microManaging glucose and lipid metabolism in skeletal muscle: Role of microRNAs

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1861, Issue 12, 2016, Pages 2130-2138

  Massart, Julie ^a   Katayama, Mutsumi ^a   Krook, Anna ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Exercise; Metabolism; microRNA; Skeletal muscle; Type 2 diabetes

Indexed keywords

FATTY ACID; GLUCOSE; LIPID; MICRORNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; TRANSCRIPTION FACTOR;

ARTICLE; BIOGENESIS; EXERCISE; GENE EXPRESSION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC REGULATION; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HUMAN; INSULIN RESISTANCE; LIPID METABOLISM; METABOLIC DISORDER; MITOCHONDRION; MOLECULAR BIOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; ANIMAL; METABOLISM; PHYSIOLOGY;

ANIMALS; GLUCOSE; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; MICRORNAS; MITOCHONDRIA; MUSCLE, SKELETAL;

EID: 84969730199     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2016.05.006     Document Type: Article

References (81)

1. [1] DeFronzo, R.A., Tripathy, D., Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32:Suppl. 2 (2009), S157–S163, 10.2337/dc09-S302.
2. [2] Samuel, V.T., Shulman, G.I., Mechanisms for insulin resistance: common threads and missing links. Cell 148:5 (2012), 852–871, 10.1016/j.cell.2012.02.017.
3. [3] Mootha, V.K., Lindgren, C.M., Eriksson, K.F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstrale, M., Laurila, E., Houstis, N., Daly, M.J., Patterson, N., Mesirov, J.P., Golub, T.R., Tamayo, P., Spiegelman, B., Lander, E.S., Hirschhorn, J.N., Altshuler, D., Groop, L.C., PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34:3 (2003), 267–273, 10.1038/ng1180.
4. [4] Kovanda, A., Režen, T., Rogelj, B., MicroRNA in skeletal muscle development, growth, atrophy, and disease. Wiley Interdiscip. Rev. RNA 5:4 (2014), 509–525, 10.1002/wrna.1227.
5. [5] Londin, E., Loher, P., Telonis, A.G., Quann, K., Clark, P., Jing, Y., Hatzimichael, E., Kirino, Y., Honda, S., Lally, M., Ramratnam, B., Comstock, C.E.S., Knudsen, K.E., Gomella, L., Spaeth, G.L., Hark, L., Katz, L.J., Witkiewicz, A., Rostami, A., Jimenez, S.A., Hollingsworth, M.A., Yeh, J.J., Shaw, C.A., McKenzie, S.E., Nelson, P.T., Zupo, S., Van Roosbroeck, K., Keating, M.J., Calin, G.A., Yeo, C., Jimbo, M., Cozzitorto, J., Brody, J.R., Delgrosso, K., Mattick, J.S., Fortina, P., Rigoutsos, I., Analysis of 13 cell types reveals evidence for the expression of numerous novel primate- and tissue-specific microRNAs. Proc. Natl. Acad. Sci. U. S. A. 112:10 (2015), E1106–E1115, 10.1073/pnas.1420955112.
6. [6] Lewis, B.P., Shih, I.H., Jones-Rhoades, M.W., Bartel, D.P., Burge, C.B., Prediction of mammalian microRNA targets. Cell 115:7 (2003), 787–798, 10.1016/s0092-8674(03)01018-3.
7. [7] Pasquinelli, A.E., MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat. Rev. Genet. 13:4 (2012), 271–282, 10.1038/nrg3162.
8. [8] Bartel, D.P., MicroRNAs: target recognition and regulatory functions. Cell 136:2 (2009), 215–233, 10.1016/j.cell.2009.01.002.
9. [9] Vasudevan, S., Tong, Y., Steitz, J.A., Switching from repression to activation: microRNAs can up-regulate translation. Science 318:5858 (2007), 1931–1934, 10.1126/science.1149460.
10. [10] Orom, U.A., Nielsen, F.C., Lund, A.H., MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell 30:4 (2008), 460–471, 10.1016/j.molcel.2008.05.001.
