Current approaches for efficient genetic editing in human pluripotent stem cells

Abstract

Human pluripotent stem cells have been much anticipated as a powerful system to study developmental events, model genetic disorders, and serve as a source of autologous cells for cell therapy in genetic disorders. Precise genetic manipulation is crucial to all these applications, and many recent advances have been made in site specific nuclease systems like zinc finger nucleases, TALENs, and CRISPR/Cas. In this review, we address the importance of site-specific genome modification and how this technology can be applied to manipulate human pluripotent stem cells.

Keywords

gene targeting / human pluripotent stem cells / TALEN / ZFN / CRISPR/Cas

References

[1] Bibikova M, Beumer K, Trautman J K, Carroll D (2003). Enhancing gene targeting with designed zinc finger nucleases. Science, 300(5620): 764

[2] Bibikova M, Golic M, Golic K G, Carroll D (2002). Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics, 161(3): 1169–1175

[3] Bogdanove A J, Voytas D F (2011). TAL effectors: customizable proteins for DNA targeting. Science, 333(6051): 1843–1846

[4] Brunet E, Simsek D, Tomishima M, DeKelver R, Choi V M, Gregory P, Urnov F, Weinstock D M, Jasin M (2009). Chromosomal translocations induced at specified loci in human stem cells. Proc Natl Acad Sci USA, 106(26): 10620–10625

[5] Bultmann S, Morbitzer R, Schmidt C S, Thanisch K, Spada F, Elsaesser J, Lahaye T, Leonhardt H (2012). Targeted transcriptional activation of silent oct4 pluripotency gene by combining designer TALEs and inhibition of epigenetic modifiers. Nucleic Acids Res, 40(12): 5368–5377

[6] Carroll D (2011). Genome engineering with zinc-finger nucleases. Genetics, 188(4): 773–782

[7] Cermak T, Doyle E L, Christian M, Wang L, Zhang Y, Schmidt C, Baller J A, Somia N V, Bogdanove A J, Voytas D F (2011). Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res, 39(12): e82

[8] Chaikind B, Kilambi K P, Gray J J, Ostermeier M (2012). Targeted DNA methylation using an artificially bisected M.HhaI fused to zinc fingers. PLoS ONE, 7(9): e44852

[9] Chang C J, Bouhassira E E (2012). Zinc-finger nuclease-mediated correction of α-thalassemia in iPS cells. Blood, 120(19): 3906–3914

[10] Cho S W, Kim S, Kim J M, Kim J S (2013). Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol, 31(3): 230–232

[11] Christian M, Cermak T, Doyle E L, Schmidt C, Zhang F, Hummel A, Bogdanove A J, Voytas D F (2010). Targeting DNA double-strand breaks with TAL effector nucleases. Genetics, 186(2): 757–761

[12] 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 (2013). Multiplex genome engineering using CRISPR/Cas systems. Science, 339(6121): 819–823

[13] Ding Q, Lee Y K, Schaefer E A, Peters D T, Veres A, Kim K, Kuperwasser N, Motola D L, Meissner T B, Hendriks W T, Trevisan M, Gupta R M, Moisan A, Banks E, Friesen M, Schinzel R T, Xia F, Tang A, Xia Y, Figueroa E, Wann A, Ahfeldt T, Daheron L, Zhang F, Rubin L L, Peng L F, Chung R T, Musunuru K, Cowan C A (2013). A TALEN genome-editing system for generating human stem cell-based disease models. Cell Stem Cell, 12(2): 238–251

[14] Doetschman T, Gregg R G, Maeda N, Hooper M L, Melton D W, Thompson S, Smithies O (1987). Targetted correction of a mutant HPRT gene in mouse embryonic stem cells. Nature, 330(6148): 576–578

[15] Doyle J P, Dougherty J D, Heiman M, Schmidt E F, Stevens T R, Ma G, Bupp S, Shrestha P, Shah R D, Doughty M L, Gong S, Greengard P, Heintz N (2008). Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell, 135(4): 749–762

[16] Durai S, Mani M, Kandavelou K, Wu J, Porteus M H, Chandrasegaran S (2005). Zinc finger nucleases: custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Res, 33(18): 5978–5990

[17] Heiman M, Schaefer A, Gong S, Peterson J D, Day M, Ramsey K E, Suárez-Fariñas M, Schwarz C, Stephan D A, Surmeier D J, Greengard P, Heintz N (2008). A translational profiling approach for the molecular characterization of CNS cell types. Cell, 135(4): 738–748

