Precise correction of disease mutations in induced pluripotent stem cells derived from patients with limb girdle muscular dystrophy

Molecular Therapy

Volumn 24, Issue 4, 2016, Pages 685-696

  Turan, Soeren ^a   Farruggio, Alfonso P ^a   Srifa, Waracharee ^a   Day, John W ^a   Calos, Michele P ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SARCOGLYCAN; COMPLEMENTARY DNA; DYSFERLIN; OLIGONUCLEOTIDE; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; DYSF PROTEIN, HUMAN; MEMBRANE PROTEIN; MUSCLE PROTEIN; SARCOGLYCAN;

ARTICLE; CELL THERAPY; CHROMOSOME 22; CONTROLLED STUDY; CRISPR CAS SYSTEM; GENE EDITING; GENE LOCUS; GENE MUTATION; GENE TRANSFER; GENETIC ENGINEERING; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; LIMB GIRDLE MUSCULAR DYSTROPHY; NONSENSE MUTATION; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ALLELE; BIOLOGICAL THERAPY; CELL LINE; FEMALE; GENE THERAPY; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MUSCULAR DYSTROPHIES, LIMB-GIRDLE; MUTATION; PATHOLOGY; PROCEDURES;

ALLELES; CELL LINE; CELL- AND TISSUE-BASED THERAPY; CRISPR-CAS SYSTEMS; FEMALE; GENE EDITING; GENETIC THERAPY; HOMOLOGOUS RECOMBINATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MEMBRANE PROTEINS; MUSCLE PROTEINS; MUSCULAR DYSTROPHIES, LIMB-GIRDLE; MUTATION; SARCOGLYCANS;

EID: 84961219527     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2016.40     Document Type: Article

References (44)

