CRISPR Gene Editing in Stem Cells

25 128

wide CRISPR Screen in Primary Immune Cells to Dissect Regulatory Net-
works. Cell 162, 675–686.
Polo, J.M., Liu, S., Figueroa, M.E., Kulalert, W., Eminli, S., Tan, K.Y., Aposto-
lou, E., Stadtfeld, M., Li, Y., Shioda, T., et al. (2010). Cell type of origin influ-
ences the molecular and functional properties of mouse induced pluripotent
stem cells. Nat. Biotechnol. 28, 848–855.
Ran, F.A., Cong, L., Yan, W.X., Scott, D.A., Gootenberg, J.S., Kriz, A.J., Zet-
sche, B., Shalem, O., Wu, X., Makarova, K.S., et al. (2015). In vivo genome
editing using Staphylococcus aureus Cas9. Nature 520, 186–191.
Reinhardt,P., Schmid, B., Burbulla,L.F., Scho¨ ndorf,D.C.,Wagner, L., Glatza, M.,
Ho¨ ing,S.,Hargus,G.,Heck,S.A., Dhingra,A., etal.(2013).Geneticcorrection ofa
LRRK2 mutation in human iPSCs links parkinsonian neurodegeneration to ERK-
dependent changes in gene expression. Cell Stem Cell 12, 354–367.
Rideout, W.M., 3rd, Hochedlinger, K., Kyba, M., Daley, G.Q., and Jaenisch, R.
(2002). Correction of a genetic defect by nuclear transplantation and combined
cell and gene therapy. Cell 109, 17–27.
Robert, F., Barbeau, M., E´ thier, S., Dostie, J., and Pelletier, J. (2015). Pharma-
cological inhibition of DNA-PK stimulates Cas9-mediated genome editing.
Genome Med. 7, 93.
Robinton, D.A., and Daley, G.Q. (2012). The promise of induced pluripotent
stem cells in research and therapy. Nature 481, 295–305.
Rouet, P., Smih, F., and Jasin, M. (1994a). Expression of a site-specific endo-
nuclease stimulates homologous recombination in mammalian cells. Proc.
Natl. Acad. Sci. USA 91, 6064–6068.
Rouet, P., Smih, F., and Jasin, M. (1994b). Introduction of double-strand
breaks into the genome of mouse cells by expression of a rare-cutting endo-
nuclease. Mol. Cell. Biol. 14, 8096–8106.
Rouhani, F., Kumasaka, N., de Brito, M.C., Bradley, A., Vallier, L., and Gaffney,
D. (2014). Genetic background drives transcriptional variation in human
induced pluripotent stem cells. PLoS Genet. 10, e1004432.
Ruby, K.M., and Zheng, B. (2009). Gene targeting in a HUES line of human
embryonic stem cells via electroporation. Stem Cells 27, 1496–1506.
Ryan, S.D., Dolatabadi, N., Chan, S.F., Zhang, X., Akhtar, M.W., Parker, J.,
Soldner, F., Sunico, C.R., Nagar, S., Talantova, M., et al. (2013). Isogenic
human iPSC Parkinson’s model shows nitrosative stress-induced dysfunction
in MEF2-PGC1a transcription. Cell 155, 1351–1364.
Sato, T., and Clevers, H. (2013). Growing self-organizing mini-guts from a sin-
gle intestinal stem cell: mechanism and applications. Science 340, 1190–1194.
Sato, T., Vries, R.G., Snippert, H.J., van de Wetering, M., Barker, N., Stange,
D.E., van Es, J.H., Abo, A., Kujala, P., Peters, P.J., and Clevers, H. (2009). Sin-
gle Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal
niche. Nature 459, 262–265.
Sato, T., Stange, D.E., Ferrante, M., Vries, R.G., Van Es, J.H., Van den Brink, S.,
Van Houdt, W.J., Pronk, A., Van Gorp, J., Siersema, P.D., and Clevers, H. (2011).
Long-term expansion of epithelial organoids from human colon, adenoma,
adenocarcinoma, and Barrett’s epithelium. Gastroenterology 141, 1762–1772.
Schwank, G., Koo, B.K., Sasselli, V., Dekkers, J.F., Heo, I., Demircan, T., Sa-
saki, N., Boymans, S., Cuppen, E., van der Ent, C.K., et al. (2013). Functional
repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic
fibrosis patients. Cell Stem Cell 13, 653–658.
Sebastiano, V., Zhen, H.H., Haddad, B., Bashkirova, E., Melo, S.P., Wang, P.,
Leung, T.L., Siprashvili, Z., Tichy, A., Li, J., et al. (2014). Human COL7A1-cor-
rected induced pluripotent stem cells for the treatment of recessive dystrophic
epidermolysis bullosa. Sci. Transl. Med. 6, 264ra163.
Sexton, A.N., Regalado, S.G., Lai, C.S., Cost, G.J., O’Neil, C.M., Urnov, F.D.,
Gregory, P.D., Jaenisch, R., Collins, K., and Hockemeyer, D. (2014). Genetic
and molecular identification of three human TPP1 functions in telomerase ac-
tion: recruitment, activation, and homeostasis set point regulation. Genes Dev.
28, 1885–1899.
Shalem, O., Sanjana, N.E., Hartenian, E., Shi, X., Scott, D.A., Mikkelsen, T.S.,
Heckl, D., Ebert, B.L., Root, D.E., Doench, J.G., and Zhang, F. (2014). Genome-
scale CRISPR-Cas9 knockout screening in human cells. Science 343, 84–87.
