MiR-186 inhibits muscle cell differentiation through myogenin regulation

Journal of Biological Chemistry

Volumn 289, Issue 7, 2014, Pages 3923-3935

  Antoniou, Antonis ^a   Mastroyiannopoulos, Nikolaos P ^a   Uney, James B ^b   Phylactou, Leonidas A ^a  

^a CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DIFFERENTIATION; GENE REGULATION; MICRORNA; MUSCLE; MYOGENESIS; MYOGENIN;

3' UNTRANSLATED REGIONS; ANIMALS; CELL DIFFERENTIATION; CELL LINE; MICE; MICRORNAS; MUSCLE, SKELETAL; MYOGENIN; RNA-BINDING PROTEINS;

EID: 84894118746     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.507343     Document Type: Article

References (53)

1. Lassar, A. B., Skapek, S. X., and Novitch, B. (1994) Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr. Opin. Cell Biol. 6, 788-794
2. Sabourin, L. A., and Rudnicki, M. A. (2000) The molecular regulation of myogenesis. Clin. Genet. 57, 16-25
3. Weintraub, H. (1993) The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75, 1241-1244
4. Chargé, S. B., and Rudnicki, M. A. (2004) Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84, 209-238
5. Pownall, M. E., Gustafsson, M. K., and Emerson, C. P., Jr. (2002) Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 18, 747-783
6. Yun, K., and Wold, B. (1996) Skeletal muscle determination and differentiation: story of a core regulatory network and its context. Curr. Opin. Cell Biol. 8, 877-889
7. Braun, T., Bober, E., Buschhausen-Denker, G., Kohtz, S., Grzeschik, K. H., and Arnold, H. H. (1989) Differential expression of myogenic determination genes in muscle cells: possible autoactivation by the Myf gene products. EMBO J. 8, 3617-3625
8. Thayer, M. J., Tapscott, S. J., Davis, R. L., Wright, W. E., Lassar, A. B., and Weintraub, H. (1989) Positive autoregulation of the myogenic determination gene MyoD1. Cell 58, 241-248
9. Brennan, T. J., Edmondson, D. G., and Olson, E. N. (1990) Aberrant regulation of MyoD1 contributes to the partially defective myogenic phenotype of BC3H1 cells. J. Cell Biol. 110, 929-937
10. Fuso, A., Ferraguti, G., Grandoni, F., Ruggeri, R., Scarpa, S., Strom, R., and Lucarelli, M. (2010) Early demethylation of non-CpG, CpC-rich, elements in the myogenin 5-flanking region: a priming effect on the spreading of active demethylation. Cell Cycle 9, 3965-3976
11. Yee, S. P., and Rigby, P. W. (1993) The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev. 7, 1277-1289
12. Myer, A., Olson, E. N., and Klein, W. H. (2001) MyoD cannot compensate for the absence of myogenin during skeletal muscle differentiation in murine embryonic stem cells. Dev. Biol. 229, 340-350
13. Hasty, P., Bradley, A., Morris, J. H., Edmondson, D. G., Venuti, J. M., Olson, E. N., and Klein, W. H. (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501-506
14. Molkentin, J. D., and Olson, E. N. (1996) Defining the regulatory networks for muscle development. Curr. Opin. Genet. Dev. 6, 445-453
15. Edmondson, D. G., and Olson, E. N. (1990) A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes Dev. 4, 1450
16. Rhodes, S. J., and Konieczny, S. F. (1989) Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev. 3, 2050-2061
17. Wright, W. E., Sassoon, D. A., and Lin, V. K. (1989) Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56, 607-617
