The Predominant microRNAs in β-cell Clusters for Insulin Regulation and Diabetic Control

Author(s): Adele Soltani, Arefeh Jafarian, Abdolamir Allameh*

Journal Name: Current Drug Targets

Volume 21 , Issue 7 , 2020

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

micro (mi)-RNAs are vital regulators of multiple processes including insulin signaling pathways and glucose metabolism. Pancreatic β-cells function is dependent on some miRNAs and their target mRNA, which together form a complex regulative network. Several miRNAs are known to be directly involved in β-cells functions such as insulin expression and secretion. These small RNAs may also play significant roles in the fate of β-cells such as proliferation, differentiation, survival and apoptosis. Among the miRNAs, miR-7, miR-9, miR-375, miR-130 and miR-124 are of particular interest due to being highly expressed in these cells. Under diabetic conditions, although no specific miRNA profile has been noticed, the expression of some miRNAs and their target mRNAs are altered by posttranscriptional mechanisms, exerting diverse signs in the pathobiology of various diabetic complications. The aim of this review article is to discuss miRNAs involved in the process of stem cells differentiation into β-cells, resulting in enhanced β-cell functions with respect to diabetic disorders. This paper will also look into the impact of miRNA expression patterns on in vitro proliferation and differentiation of β-cells. The efficacy of the computational genomics and biochemical analysis to link the changes in miRNA expression profiles of stem cell-derived β-cells to therapeutically relevant outputs will be discussed as well.

Keywords: β-cells function, diabetes mellitus, microRNA, differentiation, insulin, IPC.

[1]
Bartel DP. Bartel DP. MicroRNAs: target recognition and regulatory functions. cell. 2009; 136(2): 215-33
[2]
Dumortier O, Hinault C, Gautier N, Patouraux S, Casamento V, Van Obberghen E. Maternal protein restriction leads to pancreatic failure in offspring: role of misexpressed microRNA-375. Diabetes 2014; 63(10): 3416-27.
[http://dx.doi.org/10.2337/db13-1431] [PMID: 24834976]
[3]
Hashimoto N, Tanaka T. Role of miRNAs in the pathogenesis and susceptibility of diabetes mellitus. J Hum Genet 2017; 62(2): 141-50.
[http://dx.doi.org/10.1038/jhg.2016.150] [PMID: 27928162]
[4]
Rajewsky N. microRNA target predictions in animals. Nat Genet 2006; 38(6s)(Suppl.): S8-S13.
[http://dx.doi.org/10.1038/ng1798] [PMID: 16736023]
[5]
Rottiers V, Näär AM. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 2012; 13(4): 239-50.
[http://dx.doi.org/10.1038/nrm3313] [PMID: 22436747]
[6]
Kredo-Russo S, Ness A, Mandelbaum AD, Walker MD, Hornstein E. Regulation of pancreatic microRNA-7 expression. Experimentaldiabetes research 2012; 2012
[http://dx.doi.org/10.1155/2012/695214]
[7]
Vasa-Nicotera M, Chen H, Tucci P, et al. miR-146a is modulated in human endothelial cell with aging. Atherosclerosis 2011; 217(2): 326-30.
[http://dx.doi.org/10.1016/j.atherosclerosis.2011.03.034] [PMID: 21511256]
[8]
Hennessy 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(2): 457-62.
[http://dx.doi.org/10.1016/j.bbrc.2010.04.116] [PMID: 20417623]
[9]
Bravo-Egana V, Rosero S, Molano RD, et al. Quantitative differential expression analysis reveals miR-7 as major islet microRNA. Biochem Biophys Res Commun 2008; 366(4): 922-6.
[http://dx.doi.org/10.1016/j.bbrc.2007.12.052] [PMID: 18086561]
[10]
Correa-Medina M, Bravo-Egana V, Rosero S, et al. MicroRNA miR-7 is preferentially expressed in endocrine cells of the developing and adult human pancreas. Gene Expr Patterns 2009; 9(4): 193-9.
[http://dx.doi.org/10.1016/j.gep.2008.12.003] [PMID: 19135553]
[11]
Joglekar MV, Joglekar VM, Hardikar AA. Expression of islet-specific microRNAs during human pancreatic development. Gene Expr Patterns 2009; 9(2): 109-13.
