Regulation of insulin resistance by multiple MiRNAs via targeting the GLUT4 signalling pathway

Cellular Physiology and Biochemistry

Volumn 38, Issue 5, 2016, Pages 2063-2078

  Zhou, Tong ^a   Meng, Xianhong ^a   Che, Hui ^a   Shen, Nannan ^a   Xiao, Dan ^a   Song, Xiaotong ^a   Liang, Meihua ^a   Fu, Xuelian ^a   Ju, Jiaming ^a   Li, Yang ^a   Xu, Chaoqian ^a   Zhang, Yong ^a,b   Wang, Lihong ^a,b  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b Biopharmaceutical Institute   (China)

Author keywords

Glucose transporter 4; Insulin resistant L6 cells; MiR 106b; MiR 27a; MiR 30d; Mitogen activated protein kinase 14; MTg AMO; Phosphatidylinositol 3 kinase regulatory subunit beta; Type 2 diabetes mellitus

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; GLUCOSE; GLUCOSE TRANSPORTER 4; MESSENGER RNA; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE 14; PHOSPHATIDYLINOSITOL 3 KINASE; 3' UNTRANSLATED REGION; ANTAGOMIR; PIK3CB PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROL GROUP; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GENE TARGETING; GENETIC TRANSFECTION; GLUCOSE INTAKE; GLUCOSE TRANSPORT; IMMUNOFLUORESCENCE; INSULIN RESISTANCE; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; 3' UNTRANSLATED REGION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMICALLY INDUCED; EXPERIMENTAL DIABETES MELLITUS; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; RAT; SEQUENCE ALIGNMENT; SKELETAL MUSCLE; WISTAR RAT;

3' UNTRANSLATED REGIONS; ANIMALS; ANTAGOMIRS; BASE SEQUENCE; CELL LINE; DIABETES MELLITUS, EXPERIMENTAL; DOWN-REGULATION; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; INSULIN RESISTANCE; MALE; MICRORNAS; MITOGEN-ACTIVATED PROTEIN KINASE 14; MUSCLE, SKELETAL; PHOSPHATIDYLINOSITOL 3-KINASES; RATS; RATS, WISTAR; RNA, MESSENGER; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 84973154959     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000445565     Document Type: Article

References (50)

