Molecular, Physiological, and Motor Performance Defects in DMSXL Mice Carrying >1,000 CTG Repeats from the Human DM1 Locus

PLoS Genetics

Volumn 8, Issue 11, 2012, Pages

  Huguet, Aline ^a   Medja, Fadia ^b   Nicole, Annie ^a   Vignaud, Alban ^b,c   Guiraud Dogan, Céline ^d   Ferry, Arnaud ^b,e   Decostre, Valérie ^b   Hogrel, Jean Yves ^b   Metzger, Friedrich ^f   Hoeflich, Andreas ^g   Baraibar, Martin ^h   Gomes Pereira, Mário ^a   Puymirat, Jack ⁱ   Bassez, Guillaume ^d   Furling, Denis ^b   Munnich, Arnold ^a   Gourdon, Geneviève ^a  

^a IMAGINE INSTITUTE   (France)

^b INSERM   (France)

^c GÉNÉTHON   (France)

^d FACULTÉ DE MÉDECINE   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f F HOFFMANN LA ROCHE LTD   (Switzerland)

^g LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^h SORBONNE UNIVERSITÉ   (France)

ⁱ UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MYOTONIC DYSTROPHY PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; GENE LOCUS; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GROWTH RETARDATION; HISTOPATHOLOGY; HUMAN; MALE; MOTOR PERFORMANCE; MOUSE; MUSCLE STRENGTH; MYOTONIC DYSTROPHY; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; TRINUCLEOTIDE REPEAT;

ANIMALS; CELL NUCLEUS; ENDOPEPTIDASES; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; MYOTONIC DYSTROPHY; PROTEIN-SERINE-THREONINE KINASES; RNA SPLICING; TRINUCLEOTIDE REPEAT EXPANSION;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 84870709348     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003043     Document Type: Article

References (55)

