MicroRNA-494, upregulated by tumor necrosis factor-α, desensitizes insulin effect in C2C12 muscle cells

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Lee, Hyunjoo ^a   Jee, Yuna ^a   Hong, Kyungki ^a   Hwang, Gwi Seo ^a   Chun, Kwang Hoon ^a  

^a Gachon University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AKT SUBSTRATE OF 160; GLUCOSE TRANSPORTER 4; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; MICRORNA; MICRORNA 494; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN KINASE B; S6 KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; C2C12 CELL; CELL LINE; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; ENZYME PHOSPHORYLATION; GENE; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HORMONE ACTION; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN SIGNALING; MICROARRAY ANALYSIS; MOUSE; MUSCLE CELL; MYOBLAST; MYOTUBE; NONHUMAN; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SLC2A4 GENE; STXBP5 GENE; UPREGULATION;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; GLYCOGEN SYNTHASE KINASE 3; GTPASE-ACTIVATING PROTEINS; HUMANS; INSULIN; INSULIN RESISTANCE; MICE; MICRORNAS; MYOBLASTS; PTEN PHOSPHOHYDROLASE; RATS; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84892619023     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083471     Document Type: Article

References (80)

1. Van Gaal LF, Mertens IL, De Block CE (2006) Mechanisms linking obesity with cardiovascular disease. Nature 444: 875-880. doi:10.1038/nature05487. PubMed: 17167476.
2. Powell K (2007) Obesity: the two faces of fat. Nature 447: 525-527. doi: 10.1038/447525a. PubMed: 17538594.
3. Eckel RH, Grundy SM, Zimmet PZ (2005) The metabolic syndrome. Lancet 365: 1415-1428. doi:10.1016/S0140-6736(05)66378-7. PubMed: 15836891.
4. Taubes G (2009) Insulin resistance. Prosperity's plague. Science 325: 256-260. doi:10.1126/science.325-256. PubMed: 19608888.
5. Shulman GI (2000) Cellular mechanisms of insulin resistance. J Clin Invest 106: 171-176. doi:10.1172/JCI10583. PubMed: 10903330.
6. Hotamisligil GS, Shargill NS, Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87-91. doi:10.1126/science.7678183. PubMed: 7678183.
7. Bastard JP, Jardel C, Bruckert E, Blondy P, Capeau J et al. (2000) Elevated levels of interleukin 6 are reduced in serum and subcutaneous adipose tissue of obese women after weight loss. J Clin Endocrinol Metab 85: 3338-3342. doi:10.1210/jc.85.9.3338. PubMed: 10999830.
8. Fernandez-Real JM, Vayreda M, Richart C, Gutierrez C, Broch M et al. (2001) Circulating interleukin 6 levels, blood pressure, and insulin sensitivity in apparently healthy men and women. J Clin Endocrinol Metab 86: 1154-1159. doi:10.1210/jc.86.3.1154. PubMed: 11238501.
9. Takahashi K, Mizuarai S, Araki H, Mashiko S, Ishihara A et al. (2003) Adiposity elevates plasma MCP-1 levels leading to the increased CD11b-positive monocytes in mice. J Biol Chem 278: 46654-46660. doi:10.1074/jbc.M309895200. PubMed: 13129912.
10. Xu H, Barnes GT, Yang Q, Tan G, Yang D et al. (2003) Chronic inflammation in fat plays a crucial role in the development of obesityrelated insulin resistance. J Clin Invest 112: 1821-1830. doi:10.1172/JCI19451. PubMed: 14679177.
11. Rotter V, Nagaev I, Smith U (2003) Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. J Biol Chem 278: 45777-45784. doi:10.1074/jbc.M301977200. PubMed: 12952969.
12. Klover PJ, Zimmers TA, Koniaris LG, Mooney RA (2003) Chronic exposure to interleukin-6 causes hepatic insulin resistance in mice. Diabetes 52: 2784-2789. doi:10.2337/diabetes.52.11.2784. PubMed: 14578297.
13. Sell H, Dietze-Schroeder D, Kaiser U, Eckel J (2006) Monocyte chemotactic protein-1 is a potential player in the negative cross-talk between adipose tissue and skeletal muscle. Endocrinology 147: 2458-2467. doi:10.1210/en.2005- 0969. PubMed: 16439461.
14. Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T et al. (2006) Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 281: 26602-26614. doi:10.1074/jbc.M601284200. PubMed: 16809344.
15. Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G (2001) Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 280: E745-E751. PubMed: 11287357.
16. Maury E, Brichard SM (2010) Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol 314: 1-16. doi:10.1016/j.mce.2009.07.031. PubMed: 19682539.
17. Carswell EA, Old LJ, Kassel RL, Green S, Fiore N et al. (1975) An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci U S A 72: 3666-3670. doi:10.1073/pnas.72.9.3666. PubMed: 1103152.
18. Katsuki A, Sumida Y, Murashima S, Murata K, Takarada Y et al. (1998) Serum levels of tumor necrosis factor-alpha are increased in obese patients with noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 83: 859-862. doi:10.1210/jc.83.3.859. PubMed: 9506740.
19. Saghizadeh M, Ong JM, Garvey WT, Henry RR, Kern PA (1996) The expression of TNF alpha by human muscle. Relationship to insulin resistance. J Clin Invest 97: 1111-1116. doi:10.1172/JCI118504. PubMed: 8613535.
20. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM (1995) Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J Clin Invest 95: 2409-2415. doi: 10.1172/JCI117936. PubMed: 7738205.
21. Hofmann C, Lorenz K, Braithwaite SS, Colca JR, Palazuk BJ et al. (1994) Altered gene expression for tumor necrosis factor-alpha and its receptors during drug and dietary modulation of insulin resistance. Endocrinology 134: 264-270. doi:10.1210/en.134.1.264. PubMed: 8275942.
22. Lowell BB, S-Susulic V, Hamann A, Lawitts JA, Himms-Hagen J et al. (1993) Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature 366: 740-742. doi:10.1038/366740a0. PubMed: 8264795.
23. de Alvaro C, Teruel T, Hernandez R, Lorenzo M (2004) Tumor necrosis factor alpha produces insulin resistance in skeletal muscle by activation of inhibitor kappaB kinase in a p38 MAPK-dependent manner. J Biol Chem 279: 17070-17078. doi:10.1074/jbc.M312021200. PubMed: 14764603.
24. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS (1997) Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 389: 610-614. doi:10.1038/39335. PubMed: 9335502.
25. Uysal KT, Wiesbrock SM, Hotamisligil GS (1998) Functional analysis of tumor necrosis factor (TNF) receptors in TNF-alpha-mediated insulin resistance in genetic obesity. Endocrinology 139: 4832-4838. doi: 10.1210/en.139.12.4832. PubMed: 9832419.
26. Ventre J, Doebber T, Wu M, MacNaul K, Stevens K et al. (1997) Targeted disruption of the tumor necrosis factor-alpha gene: metabolic consequences in obese and nonobese mice. Diabetes 46: 1526-1531. doi:10.2337/diabetes.46.9.1526. PubMed: 9287059.
27. Yuan M, Konstantopoulos N, Lee J, Hansen L, Li ZW et al. (2001) Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science 293: 1673-1677. doi:10.1126/ science.1061620. PubMed: 11533494.
28. Gao Z, Hwang D, Bataille F, Lefevre M, York D et al. (2002) Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J Biol Chem 277: 48115-48121. doi:10.1074/jbc.M209459200. PubMed: 12351658.
29. Hirosumi J, Tuncman G, Chang L, Görgün CZ, Uysal KT et al. (2002) A central role for JNK in obesity and insulin resistance. Nature 420: 333-336. doi:10.1038/nature01137. PubMed: 12447443.
30. Aguirre V, Uchida T, Yenush L, Davis R, White MF (2000) The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J Biol Chem 275: 9047-9054
31. Engelman JA, Berg AH, Lewis RY, Lisanti MP, Scherer PE (2000) Tumor necrosis factor alpha-mediated insulin resistance, but not dedifferentiation, is abrogated by MEK1/2 inhibitors in 3T3-L1 adipocytes. Mol Endocrinol 14: 1557-1569. doi:10.1210/me.14.10.1557. PubMed: 11043572.
32. Ozes ON, Akca H, Mayo LD, Gustin JA, Maehama T et al. (2001) A phosphatidylinositol 3-kinase/Akt/mTOR pathway mediates and PTEN antagonizes tumor necrosis factor inhibition of insulin signaling through insulin receptor substrate-1. Proc Natl Acad Sci U S A 98: 4640-4645. doi:10.1073/pnas.051042298. PubMed: 11287630.
