Mutant DMPK 3′-UTR transcripts disrupt C2C12 myogenic differentiation by compromising MyoD

Journal of Cell Biology

Volumn 159, Issue 3, 2002, Pages 419-429

  Amack, Jeffrey D ^a,c   Reagan, Shannon R ^a   Mahadevan, Mani S ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

Differentiation; Muscle development; MyoD; Myotonic dystrophy; Trinucleotide repeats

Indexed keywords

MYOD PROTEIN; MYOTONIC DYSTROPHY PROTEIN KINASE; PROTEIN KINASE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; E BOX ELEMENT; GENE MUTATION; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; MYOTONIC DYSTROPHY; NONHUMAN; PRIORITY JOURNAL;

3' UNTRANSLATED REGIONS; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MODELS, BIOLOGICAL; MUSCLE PROTEINS; MUTATION; MYOBLASTS; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; MYOGENIN; MYOTONIC DYSTROPHY; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; RNA; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 0037064571     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200206020     Document Type: Article

References (54)

1. Amack, J.D., and M.S. Mahadevan. 2001. The myotonic dystrophy expanded CUG repeat tract is necessary but not sufficient to disrupt C2C12 myoblast differentiation. Hum. Mol. Genet. 10:1879-1887.
2. Amack, J.D., A.P. Paguio, and M.S. Mahadevan. 1999. Cis and trans effects of the myotonic dystrophy (DM) mutation in a cell culture model. Hum. Mol. Genet. 8:1975-1984.
3. Andres, V., and K. Walsh. 1996. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J. Cell Biol. 132:657-666.
4. Betgstrom, D.A., B.H. Penn, A. Strand, R.L. Perry, M.A. Rudnicki, and S.J. Tapscott. 2002. Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol. Cell. 9:587-600.
5. Blau, H.M., C.P. Chiu, and C. Webster. 1983. Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell. 32:1171-1180.
6. Brook, J.D., M.E. McCurrach, H.G. Harley, A.J. Bucklet, D. Church, H. Aburatani, K. Hunter, V.P. Stanton, J.P. Thirion, T. Hudson, et al. 1992. Molecular basis of myotonic dystrophy: Expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell. 69:385.
7. Cornelison, D.D., B.B. Olwin, M.A. Rudnicki, and B.J. Wold. 2000. MyoD(-/-) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev. Biol. 224:122-137.
8. Davis, B.M., M.E. McCurrach, K.L. Taneja, R.H. Singer, and D.E. Housman. 1997. Expansion of a CUG trinucleotide repeat in the 3' untranslated region of myotonic dystrophy protein kinase transcripts results in nuclear retention of transcripts. Proc. Natl. Acad. Sci. USA. 94:7388-7393.
9. Fardaei, M., K. Larkin, J.D. Brook, and M.G. Harnshere. 2001. In vivo co-localisation of MBNL protein with DMPK expanded-repeat transcripts. Nucleic Acids Res. 29:2766-2771.
10. Fardaei, M., M.T. Rogers, H.M. Thorpe, K. Larkin, M.G. Hamshere, P.S. Harper, and J.D. Brook. 2002. Three proteins, MBNL, MBLL and MBXL, co-localize in vivo with nuclear foci of expanded-repeat transcripts in DM1 and DM2 cells. Hum. Mol. Genet. 11:805-814.
11. Farkas-Bargeton, E., J.P. Barbet, S. Dancea, R. Wehrle, A. Checouri, and O. Dulac. 1988. Immaturity of muscle fibers in the congenital form of myotonic dystrophy: Its consequences and its origin. J. Neurol. Sci. 83:145-159.
12. Fu, Y.H., A. Pizzuti, R.G. Fenwick, Jr., J. King, S. Rajnarayan, P.W. Dunne, J. Dubel, G.A. Nasser, T. Ashizawa, P. de Jong, et al. 1992. An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science. 255:1256-1258.
13. Furling, D., L. Coiffier, V. Mouly, J.P. Barber, J.L. St Guily, K. Taneja, G. Gourdon, C. Junien, and G.S. Buder-Browne. 2001. Defective satellite cells in congenital myotonic dystrophy. Hum. Mol. Genet. 10:2079-2087.
