CRISPR-mediated genotypic and phenotypic correction of a chronic granulomatous disease mutation in human iPS cells

Experimental Hematology

Volumn 43, Issue 10, 2015, Pages 838-848.e3

  Flynn, Rowan ^a   Grundmann, Alexander ^a   Renz, Peter ^a   Hänseler, Walther ^a   James, William S ^a   Cowley, Sally A ^a   Moore, Michael D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME B; CYTOCHROME B 245 HEAVY CHAIN PROTEIN; MESSENGER RNA; OLIGONUCLEOTIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG; CYBB PROTEIN, HUMAN; MEMBRANE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CELL LINE; CGD2 CELL LINE; CHRONIC GRANULOMATOUS DISEASE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; CYBB GENE; EXON; GENE; GENE LOCUS; GENOTYPE; HEK293 CELL LINE; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; INTRON; MUTATIONAL ANALYSIS; OXIDATIVE STRESS; PHAGOCYTE; PHENOTYPE; PLURIPOTENT STEM CELL; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA EDITING; BIOSYNTHESIS; CRISPR CAS SYSTEM; ENZYMOLOGY; GENE THERAPY; GENETICS; GRANULOMATOUS DISEASE, CHRONIC; INDUCED PLURIPOTENT STEM CELL; MUTATION; PATHOLOGY; RESPIRATORY BURST;

CRISPR-CAS SYSTEMS; GENETIC THERAPY; GRANULOMATOUS DISEASE, CHRONIC; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INTRONS; MEMBRANE GLYCOPROTEINS; MUTATION; NADPH OXIDASE; RESPIRATORY BURST;

EID: 84942519810     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2015.06.002     Document Type: Article

References (50)

