DOI QR코드

DOI QR Code

Dynamical Expression of MicroRNA-127-3p in Proliferating and Differentiating C2C12 Cells

  • Li, Jie (College of Animal Science and Technology, Gansu Agricultural University) ;
  • Wang, Gaofu (Chongqing Academy of Animal Science) ;
  • Jiang, Jing (Chongqing Academy of Animal Science) ;
  • Zhou, Peng (Chongqing Academy of Animal Science) ;
  • Liu, Liangjia (Chongqing Academy of Animal Science) ;
  • Zhao, Jinhong (Chongqing Academy of Animal Science) ;
  • Wang, Lin (Chongqing Academy of Animal Science) ;
  • Huang, Yongfu (Chongqing Academy of Animal Science) ;
  • Ma, Youji (College of Animal Science and Technology, Gansu Agricultural University) ;
  • Ren, Hangxing (Chongqing Academy of Animal Science)
  • Received : 2015.11.25
  • Accepted : 2016.01.19
  • Published : 2016.12.01

Abstract

MicroRNAs (miRNAs) are highly conserved, short non-coding RNAs that regulate gene expression at the posttranscriptional level. Although many miRNAs are identified in muscles and muscle cells, their individual roles are still not fully understood. In the present study, we investigated a muscle highly-expressed miRNA, miR-127-3p, in C2C12 myoblasts and tissues of goats with different muscle phenotypes (Boer vs Wushan black goats). Our results demonstrated that i) miR-127-3p was extensively expressed in tissues of goats; ii) miR-127-3p was higher expressed in muscle, spleen, heart, and skin in the muscular goats (Boer goats) than the control (Wushan black goats). Then we further characterized the dynamical expression of miR-127-3p, MyoD, MyoG, Myf5, Mef2c, and Myosin in the proliferating and differentiating C2C12 myoblasts at day of 0, 1, 3, 5, and 7 in culture mediums. Especially, we found that miR-127-3p was significantly higher expressed in the proliferating than differentiating cells. Our findings suggest that miR-127-3p probably plays roles in the proliferation and differentiation of myoblasts, which further underlies regulation of muscle phenotype in goats.