1. Harper PS (2001) Myotonic Dystrophy, 3rd edition; Saunders WB, editor. London Philadelphia.
2. Echenne B, Rideau A, Roubertie A, Sebire G, Rivier F, et al. (2008) Myotonic dystrophy type I in childhood Long-term evolution in patients surviving the neonatal period. Eur J Paediatr Neurol 12: 210-223.
3. Aslanidis C, Jansen G, Amemiya C, Shutler G, Mahadevan M, et al. (1992) Cloning of the essential myotonic dystrophy region and mapping of the putative defect. Nature 355: 548-551.
4. Brook JD, McCurrach ME, Harley HG, Buckler HJ, Church D, 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 68: 799-808.
5. Fu YH, Pizzuti A, Fenwick RG Jr, King J, Rajnarayan S, et al. (1992) An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 255: 1256-1258.
6. Gomes-Pereira M, Cooper TA, Gourdon G, (2011) Myotonic dystrophy mouse models: towards rational therapy development. Trends Mol Med 17: 506-517.
7. Sicot G, Gourdon G, Gomes-Pereira M, (2011) Myotonic dystrophy, when simple repeats reveal complex pathogenic entities: new findings and future challenges. Hum Mol Genet 20: R116-123.
8. Timchenko LT, (1999) Myotonic Dystrophy: the role of RNA CUG triplet repeats. Am J Hum Genet 64: 360-364.
9. Miller JW, Urbinati CR, Teng-Umnuay P, Stenberg MG, Byrne BJ, et al. (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J 19: 4439-4448.
10. Mankodi A, Urbinati CR, Yuan QP, Moxley RT, Sansone V, et al. (2001) Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2. Hum Mol Genet 10: 2165-2170.
11. Fardaei M, Larkin K, Brook JD, Hamshere MG, (2001) In vivo co-localisation of MBNL protein with DMPK expanded-repeat transcripts. Nucleic Acids Res 29: 2766-2771.
12. Charlet BN, Savkur RS, Singh G, Philips AV, Grice EA, et al. (2002) Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol Cell 10: 45-53.
13. Fardaei M, Rogers MT, Thorpe HM, Larkin K, Hamshere MG, et al. (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.
14. Faustino NA, Cooper TA, (2003) Pre-mRNA splicing and human disease. Genes Dev 17: 419-437.
15. Ranum LP, Day JW, (2002) Myotonic dystrophy: clinical and molecular parallels between myotonic dystrophy type 1 and type 2. Curr Neurol Neurosci Rep 2: 465-470.
16. Cho DH, Thienes CP, Mahoney SE, Analau E, Filippova GN, et al. (2005) Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol Cell 20: 483-489.
17. Zu T, Gibbens B, Doty NS, Gomes-Pereira M, Huguet A, et al. (2011) Non-ATG-initiated translation directed by microsatellite expansions. Proc Natl Acad Sci U S A 108: 260-265.
18. Seznec H, Lia-Baldini AS, Duros C, Fouquet C, Lacroix C, et al. (2000) Transgenic mice carrying large human genomic sequences with expanded CTG repeat mimic closely the DM CTG repeat intergenerational and somatic instability. Hum Mol Genet 9: 1185-1194.
19. Gourdon G, Radvanyi F, Lia AS, Duros C, Blanche M, et al. (1997) Moderate instability of a 55 CTG repeat in transgenic mice carrying a 45 kb genomic region from an affected DM patient. Nat Genet 15: 190-192.
20. Lia AS, Seznec H, Hofmann-Radvanyi H, Radvanyi F, Duros C, et al. (1998) Somatic instability of the CTG repeat in mice transgenic for the myotonic dystrophy region is age dependent but not correlated to the relative intertissue transcription levels and proliferative capacities. Hum Mol Genet 7: 1285-1291.
21. Panaite PA, Gantelet E, Kraftsik R, Gourdon G, Kuntzer T, et al. (2008) Myotonic dystrophy transgenic mice exhibit pathologic abnormalities in diaphragm neuromuscular junctions and phrenic nerves. J Neuropathol Exp Neurol 67: 763-772.
22. Vignaud A, Ferry A, Huguet A, Baraibar M, Trollet C, et al. (2010) Progressive skeletal muscle weakness in transgenic mice expressing CTG expansions is associated with the activation of the ubiquitin-proteasome pathway. Neuromuscul Disord 20: 319-325.
23. Gomes-Pereira M, Foiry L, Nicole A, Huguet A, Junien C, et al. (2007) CTG trinucleotide repeat "big jumps": large expansions, small mice. PLoS Genet 3: e52 doi:10.1371/journal.pgen.0030052.
24. Seznec H, Agbulut O, Sergeant N, Savouret C, Ghestem A, et al. (2001) Mice transgenic for the human myotonic dystrophy region with expanded CTG repeats display muscular and brain abnormalities. Hum Mol Genet 10: 2717-2726.
25. Guiraud-Dogan C, Huguet A, Gomes-Pereira M, Brisson E, Bassez G, et al. (2007) DM1 CTG expansions affect insulin receptor isoforms expression in various tissues of transgenic mice. Biochim Biophys Acta 1772: 1183-1191.
26. Wojciechowska M, Krzyzosiak WJ, (2011) Cellular toxicity of expanded RNA repeats: focus on RNA foci. Hum Mol Genet 20: 3811-3821.
27. Hsu RJ, Hsiao KM, Lin MJ, Li CY, Wang LC, et al. (2011) Long tract of untranslated CAG repeats is deleterious in transgenic mice. PLoS ONE 6: e16417 doi:10.1371/journal.pone.0016417.
28. Wheeler TM, Lueck JD, Swanson MS, Dirksen RT, Thornton CA, (2007) Correction of ClC-1 splicing eliminates chloride channelopathy and myotonia in mouse models of myotonic dystrophy. J Clin Invest 117: 3952-3957.