1. Li H.L., 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, 4:143-154.
2. Yusa K., Rashid S.T., Strick-Marchand H., et al. Targeted gene correction of alpha1-antitrypsin deficiency in induced pluripotent stem cells. Nature 2011, 478:391-394.
3. Segal B.H., Leto T.L., Gallin J.I., Malech H.L., Holland S.M. Genetic, biochemical, and clinical features of chronic granulomatous disease. Medicine (Baltimore) 2000, 79:170-200.
4. Ott M.G., Schmidt M., Schwarzwaelder K., et al. Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat Med 2006, 12:401-409.
5. Stein S., Ott M.G., Schultze-Strasser S., et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med 2010, 16:198-204.
6. Dorer M.S., Sessler T.H., Salama N.R. Recombination and DNA repair in Helicobacter pylori. Annu Rev Microbiol 2011, 65:329-348.
7. ten Asbroek A.L., Ouellette M., Borst P. Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature 1990, 348:174-175.
8. Thomas K.R., Capecchi M.R. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 1987, 51:503-512.
9. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337:816-821.
10. Mali P., Yang L., Esvelt K.M., et al. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
11. Roos D. The genetic basis of chronic granulomatous disease. Immunol Rev 1994, 138:121-157.
12. Jiang Y., Cowley S.A., Siler U., et al. Derivation and functional analysis of patient-specific induced pluripotent stem cells as an in vitro model of chronic granulomatous disease. Stem Cells 2012, 30:599-611.
13. Brault J., Goutagny E., Telugu N., et al. Optimized generation of functional neutrophils and macrophages from patient-specific induced pluripotent stem cells: Ex vivo models of X(0)-linked, AR22(0)- and AR47(0)- chronic granulomatous diseases. Biores Open Access 2014, 3:311-326.
14. Hartfield E.M., Yamasaki-Mann M., Ribeiro H.J., et al. Physiological characterisation of human iPS-derived dopaminergic neurons. PLoS One 2014, 9:e87388.
15. van Wilgenburg B., Browne C., Vowles J., Cowley S.A. Efficient, long term production of monocyte-derived macrophages from human pluripotent stem cells under partly-defined and fully-defined conditions. PLoS One 2013, 8:e71098.
16. Cong L., Ran F.A., Cox D., et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
17. Demaison C., Parsley K., Brouns G., et al. High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency correction of imunodeficiency. virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther 2002, 13:803-813.
18. Matsuda T., Cepko C.L. Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc Natl Acad Sci U S A 2004, 101:16-22.
19. Chia R., Achilli F., Festing M.F., Fisher E.M. The origins and uses of mouse outbred stocks. Nat Genet 2005, 37:1181-1186.
20. Gardner R.L. Investigation of cell lineage and differentiation in the extraembryonic endoderm of the mouse embryo. J Embryol Exp Morphol 1982, 68:175-198.
21. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
22. Holland S.M. Chronic granulomatous disease. Clin Rev Allergy Immunol 2012, 38:3-10.
23. Mardiney M., Jackson S.H., Spratt S.K., Li F., Holland S.M., Malech H.L. Enhanced host defense after gene transfer in the murine p47phox-deficient model of chronic granulomatous disease. Blood 1997, 89:2268-2275.
24. Woodman R.C., Newburger P.E., Anklesaria P., et al. A new X-linked variant of chronic granulomatous disease characterized by the existence of a normal clone of respiratory burst-competent phagocytic cells. Blood 1995, 85:231-241.
25. Ran F.A., Hsu P.D., Lin C.Y., et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 2013, 154:1380-1389.
26. Karlsson K.R., Cowley S., Martinez F.O., et al. Homogeneous monocytes and macrophages from human embryonic stem cells following coculture-free differentiation in M-CSF and IL-3. Exp Hematol 2008, 36:1167-1175.
27. Henderson L.M., Chappell J.B. Dihydrorhodamine 123: A fluorescent probe for superoxide generation?. Eur J Biochem 1993, 217:973-980.
28. Mukherjee S., Santilli G., Blundell M.P., Navarro S., Bueren J.A., Thrasher A.J. Generation of functional neutrophils from a mouse model of X-linked chronic granulomatous disorder using induced pluripotent stem cells. PLoS One 2011, 6:e17565.
29. Brendel C., Hänseler W., Wohlgensinger V., et al. Human miR223 promoter as a novel myelo-specific promoter for chronic granulomatous disease gene therapy. Hum Gene Ther Methods 2013, 24:151-159.
30. Chiriaco M., Farinelli G., Capo V., et al. Dual-regulated lentiviral vector for gene therapy of X-linked chronic granulomatosis. Mol Ther 2014, 22:1472-1483.
31. Santilli G., Almarza E., Brendel C., et al. Biochemical correction of X-CGD by a novel chimeric promoter regulating high levels of transgene expression in myeloid cells. Mol Ther 2011, 19:122-132.
32. Merling R.K., Sweeney C.L., Chu J., et al. An AAVS1-targeted minigene platform for correction of iPSCs from all five types of chronic granulomatous disease. Mol Ther 2015, 23:147-157.
33. Zou J., Sweeney C.L., Chou B.K., et al. Oxidase-deficient neutrophils from X-linked chronic granulomatous disease iPS cells: Functional correction by zinc finger nuclease-mediated safe harbor targeting. Blood 2011, 117:5561-5572.
34. Meischl C., Boer M., Ahlin A., Roos D. A new exon created by intronic insertion of a rearranged LINE-1 element as the cause of chronic granulomatous disease. Eur J Hum Genet 2000, 8:697-703.
35. Genovese P., Schiroli G., Escobar G., et al. Targeted genome editing in human repopulating haematopoietic stem cells. Nature 2014, 510:235-240.
36. McKinney-Freeman S., Cahan P., Li H., et al. The transcriptional landscape of hematopoietic stem cell ontogeny. Cell Stem Cell 2012, 11:701-714.
37. Park T.S., Zimmerlin L., Zambidis E.T. Efficient and simultaneous generation of hematopoietic and vascular progenitors from human induced pluripotent stem cells. Cytometry A 2013, 83:114-126.
38. Vandekerckhove B., Vanhee S., Van Coppernolle S., et al. In vitro generation of immune cells from pluripotent stem cells. Front Biosci (Landmark Ed) 2011, 16:1488-1504.
39. Bai Q., Ramirez J.M., Becker F., et al. Temporal analysis of genome alterations induced by single-cell passaging in human embryonic stem cells. Stem Cells Dev 2015, 24:653-662.
40. Cheng L., Hansen N.F., Zhao L., et al. Low incidence of DNA sequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression. Cell Stem Cell 2012, 10:337-344.
41. Laurent L.C., Ulitsky I., Slavin I., et al. Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell 2011, 8:106-118.
42. Lefort N., Feyeux M., Bas C., et al. Human embryonic stem cells reveal recurrent genomic instability at 20q11.21. Nat Biotechnol 2008, 26:1364-1366.
43. Mayshar Y., Ben-David U., Lavon N., et al. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 2010, 7:521-531.
44. Quinlan A.R., Boland M.J., Leibowitz M.L., et al. Genome sequencing of mouse induced pluripotent stem cells reveals retroelement stability and infrequent DNA rearrangement during reprogramming. Cell Stem Cell 2011, 9:366-373.
45. Cradick T.J., Fine E.J., Antico C.J., Bao G. CRISPR/Cas9 systems targeting beta-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res 2013, 41:9584-9592.
46. Fu Y., Foden J.A., Khayter C., et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 2013, 31:822-826.
47. Cho S.W., Kim S., Kim Y., et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 2014, 24:132-141.
48. Tebas P., Stein D., Tang W.W., et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N Engl J Med 2014, 370:901-910.
49. Marques B., Liguori L., Paclet M.H., et al. Liposome-mediated cellular delivery of active gp91(phox). PLoS One 2007, 2:e856.
50. Taylor R.M., Burritt J.B., Baniulis D., et al. Site-specific inhibitors of NADPH oxidase activity and structural probes of flavocytochrome b: characterization of six monoclonal antibodies to the p22phox subunit. J Immunol 2004, 173:7349-7357.