Efficient CRISPR-Cas9-Mediated Generation of Knockin Human Pluripotent Stem Cells Lacking Undesired Mutations at the Targeted Locus

Cell Reports

Volumn 11, Issue 6, 2015, Pages 875-883

  Merkle, Florian T ^a,b,c,d   Neuhausser, Werner M ^a,b,d,e,f   Santos, David ^a,b   Valen, Eivind ^b,g   Gagnon, James A ^b   Maas, Kristi ^a,b,d,e,f   Sandoe, Jackson ^a,b   Schier, Alexander F ^b,d,h   Eggan, Kevin ^a,b,c,d  

^a Harvard University   (United States)

^b HARVARD UNIVERSITY   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d HARVARD STEM CELL INSTITUTE   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f BOSTON IVF   (United States)

^g UNIVERSITY OF BERGEN   (Norway)

^h MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; NUCLEASE; PROTEIN CAS9; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CONTROLLED STUDY; GENE FUNCTION; GENE INACTIVATION; GENE LOCUS; GENE MUTATION; GENE TARGETING; HETEROZYGOTE; HUMAN; HUMAN CELL; INDEL MUTATION; MOLECULAR CLONING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; CELL CLONE; CRISPR CAS SYSTEM; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROCEDURES;

BASE SEQUENCE; CLONE CELLS; CRISPR-CAS SYSTEMS; GENE KNOCK-IN TECHNIQUES; GENE TARGETING; GENETIC LOCI; HUMANS; INDEL MUTATION; MOLECULAR SEQUENCE DATA; MUTATION; PLURIPOTENT STEM CELLS;

EID: 84929276488     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.04.007     Document Type: Article

References (49)

