Circulating microRNA as a diagnostic marker in populations with type 2diabetes mellitus and diabetic complications

Journal of the Chinese Medical Association

Volumn 78, Issue 4, 2015, Pages 204-211

  Chien, Hung Yu ^a   Lee, Tai Ping ^a,b   Chen, Chang Yi ^b   Chiu, Yen Hui ^a   Lin, Yi Chun ^a   Lee, Lon Shyong ^a   Li, Wan Chun ^a,b  

^a TAIPEI CITY HOSPITAL   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Biomarkers; Complications; Diabetes mellitus; Diagnosis; MicroRNAs

Indexed keywords

BIOLOGICAL MARKER; MESSENGER RNA; MICRORNA;

ADIPOSE TISSUE; ALBUMINURIA; ARTICLE; BODY FLUID; DIABETIC NEPHROPATHY; DIABETIC PATIENT; DISEASE COURSE; HUMAN; IMMUNOGLOBULIN A NEPHROPATHY; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN SENSITIVITY; KIDNEY FIBROSIS; LIVER; MUSCLE; NON INSULIN DEPENDENT DIABETES MELLITUS; PERIPHERAL BLOOD MONONUCLEAR CELL; PROGNOSIS; TARGET ORGAN; BLOOD; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 2;

BIOMARKERS; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 2; HUMANS; MICRORNAS;

EID: 84928205075     PISSN: 17264901     EISSN: 17287731     Source Type: Journal    
DOI: 10.1016/j.jcma.2014.11.002     Document Type: Review

References (93)

