A Single CRISPR-Cas9 Deletion Strategy that Targets the Majority of DMD Patients Restores Dystrophin Function in hiPSC-Derived Muscle Cells

Cell Stem Cell

Volumn 18, Issue 4, 2016, Pages 533-540

  Young, Courtney S ^a,b   Hicks, Michael R ^a   Ermolova, Natalia V ^a,b   Nakano, Haruko ^a   Jan, Majib ^a,c   Younesi, Shahab ^a,c   Karumbayaram, Saravanan ^a   Kumagai Cresse, Chino ^a,b   Wang, Derek ^a   Zack, Jerome A ^a   Kohn, Donald B ^a   Nakano, Atsushi ^a   Nelson, Stanley F ^a,b   Miceli, M Carrie ^a   Spencer, Melissa J ^a,b   Pyle, April D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; GLYCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BECKER MUSCULAR DYSTROPHY; CONTROLLED STUDY; CRISPR CAS SYSTEM; DUCHENNE MUSCULAR DYSTROPHY; GENE DELETION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; MOUSE; MYOTUBE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKELETAL MUSCLE; ANIMAL; CYTOLOGY; DEFICIENCY; GENE EDITING; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PATHOLOGY; PROCEDURES; SCID MOUSE;

ANIMALS; CRISPR-CAS SYSTEMS; DYSTROPHIN; GENE DELETION; GENE EDITING; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, SCID; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE;

EID: 84962787321     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2016.01.021     Document Type: Article

References (23)