[18] Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, DeKelver R C, Katibah G E, Amora R, Boydston E A, Zeitler B, Meng X, Miller J C, Zhang L, Rebar E J, Gregory P D, Urnov F D, Jaenisch R (2009). Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol, 27(9): 851–857

[19] Hockemeyer D, Wang H, Kiani S, Lai C S, Gao Q, Cassady J P, Cost G J, Zhang L, Santiago Y, Miller J C, Zeitler B, Cherone J M, Meng X, Hinkley S J, Rebar E J, Gregory P D, Urnov F D, Jaenisch R (2011). Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol, 29(8): 731–734

[20] Hwang W Y, Fu Y, Reyon D, Maeder M L, Tsai S Q, Sander J D, Peterson R T, Yeh J R, Joung J K (2013). Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol, 31(3): 227–229

[21] Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna J A, Charpentier E (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337(6096): 816–821

[22] Kim Y, Kweon J, Kim A, Chon J K, Yoo J Y, Kim H J, Kim S, Lee C, Jeong E, Chung E, Kim D, Lee M S, Go E M, Song H J, Kim H, Cho N, Bang D, Kim S, Kim J S (2013). A library of TAL effector nucleases spanning the human genome. Nat Biotechnol, 31(3): 251–258

[23] Lengner C J, Gimelbrant A A, Erwin J A, Cheng A W, Guenther M G, Welstead G G, Alagappan R, Frampton G M, Xu P, Muffat J, Santagata S, Powers D, Barrett C B, Young R A, Lee J T, Jaenisch R, Mitalipova M (2010). Derivation of pre-X inactivation human embryonic stem cells under physiological oxygen concentrations. Cell, 141(5): 872–883

[24] Liu H, Ye Z, Kim Y, Sharkis S, Jang Y Y (2010). Generation of endoderm-derived human induced pluripotent stem cells from primary hepatocytes. Hepatology, 51(5): 1810–1819

[25] Maeder M L, Thibodeau-Beganny S, Osiak A, Wright D A, Anthony R M, Eichtinger M, Jiang T, Foley J E, Winfrey R J, Townsend J A, Unger-Wallace E, Sander J D, Müller-Lerch F, Fu F, Pearlberg J, Göbel C, Dassie J P, Pruett-Miller S M, Porteus M H, Sgroi D C, Iafrate A J, Dobbs D, McCray P B Jr, Cathomen T, Voytas D F, Joung J K (2008). Rapid “open-source” engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell, 31(2): 294–301

[26] Mali P, Aach J, Lee J H, Levner D, Nip L, Church G M (2013). Barcoding cells using cell-surface programmable DNA-binding domains. Nat Methods, 10(5): 403–406

[27] Mali P, Yang L, Esvelt K M, Aach J, Guell M, DiCarlo J E, Norville J E, Church G M (2013). RNA-guided human genome engineering via Cas9. Science, 339(6121): 823–826

[28] Miller J C, Tan S, Qiao G, Barlow K A, Wang J, Xia D F, Meng X, Paschon D E, Leung E, Hinkley S J, Dulay G P, Hua K L, Ankoudinova I, Cost G J, Urnov F D, Zhang H S, Holmes M C, Zhang L, Gregory P D, Rebar E J (2011). A TALE nuclease architecture for efficient genome editing. Nat Biotechnol, 29(2): 143–148

[29] Mussolino C, Cathomen T (2011). On target? Tracing zinc-finger-nuclease specificity. Nat Methods, 8(9): 725–726

[30] Nishiyama A, Xin L, Sharov A A, Thomas M, Mowrer G, Meyers E, Piao Y, Mehta S, Yee S, Nakatake Y, Stagg C, Sharova L, Correa-Cerro L S, Bassey U, Hoang H, Kim E, Tapnio R, Qian Y, Dudekula D, Zalzman M, Li M, Falco G, Yang H T, Lee S L, Monti M, Stanghellini I, Islam M N, Nagaraja R, Goldberg I, Wang W, Longo D L, Schlessinger D, Ko M S (2009). Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors. Cell Stem Cell, 5(4): 420–433

[31] Piganeau M, Ghezraoui H, De Cian A, Guittat L, Tomishima M, Perrouault L, René O, Katibah G E, Zhang L, Holmes M C, Doyon Y, Concordet J P, Giovannangeli C, Jasin M, Brunet E (2013). Cancer translocations in human cells induced by zinc finger and TALE nucleases. Genome Res, 23(7): 1182–1193

