Delivering on the promise of gene editing for cystic fibrosis

Cutting, 2015, Cystic fibrosis genetics: from molecular understanding to clinical application, Nat Rev Genet, 16, 45, 10.1038/nrg3849 Sosnay, 2013, Defining the disease liability of variants in the cystic fibrosis transmembrane conductance regulator gene, Nat Genet, 45, 1160, 10.1038/ng.2745 Bobadilla, 2002, Cystic fibrosis: a worldwide analysis of CFTR mutations--correlation with incidence data and application to screening, Hum Mutat, 19, 575, 10.1002/humu.10041 Drumm, 2012, Genetic variation and clinical heterogeneity in cystic fibrosis, Annu Rev Pathol, 7, 267, 10.1146/annurev-pathol-011811-120900 Egan, 2016, Genetics of cystic fibrosis: clinical implications, Clin Chest Med, 37, 9, 10.1016/j.ccm.2015.11.002 De Lisle, 2013, The cystic fibrosis intestine, Cold Spring Harb Perspect Med, 3, a009753, 10.1101/cshperspect.a009753 Davis, 2006, Cystic fibrosis since 1938, Am J Respir Crit Care Med, 173, 475, 10.1164/rccm.200505-840OE Ramsey, 2011, A CFTR potentiator in patients with cystic fibrosis and the G551D mutation, N Engl J Med, 365, 1663, 10.1056/NEJMoa1105185 Rowe, 2017, Tezacaftor-ivacaftor in residual-function heterozygotes with cystic fibrosis, N Engl J Med, 377, 2024, 10.1056/NEJMoa1709847 Sawicki, 2015, Sustained Benefit from ivacaftor demonstrated by combining clinical trial and cystic fibrosis patient registry data, Am J Respir Crit Care Med, 192, 836, 10.1164/rccm.201503-0578OC Taylor-Cousar, 2017, Tezacaftor-Ivacaftor in Patients with Cystic Fibrosis Homozygous for Phe508del, N Engl J Med, 377, 2013, 10.1056/NEJMoa1709846 Wainwright, 2015, Lumacaftor-Ivacaftor in Patients with Cystic Fibrosis Homozygous for Phe508del CFTR, N Engl J Med, 373, 220, 10.1056/NEJMoa1409547 Davies, 2018, VX-659-Tezacaftor-Ivacaftor in Patients with Cystic Fibrosis and One or Two Phe508del Alleles, N Engl J Med, 379, 1599, 10.1056/NEJMoa1807119 Keating, 2018, VX-445-Tezacaftor-Ivacaftor in Patients with Cystic Fibrosis and One or Two Phe508del Alleles, N Engl J Med, 379, 1612, 10.1056/NEJMoa1807120 Gallagher, 2018, Repair of a site-specific DNA cleavage: old-school lessons for cas9-mediated gene editing, ACS Chem Biol, 13, 397, 10.1021/acschembio.7b00760 Lee, 2015, Mating-type gene switching in Saccharomyces cerevisiae, Microbiol Spectr, 3, 10.1128/microbiolspec.MDNA3-0013-2014 Jasin, 2016, The democratization of gene editing: insights from site-specific cleavage and double-strand break repair, DNA Repair (Amst), 44, 6, 10.1016/j.dnarep.2016.05.001 Fernandez, 2017, A history of genome editing in mammals, Mamm Genome, 28, 237, 10.1007/s00335-017-9699-2 Chandrasegaran, 2016, Origins of programmable nucleases for genome engineering, J Mol Biol, 428, 963, 10.1016/j.jmb.2015.10.014 Hsu, 2014, Development and applications of CRISPR-Cas9 for genome engineering, Cell, 157, 1262, 10.1016/j.cell.2014.05.010 Knott, 2018, CRISPR-Cas guides the future of genetic engineering, Science, 361, 866, 10.1126/science.aat5011 Jackson, 2017, CRISPR-Cas: adapting to change, Science, 356, 10.1126/science.aal5056 Leon, 2018, How bacteria control the CRISPR-Cas arsenal, Curr Opin Microbiol, 42, 87, 10.1016/j.mib.2017.11.005 Jiang, 2017, CRISPR-Cas9 structures and mechanisms, Annu Rev Biophys, 46, 505, 10.1146/annurev-biophys-062215-010822 Hynes, 2014, Adaptation in bacterial