1. V. Arechavala-Gomeza, K. Anthony, J. Morgan, and F. Muntoni Antisense oligonucleotide-mediated exon skipping for Duchenne muscular dystrophy: progress and challenges Curr. Gene Ther. 12 2012 152 160
2. C. Béroud, S. Tuffery-Giraud, M. Matsuo, D. Hamroun, V. Humbertclaude, N. Monnier, M.P. Moizard, M.A. Voelckel, L.M. Calemard, P. Boisseau, and et al. Multiexon skipping leading to an artificial DMD protein lacking amino acids from exons 45 through 55 could rescue up to 63% of patients with Duchenne muscular dystrophy Hum. Mutat. 28 2007 196 202
3. C.L. Bladen, D. Salgado, S. Monges, M.E. Foncuberta, K. Kekou, K. Kosma, H. Dawkins, L. Lamont, A.J. Roy, T. Chamova, and et al. The TREAT-NMD DMD Global Database: analysis of more than 7,000 Duchenne muscular dystrophy mutations Hum. Mutat. 36 2015 395 402
4. D. Cacchiarelli, T. Incitti, J. Martone, M. Cesana, V. Cazzella, T. Santini, O. Sthandier, and I. Bozzoni miR-31 modulates dystrophin expression: new implications for Duchenne muscular dystrophy therapy EMBO Rep. 12 2011 136 141
5. A. Carsana, G. Frisso, M.R. Tremolaterra, R. Lanzillo, D.F. Vitale, L. Santoro, and F. Salvatore Analysis of dystrophin gene deletions indicates that the hinge III region of the protein correlates with disease severity Ann. Hum. Genet. 69 2005 253 259
6. T.J. Cradick, P. Qiu, C.M. Lee, E.J. Fine, and G. Bao COSMID: A web-based tool for identifying and validating CRISPR/Cas off-target sites Mol. Ther. Nucleic Acids 3 2014 e214
7. M. Dekel-Naftali, A. Aviram-Goldring, T. Litmanovitch, J. Shamash, H. Reznik-Wolf, I. Laevsky, M. Amit, J. Itskovitz-Eldor, Y. Yung, A. Hourvitz, and et al. Screening of human pluripotent stem cells using CGH and FISH reveals low-grade mosaic aneuploidy and a recurrent amplification of chromosome 1q Eur. J. Hum. Genet. 20 2012 1248 1255
8. Y. Echigoya, Y. Aoki, B. Miskew, D. Panesar, A. Touznik, T. Nagata, J. Tanihata, A. Nakamura, K. Nagaraju, and T. Yokota Long-term efficacy of systemic multiexon skipping targeting dystrophin exons 45-55 with a cocktail of vivo-morpholinos in mdx52 mice Mol. Ther. Nucleic Acids 4 2015 e225
9. X. Guan, D.L. Mack, C.M. Moreno, J.L. Strande, J. Mathieu, Y. Shi, C.D. Markert, Z. Wang, G. Liu, M.W. Lawlor, and et al. Dystrophin-deficient cardiomyocytes derived from human urine: new biologic reagents for drug discovery Stem Cell Res. (Amst.) 12 2014 467 480
10. S.Q. Harper, M.A. Hauser, C. DelloRusso, D. Duan, R.W. Crawford, S.F. Phelps, H.A. Harper, A.S. Robinson, J.F. Engelhardt, S.V. Brooks, and J.S. Chamberlain Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy Nat. Med. 8 2002 253 261
11. H.L. Li, N. Fujimoto, N. Sasakawa, S. Shirai, T. Ohkame, T. Sakuma, M. Tanaka, N. Amano, A. Watanabe, H. Sakurai, and et al. Precise correction of the dystrophin gene in duchenne muscular dystrophy patient induced pluripotent stem cells by TALEN and CRISPR-Cas9 Stem Cell Reports 4 2015 143 154
12. C. Long, J.R. McAnally, J.M. Shelton, A.A. Mireault, R. Bassel-Duby, and E.N. Olson Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA Science 345 2014 1184 1188
13. C. Long, L. Amoasii, A.A. Mireault, J.R. McAnally, H. Li, E. Sanchez-Ortiz, S. Bhattacharyya, J.M. Shelton, R. Bassel-Duby, and E.N. Olson Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy Science 351 2016 400 403
14. A. Menke, and H. Jockusch Extent of shock-induced membrane leakage in human and mouse myotubes depends on dystrophin J. Cell Sci. 108 1995 727 733
15. A. Nakamura, K. Yoshida, K. Fukushima, H. Ueda, N. Urasawa, J. Koyama, Y. Yazaki, M. Yazaki, T. Sakai, S. Haruta, and et al. Follow-up of three patients with a large in-frame deletion of exons 45-55 in the Duchenne muscular dystrophy (DMD) gene J. Clin. Neurosci. 15 2008 757 763
16. C.E. Nelson, C.H. Hakim, D.G. Ousterout, P.I. Thakore, E.A. Moreb, R.M.C. Rivera, S. Madhavan, X. Pan, F.A. Ran, W.X. Yan, and et al. In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy Science 351 2016 403 407
17. D.G. Ousterout, A.M. Kabadi, P.I. Thakore, W.H. Majoros, T.E. Reddy, and C.A. Gersbach Multiplex CRISPR/Cas9-based genome editing for correction of dystrophin mutations that cause Duchenne muscular dystrophy Nat. Commun. 6 2015 6244
18. T. Partridge Myoblast transplantation Neuromuscul. Disord. 12 Suppl 1 2002 S3 S6
19. J.M.S. Pearce, R.J.T. Pennington, and J.N. Walton Serum enzyme studies in muscle disease: Part III Serum creatine kinase activity in relatives of patients with the Duchenne type of muscular dystrophy J. Neurol. Neurosurg. Psychiatry 27 1964 181 185
20. M. Tabebordbar, K. Zhu, J.K.W. Cheng, W.L. Chew, J.J. Widrick, W.X. Yan, C. Maesner, E.Y. Wu, R. Xiao, F.A. Ran, and et al. In vivo gene editing in dystrophic mouse muscle and muscle stem cells Science 351 2016 407 411
21. A. Taglia, R. Petillo, P. D'Ambrosio, E. Picillo, A. Torella, C. Orsini, M. Ergoli, M. Scutifero, L. Passamano, A. Palladino, and et al. Clinical features of patients with dystrophinopathy sharing the 45-55 exon deletion of DMD gene Acta Myol. 34 2015 9 13
22. D. Wojtal, D.U. Kemaladewi, Z. Malam, S. Abdullah, T.W.Y. Wong, E. Hyatt, Z. Baghestani, S. Pereira, J. Stavropoulos, V. Mouly, and et al. Spell Checking Nature: Versatility of CRISPR/Cas9 for Developing Treatments for Inherited Disorders Am. J. Hum. Genet. 98 2016 90 101
23. L. Xu, K.H. Park, L. Zhao, J. Xu, M. El Refaey, Y. Gao, H. Zhu, J. Ma, and R. Han CRISPR-mediated genome editing restores dystrophin expression and function in mdx mice Mol. Ther. 2015 10.1038/mt.2015.192 in press. Published online October 9, 2015