11. [11] Ha, M., Kim, V.N., Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15:8 (2014), 509–524, 10.1038/nrm3838.
12. [12] Gallagher, I.J., Scheele, C., Keller, P., Nielsen, A.R., Remenyi, J., Fischer, C.P., Roder, K., Babraj, J., Wahlestedt, C., Hutvagner, G., Pedersen, B.K., Timmons, J.A., Integration of microRNA changes in vivo identifies novel molecular features of muscle insulin resistance in type 2 diabetes. Genome Med. 2:2 (2010), 1–18, 10.1186/gm130.
13. [13] Bork-Jensen, J., Scheele, C., Christophersen, D.V., Nilsson, E., Friedrichsen, M., Fernandez-Twinn, D.S., Grunnet, L.G., Litman, T., Holmstrøm, K., Vind, B., Højlund, K., Beck-Nielsen, H., Wojtaszewski, J., Ozanne, S.E., Pedersen, B.K., Poulsen, P., Vaag, A., Glucose tolerance is associated with differential expression of microRNAs in skeletal muscle: results from studies of twins with and without type 2 diabetes. Diabetologia 58:2 (2014), 363–373, 10.1007/s00125-014-3434-2.
14. [14] 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. 21:11 (2007), 2785–2794, 10.1210/me.2007-0167.
15. [15] Huang, B., Qin, W., Zhao, B., Shi, Y., Yao, C., Li, J., Xiao, H., Jin, Y., MicroRNA expression profiling in diabetic GK rat model. Acta Biochim. Biophys. Sin. Shanghai 41:6 (2009), 472–477, 10.1093/abbs/gmp035.
16. [16] Herrera, B.M., Lockstone, H.E., Taylor, J.M., Ria, M., Barrett, A., Collins, S., Kaisaki, P., Argoud, K., Fernandez, C., Travers, M.E., Grew, J.P., Randall, J.C., Gloyn, A.L., Gauguier, D., McCarthy, M.I., Lindgren, C.M., Global microRNA expression profiles in insulin target tissues in a spontaneous rat model of type 2 diabetes. Diabetologia 53:6 (2010), 1099–1109, 10.1007/s00125-010-1667-2.
17. [17] Karolina, D.S., Armugam, A., Tavintharan, S., Wong, M.T., Lim, S.C., Sum, C.F., Jeyaseelan, K., MicroRNA 144 impairs insulin signaling by inhibiting the expression of insulin receptor substrate 1 in type 2 diabetes mellitus. PLoS One, 6(8), 2011, e22839, 10.1371/journal.pone.0022839.
18. [18] Chen, G.Q., Lian, W.J., Wang, G.M., Wang, S., Yang, Y.Q., Zhao, Z.W., Altered microRNA expression in skeletal muscle results from high-fat diet-induced insulin resistance in mice. Mol. Med. Rep. 5:5 (2012), 1362–1368, 10.3892/mmr.2012.824.
19. [19] Mohamed, J.S., Hajira, A., Pardo, P.S., Boriek, A.M., MicroRNA-149 inhibits PARP-2 and promotes mitochondrial biogenesis via SIRT-1/PGC-1α network in skeletal muscle. Diabetes 63:5 (2014), 1546–1559, 10.2337/db13-1364.
20. [20] Kho, A.T., Kang, P.B., Kohane, I.S., Kunkel, L.M., Transcriptome-scale similarities between mouse and human skeletal muscles with normal and myopathic phenotypes. BMC Musculoskelet. Disord., 7, 2006, 23-23, 10.1186/1471-2474-7-23.
21. [21] Williams, A.H., Liu, N., van Rooij, E., Olson, E.N., MicroRNA control of muscle development and disease. Curr. Opin. Cell Biol. 21:3 (2009), 461–469, 10.1016/j.ceb.2009.01.029.
22. [22] Chen, J.-F., Mandel, E.M., Thomson, J.M., Wu, Q., Callis, T.E., Hammond, S.M., Conlon, F.L., Wang, D.-Z., The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38:2 (2006), 228–233, 10.1038/ng1725.