[http://dx.doi.org/10.1016/j.gep.2008.10.001] [PMID: 18977315]
[12]
Esguerra JLS, Bolmeson C, Cilio CM, Eliasson L. Differential glucose-regulation of microRNAs in pancreatic islets of non-obese type 2 diabetes model Goto-Kakizaki rat. PLoS One 2011; 6(4)e18613
[http://dx.doi.org/10.1371/journal.pone.0018613] [PMID: 21490936]
[13]
Filios SR, Shalev A. β-Cell MicroRNAs: Small but Powerful. Diabetes 2015; 64(11): 3631-44.
[http://dx.doi.org/10.2337/db15-0831] [PMID: 26494215]
[14]
Pullen TJ, da Silva Xavier G, Kelsey G, Rutter GA. miR-29a and miR-29b contribute to pancreatic β-cell-specific silencing of monocarboxylate transporter 1 (Mct1). Mol Cell Biol 2011; 31(15): 3182-94.
[http://dx.doi.org/10.1128/MCB.01433-10] [PMID: 21646425]
[15]
Lovis P, Roggli E, Laybutt DR, et al. Alterations in microRNA expression contribute to fatty acid-induced pancreatic β-cell dysfunction. Diabetes 2008; 57(10): 2728-36.
[http://dx.doi.org/10.2337/db07-1252] [PMID: 18633110]
[16]
Gregory PA, Bert AG, Paterson EL, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10(5): 593-601.
[http://dx.doi.org/10.1038/ncb1722] [PMID: 18376396]
[17]
Filios SR, Xu G, Chen J, Hong K, Jing G, Shalev A. MicroRNA-200 is induced by thioredoxin-interacting protein and regulates Zeb1 protein signaling and beta cell apoptosis. J Biol Chem 2014; 289(52): 36275-83.
[http://dx.doi.org/10.1074/jbc.M114.592360] [PMID: 25391656]
[18]
Jacovetti C, Abderrahmani A, Parnaud G, et al. MicroRNAs contribute to compensatory β cell expansion during pregnancy and obesity. J Clin Invest 2012; 122(10): 3541-51.
[http://dx.doi.org/10.1172/JCI64151] [PMID: 22996663]
[19]
Latreille M, Hausser J, Stützer I, et al. MicroRNA-7a regulates pancreatic β cell function. J Clin Invest 2014; 124(6): 2722-35.
[http://dx.doi.org/10.1172/JCI73066] [PMID: 24789908]
[20]
Joglekar MV, Parekh VS, Mehta S, Bhonde RR, Hardikar AA. MicroRNA profiling of developing and regenerating pancreas reveal post-transcriptional regulation of neurogenin3. Dev Biol 2007; 311(2): 603-12.
[http://dx.doi.org/10.1016/j.ydbio.2007.09.008] [PMID: 17936263]
[21]
Lee CS, Sund NJ, Vatamaniuk MZ, Matschinsky FM, Stoffers DA, Kaestner KH. Foxa2 controls Pdx1 gene expression in pancreatic β-cells in vivo. Diabetes 2002; 51(8): 2546-51.
[http://dx.doi.org/10.2337/diabetes.51.8.2546] [PMID: 12145169]
[22]
Rosero S, Bravo-Egana V, Jiang Z, et al. MicroRNA signature of the human developing pancreas. BMC Genomics 2010; 11(1): 509.
[http://dx.doi.org/10.1186/1471-2164-11-509] [PMID: 20860821]
[23]
Guay C, Regazzi R. New emerging tasks for microRNAs in the control of β-cell activities. Biochim Biophys Acta 2016; 1861(12 Pt B): 2121-9.
[http://dx.doi.org/10.1016/j.bbalip.2016.05.003] [PMID: 27178175]
[24]
Babon JJ, Nicola NA. The biology and mechanism of action of suppressor of cytokine signaling 3. Growth Factors 2012; 30(4): 207-19.
[http://dx.doi.org/10.3109/08977194.2012.687375] [PMID: 22574771]
[25]
Joglekar MV, Parekh VS, Hardikar AA. New pancreas from old: microregulators of pancreas regeneration. Trends Endocrinol Metab 2007; 18(10): 393-400.
[http://dx.doi.org/10.1016/j.tem.2007.10.001] [PMID: 18023200]
[26]
Wang Y, Liu J, Liu C, Naji A, Stoffers DA. MicroRNA-7 regulates the mTOR pathway and proliferation in adult pancreatic β-cells. Diabetes 2013; 62(3): 887-95.
