MicroRNA-194 modulates glucose metabolism and its skeletal muscle expression is reduced in diabetes

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Latouche, Celine ^a   Natoli, Alaina ^a   Reddy Luthmoodoo, Medini ^a   Heywood, Sarah E ^a   Armitage, James A ^b   Kingwell, Bronwyn A ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b DEAKIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 194; UNCLASSIFIED DRUG; GLUCOSE; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; INSULIN; MIRN194 MICRORNA, HUMAN; MIRN194 MICRORNA, RAT; PROTEIN KINASE B;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE COURSE; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; GLUCONEOGENESIS; GLUCOSE METABOLISM; GLUCOSE OXIDATION; HUMAN; HUMAN TISSUE; IMPAIRED GLUCOSE TOLERANCE; IN VITRO STUDY; INSULIN RESISTANCE; LIPID DIET; MALE; MICROARRAY ANALYSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PREGNANCY; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE CELL; WESTERN BLOTTING; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CELL LINE; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; MYOBLAST; OXIDATIVE PHOSPHORYLATION; PATHOLOGY; PREDIABETIC STATE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

ANIMALS; CELL LINE; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INSULIN; INSULIN RESISTANCE; MALE; MICE, INBRED C57BL; MICRORNAS; MITOCHONDRIA; MUSCLE, SKELETAL; MYOBLASTS; OXIDATIVE PHOSPHORYLATION; PREDIABETIC STATE; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84968764964     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0155108     Document Type: Article

References (54)

1. Ambros V. The functions of animal microRNAs. Nature. 2004; 431(7006):350-5. doi: 10.1038/nature02871 PMID: 15372042.
2. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116(2):281-97. PMID: 14744438.
3. Lu M, Zhang Q, Deng M, Miao J, Guo Y, Gao W, et al. An analysis of human microRNA and disease associations. PLoS One. 2008; 3(10):e3420. doi:10.1371/journal.pone.0003420 PMID: 18923704; PubMed Central PMCID: PMC2559869.
4. van Rooij E. The art of microRNA research. Circ Res. 2011; 108(2):219-34. doi:10.1161/CIRCRESAHA.110.227496 PMID: 21252150.
5. Lorenzen J, Kumarswamy R, Dangwal S, Thum T. MicroRNAs in diabetes and diabetes-associated complications. RNA Biol. 2012; 9(6):820-7. doi:10.4161/rna.20162 PMID: 22664916.
6. Kumar M, Nath S, Prasad HK, Sharma GD, Li Y. MicroRNAs: a new ray of hope for diabetes mellitus. Protein Cell. 2012; 3(10):726-38. doi:10.1007/s13238-012-2055-0 PMID: 23055040.
7. Poy MN, Spranger M, Stoffel M. microRNAs and the regulation of glucose and lipid metabolism. Diabetes Obes Metab. 2007; 9 Suppl 2:67-73. doi:10.1111/j.1463-1326.2007.00775.x PMID: 17919180.
8. Rottiers V, Najafi-Shoushtari SH, Kristo F, Gurumurthy S, Zhong L, Li Y, et al. MicroRNAs in metabolism and metabolic diseases. Cold Spring Harb Symp Quant Biol. 2011; 76:225-33. doi:10.1101/sqb.2011.76.011049 PMID: 22156303; PubMed Central PMCID: PMC3880782.
9. Alfaradhi MZ, Ozanne SE. Developmental programming in response to maternal overnutrition. Front Genet. 2011; 2:27. doi:10.3389/fgene.2011.00027 PMID: 22303323; PubMed Central PMCID: PMC3268582.
10. Armitage JA, Poston L, Taylor PD. Developmental origins of obesity and the metabolic syndrome: the role of maternal obesity. Front Horm Res. 2008; 36:73-84. doi:10.1159/0000115355 PMID: 18230895.
11. Nivoit P, Morens C, Van Assche FA, Jansen E, Poston L, Remacle C, et al. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia. 2009; 52(6):1133-42. doi:10.1007/s00125-009-1316-9 PMID: 19288075.
12. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EH, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008; 51(2):383-92. doi:10.1161/HYPERTENSIONAHA.107.101477 PMID: 18086952.
13. Taylor PD, McConnell J, Khan IY, Holemans K, Lawrence KM, Asare-Anane H, et al. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol. 2005; 288(1):R134-9. doi:10.1152/ajpregu.00355.2004 PMID: 15388492.
14. Bayol SA, Simbi BH, Stickland NC. A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol. 2005; 567(Pt 3):951-61. doi:10.1113/jphysiol.2005.088989 PMID: 16020464; PubMed Central PMCID: PMC1474235.
15. Latouche C, Heywood SE, Henry SL, Ziemann M, Lazarus R, El-Osta A, et al. Maternal overnutrition programs changes in the expression of skeletal muscle genes that are associated with insulin resistance and defects of oxidative phosphorylation in adult male rat offspring. J Nutr. 2014; 144(3):237-44. doi:10.3945/jn.113.186775 PMID: 24381224.