23. [23] Chen, J.-F., Tao, Y., Li, J., Deng, Z., Yan, Z., Xiao, X., Wang, D.-Z., microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J. Cell Biol. 190:5 (2010), 867–879, 10.1083/jcb.200911036.
24. [24] Granjon, A., Gustin, M.P., Rieusset, J., Lefai, E., Meugnier, E., Guller, I., Cerutti, C., Paultre, C., Disse, E., Rabasa-Lhoret, R., Laville, M., Vidal, H., Rome, S., 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 58:11 (2009), 2555–2564, 10.2337/db09-0165.
25. [25] Rezen, T., Kovanda, A., Eiken, O., Mekjavic, I.B., Rogelj, B., Expression changes in human skeletal muscle miRNAs following 10 days of bed rest in young healthy males. Acta Physiol (Oxford) 210:3 (2014), 655–666, 10.1111/apha.12228.
26. [26] McCarthy, J.J., Esser, K.A., MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J. Appl. Physiol. 102:1 (2007), 306–313, 10.1152/japplphysiol.00932.2006.
27. [27] Fan, J.Y., Yang, Y., Xie, J.Y., Lu, Y.L., Shi, K., Huang, Y.Q., MicroRNA-144 mediates metabolic shift in ovarian cancer cells by directly targeting Glut1. Tumour Biol., 2015, 10.1007/s13277-015-4558-9.
28. [28] Motohashi, N., Alexander, M.S., Shimizu-Motohashi, Y., Myers, J.A., Kawahara, G., Kunkel, L.M., Regulation of IRS1/Akt insulin signaling by microRNA-128a during myogenesis. J. Cell Sci. 126:Pt 12 (2013), 2678–2691, 10.1242/jcs.119966.
29. [29] Yang, W.M., Jeong, H.J., Park, S.W., Lee, W., Obesity-induced miR-15b is linked causally to the development of insulin resistance through the repression of the insulin receptor in hepatocytes. Mol. Nutr. Food Res. 59:11 (2015), 2303–2314, 10.1002/mnfr.201500107.
30. [30] Lu, H., Buchan, R.J., Cook, S.A., MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovasc. Res. 86:3 (2010), 410–420, 10.1093/cvr/cvq010.
31. [31] Chuang, T.-Y., Wu, H.-L., Chen, C.-C., Gamboa, G.M., Layman, L.C., Diamond, M.P., Azziz, R., Chen, Y.-H., MicroRNA-223 expression is upregulated in insulin resistant human adipose tissue. J. Diabetes Res., 2015, 2015, 8, 10.1155/2015/943659.
32. [32] Zhang, J., Zhang, L., Fan, R., Guo, N., Xiong, C., Wang, L., Jin, S., Li, W., Lu, J., The polymorphism in the let-7 targeted region of the Lin28 gene is associated with increased risk of type 2 diabetes mellitus. Mol. Cell. Endocrinol. 375:1–2 (2013), 53–57, 10.1016/j.mce.2013.04.022.
33. [33] Frost, R.J.A., Olson, E.N., Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs. Proc. Natl. Acad. Sci. 108:52 (2011), 21075–21080, 10.1073/pnas.1118922109.
34. [34] Zhu, H., Shyh-Chang, N., Segre, A.V., Shinoda, G., Shah, S.P., Einhorn, W.S., Takeuchi, A., Engreitz, J.M., Hagan, J.P., Kharas, M.G., Urbach, A., Thornton, J.E., Triboulet, R., Gregory, R.I., Altshuler, D., Daley, G.Q., The Lin28/let-7 axis regulates glucose metabolism. Cell 147:1 (2011), 81–94, 10.1016/j.cell.2011.08.033.
35. [35] Jiang, L.Q., Franck, N., Egan, B., Sjögren, R.J.O., Katayama, M., Duque-Guimaraes, D., Arner, P., Zierath, J.R., Krook, A., Autocrine role of interleukin-13 on skeletal muscle glucose metabolism in type 2 diabetic patients involves microRNA let-7. Am. J. Physiol. Endocrinol. Metab. 305:11 (2013), E1359–E1366, 10.1152/ajpendo.00236.2013.