[http://dx.doi.org/10.2337/db12-0451] [PMID: 23223022]
[27]
Zhang Z-W, Zhang L-Q, Ding L, et al. MicroRNA-19b downregulates insulin 1 through targeting transcription factor NeuroD1. FEBS Lett 2011; 585(16): 2592-8.
[http://dx.doi.org/10.1016/j.febslet.2011.06.039] [PMID: 21781967]
[28]
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]
[29]
Kaviani M, Azarpira N, Karimi MH, Al-Abdullah I. The role of microRNAs in islet β-cell development. Cell Biol Int 2016; 40(12): 1248-55.
[http://dx.doi.org/10.1002/cbin.10691] [PMID: 27743454]
[30]
Keller DM, McWeeney S, Arsenlis A, et al. Characterization of pancreatic transcription factor Pdx-1 binding sites using promoter microarray and serial analysis of chromatin occupancy. J Biol Chem 2007; 282(44): 32084-92.
[http://dx.doi.org/10.1074/jbc.M700899200] [PMID: 17761679]
[31]
Domínguez-Bendala J, Klein D, Pastori RL. MicroRNAs in pancreas and islet development MicroRNA in Regenerative Medicine. Elsevier 2015; pp. 401-18.
[32]
Ramachandran D, Roy U, Garg S, Ghosh S, Pathak S, Kolthur-Seetharam U. Sirt1 and mir-9 expression is regulated during glucose-stimulated insulin secretion in pancreatic β-islets. FEBS J 2011; 278(7): 1167-74.
[http://dx.doi.org/10.1111/j.1742-4658.2011.08042.x] [PMID: 21288303]
[33]
Plaisance V, Abderrahmani A, Perret-Menoud V, Jacquemin P, Lemaigre F, Regazzi R. MicroRNA-9 controls the expression of Granuphilin/Slp4 and the secretory response of insulin-producing cells. J Biol Chem 2006; 281(37): 26932-42.
[http://dx.doi.org/10.1074/jbc.M601225200] [PMID: 16831872]
[34]
Sun L-L, Jiang B-G, Li W-T, Zou J-J, Shi Y-Q, Liu Z-M. MicroRNA-15a positively regulates insulin synthesis by inhibiting uncoupling protein-2 expression. Diabetes Res Clin Pract 2011; 91(1): 94-100.
[http://dx.doi.org/10.1016/j.diabres.2010.11.006] [PMID: 21146880]
[35]
Kim J-W, You Y-H, Jung S, et al. miRNA-30a-5p-mediated silencing of Beta2/NeuroD expression is an important initial event of glucotoxicity-induced beta cell dysfunction in rodent models. Diabetologia 2013; 56(4): 847-55.
[http://dx.doi.org/10.1007/s00125-012-2812-x] [PMID: 23338554]
[36]
Tang X, Muniappan L, Tang G, Özcan S. Identification of glucose-regulated miRNAs from pancreatic β cells reveals a role for miR-30d in insulin transcription. RNA 2009; 15(2): 287-93.
[http://dx.doi.org/10.1261/rna.1211209] [PMID: 19096044]
[37]
Wijesekara N, Zhang LH, Kang MH, et al. miR-33a modulates ABCA1 expression, cholesterol accumulation, and insulin secretion in pancreatic islets. Diabetes 2012; 61(3): 653-8.
[http://dx.doi.org/10.2337/db11-0944] [PMID: 22315319]
[38]
Lovis P, Gattesco S, Regazzi R. Regulation of the expression of components of the exocytotic machinery of insulin-secreting cells by microRNAs. Biol Chem 2008; 389(3): 305-12.
[http://dx.doi.org/10.1515/BC.2008.026] [PMID: 18177263]
[39]
Aizawa T, Komatsu M. Rab27a: a new face in β cell metabolism-secretion coupling. J Clin Invest 2005; 115(2): 227-30.
[PMID: 15690078]
[40]
Eliasson L. The small RNA miR-375 - a pancreatic islet abundant miRNA with multiple roles in endocrine beta cell function. Mol Cell Endocrinol 2017; 456: 95-101.
[http://dx.doi.org/10.1016/j.mce.2017.02.043] [PMID: 28254488]
[41]
Association AD. American Diabetes Association. 2. Classification and diagnosis of diabetes. Diabetes Care 2016; 39(Suppl. 1): S13-22.
[http://dx.doi.org/10.2337/dc16-S005] [PMID: 26696675]
[42]
Pociot F, McDermott MF. Genetics of type 1 diabetes mellitus. Genes Immun 2002; 3(5): 235-49.