18. Venuti, J. M., Morris, J. H., Vivian, J. L., Olson, E. N., and Klein, W. H. (1995) Myogenin is required for late but not early aspects of myogenesis during mouse development. J. Cell Biol. 128, 563-576
19. Faralli, H., and Dilworth, F. J. (2012) Turning on myogenin in muscle: a paradigm for understanding mechanisms of tissue-specific gene expression. Comp Funct Genomics 2012, 836374
20. Flynn, J. M., Meadows, E., Fiorotto, M., and Klein, W. H. (2010) Myogenin regulates exercise capacity and skeletal muscle metabolism in the adult mouse. PLoS One 5, e13535
21. Zhao, P., Iezzi, S., Carver, E., Dressman, D., Gridley, T., Sartorelli, V., and Hoffman, E. P. (2002) Slug is a novel downstream target of MyoD. Temporal profiling in muscle regeneration. J. Biol. Chem. 277, 30091-30101
22. Sassoon, D., Lyons, G., Wright, W. E., Lin, V., Lassar, A., Weintraub, H., and Buckingham, M. (1989) Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature 341, 303-307
23. Mastroyiannopoulos, N. P., Nicolaou, P., Anayasa, M., Uney, J. B., and Phylactou, L. A. (2012) Down-regulation of myogenin can reverse terminal muscle cell differentiation. PLoS One 7, e29896
24. Meadows, E., Flynn, J. M., and Klein, W. H. (2011) Myogenin regulates exercise capacity but is dispensable for skeletal muscle regeneration in adult mdx mice. PLoS One 6, e16184
25. Liu, Q. C., Zha, X. H., Faralli, H., Yin, H., Louis-Jeune, C., Perdiguero, E., Pranckeviciene, E., Muñoz-Canoves, P., Rudnicki, M. A., Brand, M., Perez-Iratxeta, C., and Dilworth, F. J. (2012) Comparative expression profiling identifies differential roles for Myogenin and p38alpha MAPK signaling in myogenesis. J. Mol. Cell Biol. 4, 386-397
26. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233
27. Hamilton, A. J., and Baulcombe, D. C. (1999) A species of small antisense RNAin posttranscriptional gene silencing in plants. Science 286, 950-952
28. Ambros, V. (2004) The functions of animal microRNAs. Nature 431, 350-355
29. Lim, L. P., Lau, N. C., Garrett-Engele, P., Grimson, A., Schelter, J. M., Castle, J., Bartel, D. P., Linsley, P. S., and Johnson, J. M. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769-773
30. Chen, J. F., Mandel, E. M., Thomson, J. M., Wu, Q., Callis, T. E., Hammond, S. M., Conlon, F. L., and Wang, D. Z. (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38, 228-233
31. Granjon, A., Gustin, M. P., Rieusset, J., Lefai, E., Meugnier, E., Güller, I., Cerutti, C., Paultre, C., Disse, E., Rabasa-Lhoret, R., Laville, M., Vidal, H., and Rome, S. (2009) 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, 2555-2564
32. Callis, T. E., Deng, Z., Chen, J. F., and Wang, D. Z. (2008) Muscling through the microRNA world. Exp. Biol. Med. 233, 131-138
33. Crist, C. G., Montarras, D., and Buckingham, M. (2012) Muscle satellite cells are primed for myogenesis but maintain quiescence with sequestration of Myf5 mRNA targeted by microRNA-31 in mRNP granules. Cell Stem Cell 11, 118-126
34. Zhang, H., Li, Y., Huang, Q., Ren, X., Hu, H., Sheng, H., and Lai, M. (2011) MiR-148a promotes apoptosis by targeting Bcl-2 in colorectal cancer. Cell Death Differ. 18, 1702-1710
35. Crist, C. G., Montarras, D., Pallafacchina, G., Rocancourt, D., Cumano, A., Conway, S. J., and Buckingham, M. (2009) Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression. Proc. Natl. Acad. Sci. U.S.A. 106, 13383-13387
36. Huang, Z., Chen, X., Yu, B., He, J., and Chen, D. (2012) MicroRNA-27a promotes myoblast proliferation by targeting myostatin. Biochem. Biophys. Res. Commun. 423, 265-269