1. Barrangou R., Fremaux C., Deveau H., Richards M., Boyaval P., Moineau S., Romero D.A., Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007, 315:1709-1712.
2. Bellin M., Marchetto M.C., Gage F.H., Mummery C.L. Induced pluripotent stem cells: the new patient?. Nat. Rev. Mol. Cell Biol. 2012, 13:713-726.
3. Byrne S.M., Mali P., Church G.M. Genome editing in human stem cells. Methods Enzymol. 2014, 546:119-138.
4. Chen G., Gulbranson D.R., Hou Z., Bolin J.M., Ruotti V., Probasco M.D., Smuga-Otto K., Howden S.E., Diol N.R., Propson N.E., et al. Chemically defined conditions for human iPSC derivation and culture. Nat. Methods 2011, 8:424-429.
5. Cho S.W., Kim S., Kim J.M., Kim J.S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 2013, 31:230-232.
6. Cho S.W., Kim S., Kim Y., Kweon J., Kim H.S., Bae S., Kim J.-S. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res. 2014, 24:132-141.
7. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A., Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
8. Egawa N., Kitaoka S., Tsukita K., Naitoh M., Takahashi K., Yamamoto T., Adachi F., Kondo T., Okita K., Asaka I., et al. Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci. Transl. Med. 2012, 4:ra104.
9. Elliott B., Richardson C., Winderbaum J., Nickoloff J.A., Jasin M. Gene conversion tracts from double-strand break repair in mammalian cells. Mol. Cell. Biol. 1998, 18:93-101.
10. Frock R.L., Hu J., Meyers R.M., Ho Y.-J., Kii E., Alt F.W. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat. Biotechnol. 2015, 33:179-186.
11. Fu Y., Foden J.A., Khayter C., Maeder M.L., Reyon D., Joung J.K., Sander J.D. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 2013, 31:822-826.
12. Fu Y., Sander J.D., Reyon D., Cascio V.M., Joung J.K. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 2014, 32:279-284.
13. Gagnon J.A., Valen E., Thyme S.B., Huang P., Ahkmetova L., Pauli A., Montague T.G., Zimmerman S., Richter C., Schier A.F. Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. PLoS ONE 2014, 9:e98186.
14. Garneau J.E., Dupuis M.-È., Villion M., Romero D.A., Barrangou R., Boyaval P., Fremaux C., Horvath P., Magadán A.H., Moineau S. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 2010, 468:67-71.
15. González F., Zhu Z., Shi Z.D., Lelli K., Verma N., Li Q.V., Huangfu D. An iCRISPR platform for rapid, multiplexable, and inducible genome editing in human pluripotent stem cells. Cell Stem Cell 2014, 15:215-226.
16. Goulburn A.L., Alden D., Davis R.P., Micallef S.J., Ng E.S., Yu Q.C., Lim S.M., Soh C.-L., Elliott D.A., Hatzistavrou T., et al. A targeted NKX2.1 human embryonic stem cell reporter line enables identification ofhuman basal forebrain derivatives. Stem Cells 2011, 29:462-473.
17. Grskovic M., Javaherian A., Strulovici B., Daley G.Q. Induced pluripotent stem cells-opportunities for disease modelling and drug discovery. Nat. Rev. Drug Discov. 2011, 10:915-929.
18. Hou Z., Zhang Y., Propson N.E., Howden S.E., Chu L.-F., Sontheimer E.J., Thomson J.A. Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 2013, 110:15644-15649.
19. Hsu P.D., Scott D.A., Weinstein J.A., Ran F.A., Konermann S., Agarwala V., Li Y., Fine E.J., Wu X., Shalem O., et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 2013, 31:827-832.
20. 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.
21. Jinek M., East A., Cheng A., Lin S., Ma E., Doudna J. RNA-programmed genome editing in human cells. eLife 2013, 2:e00471.
22. Kim D., Bae S., Park J., Kim E., Kim S., Yu H.R., Hwang J., Kim J.-I., Kim J.-S. Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells. Nat. Methods 2015, 12:237-243.
23. Kiskinis E., Sandoe J., Williams L.A., Boulting G.L., Moccia R., Wainger B.J., Han S., Peng T., Thams S., Mikkilineni S., et al. Pathways disrupted in human ALS motor neurons identified through genetic correction of mutant SOD1. Cell Stem Cell 2014, 14:781-795.
24. Liu Y., Rao M. Gene targeting in human pluripotent stem cells. Methods Mol. Biol. 2011, 767:355-367.
25. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
26. Merkle F.T., Eggan K. Modeling human disease with pluripotent stem cells: from genome association to function. Cell Stem Cell 2013, 12:656-668.
27. Metzger M.J., McConnell-Smith A., Stoddard B.L., Miller A.D. Single-strand nicks induce homologous recombination with less toxicity than double-strand breaks using an AAV vector template. Nucleic Acids Res. 2011, 39:926-935.
28. Mojica F.J.M., Díez-Villaseñor C., García-Martínez J., Almendros C. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 2009, 155:733-740.
29. Montague T.G., Cruz J.M., Gagnon J.A., Church G.M., Valen E. CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. 2014, 42:W401-W407.
30. Pattanayak V., Lin S., Guilinger J.P., Ma E., Doudna J.A., Liu D.R. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 2013, 31:839-843.
31. Ran F.A., Hsu P.D., Lin C.-Y., Gootenberg J.S., Konermann S., Trevino A.E., Scott D.A., Inoue A., Matoba S., Zhang Y., Zhang F. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 2013, 154:1380-1389.
32. Reinhardt P., Schmid B., Burbulla L.F., Schöndorf D.C., Wagner L., Glatza M., Höing S., Hargus G., Heck S.A., Dhingra A., et al. Genetic correction of a LRRK2 mutation in human iPSCs links parkinsonian neurodegeneration to ERK-dependent changes in gene expression. Cell Stem Cell 2013, 12:354-367.
33. Rouet P., Smih F., Jasin M. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc. Natl. Acad. Sci. USA 1994, 91:6064-6068.
34. Ruby K.M., Zheng B. Gene targeting in a HUES line of human embryonic stem cells via electroporation. Stem Cells 2009, 27:1496-1506.
35. Sandoe J., Eggan K. Opportunities and challenges of pluripotent stem cell neurodegenerative disease models. Nat. Neurosci. 2013, 16:780-789.
36. Schwank G., Koo B.-K., Sasselli V., Dekkers J.F., Heo I., Demircan T., Sasaki N., Boymans S., Cuppen E., van der Ent C.K., et al. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell 2013, 13:653-658.
37. Smith C., Gore A., Yan W., Abalde-Atristain L., Li Z., He C., Wang Y., Brodsky R.A., Zhang K., Cheng L., Ye Z. Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell 2014, 15:12-13.
38. Suzuki K., Yu C., Qu J., Li M., Yao X., Yuan T., Goebl A., Tang S., Ren R., Aizawa E., et al. Targeted gene correction minimally impacts whole-genome mutational load in human-disease-specific induced pluripotent stem cell clones. Cell Stem Cell 2014, 15:31-36.
39. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
40. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., Jones J.M. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
41. Tsai S.Q., Zheng Z., Nguyen N.T., Liebers M., Topkar V.V., Thapar V., Wyvekens N., Khayter C., Iafrate A.J., Le L.P., et al. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat. Biotechnol. 2015, 33:187-197.
42. Veres A., Gosis B.S., Ding Q., Collins R., Ragavendran A., Brand H., Erdin S., Cowan C.A., Talkowski M.E., Musunuru K. Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell 2014, 15:27-30.
43. Wang X., Wang Y., Wu X., Wang J., Wang Y., Qiu Z., Chang T., Huang H., Lin R.-J., Yee J.-K. Unbiased detection of off-target cleavage by CRISPR-Cas9 and TALENs using integrase-defective lentiviral vectors. Nat. Biotechnol. 2015, 33:175-178.
44. Wiedenheft B., Sternberg S.H., Doudna J.A. RNA-guided genetic silencing systems in bacteria and archaea. Nature 2012, 482:331-338.
45. Xue H., Wu S., Papadeas S.T., Spusta S., Swistowska A.M., MacArthur C.C., Mattson M.P., Maragakis N.J., Capecchi M.R., Rao M.S., et al. A targeted neuroglial reporter line generated by homologous recombination in human embryonic stem cells. Stem Cells 2009, 27:1836-1846.
46. Yang H., Wang H., Shivalila C.S., Cheng A.W., Shi L., Jaenisch R. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 2013, 154:1370-1379.
47. Yang L., Grishin D., Wang G., Aach J., Zhang C.-Z., Chari R., Homsy J., Cai X., Zhao Y., Fan J.-B., et al. Targeted and genome-wide sequencing reveal single nucleotide variations impacting specificity of Cas9 in human stem cells. Nat. Commun. 2014, 5:5507.
48. Yang H., Wang H., Jaenisch R. Generating genetically modified mice using CRISPR/Cas-mediated genome engineering. Nat. Protoc. 2014, 9:1956-1968.
49. Zwaka T.P., Thomson J.A. Homologous recombination in human embryonic stem cells. Nat. Biotechnol. 2003, 21:319-321.