1. Chiassoli JL, Josse RG, Gomis R, Hanefeld M, Karasik A, Laakso M: STOP-NIDDM Trail Research Group: Acarbose for prevention of type 2 diabetes mellitus: the STOP-NIDDM randomised trial. Lancet 2002;359:2072-2077.
2. Navas-Acien A, Silbergeld EK, Streeter RA, Clark JM, Burke TA, Guallar E: Arsenic exposure and type 2 diabetes: a systematic review of the experimental and epidemiological evidence. Environ Health Perspect 2006;114:641-648.
3. Ginter E, Simko V: Diabetes type 2 pandemic in 21st century. Bratisl Lek Listy 2010;111:134-137.
4. Sung KC, Jeong WS, Wild SH, Byrne CD: Combined influence of insulin resistance, overweight/obesity and fatty liver as risk factors for type 2 diabetes. Diabetes Care 2012;35:717-722.
5. Tsai S, Clemente-Casares X, Revelo XS, Winer S, Winer DA: Are obesity-related insulin resistance and type 2 diabetes autoimmune diseases? Diabetes 2015;64:1886-1897.
6. Poletto AC, David-Silva A, Yamamoto AP, Machado UF, Furuya DT: Reduced Slc2a4/GLUT4 expression in subcutaneous adipose tissue of monosodium glutamate obese mice is recovered after atorvastatin treatment. Diabetol Metab Syndr 2015;7:18.
7. Fang P, Shi M, Guo L, He B, Wang Q, Yu M, Bo P, Zhang Z: Effect of endogenous galanin on glucose transporter 4 expression in cardiac muscle of type 2 diabetic rats. Peptides 2014;62:159-163.
8. Castorena CM, Arias EB, Sharma N, Bogan JS, Cartee GD: Fiber type effects on contraction-stimulated glucose uptake and GLUT4 abundance in single fibers from rat skeletal muscle. Am J Physiol Endocrinol Metab 2015;308:E223-230.
9. Baranowski M, Zabielski P, Btachnio-Zabielska AU, Harasim E, Chabowski A,Górski J: Insulin-sensitizing effect of LXR agonist T0901317 in high-fat fed rats is associated with restored muscle GLUT4 expression and insulin-stimulated AS160 phosphorylation. Cell Physiol Biochem 2014;33:1047-1057.
10. Yoshino H, Seki N, Itesako T, Chiyomaru T, Nakagawa M, Enokida HAberrant expression of microRNAs in bladder cancer. Nat Rev Urol 2013;10:396-404.
11. Yang GH, Wang F, Yu J, Wang XS, Yuan JY, Zhang JW: MicroRNAs are involved in erythroid differentiation control. J Cell Biochem 2009;107:548-556.
12. Zhang Z, Chang H, Li Y, Zhang T, Zou J, Zheng X, Wu J: MicroRNAs: potential regulators involved in human anencephaly. Int J Biochem Cell Biol 2010;42:367-374.
13. Gauthier BR, Wollheim CB: MicroRNAs: 'ribo-regulators' of glucose homeostasis. Nat Med 2006;12:36-38.
14. Hammond SM. Micro RNA therapeutics: a new niche for antisense nucleic acids. Trends Mol Med 2006;12:99-101.
15. Yang B, Lin H, Xiao J, Lu Y, Luo X, Li B, Zhang Y, Xu C, Bai Y, Wang H, Chen G, Wang Z: The muscle-specific micro RNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat Med 2007;13:486-491.
16. Wijesekara N, Zhang LH, Kang MH, Abraham T, Bhattacharjee A, Warnock GL, Verchere CB, Hayden MR: miR-33a modulates ABCA1 expression, cholesterol accumulation, and insulin secretion in pancreatic islets. Diabetes 2012;61:653-658.
17. Wang L, Zhang N, Pan HP, Wang Z, Cao ZY: MiR-499-5p Contributes to Hepatic Insulin Resistance by Suppressing PTEN. Cell Physiol Biochem 2015;36:2357-2365.
18. Baroukh N, Ravier MA, Loder MK, Hill EV, Bounacer A, Scharfmann R, Rutter GA, Van Obberghen E: MicroRNA-124a regulates Foxa2 expression and intracellular signaling in pancreatic beta-cell lines. J Biol Chem 2007;282:19575-19588.
19. Dou L, Wang S, Sui X, Meng X, Shen T, Huang X, Guo J, Fang W, Man Y, Xi J, Li J: MiR-301a mediates the effect of IL-6 on the AKT/GSK pathway and hepatic glycogenesis by regulating PTEN expression. Cell Physiol Biochem 2015;35:1413-1424.
20. Chuang TY, Wu HL, Chen CC, Gamboa GM, Layman LC, Diamond MP, Azziz R, Chen YH: MicroRNA-223 Expression Is Upregulated in Insulin Resistant Human Adipose Tissue. J Diabetes Res 2015;2015:943659.
21. Poy MN, Spranger M, Stoffel M: microRNAs and the regulation of glucose and lipid metabolism. Diabetes Obes Metab 2007;9:67-73.
22. Xu P, Vernooy SY, Guo M, Hay BA: The Drosophila microRNA Mir-14 suppresses cell death and is required for normal fat metabolism. Curr Biol 2003;13:790-795.
23. Feng YY, Xu XQ, Ji CB, Shi CM, Guo XR, Fu JF: Aberrant hepatic microRNA expression in nonalcoholic fatty liver disease. Cell Physiol Biochem 2014;34:1983-1997.
24. 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.
25. Chakraborty C, Doss CG, Bandyopadhyay S, Agoramoorthy G: Influence of miRNA in insulin signaling pathway and insulin resistance: micro-molecules with a major role in type-2 diabetes. Wiley Interdiscip Rev RNA 2014;5:697-712.
26. Horie T, Ono K, Nishi H, Iwanaga Y, Nagao K, Kinoshita M, Kuwabara Y, Takanabe R, Hasegawa K, Kita T, Kimura T: MicroRNA-133 regulates the expression of GLUT4 by targeting KLF15 and is involved in metabolic control in cardiac myocytes. Biochem Biophys Res Commun 2009;389:315-320.
27. Lu H, Buchan RJ, Cook SA: MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovasc Res 2010;86:410-420.