[32] Porteus M H, Baltimore D (2003). Chimeric nucleases stimulate gene targeting in human cells. Science, 300(5620): 763

[33] Qi L S, Larson M H, Gilbert L A, Doudna J A, Weissman J S, Arkin A P, Lim W A (2013). Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 152(5): 1173–1183

[34] Sermon K D, Simon C, Braude P, Viville S, Borstlap J, Veiga A (2009). Creation of a registry for human embryonic stem cells carrying an inherited defect: joint collaboration between ESHRE and hESCreg. Hum Reprod, 24(7): 1556–1560

[35] Smih F, Rouet P, Romanienko P J, Jasin M (1995). Double-strand breaks at the target locus stimulate gene targeting in embryonic stem cells. Nucleic Acids Res, 23(24): 5012–5019

[36] Soldner F, Laganière J, Cheng A W, Hockemeyer D, Gao Q, Alagappan R, Khurana V, Golbe L I, Myers R H, Lindquist S, Zhang L, Guschin D, Fong L K, Vu B J, Meng X, Urnov F D, Rebar E J, Gregory P D, Zhang H S, Jaenisch R (2011). Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell, 146(2): 318–331

[37] Stephenson E L, Mason C, Braude P R (2009). Preimplantation genetic diagnosis as a source of human embryonic stem cells for disease research and drug discovery. BJOG, 116(2): 158–165

[38] Sussman D, Chadsey M, Fauce S, Engel A, Bruett A, Monnat R Jr, Stoddard B L, Seligman L M (2004). Isolation and characterization of new homing endonuclease specificities at individual target site positions. J Mol Biol, 342(1): 31–41

[39] Tachibana M, Amato P, Sparman M, Gutierrez N M, Tippner-Hedges R, Ma H, Kang E, Fulati A, Lee H S, Sritanaudomchai H, Masterson K, Larson J, Eaton D, Sadler-Fredd K, Battaglia D, Lee D, Wu D, Jensen J, Patton P, Gokhale S, Stouffer R L, Wolf D, Mitalipov S (2013). Human embryonic stem cells derived by somatic cell nuclear transfer. Cell, 153(6): 1228–1238

[40] Tomishima M J, Hadjantonakis A K, Gong S, Studer L (2007). Production of green fluorescent protein transgenic embryonic stem cells using the GENSAT bacterial artificial chromosome library. Stem Cells, 25(1): 39–45

[41] Urnov F D, Rebar E J, Holmes M C, Zhang H S, Gregory P D (2010). Genome editing with engineered zinc finger nucleases. Nat Rev Genet, 11(9): 636–646

[42] Wang H, Yang H, Shivalila C S, Dawlaty M M, Cheng A W, Zhang F, Jaenisch R (2013). One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell, 153(4): 910–918

[43] Wang Y, Zheng C G, Jiang Y, Zhang J, Chen J, Yao C, Zhao Q, Liu S, Chen K, Du J, Yang Z, Gao S (2012). Genetic correction of β-thalassemia patient-specific iPS cells and its use in improving hemoglobin production in irradiated SCID mice. Cell Res, 22(4): 637–648

[44] Xiao A, Wang Z, Hu Y, Wu Y, Luo Z, Yang Z, Zu Y, Li W, Huang P, Tong X, Zhu Z, Lin S, Zhang B (2013). Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res,

[45] Yamanaka S, Blau H M (2010). Nuclear reprogramming to a pluripotent state by three approaches. Nature, 465(7299): 704–712

[46] Yu J, Thomson J A (2008). Pluripotent stem cell lines. Genes Dev, 22(15): 1987–1997

[47] Yusa K, Rashid S T, Strick-Marchand H, Varela I, Liu P Q, Paschon D E, Miranda E, Ordóñez A, Hannan N R, Rouhani F J, Darche S, Alexander G, Marciniak S J, Fusaki N, Hasegawa M, Holmes M C, Di Santo J P, Lomas D A, Bradley A, Vallier L (2011). Targeted gene correction of α1-antitrypsin deficiency in induced pluripotent stem cells. Nature, 478(7369): 391–394

[48] Zou J, Maeder M L, Mali P, Pruett-Miller S M, Thibodeau-Beganny S, Chou B K, Chen G, Ye Z, Park I H, Daley G Q, Porteus M H, Joung J K, Cheng L (2009). Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell, 5(1): 97–110

[49] Zou J, Mali P, Huang X, Dowey S N, Cheng L (2011). Site-specific gene correction of a point mutation in human iPS cells derived from an adult patient with sickle cell disease. Blood, 118(17): 4599–4608

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