MicroRNAs in diabetes and diabetes-associated complications

RNA Biology

Volumn 9, Issue 6, 2012, Pages 820-827

  Lorenzen, Johan M ^a,b   Kumarswamy, Regalla ^a   Dangwal, Seema ^a   Thum, Thomas ^a,c  

^a Institute of Molecular and Translational Therapeutic Strategies (IMTTS)   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

Diabetes; Diabetic cardiomyopathy; Diabetic nephropathy; MicroRNAs

Indexed keywords

MICRORNA; MICRORNA 1; MICRORNA 125B; MICRORNA 133A; MICRORNA 143; MICRORNA 146A; MICRORNA 192; MICRORNA 21; MICRORNA 223; MICRORNA 29A; MICRORNA 29B; MICRORNA 29C; MICRORNA 373; MICRORNA 375; MICRORNA 377; MICRORNA 503; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; BIOGENESIS; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; DIABETIC NEPHROPATHY; DISEASE COURSE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; LIVER; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOGENESIS; REVIEW; SKELETAL MUSCLE; SMOOTH MUSCLE FIBER;

EID: 84863427869     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.20162     Document Type: Review

References (61)

1. Cory S, Ussery-Hall A, Griffin-Blake S, Easton A, Vigeant J, Balluz L, et al.; Centers for Disease Control and Prevention (CDC). Prevalence of selected risk behaviors and chronic diseases and conditions-steps communities, United States 2006-2007. MMWR Surveill Summ 2010; 59:1-37; PMID:20864923.
2. Atkinson MA, Maclaren NK. The pathogenesis of insulin-dependent diabetes mellitus. N Engl J Med 1994; 331:1428-36; PMID:7969282; http://dx.doi.org/10. 1056/NEJM199411243312107.
3. Rhodes CJ. Type 2 diabetes-a matter of beta-cell life and death? Science 2005; 307:380-4; PMID:15662003; http://dx.doi.org/10.1126/science.1104345.
4. Weir GC, Bonner-Weir S. Five stages of evolving beta-cell dysfunction during progression to diabetes. Diabetes 2004; 53:16-21; PMID:15561905; http://dx.doi.org/10.2337/diabetes.53.suppl-3.S16.
5. Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, et al. Prevalence of obesity, diabetes and obesity-related health risk factors, 2001. JAMA 2003; 289:76-9; PMID:12503980; http://dx.doi.org/10.1001/jama.289.1.76.
6. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA 2008; 105:13027-32; PMID:18723672; http://dx.doi.org/10.1073/pnas.0805038105.
7. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008; 456:980-4; PMID:19043405; http://dx.doi.org/10.1038/nature07511.
8. Lorenzen JM, Volkmann I, Fiedler J, Schmidt M, Scheffner I, Haller H, et al. Urinary miR-210 as a mediator of acute T-cell mediated rejection in renal allograft recipients. Am J Transplant 2011; 11:2221-7; PMID:21812927; http://dx.doi.org/10.1111/j.1600-6143.2011.03679.x.
9. Fiedler J, Jazbutyte V, Kirchmaier BC, Gupta SK, Lorenzen J, Hartmann D, et al. MicroRNA-24 regulates vascularity after myocardial infarction. Circulation 2011; 124:720-30; PMID:21788589; http://dx.doi.org/10.1161/ CIRCULATIONAHA.111.039008.
10. Lorenzen JM, Kielstein JT, Hafer C, Gupta SK, Kümpers P, Faulhaber-Walter R, et al. Circulating miR-210 predicts survival in critically ill patients with acute kidney injury. Clin J Am Soc Nephrol 2011; 6:1540-6; PMID:21700819; http://dx.doi.org/10.2215/CJN.00430111.
11. Montgomery RL, Hullinger TG, Semus HM, Dickinson BA, Seto AG, Lynch JM, et al. Therapeutic inhibition of miR-208a improves cardiac function and survival during heart failure. Circulation 2011; 124:1537-47; PMID:21900086; http://dx.doi.org/10.1161/CIRCULATIONAHA.111.030932.
