Compound loss of muscleblind-like function in myotonic dystrophy

EMBO Molecular Medicine

Volumn 5, Issue 12, 2013, Pages 1887-1900

  Lee, Kuang Yung ^a,b   Li, Moyi ^a   Manchanda, Mini ^a   Batra, Ranjan ^a   Charizanis, Konstantinos ^a   Mohan, Apoorva ^a   Warren, Sonisha A ^a   Chamberlain, Christopher M ^a   Finn, Dustin ^a   Hong, Hannah ^a   Ashraf, Hassan ^a   Kasahara, Hideko ^a   Ranum, Laura P W ^a   Swanson, Maurice S ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Mbnl1; Mbnl2; Muscleblind like; Myotonic dystrophy; RNA mediated disease

Indexed keywords

MBNL1 PROTEIN; MBNL2 PROTEIN; MUSCLE PROTEIN; RNA; UNCLASSIFIED DRUG;

ADULT; ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GRIP STRENGTH; HEART CONDUCTION; HEART MUSCLE CONTRACTILITY; HUMAN; HUMAN TISSUE; MOUSE; MUSCLE WEAKNESS; MYOTONIC DYSTROPHY; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PR INTERVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; QT INTERVAL; RNA PROCESSING; SPLICING DEFECT;

MBNL1; MBNL2; MUSCLEBLIND-LIKE; MYOTONIC DYSTROPHY; RNA-MEDIATED DISEASE;

ANIMALS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; ELECTROCARDIOGRAPHY; KAPLAN-MEIER ESTIMATE; LONGEVITY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSATELLITE REPEATS; MUSCLE, SKELETAL; MYOCARDIUM; MYOTONIC DYSTROPHY; RNA SPLICING; RNA-BINDING PROTEINS;

EID: 84896959065     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201303275     Document Type: Article

References (63)

