RNA pathogenesis of the myotonic dystrophies

Neuromuscular Disorders

Volumn 15, Issue 1, 2005, Pages 5-16

  Day, John W ^a,b   Ranum, Laura P W ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

DM1; DM2; DM3; Microsatellite expansion; Myotonic dystrophy; Myotonic dystrophy type 1; Myotonic dystrophy type 2; PDM; PROMM; Proximal myotonic dystrophy; Proximal myotonic myopathy; Tetranucleotide; Trinucleotide

Indexed keywords

CHLORIDE CHANNEL; INSULIN; INSULIN RECEPTOR; TAU PROTEIN; TROPONIN I; MYOTONIC DYSTROPHY PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; RNA;

CLINICAL FEATURE; GENE MUTATION; HUMAN; INSULIN RESISTANCE; MYOTONIC DYSTROPHY; ONSET AGE; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RNA PROCESSING; RNA SPLICING; SKELETAL MUSCLE; UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ANIMAL; CHEMICAL STRUCTURE; CLASSIFICATION; GENE LINKAGE DISEQUILIBRIUM; GENETICS; HISTORY; METABOLISM; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; TRINUCLEOTIDE REPEAT;

ALTERNATIVE SPLICING; ANIMALS; CHLORIDE CHANNELS; HISTORY, 19TH CENTURY; HISTORY, 20TH CENTURY; HUMANS; LINKAGE DISEQUILIBRIUM; MODELS, MOLECULAR; MUSCLE, SKELETAL; MUTATION; MYOTONIC DYSTROPHY; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, INSULIN; RNA; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 15044354661     PISSN: 09608966     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nmd.2004.09.012     Document Type: Review

References (109)

