Spell Checking Nature: Versatility of CRISPR/Cas9 for Developing Treatments for Inherited Disorders

American Journal of Human Genetics

Volumn 98, Issue 1, 2016, Pages 90-101

  Wojtal, Daria ^a,b   Kemaladewi, Dwi U ^a   Malam, Zeenat ^a   Abdullah, Sarah ^a   Wong, Tatianna W Y ^a   Hyatt, Elzbieta ^a   Baghestani, Zahra ^a   Pereira, Sergio ^a,c   Stavropoulos, James ^d   Mouly, Vincent ^e   Mamchaoui, Kamel ^e   Muntoni, Francesco ^f   Voit, Thomas ^g   Gonorazky, Hernan D ^a,d   Dowling, James J ^a,b,d,h   Wilson, Michael D ^a,b   Mendoza Londono, Roberto ^d,h   Ivakine, Evgueni A ^a   Cohn, Ronald D ^a,b,d,h  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e INSERM   (France)

^f GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

^h HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; FIBROBLAST GROWTH FACTOR RECEPTOR 3; GUIDE RNA; UTROPHIN;

ACHONDROPLASIA; ADULT; ALLELE; ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; EXON; FIBROBLAST; GENETIC DISORDER; GENOME; HUMAN; HUMAN CELL; PRIMARY CELL; PRIORITY JOURNAL; X CHROMOSOME; GENE EXPRESSION; GENETIC DISEASES, INBORN; GENETICS; MUSCULAR DYSTROPHY, DUCHENNE;

ALLELES; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; GENE EXPRESSION; GENETIC DISEASES, INBORN; HUMANS; MUSCULAR DYSTROPHY, DUCHENNE;

EID: 84954388645     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2015.11.012     Document Type: Article

References (68)

