Mice lacking the myotonic dystrophy protein kinase develop a late onset progressive myopathy

Nature Genetics

Volumn 13, Issue 3, 1996, Pages 325-335

  Reddy, Sita ^a,e   Smith, Daniel B J ^b   Rich, Mark M ^b   Leferovich, John M ^b   Reilly, Patricia ^a   Davis, Brigid M ^a   Tran, Khoa ^a   Rayburn, Helen ^a   Bronson, Roderick ^c   Cros, Didier ^d   Balice Gordon, Rita J ^b   Housman, David ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c TUFTS UNIVERSITY   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MESSENGER RNA; PROTEIN KINASE;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROMYOGRAPHY; FORCE; IMMUNOHISTOCHEMISTRY; INNERVATION; MOUSE; MUSCLE CELL; MUSCLE FATIGUE; MUSCLE REGENERATION; MYOPATHY; MYOTONIC DYSTROPHY; NERVE CONDUCTION; NEUROMUSCULAR SYNAPSE; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; ULTRASTRUCTURE;

ANIMALS; ELECTROMYOGRAPHY; FEMALE; HOMOZYGOTE; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE FATIGUE; MUSCLE FIBERS; MUSCLE, SKELETAL; MUTATION; MYOTONIC DYSTROPHY; PROTEIN-SERINE-THREONINE KINASES; REGENERATION;

EID: 8944259903     PISSN: 10614036     EISSN: None     Source Type: Journal    
DOI: 10.1038/ng0796-325     Document Type: Article

References (78)