1. Meservy JL, Sargent RG, Iyer RR, et al. Long CTG tracts from the myotonic dystrophy gene induce deletions and rearrangements during recombination at the APRT locus in CHO cells. Mol Cell Biol 2003;23:3152-62.
2. Verkerk AJMH, Pieretti M, Sutcliffe JS, et al. Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 1991;65:905-14.
3. la Spada AR, Wilson EM, Lubahn DB, Hardin AE, Fischbeck KH. Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 1991;352:77-9.
4. Pandolfo M. Molecular genetics and pathogenesis of Friedreich ataxia. Neuromuscul Disord 1998;8:409-15.
5. Orr HT, Chung M-y, Banfi S, et al. Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1. Nat Genet 1993;4:211-26.
6. Pulst S-M, Nechiporuk A, Nechiporuk T, et al. Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2. Nat Genet 1996;14:269-76.
7. Kawaguchi Y, Okamoto T, Taniwaki M, et al. CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat Genet 1994;8:221-8.
8. Liquori C, Ricker K, Moseley ML, et al. Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9. Science 2001; 293:864-7.
9. Matsuura T, Yamagata T, Burgess DL, et al. Large expansion of the ATTCT pentanucleotide repeat in spinocerebellar ataxia type 10. Nat Genet 2000;26:191-4.
10. Brais B, Bouchard JP, Xie YG, et al. Short GCG expansions in the PABP2 gene cause oculopharyngeal muscular dystrophy. Nat Genet 1998;18:164-7.
11. Abu-Baker A, Messaed C, Laganiere J, et al. Involvement of the ubiquitin-proteasome pathway and molecular chaperones in oculopharyngeal muscular dystrophy. Hum Mol Genet 2003;12:2609-23.
12. Steinert H. Myopathologische Beitrage 1. Uber das klinischeund anatomische Bild des Muskelschwunds der Myotoniker. Dtsch Z Nervenheilkd 1909;37:58-104.
13. Batten F, Gibb H. Myotonia atrophica. Brain 1909;32:187-205.
14. Thomsen J. Tonische krampfe in sillkurlich beweglichen Muskeln infole von erebter paychischer disposition (ataxia muscularis). Arch Psychiatr Nervenkr 1876;6:702-18.
15. Harper PS. Myotonic dystrophy, vol. 37. London: W.B. Saunders; 2001.
16. Brook JD, McCurrah ME, Harley HG, 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.
17. Fu YH, Pizzuti A, Fenwick Jr. RG, et al. An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 1992;255: 1256-8.
18. Ricker K, Koch MC, Lehmann-Horn F, et al. Proximal myotonic myopathy: a new dominant disorder with myotonia, muscle weakness, and cataracts. Neurology 1994;44:1448-52.
19. Thornton CA, Griggs RC, Moxley RT. Myotonic dystrophy with no trinucleotide repeat expansion. Ann Neurol 1994;35:269-72.
20. Moxley R. Proximal myotonic myopathy: mini-review of a recently delineated clinical disorder. Neuromuscul Disord 1996;6:87-93.
21. Udd B, Krahe R, Wallgren-Petterson C, Falck B, Kalimo H. Proximal myotonic dystrophy - a family with autosomal domiant muscular dystrophy, cataracts, hearing loss and hypogonadism: heterogeneity of proximal myotonic syndromes? Neuromuscul Disord 1997;7:217-28.
22. Ranum L, Rasmussen P, Benzow K, Koob M, Day J. Genetic mapping of a second myotonic dystrophy locus. Nat Genet 1998;19: 196-8.
23. Day JW, Roelofs R, Leroy B, et al. Clinical and genetic characteristics of a five-generation family with a novel form of myotonic dystrophy (DM2). Neuromuscul Disord 1999;9:19-27.
24. Consortium IMD. New nomenclature and DNA testing guidelines for myotonic dystrophy type 1 (DM1). The International Myotonic Dystrophy Consortium (IDMC). Neurology 2000;54:1218-21.
25. Harper PS. Congenital myotonic dystrophy in Britain. I. Clinical aspects. Arch Dis Child 1975;50:505-13.
26. Day JW, Ricker K, Jacobsen JF, et al. Myotonic dystrophy type 2: molecular, diagnostic and clinical spectrum. Neurology 2003;60: 657-64.
27. O'Brien TA, Harper PS. Course, prognosis and complications of childhood-onset myotonic dystrophy. Dev Med Child Neurol 1984; 26:62-7.
28. Steyaert J, de Die-Smulders C, Fryns JP, Goossens E, Willekens D. Behavioral phenotype in childhood type of dystrophia myotonica. Am J Med Genet 2000;96:888-9.
29. de Die-Smulders CE, Howeler CJ, Thijs C, et al. Age and causes of death in adult-onset myotonic dystrophy. Brain 1998;121(Pt 8): 1557-63.
