Genome modification leads to phenotype reversal in human myotonic dystrophy type 1 induced pluripotent stem cell-derived neural stem cells

Stem Cells

Volumn 33, Issue 6, 2015, Pages 1829-1838

  Xia, Guangbin ^a,b   Gao, Yuanzheng ^a   Jin, Shouguang ^c   Subramony, S H ^a,b   Terada, Naohiro ^b   Ranum, Laura P W ^a,b,c   Swanson, Maurice S ^a,b,c   Ashizawa, Tetsuo ^a,b  

^a UNIVERSITY OF FLORIDA   (United States)

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

^c Hepatology and Nutrition   (United States)

Author keywords

Cell transplantation; Gene targeting; Genomics; Muscular dystrophy; Neural Stem Cell; Pluripotency

Indexed keywords

CRE RECOMBINASE; NUCLEAR RNA; PUROMYCIN; TAU PROTEIN; MICROTUBULE ASSOCIATED PROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CELL CULTURE; CELL TRANSFER; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC TRANSFECTION; GENOME; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INDUCED PLURIPOTENT STEM CELL DERIVED NEURAL STEM CELL; MYOTONIC DYSTROPHY; NEURAL STEM CELL; PHENOTYPE; PLURIPOTENT STEM CELL; STEM CELL; CYTOLOGY; HUMAN GENOME; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PATHOLOGY;

IPS;

GENOME, HUMAN; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICROTUBULE-ASSOCIATED PROTEINS; MYOTONIC DYSTROPHY; NEURAL STEM CELLS; PHENOTYPE; PLURIPOTENT STEM CELLS;

EID: 84929832278     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1970     Document Type: Article

References (78)