CRISPR-Cas immunity can be driven by defective phages, Nat Commun, 5, 4399, 10.1038/ncomms5399 Shou, 2018, Precise and predictable CRISPR chromosomal rearrangements reveal principles of cas9-mediated nucleotide insertion, Mol Cell, 71, 10.1016/j.molcel.2018.06.021 Lemos, 2018, CRISPR/Cas9 cleavages in budding yeast reveal templated insertions and strand-specific insertion/deletion profiles, Proc Natl Acad Sci U S A, 115, E2040, 10.1073/pnas.1716855115 Taheri-Ghahfarokhi, 2018, Decoding non-random mutational signatures at Cas9 targeted sites, Nucleic Acids Res, 46, 8417, 10.1093/nar/gky653 Richardson, 2018, CRISPR-Cas9 genome editing in human cells occurs via the Fanconi anemia pathway, Nat Genet, 50, 1132, 10.1038/s41588-018-0174-0 Chen, 2017, Enhanced proofreading governs CRISPR-Cas9 targeting accuracy, Nature, 550, 407, 10.1038/nature24268 Fu, 2013, High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells, Nat Biotechnol, 31, 822, 10.1038/nbt.2623 Hsu, 2013, DNA targeting specificity of RNA-guided Cas9 nucleases, Nat Biotechnol, 31, 827, 10.1038/nbt.2647 Cong, 2013, Multiplex genome engineering using CRISPR/Cas systems, Science, 339, 819, 10.1126/science.1231143 Cho, 2013, Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease, Nat Biotechnol, 31, 230, 10.1038/nbt.2507 Mali, 2013, RNA-guided human genome engineering via Cas9, Science, 339, 823, 10.1126/science.1232033 Kosicki, 2018, Repair of double-strand breaks induced by CRISPR-Cas9 leads to large deletions and complex rearrangements, Nat Biotechnol, 36, 765, 10.1038/nbt.4192 Wang, 2013, One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering, Cell, 153, 910, 10.1016/j.cell.2013.04.025 Paquet, 2016, Efficient introduction of specific homozygous and heterozygous mutations using CRISPR/Cas9, Nature, 533, 125, 10.1038/nature17664 Capecchi, 2005, Gene targeting in mice: functional analysis of the mammalian genome for the twenty-first century, Nat Rev Genet, 6, 507, 10.1038/nrg1619 Nishiyama, 2017, Virus-mediated genome editing via homology-directed repair in mitotic and postmitotic cells in mammalian brain, Neuron, 96, 755, 10.1016/j.neuron.2017.10.004 Sander, 2014, CRISPR-Cas systems for editing, regulating and targeting genomes, Nat Biotechnol, 32, 347, 10.1038/nbt.2842 Haapaniemi, 2018, CRISPR-Cas9 genome editing induces a p53-mediated DNA damage response, Nat Med, 24, 927, 10.1038/s41591-018-0049-z Ihry, 2018, p53 inhibits CRISPR-Cas9 engineering in human pluripotent stem cells, Nat Med, 24, 939, 10.1038/s41591-018-0050-6 van den Berg, 2018, A limited number of double-strand DNA breaks is sufficient to delay cell cycle progression, Nucleic Acids Res, 46, 10132, 10.1093/nar/gky786 Gaudelli, 2017, Programmable base editing of A*T to G*C in genomic DNA without DNA cleavage, Nature, 551, 464, 10.1038/nature24644 Kim, 2017, Highly efficient RNA-guided base editing in mouse embryos, Nat Biotechnol, 35, 435, 10.1038/nbt.3816 Kim, 2017, Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions, Nat Biotechnol, 35, 371, 10.1038/nbt.3803 Komor, 2016, Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage, Nature, 533, 420, 10.1038/nature17946 Gehrke, 2018, An APOBEC3A-Cas9 base editor with minimized bystander and off-target activities, Nat Biotechnol, 36, 977, 10.1038/nbt.4199 Lei, 2018, APOBEC3 induces mutations during repair of