Keywords

References

  1. Anderson, C., H. Catoe, and R. Werner. 2006. MIR-206 regulates connexin43 expression during skeletal muscle development. Nucleic Acids. Res. 34:5863-5871. https://doi.org/10.1093/nar/gkl743
  2. Benetatos, L., E. Hatzimichael, E. Londin, G. Vartholomatos, P. Loher, I. Rigoutsos, and E. Briasoulis. 2013. The microRNAs within the DLK1-DIO3 genomic region involvement in disease pathogenesis. Cell. Mol. Life Sci. 70:795-814. https://doi.org/10.1007/s00018-012-1080-8
  3. Bhaskaran, M., Y. Wang, H. Zhang, T. Weng, P. Baviskar, Y. Guo, D. Gou, and L. Liu. 2009. MicroRNA-127 modulates fetal lung development. Physiol. Genomics 37:268-278. https://doi.org/10.1152/physiolgenomics.90268.2008
  4. Bushati, N. A. and S. M. Cohen. 2007. MicroRNA functions. Annu. Rev. Cell Dev. Biol. 23:175-205. https://doi.org/10.1146/annurev.cellbio.23.090506.123406
  5. Cardinali, B., L. Castellani, P. Fasanaro, A. Basso, S. Alema, F. Martelli, and G. Falcone. 2009. Microrna-221 and microrna- 222 modulate differentiation and maturation of skeletal muscle cells. PLoS ONE 4:e7607. https://doi.org/10.1371/journal.pone.0007607
  6. Chekulaeva, M. and W. Filipowicz. 2009. Mechanisms of miRNAmediated post-transcriptional regulation in animal cells. Curr. Opin. Cell Biol. 21:452-460. https://doi.org/10.1016/j.ceb.2009.04.009
  7. Chen, J. F., E. M. Mandel, J. M. Thomson, Q. Wu, T. E. Callis, S. M. Hammond, F. L. Conlon, and D. Z. Wang. 2006. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38:228-233. https://doi.org/10.1038/ng1725
  8. Crist, C. G., M. Didier, G. Pallafacchina, D. Rocancourt, A. Cumano, S. J. Conway, and M. Buckingham. 2009. Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression. Proc. Natl. Acad. Sci. USA. 106:13383-13387. https://doi.org/10.1073/pnas.0900210106
  9. Dey, B. K., J. Gagan, and A. Dutta. 2011. MiR-206 and miR-486 induce myoblast differentiation by downregulating Pax7. Mol. Cell. Biol. 31:203-214. https://doi.org/10.1128/MCB.01009-10
  10. Dey, B. K., G. Jeffrey, Y. Zhen, and D. Anindya. 2012. MiR-26a is required for skeletal muscle differentiation and regeneration in mice. Gene Dev. 26:2180-2191. https://doi.org/10.1101/gad.198085.112
  11. Feng, Y., J. H. Cao, X. Y. Li, and S. H. Zhao. 2011. Inhibition of miR-214 expression represses proliferation and differentiation of C2C12 myoblasts. Cell. Biochem. Funct. 29:378-383. https://doi.org/10.1002/cbf.1760
  12. Lim, L. P., N. C. Lau, P. Garrett-Engele, A. Grimson, J. M. Schelter, J. Castle, D. P. Bartel, P. S. Linsley, and J. M. Johnson. 2005. Microarray analysis shows that some microRNAs down-regulate large numbers of target mRNAs. Nature 433:769-773. https://doi.org/10.1038/nature03315
  13. Naguibneva, I., M. Ameyar-Zazoua, A. Polesskaya, S. Ait-Si-Ali, R. Groisman, M. Souidi, S. Cuvellier, and A. Harel-Bellan. 2006. The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation. Nat. Cell. Biol. 8:278-284. https://doi.org/10.1038/ncb1373
  14. Pan, C., H. Chen, L. Wang, S. Yang, H. Fu, Y. Zheng, M. Miao, and B. Jiao. 2012. Down-regulation of MiR-127 facilitates hepatocyte proliferation during rat liver regeneration. PLoS ONE 7:e39151. https://doi.org/10.1371/journal.pone.0039151
  15. Lewis, B. P., I. H. Shih, M. W. Jones-Rhoades, D. P. Bartel, and C. B. Burge. 2003. Prediction of mammalian microRNA targets. Cell 115:787-798. https://doi.org/10.1016/S0092-8674(03)01018-3
  16. Rao, P. K., R. M. Kumar, M. Farkhondeh, S. Baskervile, and H. F. Lodish. 2006. Myogenic factors that regulate expression of muscle-specific microRNAs. Proc. Natl. Acad. Sci. USA. 103:8721-8726. https://doi.org/10.1073/pnas.0602831103
  17. Robertus, J. L., G. Harms, T. Blokzijl, M. Booman, D. de Jong, G. van Imhoff, S. Rosati, E. Schuuring, P. Kluin, and A. van den Berg. 2009. Specific expression of miR-17-5p and miR-127 in testicular and central nervous system diffuse large B-cell lymphoma. Mod. Pathol. 22:547-555. https://doi.org/10.1038/modpathol.2009.10
  18. Sarkar, S., B. K. Dey, and A. Dutta. 2010. MiR-322/424 and miR- 503 are induced during muscle differentiation and promote cell cycle quiescence and differentiation by down-regulation of Cdc25A. Mol. Biol. Cell 21:2138-2149. https://doi.org/10.1091/mbc.E10-01-0062
  19. Seok, H. Y., M. Tatsuguchi, T. E. Callis, A. He, W. T. Pu, and D. Z. Wang. 2011. MiR-155 inhibits expression of the MEF2A protein to repress skeletal muscle differentiation. J. Biol. Chem. 286:35339-35346. https://doi.org/10.1074/jbc.M111.273276
  20. Singh, K. and F. J. Dilworth. 2013. Differential modulation of cell cycle progression distinguishes members of the myogenic regulatory factor family of transcription factors. FEBS J. 280:3991-4003. https://doi.org/10.1111/febs.12188
  21. Ge, Y., Y. Sun, and J. Chen 2011. IGF-II is regulated by microRNA-125b in skeletal myogenesis. J. Cell. Biol. 192:69-81. https://doi.org/10.1083/jcb.201007165
  22. van Rooij, E., D. Quiat, B. A. Johnson, L. B. Sutherland, X. Qi, J. A. Richardson, R. J. Kelm Jr., and E. N. Olson. 2009. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev. Cell. 17:662-673. https://doi.org/10.1016/j.devcel.2009.10.013
  23. Wei, W., H. B. He, W. Y. Zhang, H. X. Zhang, J. B. Bai, H. Z. Liu, J. H. Cao, K. C. Chang, X. Y. Li, and S. H. Zhao. 2013. MiR- 29 targets Akt3 to reduce proliferation and facilitate differentiation of myoblasts in skeletal muscle development. Cell Death Dis. 4:e668. https://doi.org/10.1038/cddis.2013.184
  24. Wilfred, B. R., W. X. Wang, and P. T. Nelson. 2007. Energizing miRNA research: A review of the role of miRNAs in lipid metabolism, with a prediction that miR-103/107 regulates human metabolic pathways. Mol. Genet. Metab. 91:209-217. https://doi.org/10.1016/j.ymgme.2007.03.011
  25. Xie, T., J. Liang, N. Liu, Q. Wang, Y. Li, P. W. Noble, and D. Jiang. 2012. MicroRNA-127 inhibits lung inflammation by targeting IgG $Fc{\gamma}$ receptor I. J. Immunol. 188:2437-2444. https://doi.org/10.4049/jimmunol.1101070
  26. Yang, Y., Y. Li, R. Liang, R. Zhou, H. Ao, Y. Mu, S. Yang, K. Li, and Z. Tang. 2014. Dynamic expression of microRNA-127 during porcine prenatal and postnatal skeletal muscle development. J. Integr. Agric. 13:1331-1339. https://doi.org/10.1016/S2095-3119(13)60419-0
  27. Zhang, S., F. Zhao, C. Wei, X. Sheng, H. Ren, L. Xu, J. Lu, J. Liu, L. Zhang, and L. Du. 2013. Identification and characterization of the miRNA transcriptome of Ovis aries. PLoS ONE. 8:e58905. https://doi.org/10.1371/journal.pone.0058905

Cited by

  1. miR-127 enhances myogenic cell differentiation by targeting S1PR3 vol.8, pp.3, 2017, https://doi.org/10.1038/cddis.2017.128
  2. in C2C12 myoblasts vol.22, pp.5, 2018, https://doi.org/10.1080/19768354.2018.1512520
  3. Deciphering the miRNA transcriptome of Rongchang pig longissimus dorsi at weaning and slaughter time points vol.104, pp.3, 2016, https://doi.org/10.1111/jpn.13314
  4. In vitro CSC-derived cardiomyocytes exhibit the typical microRNA-mRNA blueprint of endogenous cardiomyocytes vol.4, pp.1, 2016, https://doi.org/10.1038/s42003-021-02677-y