[http://dx.doi.org/10.1038/sj.gene.6363875] [PMID: 12140742]
[43]
Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 2003; 52(1): 102-10.
[http://dx.doi.org/10.2337/diabetes.52.1.102] [PMID: 12502499]
[44]
Gaulton KJ, Ferreira T, Lee Y, et al. DIAbetes Genetics Replication And Meta-analysis (DIAGRAM) Consortium . Genetic fine. mapping and genomic annotation defines causal mechanisms at type 2 diabetes susceptibility loci. Nat Genet 2015; 47(12): 1415-25.
[http://dx.doi.org/10.1038/ng.3437] [PMID: 26551672]
[45]
Halban PA, Polonsky KS, Bowden DW, et al. β-cell failure in type 2 diabetes: postulated mechanisms and prospects for prevention and treatment. J Clin Endocrinol Metab 2014; 99(6): 1983-92.
[http://dx.doi.org/10.1210/jc.2014-1425] [PMID: 24712577]
[46]
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]
[47]
Poy MN, Hausser J, Trajkovski M, et al. miR-375 maintains normal pancreatic α- and β-cell mass. Proc Natl Acad Sci USA 2009; 106(14): 5813-8.
[http://dx.doi.org/10.1073/pnas.0810550106] [PMID: 19289822]
[48]
Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RH. Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol 2007; 5(8)e203
[http://dx.doi.org/10.1371/journal.pbio.0050203] [PMID: 17676975]
[49]
Nieto M, Hevia P, Garcia E, et al. Antisense miR-7 impairs insulin expression in developing pancreas and in cultured pancreatic buds. Cell Transplant 2012; 21(8): 1761-74.
[http://dx.doi.org/10.3727/096368911X612521] [PMID: 22186137]
[50]
Fukuda M. Rab27 and its effectors in secretory granule exocytosis: a novel docking machinery composed of a Rab27· effector complex. Portland Press Limited 2006.
[51]
Bordone L, Motta MC, Picard F, et al. Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic β cells. PLoS Biol 2006; 4(2)e31
[http://dx.doi.org/10.1371/journal.pbio.0040031] [PMID: 16366736]
[52]
Lee J-H, Song M-Y, Song E-K, et al. Overexpression of SIRT1 protects pancreatic β-cells against cytokine toxicity by suppressing the nuclear factor-kappaB signaling pathway. Diabetes 2009; 58(2): 344-51.
[http://dx.doi.org/10.2337/db07-1795] [PMID: 19008341]
[53]
Moynihan KA, Grimm AA, Plueger MM, et al. Increased dosage of mammalian Sir2 in pancreatic β cells enhances glucose-stimulated insulin secretion in mice. Cell Metab 2005; 2(2): 105-17.
[http://dx.doi.org/10.1016/j.cmet.2005.07.001] [PMID: 16098828]
[54]
Bagge A, Clausen TR, Larsen S, et al. MicroRNA-29a is up-regulated in beta-cells by glucose and decreases glucose-stimulated insulin secretion. Biochem Biophys Res Commun 2012; 426(2): 266-72.
[http://dx.doi.org/10.1016/j.bbrc.2012.08.082] [PMID: 22940552]
[55]
Gomes PR, Graciano MF, Pantaleão LC, et al. Long-term disruption of maternal glucose homeostasis induced by prenatal glucocorticoid treatment correlates with miR-29 upregulation. Am J Physiol Endocrinol Metab 2014; 306(1): E109-20.
[http://dx.doi.org/10.1152/ajpendo.00364.2013] [PMID: 24253049]
[56]
Bagge A, Dahmcke CM, Dalgaard LT. Syntaxin-1a is a direct target of miR-29a in insulin-producing β-cells. Horm Metab Res 2013; 45(6): 463-6.
[http://dx.doi.org/10.1055/s-0032-1333238] [PMID: 23315993]
[57]
Otonkoski T, Kaminen N, Ustinov J, et al. Physical exercise-induced hyperinsulinemic hypoglycemia is an autosomal-dominant trait characterized by abnormal pyruvate-induced insulin release. Diabetes 2003; 52(1): 199-204.
[http://dx.doi.org/10.2337/diabetes.52.1.199] [PMID: 12502513]
[58]
Roggli E, Gattesco S, Caille D, et al. Changes in microRNA expression contribute to pancreatic β-cell dysfunction in prediabetic NOD mice. Diabetes 2012; 61(7): 1742-51.
