Targeted inversion and reversion of the blood coagulation factor 8 gene in human iPS cells using TALENs

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 25, 2014, Pages 9253-9258

  Park, Chul Yong ^a   Kim, Jungeun ^b,c   Kweon, Jiyeon ^b,c   Son, Jeong Sang ^d   Lee, Jae Souk ^a   Yoo, Jeong Eun ^a   Cho, Sung Rae ^a   Kim, Jong Hoon ^d   Kim, Jin Soo ^b,c   Kim, Dong Wook ^a  

^a Yonsei University College of Medicine   (South Korea)

^b Institute for Basic Science   (South Korea)

^c Seoul National University   (South Korea)

^d Korea University   (South Korea)

Author keywords

Cas9; CRISPR; Genome editing; ZFN

Indexed keywords

BLOOD CLOTTING FACTOR 8; NUCLEASE; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CHROMOSOME INVERSION; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DISEASE ASSOCIATION; EMBRYO; GENETIC DISORDER; HEMOPHILIA A; HUMAN; HUMAN CELL; MOLECULAR CLONING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVERTANT;

CAS9; CRISPR; GENOME EDITING; ZFN;

CHROMOSOME INVERSION; DEOXYRIBONUCLEASES; FACTOR VIII; GENE TARGETING; HEK293 CELLS; HEMOPHILIA A; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MODELS, BIOLOGICAL;

EID: 84903436131     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1323941111     Document Type: Article

References (55)