33. Stephens JM, Pekala PH (1991) Transcriptional repression of the GLUT4 and C/EBP genes in 3T3-L1 adipocytes by tumor necrosis factor-alpha. J Biol Chem 266: 21839-21845. PubMed: 1939208.
34. Emanuelli B, Peraldi P, Filloux C, Chavey C, Freidinger K et al. (2001) SOCS-3 inhibits insulin signaling and is up-regulated in response to tumor necrosis factor-alpha in the adipose tissue of obese mice. J Biol Chem 276: 47944-47949. PubMed: 11604392.
35. Rui L, Yuan M, Frantz D, Shoelson S, White MF (2002) SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J Biol Chem 277: 42394-42398. doi:10.1074/jbc.C200444200. PubMed: 12228220.
36. Emanuelli B, Peraldi P, Filloux C, Sawka-Verhelle D, Hilton D et al. (2000) SOCS-3 is an insulin-induced negative regulator of insulin signaling. J Biol Chem 275: 15985-15991. doi:10.1074/jbc.275.21.15985. PubMed: 10821852.
37. Feingold KR, Doerrler W, Dinarello CA, Fiers W, Grunfeld C (1992) Stimulation of lipolysis in cultured fat cells by tumor necrosis factor, interleukin-1, and the interferons is blocked by inhibition of prostaglandin synthesis. Endocrinology 130: 10-16. doi:10.1210/en.130.1.10. PubMed: 1370149.
38. Guilherme A, Virbasius JV, Puri V, Czech MP (2008) Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 9: 367-377. doi:10.1038/nrm2391. PubMed: 18401346.
39. Pape ME, Kim KH (1988) Effect of tumor necrosis factor on acetylcoenzyme A carboxylase gene expression and preadipocyte differentiation. Mol Endocrinol 2: 395-403. doi:10.1210/mend-2-5-395. PubMed: 2901666.
40. Ruan H, Pownall HJ, Lodish HF (2003) Troglitazone antagonizes tumor necrosis factor-alpha-induced reprogramming of adipocyte gene expression by inhibiting the transcriptional regulatory functions of NF-kappaB. J Biol Chem 278: 28181-28192. doi:10.1074/jbc.M303141200. PubMed: 12732648.
41. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297. doi:10.1016/S0092-8674(04)00045-5. PubMed: 14744438.
42. Wu L, Fan J, Belasco JG (2006) MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci U S A 103: 4034-4039. doi:10.1073/pnas.0510928103. PubMed: 16495412.
43. Humphreys DT, Westman BJ, Martin DI, Preiss T (2005) MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc Natl Acad Sci U S A 102: 16961-16966. doi:10.1073/pnas.0506482102. PubMed: 16287976.
44. Mathonnet G, Fabian MR, Svitkin YV, Parsyan A, Huck L et al. (2007) MicroRNA inhibition of translation initiation in vitro by targeting the capbinding complex eIF4F. Science 317: 1764-1767. doi:10.1126/science.1146067. PubMed: 17656684.
45. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9: 102-114. PubMed: 18197166.
46. Winter J, Jung S, Keller S, Gregory RI, Diederichs S (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11: 228-234. doi:10.1038/ncb0309-228. PubMed: 19255566.
47. Trajkovski M, Hausser J, Soutschek J, Bhat B, Akin A et al. (2011) MicroRNAs 103 and 107 regulate insulin sensitivity. Nature 474: 649-653. doi:10.1038/nature10112. PubMed: 21654750.
48. Kornfeld JW, Baitzel C, Könner AC, Nicholls HT, Vogt MC et al. (2013) Obesity-induced overexpression of miR-802 impairs glucose metabolism through silencing of Hnf1b. Nature 494: 111-115. doi: 10.1038/nature11793. PubMed: 23389544.
49. Li G, Barrett EJ, Barrett MO, Cao W, Liu Z (2007) Tumor necrosis factor-alpha induces insulin resistance in endothelial cells via a p38 mitogen-activated protein kinase-dependent pathway. Endocrinology 148: 3356-3363. doi:10.1210/en.2006-1441. PubMed: 17446186.
50. Bouzakri K, Zierath JR (2007) MAP4K4 gene silencing in human skeletal muscle prevents tumor necrosis factor-alpha-induced insulin resistance. J Biol Chem 282: 7783-7789. doi:10.1074/jbc.M608602200. PubMed: 17227768.
51. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444: 860-867. doi:10.1038/nature05485. PubMed: 17167474.
52. Lorenzo M, Fernández-Veledo S, Vila-Bedmar R, Garcia-Guerra L, De Alvaro C et al. (2008) Insulin resistance induced by tumor necrosis factor-alpha in myocytes and brown adipocytes. J Anim Sci 86: E94-104. PubMed: 17940160.
53. Liu L, Jiang Y, Zhang H, Greenlee AR, Han Z (2010) Overexpressed miR-494 down-regulates PTEN gene expression in cells transformed by anti-benzo(a)pyrene- trans-7,8-dihydrodiol-9,10-epoxide. Life Sci 86: 192-198. doi:10.1016/j.lfs. 2009.12.002. PubMed: 20006626.
54. Liu Y, Malaviarachchi P, Beggs M, Emanuel PD (2010) PTEN transcript variants caused by illegitimate splicing in "aged" blood samples and EBV-transformed cell lines. Hum Genet 128: 609-614. doi:10.1007/s00439-010-0886- 4. PubMed: 20839010.
55. Wang X, Zhang X, Ren XP, Chen J, Liu H et al. (2010) MicroRNA-494 targeting both proapoptotic and antiapoptotic proteins protects against ischemia/reperfusion-induced cardiac injury. Circulation 122: 1308-1318. doi:10.1161/CIRCULATIONAHA.110.964684. PubMed: 20837890.
56. Romano G, Acunzo M, Garofalo M, Di Leva G, Cascione L et al. (2012) MiR-494 is regulated by ERK1/2 and modulates TRAIL-induced apoptosis in non-small-cell lung cancer through BIM down-regulation. Proc Natl Acad Sci U S A 109: 16570-16575. doi:10.1073/pnas.1207917109. PubMed: 23012423.
57. Yamamoto H, Morino K, Nishio Y, Ugi S, Yoshizaki T et al. (2012) MicroRNA-494 regulates mitochondrial biogenesis in skeletal muscle through mitochondrial transcription factor A and Forkhead box j3. Am J Physiol Endocrinol Metab 303: E1419-E1427. doi:10.1152/ajpendo.00097.2012. PubMed: 23047984.
58. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115: 787-798. doi: 10.1016/S0092-8674(03)01018-3. PubMed: 14697198.
59. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39: 1278-1284. doi:10.1038/ng2135. PubMed: 17893677.
60. Widberg CH, Bryant NJ, Girotti M, Rea S, James DE (2003) Tomosyn interacts with the t-SNAREs syntaxin4 and SNAP23 and plays a role in insulin-stimulated GLUT4 translocation. J Biol Chem 278: 35093-35101. doi:10.1074/jbc.M304261200. PubMed: 12832401.
61. Denley A, Carroll JM, Brierley GV, Cosgrove L, Wallace J et al. (2007) Differential activation of insulin receptor substrates 1 and 2 by insulinlike growth factor-activated insulin receptors. Mol Cell Biol 27: 3569-3577. doi:10.1128/MCB.01447-06. PubMed: 17325037.
62. Davey JR, Humphrey SJ, Junutula JR, Mishra AK, Lambright DG et al. (2012) TBC1D13 is a RAB35 specific GAP that plays an important role in GLUT4 trafficking in adipocytes. Traffic 13: 1429-1441. doi:10.1111/j.1600-0854.2012. 01397.x. PubMed: 22762500.
63. Ravichandran LV, Chen H, Li Y, Quon MJ (2001) Phosphorylation of PTP1B at Ser(50) by Akt impairs its ability to dephosphorylate the insulin receptor. Mol Endocrinol 15: 1768-1780. doi:10.1210/me.15.10.1768. PubMed: 11579209.
64. Horng T, Hotamisligil GS (2011) Linking the inflammasome to obesity-related disease. Nat Med 17: 164-165. doi:10.1038/nm0211-164. PubMed: 21297609.
65. Cheung AT, Ree D, Kolls JK, Fuselier J, Coy DH et al. (1998) An in vivo model for elucidation of the mechanism of tumor necrosis factor-alpha (TNF-alpha)-induced insulin resistance: evidence for differential regulation of insulin signaling by TNF-alpha. Endocrinology 139: 4928-4935. doi:10.1210/en.139.12.4928. PubMed: 9832430.