14. Halevy, O., B.G. Novitch, D.B. Spicer, S.X. Skapek, J. Rhee, G.J. Hannon, D. Beach, and A.B. Lassar. 1995. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science. 267:1018-1021.
15. Harper, P.S. 1989. Myotonic Dystrophy. Second edition. W.B. Saunders Co., London. 384 pp.
16. Harvey, B., M.D. Satnat, W. Shirley, M.D. Silbert. 1976. Maturational artest of fetal muscle in neonatal myotonic dystrophy. Arch. Neurol. 33:466-474.
17. Hasty, P., A. Bradley, J.H. Morris, D.G. Edmondson, J.M. Venuti, E.N. Olson, and W.H. Klein. 1993. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature. 364:501-506.
18. Hollenberg, S.M., P.F. Cheng, and H. Weinttaub. 1993. Use of a conditional MyoD transcription factor in studies of MyoD trans-activation and muscle determination. Proc. Natl. Acad. Sci. USA. 90:8028-8032.
19. Katagiri, T., S. Akiyama, M. Namiki, M. Komaki, A. Yamaguchi, V. Rosen, J.M. Wozney, A. Fujisawa-Sehara, and T. Suda. 1997. Bone morphogenetic protein-2 inhibits terminal differentiation of myogenic cells by suppressing the transcriptional activity of MyoD and myogenin. Exp. Cell Res. 230:342-351.
20. Kitzmann, M., G. Carnac, M. Vandromme, M. Primig, N.J. Lamb, and A. Fernandez. 1998. The muscle regulatory factors MyoD and myf-5 undergo distinct cell cycle-specific expression in muscle cells. J. Cell Biol. 142:1447-1459.
21. Kitzmann, M., M. Vandromme, V. Schaeffer, G. Carnac, J.C. Labbe, N. Lamb, and A. Fernandez. 1999. Cdk1- and cdk2-mediated phosphorylation of MyoD Ser200 in growing C2 myoblasts: Role in modulating MyoD half-life and myogenic activity. Mol. Cell. Biol. 19:3167-3176.
22. Lassar, A.B., J.N. Buskin, D. Lockshon, R.L. Davis, S. Apone, S.D. Hauschka, and H. Weintraub. 1989. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell. 58:823-831.
23. Lindon, C., D. Montarras, and C. Pinset. 1998. Cell cycle-regulated expression of the muscle determination factor Myf5 in proliferating myoblasts. J. Cell Biol. 140:111-118.
24. Liquoti, C.L., K. Ricker, M.L. Moseley, J.F. Jacobsen, W. Kress, S.L. Naylor, J.W. Day, and L.P. Ranum. 2001. Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9. Science. 293:864-867.
25. Lu, X., N.A. Timchenko, and L.T. Timchenko. 1999. Cardiac elav-type RNA-binding protein (ETR-3) binds to RNA CUG repeats expanded in myotonic dystrophy. Hum. Mol. Genet. 8:53-60.
26. Mahadevan, M., C. Tsilfidis, L. Sabourin, G. Shutlet, C. Amemiya, G. Jansen, C. Neville, M. Narang, J. Barcelo, K. O'Hoy, et al. 1992. Myotonic dystrophy mutation: An unstable CTG repeat in the 3' untranslated region of the gene. Science. 255:1253-1255.
27. Mankodi, A., E. Logigian, L. Callahan, C. McClain, R. White, D. Henderson, M. Krym, and C.A. Thornton. 2000. Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science. 289:1769-1773.
28. Mankodi, A., C.R. Urbinati, Q.P. Yuan, R.T. Moxley, V. Sansone, M. Krym, D. Henderson, M. Schalling, M.S. Swanson, and C.A. Thornton. 2001. Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2. Hum. Mol. Genet. 10:2165-2170.
29. Miller, J.W., C.R. Urbinati, P. Teng-Umnuay, M.G. Stenbetg, B.J. Byrne, C.A. Thornton, and M.S. Swanson. 2000. Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J. 19:4439-4448.
30. Montarras, D., F. Aurade, T. Johnson, J. Ilan, F. Gros, and C. Pinset. 1996. Autonomous differentiation in the mouse myogenic cell line, C2, involves a mutual positive control between insulin-like growth factor II and MyoD, operating as early as at the myoblast stage. J. Cell Sci. 109:551-560.
31. Nabeshima, Y., K. Hanaoka, M. Hayasaka, E. Esumi, S. Li, and I. Nonaka. 1993. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature. 364:532-535.
32. Philips, A.V., L.T. Timchenko, and T.A. Cooper. 1998. Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science. 280:737-741.