1. R. Barrangou, C. Fremaux, H. Deveau, M. Richards, P. Boyaval, S. Moineau, D.A. Romero, and P. Horvath CRISPR provides acquired resistance against viruses in prokaryotes Science 315 2007 1709 1712
2. A. Bolotin, B. Quinquis, A. Sorokin, and S.D. Ehrlich Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin Microbiology 151 2005 2551 2561
3. F.J. Mojica, C. Díez-Villaseñor, J. García-Martínez, and E. Soria Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements J. Mol. Evol. 60 2005 174 182
4. C. Pourcel, G. Salvignol, and G. Vergnaud CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies Microbiology 151 2005 653 663
5. B. Wiedenheft, S.H. Sternberg, and J.A. Doudna RNA-guided genetic silencing systems in bacteria and archaea Nature 482 2012 331 338
6. L. Cong, F.A. Ran, D. Cox, S. Lin, R. Barretto, N. Habib, P.D. Hsu, X. Wu, W. Jiang, L.A. Marraffini, and F. Zhang Multiplex genome engineering using CRISPR/Cas systems Science 339 2013 819 823
7. P. Mali, L. Yang, K.M. Esvelt, J. Aach, M. Guell, J.E. DiCarlo, J.E. Norville, and G.M. Church RNA-guided human genome engineering via Cas9 Science 339 2013 823 826
8. E. Deltcheva, K. Chylinski, C.M. Sharma, K. Gonzales, Y. Chao, Z.A. Pirzada, M.R. Eckert, J. Vogel, and E. Charpentier CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III Nature 471 2011 602 607
9. M. Jinek, K. Chylinski, I. Fonfara, M. Hauer, J.A. Doudna, and E. Charpentier A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science 337 2012 816 821
10. Y. Fu, J.D. Sander, D. Reyon, V.M. Cascio, and J.K. Joung Improving CRISPR-Cas nuclease specificity using truncated guide RNAs Nat. Biotechnol. 32 2014 279 284
11. F.J. Mojica, C. Díez-Villaseñor, J. García-Martínez, and C. Almendros Short motif sequences determine the targets of the prokaryotic CRISPR defence system Microbiology 155 2009 733 740
12. P.D. Hsu, E.S. Lander, and F. Zhang Development and applications of CRISPR-Cas9 for genome engineering Cell 157 2014 1262 1278
13. L.S. Qi, M.H. Larson, L.A. Gilbert, J.A. Doudna, J.S. Weissman, A.P. Arkin, and W.A. Lim Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression Cell 152 2013 1173 1183
14. L.A. Gilbert, M.H. Larson, L. Morsut, Z. Liu, G.A. Brar, S.E. Torres, N. Stern-Ginossar, O. Brandman, E.H. Whitehead, J.A. Doudna, and et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes Cell 154 2013 442 451
15. P. Mali, J. Aach, P.B. Stranges, K.M. Esvelt, M. Moosburner, S. Kosuri, L. Yang, and G.M. Church CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering Nat. Biotechnol. 31 2013 833 838
16. P. Perez-Pinera, D.G. Ousterout, J.M. Brunger, A.M. Farin, K.A. Glass, F. Guilak, G.E. Crawford, A.J. Hartemink, and C.A. Gersbach Synergistic and tunable human gene activation by combinations of synthetic transcription factors Nat. Methods 10 2013 239 242
17. M.L. Maeder, S.J. Linder, V.M. Cascio, Y. Fu, Q.H. Ho, and J.K. Joung CRISPR RNA-guided activation of endogenous human genes Nat. Methods 10 2013 977 979
18. R.R. Beerli, B. Dreier, and C.F. Barbas 3rd Positive and negative regulation of endogenous genes by designed transcription factors Proc. Natl. Acad. Sci. USA 97 2000 1495 1500
19. S. Memedula, and A.S. Belmont Sequential recruitment of HAT and SWI/SNF components to condensed chromatin by VP16 Curr. Biol. 13 2003 241 246
20. I.B. Hilton, A.M. D'Ippolito, C.M. Vockley, P.I. Thakore, G.E. Crawford, T.E. Reddy, and C.A. Gersbach Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers Nat. Biotechnol. 33 2015 510 517
21. X. Huang, Y. Wang, W. Yan, C. Smith, Z. Ye, J. Wang, Y. Gao, L. Mendelsohn, and L. Cheng Production of Gene-Corrected Adult Beta Globin Protein in Human Erythrocytes Differentiated from Patient iPSCs After Genome Editing of the Sickle Point Mutation Stem Cells 33 2015 1470 1479
22. G. Schwank, B.K. Koo, V. Sasselli, J.F. Dekkers, I. Heo, T. Demircan, N. Sasaki, S. Boymans, E. Cuppen, C.K. van der Ent, and et al. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients Cell Stem Cell 13 2013 653 658
23. 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
24. 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
25. 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
26. K. Mamchaoui, C. Trollet, A. Bigot, E. Negroni, S. Chaouch, A. Wolff, P.K. Kandalla, S. Marie, J. Di Santo, J.L. St Guily, and et al. Immortalized pathological human myoblasts: towards a universal tool for the study of neuromuscular disorders Skelet. Muscle 1 2011 34