12. Ambros V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell 1989; 57:49-57; PMID:2702689; http://dx.doi.org/10.1016/0092-8674(89)90171-2.
13. Chalfie M, Horvitz HR, Sulston JE. Mutations that lead to reiterations in the cell lineages of C. elegans. Cell 1981; 24:59-69; PMID:7237544; http://dx.doi.org/10.1016/0092-8674(81)90501-8.
14. Bauersachs J, Thum T. Biogenesis and regulation of cardiovascular microRNAs. Circ Res 2011; 109:334-47; PMID:21778437; http://dx.doi.org/10.1161/ CIRCRESAHA.110.228676.
15. Caporali A, Meloni M, Völlenkle C, Bonci D, Sala-Newby GB, Addis R, et al. Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation 2011; 123:282-91; PMID:21220732; http://dx.doi.org/10. 1161/CIRCULATIONAHA.110.952325.
16. Zampetaki A, Kiechl S, Drozdov I, Willeit P, Mayr U, Prokopi M, et al. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res 2010; 107:810-7; PMID:20651284; http://dx.doi.org/10.1161/CIRCRESAHA.110.226357.
17. Feng B, Chen S, McArthur K, Wu Y, Sen S, Ding Q, et al. miR-146a-Mediated extracellular matrix protein production in chronic diabetes complications. Diabetes 2011; 60:2975-84; PMID:21885871; http://dx.doi.org/10.2337/db11-0478.
18. Ross R. Cell biology of atherosclerosis. Annu Rev Physiol 1995; 57:791-804; PMID:7778883; http://dx.doi.org/10.1146/annurev.ph.57.030195.004043.
19. Villeneuve 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 Suv39 h1. Diabetes 2010; 59:2904-15; PMID:20699419; http://dx.doi.org/10.2337/db10-0208.
20. Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, et al. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 1996; 84:491-5; PMID:8608603; http://dx.doi.org/10.1016/S0092-8674(00)81294-5.
21. Villeneuve LM, Reddy MA, Lanting LL, Wang M, Meng L, Natarajan R. Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci USA 2008; 105:9047-52; PMID:18579779; http://dx.doi.org/10.1073/pnas.0803623105.
22. Ohneda K, Ee H, German M. Regulation of insulin gene transcription. Semin Cell Dev Biol 2000; 11:227-33; PMID:10966856; http://dx.doi.org/10.1006/scdb. 2000.0171.
23. Lynn FC, Skewes-Cox P, Kosaka Y, McManus MT, Harfe BD, German MS. MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes 2007; 56:2938-45; PMID:17804764; http://dx.doi.org/10.2337/db07-0175.
24. Tang X, Muniappan L, Tang G, Ozcan S. Identification of glucose-regulated miRNAs from pancreatic beta cells reveals a role for miR-30d in insulin transcription. RNA 2009; 15:287-93; PMID:19096044; http://dx.doi.org/10.1261/ rna.1211209.
25. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004; 432:226-30; PMID:15538371; http://dx.doi.org/10.1038/nature03076.
26. Poy MN, Hausser J, Trajkovski M, Braun M, Collins S, Rorsman P, et al. miR-375 maintains normal pancreatic alpha- and beta-cell mass. Proc Natl Acad Sci USA 2009; 106:5813-8; PMID:19289822; http://dx.doi.org/10.1073/pnas. 0810550106.
27. Bock T, Pakkenberg B, Buschard K. Increased islet volume but unchanged islet number in ob/ob mice. Diabetes 2003; 52:1716-22; PMID:12829638; http://dx.doi.org/10.2337/diabetes.52.7.1716.
28. El Ouaamari A, Baroukh N, Martens GA, Lebrun P, Pipeleers D, van Obberghen E. miR-375 targets 3′-phosphoinositide-dependent protein kinase-1 and regulates glucose-induced biological responses in pancreatic beta-cells. Diabetes 2008; 57:2708-17; PMID:18591395; http://dx.doi.org/10.2337/ db07-1614.