[http://dx.doi.org/10.2337/db11-1086] [PMID: 22537941]
[59]
Silva VA, Polesskaya A, Sousa TA, et al. Expression and cellular localization of microRNA-29b and RAX, an activator of the RNA-dependent protein kinase (PKR), in the retina of streptozotocin-induced diabetic rats. Mol Vis 2011; 17: 2228-40.
[PMID: 21897745]
[60]
Wang G, Kwan BC-H, Lai FM-M, Chow K-M, Li PK-T, Szeto C-C. Urinary miR-21, miR-29, and miR-93: novel biomarkers of fibrosis. Am J Nephrol 2012; 36(5): 412-8.
[http://dx.doi.org/10.1159/000343452] [PMID: 23108026]
[61]
Dooley J, Garcia-Perez JE, Sreenivasan J, et al. The microRNA-29 family dictates the balance between homeostatic and pathological glucose handling in diabetes and obesity. Diabetes 2016; 65(1): 53-61.
[http://dx.doi.org/10.2337/db15-0770] [PMID: 26696639]
[62]
Bai C, Li X, Gao Y, et al. Role of microRNA-21 in the formation of insulin-producing cells from pancreatic progenitor cells. Biochim Biophys Acta 2016; 1859(2): 280-93.
[http://dx.doi.org/10.1016/j.bbagrm.2015.12.001] [PMID: 26655730]
[63]
Huang JC, Babak T, Corson TW, et al. Using expression profiling data to identify human microRNA targets. Nat Methods 2007; 4(12): 1045-9.
[http://dx.doi.org/10.1038/nmeth1130] [PMID: 18026111]
[64]
Roggli E, Britan A, Gattesco S, et al. Involvement of microRNAs in the cytotoxic effects exerted by proinflammatory cytokines on pancreatic β-cells. Diabetes 2010; 59(4): 978-86.
[http://dx.doi.org/10.2337/db09-0881] [PMID: 20086228]
[65]
Fujimoto K, Shibasaki T, Yokoi N, et al. Piccolo, a Ca2+ sensor in pancreatic β-cells. Involvement of cAMP-GEFII.Rim2. Piccolo complex in cAMP-dependent exocytosis. J Biol Chem 2002; 277(52): 50497-502.
[http://dx.doi.org/10.1074/jbc.M210146200] [PMID: 12401793]
[66]
Ruan Q, Wang T, Kameswaran V, et al. The microRNA-21-PDCD4 axis prevents type 1 diabetes by blocking pancreatic β cell death. Proc Natl Acad Sci USA 2011; 108(29): 12030-5.
[http://dx.doi.org/10.1073/pnas.1101450108] [PMID: 21730150]
[67]
Baroukh N, Ravier MA, Loder MK, et al. MicroRNA-124a regulates Foxa2 expression and intracellular signaling in pancreatic β-cell lines. J Biol Chem 2007; 282(27): 19575-88.
[http://dx.doi.org/10.1074/jbc.M611841200] [PMID: 17462994]
[68]
Krek A, Grün D, Poy MN, et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37(5): 495-500.
[http://dx.doi.org/10.1038/ng1536] [PMID: 15806104]
[69]
Sebastiani G, Po A, Miele E, et al. MicroRNA-124a is hyperexpressed in type 2 diabetic human pancreatic islets and negatively regulates insulin secretion. Acta Diabetol 2015; 52(3): 523-30.
[http://dx.doi.org/10.1007/s00592-014-0675-y] [PMID: 25408296]
[70]
Friedman JR, Kaestner KH. The Foxa family of transcription factors in development and metabolism. Cell Mol Life Sci 2006; 63(19-20): 2317-28.
[http://dx.doi.org/10.1007/s00018-006-6095-6] [PMID: 16909212]
[71]
Jing G, Westwell-Roper C, Chen J, Xu G, Verchere CB, Shalev A. Thioredoxin-interacting protein promotes islet amyloid polypeptide expression through miR-124a and FoxA2. J Biol Chem 2014; 289(17): 11807-15.
[http://dx.doi.org/10.1074/jbc.M113.525022] [PMID: 24627476]
[72]
Minn AH, Hafele C, Shalev A. Thioredoxin-interacting protein is stimulated by glucose through a carbohydrate response element and induces β-cell apoptosis. Endocrinology 2005; 146(5): 2397-405.