1. Wild S., Roglic G., Green A., Sicree R., King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004, 27:1047-1053.
2. Prentki M., Vischer S., Glennon M.C., Regazzi R., Deeney J.T., Corkey B.E. Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J Biol Chem 1992, 267:5802-5810.
3. Halban P.A., German M.S., Kahn S.E., Weir G.C. Current status of islet cell replacement and regeneration therapy. J Clin Endocrinol Metab 2010, 95:1034-1043.
4. Bornfeldt K.E., Tabas I. Insulin resistance, hyperglycemia, and atherosclerosis. Cell Metab 2011, 14:575-585.
5. Yang W.C., Hwang S.J., Chiang S.S., Chen H.F., Tsai S.T. The impact of diabetes on economic costs in dialysis patients: experiences in Taiwan. Diabetes Res Clin Pract 2009, 54:S47-54.
6. Brown S.H., Abdelhafiz A.H. Trials review: cardiovascular outcome with intensive glycemic control and implications for patients with type 2 diabetes. Postgrad Med J 2009, 121:31-41.
7. Weir G.C., Bonner-Weir S. Five stages of evolving beta-cell dysfunction during progression to diabetes. Diabetes 2005, 53:S16-21.
8. Bain J.R., Stevens R.D., Wenner B.R., Ilkayeva O., Muoio D.M., Newgard C.B. Metabolomics applied to diabetes research: moving from information to knowledge. Diabetes 2009, 58:2429-2443.
9. Etheridge A., Gomes C.P., Pereira R.W., Galas D., Wang K. The complexity, function and applications of RNA in circulation. Front Genet 2013, 4:115.
10. Gilad S., Meiri E., Yogev Y., Benjamin S., Lebanony D., Yerushalmi N., et al. Serum microRNAs are promising novel biomarkers. PLoS One 2008, 3:e3148.
11. Chen X., Ba Y., Ma L., Cai X., Yin Y., Wang K., 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.
12. Park N.J., Zhou H., Elashoff D., Henson B.S., Kastratovic D.A., Abemayor E., et al. Salivary microRNA: discovery, characterization, and clinical utility for oral cancer detection. Clin Cancer Res 2009, 15:5473-5477.
13. Weber J.A., Baxter D.H., Zhang S., Huang D.Y., Huang K.H., Lee M.J., et al. The microRNA spectrum in 12 body fluids. Clin Chem 2010, 56:1733-1741.
14. Kong Y.W., Cannell I.G., de Moor C.H., Hill K., Garside P.G., Hamilton T.L., et al. The mechanism of micro-RNA-mediated translation repression is determined by the promoter of the target gene. Proc Natl Acad Sci U S A 2008, 105:8866-8871.
15. Kloosterman W.P., Plasterk R.H. The diverse functions of microRNAs in animal development and disease. Dev Cell 2006, 11:441-450.
16. Baek D., Villen J., Shin C., Camargo F.D., Gygi S.P., Bartel D.P. The impact of microRNAs on protein output. Nature 2008, 455:64-71.
17. Bhattacharyya S.N., Habermacher R., Martine U., Closs E.I., Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 2006, 125:1111-1124.
18. Guo H., Ingolia N.T., Weissman J.S., Bartel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
19. Miranda K.C., Huynh T., Tay Y., Ang Y.S., Tam W.L., Thomson A.M., et al. A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell 2006, 126:1203-1217.
20. Kantharidis P., Wang B., Carew R.M., Lan H.Y. Diabetes complications: the microRNA perspective. Diabetes 2011, 60:1832-1837.
21. Xu J., Zhao J., Evan G., Xiao C., Cheng Y., Xiao J. Circulating microRNAs: novel biomarkers for cardiovascular diseases. J Mol Med 2012, 90:865-875.
22. Koutsis G., Siasos G., Spengos K. The emerging role of microRNA in stroke. Curr Top Med Chem 2013, 13:1573-1588.
23. Nesca V., Guay C., Jacovetti C., Menoud V., Peyot M.L., Laybutt D.R., 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, 56:2203-2212.
24. Lynn F.C., Skewes-Cox P., Kosaka Y., McManus M.T., Harfe B.D., German M.S. MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes 2007, 56:2938-2945.
25. Poy M.N., 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 U S A 2009, 106:5813-5818.
26. 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, 15:287-293.