29. Frost RJ, Olson EN. Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs. Proc Natl Acad Sci USA 2011; 108:21075-80; PMID:22160727; http://dx.doi.org/10.1073/pnas.1118922109.
30. Zhu H, Shyh-Chang N, Segrè AV, Shinoda G, Shah SP, Einhorn WS, et al.; DIAGRAM Consortium; MAGIC Investigators. The Lin28/let-7 axis regulates glucose metabolism. Cell 2011; 147:81-94; PMID:21962509; http://dx.doi.org/10. 1016/j.cell.2011.08.033.
31. Fischer VW, Barner HB, Leskiw ML. Capillary basal laminar thichness in diabetic human myocardium. Diabetes 1979; 28:713-9; PMID:446928; http://dx.doi.org/10.2337/diabetes.28.8.713.
32. Factor SM, Okun EM, Minase T. Capillary microaneurysms in the human diabetic heart. N Engl J Med 1980; 302:384-8; PMID:7351930; http://dx.doi.org/ 10.1056/NEJM198002143020706.
33. van Hoeven KH, Factor SM. A comparison of the pathological spectrum of hypertensive, diabetic and hypertensive-diabetic heart disease. Circulation 1990; 82:848-55; PMID:2394006; http://dx.doi.org/10.1161/01.CIR.82.3.848.
34. 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; 179:639-50; PMID:21704010; http://dx.doi.org/10.1016/j.ajpath.2011.04.034.
35. Lu H, Buchan RJ, Cook SA. MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovasc Res 2010; 86:410-20; PMID:20080987; http://dx.doi.org/10.1093/cvr/cvq010.
36. Jordan SD, Krüger M, Willmes DM, Redemann N, Wunderlich FT, Brönneke HS, et al. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat Cell Biol 2011; 13:434-46; PMID:21441927; http://dx.doi.org/10.1038/ncb2211.
37. Elia L, Quintavalle M, Zhang J, Contu R, Cossu L, Latronico MV, et al. The knockout of miR-143 and -145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ 2009; 16:1590-8; PMID:19816508; http://dx.doi.org/10.1038/cdd.2009.153.
38. Trajkovski M, Hausser J, Soutschek J, Bhat B, Akin A, Zavolan M, et al. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature 2011; 474:649-53; PMID:21654750; http://dx.doi.org/10.1038/nature10112.
39. Granjon A, Gustin MP, Rieusset J, Lefai E, Meugnier E, Güller I, et al. The microRNA signature in response to insulin reveals its implication in the transcriptional action of insulin in human skeletal muscle and the role of a sterol regulatory element-binding protein-1c/myocyte enhancer factor 2C pathway. Diabetes 2009; 58:2555-64; PMID:19720801; http://dx.doi.org/10.2337/db09-0165.
40. Dif N, Euthine V, Gonnet E, Laville M, Vidal H, Lefai E. Insulin activates human sterol-regulatory-element-binding protein-1c (SREBP-1c) promoter through SRE motifs. Biochem J 2006; 400:179-88; PMID:16831124; http://dx.doi.org/10.1042/BJ20060499.
41. He A, Zhu L, Gupta N, Chang Y, Fang F. Overexpression of micro ribonucleic acid 29, highly upregulated in diabetic rats, leads to insulin resistance in 3T3-L1 adipocytes. Mol Endocrinol 2007; 21:2785-94; PMID:17652184; http://dx.doi.org/10.1210/me.2007-0167.
42. Fioretto P, Steffes MW, Brown DM, Mauer SM. An overview of renal pathology in insulin-dependent diabetes mellitus in relationship to altered glomerular hemodynamics. Am J Kidney Dis 1992; 20:549-58; PMID:1462981.
43. Adler S. Diabetic nephropathy: Linking histology, cell biology and genetics. Kidney Int 2004; 66:2095-106; PMID:15496194; http://dx.doi.org/10. 1111/j.1523-755.2004.00988.x.
44. Susztak K, Raff AC, Schiffer M, Böttinger EP. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 2006; 55:225-33; PMID:16380497; http://dx.doi.org/10.2337/diabetes.55.01.06.db05-0894.