36. [36] Kallen, A.N., Zhou, X.-B., Xu, J., Qiao, C., Ma, J., Yan, L., Lu, L., Liu, C., Yi, J.-S., Zhang, H., Min, W., Bennett, A.M., Gregory, R.I., Ding, Y., Huang, Y., The imprinted H19 LncRNA antagonizes Let-7 MicroRNAs. Mol. Cell 52:1 (2013), 101–112, 10.1016/j.molcel.2013.08.027.
37. [37] Gao, Y., Wu, F., Zhou, J., Yan, L., Jurczak, M.J., Lee, H.-Y., Yang, L., Mueller, M., Zhou, X.-B., Dandolo, L., Szendroedi, J., Roden, M., Flannery, C., Taylor, H., Carmichael, G.G., Shulman, G.I., Huang, Y., The H19/let-7 double-negative feedback loop contributes to glucose metabolism in muscle cells. Nucleic Acids Res. 42:22 (2014), 13799–13811, 10.1093/nar/gku1160.
38. [38] Fang, R., Xiao, T., Fang, Z., Sun, Y., Li, F., Gao, Y., Feng, Y., Li, L., Wang, Y., Liu, X., Chen, H., Liu, X.Y., Ji, H., MicroRNA-143 (miR-143) regulates cancer glycolysis via targeting hexokinase 2 gene. J. Biol. Chem. 287:27 (2012), 23227–23235, 10.1074/jbc.M112.373084.
39. [39] Glass, C.K., Olefsky, J.M., Inflammation and lipid signaling in the etiology of insulin resistance. Cell Metab. 15:5 (2012), 635–645, 10.1016/j.cmet.2012.04.001.
40. [40] Lee, H., Jee, Y., Hong, K., Hwang, G.S., Chun, K.H., MicroRNA-494, upregulated by tumor necrosis factor-alpha, desensitizes insulin effect in C2C12 muscle cells. PLoS One, 8(12), 2013, e83471, 10.1371/journal.pone.0083471.
41. [41] Katayama, M., Sjögren Rasmus, J.O., Egan, B., Krook, A., miRNA let-7 expression is regulated by glucose and TNF-α by a remote upstream promoter. Biochem. J. 472:2 (2015), 147–156, 10.1042/bj20150224.
42. [42] Nielsen, S., Scheele, C., Yfanti, C., Åkerström, T., Nielsen, A.R., Pedersen, B.K., Laye, M., Muscle specific microRNAs are regulated by endurance exercise in human skeletal muscle. Am. J. Phys. 588:Pt 20 (2010), 4029–4037, 10.1113/jphysiol.2010.189860.
43. [43] Rome, S., Clément, K., Rabasa-Lhoret, R., Loizon, E., Poitou, C., Barsh, G.S., Riou, J.-P., Laville, M., Vidal, H., Microarray profiling of human skeletal muscle reveals that insulin regulates ∼ 800 genes during a hyperinsulinemic clamp. J. Biol. Chem. 278:20 (2003), 18063–18068, 10.1074/jbc.M300293200.
44. [44] Meugnier, E., Faraj, M., Rome, S., Beauregard, G., Michaut, A., Pelloux, V., Chiasson, J.-L., Laville, M., Clement, K., Vidal, H., Rabasa-Lhoret, R., Acute hyperglycemia induces a global downregulation of gene expression in adipose tissue and skeletal muscle of healthy subjects. Diabetes 56:4 (2007), 992–999, 10.2337/db06-1242.
45. [45] Colberg, S.R., Sigal, R.J., Fernhall, B., Regensteiner, J.G., Blissmer, B.J., Rubin, R.R., Chasan-Taber, L., Albright, A.L., Braun, B., Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement. Diabetes Care 33:12 (2010), e147–e167, 10.2337/dc10-9990.
46. [46] Egan, B., Zierath, J.R., Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 17:2 (2013), 162–184, 10.1016/j.cmet.2012.12.012.
