Progressive skeletal muscle weakness in transgenic mice expressing CTG expansions is associated with the activation of the ubiquitin-proteasome pathway

Neuromuscular Disorders

Volumn 20, Issue 5, 2010, Pages 319-325

  Vignaud, Alban ^a,b,c   Ferry, Arnaud ^b,c,d   Huguet, Aline ^e   Baraibar, Martin ^a   Trollet, Capucine ^a,b,c   Hyzewicz, Janek ^a   Butler Browne, Gillian ^a,b,c   Puymirat, Jack ^f   Gourdon, Genevieve ^e   Furling, Denis ^a,b,c  

^a SORBONNE UNIVERSITÉ   (France)

^b Sorbonne Université   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e INSERM   (France)

^f UNIVERSITÉ LAVAL   (Canada)

Author keywords

CTG repeat; DMPK gene; Myotonic dystrophy; Transgenic mouse

Indexed keywords

ATROGIN 1; PROTEASOME; UBIQUITIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION; GRIP STRENGTH; HETEROZYGOSITY; IMMUNOHISTOCHEMISTRY; MOUSE; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE MASS; MUSCLE WEAKNESS; MYOTONIC DYSTROPHY; MYOTONIC DYSTROPHY TYPE 1; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENE; TRINUCLEOTIDE REPEAT;

AGE FACTORS; ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HAND STRENGTH; HUMANS; LAMININ; MICE; MICE, TRANSGENIC; MUSCLE PROTEINS; MUSCLE STRENGTH; MUSCLE WEAKNESS; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; MYOTONIC DYSTROPHY; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; STATISTICS, NONPARAMETRIC; TRINUCLEOTIDE REPEAT EXPANSION; UBIQUITIN;

EID: 77952011880     PISSN: 09608966     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nmd.2010.03.006     Document Type: Article

References (41)

