Genome editing of monogenic neuromuscular diseases: A systematic review

JAMA Neurology

Volumn 73, Issue 11, 2016, Pages 1349-1355

  Long, Chengzu ^a   Amoasii, Leonela ^a   Bassel Duby, Rhonda ^a   Olson, Eric N ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CRISPR ASSOCIATED PROTEIN; DNA; DYSTROPHIN; LIPOSOME; NANOMATERIAL; PARVOVIRUS VECTOR; POLYMER; RNA; SURVIVAL MOTOR NEURON PROTEIN 1; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; ZINC FINGER NUCLEASE;

AMYOTROPHIC LATERAL SCLEROSIS; CELL CULTURE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CRISPR CAS SYSTEM; DNA END JOINING REPAIR; DNA STRAND BREAKAGE; DUCHENNE MUSCULAR DYSTROPHY; EXON SKIPPING; FEASIBILITY STUDY; GENETIC ENGINEERING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTERNET; MUSCULAR DYSTROPHY; MYOTONIC DYSTROPHY; NEUROMUSCULAR DISEASE; NONVIRAL GENE DELIVERY SYSTEM; PATIENT SAFETY; PRIORITY JOURNAL; REVIEW; RNA EDITING; SPINAL MUSCULAR ATROPHY; SYSTEMATIC REVIEW; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM; ANIMAL; GENE EDITING; GENE THERAPY; GENETICS; MUSCULAR ATROPHY, SPINAL; MUSCULAR DYSTROPHY, DUCHENNE; PROCEDURES;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; GENE EDITING; GENETIC THERAPY; HUMANS; MUSCULAR ATROPHY, SPINAL; MUSCULAR DYSTROPHY, DUCHENNE; MYOTONIC DYSTROPHY;

EID: 84996629778     PISSN: 21686149     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamaneurol.2016.3388     Document Type: Review

References (58)