1. Harper, P.S. in Myotonic Dystrophy. 2nd. ed. (W.B. Saunders, 1989).
2. Howeler, C.J., Busch, H.F., Geraedts, J.P., Niermeijer, M.F. & Staal, A. Anticipation in myotonic dystrophy: Fact or fiction? Brain 112, 779-797 (1989).
3. O'Brien, T. & Harper, P.S. Course, prognosis and complications of childhood-onset myotonic dystrophy. Dev. Med. Child. Neurol. 26, 62-67 (1984).
4. Brook, J.D. et al. 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 68, 799-808 (1992).
5. Fu, Y-H. et al. An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 255, 1256-1258 (1992).
6. Mahadevan, M. et al. Myotonic dystrophy mutation: an unstable CTG repeat in the 3′ untranslated region of the gene. Science 255, 1253-1255 (1992).
7. Harley, H. et al. Size of the unstable CTG repeat sequence in relation to phenotype and parental transmission in myotonic dystrophy. Am. J. Hum. Genet. 52, 1164-1174 (1993).
8. La Spada, A.R., Wilson, E.M., Lubahn, D.B., Harding, A.E. & Fishbeck, K.H. Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 352, 77-79 (1991).
9. Verkerk, A.J.M.H. et al. Identification of a gene (FMR-1) containing a CGG repeat coincident with a fragile X breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 65, 905-914 (1991).
10. The Huntington's Disease Research Group. A novel gene encoding a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosome. Cell 72, 971-983 (1993).
11. Knight, S.J. et al. Trinucleotide repeat amplification and hypermethylation of a CpG island in FRAXE mental retardation. Cell 74, 127-134 (1993).
12. Orr, H.T. et al. Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1. Nature Genet. 4, 221-226 (1993).
13. Burke, J.R. et al. The Haw River syndrome: dentatorubropallidoluysian atrophy (DRPLA) in an African-American family. Nature Genet 7, 521-524 (1994).
14. Koide, R. et al. Unstable expansion of CAG repeat in hereditary dentatorubralpallidoluysian atrophy (DRPLA). Nature Genet. 61994).
15. Nancarrow, J.K. et al. Implications of FRA 16A structure for the mechanism of chromosomal fragile site genesis. Science 264, 1938-1941 (1994).
16. Pleretti, M. et al. Absence of expression of the FMR-1 gene in fragile X syndrome. Cell 66, 817-822 (1991).
17. Feng, Y. et al. Translational supression by trinucleotide repeat at FMR1. Science 268, 731-734 (1995).
18. Housman, D. Gain of glutamines, gain of function. Nature Genet. 10, 3-4 (1995).
19. Fu, Y.-H. et al. Decreased expression of myotonin-protein kinase messenger RNA and protein in adult form of myotonic dystrophy. Science 260, 235-237 (1993).
20. Sabouri, L.A. et al. Effect of the myotonic dystrophy (DM) mutation on mRNA levels of the DM gene. Nature Genet. 4, 233-238 (1993).
21. Carango, P., Noble, J.E., Marks, H.G. & Funanage, V.L. Absence of myotonic dystrophy protein kinase (DMPK) mRNA as a result of a triplet repeat expansion in myotonic dystrophy. Genomics 18, 340-348 (1993).
22. Hofmann-Radvanyi, H. et al. Myotonic dystrophy: Absence of CTG enlarged transcript in congenital forms and low expression of the normal allele. Hum. Mol. Genet. 2, 1263-1267 (1993).
23. Novelli, G. et al. Failure in detecting mRNA transcripts from the mutated allele in myotonic dystrophy muscle. Biochem. Med. Metabol. Biol. 50, 85-92 (1993).
24. Koga, R. et al. Decreased myotonin-protein kinase in skeletal and cardiac muscles in myotonic dystrophy. Biochem. Biophys. Res, Commun. 202, 577-585 (1994).
25. Krahe, R. et al. Effect of myotonic dystrophy trinucleotide repeat expansion on DMPK transcription and processing. Genomics 28 (1995).
26. Wang, J. et al. Myotonic dystrophy: evidence for a possible dominant-negative RNA mutation. Hum. Mol. Gen. 4, 599-606 (1995).
27. Maeda, M. et al. Identification, tissue-specific expression, and subcellular localization of the 80 and 71 kDa forms of myotonic dystrophy kinase protein. J. Biol. Chem. 270, 20246-20249 (1995).
28. Jansen, G. et al. Characterization of the myotonic dystrophy region predicts multiple protein isoform-encoding mRNAs. Nature Genet. 1, 261-266 (1992).