[http://dx.doi.org/10.1210/en.2004-1378] [PMID: 15705778]
[73]
Melkman-Zehavi T, Oren R, Kredo-Russo S, et al. miRNAs control insulin content in pancreatic β-cells via downregulation of transcriptional repressors. EMBO J 2011; 30(5): 835-45.
[http://dx.doi.org/10.1038/emboj.2010.361] [PMID: 21285947]
[74]
Bouzakri K, Ribaux P, Halban PA. Silencing mitogen-activated protein 4 kinase 4 (MAP4K4) protects beta cells from tumor necrosis factor-α-induced decrease of IRS-2 and inhibition of glucose-stimulated insulin secretion. J Biol Chem 2009; 284(41): 27892-8.
[http://dx.doi.org/10.1074/jbc.M109.048058] [PMID: 19690174]
[75]
Zhao X, Mohan R, Özcan S, Tang X. MicroRNA-30d induces insulin transcription factor MafA and insulin production by targeting mitogen-activated protein 4 kinase 4 (MAP4K4) in pancreatic β-cells. J Biol Chem 2012; 287(37): 31155-64.
[http://dx.doi.org/10.1074/jbc.M112.362632] [PMID: 22733810]
[76]
Kaneto H, Miyatsuka T, Fujitani Y, et al. Role of PDX-1 and MafA as a potential therapeutic target for diabetes. Diabetes Res Clin Pract 2007; 77(3)(Suppl. 1): S127-37.
[http://dx.doi.org/10.1016/j.diabres.2007.01.046] [PMID: 17449132]
[77]
Kaneto H, Matsuoka TA, Kawashima S, et al. Role of MafA in pancreatic beta-cells. Adv Drug Deliv Rev 2009; 61(7-8): 489-96.
[http://dx.doi.org/10.1016/j.addr.2008.12.015] [PMID: 19393272]
[78]
Nesca V, Guay C, Jacovetti C, et al. Identification of particular groups of microRNAs that positively or negatively impact on beta cell function in obese models of type 2 diabetes. Diabetologia 2013; 56(10): 2203-12.
[http://dx.doi.org/10.1007/s00125-013-2993-y] [PMID: 23842730]
[79]
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]
[80]
Zheng Y, Wang Z, Tu Y, et al. miR-101a and miR-30b contribute to inflammatory cytokine-mediated β-cell dysfunction. Lab Invest 2015; 95(12): 1387-97.
[http://dx.doi.org/10.1038/labinvest.2015.112] [PMID: 26367486]
[81]
Dou L, Zhao T, Wang L, et al. miR-200s contribute to interleukin-6 (IL-6)-induced insulin resistance in hepatocytes. J Biol Chem 2013; 288(31): 22596-606.
[http://dx.doi.org/10.1074/jbc.M112.423145] [PMID: 23798681]
[82]
Gu G, Dubauskaite J, Melton DA. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002; 129(10): 2447-57.
[PMID: 11973276]
[83]
Lee CS, De León DD, Kaestner KH, Stoffers DA. Regeneration of pancreatic islets after partial pancreatectomy in mice does not involve the reactivation of neurogenin-3. Diabetes 2006; 55(2): 269-72.
[PMID: 16361411]
[84]
Bao L, Fu X, Si M, et al. MicroRNA-185 targets SOCS3 to inhibit beta-cell dysfunction in diabetes. PLoS One 2015; 10(2)e0116067
[http://dx.doi.org/10.1371/journal.pone.0116067] [PMID: 25658748]
[85]
Wei R, Yang J, Liu GQ, et al. Dynamic expression of microRNAs during the differentiation of human embryonic stem cells into insulin-producing cells. Gene 2013; 518(2): 246-55.
[http://dx.doi.org/10.1016/j.gene.2013.01.038] [PMID: 23370336]
[86]
Bai C, Gao Y, Zhang X, Yang W, Guan W. MicroRNA-34c acts as a bidirectional switch in the maturation of insulin-producing cells derived from mesenchymal stem cells. Oncotarget 2017; 8(63): 106844-57.
[http://dx.doi.org/10.18632/oncotarget.21883] [PMID: 29290993]
[87]
Jafarian A, Taghikani M, Abroun S, et al. The generation of insulin producing cells from human mesenchymal stem cells by MiR-375 and Anti-MiR-9. PLoS One 2015; 10(6)e0128650
[http://dx.doi.org/10.1371/journal.pone.0128650] [PMID: 26047014]
[88]
Kato T, Shimano H, Yamamoto T, et al. Granuphilin is activated by SREBP-1c and involved in impaired insulin secretion in diabetic mice. Cell Metab 2006; 4(2): 143-54.