CRISPR-Cas9-generated DNA breaks, Nat Struct Mol Biol, 25, 45, 10.1038/s41594-017-0004-6 Zafra, 2018, Optimized base editors enable efficient editing in cells, organoids and mice, Nat Biotechnol, 36, 888, 10.1038/nbt.4194 Komor, 2018, Editing the genome without double-stranded DNA breaks, ACS Chem Biol, 13, 383, 10.1021/acschembio.7b00710 Rees, 2018, Base editing: precision chemistry on the genome and transcriptome of living cells, Nat Rev Genet, 19, 770, 10.1038/s41576-018-0059-1 McNeer, 2015, Nanoparticles that deliver triplex-forming peptide nucleic acid molecules correct F508del CFTR in airway epithelium, Nat Commun, 6, 6952, 10.1038/ncomms7952 Ricciardi, 2018, In utero nanoparticle delivery for site-specific genome editing, Nat Commun, 9, 2481, 10.1038/s41467-018-04894-2 Ricciardi, 2018, Peptide nucleic acids as a tool for site-specific gene editing, Molecules, 23, 10.3390/molecules23030632 Piel, 2010, Global distribution of the sickle cell gene and geographical confirmation of the malaria hypothesis, Nat Commun, 1, 104, 10.1038/ncomms1104 Romeo, 1989, Why is the cystic fibrosis gene so frequent?, Hum Genet, 84, 1, 10.1007/BF00210660 Farrell, 2018, Estimating the age of p.(Phe508del) with family studies of geographically distinct European populations and the early spread of cystic fibrosis, Eur J Hum Genet, 26, 1832, 10.1038/s41431-018-0234-z Tsui, 2013, The cystic fibrosis gene: a molecular genetic perspective, Cold Spring Harb Perspect Med, 3, a009472, 10.1101/cshperspect.a009472 Cystic Fibrosis Mutation Database (CFTR1). http://www.genet.sickkids.on.ca/cftr/Home.html. Clinical and Functional Translation of CFTR (CFTR2). https://www.cftr2.org. Laoharawee, 2018, Dose-Dependent prevention of metabolic and neurologic disease in murine MPS II by ZFN-mediated in vivo genome editing, Mol Ther, 26, 1127, 10.1016/j.ymthe.2018.03.002 Qasim, 2017, Molecular remission of infant B-ALL after infusion of universal TALEN gene-edited CAR T cells, Sci Transl Med, 9, 10.1126/scitranslmed.aaj2013 Li, 2011, In vivo genome editing restores haemostasis in a mouse model of haemophilia, Nature, 475, 217, 10.1038/nature10177 Sharma, 2015, In vivo genome editing of the albumin locus as a platform for protein replacement therapy, Blood, 126, 1777, 10.1182/blood-2014-12-615492 Amoasii, 2018, Gene editing restores dystrophin expression in a canine model of Duchenne muscular dystrophy, Science, 362, 86, 10.1126/science.aau1549 Yin, 2014, Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype, Nat Biotechnol, 32, 551, 10.1038/nbt.2884 Bednarski, 2016, Targeted Integration of a Super-Exon into the CFTR Locus Leads to Functional Correction of a Cystic Fibrosis Cell Line Model, PloS One, 11, 10.1371/journal.pone.0161072 Harrison, 2018, Gene editing & stem cells, J Cyst Fibros, 17, 10, 10.1016/j.jcf.2017.11.018 Ichise, 2014, The Cd6 gene as a permissive locus for targeted transgenesis in the mouse, Genesis, 52, 440, 10.1002/dvg.22779 Montoliu, 2000, Variegation associated with lacZ in transgenic animals: a warning note, Transgenic Res, 9, 237, 10.1023/A:1008995730285 Robertson, 1995, Position-dependent variegation of globin transgene expression in mice, Proc Natl Acad Sci U S A, 92, 5371, 10.1073/pnas.92.12.5371 Suzuki, 2016, In vivo genome editing via CRISPR/Cas9 mediated homology-independent targeted integration, Nature, 