27. Mi Q.S., He H.Z., Dong Z., Isales C., Zhou L. MicroRNA deficiency in pancreatic islet cells exacerbates streptozotocin-induced murine autoimmune diabetes. Cell Cycle 2010, 9:3127-3129.
28. Ruan Q., Wang T., Kameswaran V., Wei Q., Johnson D.S., Matschinsky F., et al. The microRNA-21-PDCD4 axis prevents type 1 diabetes by blocking pancreatic beta cell death. Proc Natl Acad Sci U S A 2011, 108:12030-12035.
29. Xu G., Chen J., Jing G., Shalev A. Thioredoxin-interacting protein regulates insulin transcription through microRNA-204. Nat Med 2013, 19:1141-1146.
30. Jacovetti C., Abderrahmani A., Parnaud G., Jonas J.C., Peyot M.L., Cornu M., et al. MicroRNAs contribute to compensatory β cell expansion during pregnancy and obesity. J Clin Invest 2012, 122:3541-3551.
31. Shi Z., Zhao C., Guo X., Ding H., Cui Y., Shen R., et al. Differential expression of microRNAs in omental adipose tissue from gestational diabetes mellitus subjects reveals miR-222 as a regulator of ERα expression in estrogen-induced insulin resistance. Endocrinology 2014, 155:1982-1990.
32. Tattikota S.G., Rathjen T., McAnulty S.J., Wessels H.H., Akerman I., van de Bunt M., et al. Argonaute2 mediates compensatory expansion of the pancreatic β cell. Cell Metab 2014, 19:122-134.
33. Zhao C., Zhang T., Shi Z., Ding H., Ling X. MicroRNA-518d regulates PPARα protein expression in the placentas of females with gestational diabetes mellitus. Mol Med Rep 2014, 9:2085-2090.
34. Zhao E., Keller M.P., Rabaglia M.E., Oler A.T., Stapleton D.S., Schueler K.L., et al. Obesity and genetics regulate microRNAs in islets, liver, and adipose of diabetic mice. Mamm Genome 2009, 20:476-485.
35. Fernandez-Valverde S.L., Taft R.J., Mattick J.S. MicroRNAs in β-cell biology, insulin resistance, diabetes and its complications. Diabetes 2011, 60:1825-1831.
36. Williams M.D., Mitchell G.M. MicroRNAs in insulin resistance and obesity. Exp Diabetes Res 2012, 2012:484696.
37. Honardoost M., Reza Sarookhani M., Arefian E., Soleimani M. Insulin resistance associated genes and miRNAs. Appl Biochem Biotechnol 2014, 174:63-80.
38. 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, 21:2785-2794.
39. Ling H.Y., Ou H.S., Feng S.D., Zhang X.Y., Tuo Q.H., Chen L.X., et al. Changes in microRNA (miR) profile and effects of miR-320 in insulin-resistant 3T3-L1 adipocytes. Clin Exp Pharmacol Physiol 2009, 36:e32-e39.
40. Xie H., Lim B., Lodish H.F. MicroRNAs induced during adipogenesis that accelerate fat cell development are downregulated in obesity. Diabetes 2009, 58:1050-1057.
41. Ling H.Y., Hu B., Hu X.B., Zhong J., Feng S.D., Qin L., et al. MiRNA-21 reverses high glucose and high insulin induced insulin resistance in 3T3-L1 adipocytes through targeting phosphatase and tensin homologue. Exp Clin Endocrinol Diabetes 2012, 120:553-559.
42. Chen Y.H., Heneidi S., Lee J.M., Layman L.C., Stepp D.W., Gamboa G.M., et al. miRNA-93 inhibits GLUT4 and is overexpressed in adipose tissue of polycystic ovary syndrome patients and women with insulin resistance. Diabetes 2013, 62:2278-2286.
43. Granjon A., Gustin M.P., 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, 58:2555-2564.
44. Lu H., Buchan R.J., Cook S.A. MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovasc Res 2010, 86:410-420.
45. Frost R.J., Olson E.N. Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs. Proc Natl Acad Sci U S A 2011, 108:21075-21080.
46. Jordan S.D., Krüger M., Willmes D.M., Redemann N., Wunderlich F.T., Brönneke H.S., et al. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat Cell Biol 2011, 13:434-446.
47. Zhou B., Li C., Qi W., Zhang Y., Zhang F., Wu J.X., et al. Downregulation of miR-181a upregulates sirtuin-1 (SIRT1) and improves hepatic insulin sensitivity. Diabetologia 2012, 55:2032-2043.
48. Kornfeld J.W., Baitzel C., Könner A.C., Nicholls H.T., Vogt M.C., Herrmanns K., et al. Obesity-induced overexpression of miR-802 impairs glucose metabolism through silencing of Hnf1b. Nature 2013, 494:111-115.