1. Chamberlain CM, Ranum LP (2012) Mouse model of muscleblind-like 1 overexpression: Skeletal muscle effects and therapeutic promise. Hum Mol Genet 21: 4645-4654
2. Charizanis K, Lee KY, Batra R, Goodwin M, Zhang C, Yuan Y, Shiue L, Cline M, Scotti MM, Xia G et al (2012) Muscleblind-like 2-mediated alternative splicing in the developing brain and dysregulation in myotonic dystrophy. Neuron 75: 437-450
3. Du H, Cline MS, Osborne RJ, Tuttle DL, Clark TA, Donohue JP, Hall MP, Shiue L, Swanson MS, Thornton CA et al (2010) Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat Struct Mol Biol 17: 187-193
4. Fugier C, Klein AF, Hammer C, Vassilopoulos S, Ivarsson Y, Toussaint A, Tosch V, Vignaud A, Ferry A, Messaddeq N et al (2011) Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy. Nat Med 17: 720-725
5. Gehman LT, Meera P, Stoilov P, Shiue L, O'Brien JE, Meisler MH, Ares M, Jr., Otis TS, Black DL (2012) The splicing regulator Rbfox2 is required for both cerebellar development and mature motor function. Genes Dev 26: 445-460
6. Gehman LT, Stoilov P, Maguire J, Damianov A, Lin CH, Shiue L, Ares M, Jr., Mody I, Black DL (2011) The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain. Nat Genet 43: 706-711
7. Gehrmann J, Berul CI (2000) Cardiac electrophysiology in genetically engineered mice. J Cardiovasc Electrophysiol 11: 354-368
8. Groh WJ, Groh MR, Saha C, Kincaid JC, Simmons Z, Ciafaloni E, Pourmand R, Otten RF, Bhakta D, Nair GV et al (2008) Electrocardiographic abnormalities and sudden death in myotonic dystrophy type 1. New Engl J Med 358: 2688-2697
9. Groh WJ, Lowe MR, Zipes DP (2002) Severity of cardiac conduction involvement and arrhythmias in myotonic dystrophy type 1 correlates with age and CTG repeat length. J Cardiovasc Electrophysiol 13: 444-448
10. Han H, Irimia M, Ross PJ, Sung H-K, Alipanahi B, David L, Golipour A, Gabut M, Michael IP, Nachman EN et al (2013) MBNL proteins repress ES-cell-specific alternative splicing and reprogramming. Nature 498: 241-245
11. Hermans MC, Faber CG, Bekkers SC, de Die-Smulders CE, Gerrits MM, Merkies IS, Snoep G, Pinto YM, Schalla S (2012) Structural and functional cardiac changes in myotonic dystrophy type 1: A cardiovascular magnetic resonance study. J Cardiov Magn Reson 14: 48
12. Higham CF, Morales F, Cobbold CA, Haydon DT, Monckton DG (2012) High levels of somatic DNA diversity at the myotonic dystrophy type 1 locus are driven by ultra-frequent expansion and contraction mutations. Hum Mol Genet 21: 2450-2463
13. Ho TH, Charlet BN, Poulos MG, Singh G, Swanson MS, Cooper TA (2004) Muscleblind proteins regulate alternative splicing. EMBO J 23: 3103-3112
14. Holt I, Jacquemin V, Fardaei M, Sewry CA, Butler-Browne GS, Furling D, Brook JD, Morris GE (2009) Muscleblind-like proteins: Similarities and differences in normal and myotonic dystrophy muscle. Am J Pathol 174: 216-227
15. Jiang H, Mankodi A, Swanson MS, Moxley RT, Thornton CA (2004) Myotonic dystrophy type 1 is associated with nuclear foci of mutant RNA, sequestration of muscleblind proteins and deregulated alternative splicing in neurons. Hum Mol Genet 13: 3079-3088
16. Kanadia RN, Johnstone KA, Mankodi A, Lungu C, Thornton CA, Esson D, Timmers AM, Hauswirth WW, Swanson MS (2003) A muscleblind knockout model for myotonic dystrophy. Science 302: 1978-1980
17. Kanadia RN, Shin J, Yuan Y, Beattie SG, Wheeler TM, Thornton CA, Swanson MS (2006) Reversal of RNA missplicing and myotonia after muscleblind overexpression in a mouse poly(CUG) model for myotonic dystrophy. Proc Natl Acad Sci USA 103: 11748-11753
18. Kasahara H, Wakimoto H, Liu M, Maguire CT, Converso KL, Shioi T, Huang WY, Manning WJ, Paul D, Lawitts J et al (2001) Progressive atrioventricular conduction defects and heart failure in mice expressing a mutant Csx/Nkx2.5 homeoprotein. J Clin Invest 108: 189-201
19. Kimura T, Nakamori M, Lueck JD, Pouliquin P, Aoike F, Fujimura H, Dirksen RT, Takahashi MP, Dulhunty AF, Sakoda S (2005) Altered mRNA splicing of the skeletal muscle ryanodine receptor and sarcoplasmic/endoplasmic reticulum Ca2 + -ATPase in myotonic dystrophy type 1. Hum Mol Genet 14: 2189-2200
