Anatomy and Cell Biology

Korean Association of Anatomists (대한해부학회)
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Induced pluripotent stem cells and personalized medicine: current progress and future perspectives

  • Chun, Yong-Soon (Department of Surgery, Gachon University Gil Hospital) ;
  • Byun, ,Kyung-Hee (Department of Anatomy and Cell Biology, Gachon University) ;
  • Lee, Bong-Hee (Department of Anatomy and Cell Biology, Gachon University)
  • Published : 2011.12.31
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Abstract

Generation of induced pluripotent stem cells (iPSCs) has revolutionized the field of regenerative medicine by providing researchers with a unique tool to derive disease-specific stem cells for study. iPSCs can self-renew and can differentiate into many cell types, off ering a potentially unlimited source of cells for targeted differentiation into somatic effector cells. Hence, iPSCs are likely to be invaluable for therapeutic applications and disease-related research. In this review, we summarize the recent progress of iPSC generation that has been made with an emphasis on both basic and clinical applications including disease modeling, drug toxicity screening/drug discovery and cell replacement therapy.

Keywords

References

  1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-7. https://doi.org/10.1126/science.282.5391.1145
  2. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-76. https://doi.org/10.1016/j.cell.2006.07.024
  3. 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;131:861-72. https://doi.org/10.1016/j.cell.2007.11.019
  4. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917-20. https://doi.org/10.1126/science.1151526
  5. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, Lerou PH, Lensch MW, Daley GQ. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008;451:141-6. https://doi.org/10.1038/nature06534
  6. Delgado JP, Parouchev A, Allain JE, Pennarun G, Gauthier LR, Dutrillaux AM, Dutrillaux B, Di Santo J, Capron F, Boussin FD, Weber A. Long-term controlled immortalization of a primate hepatic progenitor cell line after Simian virus 40 T-Antigen gene transfer. Oncogene 2005;24:541-51. https://doi.org/10.1038/sj.onc.1208089
  7. Park IH, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A, Lensch MW, Cowan C, Hochedlinger K, Daley GQ. Diseasespecific induced pluripotent stem cells. Cell 2008;134:877-86. https://doi.org/10.1016/j.cell.2008.07.041
  8. Raya A, Rodriguez-Piza I, Guenechea G, Vassena R, Navarro S, Barrero MJ, Consiglio A, Castella M, Rio P, Sleep E, Gonzalez F, Tiscornia G, Garreta E, Aasen T, Veiga A, Verma IM, Surralles J, Bueren J, Izpisua Belmonte JC. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 2009;460:53-9. https://doi.org/10.1038/nature08129
  9. Ye L, Chang JC, Lin C, Sun X, Yu J, Kan YW. Induced pluripotent stem cells offer new approach to therapy in thalassemia and sickle cell anemia and option in prenatal diagnosis in genetic diseases. Proc Natl Acad Sci U S A 2009;106:9826-30. https://doi.org/10.1073/pnas.0904689106
  10. Ku S, Soragni E, Campau E, Thomas EA, Altun G, Laurent LC, Loring JF, Napierala M, Gottesfeld JM. Friedreich's ataxia induced pluripotent stem cells model intergenerational GAA.TTC triplet repeat instability. Cell Stem Cell 2010;7:631-7. https://doi.org/10.1016/j.stem.2010.09.014
  11. Ebert AD, Yu J, Rose FF Jr, Mattis VB, Lorson CL, Thomson JA, Svendsen CN. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009;457:277-80. https://doi.org/10.1038/nature07677
  12. Lee G, Papapetrou EP, Kim H, Chambers SM, Tomishima MJ, Fasano CA, Ganat YM, Menon J, Shimizu F, Viale A, Tabar V, Sadelain M, Studer L. Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 2009;461:402-6. https://doi.org/10.1038/nature08320
  13. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, Hargus G, Blak A, Cooper O, Mitalipova M, Isacson O, Jaenisch R. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 2009;136:964-77. https://doi.org/10.1016/j.cell.2009.02.013
