Genome Therapy of Myotonic Dystrophy Type 1 iPS Cells for Development of Autologous Stem Cell Therapy

Molecular Therapy

Volumn 24, Issue 8, 2016, Pages 1378-1387

  Gao, Yuanzheng ^a,b   Guo, Xiuming ^a,b,c   Santostefano, Katherine ^a   Wang, Yanlin ^a,b,d   Reid, Tammy ^a,e   Zeng, Desmond ^a,b   Terada, Naohiro ^a   Ashizawa, Tetsuo ^a,b   Xia, Guangbin ^a,b  

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

^b UNIVERSITY OF FLORIDA   (United States)

^c CHONGQING MEDICAL UNIVERSITY   (China)

^d THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

^e Hepatology and Nutrition   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOTONIC DYSTROPHY PROTEIN KINASE; NUCLEAR RNA; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; POLYADENYLIC ACID; PROTEIN BINDING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CARDIAC MUSCLE CELL; CELL CLONE; CONTROLLED STUDY; CTG REPEAT; DMPK GENE; DNA STRUCTURE; DOUBLE STRANDED DNA BREAK; GENE INSERTION; GENE THERAPY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; INTRON; MOUSE; MYOTONIC DYSTROPHY TYPE 1 INDUCED PLURIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PHENOTYPE; REGULATORY RNA SEQUENCE; RNA SPLICING; TERATOMA; TRANSCRIPTION TERMINATION; ANIMAL; AUTOTRANSPLANTATION; CELL DIFFERENTIATION; CELL NUCLEUS; CELL TRANSFORMATION; CYTOLOGY; DISEASE MODEL; GENE LOCUS; GENE TARGETING; GENETICS; METABOLISM; MYOTONIC DYSTROPHY; PATHOLOGY; STEM CELL TRANSPLANTATION; TRINUCLEOTIDE REPEAT;

ANIMALS; CELL DIFFERENTIATION; CELL NUCLEUS; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; GENE TARGETING; GENETIC LOCI; GENETIC THERAPY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MYOCYTES, CARDIAC; MYOTONIC DYSTROPHY; MYOTONIN-PROTEIN KINASE; POLY A; PROTEIN BINDING; RNA SPLICING; STEM CELL TRANSPLANTATION; TERATOMA; TRANSCRIPTION ACTIVATOR-LIKE EFFECTOR NUCLEASES; TRANSPLANTATION, AUTOLOGOUS; TRINUCLEOTIDE REPEATS;

EID: 84976359265     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2016.97     Document Type: Article

References (46)