1. Graw J, et al. (2005) Haemophilia A: From mutation analysis to new therapies. Nat Rev Genet 6(6):488-501. (Pubitemid 40733893)
2. Bolton-Maggs PH, Pasi KJ (2003) Haemophilias A and B. Lancet 361(9371):1801-1809. (Pubitemid 36638432)
3. Lakich D, Kazazian HH, Jr., Antonarakis SE, Gitschier J (1993) Inversions disrupting the factor VIII gene are a common cause of severe haemophilia A. Nat Genet 5(3):236-241. (Pubitemid 23330385)
4. Naylor J, Brinke A, Hassock S, Green PM, Giannelli F (1993) Characteristic mRNA abnormality found in half the patients with severe haemophilia A is due to large DNA inversions. Hum Mol Genet 2(11):1773-1778. (Pubitemid 23326598)
5. Bagnall RD, Waseem N, Green PM, Giannelli F (2002) Recurrent inversion breaking intron 1 of the factor VIII gene is a frequent cause of severe hemophilia A. Blood 99(1):168-174. (Pubitemid 34532979)
6. Nathwani AC, et al. (2011) Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 365(25):2357-2365.
7. Porteus MH, Baltimore D (2003) Chimeric nucleases stimulate gene targeting in human cells. Science 300(5620):763. (Pubitemid 36532103)
8. Bibikova M, Beumer K, Trautman JK, Carroll D (2003) Enhancing gene targeting with designed zinc finger nucleases. Science 300(5620):764. (Pubitemid 36532104)
9. Urnov FD, et al. (2005) Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435(7042):646-651. (Pubitemid 40825505)
10. Kim HJ, Lee HJ, Kim H, Cho SW, Kim JS (2009) Targeted genome editing in human cells with zinc finger nucleases constructed via modular assembly. Genome Res 19(7):1279-1288.
11. Miller JC, et al. (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29(2):143-148.
12. Kim Y, et al. (2013) A library of TAL effector nucleases spanning the human genome. Nat Biotechnol 31(3):251-258.
13. Kim YK, et al. (2013) TALEN-based knockout library for human microRNAs. Nat Struct Mol Biol 20(12):1458-1464.
14. Cho SW, Lee J, Carroll D, Kim JS, Lee J (2013) Heritable gene knockout in Caenorhabditis elegans by direct injection of Cas9-sgRNA ribonucleoproteins. Genetics 195(3):1177-1180.
15. Sung YH, et al. (2014) Highly efficient gene knockout in mice and zebrafish with RNA-guided endonucleases. Genome Res 24(1):125-131.
16. Cho SW, et al. (2014) Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 24(1):132-141.
17. Cho SW, Kim S, Kim JM, Kim JS (2013) Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 31(3):230-232.
18. Cong L, et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819-823.
19. Hwang WY, et al. (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31(3):227-229.
20. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31(3):233-239.
21. Mali P, et al. (2013) RNA-guided human genome engineering via Cas9. Science 339(6121):823-826.
22. Lee HJ, Kim E, Kim JS (2010) Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res 20(1):81-89.
23. Kim S, Lee HJ, Kim E, Kim JS (2010) Analysis of targeted chromosomal deletions induced by zinc finger nucleases. Cold Spring Harb Protoc 10.1101/pdb.prot5477.
24. Lee HJ, Kweon J, Kim E, Kim S, Kim JS (2012) Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases. Genome Res 22(3):539-548.
25. Feuk L, Carson AR, Scherer SW (2006) Structural variation in the human genome. Nat Rev Genet 7(2):85-97. (Pubitemid 43128895)
26. Zelechowska MG, van Mourik JA, Brodniewicz-Proba T (1985) Ultrastructural localization of factor VIII procoagulant antigen in human liver hepatocytes. Nature 317(6039):729-730. (Pubitemid 16223639)
27. Hollestelle MJ, et al. (2001) Tissue distribution of factor VIII gene expression in vivo - a closer look. Thromb Haemost 86(3):855-861. (Pubitemid 32834197)
28. Shahani T, et al. (2010) Activation of human endothelial cells from specific vascular beds induces the release of a FVIII storage pool. Blood 115(23):4902-4909.
29. Terraube V, O'Donnell JS, Jenkins PV (2010) Factor VIII and von Willebrand factor interaction: Biological, clinical and therapeutic importance. Haemophilia 16(1):3-13.
30. Iafrate AJ, et al. (2004) Detection of large-scale variation in the human genome. Nat Genet 36(9):949-951. (Pubitemid 39167488)
31. Redon R, et al. (2006) Global variation in copy number in the human genome. Nature 444(7118):444-454. (Pubitemid 44809057)
32. Stankiewicz P, Lupski JR (2010) Structural variation in the human genome and its role in disease. Annu Rev Med 61:437-455.
33. Carlson DF, et al. (2012) Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci USA 109(43):17382-17387.
34. Gupta A, et al. (2013) Targeted chromosomal deletions and inversions in zebrafish. Genome Res 23(6):1008-1017.
35. Kim H, Kim JS (2014) A guide to genome engineering with programmable nucleases. Nat Rev Genet 15(5):321-334.
36. Kim S, Lee MJ, Kim H, Kang M, Kim JS (2011) Preassembled zinc-finger arrays for rapid construction of ZFNs. Nat Methods 8(1):7.
37. Kim E, et al. (2012) Precision genome engineering with programmable DNA-nicking enzymes. Genome Res 22(7):1327-1333.
38. Kim Y, Kweon J, Kim JS (2013) TALENs and ZFNs are associated with different mutation signatures. Nat Methods 10(3):185.
39. Sung YH, et al. (2013) Knockout mice created by TALEN-mediated gene targeting. Nat Biotechnol 31(1):23-24.
40. Kim H, et al. (2011) Surrogate reporters for enrichment of cells with nuclease-induced mutations. Nat Methods 8(11):941-943.
41. Kim H, et al. (2013) Magnetic separation and antibiotics selection enable enrichment of cells with ZFN/TALEN-induced mutations. PLoS ONE 8(2):e56476.
42. Ramakrishna S, et al. (2014) Surrogate reporter-based enrichment of cells containing RNA-guided Cas9 nuclease-induced mutations. Nat Commun 5:3378.
43. Nikiforova MN, et al. (2000) Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 290(5489):138-141.
44. Bondeson ML, et al. (1995) Inversion of the IDS gene resulting from recombination with IDS-related sequences is a common cause of the Hunter syndrome. Hum Mol Genet 4(4):615-621.
45. Guo J, Gaj T, Barbas CF, 3rd (2010) Directed evolution of an enhanced and highly efficient FokI cleavage domain for zinc finger nucleases. J Mol Biol 400(1):96-107.
46. Hu Y, Smyth GK (2009) ELDA: Extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 347(1-2):70-78.
47. Kim DS, et al. (2010) Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev 6(2):270-281.
48. Jang J, et al. (2012) Disease-specific induced pluripotent stem cells: A platform for human disease modeling and drug discovery. Exp Mol Med 44(3):202-213.
49. Okita K, et al. (2011) A more efficient method to generate integration-free human iPS cells. Nat Methods 8(5):409-412.
50. Sugii S, et al. (2010) Human and mouse adipose-derived cells support feeder-independent induction of pluripotent stem cells. Proc Natl Acad Sci USA 107(8):3558-3563.
51. Jang J, et al. (2011) Induced pluripotent stem cell models from X-linked adrenoleukodystrophy patients. Ann Neurol 70(3):402-409.
52. Si-Tayeb K, et al. (2010) Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51(1):297-305.
53. Jia F, et al. (2010) A nonviral minicircle vector for deriving human iPS cells. Nat Methods 7(3):197-199.
54. Yoo CH, et al. (2013) Endothelial progenitor cells from human dental pulp-derived iPS cells as a therapeutic target for ischemic vascular diseases. Biomaterials 34(33):8149-8160.
55. Desbordes SC, et al. (2008) High-throughput screening assay for the identification of compounds regulating self-renewal and differentiation in human embryonic stem cells. Cell Stem Cell 2(6):602-612. (Pubitemid 351729221)