Expression of miR-1, miR-133a, miR-133b and miR-206 increases during development of human skeletal muscle

Andrie Koutsoulidou1, Nikolaos P. Mastroyiannopoulos1, Denis Furling2, James B. Uney3, Leonidas A. Phylactou1
1Department of Molecular Genetics, Function & Therapy, The Cyprus Institute of Neurology & Genetics, P.O. Box 2346, 1683, Nicosia, Cyprus
2UPMC Univ Paris 06, UM76, Institut de Myologie, and INSERM, U974 and CNRS, UMR7215, Paris, France
3The Henry Wellcome Laboratories for Integrative Neuroscience and Endocrinology, Dorothy Hodgkin Building, University of Bristol, Whitson Street, Bristol, BS1 3NY, UK

Tóm tắt

Abstract Background MicroRNAs (miRNAs) are small RNA molecules that post-transcriptionally regulate gene expression and have been shown to play an important role during development. miR-1, miR-133a, miR-133b and miR-206 are expressed in muscle tissue and induced during muscle cell differentiation, a process that directs myoblasts to differentiate into mature myotubes, which are organized into myofibers. Although miR-1, miR-133a, miR-133b and miR-206 are well-studied in muscle, there is no information about their expression and function during human development. The purpose of this study was to determine the profile of these miRNAs in muscle cells isolated from different stages of human development. Results We examined the levels of miR-1, miR-133a, miR-133b and miR-206 during the development of human foetus. All four miRNA levels were found increased during late stages of human foetal muscle development. Increases in the expression levels of these miRNAs were proportional to the capacity of myoblasts to form myotubes. Changes in miRNA levels during human foetal development were accompanied by endogenous alterations in their known targets and also in their inducer, MyoD. Ectopic MyoD expression caused an induction of muscle cell differentiation in vitro, accompanied by an increase in the levels of miR-1, miR-133a, miR-133b and miR-206. Conclusions This study provides data about the profile of four miRNAs in human muscle cells isolated during different stages of foetal development. These results may shed light on the differentiation of muscle cells and regulation of muscle formation through miRNAs, during the development of human foetus.

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Tài liệu tham khảo

Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004, 116: 281-297. 10.1016/S0092-8674(04)00045-5.

Krol J, Loedige I, Filipowicz W: The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet. 2010, 11: 597-610.

Garzon R, Marcucci G, Croce CM: Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov. 2010, 9: 775-789. 10.1038/nrd3179.

Townley-Tilson WH, Callis TE, Wang D: MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease. Int J Biochem Cell Biol. 2010, 42: 1252-1255. 10.1016/j.biocel.2009.03.002.

Ivey KN, Srivastava D: MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell. 2010, 7: 36-41. 10.1016/j.stem.2010.06.012.

Williams AH, Liu N, van Rooij E, Olson EN: MicroRNA control of muscle development and disease. Curr Opin Cell Biol. 2009, 21: 461-469. 10.1016/j.ceb.2009.01.029.

Sabourin LA, Rudnicki MA: The molecular regulation of myogenesis. Clin Genet. 2000, 57: 16-25.

Parker MH, Seale P, Rudnicki MA: Looking back to the embryo: defining transcriptional networks in adult myogenesis. Nat Rev Genet. 2003, 4: 497-507.

Relaix F: Skeletal muscle progenitor cells: from embryo to adult. Cell Mol Life Sci. 2006, 63: 1221-1225. 10.1007/s00018-006-6015-9.

Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ: The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet. 2006, 38: 228-233. 10.1038/ng1725.

Kim HK, Lee YS, Sivaprasad U, Malhotra A, Dutta A: Muscle-specific microRNA miR-206 promotes muscle differentiation. J Cell Biol. 2006, 174: 677-687. 10.1083/jcb.200603008.

Rao PK, Kumar RM, Farkhondeh M, Baskerville S, Lodish HF: Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci USA. 2006, 103: 8721-8726. 10.1073/pnas.0602831103.

Liu N, Williams AH, Kim Y, McAnally J, Bezprozvannaya S, Sutherland LB, Richardson JA, Bassel-Duby R, Olson EN: An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc Natl Acad Sci USA. 2007, 104: 20844-20849. 10.1073/pnas.0710558105.

Rosenberg MI, Georges SA, Asawachaicharn A, Analau E, Tapscott SJ: MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J Cell Biol. 2006, 175: 77-85. 10.1083/jcb.200603039.

Anderson C, Catoe H, Werner R: MIR-206 regulates connexin43 expression during skeletal muscle development. Nucleic Acids Res. 2006, 34: 5863-5871. 10.1093/nar/gkl743.

Song G, Wang L: Nuclear receptor SHP activates miR-206 expression via a cascade dual inhibitory mechanism. PLoS One. 2009, 4: e6880-10.1371/journal.pone.0006880.

Hirai H, Verma M, Watanabe S, Tastad C, Asakura Y, Asakura A: MyoD regulates apoptosis of myoblasts through microRNA-mediated down-regulation of Pax3. J Cell Biol. 2010, 191: 347-365. 10.1083/jcb.201006025.

Edom-Vovard F, Mouly V, Barbet JP, Butler-Browne GS: The four populations of myoblasts involved in human limb muscle formation are present from the onset of primary myotube formation. J Cell Sci. 1999, 112 (Pt 2): 191-199.

Takada S, Berezikov E, Yamashita Y, Lagos-Quintana M, Kloosterman WP, Enomoto M, Hatanaka H, Fujiwara S, Watanabe H, Soda M, et al: Mouse microRNA profiles determined with a new and sensitive cloning method. Nucleic Acids Res. 2006, 34: e115-10.1093/nar/gkl653.

Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, de Bruijn E, Horvitz HR, Kauppinen S, Plasterk RH: MicroRNA expression in zebrafish embryonic development. Science. 2005, 309: 310-311. 10.1126/science.1114519.

Lu J, McKinsey TA, Zhang CL, Olson EN: Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases. Mol Cell. 2000, 6: 233-244. 10.1016/S1097-2765(00)00025-3.

McKinsey TA, Zhang CL, Lu J, Olson EN: Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature. 2000, 408: 106-111. 10.1038/35040593.

Tapscott SJ: The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development. 2005, 132: 2685-2695. 10.1242/dev.01874.

Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R: MyoD or Myf-5 is required for the formation of skeletal muscle. Cell. 1993, 75: 1351-1359. 10.1016/0092-8674(93)90621-V.

Kitzmann M, Fernandez A: Crosstalk between cell cycle regulators and the myogenic factor MyoD in skeletal myoblasts. Cell Mol Life Sci. 2001, 58: 571-579. 10.1007/PL00000882.

Weintraub H, Tapscott SJ, Davis RL, Thayer MJ, Adam MA, Lassar AB, Miller AD: Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc Natl Acad Sci USA. 1989, 86: 5434-5438. 10.1073/pnas.86.14.5434.

Sabourin LA, Girgis-Gabardo A, Seale P, Asakura A, Rudnicki MA: Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle. J Cell Biol. 1999, 144: 631-643. 10.1083/jcb.144.4.631.

Decary S, Mouly V, Hamida CB, Sautet A, Barbet JP, Butler-Browne GS: Replicative potential and telomere length in human skeletal muscle: implications for satellite cell-mediated gene therapy. Hum Gene Ther. 1997, 8: 1429-1438. 10.1089/hum.1997.8.12-1429.

Yuan JS, Reed A, Chen F, Stewart CN: Statistical analysis of real-time PCR data. BMC Bioinformatics. 2006, 7: 85-10.1186/1471-2105-7-85.