1. World Health Organization. Genes and human disease. http://www.who.int/genomics/public/geneticdiseases/en/index2.html. Accessed August 19, 2016.
2. Kaplan JC, Hamroun D. The 2016 version of the gene table of monogenic neuromuscular disorders (nuclear genome). Neuromuscul Disord. 2015;25 (12):991-1020.
3. Pósfai G, Kolisnychenko V, Bereczki Z, Blattner FR. Markerless gene replacement in Escherichia coli stimulated by a double-strand break in the chromosome. Nucleic Acids Res. 1999;27(22): 4409-4415.
4. Kim YG, Cha J, Chandrasegaran S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A. 1996;93 (3):1156-1160.
5. Kim JS, Lee HJ, Carroll D. Genome editing with modularly assembled zinc-finger nucleases. Nat Methods. 2010;7(2):91-92.
6. Christian M, Cermak T, Doyle EL, et al. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics. 2010;186(2):757-761.
7. Cong L, Ran FA, Cox D, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819-823.
8. Mali P, Yang L, Esvelt KM, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339(6121):823-826.
9. Symington LS, Gautier J. Double-strand break end resection and repair pathway choice. Annu Rev Genet. 2011;45:247-271.
10. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096): 816-821.
11. Zetsche B, Gootenberg JS, Abudayyeh OO, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 2015;163(3):759-771.
12. Schwank G, Koo BK, Sasselli V, et al. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell. 2013;13(6):653-658.
13. Swiech L, Heidenreich M, Banerjee A, et al. In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat Biotechnol. 2015;33(1):102-106.
14. Yin H, Song CQ, Dorkin JR, et al. Therapeutic genome editing by combined viral and non-viral delivery of CRISPR system components in vivo. Nat Biotechnol. 2016;34(3):328-333.
15. Yang Y,Wang L, Bell P, et al. A dual AAV system enables the Cas9-mediated correction of a metabolic liver disease in newborn mice. Nat Biotechnol. 2016;34(3):334-338.
16. Long C, Amoasii L, Mireault AA, et al. Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science. 2016;351(6271):400-403.
17. Nelson CE, Hakim CH, Ousterout DG, et al. In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science. 2016;351(6271):403-407.
18. Tabebordbar M, Zhu K, Cheng JK, et al. In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science. 2016;351(6271):407-411.
19. Mendell JR, Shilling C, Leslie ND, et al. Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann Neurol. 2012;71 (3):304-313.
20. Fairclough RJ,Wood MJ, Davies KE. Therapy for Duchenne muscular dystrophy: renewed optimism from genetic approaches. Nat Rev Genet. 2013;14(6):373-378.
21. Long C,McAnally JR, Shelton JM, Mireault AA, Bassel-Duby R, Olson EN. Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA. Science. 2014;345(6201): 1184-1188.
22. Xu L, Park KH, Zhao L, et al. CRISPR-mediated genome editing restores dystrophin expression and function in mdx mice. Mol Ther. 2016;24(3):564-569.
23. Li HL, Fujimoto N, Sasakawa N, 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. 2015;4(1):143-154.
24. Ousterout DG, Kabadi AM, Thakore PI, Majoros WH, Reddy TE, Gersbach CA. Multiplex CRISPR/Cas9-based genome editing for correction of dystrophin mutations that cause Duchenne muscular dystrophy. Nat Commun. 2015;6:6244.
25. Wojtal D, Kemaladewi DU, Malam Z, et al. Spell checking nature: versatility of CRISPR/Cas9 for developing treatments for inherited disorders. Am J Hum Genet. 2016;98(1):90-101.
26. Maggio I, Stefanucci L, Janssen JM, 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. 2016;44(3): 1449-1470.
27. Iyombe-Engembe JP, Ouellet DL, Barbeau X, et al. Efficient restoration of the dystrophin gene reading frame and protein structure in DMD myoblasts using the CinDel method. Mol Ther Nucleic Acids. 2016;5:e283.
28. Young CS, Hicks MR, Ermolova NV, 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. 2016;18(4):533-540.
29. Aartsma-Rus A. Overview on DMD exon skipping. Methods Mol Biol. 2012;867:97-116.
30. Mikuni T, Nishiyama J, Sun Y, Kamasawa N, Yasuda R. High-throughput, high-resolution mapping of protein localization in mammalian brain by in vivo genome editing. Cell. 2016;165(7): 1803-1817.
31. National Human Genome Research Institute. Learning about spinal muscular atrophy. https://www.genome.gov/20519681/learning-about-spinal-muscular-atrophy/#top. Updated February 19, 2012. Accessed August 19, 2016.
32. Hendrickson BC, Donohoe C, Akmaev VR, et al. Differences in SMN1 allele frequencies among ethnic groups within North America. J Med Genet. 2009;46(9):641-644.
33. Mercuri E, Bertini E, Iannaccone ST. Childhood spinal muscular atrophy: controversies and challenges. Lancet Neurol. 2012;11(5):443-452.
34. Lorson CL, Hahnen E, Androphy EJ, Wirth B. A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc Natl Acad Sci U S A. 1999;96(11): 6307-6311.
35. Corti S, Nizzardo M, Simone C, et al. Genetic correction of human induced pluripotent stem cells from patients with spinal muscular atrophy. Sci Transl Med. 2012;4(165):165ra162.
36. Ogino S, Gao S, Leonard DG, Paessler M, Wilson RB. Inverse correlation between SMN1 and SMN2 copy numbers: evidence for gene conversion from SMN2 to SMN1. Eur J Hum Genet. 2003;11(9): 723.
37. DiMatteo D, Callahan S, Kmiec EB. Genetic conversion of an SMN2 gene to SMN1: A novel approach to the treatment of spinal muscular atrophy. Exp Cell Res. 2008;314(4):878-886.
38. DeJesus-Hernandez M, Mackenzie IR, Boeve BF, et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron. 2011; 72(2):245-256.
39. Mutihac R, Ababneh N, Scaber J,Wade-Martins R, Cowley S, Talbot K. Modelling amyotrophic lateral sclerosis (ALS) using mutant and CAS9/CRISPR-corrected motor neurons from patients with C9ORF72 mutations reveals disease-specific cellular phenotypes. J Neurol Sci. 2015;357(suppl 1):e48.
40. National Human Genome Research Institute. Learning more aboutmyotonic dystrophy. https://www.genome.gov/25521207/learning-about-myotonic-dystrophy/. Updated June 4, 2012. Accessed August 19, 2016.
41. Meola G, Cardani R. Myotonic dystrophies: an update on clinical aspects, genetic, pathology, and molecular pathomechanisms. Biochim Biophys Acta. 2015;1852(4):594-606.
42. Lee JE, Cooper TA. Pathogenic mechanisms of myotonic dystrophy. Biochem Soc Trans. 2009;37(pt 6):1281-1286.
43. Gao Y, Guo X, Santostefano K, et al. Genome therapy ofmyotonic dystrophy type 1 iPS cells for development of autologous stem cell therapy [published online June 28, 2016]. Mol Ther. doi:10 .1038/mt.2016.97
44. Cummings CJ, Zoghbi HY. Fourteen and counting: unraveling trinucleotide repeat diseases. Hum Mol Genet. 2000;9(6):909-916.
45. Hsu PD, Scott DA,Weinstein JA, et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol. 2013;31(9):827-832.
46. Jiang F, Taylor DW, Chen JS, et al. Structures of a CRISPR-Cas9 R-loop complex primed for DNA cleavage. Science. 2016;351(6275):867-871.
47. Nishimasu H, Ran FA, Hsu PD, et al. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell. 2014;156(5):935-949.
48. Mali P, Aach J, Stranges PB, et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol. 2013;31(9): 833-838.
49. Shen B, ZhangW, Zhang J, et al. Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat Methods. 2014;11(4): 399-402.
50. Ran FA, Hsu PD, Lin CY, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell. 2013;154(6):1380-1389.
51. Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol. 2014;32(3): 279-284.
52. Hsu PD, Scott DA,Weinstein JA, et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol. 2013;31(9):827-832.
53. Kleinstiver BP, Pattanayak V, Prew MS, et al. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature. 2016;529(7587):490-495.
54. Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F. Rationally engineered Cas9 nucleases with improved specificity. Science. 2016; 351(6268):84-88.
55. Maggio I, Chen X, Gonçalves MA. The emerging role of viral vectors as vehicles for DMD gene editing. Genome Med. 2016;8(1):59.
56. Burrow KL, Coovert DD, Klein CJ, et al; CIDD Study Group. Dystrophin expression and somatic reversion in prednisone-treated and untreated Duchenne dystrophy. Neurology. 1991;41(5):661-666.
57. Carroll KJ, Makarewich CA,McAnally J, et al. A mouse model for adult cardiac-specific gene deletion with CRISPR/Cas9. Proc Natl Acad Sci U S A. 2016;113(2):338-343.
58. Dow LE, Fisher J, O'Rourke KP, et al. Inducible in vivo genome editing with CRISPR-Cas9. Nat Biotechnol. 2015;33(4):390-394.