49. Xiao F., Yu J., Liu B., Guo Y., Li K., Deng J., et al. A novel function of microRNA 130a-3p in hepatic insulin sensitivity and liver steatosis. Diabetes 2014, 63:2631-2642.
50. Ai J., Zhang R., Li Y., Pu J., Lu Y., Jiao J., et al. Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun 2010, 391:73-77.
51. Mendell J.T. MicroRNAs: critical regulators of development, cellular physiology and malignancy. Cell Cycle 2005, 4:1179-1184.
52. El-Hefnawy T., Raja S., Kelly L., Bigbee W.L., Kirkwood J.M., Luketich J.D., et al. Characterization of amplifiable, circulating RNA in plasma and its potential as a tool for cancer diagnostics. Clin Chem 2004, 50:564-573.
53. Kosaka 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.
54. Arroyo J.D., Chevillet J.R., Kroh E.M., Ruf I.K., Pritchard C.C., Gibson D.F., et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A 2011, 108:5003-5008.
55. Vickers K.C., Palmisano B.T., Shoucri B.M., Shamburek R.D., Remaley A.T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011, 13:423-433.
56. Creemers E.E., Tijsen A.J., Pinto Y.M. Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease?. Circ Res 2012, 110:483-495.
57. Diehl P., Fricke A., Sander L., Stamm J., Bassler N., Htun N., et al. Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res 2012, 93:633-644.
58. Guay C., Regazzi R. Circulating microRNAs as novel biomarkers for diabetes mellitus. Nat Rev Endocrinol 2013, 9:513-521.
59. Erener S., Mojibian M., Fox J.K., Denroche H.C., Kieffer T.J. Circulating miR-375 as a biomarker of β-cell death and diabetes in mice. Endocrinology 2013, 154:603-608.
60. Dehwah M.A., Xu A., Huang Q. MicroRNAs and type 2 diabetes/obesity. J Genet Genomics 2012, 39:11-18.
61. Ferland-McCollough D., Ozanne S.E., Siddle K., Willis A.E., Bushell M. The involvement of microRNAs in type 2 diabetes. Biochem Soc Trans 2010, 38:1565-1570.
62. Wang X., Sundquist J., Zöller B., Memon A.A., Palmér K., Sundquist K., et al. Determination of 14 circulating microRNAs in Swedes and Iraqis with and without diabetes mellitus type 2. PLoS One 2014, 9:e86792.
63. Fleischhacker S.N., Bauersachs S., Wehner A., Hartmann K., Weber K. Differential expression of circulating microRNAs in diabetic and healthy lean cats. Vet J 2013, 197:688-693.
64. 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, 107:810-817.
65. Rong Y., Bao W., Shan Z., Liu J., Yu X., Xia S., et al. Increased microRNA-146a levels in plasma of patients with newly diagnosed type 2 diabetes mellitus. PLoS One 2013, 8:e73272.
66. Zhang T., Lv C., Li L., Chen S., Liu S., Wang C., et al. Plasma miR-126 is a potential biomarker for early prediction of type 2 diabetes mellitus in susceptible individuals. Biomed Res Int 2013, 2013:761617.
67. Kong L., Zhu J., Han W., Jiang X., Xu M., Zhao Y., et al. Significance of serum microRNAs in pre-diabetes and newly diagnosed type 2 diabetes: a clinical study. Acta Diabetol 2011, 48:61-69.
68. Bonner C., Nyhan K.C., Bacon S., Kyithar M.P., Schmid J., Concannon C.G., et al. Identification of circulating microRNAs in HNF1A-MODY carriers. Diabetologia 2013, 56:1743-1751.
69. Karolina D.S., Armugam A., Tavintharan S., Wong M.T., Lim S.C., Sum C.F., et al. MicroRNA 144 impairs insulin signaling by inhibiting the expression of insulin receptor substrate 1 in type 2 diabetes mellitus. PLoS One 2011, 6:e22839.
70. Corral-Fernández N.E., Salgado-Bustamante M., Martínez-Leija M.E., Cortez-Espinosa N., García-Hernández M.H., Reynaga-Hernández E., 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.
71. Collares C.V., Evangelista A.F., Xavier D.J., Rassi D.M., Arns T., Foss-Freitas M.C., 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.