540, 144, 10.1038/nature20565 Bak, 2018, Gene editing on center stage, Trends Genet, 34, 600, 10.1016/j.tig.2018.05.004 Sanz, 2017, Cas9/gRNA targeted excision of cystic fibrosis-causing deep-intronic splicing mutations restores normal splicing of CFTR mRNA, PloS One, 12, 10.1371/journal.pone.0184009 Strug, 2018, Recent advances in developing therapeutics for cystic fibrosis, Hum Mol Genet, 27, R173, 10.1093/hmg/ddy188 Hogan, 2014, Repair and regeneration of the respiratory system: complexity, plasticity, and mechanisms of lung stem cell function, Cell Stem Cell, 15, 123, 10.1016/j.stem.2014.07.012 Randell, 2006, Airway epithelial stem cells and the pathophysiology of chronic obstructive pulmonary disease, Proc Am Thorac Soc, 3, 718, 10.1513/pats.200605-117SF Montoro, 2018, A revised airway epithelial hierarchy includes CFTR-expressing ionocytes, Nature, 560, 319, 10.1038/s41586-018-0393-7 Rock, 2009, Basal cells as stem cells of the mouse trachea and human airway epithelium, Proc Natl Acad Sci U S A, 106, 12771, 10.1073/pnas.0906850106 Plasschaert, 2018, A single-cell atlas of the airway epithelium reveals the CFTR-rich pulmonary ionocyte, Nature, 560, 377, 10.1038/s41586-018-0394-6 Hart, 2017, Genetic therapies for cystic fibrosis lung disease, Curr Opin Pharmacol, 34, 119, 10.1016/j.coph.2017.10.006 Flotte, 1992, Gene expression from adeno-associated virus vectors in airway epithelial cells, Am J Respir Cell Mol Biol, 7, 349, 10.1165/ajrcmb/7.3.349 Rosenfeld, 1992, In vivo transfer of the human cystic fibrosis transmembrane conductance regulator gene to the airway epithelium, Cell, 68, 143, 10.1016/0092-8674(92)90213-V Olsen, 1992, Correction of the apical membrane chloride permeability defect in polarized cystic fibrosis airway epithelia following retroviral-mediated gene transfer, Hum Gene Ther, 3, 253, 10.1089/hum.1992.3.3-253 Stocker, 2009, Single-dose lentiviral gene transfer for lifetime airway gene expression, J Gene Med, 11, 861, 10.1002/jgm.1368 Mitomo, 2010, Toward gene therapy for cystic fibrosis using a lentivirus pseudotyped with Sendai virus envelopes, Mol Ther, 18, 1173, 10.1038/mt.2010.13 Cooney, 2018, Widespread airway distribution and short-term phenotypic correction of cystic fibrosis pigs following aerosol delivery of piggyBac/adenovirus, Nucleic Acids Res, 46, 9591, 10.1093/nar/gky773 Cooney, 2018, Cystic fibrosis gene therapy: looking back, looking forward, Genes (Basel), 9, 10.3390/genes9110538 Alton, 2015, Repeated nebulisation of non-viral CFTR gene therapy in patients with cystic fibrosis: a randomised, double-blind, placebo-controlled, phase 2b trial, Lancet Respir Med, 3, 684, 10.1016/S2213-2600(15)00245-3 Mastorakos, 2015, Highly compacted biodegradable DNA nanoparticles capable of overcoming the mucus barrier for inhaled lung gene therapy, Proc Natl Acad Sci U S A, 112, 8720, 10.1073/pnas.1502281112 Carlon, 2010, Efficient gene transfer into the mouse lung by fetal intratracheal injection of rAAV2/6.2, Mol Ther, 18, 2130, 10.1038/mt.2010.153 Keswani, 2012, Pseudotyped AAV vector-mediated gene transfer in a human fetal trachea xenograft model: implications for in utero gene therapy for cystic fibrosis, PloS One, 7, 10.1371/journal.pone.0043633 Rossidis, 2018, In Utero CRISPR-mediated therapeutic editing of metabolic genes, Nat Med, 24, 1513, 10.1038/s41591-018-0184-6