47. [47] Drummond, M.J., McCarthy, J.J., Fry, C.S., Esser, K.A., Rasmussen, B.B., Aging differentially affects human skeletal muscle microRNA expression at rest and after an anabolic stimulus of resistance exercise and essential amino acids. Am. J. Physiol. Endocrinol. Metab. 295:6 (2008), E1333–E1340, 10.1152/ajpendo.90562.2008.
48. [48] Keller, P., Vollaard, N.B., Gustafsson, T., Gallagher, I.J., Sundberg, C.J., Rankinen, T., Britton, S.L., Bouchard, C., Koch, L.G., Timmons, J.A., A transcriptional map of the impact of endurance exercise training on skeletal muscle phenotype. J. Appl. Physiol. 110:1 (2011), 46–59, 10.1152/japplphysiol.00634.2010 (1985).
49. [49] Safdar, A., Abadi, A., Akhtar, M., Hettinga, B.P., Tarnopolsky, M.A., miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6J male mice. PLoS One, 4(5), 2009, e5610, 10.1371/journal.pone.0005610.
50. [50] Aoi, W., Naito, Y., Mizushima, K., Takanami, Y., Kawai, Y., Ichikawa, H., Yoshikawa, T., The microRNA miR-696 regulates PGC-1α in mouse skeletal muscle in response to physical activity. Am. J. Physiol. Endocrinol. Metab. 298:4 (2010), E799–E806, 10.1152/ajpendo.00448.2009.
51. [51] Rowlands, D.S., Page, R.A., Sukala, W.R., Giri, M., Ghimbovschi, S.D., Hayat, I., Cheema, B.S., Lys, I., Leikis, M., Sheard, P.W., Wakefield, S.J., Breier, B., Hathout, Y., Brown, K., Marathi, R., Orkunoglu-Suer, F.E., Devaney, J.M., Leiken, B., Many, G., Krebs, J., Hopkins, W.G., Hoffman, E.P., Multi-omic integrated networks connect DNA methylation and miRNA with skeletal muscle plasticity to chronic exercise in Type 2 diabetic obesity. Physiol. Genomics 46:20 (2014), 747–765, 10.1152/physiolgenomics.00024.2014.
52. [52] Correia, J.C., Ferreira, D.M., Ruas, J.L., Intercellular: local and systemic actions of skeletal muscle PGC-1 s. Trends Endocrinol. Metab. 26:6 (2015), 305–314, 10.1016/j.tem.2015.03.010.
53. [53] Egan, B., O'Connor, P.L., Zierath, J.R., O'Gorman, D.J., Time course analysis reveals gene-specific transcript and protein kinetics of adaptation to short-term aerobic exercise training in human skeletal muscle. PLoS One, 8(9), 2013, e74098, 10.1371/journal.pone.0074098.
54. [54] Russell, A.P., Lamon, S., Boon, H., Wada, S., Güller, I., E.L., B., Chibalin, A.V., Zierath, J.R., Snow, R.J., Stepto, N., Wadley, G.D., Akimoto, T., Regulation of miRNAs in human skeletal muscle following acute endurance exercise and short-term endurance training. J. Physiol. 591:18 (2013), 4637–4653, 10.1113/jphysiol.2013.255695.
55. [55] Russell, A.P., Wada, S., Vergani, L., Hock, M.B., Lamon, S., Léger, B., Ushida, T., Cartoni, R., Wadley, G.D., Hespel, P., Kralli, A., Soraru, G., Angelini, C., Akimoto, T., Disruption of skeletal muscle mitochondrial network genes and miRNAs in amyotrophic lateral sclerosis. Neurobiol. Dis. 49:1 (2013), 107–117, 10.1016/j.nbd.2012.08.015.
56. [56] Ramachandran, D., Roy, U., Garg, S., Ghosh, S., Pathak, S., Kolthur-Seetharam, U., Sirt1 and mir-9 expression is regulated during glucose-stimulated insulin secretion in pancreatic beta-islets. FEBS J. 278:7 (2011), 1167–1174, 10.1111/j.1742-4658.2011.08042.x.