33. Puri, P.L., and V. Sartorelli. 2000. Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. J. Cell. Physiol. 185:155-173.
34. Rudnicki, M.A., and R. Jaenisch. 1995. The MyoD family of transcription factors and skeletal myogenesis. Bioessays. 17:203-209.
35. Rudnicki, M.A., P.N. Schnegelsberg, R.H. Stead, T. Braun, H.H. Arnold, and R. Jaenisch. 1993. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell. 75:1351-1359.
36. Sabourin, L.A., A. Girgis-Gabardo, P. Seale, A. Asakura, and M.A. Rudnicki. 1999. Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle. J. Cell Biol. 144:631-643.
37. Savkur, R.S., A.V. Philips, and T.A. Cooper. 2001. Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat. Genet. 29:40-47.
38. Song, A., Q. Wang, M.G. Goebl, and M.A. Harrington. 1998. Phosphorylation of nuclear MyoD is required for its rapid degradation. Mol. Cell. Biol. 18:4994-4999.
39. Taneja, K.L., M. McCurrach, M. Schalling, D. Housman, and R.H. Singer. 1995. Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues. J. Cell Biol. 128:995-1002.
40. Tapscott, S.J., and C.A. Thornton. 2001. Biomedicine. Reconstructing myotonic dystrophy. Science. 293:816-817.
41. Tapscott, S.J., M.J. Thayet, and H. Weintraub. 1993. Deficiency in rhabdomyosarcomas of a factor required for MyoD activity and myogenesis. Science. 259:1450-1453.
42. Tedesco, D., M. Caruso, L. Fischer-Fantuzzi, and C. Vesco. 1995. The inhibition of cultured myoblasr differentiation by the simian virus 40 large T antigen occurs after myogenin expression and Rb up-regulation and is not exerted by transformation-competent cytoplasmic mutants. J Virol. 69:6947-6957.
43. Tian, B., R.J. White, T. Xia, S. Welle, D.H. Turner, M.B. Mathews, and C.A. Thornton. 2000. Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR. RNA. 6:79-87.
44. Timchenko, L.T., J.W. Miller, N.A. Timchenko, D.R. DeVore, K.V. Datar, L. Lin, R. Roberts, C.T. Caskey, and M.S. Swanson. 1996. Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucleic Acids Res. 24:4407-4414.
45. Timchenko, N.A., A.L. Welm, X. Lu, and L.T. Timchenko. 1999. CUG repeat binding protein (CUGBP1) interacts with the 5' region of C/EBPβ mRNA and regulates translation of C/EBPβ isoforms. Nucleic Acids Res. 27:4517-4525.
46. Timchenko, N.A., P. Iakova, Z.J. Cai, J.R. Smith, and L.T. Timchenko. 2001. Molecular basis for impaired muscle differentiation in myotonic dystrophy. Mol. Cell. Biol. 21:6927-6938.
47. Tiscornia, G., and M.S. Mahadevan. 2000. Myotonic dystrophy: The role of the CUG triplet repeats in splicing of a novel DMPK exon and altered cytoplasmic DMPK mRNA isoform ratios. Mol. Cell. 5:959-967.
48. Wang, B.C., W.S. Kennan, J. Yasukawa-Barnes, M.J. Lindstrom, and M.N. Gould. 1991. Carcinoma induction following direct in situ transfer of v-Ha-ras into rat mammary epithelial cells using replication-defective retrovirus vectors. Cancer Res. 51:2642-2648.
49. Wei, Q., and B.M. Paterson. 2001. Regulation of MyoD function in the dividing myoblast. FEBS Lett. 490:171-178.
50. Weintraub, H. 1993. The MyoD family and myogenesis: Redundancy, networks, and thresholds. Cell. 75:1241-1244.
51. Weintraub, H., S.J. Tapscott, R.L. Davis, M.J. Thayer, M.A. Adam, A.B. Lassar, and A.D. Millet. 1989. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc. Natl. Acad. Sci. USA. 86:5434-5438.
52. Weintraub, H., R. Davis, D. Lockshon, and A. Lassar. 1990. MyoD binds cooperatively to two sites in a target enhancer sequence: Occupancy of two sites is required for activation. Proc. Natl. Acad. Sci. USA. 87:5623-5627.
53. Yaffe, D., and O. Saxel. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 270:725-727.
54. Yee, S.P., and P.W. Rigby. 1993. The regulation ofmyogenin gene expression during the embryonic development of the mouse. Genes Dev. 7:1277-1289.