1. Takahashi, K, Tanabe, K, Ohnuki, M, Narita, M, Ichisaka, T, Tomoda, K, et al. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872
2. Awaya, T, Kato, T, Mizuno, Y, Chang, H, Niwa, A, Umeda, K, et al. (2012). Selective development of myogenic mesenchymal cells from human embryonic, and induced pluripotent stem cells. PLoS One 7: e51638
3. Chal, J, Oginuma, M, Al Tanoury, Z, Gobert, B, Sumara, O, Hick, A, et al. (2015). Differentiation of pluripotent stem cells to muscle fiber to model Duchenne muscular dystrophy. Nat Biotechnol 33: 962-969
4. Aarts, M, and te Riele, H. (2011). Progress, and prospects: oligonucleotide-directed gene modification in mouse embryonic stem cells: a route to therapeutic application. Gene Ther 18: 213-219
5. Ding, Q, Lee, YK, Schaefer, EA, Peters, DT, Veres, A, Kim, K, et al. (2013). A TALEN genome-editing system for generating human stem cell-based disease models. Cell Stem Cell 12: 238-251
6. Deng, C, and Capecchi, MR. (1992). Reexamination of gene targeting frequency as a function of the extent of homology between the targeting vector, and the target locus. Mol Cell Biol 12: 3365-3371
7. Igoucheva, O, Alexeev, V, and Yoon, K. (2001). Targeted gene correction by small single-stranded oligonucleotides in mammalian cells. Gene Ther 8: 391-399
8. Urnov, FD, Miller, JC, Lee, YL, Beausejour, CM, Rock, JM, Augustus, S, et al. (2005). Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435: 646-651
9. Yang, L, Guell, M, Byrne, S, Yang, JL, De Los Angeles, A, Mali, P, et al. (2013). Optimization of scarless human stem cell genome editing. Nucleic Acids Res 41: 9049-9061
10. Carroll, D. (2014). Genome engineering with targetable nucleases. Annu Rev Biochem 83: 409-439
11. Zhao, C, Farruggio, AP, Bjornson, CR, Chavez, CL, Geisinger, JM, Neal, TL, et al. (2014). Recombinase-mediated reprogramming, and dystrophin gene addition in mdx mouse induced pluripotent stem cells. PLoS One 9: e96279
12. Zhu, F, Gamboa, M, Farruggio, AP, Hippenmeyer, S, Tasic, B, Schüle, B, et al. (2014). DICE, an efficient system for iterative genomic editing in human pluripotent stem cells. Nucleic Acids Res 42: e34
13. Mitsuhashi, S, and Kang, PB. (2012). Update on the genetics of limb girdle muscular dystrophy. Semin Pediatr Neurol 19: 211-218
14. Piccolo, F, Moore, SA, Ford, GC, and Campbell, KP. (2000). Intracellular accumulation, and reduced sarcolemmal expression of dysferlin in limb-girdle muscular dystrophies. Ann Neurol 48: 902-912
15. Bansal, D, Miyake, K, Vogel, SS, Groh, S, Chen, CC, Williamson, R, et al. (2003). Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423: 168-172
16. Liu, J, Aoki, M, Illa, I, Wu, C, Fardeau, M, Angelini, C, et al. (1998). Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy, and limb girdle muscular dystrophy. Nat Genet 20: 31-36
17. Piccolo, F, Roberds, SL, Jeanpierre, M, Leturcq, F, Azibi, K, Beldjord, C, et al. (1995). Primary adhalinopathy: a common cause of autosomal recessive muscular dystrophy of variable severity. Nat Genet 10: 243-245
18. Kawai, H, Akaike, M, Endo, T, Adachi, K, Inui, T, Mitsui, T, et al. (1995). Adhalin gene mutations in patients with autosomal recessive childhood onset muscular dystrophy with adhalin deficiency. J Clin Invest 96: 1202-1207
19. Fougerousse, F, Bartoli, M, Poupiot, J, Arandel, L, Durand, M, Guerchet, N, et al. (2007). Phenotypic correction of alpha-sarcoglycan deficiency by intra-Arterial injection of a muscle-specific serotype 1 rAAV vector. Mol Ther 15: 53-61
20. Cradick, TJ, Fine, EJ, Antico, CJ, and Bao, G. (2013). CRISPR/Cas9 systems targetingβ-globin, and CCR5 genes have substantial off-Target activity. Nucleic Acids Res 41: 9584-9592
21. Carrié, A, Piccolo, F, Leturcq, F, de Toma, C, Azibi, K, Beldjord, C, et al. (1997). Mutational diversity, and hot spots in the alpha-sarcoglycan gene in autosomal recessive muscular dystrophy (LGMD2D). J Med Genet 34: 470-475
22. Byrne, SM, Ortiz, L, Mali, P, Aach, J, and Church, GM. (2015). Multi-kilobase homozygous targeted gene replacement in human induced pluripotent stem cells. Nucleic Acids Res 43: e21
23. Tasic, B, Hippenmeyer, S, Wang, C, Gamboa, M, Zong, H, Chen-Tsai, Y, et al. (2011). Site-specific integrase-mediated transgenesis in mice via pronuclear injection. Proc Natl Acad Sci USA 108: 7902-7907
