Adenoviral vectors encoding CRISPR/Cas9 multiplexes rescue dystrophin synthesis in unselected populations of DMD muscle cells

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Maggio, Ignazio ^a   Liu, Jin ^a   Janssen, Josephine M ^a   Chen, Xiaoyu ^a   Gonçalves, Manuel A F V ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DMD PROTEIN, HUMAN; DYSTROPHIN;

ADENOVIRIDAE; BIOSYNTHESIS; CRISPR CAS SYSTEM; DUCHENNE MUSCULAR DYSTROPHY; GENE EDITING; GENE THERAPY; GENE VECTOR; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MUTATION; PATHOLOGY;

ADENOVIRIDAE; CRISPR-CAS SYSTEMS; DYSTROPHIN; GENE EDITING; GENETIC THERAPY; GENETIC VECTORS; HELA CELLS; HUMANS; MUSCULAR DYSTROPHY, DUCHENNE; MUTATION;

EID: 84995471894     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep37051     Document Type: Article

References (53)

1. Mendell, J. R. et al. Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann. Neurol. 71, 304-313 (2012).
2. Guiraud, S. et al. The Pathogenesis and Therapy of Muscular Dystrophies. Annu. Rev. Genomics. Hum. Genet. 16, 281-308 (2015).
3. Cohn, R. D., Campbell, K. P. Molecular basis of muscular dystrophies. Muscle Nerve 23, 1456-1471 (2000).
4. Hoffman, E. P., Brown, R. H. Jr., Kunkel, L. M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928 (1987).
5. Bladen, C. L. et al. The TREAT-NMD DMD Global Database: analysis of more than 7, 000 Duchenne muscular dystrophy mutations. Hum. Mutat. 36, 395-402 (2015).
6. Guiraud, S., Chen, H., Burns, D. T., Davies, K. E. Advances in genetic therapeutic strategies for Duchenne muscular dystrophy. Exp. Physiol. 100, 1458-1467 (2015).
7. Konieczny, P., Swiderski, K., Chamberlain, J. S. Gene and cell-mediated therapies for muscular dystrophy. Muscle Nerve 47, 649-663 (2013).
8. Chen, X., Gonçalves, M. A. Engineered viruses as genome editing devices. Mol. Ther. 24, 447-457 (2016).
9. Ousterout, D. G. et al. Reading frame correction by targeted genome editing restores dystrophin expression in cells from Duchenne muscular dystrophy patients. Mol. Ther. 21, 1718-1726 (2013).
10. Li, H. L. 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, 143-154 (2015).
11. Ousterout, D. G. et al. Correction of dystrophin expression in cells from Duchenne muscular dystrophy patients through genomic excision of exon 51 by zinc finger nucleases. Mol. Ther. 23, 523-532 (2015).
12. Gaj, T., Gersbach, C. A., Barbas, C. F. 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends. Biotechnol. 31, 397-405 (2013).
13. Maggio, I., Gonçalves, M. A. Genome editing at the crossroads of delivery, specificity, and fidelity. Trends. Biotechnol. 33, 280-291 (2015).
14. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
15. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013).
16. Jinek, M. et al. RNA-programmed genome editing in human cells. eLife 2, e00471 (2013).
17. Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 (2012).
18. Canver, M. C. et al. Characterization of genomic deletion efficiency mediated by clustered regularly interspaced palindromic repeats (CRISPR)/Cas9 nuclease system in mammalian cells. J. Biol. Chem. 289, 21312-21324 (2014).
19. Ousterout, D. G., Kabadi, A. M., Thakore, P. I., Majoros, W. H., Reddy, T. E. Multiplex CRISPR/Cas9-based genome editing for correction of dystrophin mutations that cause Duchenne muscular dystrophy. Nat. Comm. 6, 6244 (2015).
20. Maggio, I. et al. Selection-free gene repair after adenoviral vector transduction of designer nucleases: rescue of dystrophin synthesis in DMD muscle cell populations. Nucleic Acids Res. 44, 1449-1470 (2016).
21. Young, C. S. et al. A Single CRISPR-Cas9 Deletion Strategy that Targets the Majority of DMD Patients Restores Dystrophin Function in hiPSC-Derived Muscle Cells. Cell Stem Cell 18, 533-540 (2016).
22. Xu, L. et al. CRISPR-mediated Genome Editing Restores Dystrophin Expression and Function in mdx Mice. Mol. Ther. 24, 564-569 (2016).
23. Long, C. et al. Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science 351, 400-403 (2016).
24. Nelson, C. E. et al. In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351, 403-407 (2016).
25. Tabebordbar, M. et al. In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science 351, 407-411 (2016).
26. Gonçalves, M. A. et al. Transduction of myogenic cells by retargeted dual high-capacity hybrid viral vectors: robust dystrophin synthesis in duchenne muscular dystrophy muscle cells. Mol. Ther. 13, 976-986 (2006).