1. Romeo, V (2012). Myotonic Dystrophy Type 1 or Steinert's disease. Adv Exp Med Biol 724: 239-257.
2. Reardon, W, Newcombe, R, Fenton, I, Sibert, J and Harper, PS (1993). The natural history of congenital myotonic dystrophy: mortality and long term clinical aspects. Arch Dis Child 68: 177-181.
3. Brook, JD, McCurrach, ME, Harley, HG, Buckler, AJ, Church, D, Aburatani, H 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 69: 385.
4. Mahadevan, M, Tsilfidis, C, Sabourin, L, Shutler, G, Amemiya, C, Jansen, G et al. (1992). Myotonic dystrophy mutation: an unstable CTG repeat in the 3' untranslated region of the gene. Science 255: 1253-1255.
5. Fu, YH, Pizzuti, A, Fenwick, RG Jr, King, J, Rajnarayan, S, Dunne, PW et al. (1992). An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 255: 1256-1258.
6. Ashizawa, T, Monckton, DG, Vaishnav, S, Patel, BJ, Voskova, A and Caskey, CT (1996). Instability of the expanded (CTG) repeats in the myotonin protein kinase gene in cultured lymphoblastoid cell lines from patients with myotonic dystrophy. Genomics 36: 47-53.
7. Salehi, LB, Bonifazi, E, Stasio, ED, Gennarelli, M, Botta, A, Vallo, L, et al. (2007). Risk prediction for clinical phenotype in myotonic dystrophy type 1: data from 2,650 patients. Genet Test 11: 84-90.
8. The International Myotonic Dystrophy Consortium (IDMC). (2000). New nomenclature and DNA testing guidelines for myotonic dystrophy type 1 (DM1). Neurology 54: 1218-1221.
9. Morales, F, Couto, JM, Higham, CF, Hogg, G, Cuenca, P, Braida, C 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.
10. Thornton, CA (2014). Myotonic dystrophy. Neurol Clin 32: 705-19.
11. Turner, C and Hilton-Jones, D (2014). Myotonic dystrophy: diagnosis, management and new therapies. Curr Opin Neurol 27: 599-606.
12. Reynolds, BA and Weiss, S (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
13. Lois, C and Alvarez-Buylla, A (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 90: 2074-2077.
14. Xia, G, Gao, Y, Jin, S, Subramony, SH, Terada, N, Ranum, LP et al. (2015). Genome modification leads to phenotype reversal in human myotonic dystrophy type 1 induced pluripotent stem cell-derived neural stem cells. Stem Cells 33: 1829-1838.
15. Esvelt, KM and Wang, HH (2013). Genome-scale engineering for systems and synthetic biology. Mol Syst Biol 9: 641.
16. Tan, WS, Carlson, DF, Walton, MW, Fahrenkrug, SC and Hackett, PB (2012). Precision editing of large animal genomes. Adv Genet 80: 37-97.
17. Maggio, I and Goncalves, MA (2015). Genome editing at the crossroads of delivery, specificity, and fidelity. Trends Biotechnol 33: 280-291.
18. Perez, EE, Wang, J, Miller, JC, Jouvenot, Y, Kim, KA, Liu, O et al. (2008). Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat Biotechnol 26: 808-816.
19. Maier, DA, Brennan, AL, Jiang, S, Binder-Scholl, GK, Lee, G, Plesa, G et al. (2013). Efficient clinical scale gene modification via zinc finger nuclease-targeted disruption of the HIV co-receptor CCR5. Hum Gene Ther 24: 245-258.
20. Tebas, P, Stein, D, Tang, WW, Frank, I, Wang, SQ, Lee, G et al. (2014). Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N Engl J Med 370: 901-910.
21. Otten, AD and Tapscott, SJ (1995). Triplet repeat expansion in myotonic dystrophy alters the adjacent chromatin structure. Proc Natl Acad Sci USA 92: 5465-5469.
22. Cho, DH, Thienes, CP, Mahoney, SE, Analau, E, Filippova, GN and Tapscott, SJ (2005). Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol Cell 20: 483-489.
23. Steinbach, P, Gläser, D, Vogel, W, Wolf, M and Schwemmle, S (1998). The DMPK gene of severely affected myotonic dystrophy patients is hypermethylated proximal to the largely expanded CTG repeat. Am J Hum Genet 62: 278-285.
24. Wansink, DG, van Herpen, RE, Coerwinkel-Driessen, MM, Groenen, PJ, Hemmings, BA and Wieringa, B (2003). Alternative splicing controls myotonic dystrophy protein kinase structure, enzymatic activity, and subcellular localization. Mol Cell Biol 23: 5489-5501.
25. Reddy, S, Smith, DB, Rich, MM, Leferovich, JM, Reilly, P, Davis, BM et al. (1996). Mice lacking the myotonic dystrophy protein kinase develop a late onset progressive myopathy. Nat Genet 13: 325-335.