29. Mahadevan, M.S. et al. Structure and genomic sequence of the myotonic dystrophy (DM kinase) Gene 2, 299-304 (1993).
30. Kamps, M.P., Taylor, S.S. & Sefton, B.M. Direct evidence that oncogenic tyrosine kinases and cyclic AMP-dependent protein kinases have homologous ATP binding sites. Nature 310, 589-592 (1984).
31. Hanks, S.K., Quinn, A.M. & Hunter, T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42-52 (1988).
32. Sacco, P., Jones, D.A., Dick, J.R.T. & Vrbova, G. Contractile properties and susceptibility to exercise induced damage of normal and mdx tibialis anterior muscle. Clin. Sci. 82, 227-336 (1992).
33. Burke, R.E. Physiology of Motor Units in Myology 2nd. ed. (eds. Andrew G. Engel & Clara Franzini-Armstrong) 1, 464-484 (McGraw-Hill Inc., New York 1994).
34. Balice-Gordon, R.J. & Lichtman, J.W. In vivo visualization of the growth of pre and postsynaptic elements of mouse neuromuscular junctions. J. Neurosci. 10, 894-908 (1990).
35. Wernig, A. & Herrera, A.A. Sprouting and remodelling at the nerve-muscle junction. Prog. Neurobiol. 7, 251-291 (1986).
36. Morgan-Hughes, J.A. Mitochondrial diseases in Myology 2nd.ed. (eds. Andrew G. Engel and Clara Franzini-Armstrong) 1610-1660 (McGraw-Hill Inc., New York 1994).
37. Moss, F.P. & Leblond, C.P. Satellite cells as a source of nuclei in muscles of growing rats. Anat. Rec. 170, 421-436 (1970).
38. Campion, D.R. The muscle satellite cell: A review. Int. Rev. Cytol. 87, 225-251 (1984).
39. Grounds, M.D., Garrett, K., Lai, M.C., Wright, W.E. & Beilharz, M.W. Identification of skeletal muscle precursor cells in vivo by use of MyoD and myogenin probes. Cell Tissue Res. 267, 99-104 (1992).
40. Koishi, K., Zhang, M., McLennan, I.S. & Haris, A.J. MyoD protein accumalates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Developmental Dynamics 202, 244-254 (1995).
41. Beilharz, M.W., Lareu, R.R., Garrett, K.L., Grounds, M.D. & Fletcher, S. Quantitation of muscle precursor cell activity in skeletal muscle by northern analysis of MyoD and Myogenin expression: Application to dystrophic (mdx) mouse model. Mol. and Cell. Neurosciences 3, 326-331 (1992).
42. Gambke, B. & Rubinstein, N.A. A monoclonal antibody to embryonic myosin heavy chain of rat skeletal muscle. J. Biol. Chem. 259, 12092-12100 (1984).
43. Bancroft, J.D. & Stevens, A. Theory and Practice of Histological Techniques.(1990).
44. Casanova, G. & Jerusalem, F. Myopathology of myotonic dystrophy. A morphometric study. Acta Neuropathol 45, 231 (1979).
45. Anderson, J.E., Ovalle, W.K. & Bressler, B.H. Electron Microscopic and Autoradiographic Characterization of Hindlimb Muscle Regeneration in mdx Mouse. Anat. Rec. 219, 243-257 (1987).
46. Camwath, J.W. & Shotton, D.M. Muscular dystrophy in the mdx mouse: Histopathology of the soleus and extensor digitorum longus muscles. J. Neurol. Sci. 80, 39-54 (1987).
47. Fitzsimons, R.B. & Hoh, J.F.Y. Embryonic and foetal myosins in human skeletal muscle: the presence of foetal myosins in Duchenne muscular dystrophy and infantile spinal muscular atrophy. J. Neurol. Sci. 52, 367-384 (1981).
48. Karsch-Mizrachi, I., Travis, M., Blau, H. & Leinwald, L.A. Expression and DNA sequence of a human embryonic skeletal muscle myosin heavy chain gene. Nuc. Acids. Res. 17, 6167-6179 (1989).
49. McComas, A.J., Campbell, M.J. & Sica, R.E.P. Electrophysiological study of dystrophica myotonica. J. Neurol. Neurosurg. Psychiat. 34, 132-139 (1971).
50. Belanger, A.Y. & McComas, A.J. Contractile properties of muscles in myotonic dystrphy. J. Neuro Neurosurg. Psychiat. 46, 625-631 (1983).
51. Taylor, R.G., Abresch, R.T., Lieberman, J.S., Fowler, W.MN. & Entrikin, R.K. In vivo quantification of muscle contractility in humans: healthy subjects and patients with myotonic muscular dystrophy. Arch. Pnys. Med. Rehabil. 73, 233-236 (1992).
52. Salvatori, S., Biral, D., Furlan, S. & O., M. Identification and localization of the myotonic dystrophy gene product in skeletal and cardiac muscles. Biochem. Biophys. Res. Commun. 203, 1365-1370 (1994).