[http://dx.doi.org/10.1016/j.cmet.2006.06.009] [PMID: 16890542]
[89]
Sebastiani G, Valentini M, Grieco GE, et al. MicroRNA expression profiles of human iPSCs differentiation into insulin-producing cells. Acta Diabetol 2017; 54(3): 265-81.
[http://dx.doi.org/10.1007/s00592-016-0955-9] [PMID: 28039581]
[90]
Shaer A, Azarpira N, Karimi MH, Soleimani M, Dehghan S. Differentiation of human-induced pluripotent stem cells into insulin-producing clusters by microRNA-7. Exp Clin Transplant 2016; 14(5): 555-63.
[PMID: 26103160]
[91]
Kato M, Castro NE, Natarajan R. MicroRNAs: potential mediators and biomarkers of diabetic complications. Free Radic Biol Med 2013; 64: 85-94.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.06.009] [PMID: 23770198]
[92]
Cnop M, Foufelle F, Velloso LA. Endoplasmic reticulum stress, obesity and diabetes. Trends Mol Med 2012; 18(1): 59-68.
[http://dx.doi.org/10.1016/j.molmed.2011.07.010] [PMID: 21889406]
[93]
He A, Zhu L, Gupta N, Chang Y, Fang F. Overexpression of micro ribonucleic acid 29, highly up-regulated in diabetic rats, leads to insulin resistance in 3T3-L1 adipocytes. Mol Endocrinol 2007; 21(11): 2785-94.
[http://dx.doi.org/10.1210/me.2007-0167] [PMID: 17652184]
[94]
Newsholme P, Keane D, Welters HJ, Morgan NG. Life and death decisions of the pancreatic β-cell: the role of fatty acids. Clin Sci (Lond) 2007; 112(1): 27-42.
[http://dx.doi.org/10.1042/CS20060115] [PMID: 17132138]
[95]
Leiter LA. β-cell preservation: a potential role for thiazolidinediones to improve clinical care in Type 2 diabetes. Diabet Med 2005; 22(8): 963-72.
[http://dx.doi.org/10.1111/j.1464-5491.2005.01605.x] [PMID: 16026359]
[96]
Weir GC, Marselli L, Marchetti P, Katsuta H, Jung MH, Bonner-Weir S. Towards better understanding of the contributions of overwork and glucotoxicity to the β-cell inadequacy of type 2 diabetes. Diabetes Obes Metab 2009; 11(Suppl. 4): 82-90.
[http://dx.doi.org/10.1111/j.1463-1326.2009.01113.x] [PMID: 19817791]
[97]
Kovacs B, Lumayag S, Cowan C, Xu S. MicroRNAs in early diabetic retinopathy in streptozotocin-induced diabetic rats. Invest Ophthalmol Vis Sci 2011; 52(7): 4402-9.
[http://dx.doi.org/10.1167/iovs.10-6879] [PMID: 21498619]
[98]
McArthur K, Feng B, Wu Y, Chen S, Chakrabarti S. MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy. Diabetes 2011; 60(4): 1314-23.
[http://dx.doi.org/10.2337/db10-1557] [PMID: 21357793]
[99]
Ito T, Yang M, May WS. RAX, a cellular activator for double-stranded RNA-dependent protein kinase during stress signaling. J Biol Chem 1999; 274(22): 15427-32.
[http://dx.doi.org/10.1074/jbc.274.22.15427] [PMID: 10336432]
[100]
Zhang L, Yu J, Ye M, Zhao H. Upregulation of CKIP-1 inhibits high-glucose induced inflammation and oxidative stress in HRECs and attenuates diabetic retinopathy by modulating Nrf2/ARE signaling pathway: an in vitro study. Cell Biosci 2019; 9(1): 67.
[http://dx.doi.org/10.1186/s13578-019-0331-x] [PMID: 31462987]
[101]
Shan Z-X, Lin Q-X, Deng C-Y, et al. miR-1/miR-206 regulate Hsp60 expression contributing to glucose-mediated apoptosis in cardiomyocytes. FEBS Lett 2010; 584(16): 3592-600.
