproic acid-regulated microRNAs: potential targets for cerebral ischemia. Am J Transl Res 2012; 4(3): 316-32.
[PMID: 22937209]
[83]
Zurawek M, Dzikiewicz-Krawczyk A, Izykowska K, et al. miR-487a-3p upregulated in type 1 diabetes targets CTLA4 and FOXO3. Diabetes Res Clin Pract 2018; 142: 146-53.
[http://dx.doi.org/10.1016/j.diabres.2018.05.044] [PMID: 29859273]
[84]
Zhang X, Gu H, Wang L, Huang F, Cai J. MiR-885-3p is down-regulated in peripheral blood mononuclear cells from T1D patients and regulates the inflammatory response via targeting TLR4/NF-κB signaling. J Gene Med 2020; 22(1): e3145.
[http://dx.doi.org/10.1002/jgm.3145] [PMID: 31763742]
[85]
Garcia-Diaz DF, Camacho-Guillén P, Codner E, Pérez-Bravo F. miR15a and miR16 in Chilean type 1 diabetes patients: possible association with apoptosis, inflammatory, or autoimmunity markers. J Endocrinol Invest 2018; 41(9): 1083-8.
[http://dx.doi.org/10.1007/s40618-018-0837-9] [PMID: 29383679]
[86]
Garcia-Contreras M, Shah SH, Tamayo A, et al. Plasma-derived exosome characterization reveals a distinct microRNA signature in long duration Type 1 diabetes. Sci Rep 2017; 7(1): 5998.
[http://dx.doi.org/10.1038/s41598-017-05787-y] [PMID: 28729721]
[87]
Figliolini F, Cantaluppi V, De Lena M, et al. Isolation, characterization and potential role in beta cell-endothelium cross-talk of extracellular vesicles released from human pancreatic islets. PLoS One 2014; 9(7): e102521.
[http://dx.doi.org/10.1371/journal.pone.0102521] [PMID: 25028931]
[88]
Rivas MA, Venturutti L, Huang YW, Schillaci R, Huang TH, Elizalde PV. Downregulation of the tumor-suppressor miR-16 via progestin-mediated oncogenic signaling contributes to breast cancer development. Breast Cancer Res 2012; 14(3): R77.
[http://dx.doi.org/10.1186/bcr3187] [PMID: 22583478]
[89]
Caporali A, Emanueli C. MicroRNA-503 and the extended microRNA-16 family in angiogenesis. Trends Cardiovasc Med 2011; 21(6): 162-6.
[http://dx.doi.org/10.1016/j.tcm.2012.05.003] [PMID: 22814423]
[90]
Cimmino A, Calin GA, Fabbri M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 2005; 102(39): 13944-9.
[http://dx.doi.org/10.1073/pnas.0506654102] [PMID: 16166262]
[91]
Churov AV, Oleinik EK, Knip M. MicroRNAs in rheumatoid arthritis: altered expression and diagnostic potential. Autoimmun Rev 2015; 14(11): 1029-37.
[http://dx.doi.org/10.1016/j.autrev.2015.07.005] [PMID: 26164649]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy