BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

miR-3074-3p promotes myoblast differentiation by targeting Cav1

  • Lee, Bora (Aging Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Shin, Yeo Jin (Aging Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Lee, Seung-Min (Aging Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Son, Young Hoon (Aging Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Yang, Yong Ryoul (Aging Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Lee, Kwang-Pyo (Aging Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
  • Received : 2020.01.13
  • Accepted : 2020.04.01
  • Published : 2020.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Muscle fibers are generally formed as multinucleated fibers that are differentiated from myoblasts. Several reports have identified transcription factors and proteins involved in the process of muscle differentiation, but the roles of microRNAs (miRNAs) in myogenesis remain unclear. Here, comparative analysis of the miRNA expression profiles in mouse myoblasts and gastrocnemius (GA) muscle uncovered miR-3074-3p as a novel miRNA showing markedly reduced expression in fully differentiated adult skeletal muscle. Interestingly, elevating miR-3074-3p promoted myogenesis in C2C12 cells, primary myoblasts, and HSMMs, resulting in increased mRNA expression of myogenic makers such as Myog and MyHC. Using a target prediction program, we identified Caveolin-1 (Cav1) as a target mRNA of miR-3074-3p and verified that miR-3074-3p directly interacts with the 3' untranslated region (UTR) of Cav1 mRNA. Consistent with the findings in miR-3074-3p-overexpressing myoblasts, knockdown of Cav1 promoted myogenesis in C2C12 cells and HSMMs. Taken together, our results suggest that miR-3074-3p acts a positive regulator of myogenic differentiation by targeting Cav1.

Keywords

References

  1. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9, 493-495 https://doi.org/10.1083/jcb.9.2.493
  2. Relaix F and Zammit PS (2012) Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 139, 2845-2856 https://doi.org/10.1242/dev.069088
  3. Bernet JD, Doles JD, Hall JK, Kelly Tanaka K, Carter TA and Olwin BB (2014) p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat Med 20, 265-271 https://doi.org/10.1038/nm.3465
  4. He WA, Berardi E, Cardillo VM et al (2013) NF-kappaBmediated Pax7 dysregulation in the muscle microenvironment promotes cancer cachexia. J Clin Invest 123, 4821-4835 https://doi.org/10.1172/JCI68523
  5. Blau HM, Webster C and Pavlath GK (1983) Defective myoblasts identified in Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 80, 4856-4860 https://doi.org/10.1073/pnas.80.15.4856
  6. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 https://doi.org/10.1016/S0092-8674(04)00045-5
  7. Ambros V (2004) The functions of animal microRNAs. Nature 431, 350-355 https://doi.org/10.1038/nature02871
  8. O'Rourke JR, Georges SA, Seay HR et al (2007) Essential role for Dicer during skeletal muscle development. Dev Biol 311, 359-368 https://doi.org/10.1016/j.ydbio.2007.08.032
  9. Eisenberg I, Eran A, Nishino I et al (2007) Distinctive patterns of microRNA expression in primary muscular disorders. Proc Natl Acad Sci U S A 104, 17016-17021 https://doi.org/10.1073/pnas.0708115104
  10. Thum T, Galuppo P, Wolf C et al (2007) MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation 116, 258-267 https://doi.org/10.1161/CIRCULATIONAHA.107.687947
  11. Dey BK, Gagan J, Yan Z and Dutta A (2012) miR-26a is required for skeletal muscle differentiation and regeneration in mice. Genes Dev 26, 2180-2191 https://doi.org/10.1101/gad.198085.112
  12. Liu N, Williams AH, Maxeiner JM et al (2012) microRNA-206 promotes skeletal muscle regeneration and delays progression of Duchenne muscular dystrophy in mice. J Clin Invest 122, 2054-2065 https://doi.org/10.1172/JCI62656
  13. Cheung TH, Quach NL, Charville GW et al (2012) Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482, 524-528 https://doi.org/10.1038/nature10834
  14. Callis TE, Chen JF and Wang DZ (2007) MicroRNAs in skeletal and cardiac muscle development. DNA Cell Biol 26, 219-225 https://doi.org/10.1089/dna.2006.0556
  15. McCarthy JJ and Esser KA (2007) MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J Appl Physiol (1985) 102, 306-313 https://doi.org/10.1152/japplphysiol.00932.2006
  16. McCarthy JJ, Esser KA, Peterson CA and Dupont-Versteegden EE (2009) Evidence of MyomiR network regulation of beta-myosin heavy chain gene expression during skeletal muscle atrophy. Physiol Genomics 39, 219-226 https://doi.org/10.1152/physiolgenomics.00042.2009
  17. Townley-Tilson WH, Callis TE and Wang D (2010) MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease. Int J Biochem Cell Biol 42, 1252-1255 https://doi.org/10.1016/j.biocel.2009.03.002
  18. McCarthy JJ (2011) The MyomiR network in skeletal muscle plasticity. Exerc Sport Sci Rev 39, 150-154 https://doi.org/10.1097/JES.0b013e31821c01e1
  19. Bagheri A, Khorram Khorshid HR, Mowla SJ et al (2017) Altered miR-223 Expression in Sputum for Diagnosis of Non-Small Cell Lung Cancer. Avicenna J Med Biotechnol 9, 189-195
  20. Kim JY, Park YK, Lee KP et al (2014) Genome-wide profiling of the microRNA-mRNA regulatory network in skeletal muscle with aging. Aging (Albany NY) 6, 524-544 https://doi.org/10.18632/aging.100677
  21. Lee KP, Shin YJ, Panda AC et al (2015) miR-431 promotes differentiation and regeneration of old skeletal muscle by targeting Smad4. Genes Dev 29, 1605-1617 https://doi.org/10.1101/gad.263574.115
  22. Ha M and Kim VN (2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15, 509-524 https://doi.org/10.1038/nrm3838
  23. Han J, Lee Y, Yeom KH, Kim YK, Jin H and Kim VN (2004) The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 18, 3016-3027 https://doi.org/10.1101/gad.1262504
  24. Volonte D, Liu Y and Galbiati F (2005) The modulation of caveolin-1 expression controls satellite cell activation during muscle repair. FASEB J 19, 237-239
  25. Sabourin LA and Rudnicki MA (2000) The molecular regulation of myogenesis. Clin Genet 57, 16-25 https://doi.org/10.1034/j.1399-0004.2000.570103.x
  26. Sartorelli V and Caretti G (2005) Mechanisms underlying the transcriptional regulation of skeletal myogenesis. Curr Opin Genet Dev 15, 528-535 https://doi.org/10.1016/j.gde.2005.04.015
  27. Wang YX and Rudnicki MA (2011) Satellite cells, the engines of muscle repair. Nat Rev Mol Cell Biol 13, 127-133 https://doi.org/10.1038/nrm3265
  28. Ge Y and Chen J (2011) MicroRNAs in skeletal myogenesis. Cell Cycle 10, 441-448 https://doi.org/10.4161/cc.10.3.14710
  29. Khanna N, Ge Y and Chen J (2014) MicroRNA-146b promotes myogenic differentiation and modulates multiple gene targets in muscle cells. PLoS One 9, e100657 https://doi.org/10.1371/journal.pone.0100657
  30. Wong CF and Tellam RL (2008) MicroRNA-26a targets the histone methyltransferase Enhancer of Zeste homolog 2 during myogenesis. J Biol Chem 283, 9836-9843 https://doi.org/10.1074/jbc.M709614200
  31. Chen JF, Mandel EM, Thomson JM et al (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
  32. Sun Y, Ge Y, Drnevich J, Zhao Y, Band M and Chen J (2010) Mammalian target of rapamycin regulates miRNA-1 and follistatin in skeletal myogenesis. J Cell Biol 189, 1157-1169 https://doi.org/10.1083/jcb.200912093
  33. Dey BK, Gagan J and Dutta A (2011) miR-206 and -486 induce myoblast differentiation by downregulating Pax7. Mol Cell Biol 31, 203-214 https://doi.org/10.1128/MCB.01009-10
  34. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR and Anderson RG (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68, 673-682 https://doi.org/10.1016/0092-8674(92)90143-z
  35. Parton RG and Simons K (2007) The multiple faces of caveolae. Nat Rev Mol Cell Biol 8, 185-194 https://doi.org/10.1038/nrm2122
  36. Han DS, Yang WS and Kao TW (2017) Dexamethasone treatment at the myoblast stage enhanced C2C12 myocyte differentiation. Int J Med Sci 14, 434-443 https://doi.org/10.7150/ijms.18427
  37. Rando TA and Blau HM (1994) Primary mouse myoblast purification, characterization, and transplantation for cellmediated gene therapy. J Cell Biol 125, 1275-1287 https://doi.org/10.1083/jcb.125.6.1275
  38. Park SY, Yun Y, Lim JS et al (2016) Stabilin-2 modulates the efficiency of myoblast fusion during myogenic differentiation and muscle regeneration. Nat Commun 7, 10871 https://doi.org/10.1038/ncomms10871