27. Knaän-Shanzer, S. et al. Endowing human adenovirus serotype 5 vectors with fiber domains of species B greatly enhances gene transfer into human mesenchymal stem cells. Stem Cells 23, 1598-1607 (2005).
28. Maggio, I. et al. Adenoviral vector delivery of RNA-guided CRISPR/Cas9 nuclease complexes induces targeted mutagenesis in a diverse array of human cells. Sci. Rep. 4, 5105 (2014).
29. Aartsma-Rus, A. et al. Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Hum. Mutat. 30, 293-299 (2009).
30. Prakash, V., Moore, M., Yáñez-Munõz, R. J. Current progress in therapeutic gene editing for monogenic diseases. Mol. Ther. 24, 465-474 (2016).
31. Maggio, I., Chen, X., Gonçalves, M. A. F. V. The emerging role of viral vectors as vehicles for DMD gene editing. Genome Med. 8, 59 (2016).
32. Gonçalves, M. A., de Vries, A. A. Adenovirus: from foe to friend. Rev. Med. Virol. 16, 167-186 (2006).
33. Crystal, R. G. Adenovirus: the first effective in vivo gene delivery vector. Hum. Gene Ther. 25, 3-11 (2014).
34. Holkers, M. et al. Differential integrity of TALE nuclease genes following adenoviral and lentiviral vector gene transfer into human cells. Nucleic Acids Res. 41, e63 (2013).
35. Koenig, M., Monaco, A. P., Kunkel, L. M. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53, 219-228 (1988).
36. Tuffery-Giraud, S. et al. Genotype-phenotype analysis in 2, 405 patients with a dystrophinopathy using the UMD-DMD database: a model of nationwide knowledgebase. Hum. Mutat. 30, 934-945 (2009).
37. Carsana, A. et al. Analysis of dystrophin gene deletions indicates that the hinge III region of the protein correlates with disease severity. Ann. Hum. Genet. 69, 253-259 (2005).
38. Nakamura, A. 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, 757-763 (2008).
39. Taglia, A. et al. Clinical features of patients with dystrophinopathy sharing the 45-55 exon deletion of DMD gene. Acta Myol. 34, 9-13 (2015).
40. van Putten, M. et al. Low dystrophin levels increase survival and improve muscle pathology and function in dystrophin/utrophin double-knockout mice. FASEB J. 27, 2484-2495 (2013).
41. Li, D., Yue, Y., Duan, D. Marginal level dystrophin expression improves clinical outcome in a strain of dystrophin/utrophin double knockout mice. PLoS One 5, e15286 (2010).
42. Briggs, D., Morgan, J. E. Recent progress in satellite cell/myoblast engraftment-relevance for therapy. FEBS J. 280, 4281-4293 (2013).
43. Negroni, E. et al. Invited review: Stem cells and muscle diseases: advances in cell therapy strategies. Neuropathol. App. Neurobiol. 41, 270-287 (2015).
44. McGreevy, J. W., Hakim, C. H., McIntosh, M. A., Duan, D. Animal models of Duchenne muscular dystrophy: from basic mechanisms to gene therapy. Dis. Model. Mec. 8, 195-213 (2015).
45. Wu, X., Kriz, A. J., Sharp, P. A. Target specificity of the CRISPR-Cas9 system. Quant. Biol. 2, 59-70 (2014).
46. Hendel, A., Fine, E. J., Bao, G., Porteus, M. H. Quantifying on-and off-target genome editing. Trends Biotechnol. 33, 132-140 (2015).
47. Havenga, M. J. et al. Serum-free transient protein production system based on adenoviral vector and PER. C6 technology: high yield and preserved bioactivity. Biotechnol. Bioeng. 100, 273-283 (2008).
48. Mamchaoui, K. et al. Immortalized pathological human myoblasts: towards a universal tool for the study of neuromuscular disorders. Skelet. Muscle 1, 34 (2011).
49. Sambrook, J. F., Russell, D. W. Molecular Cloning: A Laboratory Manual. 3rd Ed. Cold Spring Harbor Laboratory Press, NY (2001).
50. Janssen, J. M., Liu, J., Skokan, J., Gonçalves, M. A., de Vries, A. A. Development of an AdEasy-based system to produce first-and second-generation adenoviral vectors with tropism for CAR-or CD46-positive cells. Gene Med. 15, 1-11 (2013).
51. Holkers, M., Cathomen, T., Gonçalves, M. A. Construction and characterization of adenoviral vectors for the delivery of TALENs into human cells. Methods 69, 179-187 (2014).
52. Brinkman, E. K., Chen, T., Amendola, M., van Steensel, B. Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res. 42, e168 (2014).
53. Nicolas, A. et al. Assessment of the structural and functional impact of in-frame mutations of the DMD gene, using the tools included in the eDystrophin online database. Orphanet J. Rare Dis. 7, 45 (2012).