26. Narang, MA, Waring, JD, Sabourin, LA and Korneluk, RG (2000). Myotonic dystrophy (DM) protein kinase levels in congenital and adult DM patients. Eur J Hum Genet 8: 507-512.
27. Jansen, G, Bartolomei, M, Kalscheuer, V, Merkx, G, Wormskamp, N, Mariman, E et al. (1993). No imprinting involved in the expression of DM-kinase mRNAs in mouse and human tissues. Hum Mol Genet 2: 1221-1227.
28. Farini, A, Razini, P, Erratico, S, Torrente, Y and Meregalli, M (2009). Cell based therapy for Duchenne muscular dystrophy. J Cell Physiol 221: 526-534.
29. Gussoni, E, Blau, HM and Kunkel, LM (1997). The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat Med 3: 970-977.
30. Miller, RG, Sharma, KR, Pavlath, GK, Gussoni, E, Mynhier, M, Lanctot, AM et al. (1997). Myoblast implantation in Duchenne muscular dystrophy: the San Francisco study. Muscle Nerve 20: 469-478.
31. Mendell, JR, Kissel, JT, Amato, AA, King, W, Signore, L, Prior, TW et al. (1995). Myoblast transfer in the treatment of Duchenne's muscular dystrophy. N Engl J Med 333: 832-838.
32. Montarras, D, Morgan, J, Collins, C, Relaix, F, Zaffran, S, Cumano, A et al. (2005). Direct isolation of satellite cells for skeletal muscle regeneration. Science 309: 2064-2067.
33. Salani, S, Donadoni, C, Rizzo, F, Bresolin, N, Comi, GP and Corti, S (2012). Generation of skeletal muscle cells from embryonic and induced pluripotent stem cells as an in vitro model and for therapy of muscular dystrophies. J Cell Mol Med 16: 1353-1364.
34. Nakahata, T, Awaya, T, Chang, H, Mizuno, Y, Niwa, A, Fukada, S et al. (2010). [Derivation of engraftable myogenic precursors from murine ES/iPS cells and generation of disease-specific iPS cells from patients with Duchenne muscular dystrophy (DMD) and other diseases]. Rinsho Shinkeigaku 50: 889.
35. Mazin, P, Xiong, J, Liu, X, Yan, Z, Zhang, X, Li, M et al. (2013). Widespread splicing changes in human brain development and aging. Mol Syst Biol 9: 633.
36. Rao, MS (1999). Multipotent and restricted precursors in the central nervous system. Anat Rec 257: 137-148.
37. Qian, X, Shen, Q, Goderie, SK, He, W, Capela, A, Davis, AA et al. (2000). Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28: 69-80.
38. He, W, Ingraham, C, Rising, L, Goderie, S and Temple, S (2001). Multipotent stem cells from the mouse basal forebrain contribute GABAergic neurons and oligodendrocytes to the cerebral cortex during embryogenesis. J Neurosci 21: 8854-8862.
39. Terenzi, F and Ladd, AN (2010). Conserved developmental alternative splicing of muscleblind-like (MBNL) transcripts regulates MBNL localization and activity. RNA Biol 7: 43-55.
40. Nakamori, M, Sobczak, K, Puwanant, A, Welle, S, Eichinger, K, Pandya, S et al. (2013). Splicing biomarkers of disease severity in myotonic dystrophy. Ann Neurol 74: 862-872.
41. Xia, G, Gao, Y, Jin, S, Subramony, S, Terada, N, Ranum, LP, et al. (2015). Genome modification leads to phenotype reversal in human myotonic dystrophy type 1 iPS-cell derived neural stem cells. Stem Cells 33: 1829-1838.
42. Xia, G, Santostefano, KE, Goodwin, M, Liu, J, Subramony, SH, Swanson, MS et al. (2013). Generation of neural cells from DM1 induced pluripotent stem cells as cellular model for the study of central nervous system neuropathogenesis. Cell Reprogram 15: 166-177.
43. Dhaenens, CM, Tran, H, Frandemiche, ML, Carpentier, C, Schraen-Maschke, S, Sistiaga, A et al. (2011). Mis-splicing of Tau exon 10 in myotonic dystrophy type 1 is reproduced by overexpression of CELF2 but not by MBNL1 silencing. Biochim Biophys Acta 1812: 732-742.
44. Hernández-Hernández, O, Sicot, G, Dinca, DM, Huguet, A, Nicole, A, Bueé, L et al. (2013). Synaptic protein dysregulation in myotonic dystrophy type 1: Disease neuropathogenesis beyond missplicing. Rare Dis 1: e25553.
45. Philips, AV, Timchenko, LT and Cooper, TA (1998). Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 280: 737-741.
46. Jog, SP, Paul, S, Dansithong, W, Tring, S, Comai, L and Reddy, S (2012). RNA splicing is responsive to MBNL1 dose. PLoS One 7: e48825.