37. Rosenblatt, J. D., Lunt, A. I., Parry, D. J., and Partridge, T. A. (1995) Culturing satellite cells from living single muscle fiber explants. In Vitro Cell Dev. Biol. Anim. 31, 773-779
38. Yan, Z., Choi, S., Liu, X., Zhang, M., Schageman, J. J., Lee, S. Y., Hart, R., Lin, L., Thurmond, F. A., and Williams, R. S. (2003) Highly coordinated gene regulation in mouse skeletal muscle regeneration. J. Biol. Chem. 278, 8826-8836
39. Isik, M., Korswagen, H. C., and Berezikov, E. (2010) Expression patterns of intronic microRNAs in Caenorhabditis elegans. Silence 1,5
40. Baskerville, S., and Bartel, D. P. (2005) Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. Rna 11, 241-247
41. Kim, Y. K., and Kim, V. N. (2007) Processing of intronic microRNAs. EMBO J. 26, 775-783
42. Baldin, V., Lukas, J., Marcote, M. J., Pagano, M., and Draetta, G. (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev. 7, 812-821
43. Bryan, B. A., Mitchell, D. C., Zhao, L., Ma, W., Stafford, L. J., Teng, B. B., and Liu, M. (2005) Modulation of muscle regeneration, myogenesis, and adipogenesis by the Rho family guanine nucleotide exchange factor GEFT. Mol. Cell Biol. 25, 11089-11101
44. Perdiguero, E., Sousa-Victor, P., Ballestar, E., and Muñoz-Canoves, P. (2009) Epigenetic regulation of myogenesis. Epigenetics 4, 541-550
45. Rodriguez, A., Griffiths-Jones, S., Ashurst, J. L., and Bradley, A. (2004) Identification of mammalian microRNA host genes and transcription units. Genome Res. 14, 1902-1910
46. Berghella, L., De Angelis, L., De Buysscher, T., Mortazavi, A., Biressi, S., Forcales, S. V., Sirabella, D., Cossu, G., and Wold, B. J. (2008) A highly conserved molecular switch binds MSY-3 to regulate myogenin repression in postnatal muscle. Genes Dev. 22, 2125-2138
47. Deato, M. D., and Tjian, R. (2007) Switching of the core transcription machinery during myogenesis. Genes Dev. 21, 2137-2149
48. Cai, J., Wu, J., Zhang, H., Fang, L., Huang, Y., Yang, Y., Zhu, X., Li, R., and Li, M. (2013) miR-186 Downregulation Correlates with Poor Survival in Lung Adenocarcinoma, Where It Interferes with Cell-Cycle Regulation. Cancer Res. 73, 756-766
49. Bostjancic, E., Zidar, N., and Glavac, D. (2009) MicroRNA microarray expression profiling in human myocardial infarction. Dis. Markers 27, 255-268
50. Zhou, L., Qi, X., Potashkin, J. A., Abdul-Karim, F. W., and Gorodeski, G. I. (2008) MicroRNAs miR-186 and miR-150 down-regulate expression of the pro-apoptotic purinergic P2X7 receptor by activation of instability sites at the 3-untranslated region of the gene that decrease steady-state levels of the transcript. J. Biol. Chem. 283, 28274-28286
51. Adams, D. J., van der Weyden, L., Kovacic, A., Lovicu, F. J., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Ioannou, P. A., and Morris, B. J. (2000) Chromosome localization and characterization of the mouse and human zinc finger protein 265 gene. Cytogenet. Cell Genet. 88, 68-73
52. Adams, D. J., van der Weyden, L., Mayeda, A., Stamm, S., Morris, B. J., and Rasko, J. E. (2001) ZNF265-a novel spliceosomal protein able to induce alternative splicing. J. Cell Biol. 154, 25-32
53. Park, S. J., Huh, J. W., Kim, Y. H., Kim, H. S., and Chang, K. T. (2012) Intron Retention and TE Exonization Events in ZRANB2. Comp. Funct. Genomics 2012, 170208