Sheridan, C. (2015). CRISPR germline editing reverberates through biotech in-
dustry. Nat. Biotechnol. 33, 431–432.
Shi, J., Zhao, Y., Wang, K., Shi, X., Wang, Y., Huang, H., Zhuang, Y., Cai, T.,
Wang, F., and Shao, F. (2015). Cleavage of GSDMD by inflammatory caspases
determines pyroptotic cell death. Nature 526, 660–665.
Slaymaker, I.M., Gao, L., Zetsche, B., Scott, D.A., Yan, W.X., and Zhang, F.
(2016). Rationally engineered Cas9 nucleases with improved specificity. Sci-
ence 351, 84–88.
Smith, C., Gore, A., Yan, W., Abalde-Atristain, L., Li, Z., He, C., Wang, Y., Brod-
sky, R.A., Zhang, K., Cheng, L., and Ye, Z. (2014). Whole-genome sequencing
analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome
editing in human iPSCs. Cell Stem Cell 15, 12–13.
Soldner, F., and Jaenisch, R. (2012). Medicine. iPSC disease modeling. Sci-
ence 338, 1155–1156.
Soldner, F., Hockemeyer, D., Beard, C., Gao, Q., Bell, G.W., Cook, E.G., Har-
gus, G., Blak, A., Cooper, O., Mitalipova, M., et al. (2009). Parkinson’s disease
patient-derived induced pluripotent stem cells free of viral reprogramming fac-
tors. Cell 136, 964–977.
Soldner, F., Laganie` re, J., Cheng, A.W., Hockemeyer, D., Gao, Q., Alagappan,
R., Khurana, V., Golbe, L.I., Myers, R.H., Lindquist, S., et al. (2011). Generation
of isogenic pluripotent stem cells differing exclusively at two early onset Par-
kinson point mutations. Cell 146, 318–331.
Soldner, F., Stelzer, Y., Shivalila, C., Abraham, B., Latourelle, J., Barrasa, I.,
Goldmann, J.J., Myers, R., Young, R., and Jaenisch, R. (2016). Parkinson-
associated risk variant in enhancer element produces subtle effect on target
gene expression. Nature, in press. Published online April 20, 2016.
Spence, J.R., Mayhew, C.N., Rankin, S.A., Kuhar, M.F., Vallance, J.E., Tolle,
K., Hoskins, E.E., Kalinichenko, V.V., Wells, S.I., Zorn, A.M., et al. (2011).
Directed differentiation of human pluripotent stem cells into intestinal tissue
in vitro. Nature 470, 105–109.
Sterneckert, J.L., Reinhardt, P., and Scho¨ ler, H.R. (2014). Investigating human
disease using stem cell models. Nat. Rev. Genet. 15, 625–639.
Studer, L., Vera, E., and Cornacchia, D. (2015). Programming and Reprogram-
ming Cellular Age in the Era of Induced Pluripotency. Cell StemCell16, 591–600.
Suzuki, S., Sargent, R.G., Illek, B., Fischer, H., Esmaeili-Shandiz, A., Yezzi,
M.J., Lee, A., Yang, Y., Kim, S., Renz, P., et al. (2016). TALENs Facilitate Sin-
gle-step Seamless SDF Correction of F508del CFTR in Airway Epithelial Sub-
mucosal Gland Cell-derived CF-iPSCs. Mol. Ther. Nucleic Acids 5, e273.
Takahashi, K., and Yamanaka, S. (2006). Induction of pluripotent stem cells
from mouse embryonic and adult fibroblast cultures by defined factors. Cell
126, 663–676.
Takahashi, K., and Yamanaka, S. (2015). A developmental framework for
induced pluripotency. Development 142, 3274–3285.
Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K.,
and Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human
fibroblasts by defined factors. Cell 131, 861–872.
Takebe, T., Sekine, K., Enomura, M., Koike, H., Kimura, M., Ogaeri, T., Zhang,
R.R., Ueno, Y., Zheng, Y.W., Koike, N., et al. (2013). Vascularized and functional
human liver from an iPSC-derived organ bud transplant. Nature 499, 481–484.
Tanenbaum, M.E., Gilbert, L.A., Qi, L.S., Weissman, J.S., and Vale, R.D.
(2014). A protein-tagging system for signal amplification in gene expression
and fluorescence imaging. Cell 159, 635–646.
Tebas, P., Stein, D., Tang, W.W., Frank, I., Wang, S.Q., Lee, G., Spratt, S.K.,
Surosky, R.T., Giedlin, M.A., Nichol, G., et al. (2014). Gene editing of CCR5
in autologous CD4 T cells of persons infected with HIV. N. Engl. J. Med.
370, 901–910.
Tesar, P.J., Chenoweth, J.G., Brook, F.A., Davies, T.J., Evans, E.P., Mack, D.L.,
Gardner, R.L., and McKay, R.D. (2007). New cell lines frommouse epiblast share
defining features with human embryonic stem cells. Nature 448, 196–199.
Theunissen, T.W., Powell, B.E., Wang, H., Mitalipova, M., Faddah, D.A.,
Reddy, J., Fan, Z.P., Maetzel, D., Ganz, K., Shi, L., et al. (2014). Systematic
identification of culture conditions for induction and maintenance of naive
human pluripotency. Cell Stem Cell 15, 471–487.
Thomas, K.R., and Capecchi, M.R. (1987). Site-directed mutagenesis by gene
targeting in mouse embryo-derived stem cells. Cell 51, 503–512.
Cell Stem Cell 18, May 5, 2016 585
Cell Stem Cell
Review