16. Kraegen EW, Clark PW, Jenkins AB, Daley EA, Chisholm DJ, Storlien LH. Development of muscle insulin resistance after liver insulin resistance in high-fat-fed rats. Diabetes. 1991; 40(11):1397-403. PMID: 1936601.
17. Park SY, Cho YR, Kim HJ, Higashimori T, Danton C, Lee MK, et al. Unraveling the temporal pattern of diet-induced insulin resistance in individual organs and cardiac dysfunction in C57BL/6 mice. Diabetes. 2005; 54(12):3530-40. PMID: 16306372.
18. Turner N, Kowalski GM, Leslie SJ, Risis S, Yang C, Lee-Young RS, et al. Distinct patterns of tissuespecific lipid accumulation during the induction of insulin resistance in mice by high-fat feeding. Diabetologia. 2013; 56(7):1638-48. doi:10.1007/s00125-013-2913-1 PMID: 23620060.
19. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25(4):402-8. doi:10.1006/meth.2001.1262 PMID: 11846609.
20. Ceddia RB, Sweeney G. Creatine supplementation increases glucose oxidation and AMPK phosphorylation and reduces lactate production in L6 rat skeletal muscle cells. J Physiol. 2004; 555(Pt 2):409-21. doi:10.1113/jphysiol.2003.056291 PMID: 14724211; PubMed Central PMCID: PMC1664837.
21. Murea M, Ma L, Freedman BI. Genetic and environmental factors associated with type 2 diabetes and diabetic vascular complications. Rev Diabet Stud. 2012; 9(1):6-22. doi:10.1900/RDS.2012.9.6 PMID: 22972441; PubMed Central PMCID: PMC3448170.
22. Ferland-McCollough D, Ozanne SE, Siddle K, Willis AE, Bushell M. The involvement of microRNAs in Type 2 diabetes. Biochem Soc Trans. 2010; 38(6):1565-70. doi:10.1042/BST0381565 PMID: 21118127.
23. Guay C, Roggli E, Nesca V, Jacovetti C, Regazzi R. Diabetes mellitus, a microRNA-related disease? Transl Res. 2011; 157(4):253-64. doi:10.1016/j.trsl.2011.01.009 PMID: 21420036.
24. Herrera BM, Lockstone HE, Taylor JM, Ria M, Barrett A, Collins S, et al. Global microRNA expression profiles in insulin target tissues in a spontaneous rat model of type 2 diabetes. Diabetologia. 2010; 53(6):1099-109. doi:10.1007/s00125-010-1667-2 PMID: 20198361; PubMed Central PMCID: PMC2860560.
25. Pandey AK, Agarwal P, Kaur K, Datta M. MicroRNAs in diabetes: tiny players in big disease. Cell Physiol Biochem. 2009; 23(4-6):221-32. doi:10.1159/000218169 PMID: 19471090.
26. DeFronzo RA, Tripathy D. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care. 2009; 32 Suppl 2:S157-63. doi:10.2337/dc09-S302 PMID: 19875544; PubMed Central PMCID: PMCPMC2811436.
27. 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. doi:10.1210/me.2007-0167 PMID: 17652184.
28. Shantikumar S, Caporali A, Emanueli C. Role of microRNAs in diabetes and its cardiovascular complications. Cardiovasc Res. 2012; 93(4):583-93. doi:10.1093/cvr/cvr300 PMID: 22065734; PubMed Central PMCID: PMC3291087.
29. Zhang J, Zhang F, Didelot X, Bruce KD, Cagampang FR, Vatish M, et al. Maternal high fat diet during pregnancy and lactation alters hepatic expression of insulin like growth factor-2 and key microRNAs in the adult offspring. BMC Genomics. 2009; 10:478. doi:10.1186/1471-2164-10-478 PMID: 19835573; PubMed Central PMCID: PMC2770530.
30. Griffiths-Jones S. miRBase: the microRNA sequence database. Methods Mol Biol. 2006; 342:129-38. doi:10.1385/1-59745-123-1:129 PMID: 16957372.
31. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011; 39(Database issue):D152-7. doi:10.1093/nar/gkq1027 PMID: 21037258; PubMed Central PMCID: PMC3013655.
32. Maziere P, Enright AJ. Prediction of microRNA targets. Drug Discov Today. 2007; 12(11-12):452-8. doi:10.1016/j.drudis.2007.04.002 PMID: 17532529.
33. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science. 2005; 307(5712):1098-101. doi:10.1126/science.1106148 PMID: 15718470.
34. Cartee GD, Wojtaszewski JF. Role of Akt substrate of 160 kDa in insulin-stimulated and contraction-stimulated glucose transport. Appl Physiol Nutr Metab. 2007; 32(3):557-66. doi:10.1139/H07-026 PMID: 17510697.
35. Henriksen EJ, Dokken BB. Role of glycogen synthase kinase-3 in insulin resistance and type 2 diabetes. Curr Drug Targets. 2006; 7(11):1435-41. PMID: 17100583.
36. Dokken BB, Henriksen EJ. Chronic selective glycogen synthase kinase-3 inhibition enhances glucose disposal and muscle insulin action in prediabetic obese Zucker rats. Am J Physiol Endocrinol Metab. 2006; 291(2):E207-13. doi:10.1152/ajpendo.00628.2005 PMID: 16478771.