27. A.W. Cheng, H. Wang, H. Yang, L. Shi, Y. Katz, T.W. Theunissen, S. Rangarajan, C.S. Shivalila, D.B. Dadon, and R. Jaenisch Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system Cell Res. 23 2013 1163 1171
28. F.A. Ran, P.D. Hsu, J. Wright, V. Agarwala, D.A. Scott, and F. Zhang Genome engineering using the CRISPR-Cas9 system Nat. Protoc. 8 2013 2281 2308
29. P.D. Hsu, D.A. Scott, J.A. Weinstein, F.A. Ran, S. Konermann, V. Agarwala, Y. Li, E.J. Fine, X. Wu, O. Shalem, and et al. DNA targeting specificity of RNA-guided Cas9 nucleases Nat. Biotechnol. 31 2013 827 832
30. J.G. Doench, E. Hartenian, D.B. Graham, Z. Tothova, M. Hegde, I. Smith, M. Sullender, B.L. Ebert, R.J. Xavier, and D.E. Root Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation Nat. Biotechnol. 32 2014 1262 1267
31. N.E. Sanjana, O. Shalem, and F. Zhang Improved vectors and genome-wide libraries for CRISPR screening Nat. Methods 11 2014 783 784
32. 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
33. J.M. Tinsley, R.J. Fairclough, R. Storer, F.J. Wilkes, A.C. Potter, S.E. Squire, D.S. Powell, A. Cozzoli, R.F. Capogrosso, A. Lambert, and et al. Daily treatment with SMTC1100, a novel small molecule utrophin upregulator, dramatically reduces the dystrophic symptoms in the mdx mouse PLoS ONE 6 2011 e19189
34. C.L. Dennis, J.M. Tinsley, A.E. Deconinck, and K.E. Davies Molecular and functional analysis of the utrophin promoter Nucleic Acids Res. 24 1996 1646 1652
35. E.A. Burton, J.M. Tinsley, P.J. Holzfeind, N.R. Rodrigues, and K.E. Davies A second promoter provides an alternative target for therapeutic up-regulation of utrophin in Duchenne muscular dystrophy Proc. Natl. Acad. Sci. USA 96 1999 14025 14030
36. A.R. Forrest, H. Kawaji, M. Rehli, J.K. Baillie, M.J. de Hoon, V. Haberle, T. Lassmann, I.V. Kulakovskiy, M. Lizio, M. Itoh, et al. FANTOM Consortium and the RIKEN PMI and CLST (DGT) A promoter-level mammalian expression atlas Nature 507 2014 462 470
37. S. Neph, J. Vierstra, A.B. Stergachis, A.P. Reynolds, E. Haugen, B. Vernot, R.E. Thurman, S. John, R. Sandstrom, A.K. Johnson, and et al. An expansive human regulatory lexicon encoded in transcription factor footprints Nature 489 2012 83 90
38. A. Kundaje, W. Meuleman, J. Ernst, M. Bilenky, A. Yen, A. Heravi-Moussavi, P. Kheradpour, Z. Zhang, J. Wang, M.J. Ziller, et al. Roadmap Epigenomics Consortium Integrative analysis of 111 reference human epigenomes Nature 518 2015 317 330
39. E.P. Consortium ENCODE Project Consortium An integrated encyclopedia of DNA elements in the human genome Nature 489 2012 57 74
40. R. Redon, S. Ishikawa, K.R. Fitch, L. Feuk, G.H. Perry, T.D. Andrews, H. Fiegler, M.H. Shapero, A.R. Carson, W. Chen, and et al. Global variation in copy number in the human genome Nature 444 2006 444 454
41. S. Tuffery-Giraud, C. Béroud, F. Leturcq, R.B. Yaou, D. Hamroun, L. Michel-Calemard, M.P. Moizard, R. Bernard, M. Cossée, P. Boisseau, and 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 2009 934 945
42. R.J. Fairclough, M.J. Wood, and K.E. Davies Therapy for Duchenne muscular dystrophy: renewed optimism from genetic approaches Nat. Rev. Genet. 14 2013 373 378
43. K. Bushby, F. Muntoni, A. Urtizberea, R. Hughes, and R. Griggs Report on the 124th ENMC International Workshop. Treatment of Duchenne muscular dystrophy; defining the gold standards of management in the use of corticosteroids. 2-4 April 2004, Naarden, The Netherlands Neuromuscul. Disord. 14 2004 526 534
44. J. Tinsley, N. Deconinck, R. Fisher, D. Kahn, S. Phelps, J.M. Gillis, and K. Davies Expression of full-length utrophin prevents muscular dystrophy in mdx mice Nat. Med. 4 1998 1441 1444
45. F. Chiaromonte, W. Miller, and E.E. Bouhassira Gene length and proximity to neighbors affect genome-wide expression levels Genome Res. 13 2003 2602 2608
46. T. Gräslund, X. Li, L. Magnenat, M. Popkov, and C.F. Barbas 3rd Exploring strategies for the design of artificial transcription factors: targeting sites proximal to known regulatory regions for the induction of gamma-globin expression and the treatment of sickle cell disease J. Biol. Chem. 280 2005 3707 3714
47. P.M. Van Ry, P. Minogue, B.L. Hodges, and D.J. Burkin Laminin-111 improves muscle repair in a mouse model of merosin-deficient congenital muscular dystrophy Hum. Mol. Genet. 23 2014 383 396
48. C. Smith, L. Abalde-Atristain, C. He, B.R. Brodsky, E.M. Braunstein, P. Chaudhari, Y.Y. Jang, L. Cheng, and Z. Ye Efficient and allele-specific genome editing of disease loci in human iPSCs Mol. Ther. 23 2015 570 577