57. [57] Xu, Y., Zhao, C., Sun, X., Liu, Z., Zhang, J., MicroRNA-761 regulates mitochondrial biogenesis in mouse skeletal muscle in response to exercise. Biochem. Biophys. Res. Commun. 467:1 (2015), 103–108, 10.1016/j.bbrc.2015.09.113.
58. [58] Ringholm, S., Biensø, R.S., Kiilerich, K., Guadalupe-Grau, A., Aachmann-Andersen, N.J., Saltin, B., Plomgaard, P., Lundby, C., Wojtaszewski, J.F.P., Calbet, J.A., Pilegaard, H., Bed rest reduces metabolic protein content and abolishes exercise-induced mRNA responses in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 301:4 (2011), E649–E658, 10.1152/ajpendo.00230.2011.
59. [59] Camera, D.M., Ong, J.N., Coffey, V.G., Hawley, J.A., Selective modulation of microRNA expression with protein ingestion following concurrent resistance and endurance exercise in human skeletal muscle. Front. Phys., 7, 2016, 10.3389/fphys.2016.00087.
60. [60] Yamamoto, H., Morino, K., Nishio, Y., Ugi, S., Yoshizaki, T., Kashiwagi, A., Maegawa, H., MicroRNA-494 regulates mitochondrial biogenesis in skeletal muscle through mitochondrial transcription factor A and Forkhead box j3. Am. J. Physiol. Endocrinol. Metab. 303:12 (2012), E1419–E1427, 10.1152/ajpendo.00097.2012.
61. [61] Zhang, Y., Yang, L., Gao, Y.F., Fan, Z.M., Cai, X.Y., Liu, M.Y., Guo, X.R., Gao, C.L., Xia, Z.K., MicroRNA-106b induces mitochondrial dysfunction and insulin resistance in C2C12 myotubes by targeting mitofusin-2. Mol. Cell. Endocrinol. 381:1–2 (2013), 230–240, 10.1016/j.mce.2013.08.004.
62. [62] Zhang, Y., Zhao, Y.P., Gao, Y.F., Fan, Z.M., Liu, M.Y., Cai, X.Y., Xia, Z.K., Gao, C.L., Silencing miR-106b improves palmitic acid-induced mitochondrial dysfunction and insulin resistance in skeletal myocytes. Mol. Med. Rep. 11:5 (2015), 3834–3841, 10.3892/mmr.2014.3124.
63. [63] Godlewski, J., Nowicki, M.O., Bronisz, A., Nuovo, G., Palatini, J., De Lay, M., Van Brocklyn, J., Ostrowski, M.C., Chiocca, E.A., Lawler, S.E., MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells. Mol. Cell 37:5 (2010), 620–632, 10.1016/j.molcel.2010.02.018.
64. [64] Carrer, M., Liu, N., Grueter, C.E., Williams, A.H., Frisard, M.I., Hulver, M.W., Bassel-Duby, R., Olson, E.N., Control of mitochondrial metabolism and systemic energy homeostasis by microRNAs 378 and 378*. Proc. Natl. Acad. Sci. 109:38 (2012), 15330–15335, 10.1073/pnas.1207605109.
65. [65] Gan, Z., Rumsey, J., Hazen, B.C., Lai, L., Leone, T.C., Vega, R.B., Xie, H., Conley, Conley, K.E., Auwerx, J., Smith, S.R., Olson, Olson, E.N., Kralli, A., Kelly, D.P., Nuclear receptor/microRNA circuitry links muscle fiber type to energy metabolism. J. Clin. Investig. 123:6 (2013), 2564–2575, 10.1172/JCI67652.
66. [66] van Rooij, E., The art of microRNA research. Circ. Res. 108:2 (2011), 219–234, 10.1161/circresaha.110.227496.
67. [67] Pritchard, C.C., Cheng, H.H., Tewari, M., MicroRNA profiling: approaches and considerations. Nat. Rev. Genet. 13:5 (2012), 358–369, 10.1038/nrg3198.
