Current approaches for efficient genetic editing in human pluripotent stem cells

Bipasha MUKHERJEE-CLAVIN, Mark TOMISHIMA, Gabsang LEE

PDF(131 KB)
PDF(131 KB)
Front. Biol. ›› 2013, Vol. 8 ›› Issue (5) : 461-467. DOI: 10.1007/s11515-013-1275-x
MINI-REVIEW
MINI-REVIEW

Current approaches for efficient genetic editing in human pluripotent stem cells

Author information +
History +

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

Cite this article

Download citation ▾
Bipasha MUKHERJEE-CLAVIN, Mark TOMISHIMA, Gabsang LEE. Current approaches for efficient genetic editing in human pluripotent stem cells. Front Biol, 2013, 8(5): 461‒467 https://doi.org/10.1007/s11515-013-1275-x

References

[1]
Bibikova M, Beumer K, Trautman J K, Carroll D (2003). Enhancing gene targeting with designed zinc finger nucleases. Science, 300(5620): 764
CrossRef Pubmed Google scholar
[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
Pubmed
[3]
Bogdanove A J, Voytas D F (2011). TAL effectors: customizable proteins for DNA targeting. Science, 333(6051): 1843–1846
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[6]
Carroll D (2011). Genome engineering with zinc-finger nucleases. Genetics, 188(4): 773–782
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[9]
Chang C J, Bouhassira E E (2012). Zinc-finger nuclease-mediated correction of α-thalassemia in iPS cells. Blood, 120(19): 3906–3914
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[29]
Mussolino C, Cathomen T (2011). On target? Tracing zinc-finger-nuclease specificity. Nat Methods, 8(9): 725–726
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[32]
Porteus M H, Baltimore D (2003). Chimeric nucleases stimulate gene targeting in human cells. Science, 300(5620): 763
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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,
CrossRef Pubmed Google scholar
[45]
Yamanaka S, Blau H M (2010). Nuclear reprogramming to a pluripotent state by three approaches. Nature, 465(7299): 704–712
CrossRef Pubmed Google scholar
[46]
Yu J, Thomson J A (2008). Pluripotent stem cell lines. Genes Dev, 22(15): 1987–1997
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar

Acknowledgements

We would like to thank members of the Lee laboratory for valuable discussions on the manuscript. The Robertson Investigator Award from the New York Stem Cell Foundation (G.L.) and the Maryland Stem Cell Research Fund (G.L.) supported experiments in the Lee laboratory.
Competing financial interests
The authors declare no competing financial interests.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
PDF(131 KB)

Accesses

Citations

Detail

Sections
Recommended

/