49. K. Yoshimi, T. Kaneko, B. Voigt, and T. Mashimo Allele-specific genome editing and correction of disease-associated phenotypes in rats using the CRISPR-Cas platform Nat. Commun. 5 2014 4240
50. J.A. Gagnon, E. Valen, S.B. Thyme, P. Huang, L. Akhmetova, A. Pauli, T.G. Montague, S. Zimmerman, C. Richter, and A.F. Schier Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs PLoS ONE 9 2014 e98186
51. M.A. Moreno-Mateos, C.E. Vejnar, J.D. Beaudoin, J.P. Fernandez, E.K. Mis, M.K. Khokha, and A.J. Giraldez CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo Nat. Methods 12 2015 982 988
52. H.J. Lee, E. Kim, and J.S. Kim Targeted chromosomal deletions in human cells using zinc finger nucleases Genome Res. 20 2010 81 89
53. M.C. Canver, D.E. Bauer, A. Dass, Y.Y. Yien, J. Chung, T. Masuda, T. Maeda, B.H. Paw, and S.H. Orkin Characterization of genomic deletion efficiency mediated by clustered regularly interspaced palindromic repeats (CRISPR)/Cas9 nuclease system in mammalian cells J. Biol. Chem. 289 2014 21312 21324
54. S.Q. Tsai, Z. Zheng, N.T. Nguyen, M. Liebers, V.V. Topkar, V. Thapar, N. Wyvekens, C. Khayter, A.J. Iafrate, L.P. Le, and et al. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases Nat. Biotechnol. 33 2015 187 197
55. R. Chiarle, Y. Zhang, R.L. Frock, S.M. Lewis, B. Molinie, Y.J. Ho, D.R. Myers, V.W. Choi, M. Compagno, D.J. Malkin, and et al. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells Cell 147 2011 107 119
56. R.L. Frock, J. Hu, R.M. Meyers, Y.J. Ho, E. Kii, and F.W. Alt Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases Nat. Biotechnol. 33 2015 179 186
57. E. Kimura, S. Li, P. Gregorevic, B.M. Fall, and J.S. Chamberlain Dystrophin delivery to muscles of mdx mice using lentiviral vectors leads to myogenic progenitor targeting and stable gene expression Mol. Ther. 18 2010 206 213
58. Y. Zhang, and D. Duan Novel mini-dystrophin gene dual adeno-associated virus vectors restore neuronal nitric oxide synthase expression at the sarcolemma Hum. Gene Ther. 23 2012 98 103
59. S. Cirak, V. Arechavala-Gomeza, M. Guglieri, L. Feng, S. Torelli, K. Anthony, S. Abbs, M.E. Garralda, J. Bourke, D.J. Wells, and et al. Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study Lancet 378 2011 595 605
60. N.M. Goemans, M. Tulinius, J.T. van den Akker, B.E. Burm, P.F. Ekhart, N. Heuvelmans, T. Holling, A.A. Janson, G.J. Platenburg, J.A. Sipkens, and et al. Systemic administration of PRO051 in Duchenne's muscular dystrophy N. Engl. J. Med. 364 2011 1513 1522
61. Y. Aoki, T. Yokota, T. Nagata, A. Nakamura, J. Tanihata, T. Saito, S.M. Duguez, K. Nagaraju, E.P. Hoffman, T. Partridge, and S. Takeda Bodywide skipping of exons 45-55 in dystrophic mdx52 mice by systemic antisense delivery Proc. Natl. Acad. Sci. USA 109 2012 13763 13768
62. S. Jarmin, H. Kymalainen, L. Popplewell, and G. Dickson New developments in the use of gene therapy to treat Duchenne muscular dystrophy Expert Opin. Biol. Ther. 14 2014 209 230
63. L.V. Nicholson, K.M. Bushby, M.A. Johnson, D. Gardner-Medwin, and I.B. Ginjaar Dystrophin expression in Duchenne patients with "in-frame" gene deletions Neuropediatrics 24 1993 93 97
64. L.V. Nicholson, M.A. Johnson, K.M. Bushby, D. Gardner-Medwin, A. Curtis, I.B. Ginjaar, J.T. den Dunnen, J.L. Welch, T.J. Butler, E. Bakker, and et al. Integrated study of 100 patients with Xp21 linked muscular dystrophy using clinical, genetic, immunochemical, and histopathological data. Part 1. Trends across the clinical groups J. Med. Genet. 30 1993 728 736
65. M. van Putten, M. Hulsker, V.D. Nadarajah, S.H. van Heiningen, E. van Huizen, M. van Iterson, P. Admiraal, T. Messemaker, J.T. den Dunnen, P.A. 't Hoen, and A. Aartsma-Rus The effects of low levels of dystrophin on mouse muscle function and pathology PLoS ONE 7 2012 e31937
66. M. van Putten, M. Hulsker, C. Young, V.D. Nadarajah, H. Heemskerk, L. van der Weerd, P.A. 't Hoen, G.J. van Ommen, and A.M. Aartsma-Rus Low dystrophin levels increase survival and improve muscle pathology and function in dystrophin/utrophin double-knockout mice FASEB J. 27 2013 2484 2495
67. M. van Putten, E.M. van der Pijl, M. Hulsker, I.E. Verhaart, V.D. Nadarajah, L. van der Weerd, and A. Aartsma-Rus Low dystrophin levels in heart can delay heart failure in mdx mice J. Mol. Cell. Cardiol. 69 2014 17 23
68. R. de Vrueh, E.R. Baekelandt, and J.M. de Hann Update on 2004 background paper: BP 6.19 rare diseases 2013 World Health Organization http://www.who.int/medicines/areas/priority-medicines/BP6-19Rare.pdf