[http://dx.doi.org/10.1016/j.febslet.2010.07.027] [PMID: 20655308]
[102]
Shao Y, Dong LJ, Takahashi Y, et al. miRNA451a regulates RPE function through promoting mitochondrial function in proliferative diabetic retinopathy. Am J Physiol Endocrinol Metab 2019; 316(3): 443-452. 30576241
[103]
Horie T, Ono K, Nishi H, et al. MicroRNA-133 regulates the expression of GLUT4 by targeting KLF15 and is involved in metabolic control in cardiac myocytes. Biochem Biophys Res Commun 2009; 389(2): 315-20.
[http://dx.doi.org/10.1016/j.bbrc.2009.08.136] [PMID: 19720047]
[104]
Shen 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(2): 639-50.
[http://dx.doi.org/10.1016/j.ajpath.2011.04.034] [PMID: 21704010]
[105]
Zhong X, Chung ACK, Chen H-Y, 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]
[106]
Dey N, Das F, Mariappan MM, et al. MicroRNA-21 orchestrates high glucose-induced signals to TOR complex 1, resulting in renal cell pathology in diabetes. J Biol Chem 2011; 286(29): 25586-603.
[http://dx.doi.org/10.1074/jbc.M110.208066] [PMID: 21613227]
[107]
Conserva F, Barozzino M, Pesce F, et al. Urinary miRNA-27b-3p and miRNA-1228-3p correlate with the progression of Kidney Fibrosis in Diabetic Nephropathy. Sci Rep 2019; 9(1): 11357.
[http://dx.doi.org/10.1038/s41598-019-47778-1] [PMID: 31388051]
[108]
Strauer BE, Kornowski R. Stem cell therapy in perspective. Circulation 2003; 107(7): 929-34.
[http://dx.doi.org/10.1161/01.CIR.0000057525.13182.24] [PMID: 12600901]
[109]
Lahmy R, Soleimani M, Sanati MH, Behmanesh M, Kouhkan F, Mobarra N. Pancreatic islet differentiation of human embryonic stem cells by microRNA overexpression. J Tissue Eng Regen Med 2016; 10(6): 527-34.
[http://dx.doi.org/10.1002/term.1787] [PMID: 23897763]
[110]
Ong S-G, Lee WH, Kodo K, Wu JC. MicroRNA-mediated regulation of differentiation and trans-differentiation in stem cells. Adv Drug Deliv Rev 2015; 88: 3-15.
[http://dx.doi.org/10.1016/j.addr.2015.04.004] [PMID: 25887992]
[111]
Jun Y, Kim MJ, Hwang YH, et al. Microfluidics-generated pancreatic islet microfibers for enhanced immunoprotection. Biomaterials 2013; 34(33): 8122-30.
[http://dx.doi.org/10.1016/j.biomaterials.2013.07.079] [PMID: 23927952]
[112]
Walczak MP, Drozd AM, Stoczynska-Fidelus E, Rieske P, Grzela DP. Directed differentiation of human iPSC into insulin producing cells is improved by induced expression of PDX1 and NKX6.1 factors in IPC progenitors. J Transl Med 2016; 14(1): 341.
[http://dx.doi.org/10.1186/s12967-016-1097-0] [PMID: 27998294]
[113]
Piran M, Enderami SE, Piran M, Sedeh HS, Seyedjafari E, Ardeshirylajimi A. Insulin producing cells generation by overexpression of miR-375 in adipose-derived mesenchymal stem cells from diabetic patients. Biologicals 2017; 46: 23-8.
[http://dx.doi.org/10.1016/j.biologicals.2016.12.004] [PMID: 28017506]
[114]
Yau WWY, Rujitanaroj PO, Lam L, Chew SY. Directing stem cell fate by controlled RNA interference. Biomaterials 2012; 33(9): 2608-28.
[http://dx.doi.org/10.1016/j.biomaterials.2011.12.021] [PMID: 22209557]
[115]
Zhang Y, Wang Z, Gemeinhart RA. Progress in microRNA delivery. J Control Release 2013; 172(3): 962-74.
[http://dx.doi.org/10.1016/j.jconrel.2013.09.015] [PMID: 24075926]
[116]
Schade A, Delyagina E, Scharfenberg D, et al. Innovative strategy for microRNA delivery in human mesenchymal stem cells via magnetic nanoparticles. Int J Mol Sci 2013; 14(6): 10710-26.
[http://dx.doi.org/10.3390/ijms140610710] [PMID: 23702843]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 7
Year: 2020
Page: [722 - 734]
Pages: 13
DOI: 10.2174/1389450121666191230145848
Price: $65

Article Metrics

PDF: 16
HTML: 2