30. Mathieu J, Allard P, Potvin L, Prevost C, Begin P. A 10-year study of mortality in a cohort of patients with myotonic dystrophy. Neurology 1999;52:1658-62.
31. Mathieu J, Boivin H, Meunier D, Gaudreault M, Begin P. Assessment of a disease-specific muscular impairment rating scale in myotonic dystrophy. Neurology 2001;56:336-40.
32. Ricker K, Koch M, Lehmann-Horn F, et al. Proximal myotonic myopathy: clinical features of a multisystem disorder similar to myotonic dystrophy. Arch Neurol 1995;52:25-31.
33. Schoser BG, Schneider-Gold C, Kress W, et al. Muscle pathology in 57 patients with myotonic dystrophy type 2. Muscle Nerve 2004;29: 275-81.
34. Vihola A, Bassez G, Meola G, et al. Histopathological differences of myotonic dystrophy type 1 (DM1) and PROMM/DM2. Neurology 2003;60:1854-7.
35. Phillips MF, Harper PS. Cardiac disease in myotonic dystrophy. Cardiovasc Res 1997;33:13-22.
36. Colleran JA, Hawley RJ, Pinnow EE, Kokkinos PF, Fletcher RD. Value of the electrocardiogram in determining cardiac events and mortality in myotonic dystrophy. Am J Cardiol 1997;80:1494-7.
37. Schoser BG, Ricker K, Schneider-Gold C, et al. Sudden cardiac death in myotonic dystrophy type 2. Neurology 2004 (in press).
38. Hund E, Jansen O, Koch MC, et al. Proximal myotonic myopathy with MRI white matter abnormalities of the brain. Neurology 1997; 48:33-7.
39. Meola G, Sansone V, Perani D, et al. Reduced cerebral blood flow and impaired visual-spatial function in proximal myotonic myopathy. Neurology 1999;53:1042-50.
40. Martinez-Rodriguez JE, Lin L, Iranzo A, et al. Decreased hypocretin-1 (Orexin-A) levels in the cerebrospinal fluid of patients with myotonic dystrophy and excessive daytime sleepiness. Sleep 2003;26:287-90.
41. Gibbs 3rd JW, Ciafaloni E, Radtke RA. Excessive daytime somnolence and increased rapid eye movement pressure in myotonic dystrophy. Sleep 2002;25:672-5.
42. Laberge L, Begin P, Montplaisir J, Mathieu J. Sleep complaints in patients with myotonic dystrophy. J Sleep Res 2004;13:95-100.
43. Thorpy M. Excessive daytime somnolence and increased rapid eye movement pressure in myotonic dystrophy. Curr Neurol Neurosci Rep 2003;3:165-6.
44. Aminoff M, Beckley D, McIlroy M. Autonomic function in myotonic dystrophy. Arch Neurol 1985;42:16.
45. Savkur RS, Philips AV, Cooper TA. Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat Genet 2001;29:40-7.
46. Savkur RS, Philips AV, Cooper TA, et al. Insulin receptor splicing alteration in myotonic dystrophy type 2. Am J Hum Genet 2004;74: 1309-13.
47. Harper PS. Myotonic dystrophy, 2nd ed. London: W.B. Saunders; 1989.
48. Buxton J, Shelbourne P, Davies J, et al. Detection of an unstable fragment of DNA specific to individuals with myotonic dystrophy. Nature 1992;355:547-8.
49. Harley HG, Brook JD, Rundle SA, et al. Expansion of an unstable DNA region and phenotypic variation in myotonic dystrophy. Nature 1992;355:545-6.
50. 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;255:1253-5.
51. Boucher CA, King SK, Carey N, 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 1995;4:1919-25.
52. Monckton DG, Wong LJ, Ashizawa T, Caskey CT. Somatic mosaicism, germline expansions, germline reversions and intergenerational reductions in myotonic dystrophy males: small pool PCR analyses. Hum Mol Genet 1995;4:1-8.
53. Martorell L, Monckton DG, Gamez J, et al. Progression of somatic CTG repeat length heterogeneity in the blood cells of myotonic dystrophy patients. Hum Mol Genet 1998;7:307-12.
54. Hamshere MG, Harley H, Harper P, Brook JD, Brookfield JF. Myotonic dystrophy: the correlation of (CTG) repeat length in leucocytes with age at onset is significant only for patients with small expansions. J Med Genet 1999;36:59-61.
55. Tapscott SJ. Deconstructing myotonic dystrophy. Science 2000;289: 1701-2.
56. Fu Y-H, Friedman DL, Richards S, et al. Decreased expression of myotonin-protein kinase messenger RNA and protein in adult form of myotonic dystrophy. Science 1993;260:235-8.
57. Hoffmann-Radvanyi H, Lavedan C, Rabes JP, et al. Myotonic dystrophy: absence of CTG enlarged transcript in congenital forms, and low expression of the normal allele. Hum Mol Genet 1993;2: 1263-6.