1. Fu YH, Pizzuti A, Fenwick RG, Jr,. et al. An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 1992; 255: 1256-1258.
2. Ashizawa T, Sarkar PS,. Myotonic dystrophy types 1 and 2. Handb Clin Neurol 2011; 101: 193-237.
3. Romeo V,. Myotonic Dystrophy Type 1 or Steinert's disease. Adv Exp Med Biol 2012; 724: 239-257.
4. Ranum LP, Cooper TA,. RNA-mediated neuromuscular disorders. Annu Rev Neurosci 2006; 29: 259-277.
5. Lee JE, Cooper TA,. Pathogenic mechanisms of myotonic dystrophy. Biochem Soc Trans 2009; 37: 1281-1286.
6. Gomes-Pereira M, Cooper TA, Gourdon G,. Myotonic dystrophy mouse models: Towards rational therapy development. Trends Mol Med 2011; 17: 506-517.
7. Wheeler TM, Sobczak K, Lueck JD, et al., Reversal of RNA dominance by displacement of protein sequestered on triplet repeat RNA. Science 2009; 325: 336-339.
8. Lee JE, Bennett CF, Cooper TA,. RNase H-mediated degradation of toxic RNA in myotonic dystrophy type 1. Proc Natl Acad Sci USA 2012; 109: 4221-4226.
9. Langlois MA, Lee NS, Rossi JJ, et al., Hammerhead ribozyme-mediated destruction of nuclear foci in myotonic dystrophy myoblasts. Mol Ther 2003; 7: 670-680.
10. Warf MB, Nakamori M, Matthys CM, et al., Pentamidine reverses the splicing defects associated with myotonic dystrophy. Proc Natl Acad Sci USA 2009; 106: 18551-18556.
11. Mulders SA, van den Broek WJ, Wheeler TM, et al., Triplet-repeat oligonucleotide-mediated reversal of RNA toxicity in myotonic dystrophy. Proc Natl Acad Sci USA 2009; 106: 13915-13920.
12. Wheeler TM, Leger AJ, Pandey SK, et al., Targeting nuclear RNA for in vivo correction of myotonic dystrophy. Nature 2012; 488: 111-115.
13. Parkesh R, Childs-Disney JL, Nakamori M, et al., Design of a bioactive small molecule that targets the myotonic dystrophy type 1 RNA via an RNA motif-ligand database and chemical similarity searching. J Am Chem Soc 2012; 134: 4731-4742.
14. Drews K, Jozefczuk J, Prigione A, et al., Human induced pluripotent stem cells-From mechanisms to clinical applications. J Mol Med (Berl) 2012; 90: 735-745.
15. Ebben JD, Zorniak M, Clark PA, et al., Introduction to induced pluripotent stem cells: Advancing the potential for personalized medicine. World Neurosurg 2011; 76: 270-275.
16. Lengner CJ,. iPS cell technology in regenerative medicine. Ann N Y Acad Sci 2010; 1192: 38-44.
17. Wu SM, Hochedlinger K,. Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nat Cell Biol 2011; 13: 497-505.
18. Takahashi K, Tanabe K, Ohnuki M, et al., Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872.
19. Aasen T, Raya A, Barrero MJ, et al., Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 2008; 26: 1276-1284.
20. Meissner A, Wernig M, Jaenisch R,. Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat Biotechnol 2007; 25: 1177-1181.
21. Sun N, Panetta NJ, Gupta DM, et al., Feeder-free derivation of induced pluripotent stem cells from adult human adipose stem cells. Proc Natl Acad Sci USA 2009; 106: 15720-15725.
22. Boulting GL, Kiskinis E, Croft GF, et al., A functionally characterized test set of human induced pluripotent stem cells. Nat Biotechnol 2011; 29: 279-286.
23. Mankodi A, Logigian E, Callahan L, et al., Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science 2000; 289: 1769-1773.
24. 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.
25. Orengo JP, Chambon P, Metzger D, et al., 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.
26. O'Rourke JR, Swanson MS,. Mechanisms of RNA-mediated disease. J Biol Chem 2009; 284: 7419-7423.
27. Klein AF, Gasnier E, Furling D,. Gain of RNA function in pathological cases: Focus on myotonic dystrophy. Biochimie 2011; 93: 2006-2012.
28. Todd PK, Paulson HL,. RNA-mediated neurodegeneration in repeat expansion disorders. Ann Neurol 2010; 67: 291-300.
29. Dick KA, Margolis JM, Day JW, et al., Dominant non-coding repeat expansions in human disease. Genome Dyn 2006; 1: 67-83.
30. Xia G, Santostefano KE, Goodwin M, et al., Generation of neural cells from DM1 induced pluripotent stem cells as cellular model for the study of central nervous system neuropathogenesis. Cell Reprogram 2013; 15: 166-177.
31. Romeo V, Pegoraro E, Ferrati C, et al., Brain involvement in myotonic dystrophies: Neuroimaging and neuropsychological comparative study in DM1 and DM2. J Neurol 2010; 257: 1246-1255.
32. Ogata A, Terae S, Fujita M, et al., Anterior temporal white matter lesions in myotonic dystrophy with intellectual impairment: An MRI and neuropathological study. Neuroradiology 1998; 40: 411-415.
33. Maurage CA, Udd B, Ruchoux MM, et al., Similar brain tau pathology in DM2/PROMM and DM1/Steinert disease. Neurology 2005; 65: 1636-1638.
34. Yoshimura N, Otake M, Igarashi K, et al., Topography of Alzheimer's neurofibrillary change distribution in myotonic dystrophy. Clin Neuropathol 1990; 9: 234-239.
35. Mitake S, Inagaki T, Niimi T, et al., [Development of Alzheimer neurofibrillary changes in two autopsy cases of myotonic dystrophy]. Rinsho Shinkeigaku 1989; 29: 488-492.
36. Kiuchi A, Otsuka N, Namba Y, et al., Presenile appearance of abundant Alzheimer's neurofibrillary tangles without senile plaques in the brain in myotonic dystrophy. Acta Neuropathol 1991; 82: 1-5.
37. Jiang H, Mankodi A, Swanson MS, et al., 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 2004; 13: 3079-3088.
38. Sistiaga A, Urreta I, Jodar M, et al., Cognitive/personality pattern and triplet expansion size in adult myotonic dystrophy type 1 (DM1): CTG repeats, cognition and personality in DM1. Psychol Med 2010; 40: 487-495.
39. Bird TD, Follett C, Griep E,. Cognitive and personality function in myotonic muscular dystrophy. J Neurol Neurosurg Psychiatry 1983; 46: 971-980.
40. Portwood MM, Wicks JJ, Lieberman JS, et al., Intellectual and cognitive function in adults with myotonic muscular dystrophy. Arch Phys Med Rehabil 1986; 67: 299-303.