68. [68] Karbiener, M., Glantschnig, C., Scheideler, M., Hunting the needle in the haystack: a guide to obtain biologically meaningful microRNA targets. Int. J. Mol. Sci. 15:11 (2014), 20266–20289, 10.3390/ijms151120266.
69. [69] Karginov, F.V., Conaco, C., Xuan, Z., Schmidt, B.H., Parker, J.S., Mandel, G., Hannon, G.J., A biochemical approach to identifying microRNA targets. Proc. Natl. Acad. Sci. U. S. A. 104:49 (2007), 19291–19296, 10.1073/pnas.0709971104.
70. [70] Podolska, A., Kaczkowski, B., Litman, T., Fredholm, M., Cirera, S., How the RNA isolation method can affect microRNA microarray results. Acta Biochim. Pol. 58:4 (2011), 535–540.
71. [71] Matouskova, P., Bartikova, H., Bousova, I., Hanusova, V., Szotakova, B., Skalova, L., Reference genes for real-time PCR quantification of messenger RNAs and microRNAs in mouse model of obesity. PLoS One, 9(1), 2014, e86033, 10.1371/journal.pone.0086033.
72. [72] Yue, D., Liu, H., Huang, Y., Survey of computational algorithms for microRNA target prediction. Curr. Genom. 10:7 (2009), 478–492, 10.2174/138920209789208219.
73. [73] Ceafalan, L.C., Popescu, B.O., Hinescu, M.E., Cellular players in skeletal muscle regeneration. Biomed. Res. Int., 2014, 2014, 957014, 10.1155/2014/957014.
74. [74] Vanderburg, C.R., Clarke, M.S., Laser capture microdissection of metachromatically stained skeletal muscle allows quantification of fiber type specific gene expression. Mol. Cell. Biochem. 375:1–2 (2013), 159–170, 10.1007/s11010-012-1538-x.
75. [75] Stegle, O., Teichmann, S.A., Marioni, J.C., Computational and analytical challenges in single-cell transcriptomics. Nat. Rev. Genet. 16:3 (2015), 133–145, 10.1038/nrg3833.
76. [76] Murgia, M., Nagaraj, N., Deshmukh, A.S., Zeiler, M., Cancellara, P., Moretti, I., Reggiani, C., Schiaffino, S., Mann, M., Single muscle fiber proteomics reveals unexpected mitochondrial specialization. EMBO Rep. 16:3 (2015), 387–395, 10.15252/embr.201439757.
77. [77] Pillai, R.S., Bhattacharyya, S.N., Artus, C.G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E., Filipowicz, W., Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309:5740 (2005), 1573–1576, 10.1126/science.1115079.
78. [78] Nelson, P.T., Baldwin, D.A., Kloosterman, W.P., Kauppinen, S., Plasterk, R.H., Mourelatos, Z., RAKE and LNA-ISH reveal microRNA expression and localization in archival human brain. RNA 12:2 (2006), 187–191, 10.1261/rna.2258506.
79. [79] Chen, K.H., Boettiger, A.N., Moffitt, J.R., Wang, S., Zhuang, X., Spatially resolved, highly multiplexed RNA profiling in single cells. Science (New York, N.Y.), 348(6233), 2015, aaa6090, 10.1126/science.aaa6090.
80. [80] Yang, M., Liu, W., Pellicane, C., Sahyoun, C., Joseph, B.K., Gallo-Ebert, C., Donigan, M., Pandya, D., Giordano, C., Bata, A., Nickels, J.T. Jr., Identification of miR-185 as a regulator of de novo cholesterol biosynthesis and low density lipoprotein uptake. J. Lipid Res. 55:2 (2014), 226–238, 10.1194/jlr.M041335.
81. [81] Tang, H., Lee, M., Sharpe, O., Salamone, L., Noonan, E.J., Hoang, C.D., Levine, S., Robinson, W.H., Shrager, J.B., Oxidative stress-responsive microRNA-320 regulates glycolysis in diverse biological systems. FASEB J. 26:11 (2012), 4710–4721, 10.1096/fj.11-197467.