53. Dunne, P.W., Ma, L., Casey, D.L., Harati, Y. & Epstein, H.F. Localization of myotonic dystrophy protein kinase in skeletal muscle and its alteration with disease. Cell Motility and the Cytoskeleton 331995).
54. Timchenko, L. et al. Full-length myotonin protein kinase (72 KDa) displays serine kinase activity. Proc. Natl. Acad. Sci. USA 92, 5366-5370 (1995).
55. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A.M. & Sweeny, H.L. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. USA 90, 3710-3714 (1993).
56. Dubowitz, V. Muscle Biopsy 2nd. ed. (W.B. Saunders, 1985).
57. Aleu, F.P. & Afifi, A.K. Ultrastructure of muscle in myotonic dystrophy. Am. J. Pathol. 45, 221-231. (1964).
58. Johnson, A.G. Alteration of the Z lines and I-band myofilaments in human skeletal muscle. Arch Neuropathol (Berlin) 12, 218-226 (1969).
59. Johnson, A.G. & Woolf, A.L. Abnormal sarcolemmal nuclei encountered in several cases of dystrophica myotonica. Acta neuropath. (Berl.) 12, 183-188 (1969).
60. Fardeau, M. Ultrastructural lesions in progressive muscular dystrophies. A critical study of their specificity. In: J.N. Walton, N. Canal and G. Scarlata eds: Muscle Diseases, Amsterdam. Exporta Medica, 98-108 (1970).
61. Schotland, D.L. An electron microscopic investigation of myotonic dystrophy. J. Neuropath. & Exper. Neurol. 29, 241-253 (1970).
62. Bulfield, G., Siller, W.G., Wright, P.A. & Moore, K.J. X-chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. USA 81, 1189-1192 (1984).
63. Rastinjad, F. & Blau, H. Genetic complementation reveals a novel regulatory role for 3′ untranslated region in growth and differentiation. Cell 72, 903-917 (1993).
64. Wang, Y.-H., Amirhaeri, S., Kang, S., Wells, R.D. & Griffith, J.D. Preferential nucleosome assembly at DNA triplet repeats from the myotonic dystrophy gene. Science 265, 1709-1712 (1994).
65. Wang, Y.-H. & Griffith, J. Expanded CTG triplet blocks from the myotonic dystrophy gene create the strongest known natural nucleosome positioning elements. Genomics 25, 570-573 (1995).
66. Boucher, C.A. et al. A novel homeodomain encoding gene is associated with a large CpG island interrupted by the myotonic dystrophy unstable (CTG)n repeat. Hum. Mol. Genet. 4, 1919-1925 (1995).
67. Shaw, D.J. et al. Genomic organization and transcriptional units at the myotonic dystrophy locus. Genomics 18, 673-679 (1993).
68. Tybulewicz, V.L.J., Crawford, C.E., Jackson, P.K., Bronson, R.T. & Mulligan, R.C. Neonatal lethality and lymhopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65, 1153-1163 (1991).
69. Mansour, S.L., Thomas, K.R. & Capecchi, M.R. Disruption of the proto-oncogene int-2 in mouse embryo-derived stem-cells: a general strategy for targeting mutations to nonselectable genes. Nature 336, 348-352 (1988).
70. Laird, P.W. et al. Simplified mammalian DNA isolation procedure. Nucl. Acids Res. 19, 4293 (1991).
71. Hogan, B., Constantini, F. & Lacy, E. Manipulating the Mouse Embryo: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 1986).
72. Davis, R.L., Weintraub, H. & Lassar, A.B. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51, 987-1000 (1987).
73. Braun, T.G. et al. Differential expression of myogenic determination genes in muscle cells: possible autoactivation by the Myf gene products. EMBO J. 8, 3617-3625 (1989).
74. Braun, T., Buschhausan-Denker, G., Bober, E., Tannich, E. & Arnold, H.-H. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO. J. 8, 701-709 (1989).
75. Rhodes, S.J. & Konieczny, S.F. Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev. 3, 2050-2061 (1989).
76. Shackleford, G.M. & Varmus, H.E. Expression of the proto-oncogene int1 is restricted to post meiotic male germ cells and the neural tube of midgestational embryos. Cell 50, 89-95 (1987).
77. Close, K. Dynamic properties of mammalian skeletal muscle. Phys. Rev. 52, 129-197 (1972).
78. Schiaffino, S., Gorza, L., Dones, I., Cornelio, F. & Sartore, S. Fetal myosin immunoreactivity in human dystrophic muscle. Muscle Nerve 9, 51-58 (1986).