20. Kino Y, Mori D, Oma Y, Takeshita Y, Sasagawa N, Ishiura S (2004) Muscleblind protein, MBNL1/EXP, binds specifically to CHHG repeats. Hum Mol Genet. 13: 495-507
21. Koshelev M, Sarma S, Price RE, Wehrens XH, Cooper TA (2010) Heart-specific overexpression of CUGBP1 reproduces functional and molecular abnormalities of myotonic dystrophy type 1. Hum Mol Genet 19: 1066-1075
22. Kummer TT, Misgeld T, Lichtman JW, Sanes JR (2004) Nerve-independent formation of a topologically complex postsynaptic apparatus. J Cell Biol 164: 1077-1087
23. Lalande A, Salve N, Comte A, Jaulent MC, Legrand L, Walker PM, Cottin Y, Wolf JE, Brunotte F (2004) Left ventricular ejection fraction calculation from automatically selected and processed diastolic and systolic frames in short-axis cine-MRI. J Cardiov Magn Reson 6: 817-827
24. Li S, Czubryt MP, McAnally J, Bassel-Duby R, Richardson JA, Wiebel FF, Nordheim A, Olson EN (2005) Requirement for serum response factor for skeletal muscle growth and maturation revealed by tissue-specific gene deletion in mice. Proc Natl Acad Sci USA 102: 1082-1087
25. Lin X, Miller JW, Mankodi A, Kanadia RN, Yuan Y, Moxley RT, Swanson MS, Thornton CA (2006) Failure of MBNL1-dependent post-natal transitions in myotonic dystrophy. Hum Mol Genet 15: 2087-2097
26. Lopez Castel A, Cleary JD, Pearson CE (2010) Repeat instability as the basis for human diseases and as a potential target for therapy. Nat Rev Mol Cell Biol 11: 165-170
27. Malm S, Frigstad S, Sagberg E, Larsson H, Skjaerpe T (2004) Accurate and reproducible measurement of left ventricular volume and ejection fraction by contrast echocardiography: A comparison with magnetic resonance imaging. J Am Coll Cardiol 44: 1030-1035
28. Mankodi A, Logigian E, Callahan L, McClain C, White R, Henderson D, Krym M, Thornton CA (2000) Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science 289: 1769-1773
29. Mankodi A, Urbinati CR, Yuan QP, Moxley RT, Sansone V, Krym M, Henderson D, Schalling M, Swanson MS, Thornton CA (2001) Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2. Hum Mol Genet 10: 2165-2170
30. McNally EM, Sparano D (2011) Mechanisms and management of the heart in myotonic dystrophy. Heart 97: 1094-1100
31. Miller JW, Urbinati CR, Teng-Umnuay P, Stenberg MG, Byrne BJ, Thornton CA, Swanson MS (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J 19: 4439-4448
32. Mirkin SM. (2007) Expandable DNA repeats and human disease. Nature 447: 932-940
33. Mitchell GF, Jeron A, Koren G (1998) Measurement of heart rate and Q-T interval in the conscious mouse. Am J Physiol 274: H747-751
34. Morales F, Couto JM, Higham CF, Hogg G, Cuenca P, Braida C, Wilson RH, Adam B, del Valle G, Brian R et al (2012) Somatic instability of the expanded CTG triplet repeat in myotonic dystrophy type 1 is a heritable quantitative trait and modifier of disease severity. Hum Mol Genet 21: 3558-3567
35. Motta J, Guilleminault C, Billingham M, Barry W, Mason J (1979) Cardiac abnormalities in myotonic dystrophy. Electrophysiologic and histopathologic studies. Am J Med 67: 467-473
36. Orengo JP, Chambon P, Metzger D, Mosier DR, Snipes GJ, Cooper TA (2008) 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 105: 2646-2651
37. Osborne RJ, Lin X, Welle S, Sobczak K, O'Rourke JR, Swanson MS, Thornton CA (2009) Transcriptional and post-transcriptional impact of toxic RNA in myotonic dystrophy. Hum Mol Genet 18: 1471-1481
38. Panaite PA, Gantelet E, Kraftsik R, Gourdon G, Kuntzer T, Barakat-Walter I (2008) Myotonic dystrophy transgenic mice exhibit pathologic abnormalities in diaphragm neuromuscular junctions and phrenic nerves. J Neuropath Exp Neurol 67: 763-772
39. Paul S, Dansithong W, Kim D, Rossi J, Webster NJ, Comai L, Reddy S (2006) Interaction of muscleblind, CUG-BP1 and hnRNP H proteins in DM1-associated aberrant IR splicing. EMBO J 25: 4271-4283
40. Pelargonio G, Dello Russo A, Sanna T, De Martino G, Bellocci F (2002) Myotonic dystrophy and the heart. Heart 88: 665-670
41. Philips AV, Timchenko LT, Cooper TA (1998) Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 280: 737-741