58. Novelli G, Gennarelli M, Zelano G, et al. Failure in detecting mRNa transcripts from the mutated allele in myotonic dystrophy muscle. Biochem Mol Biol Int 1993;29:291-7.
59. Jansen G, Groenen PJTA, Bachner D, et al. Abnormal myotonic dystrophy protein kinase levels produce only mild myopathy in mice. Nat Genet 1996;13:316-24.
60. Reddy S, Smith DB, Rich MM, et al. Mice lacking the myotonic dystrophy protein kinase develop a late onset progressive myopathy. Nat Genet 1996;13:325-35.
61. Berul CI, Maguire CT, Gehrmann J, Reddy S. Progressive atrioventricular conduction block in a mouse myotonic dystrophy model. J Interv Card Electrophysiol 2000;4:351-8.
62. Wang Y-H, Amirhaeri S, Kang S, Wells RD, Griffith JD. Preferential nucleosome assembly at DNA triplet repeats from the myotonic dystrophy gene. Science 1994;265:669-71.
63. Otten AD, Tapscott SJ. Triplet repeat expansion in myotonic dystrophy alters the adjacent chromatin structure. Proc Natl Acad Sci USA 1995;92:5465-9.
64. Alwazzan M, Newman E, Hamshere MG, Brook JD. Myotonic dystrophy is associated with a reduced level of RNA from the DMWD allele adjacent to the expanded repeat. Hum Mol Genet 1999;8:1491-7.
65. Westerlaken JH, Van der Zee CE, Peters W, Wieringa B. The DMWD protein from the myotonic dystrophy (DM1) gene region is developmentally regulated and is present most prominently in synapse-dense brain areas. Brain Res 2003;971:116-27.
66. Junghans RP, Ebralidze A, Tiwari B. Does (CUG)n repeat in DMPK mRNA paint chromosome 19 to suppress distant genes to create the diverse phenotype of myotonic dystrophy?: a new hypothesis of long-range cis autosomal inactivation Neurogenetics 2001;3:59-67.
67. Klesert TR, Cho DH, Clark JI, et al. Mice deficient in Six5 develop cataracts: implications for myotonic dystrophy. Nat Genet 2000;25: 105-9.
68. Sarkar PS, Appukuttan B, Han J, et al. Heterozygous loss of Six5 in mice is sufficient to cause ocular cataracts. Nat Genet 2000;25: 110-4.
69. Taneja KL, McCurrach M, Schalling M, Housman D, Singer RH. Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues. J Cell Biol 1995;128:995-1002.
70. Davis BM, McCurrach ME, Taneja KL, Singer RH, Housman DE. 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: 7388-93.
71. Timchenko LT, Timchenko NA, Caskey CT, Roberts R. Novel proteins with binding specificity for DNA CTG repeats and RNA CUG repeats: implications for myotonic dystrophy. Hum Mol Genet 1996;5:115-21.
72. Philips AV, Timchenko LT, Cooper TA. Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 1998;280:737-41.
73. Lu X, Timchenko NA, Timchenko LT. Cardiac elav-type RNA-binding protein (ETR-3) binds to RNA CUG repeats expanded in myotonic dystrophy. Hum Mol Genet 1999;8:53-60.
74. Miller JW, Urbinati CR, Teng-Umnuay P, et al. Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. Eur Mol Biol Org J 2000;19:4439-48.
75. Mankodi A, Logigian E, Callahan L, et al. Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science 2000; 289:1769-73.
76. Groenen P, Wieringa B. Expanding complexity in myotonic dystrophy. Bioessays 1998;20:901-12.
77. Filippova GN, Thienes CP, Penn BH, et al. CTCF-binding sites flank CTG/CAG repeats and form a methylation-sensitive insulator at the DM1 locus. Nat Genet 2001;28:335-43.
78. Larkin K, Fardaei M. Myotonic dystrophy-a multigene disorder. Brain Res Bull 2001;56:389-95.
79. Liquori CL, Ikeda Y, Weatherspoon M, et al. Myotonic dystrophy type 2: human founder haplotype and evolutionary conservation of the repeat tract. Am J Hum Genet 2003;73:849-62.
80. Schoser BG, Kress W, Walter MC, et al. Homozygosity for CCTG mutation in myotonic dystrophy type 2. Brain 2004.
81. Schneider C, Ziegler A, Ricker K, et al. Proximal myotonic myopathy: evidence for anticipation in families with linkage to chromosome 3q. Neurology 2000;55:383-8.
82. Pellizzoni L, Lotti F, Maras B, Pierandrei-Amaldi P. Cellular nucleic acid binding protein binds a conserved region of the 5′-UTR of Xenopus laevis ribosomal protein mRNAs. J Mol Biol 1997;267: 264-75.
83. Pellizzoni L, Lotti F, Rutjes SA, Pierandrei-Amaldi P. Involvement of the Xenopus laevis Ro60 autoantigen in the alternative interaction of 1a and CNBP proteins with the 5′-UTR of L4 ribosomal protein mRNA. J Mol Biol 1998;281:593-608.