72. Meng S., Cao J.T., Zhang B., Zhou Q., Shen C.X., Wang C.Q. Downregulation of microRNA-126 in endothelial progenitor cells from diabetes patients, impairs their functional properties, via target gene Spred-1. J Mol Cell Cardiol 2012, 53:64-72.
73. Silva V.A., Polesskaya A., Sousa T.A., Corrêa V.M., André N.D., Reis R.I., 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, 17:2228-2240.
74. Roggli E., Gattesco S., Caille D., Briet C., Boitard C., Meda P., et al. Changes in microRNA expression contribute to pancreatic β-cell dysfunction in prediabetic NOD mice. Diabetes 2012, 61:1742-1751.
75. Wang G., Kwan B.C., Lai F.M., Chow K.M., Li P.K., Szeto C.C. Urinary miR-21, miR-29, and miR-93: novel biomarkers of fibrosis. Am J Nephrol 2012, 36:412-418.
76. Hayat S.A., Patel B., Khattar R.S., Malik R.A. Diabetic cardiomyopathy: mechanisms, diagnosis and treatment. Clin Sci 2004, 107:539-557.
77. Li Y., Song Y.H., Li F., Yang T., Lu Y.W., Geng Y.J. MicroRNA-221 regulates high glucose-induced endothelial dysfunction. Biochem Biophys Res Commun 2009, 381:81-83.
78. Tepper O.M., Galiano R.D., Capla J.M., Kalka C., Gagne P.J., Jacobowitz G.R., et al. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 2002, 106:2781-2786.
79. He T., Smith L.A., Harrington S., Nath K.A., Caplice N.M., Katusic Z.S. Transplantation of circulating endothelial progenitor cells restores endothelial function of denuded rabbit carotid arteries. Stroke 2004, 35:2378-2384.
80. Zeng J., Xiong Y., Li G., Liu M., He T., Tang Y., 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.
81. Simonson M.S. Phenotypic transitions and fibrosis in diabetic nephropathy. Kidney Int 2007, 71:846-854.
82. Kalluri R. EMT: when epithelial cells decide to become mesenchymal-like cells. J Clin Invest 2009, 119:1417-1419.
83. Li J.Y., Yong T.Y., Michael M.Z., Gleadle J.M. The role of microRNAs in kidney disease. Nephrology 2010, 15:599-608.
84. Kato M., Zhang J., Wang M., Lanting L., Yuan H., Rossi J.J., et al. MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci U S A 2007, 104:3432-3437.
85. Zhang Z., Peng H., Chen J., Chen X., Han F., Xu X., et al. MicroRNA-21 protects from mesangial cell proliferation induced by diabetic nephropathy in db/db mice. FEBS Lett 2009, 583:2009-2014.
86. Long J., Wang Y., Wang W., Chang B.H., Danesh F.R. MicroRNA-29c is a signature microRNA under high glucose conditions that targets Sprouty homolog 1, and its invivo knockdown prevents progression of diabetic nephropathy. J Biol Chem 2011, 286:11837-11848.
87. Alvarez M.L., Khosroheidari M., Kanchi Ravi R., DiStefano J.K. Comparison of protein, microRNA, and mRNA yields using different methods of urinary exosome isolation for the discovery of kidney disease biomarkers. Kidney Int 2012, 82:1024-1032.
88. Argyropoulos C., Wang K., McClarty S., Huang D., Bernardo J., Ellis D., et al. Urinary microRNA profiling in the nephropathy of type 1 diabetes. PLoS One 2013, 8:e54662.
89. Peng H., Zhong M., Zhao W., Wang C., Zhang J., Liu X., et al. Urinary miR-29 correlates with albuminuria and carotid intima-media thickness in type 2 diabetes patients. PLoS One 2013, 8:e82607.
90. Du B., Ma L.M., Huang M.B., Zhou H., Huang H.L., Shao P., et al. High glucose down-regulates miR-29a to increase collagen IV production in HK-2 cells. FEBS Lett 2010, 584:811-816.
91. Qin W., Chung A.C., Huang X.R., Meng X.M., Hui D.S., Yu C.M., et al. TGF-β/Smad3 signaling promotes renal fibrosis by inhibiting miR-29. J Am Soc Nephrol 2011, 22:1462-1474.
92. Yang Y., Xiao L., Li J., Kanwar Y.S., Liu F., Sun L. Urine miRNAs: potential biomarkers for monitoring progression of early stages of diabetic nephropathy. Med Hypotheses 2013, 81:274-278.
93. Pescador N., Pérez-Barba M., Ibarra J.M., Corbatón A., Martínez-Larrad M.T., Serrano-Ríos M. Serum circulating microRNA profiling for identification of potential type 2 diabetes and obesity biomarkers. PLoS One 2013, 8:e77251.