microRNAs are endogenous noncoding RNA molecules of ∼22 nucleotides that regulate gene function by modification of target mRNAs. Due to tissue specific of miR-133a and miR-1/206 for skeletal muscles, we investigated the role of miR-133a and miR-1/206 in promoting the differentiation of the C2C12 cells. The results show that directly transfecting mature miR-133a, miR-1/206, or combinations (miR-1 and miR-206, miR-1 and miR-133a, and miR-133a and miR-206) into C2C12 cells, respectively, for 5 days induces formation of myogenic progenitor cells. Overexpression of miR-133a and miR-206 in C2C12 cells greatly improved multinucleated myotube formation. microRNA-133a (miR-133a) is highly expressed during human muscle development. Using bioinformatics, we identified one putative miR-133a binding site within the 3′-untranslated region of the mouse Foxl2 mRNA. The expression of Foxl2 was shown to be downregulated by subsequent western blot analysis.
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References
1.
Alvarez-GarciaI., and MiskaE.A. (2005). MicroRNA functions in animal development and human disease. Development, 132, 4653–4662.
BenayounB.A., AnttonenM., L'HôteD., Bailly-BechetM., AnderssonN., HeikinheimoM., et al. (2012) Adult ovarian granulosa cell tumor transcriptomics: prevalence of FOXL2 target genes misregulation gives insights into the pathogenic mechanism of the p.Cys134Trp somatic mutation. Oncogene, 32, 2739–2746.
4.
BoutzP.L., ChawlaG., StoilovP., and BlackD.L. (2007). MicroRNAs regulate the expression of the alternative splicing factor nPTB during muscle development. Gene Dev, 21, 71–84.
5.
BraseJ.C., WuttigD., KunerR., and SültmannH. (2010). Serum microRNAs as non-invasive biomarkers for cancer. Mol Cancer, 9, 306.
6.
CallisT.E., ChenJ.F., and WangD.Z. (2007). MicroRNAs in skeletal and cardiac muscle development. DNA Cell Biol, 26, 219–225.
7.
ChenJ.F., MandelE.M., ThomsonM.J., WuQ.L., CallisT.E., HammondS.M., et al. (2006). The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet, 38, 228–233.
8.
ChenJ.F., TaoY.Z., LiJ., DengZ.L., YanZ., XiaoX., et al. (2010). microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J Cell Biol, 190, 867–879.
9.
ChenX., WangK.H., ChenJ.N., GuoJ.G., YinY., CaiX., et al. (2008). In vitro evidence suggests that miR-133a-mediated regulation of uncoupling protein 2 (UCP2) is an indispensable step in myogenic differentiation. J Biol Chem, 284, 5362–5369.
10.
CordesK.R., SheehyN.T., WhiteM., BerryE., MortonS.U., MuthA.N., et al. (2009). miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature, 460, 705–710.
11.
EisenbergI., AlexanderbM.S., and KunkelaL.M. (2008). miRNAS in normal and diseased skeletal muscle. J Cell Mol Med, 13, 2–11.
12.
EisenbergaI., EranbA., NishinoI., MoggioM., LamperteC., et al. (2007). Distinctive patterns of microRNA expression in primary muscular disorders. Proc Natl Acad Sci U S A, 104, 17016–17021.
13.
FabbriM. (2013). MicroRNAs and cancer: towards a personalized medicine. Curr Mol Med, 13, 751–756.
14.
GeY.J., and ChenJ. (2011). MicroRNAs in skeletal myogenesis. Cell Cycle, 10, 441–448.
15.
HaT.Y. (2011). MicroRNAs in human diseases: from cancer to cardiovascular disease. Immune Netw, 11, 135.
16.
HanM.Y., ToliJ., and AbdellatifM. (2011). MicroRNAs in the cardiovascular system. Curr Opin Cardiol, 26, 181–189.
17.
HeB., XiaoJ., RenA.J., ZhangY.F., ZhangH., ChenM., et al. (2011). Role of miR-1 and miR-133a in myocardial ischemic postconditioning. J Biomed Sci, 18, 22.
18.
HeidiD., AnnaG., StefanG., MaliS.D., ChristinaC., AndreaS., et al. (2013). The shaping and functional consequences of the microRNA landscape in breast cancer. Nature, 497, 378–382.
19.
HuangF.D., OsafuneK., MaehrR., GuoW., EijkelenboomA., ChenS., et al. (2008). Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol, 26, 1269–1275.
20.
JiangH., HuangX.H., SuZ.G., RaoL.B., WuS.S., ZhangT., et al. (2013). Genetic analysis of the forkhead transcriptional factor 2 gene in three Chinese families with blepharophimosis syndrome. Mol Vis, 19, 418–423.
21.
JinY., TymenS.D., ChenD., FangZ.J., ZhaoY., DragasD., et al. (2013). MicroRNA-99 family targets AKT/mTOR signaling pathway in dermal wound healing. PLoS One, 8, e64434.
22.
KatoY., MiyakiS., YokoyamaS., OmoriS., InoueA., HoriuchiM., et al. (2009). Real-time functional imaging for monitoring miR-133 during myogenic differentiation. Int J Biochem Cell Biol, 41, 2225–2231.
23.
KimD., KimC.H., MoonJ.I., ChungY.G., ChangM.Y., HanB.S., et al. (2009). Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell, 4, 472–476.
KoutsoulidouA., MastroyiannopoulosN.P., FurlingD., UneyJ.B., and PhylactouL.A. (2011). Expression of miR-1, miR-133a, miR-133b and miR-206 increases during development of human skeletal muscle. BMC Dev Biol, 11, 34.
26.
KrolJ., LoedigeI., and FilipowiczW. (2010). The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet, 11, 597–610.
27.
LeeT.H., SongS.H., KimK.L., YiJ.Y., ShinG.H., KimJ.Y., et al. (2009). Functional recapitulation of smooth muscle cells via induced pluripotent stem cells from human aortic smooth muscle cells. Circ Res, 106, 120–128.
28.
LimaJ.F., JinL., De AraujoA.R.C., Erikson-JohnsonM.R., OliveiraA.M., SeboT.J., et al. (2012). FOXL2 mutations in granulosa cell tumors occurring in males. Arch Pathol Lab Med, 136, 825–828.
29.
LimanaF., EspositoG., D'ArcangeloD., CarloA.D., GuidoS.R., et al. (2011). HMGB1 attenuates cardiac remodelling in the failing heart via enhanced cardiac regeneration and miR-206-mediated inhibition of TIMP-3. PLoS One, 6, e19845.
30.
LivakK.J., and SchmittgenT.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402–408.
31.
MaD.L., TaoX.C., GaoF., FanC.J., and WuD.Q. (2012). miR-224 functions as an onco-miRNA in hepatocellular carcinoma cells by activating AKT signaling. Oncol Lett, 4, 483–488.
32.
MirettiS., MartignaniE., TaulliR., BersaniF., AccorneroP., and BarattaM.A. (2011). Differential expression of microRNA-206 in skeletal muscle of female Piedmontese and Friesian cattle. Vet J, 190, 412–413.
33.
MiyoshiN., IshiiH., NaganoH., HaraguchiN., DewiD.L., KanoY., et al. (2011). Reprogramming of mouse and human cells to pluripotency using mature MicroRNAs. Cell Stem Cell, 8, 633–638.
34.
MohamedJ.S., HajiraA., LiZ.L., PaulinD., and BoriekA.M. (2011). Early growth responsive protein-1 induces desmin null airway smooth muscle hypertrophy through MicroRNA-26a. J Biol Chem, 286, 43394–43404.
35.
NishizawaT., and SuzukiH. (2013). The role of microRNA in gastric malignancy. Int J Mol Sci, 14, 9487–9496.
36.
PuriP.L., IezziS., StieglerP., ChenT.T., SchiltzR.L., MuscatG.E.O., et al. (2001). Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis. Mol Cell, 8, 885–897.
37.
RooijE.V., SutherlandL.B., LiuN., WilliamsA.H., McAnallyJ., et al. (2006). A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci U S A, 103, 18255–18260.
SunJ.G., LiaoR.X., QiuJ., JinJ.Y., WangX.X., DuanY.Z., et al. (2010). Microarray-based analysis of microRNA expression in breast cancer stem cells. J Exp Clin Cancer Res, 29, 174.
40.
TakahashiK., and YamanakaS. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663–676.
41.
TakayaT., OnoK., KawamuraT., TakanabeR., KaichiS., MorimotoT., et al. (2009). MicroRNA-1 and MicroRNA-133 in spontaneous myocardial differentiation of mouse embryonic stem cells. Circ J, 73, 1492–1497.
42.
WilliamsA.H., LiuN., van, RooijE., and OlsonE.N. (2009). MicroRNA control of muscle development and disease. Curr Opin Cell Biol, 21, 461–469.
YooA.S., SunA.X., LiL., ShcheglovitovA., PortmannT., LiY., et al. (2011). MicroRNA-mediated conversion of human fibroblasts to neurons. Nature, 476, 228–231.