1. Fu Y.H., Pizzuti A., Fenwick R.G., et al. An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 1992, 255:1256-1258.
2. Brook J.D., McCurrach M.E., Harley H.G., 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 1992, 68:799-808.
3. Mahadevan M., Tsilfidis C., Sabourin L., et al. Myotonic dystrophy mutation: an unstable CTG repeat in the 3′ untranslated region of the gene. Science 1992, 255:1253-1255.
4. Hunter A., Tsilfidis C., Mettler G., et al. The correlation of age of onset with CTG trinucleotide repeat amplification in myotonic dystrophy. J Med Genet 1992, 29:774-779.
5. Tsilfidis C., MacKenzie A.E., Mettler G., Barcelo J., Korneluk R.G. Correlation between CTG trinucleotide repeat length and frequency of severe congenital myotonic dystrophy. Nat Genet 1992, 1:192-195.
6. Anvret M., Ahlberg G., Grandell U., Hedberg B., Johnson K., Edstrom L. Larger expansions of the CTG repeat in muscle compared to lymphocytes from patients with myotonic dystrophy. Hum Mol Genet 1993, 2:1397-1400.
7. Thornton C.A., Johnson K., Moxley R.T. Myotonic dystrophy patients have larger CTG expansions in skeletal muscle than in leukocytes. Ann Neurol 1994, 35:104-107.
8. Davis B.M., McCurrach M.E., Taneja K.L., Singer R.H., Housman D.E. 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 1997, 94:7388-7393.
9. Taneja K.L., McCurrach M., Schalling M., Housman D., Singer R.H. Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues. J Cell Biol 1995, 128:995-1002.
10. Day J.W., Ranum L.P. RNA pathogenesis of the myotonic dystrophies. Neuromuscul Disord 2005, 15:5-16.
11. Mankodi A., Teng-Umnuay P., Krym M., Henderson D., Swanson M., Thornton C.A. Ribonuclear inclusions in skeletal muscle in myotonic dystrophy types 1 and 2. Ann Neurol 2003, 54:760-768.
12. Osborne R.J., Thornton C.A. RNA-dominant diseases. Hum Mol Genet 2006, 15(Spec No. 2):R162-R169.
13. Charlet B.N., Savkur R.S., Singh G., Philips A.V., Grice E.A., Cooper T.A. Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol Cell 2002, 10:45-53.
14. Mankodi A., Takahashi M.P., Jiang H., et al. Expanded CUG repeats trigger aberrant splicing of ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol Cell 2002, 10:35-44.
15. Yadava R.S., Frenzel-McCardell C.D., Yu Q., et al. RNA toxicity in myotonic muscular dystrophy induces NKX2-5 expression. Nat Genet 2008, 40:61-68.
16. Harper P.S. Myotonic dystrophy, third edn. 2001, WB Saunder, London.
17. Belanger A.Y., McComas A.J. Contractile properties of muscles in myotonic dystrophy. J Neurol Neurosurg Psychiatry 1983, 46:625-631.
18. Taylor R.G., Abresch R.T., Lieberman J.S., Fowler W.M., Entrikin R.K. In vivo quantification of muscle contractility in humans: healthy subjects and patients with myotonic muscular dystrophy. Arch Phys Med Rehabil 1992, 73:233-236.
19. Grimby G., Hedberg M., Henriksson K.G., et al. Muscle function and morphology in myotonic dystrophy. Acta Med Scand 1988, 224:349-356.
20. Seznec H., Agbulut O., Sergeant N., et al. Mice transgenic for the human myotonic dystrophy region with expanded CTG repeats display muscular and brain abnormalities. Hum Mol Genet 2001, 10:2717-2726.
21. Gourdon G., Radvanyi F., Lia A.S., et al. Moderate intergenerational and somatic instability of a 55-CTG repeat in transgenic mice. Nat Genet 1997, 15:190-192.
22. Mankodi A., Logigian E., Callahan L., et al. Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science 2000, 289:1769-1773.
23. Mahadevan M.S., Yadava R.S., Yu Q., et al. Reversible model of RNA toxicity and cardiac conduction defects in myotonic dystrophy. Nat Genet 2006, 38:1066-1070.
24. Wang G.S., Kearney D.L., De Biasi M., Taffet G., Cooper T.A. Elevation of RNA-binding protein CUGBP1 is an early event in an inducible heart-specific mouse model of myotonic dystrophy. J Clin Invest 2007, 117:2802-2811.
25. Vignaud A., Ramond F., Hourde C., Keller A., Butler-Browne G., Ferry A. Diabetes provides an unfavorable environment for muscle mass and function after muscle injury in mice. Pathobiology 2007, 74:291-300.
26. Vignaud A., Fougerousse F., Mouisel E., et al. Genetic inactivation of acetylcholinesterase causes functional and structural impairment of mouse soleus muscles. Cell Tissue Res 2008, 333:289-296.
27. Mendias C.L., Marcin J.E., Calerdon D.R., Faulkner J.A. Contractile properties of EDL and soleus muscles of myostatin-deficient mice. J Appl Physiol 2006, 101:898-905.
28. Butler-Browne G.S., Whalen R.G. Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. Dev Biol 1984, 102:324-334.
29. Kisslev A.F., Goldberg A.L. Monitoring activity and inhibition of 26S proteaosomes with fluotogenic peptides substrates. Methods Enzymol 2005, 398:364-378.
30. Bulteau A.L., Lundberg K.C., Humphries K.M., et al. Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J Biol Chem 2001, 276:30057-30063.
31. Sandri M., Sandri C., Gilbert A., et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004, 117:399-412.
32. Mammucari C., Milan G., Romanello V., et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 2007, 6:458-471.
33. Orengo J.P., Chambon P., Metzger D., Mosier D.R., Snipes G.J., Cooper T.A. Expanded CTG repeats within the DMPK 3′ UTR causes severe skeletal muscle wasting in an inducible mouse model for myotonic dystrophy. Proc Natl Acad Sci USA 2008, 105:2646-2651.
34. Bodine S.C., Latres E., Baumhueter S., et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001, 294:1704-1708.
35. Gomes M., Lecker S., Jagoe R., Navon A., Goldberg A. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 2001, 98:14440-14445.
36. Jagoe R.T., Goldberg A.L. What do we really know about the ubiquitin proteasome pathway in muscle atrophy?. Curr Opin Clin Nutr Metab Care 2001, 4:183-190.
37. Price S.R. Increased transcription of ubiquitin-proteasome system components: molecular responses associated with muscle atrophy. Int J Biochem Cell Biol 2003, 35:617-628.
38. Lecker S.H., Solomon V., Mitch W.E., Goldberg A.L. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J Nutr 1999, 129:227S-237S.
39. Gantelet E., Kraftsik R., Delaloye S., Gourdon G., Kuntzer T., Barakat-Walter I. The expansion of 300 CTG repeats in myotonic dystrophy transgenic mice does not induce sensory or motor neuropathy. Acta Neuropathol 2007, 114:175-185.
40. Guiraud-Dogan C., Huguet A., Gomes-Pereira M., et al. DM1 CTG expansions affect insulin receptor isoforms expression in various tissues of transgenic mice. Biochim Biophys Acta 2007, 1772:1183-1191.
41. Hasselgren P.O. Ubiquitination, phosphorylation, and acetylation-triple threat in muscle wasting. J Cell Physiol 2007, 213:679-689.