29. Filippova GN, Thienes CP, Penn BH, Cho DH, Hu YJ, et al. (2001) CTCF-binding sites flank CTG/CAG repeats and form a methylation-sensitive insulator at the DM1 locus. Nat Genet 28: 335-343.
30. Orengo JP, Ward AJ, Cooper TA, (2011) Alternative splicing dysregulation secondary to skeletal muscle regeneration. Ann Neurol 69: 681-690.
31. Mulders SA, van Engelen BG, Wieringa B, Wansink DG, (2010) Molecular therapy in myotonic dystrophy: focus on RNA gain-of-function. Hum Mol Genet 19: R90-97.
32. Orengo JP, Cooper TA, (2007) Alternative splicing in disease. Adv Exp Med Biol 623: 212-223.
33. Charizanis K, Lee KY, Batra R, Goodwin M, Zhang C, et al. (2012) Muscleblind-Like 2 Mediated Alternative Splicing in the Developing Brain and Dysregulation in Myotonic Dystrophy. Neuron 75: 437-450.
34. Duan C, Ren H, Gao S, (2010) Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: roles in skeletal muscle growth and differentiation. Gen Comp Endocrinol 167: 344-351.
35. Gomez-Saez JM, Fernandez-Real JM, Navarro MA, Martinez-Matos JA, Soler J, (1993) GH secretion status in myotonic dystrophy. Psychoneuroendocrinology 18: 183-190.
36. Moxley RT, Corbett AJ, Minaker KL, Rowe JW, (1984) Whole body insulin resistance in myotonic dystrophy. Ann Neurol 15: 157-162.
37. Heatwole CR, Eichinger KJ, Friedman DI, Hilbert JE, Jackson CE, et al. (2011) Open-label trial of recombinant human insulin-like growth factor 1/recombinant human insulin-like growth factor binding protein 3 in myotonic dystrophy type 1. Arch Neurol 68: 37-44.
38. Cote C, Hiba B, Hebert LJ, Vial C, Remec JF, et al. (2011) MRI of tibialis anterior skeletal muscle in myotonic dystrophy type 1. Can J Neurol Sci 38: 112-118.
39. Perseghin G, Comola M, Scifo P, Benedini S, De Cobelli F, et al. (2004) Postabsorptive and insulin-stimulated energy and protein metabolism in patients with myotonic dystrophy type 1. Am J Clin Nutr 80: 357-364.
40. Panaite PA, Kielar M, Kraftsik R, Gourdon G, Kuntzer T, et al. (2011) Peripheral neuropathy is linked to a severe form of myotonic dystrophy in transgenic mice. J Neuropathol Exp Neurol 70: 678-685.
41. Holt I, Jacquemin V, Fardaei M, Sewry CA, Butler-Browne GS, et al. (2009) Muscleblind-like proteins: similarities and differences in normal and myotonic dystrophy muscle. Am J Pathol 174: 216-227.
42. Hoeflich A, Wu M, Mohan S, Foll J, Wanke R, et al. (1999) Overexpression of insulin-like growth factor-binding protein-2 in transgenic mice reduces postnatal body weight gain. Endocrinology 140: 5488-5496.
43. Metzger F, Sajid W, Saenger S, Staudenmaier C, van der Poel C, et al. (2011) Separation of fast from slow anabolism by site-specific PEGylation of insulin-like growth factor I (IGF-I). J Biol Chem 286: 19501-19510.
44. Kisselev AF, Goldberg AL, (2005) Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol 398: 364-378.
45. Carrard G, Dieu M, Raes M, Toussaint O, Friguet B, (2003) Impact of ageing on proteasome structure and function in human lymphocytes. Int J Biochem Cell Biol 35: 728-739.
46. Ridgley JA, Pinniger GJ, Hamer PW, Grounds MD, (2009) The physiological effects of IGF-1 (class 1:Ea transgene) over-expression on exercise-induced damage and adaptation in dystrophic muscles of mdx mice. Pflugers Arch 457: 1121-1132.
47. Roche JA, Lovering RM, Bloch RJ, (2008) Impaired recovery of dysferlin-null skeletal muscle after contraction-induced injury in vivo. Neuroreport 19: 1579-1584.
48. Gorselink M, Drost MR, de Louw J, Willems PJ, Rosielle N, et al. (2000) Accurate assessment of in situ isometric contractile properties of hindlimb plantar and dorsal flexor muscle complex of intact mice. Pflugers Arch 439: 665-670.
49. Moyer M, Berger DS, Ladd AN, Van Lunteren E, (2011) Differential susceptibility of muscles to myotonia and force impairment in a mouse model of myotonic dystrophy. Muscle Nerve 43: 818-827.
50. Fuchtbauer EM, Reininghaus J, Jockusch H, (1988) Developmental control of the excitability of muscle: transplantation experiments on a myotonic mouse mutant. Proc Natl Acad Sci U S A 85: 3880-3884.
51. Agbulut O, Vignaud A, Hourde C, Mouisel E, Fougerousse F, et al. (2009) Slow myosin heavy chain expression in the absence of muscle activity. Am J Physiol Cell Physiol 296: C205-214.
52. Ward AJ, Rimer M, Killian JM, Dowling JJ, Cooper TA, (2010) CUGBP1 overexpression in mouse skeletal muscle reproduces features of myotonic dystrophy type 1. Hum Mol Genet 19: 3614-3622.
53. Lin X, Miller JW, Mankodi A, Kanadia RN, Yuan Y, et al. (2006) Failure of MBNL1-dependent post-natal splicing transitions in myotonic dystrophy. Hum Mol Genet 15: 2087-2097.
54. Mankodi A, Takahashi MP, Jiang H, Beck CL, Bowers WJ, et al. (2002) Expanded CUG repeats trigger aberrant splicing of ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol Cell 10: 35-44.
55. Futatsugi A, Kuwajima G, Mikoshiba K, (1995) Tissue-specific and developmentally regulated alternative splicing in mouse skeletal muscle ryanodine receptor mRNA. Biochem J 305 (Pt 2) (): 373-378.