37. Dokken BB, Sloniger JA, Henriksen EJ. Acute selective glycogen synthase kinase-3 inhibition enhances insulin signaling in prediabetic insulin-resistant rat skeletal muscle. Am J Physiol Endocrinol Metab. 2005; 288(6):E1188-94. doi:10.1152/ajpendo.00547.2004 PMID: 15671078.
38. Nikoulina SE, Ciaraldi TP, Mudaliar S, Mohideen P, Carter L, Henry RR. Potential role of glycogen synthase kinase-3 in skeletal muscle insulin resistance of type 2 diabetes. Diabetes. 2000; 49(2):263-71. PMID: 10868943.
39. Nicholas LM, Morrison JL, Rattanatray L, Ozanne SE, Kleemann DO, Walker SK, et al. Differential effects of exposure to maternal obesity or maternal weight loss during the periconceptional period in the sheep on insulin signalling molecules in skeletal muscle of the offspring at 4 months of age. PLoS One. 2013; 8(12):e84594. doi:10.1371/journal.pone.0084594 PMID: 24386400; PubMed Central PMCID: PMC3873457.
40. Rolo AP, Palmeira CM. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol Appl Pharmacol. 2006; 212(2):167-78. doi:10.1016/j.taap.2006.01.003 PMID: 16490224.
41. Gomes AP, Duarte FV, Nunes P, Hubbard BP, Teodoro JS, Varela AT, et al. Berberine protects against high fat diet-induced dysfunction in muscle mitochondria by inducing SIRT1-dependent mitochondrial biogenesis. Biochim Biophys Acta. 2012; 1822(2):185-95. doi:10.1016/j.bbadis.2011.10.008 PMID: 22027215; PubMed Central PMCID: PMC3366688.
42. Rolo AP, Gomes AP, Palmeira CM. Regulation of mitochondrial biogenesis in metabolic syndrome. Curr Drug Targets. 2011; 12(6):872-8. PMID: 21269264.
43. Duarte FV, Palmeira CM, Rolo AP. The Role of microRNAs in Mitochondria: Small Players Acting Wide. Genes (Basel). 2014; 5(4):865-86. doi:10.3390/genes5040865 PMID: 25264560; PubMed Central PMCID: PMC4276918.
44. Chen Y, Gelfond JA, McManus LM, Shireman PK. Reproducibility of quantitative RT-PCR array in miRNA expression profiling and comparison with microarray analysis. BMC Genomics. 2009; 10:407. doi:10.1186/1471-2164-10-407 PMID: 19715577; PubMed Central PMCID: PMC2753550.
45. Nelson PT, Wang WX, Wilfred BR, Tang G. Technical variables in high-throughput miRNA expression profiling: much work remains to be done. Biochim Biophys Acta. 2008; 1779(11):758-65. doi:10.1016/j.bbagrm.2008.03.012 PMID: 18439437; PubMed Central PMCID: PMC2660892.
46. Mao Y, Mohan R, Zhang S, Tang X. MicroRNAs as pharmacological targets in diabetes. Pharmacol Res. 2013; 75:37-47. doi:10.1016/j.phrs.2013.06.005 PMID: 23810798; PubMed Central PMCID: PMC3786207.
47. Karolina DS, Armugam A, Tavintharan S, Wong MT, Lim SC, Sum CF, 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(8):e22839. doi:10.1371/journal.pone.0022839 PMID: 21829658; PubMed Central PMCID: PMC3148231.
48. 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(1):61-9. doi:10.1007/s00592-010-0226-0 PMID: 20857148.
49. Pescador N, Perez-Barba M, Ibarra JM, Corbaton A, Martinez-Larrad MT, Serrano-Rios M. Serum circulating microRNA profiling for identification of potential type 2 diabetes and obesity biomarkers. PLoS One. 2013; 8(10):e77251. doi:10.1371/journal.pone.0077251 PMID: 24204780; PubMed Central PMCID: PMC3817315.
50. 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(6):810-7. doi:10.1161/CIRCRESAHA.110.226357 PMID: 20651284.
51. Zhao C, Dong J, Jiang T, Shi Z, Yu B, Zhu Y, et al. Early second-trimester serum miRNA profiling predicts gestational diabetes mellitus. PLoS One. 2011; 6(8):e23925. doi:10.1371/journal.pone.0023925 PMID: 21887347; PubMed Central PMCID: PMC3161072.
52. Li ZY, Na HM, Peng G, Pu J, Liu P. Alteration of microRNA expression correlates to fatty acid-mediated insulin resistance in mouse myoblasts. Mol Biosyst. 2011; 7(3):871-7. doi:10.1039/c0mb00230e PMID: 21183973.
53. van Rooij E, Sutherland LB, Liu N, Williams AH, McAnally J, Gerard RD, et al. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103(48):18255-60. doi:10.1073/pnas.0608791103 PMID: 17108080; PubMed Central PMCID: PMC1838739.
54. van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science. 2007; 316(5824):575-9. doi:10.1126/science.1139089 PMID: 17379774.