84. Ebralidze A, Wang Y, Petkova V, Ebralidse K, Junghans RP. RNA leaching of transcription factors disrupts transcription in myotonic dystrophy. Science 2004;303:383-7.
85. Amack JD, Paguio AP, Mahadevan MS. Cis and trans effects of the myotonic dystrophy (DM) mutation in a cell culture model. Hum Mol Genet 1999;8:1975-84.
86. 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: 2717-26.
87. Mankodi A, Urbinati CR, Yuan QP, et al. Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2. Hum Mol Genet 2001;10:2165-70.
88. Fardaei M, Rogers MT, Thorpe HM, et al. 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 2002;11:805-14.
89. Fardaei M, Larkin K, Brook JD, Hamshere MG. In vivo colocalisation of MBNL protein with DMPK expanded-repeat transcripts. Nucleic Acids Res 2001;29:2766-71.
90. Charlet BN, Savkur RS, Singh G, et al. Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol Cell 2002;10:45-53.
91. Sergeant N, Sablonniere B, Schraen-Maschke S, et al. Dysregulation of human brain microtubule-associated tau mRNA maturation in myotonic dystrophy type 1. Hum Mol Genet 2001;10:2143-55.
92. Moxley RT, Griggs RC, Goldblatt D. Muscle insulin resistance in myotonic dystrophy: effect of supraphysiologic insulinization. Neurology 1980;30:1077-83.
93. Seino S, Bell GI. Alternative splicing of human insulin receptor messenger RNA. Biochem Biophys Res Commun 1989;159:312-6.
94. Mankodi A, Takahashi MP, 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.
95. Buj-Bello A, Furling D, Tronchere H, et al. Muscle-specific alternative splicing of myotubularin-related 1 gene is impaired in DM1 muscle cells. Hum Mol Genet 2002;11:2297-307.
96. Kanadia RN, Johnstone KA, Mankodi A, et al. A muscleblind knockout model for myotonic dystrophy. Science 2003;302:1978-80.
97. Ho TH, Charlet BN, Poulos MG, et al. Muscleblind proteins regulate alternative splicing. Eur Mol Biol Org J 2004;23:3103-12.
98. Storbeck CJ, Drmanic S, Daniel K, et al. Inhibition of myogenesis in transgenic mice expressing the human DMPK 3′-UTR. Hum Mol Genet 2004;13:589-600.
99. Amack JD, Mahadevan MS. Myogenic defects in myotonic dystrophy. Dev Biol 2004;265:294-301.
100. Steinbach P, Glaser D, Vogel W, Wolf M, Schwemmle S. The DMPK gene of severely affected myotonic dystrophy patients is hypermethylated proximal to the largely expanded CTG repeat. Am J Hum Genet 1998;62:278-85.
101. Sabouri LA, Mahadevan MS, Narang M, et al. Effect of the myotonic dystrophy (DM) mutation on mRNA levels of the DM gene. Nat Genet 1993;4:233-8.
102. Imbert G, Kretz C, Johnson K, Mandel JL. Origin of the expansion mutation in myotonic dystrophy. Nat Genet 1993;4:72-6.
103. Neville CE, Mahadevan MS, Barcelo JM, Korneluk RG. High resolution genetic analysis suggests one ancestral predisposing haplotype for the origin of the myotonic dystrophy mutation. Hum Mol Genet 1994;3:45-51.
104. Deka R, Majumder PP, Shriver MD, et al. Distribution and evolution of CTG repeats at the myotonin protein kinase gene in human populations. Genome Res 1996;6:142-54.
105. Bachinski LL, Udd B, Meola G, et al. Confirmation of the type 2 myotonic dystrophy (CCTG)n expansion mutation in patients with proximal myotonic myopathy/proximal myotonic dystrophy of different European origins: a single shared haplotype indicates an ancestral founder effect. Am J Hum Genet 2003;73:835-48.
106. le Ber I, Martinez M, Campion D, et al. A non-DM1, non-DM2 multisystem myotonic disorder with frontotemporal dementia: phenotype and suggestive mapping of the DM3 locus to chromosome 15q21-24. Brain 2004.
107. Meola G, Sansone V, Milanese SD, et al. Lack of DM1-(CTG)n and DM2-(CCTG)n mutations in two families with autosomal dominant muscle weakness, myotonia, and cataracts: DM3? Neurology 2004; 62:A354.
108. Langlois MA, Lee NS, Rossi JJ, Puymirat J. Hammerhead ribozyme-mediated destruction of nuclear foci in myotonic dystrophy myoblasts. Mol Ther 2003;7:670-80.
109. Jiang H, Mankodi A, Swanson MS, Moxley RT, Thornton CA. Myotonic dystrophy type 1 associated with nuclear foci of mutant RNA, sequestration of muscleblind proteins, and deregulated alternative splicing in neurons. Hum Molec Gen 2004; (in press).