45. Lorenzen JM, Haller H, Thum T. MicroRNAs as mediators and therapeutic targets in chronic kidney disease. Nat Rev Nephrol 2011; 7:286-94; PMID:21423249; http://dx.doi.org/10.1038/nrneph.2011.26.
46. Krupa A, Jenkins R, Luo DD, Lewis A, Phillips A, Fraser D. Loss of MicroRNA-192 promotes fibrogenesis in diabetic nephropathy. J Am Soc Nephrol 2010; 21:438-47; PMID:20056746; http://dx.doi.org/10.1681/ASN.2009050530.
47. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 2001; 7:1267-78; PMID:11430829; http://dx.doi.org/10.1016/S1097-2765(01)00260-X.
48. Kato M, Zhang J, Wang M, Lanting L, Yuan H, Rossi JJ, et al. MicroRNA-192 in diabetic kidney glomeruli and its function in TGFbeta-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci USA 2007; 104:3432-7; PMID:17360662; http://dx.doi.org/10.1073/pnas.0611192104.
49. Putta S, Lanting L, Sun G, Lawson G, Kato M, Natarajan R. Inhibiting microRNA-192 ameliorates renal fibrosis in diabetic nephropathy. J Am Soc Nephrol 2012; 23:458-69; PMID:22223877; http://dx.doi.org/10.1681/ASN. 2011050485.
50. Kato M, Putta S, Wang M, Yuan H, Lanting L, Nair I, et al. TGFbeta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol 2009; 11:881-9; PMID:19543271; http://dx.doi.org/10.1038/ ncb1897.
51. Jiang BH, Liu LZ. PI3K/PTEN signaling in angiogenesis and tumorigenesis. Adv Cancer Res 2009; 102:19-65; PMID:19595306; http://dx.doi.org/10.1016/S0065- 230X(09)02002-8.
52. Dey N, Das F, Mariappan MM, Mandal CC, Ghosh-Choudhury N, Kasinath BS, et al. MicroRNA-21 orchestrates high glucose-induced signals to TOR complex 1, resulting in renal cell pathology in diabetes. J Biol Chem 2011; 286:25586-603; PMID:21613227; http://dx.doi.org/10.1074/jbc.M110.208066.
53. Chung AC, Huang XR, Meng X, Lan HY. miR-192 mediates TGFbeta/Smad3-driven renal fibrosis. J Am Soc Nephrol 2010; 21:1317-25; PMID:20488955; http://dx.doi.org/10.1681/ASN.2010020134.
54. Du B, Ma LM, Huang MB, Zhou H, Huang HL, Shao P, et al. High glucose downregulates miR-29a to increase collagen IV production in HK-2 cells. FEBS Lett 2010; 584:811-6; PMID:20067797; http://dx.doi.org/10.1016/j.febslet.2009. 12.053.
55. Wang Q, Wang Y, Minto AW, Wang J, Shi Q, Li X, et al. MicroRNA-377 is upregulated and can lead to increased fibronectin production in diabetic nephropathy. FASEB J 2008; 22:4126-35; PMID:18716028; http://dx.doi.org/10.1096/ fj.08-112326.
56. Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, et al. Circulating microRNAs in patients with coronary artery disease. Circ Res 2010; 107:677-84; PMID:20595655; http://dx.doi.org/10.1161/CIRCRESAHA.109. 215566.
57. Thum T. MicroRNA therapeutics in cardiovascular medicine. EMBO Mol Med 2012; 4:3-14; PMID:22162462; http://dx.doi.org/10.1002/emmm.201100191.
58. Hutvágner G, Simard MJ, Mello CC, Zamore PD. Sequence-specific inhibition of small RNA function. PLoS Biol 2004; 2:98; PMID:15024405; http://dx.doi.org/10.1371/journal.pbio.0020098.
59. Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005; 438:685-9; PMID:16258535; http://dx.doi.org/10.1038/nature04303.
60. Stenvang J, Kauppinen S. MicroRNAs as targets for antisense-based therapeutics. Expert Opin Biol Ther 2008; 8:59-81; PMID:18081537; http://dx.doi.org/10.1517/14712598.8.1.59.
61. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010; 327:198-201; PMID:19965718; http://dx.doi.org/10.1126/science.1178178.