41. Roig M, Balliu PR, Navarro C, et al., Presentation, clinical course, and outcome of the congenital form of myotonic dystrophy. Pediatr Neurol 1994; 11: 208-213.
42. Rubinsztein JS, Rubinsztein DC, McKenna PJ, et al., Mild myotonic dystrophy is associated with memory impairment in the context of normal general intelligence. J Med Genet 1997; 34: 229-233.
43. Steyaert J, Umans S, Willekens D, et al., A study of the cognitive and psychological profile in 16 children with congenital or juvenile myotonic dystrophy. Clin Genet 1997; 52: 135-141.
44. Ekstrom AB, Hakenas-Plate L, Samuelsson L, et al., Autism spectrum conditions in myotonic dystrophy type 1: a study on 57 individuals with congenital and childhood forms. Am J Med Genet B Neuropsychiatr Genet 2008; 147B: 918-926.
45. Douniol M, Jacquette A, Guile JM, et al., Psychiatric and cognitive phenotype in children and adolescents with myotonic dystrophy. Eur Child Adolesc Psychiatry 2009; 18: 705-715.
46. Liu S, Li C, Xing Y, et al., Effect of transplantation of human embryonic stem cell-derived neural progenitor cells on adult neurogenesis in aged hippocampus. Am J Stem Cells 2014; 3: 21-26.
47. Chen L, Qiu R, Xu Q,. Mesenchymal stem cell therapy for neurodegenerative diseases. J Nanosci Nanotechnol 2014; 14: 969-975.
48. de Munter JP, Melamed E, Wolters E,. Stem cell grafting in parkinsonism-Why, how and when. Parkinsonism Relat Disord 2014; 20 (suppl 1): S150-S153.
49. Thomsen GM, Gowing G, Svendsen S, et al., The past, present and future of stem cell clinical trials for ALS. Exp Neurol 2014; 262: 127-137.
50. Choi SS, Lee SR, Kim SU, et al., Alzheimer's disease and stem cell therapy. Exp Neurobiol 2014; 23: 45-52.
51. Im W, Kim M,. Cell therapy strategies vs. paracrine effect in Huntington's disease. J Mov Disord 2014; 7: 1-6.
52. Davila Lopez M, Samuelsson T,. Early evolution of histone mRNA 3' end processing. RNA 2008; 14: 1-10.
53. Liu D, Brockman JM, Dass B, et al., Systematic variation in mRNA 3'-processing signals during mouse spermatogenesis. Nucleic Acids Res 2007; 35: 234-246.
54. Gutschner T, Baas M, Diederichs S,. Noncoding RNA gene silencing through genomic integration of RNA destabilizing elements using zinc finger nucleases. Genome Res 2011; 21: 1944-1954.
55. Iiizumi S, Nomura Y, So S, et al., Simple one-week method to construct gene-targeting vectors: application to production of human knockout cell lines. Biotechniques 2006; 41: 311-316.
56. Warner JP, Barron LH, Goudie D, et al., A general method for the detection of large CAG repeat expansions by fluorescent PCR. J Med Genet 1996; 33: 1022-1026.
57. Dhaenens CM, Tran H, Frandemiche ML, et al., 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 2011; 1812: 732-742.
58. Hernandez-Hernandez O, Sicot G, Dinca DM, et al., Synaptic protein dysregulation in myotonic dystrophy type 1: Disease neuropathogenesis beyond missplicing. Rare Dis 2013; 1: e25553.
59. Li T, Huang S, Zhao X, et al., Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res 2011; 39: 6315-6325.
60. Li T, Huang S, Jiang WZ, et al., TAL nucleases (TALNs): Hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res 2011; 39: 359-372.
61. Cade L, Reyon D, Hwang WY, et al., Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENs. Nucleic Acids Res 2012; 40: 8001-8010.
62. Sander JD, Cade L, Khayter C, et al., Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 2011; 29: 697-698.
63. Tong C, Huang G, Ashton C, et al., Rapid and cost-effective gene targeting in rat embryonic stem cells by TALENs. J Genet Genomics 2012; 39: 275-280.
64. Mussolino C, Morbitzer R, Lutge F, et al., A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 2011; 39: 9283-9293.
65. Hockemeyer D, Wang H, Kiani S, et al., Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 2011; 29: 731-734.
66. Miller JC, Tan S, Qiao G, et al., A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 2011; 29: 143-148.
67. Yusa K, Rashid ST, Strick-Marchand H, et al., Targeted gene correction of alpha1-antitrypsin deficiency in induced pluripotent stem cells. Nature 2011; 478: 391-394.
68. Sebastiano V, Maeder ML, Angstman JF, et al., In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases. Stem Cells 2011; 29: 1717-1726.
69. Zou J, Mali P, Huang X, et al., Site-specific gene correction of a point mutation in human iPS cells derived from an adult patient with sickle cell disease. Blood 2011; 118: 4599-4608.
70. Urnov FD, Miller JC, Lee YL, et al., Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 2005; 435: 646-651.
71. Roth DB, Wilson JH,. Relative rates of homologous and nonhomologous recombination in transfected DNA. Proc Natl Acad Sci USA 1985; 82: 3355-3359.
72. Wansink DG, van Herpen RE, Coerwinkel-Driessen MM, et al., Alternative splicing controls myotonic dystrophy protein kinase structure, enzymatic activity, and subcellular localization. Mol Cell Biol 2003; 23: 5489-5501.
73. Zu T, Gibbens B, Doty NS, et al., Non-ATG-initiated translation directed by microsatellite expansions. Proc Natl Acad Sci USA 2011; 108: 260-265.
74. Ash PE, Bieniek KF, Gendron TF, et al., Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron 2013; 77: 639-646.
75. Cleary JD, Ranum LP,. Repeat-associated non-ATG (RAN) translation in neurological disease. Hum Mol Genet 2013; 22: R45-R51.
76. Groh M, Silva LM, Gromak N,. Mechanisms of transcriptional dysregulation in repeat expansion disorders. Biochem Soc Trans 2014; 42: 1123-1128.
77. Budworth H, McMurray CT,. Bidirectional transcription of trinucleotide repeats: Roles for excision repair. DNA Repair (Amst) 2013; 12: 672-684.
78. Cho DH, Thienes CP, Mahoney SE, et al., Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol Cell 2005; 20: 483-489.