24. Xu, C, Tabebordbar, M, Iovino, S, Ciarlo, C, Liu, J, Castiglioni, A, et al. (2013). A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species. Cell 155: 909-921
25. Soheili, T, Gicquel, E, Poupiot, J, N?Guyen, L, Le Roy, F, Bartoli, M, et al. (2012). Rescue of sarcoglycan mutations by inhibition of endoplasmic reticulum quality control is associated with minimal structural modifications. Hum Mutat 33: 429-439.
26. Nik-Ahd, F, and Bertoni, C. (2014). Ex vivo gene editing of the dystrophin gene in muscle stem cells mediated by peptide nucleic acid single stranded oligodeoxynucleotides induces stable expression of dystrophin in a mouse model for Duchenne muscular dystrophy. Stem Cells 32: 1817-1830
27. Jinek, M, Chylinski, K, Fonfara, I, Hauer, M, Doudna, JA, and Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821
28. Bialk, P, Rivera-Torres, N, Strouse, B, and Kmiec, EB. (2015). Regulation of gene editing activity directed by single-stranded oligonucleotides, and CRISPR/Cas9 systems. PLoS One 10: e0129308
29. Chen, F, Pruett-Miller, SM, Huang, Y, Gjoka, M, Duda, K, Taunton, J, et al. (2011). High-frequency genome editing using ssDNA oligonucleotides with zinc-finger nucleases. Nat Methods 8: 753-755
30. Ran, FA, Cong, L, Yan, WX, Scott, DA, Gootenberg, JS, Kriz, AJ, et al. (2015). In vivo genome editing using Staphylococcus aureus Cas9. Nature 520: 186-191
31. Kleinstiver, BP, Prew, MS, Tsai, SQ, Topkar, VV, Nguyen, NT, Zheng, Z, et al. (2015). Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523: 481-485
32. Nguyen, K, Bassez, G, Bernard, R, Krahn, M, Labelle, V, Figarella-Branger, D, et al. (2005). Dysferlin mutations in LGMD2B, Miyoshi myopathy, and atypical dysferlinopathies. Hum Mutat 26: 165
33. Smith, C, Abalde-Atristain, L, He, C, Brodsky, BR, Braunstein, EM, Chaudhari, P, et al. (2015). Efficient, and allele-specific genome editing of disease loci in human iPSCs. Mol Ther 23: 570-577
34. Soldner, F, Laganière, J, Cheng, AW, Hockemeyer, D, Gao, Q, Alagappan, R, et al. (2011). Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 146: 318-331
35. Hsu, PD, Scott, DA, Weinstein, JA, Ran, FA, Konermann, S, Agarwala, V, et al. (2013). DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31: 827-832
36. Wang, X, Wang, Y, Huang, H, Chen, B, Chen, X, Hu, J, et al. (2014). Precise gene modification mediated by TALEN, and single-stranded oligodeoxynucleotides in human cells. PLoS One 9: e93575
37. Merkert, S, Wunderlich, S, Bednarski, C, Beier, J, Haase, A, Dreyer, AK, et al. (2014). Efficient designer nuclease-based homologous recombination enables direct PCR screening for footprintless targeted human pluripotent stem cells. Stem Cell Reports 2: 107-118
38. Moehle, EA, Rock, JM, Lee, YL, et al. (2007). Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc Natl Acad Sci USA 104: 3055-3060
39. Draviam, RA, Wang, B, Shand, SH, Xiao, X, and Watkins, SC. (2006). Alpha-sarcoglycan is recycled from the plasma membrane in the absence of sarcoglycan complex assembly. Traffic 7: 793-810
40. Bartoli, M, Gicquel, E, Barrault, L, Soheili, T, Malissen, M, Malissen, B, et al. (2008). Mannosidase I inhibition rescues the human alpha-sarcoglycan R77C recurrent mutation. Hum Mol Genet 17: 1214-1221
41. Darabi, R, Arpke, RW, Irion, S, Dimos, JT, Grskovic, M, Kyba, M, et al. (2012). Human ES-, and iPS-derived myogenic progenitors restore DYSTROPHIN, and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 10: 610-619
42. Goudenege, S, Lebel, C, Huot, NB, Dufour, C, Fujii, I, Gekas, J, et al. (2012). Myoblasts derived from normal hESCs, and dystrophic hiPSCs efficiently fuse with existing muscle fibers following transplantation. Mol Ther 20: 2153-2167
43. Tedesco, FS, Gerli, MF, Perani, L, Benedetti, S, Ungaro, F, Cassano, M, et al. (2012). Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci Transl Med 4: 140ra89
44. Tanaka, A, Woltjen, K, Miyake, K, Hotta, A, Ikeya, M, Yamamoto, T, et al. (2013). Efficient, and reproducible myogenic differentiation from human iPS cells: prospects for modeling Miyoshi Myopathy in vitro. PLoS One 8: e61540