66. Defronzo RA (2009) Banting Lecture. From the triumvirate to the ominous octet: a new paradigm for the treatment of type 2 diabetes mellitus. Diabetes 58: 773-795. doi:10.2337/db09-9028. PubMed: 19336687.
67. Pendergrass M, Bertoldo A, Bonadonna R, Nucci G, Mandarino L et al. (2007) Muscle glucose transport and phosphorylation in type 2 diabetic, obese nondiabetic, and genetically predisposed individuals. Am J Physiol Endocrinol Metab 292: E92-100. PubMed: 16896161.
68. Rodin J, Wack J, Ferrannini E, DeFronzo RA (1985) Effect of insulin and glucose on feeding behavior. Metabolism 34: 826-831. doi: 10.1016/0026-0495(85) 90106-4. PubMed: 3897769.
69. He A, Zhu L, Gupta N, Chang Y, Fang F (2007) Overexpression of micro ribonucleic acid 29, highly up-regulated in diabetic rats, leads to insulin resistance in 3T3-L1 adipocytes. Mol Endocrinol 21: 2785-2794. doi:10.1210/me.2007-0167. PubMed: 17652184.
70. Horie T, Ono K, Nishi H, Iwanaga Y, Nagao K et al. (2009) MicroRNA-133 regulates the expression of GLUT4 by targeting KLF15 and is involved in metabolic control in cardiac myocytes. Biochem Biophys Res Commun 389: 315-320. doi:10.1016/j.bbrc.2009.08.136. PubMed: 19720047.
71. Ling HY, Ou HS, Feng SD, Zhang XY, Tuo QH et al. (2009) CHANGES IN microRNA (miR) profile and effects of miR-320 in insulin-resistant 3T3-L1 adipocytes. Clin Exp Pharmacol Physiol 36: e32-e39. doi: 10.1111/j.1440-1681. 2009.05207.x. PubMed: 19473196.
72. Zhao E, Keller MP, Rabaglia ME, Oler AT, Stapleton DS et al. (2009) Obesity and genetics regulate microRNAs in islets, liver, and adipose of diabetic mice. Mamm Genome 20: 476-485. doi:10.1007/s00335-009-9217-2. PubMed: 19727952.
73. Lu H, Buchan RJ, Cook SA (2010) MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovasc Res 86: 410-420. doi:10.1093/cvr/cvq010. PubMed: 20080987.
74. Lim L, Balakrishnan A, Huskey N, Jones KD, Jodari M et al. (2013) MiR-494 within an oncogenic MicroRNA megacluster regulates G1/S transition in liver tumorigenesis through suppression of MCC. Hepatology.
75. Liu Y, Lai L, Chen Q, Song Y, Xu S et al. (2012) MicroRNA-494 is required for the accumulation and functions of tumor-expanded myeloid-derived suppressor cells via targeting of PTEN. J Immunol 188: 5500-5510. doi:10.4049/jimmunol. 1103505. PubMed: 22544933.
76. Ohdaira H, Sekiguchi M, Miyata K, Yoshida K (2012) MicroRNA-494 suppresses cell proliferation and induces senescence in A549 lung cancer cells. Cell Prolif 45: 32-38. doi:10.1111/j.1365-2184.2011.00798.x. PubMed: 22151897.
77. Faraonio R, Salerno P, Passaro F, Sedia C, Iaccio A et al. (2012) A set of miRNAs participates in the cellular senescence program in human diploid fibroblasts. Cell Death Differ 19: 713-721. doi:10.1038/cdd.2011.143. PubMed: 22052189.
78. Kim WK, Park M, Kim YK, Tae YK, Yang HK et al. (2011) MicroRNA-494 downregulates KIT and inhibits gastrointestinal stromal tumor cell proliferation. Clin Cancer Res 17: 7584-7594. doi: 10.1158/1078-0432.CCR-11- 0166. PubMed: 22042971.
79. Greco S, De Simone M, Colussi C, Zaccagnini G, Fasanaro P et al. (2009) Common micro-RNA signature in skeletal muscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia. FASEB J 23: 3335-3346. doi:10.1096/fj.08-128579. PubMed: 19528256.
80. Olaru AV, Ghiaur G, Yamanaka S, Luvsanjav D, An F et al. (2011) MicroRNA down-regulated in human cholangiocarcinoma control cell cycle through multiple targets involved in the G1/S checkpoint. Hepatology 54: 2089-2098. doi:10.1002/hep.24591. PubMed: 21809359.