28. Lu Y, Xiao J, Lin H, Bai Y, Luo X, Wang Z, Yang B: A single anti-microRNA antisense oligodeoxyribonucleotide (AMO) targeting multiple microRNAs offers an improved approach for microRNA interference. Nucleic Acids Res 2009;37:e24.
29. Ai J, Wang N, Yang M, Du ZM, Zhang YC, Yang BF: Development of Wistar rat model of insulin resistance. World J Gastroenterol 2005;11:3675-3679.
30. Ai J, Yan X, Zhao L, Lu Y, Liang F, Cai B, Li G, Lu Y, Yang B: The protective effect of Darning capsule on heart function in streptozocin-induced diabetic rats with hyperlipidemia. Biol Pharm Bull 2009;32:1354-1358.
31. Shen N, Li X, Zhou T, Bilal MU, Du N, Hu Y, Qin W, Xie Y, Wang H, Wu J, Ju J, Fang Z, Wang L, Zhang Y: Shensong Yangxin Capsule prevents diabetic myocardial fibrosis by inhibiting TGF-betal/Smad signaling. ] Ethnopharmacol 2014;157:161-170.
32. Kallen AN, Zhou XB, Xu J, Qiao C, Ma J, Yan L, Lu L, Liu C, Yi JS, Zhang H, Min W, Bennett AM, Gregory RI, Ding Y, Huang Y: The imprinted H19 IncRNA antagonizes let-7 microRNAs. Mol Cell 2013;52:101-112.
33. Kong L, Zhu J, Han W, Jiang X, Xu M, Zhao Y, Dong Q Pang Z, Guan Q Gao L, Zhao J, Zhao L: Significance of serum microRNAs in pre-diabetes and newly diagnosed type 2 diabetes: a clinical study. Acta Diabetol 2011;48:61-69.
34. Zhang Y, Yang L, Gao YF, Fan ZM, Cai XY, Liu MY, Guo XR, Gao CL, Xia ZK: MicroRNA-106b induces mitochondrial dysfunction and insulin resistance in C2C12 myotubes by targeting mitofusin-2. Mol Cell Endocrinol 2013;381:230-240.
35. Herrera BM, Lockstone HE, Taylor JM, Ria M, Barrett A, Collins S, Kaisaki P, Argoud K, Fernandez C, Travers ME, Grew JP, Randall JC, Gloyn AL, Gauguier D, McCarthy MI, Lindgren CM: Global microRNA expression profiles in insulin target tissues in a spontaneous rat model of type 2 diabetes. Diabetologia 2010;53:1099-1109.
36. Cline GW, Petersen KF, Krssak M, Shen J, Hundal RS, Trajanoski Z, Inzucchi S, Dresner A, Rothman DL, Shulman GI: Impaired glucose transport as a cause of decreased insulin-stimulated muscle glycogen synthesis in type 2 diabetes. N Engl J Med 1999;341:240-246.
37. Rezende LF1, Santos GJ, Santos-Silva JC, Carneiro EM, Buschero AC: Ciliary neurotrophic factor (CNTF] protects non-obese Swiss mice against type 2 diabetes by increasing beta cell mass and reducing insulin clearance. Diabetologia 2012;55:1495-1504.
38. Sato K, Nakamura A, Shirakawa J, Muraoka T, Togashi Y, Shinoda K, Orime K, Kubota N, Kadowaki T, Terauchi Y: Impact of the dipeptidyl peptidase-4 inhibitor vildagliptin on glucose tolerance and ß-cell function and mass in insulin receptor substrate-2-knockout mice fed a high-fat diet. Endocrinology 2012;153:1093-1102.
39. LizunovVA, Stenkula KG, Lisinski I, Gavrilova 0, Yver DR, Chadt A, Al-Hasani H, Zimmerberg J, Cushman SW: Insulin stimulates fusion, but not tethering, of GLUT4 vesicles in skeletal muscle of HA-GLUT4-GFP transgenic mice. Am J Physiol Endocrinol Metab 2012;302:E950-960.
40. Baron ADI, Brechtel G, Wallace P, Edelman SV: Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans. Am J Physiol 1988;255:E769-774.
41. Blüher M, Bashan N, Shai I, Harman-Boehm I, Tarnovscki T, Avinaoch E, Stumvoll M, Dietrich A, Klöting N, Rudich A: Activated Askl-MKK4-p38MAPK/JNK stress signaling pathway in human omental fat tissue may link macrophage infiltration to whole-body Insulin sensitivity. J Clin Endocrinol Metab 2009;94:2507-2515.
42. Al-Lahham R, Deford JH, Papaconstantinou J: Mitochondrial-Generated ROS Down Regulates Insulin Signaling via Activation of the p38MAPK Stress Response Pathway. Mol Cell Endocrinol 2016;419:1-11.
43. Hemi R, Yochananov Y, Barhod E, Kasher-Meron M, Karasik A, Tirosh A, Kanety H: p38 mitogen-activated protein kinase-dependent transactivation of ErbB receptor family: a novel common mechanism for stress-induced IRS-1 serine phosphorylation and insulin resistance. Diabetes 2011;60:1134-1145.
44. Shen Y, Zhao Y, Zheng D, Chang X, Ju S, Guo L: Effects of orexin A on GLUT4 expression and lipid content via MAPK signaling in 3T3-L1 adipocytes. J Steroid Biochem Mol Biol 2013;138:376-383.
45. Engelman JA, Luo J, Cantley LC: The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 2006;7:606-619.
46. Manna P, Jain SK: Phosphatidylinositol-3,4,5-triphosphate and cellular signaling: implications for obesity and diabetes. Cell Physiol Biochem 2015;35:1253-1275.
47. Zhu H, Shyh-Chang N, Segrè AV, Shinoda G, Shah SP, Einhorn WS, Takeuchi A, Engreitz JM, Hagan JP, Kharas MG, Urbach A, Thornton JE, Triboulet R, Gregory RI; DIAGRAM Consortium; MAGIC Investigators, Altshuler D, Daley GQ: The Lin28/let-7 axis regulates glucose metabolism. Cell 2011;147:81-94.
48. Frost RJ, Olson EN: Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs. Proc Natl Acad Sci USA 2011;108:21075-21080.
49. Michelle Furtado L, Poon V, Klip A: GLUT4 activation: thoughts on possible mechanisms. Acta Physiol Scand 2003;178:287-296.
50. Ueda-Wakagi M, Mukai R, Fuse N, Mizushina Y, Ashida H: 3-0-Acyl-epicatechins Increase Glucose Uptake Activity and GLUT4 Translocation through Activation of PI3K Signaling in Skeletal Muscle Cells. Int J Mol Sci 2015;16:16288-16299.