42. Poulos MG, Batra R, Li M, Yuan Y, Zhang C, Darnell RB, Swanson MS (2013) Progressive Impairment of muscle regeneration in muscleblind-like 3 isoform knockout mice. Hum Mol Genet 22: 3547-3558
43. Prakken NH, Velthuis BK, Bosker AC, Mosterd A, Teske AJ, Mali WP, Cramer MJ (2011) Relationship of ventricular and atrial dilatation to valvular function in endurance athletes. Br J Sports Med 45: 178-184
44. Ranum LP, Cooper TA (2006) RNA-mediated neuromuscular disorders. Ann Rev Neurosci 29: 259-277
45. Rau F, Freyermuth F, Fugier C, Villemin JP, Fischer MC, Jost B, Dembele D, Gourdon G, Nicole A, Duboc D et al (2011) Misregulation of miR-1 processing is associated with heart defects in myotonic dystrophy. Nat Struct Mol Biol 18: 840-845.
46. Ravel-Chapuis A, Belanger G, Yadava RS, Mahadevan MS, DesGroseillers L, Cote J, Jasmin BJ (2012) The RNA-binding protein Staufen1 is increased in DM1 skeletal muscle and promotes alternative pre-mRNA splicing. J Cell Biol 196: 699-712
47. Sahashi K, Hua Y, Ling KK, Hung G, Rigo F, Horev G, Katsuno M, Sobue G, Ko CP, Bennett CF et al (2012) TSUNAMI: an antisense method to phenocopy splicing-associated diseases in animals. Genes Dev 26: 1874-1884
48. Sicot G, Gomes-Pereira M (2013) RNA toxicity in human disease and animal models: From the uncovering of a new mechanism to the development of promising therapies. Biochim Biophys Acta 1832: 1390-1409
49. Slawson SE, Roman BB, Williams DS, Koretsky AP (1998) Cardiac MRI of the normal and hypertrophied mouse heart. Magnet Reson Med 39: 980-987
50. Suenaga K, Lee KY, Nakamori M, Tatsumi Y, Takahashi MP, Fujimura H, Jinnai K, Yoshikawa H, Du H, Ares M Jr., et al (2012) Muscleblind-like 1 knockout mice reveal novel splicing defects in the myotonic dystrophy brain. PloS One 7: e33218
51. Tang ZZ, Yarotskyy V, Wei L, Sobczak K, Nakamori M, Eichinger K, Moxley RT, Dirksen RT, Thornton CA (2012) Muscle weakness in myotonic dystrophy associated with misregulated splicing and altered gating of Ca(V)1.1 calcium channel. Hum Mol Genet 21: 1312-11324
52. Timchenko LT, Miller JW, Timchenko NA, DeVore DR, Datar KV, Lin L, Roberts R, Caskey CT, Swanson MS (1996) Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucl Acids Res 24: 4407-4414
53. Udd B, Krahe R (2012) The myotonic dystrophies: Molecular, clinical, and therapeutic challenges. Lancet Neurol 11: 891-905
54. Valdez G, Tapia JC, Kang H, Clemenson GD, Jr., Gage FH, Lichtman JW, Sanes JR (2010) Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc Natl Acad Sci USA 107: 14863-14868
55. Venetucci L, Denegri M, Napolitano C, Priori SG (2012) Inherited calcium channelopathies in the pathophysiology of arrhythmias. Nat Rev Cardiol 9: 561-575
56. Wang ET, Cody NA, Jog S, Biancolella M, Wang TT, Treacy DJ, Luo S, Schroth GP, Housman DE, Reddy S et al (2012) Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell 150: 710-724
57. Wang GS, Kearney DL, De Biasi M, Taffet G, Cooper TA (2007) Elevation of RNA-binding protein CUGBP1 is an early event in an inducible heart-specific mouse model of myotonic dystrophy. J Clin Invest 117: 2802-2811
58. 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
59. Warf MB, Berglund JA (2007) MBNL binds similar RNA structures in the CUG repeats of myotonic dystrophy and its pre-mRNA substrate cardiac troponin T. RNA 13: 2238-2251
60. Warren SA, Briggs LE, Zeng H, Chuang J, Chang EI, Terada R, Li M, Swanson MS, Lecker SH, Willis MS et al (2012) Myosin light chain phosphorylation is critical for adaptation to cardiac stress. Circulation 126: 2575-2588
61. Wheeler TM, Thornton CA (2007) Myotonic dystrophy: RNA-mediated muscle disease. Curr Opin Neurol 20: 572-576
62. Yuan Y, Compton SA, Sobczak K, Stenberg MG, Thornton CA, Griffith JD, Swanson MS (2007) Muscleblind-like 1 interacts with RNA hairpins in splicing target and pathogenic RNAs. Nucl Acids Res 35: 5474-5486
63. Zhang C, Lee KY, Swanson MS, Darnell RB (2013) Prediction of clustered RNA-binding protein motif sites in the mammalian genome. Nucleic Acids Res 41: 6793-6807