  14. Ye Z, Zhan H, Mali P, Dowey S, Williams DM, Jang YY, Dang CV, Spivak JL, Moliterno AR, Cheng L. Human-induced pluripotent stem cells from blood cells of healthy donors and patients with acquired blood disorders. Blood 2009;114:5473-80. https://doi.org/10.1182/blood-2009-04-217406
  15. Carvajal-Vergara X, Sevilla A, D'Souza SL, Ang YS, Schaniel C, Lee DF, Yang L, Kaplan AD, Adler ED, Rozov R, Ge Y, Cohen N, Edelmann LJ, Chang B, Waghray A, Su J, Pardo S, Lichtenbelt KD, Tartaglia M, Gelb BD, Lemischka IR. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 2010;465:808-12. https://doi.org/10.1038/nature09005
  16. Ghodsizadeh A, Taei A, Totonchi M, Seifinejad A, Gourabi H, Pournasr B, Aghdami N, Malekzadeh R, Almadani N, Salekdeh GH, Baharvand H. Generation of liver disease-specific induced pluripotent stem cells along with efficient differentiation to functional hepatocyte-like cells. Stem Cell Rev 2010;6:622-32. https://doi.org/10.1007/s12015-010-9189-3
  17. Marchetto MC, Carromeu C, Acab A, Yu D, Yeo GW, Mu Y, Chen G, Gage FH, Muotri AR. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 2010;143:527-39. https://doi.org/10.1016/j.cell.2010.10.016
  18. Rashid ST, Corbineau S, Hannan N, Marciniak SJ, Miranda E, Alexander G, Huang-Doran I, Griffin J, Ahrlund-Richter L, Skepper J, Semple R, Weber A, Lomas DA, Vallier L. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J Clin Invest 2010;120:3127-36. https://doi.org/10.1172/JCI43122
  19. Zhang N, An MC, Montoro D, Ellerby LM. Characterization of human Huntington's disease cell model from induced pluripotent stem cells. PLoS Curr 2010;2:RRN1193. https://doi.org/10.1371/currents.RRN1193
  20. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005;115:209-18. https://doi.org/10.1172/JCI24282
  21. Piscaglia AC, Campanale M, Gasbarrini A, Gasbarrini G. Stem cell-based therapies for liver diseases: state of the art and new perspectives. Stem Cells Int 2010;2010:259461.
  22. Lazaro CA, Rhim JA, Yamada Y, Fausto N. Generation of hepatocytes from oval cell precursors in culture. Cancer Res 1998;58:5514-22.
  23. Herrera MB, Bruno S, Buttiglieri S, Tetta C, Gatti S, Deregibus MC, Bussolati B, Camussi G. Isolation and characterization of a stem cell population from adult human liver. Stem Cells 2006;24:2840-50. https://doi.org/10.1634/stemcells.2006-0114
  24. Sahin MB, Schwartz RE, Buckley SM, Heremans Y, Chase L, Hu WS, Verfaillie CM. Isolation and characterization of a novel population of progenitor cells from unmanipulated rat liver. Liver Transpl 2008;14:333-45. https://doi.org/10.1002/lt.21380
  25. Czyz J, Wiese C, Rolletschek A, Blyszczuk P, Cross M, Wobus AM. Potential of embryonic and adult stem cells in vitro. Biol Chem 2003;384:1391-409.
  26. Dalgetty DM, Medine CN, Iredale JP, Hay DC. Progress and future challenges in stem cell-derived liver technologies. Am J Physiol Gastrointest Liver Physiol 2009;297:G241-8. https://doi.org/10.1152/ajpgi.00138.2009
  27. Agarwal S, Holton KL, Lanza R. Efficient differentiation of functional hepatocytes from human embryonic stem cells. Stem Cells 2008;26:1117-27. https://doi.org/10.1634/stemcells.2007-1102
  28. Song Z, Cai J, Liu Y, Zhao D, Yong J, Duo S, Song X, Guo Y, Zhao Y, Qin H, Yin X, Wu C, Che J, Lu S, Ding M, Deng H. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res 2009;19:1233-42. https://doi.org/10.1038/cr.2009.107
  29. Liu H, Ye Z, Kim Y, Sharkis S, Jang YY. Generation of endodermderived human induced pluripotent stem cells from primary hepatocytes. Hepatology 2010;51:1810-9. https://doi.org/10.1002/hep.23626
  30. Sullivan GJ, Hay DC, Park IH, Fletcher J, Hannoun Z, Payne CM, Dalgetty D, Black JR, Ross JA, Samuel K, Wang G, Daley GQ, Lee JH, Church GM, Forbes SJ, Iredale JP, Wilmut I. Generation of functional human hepatic endoderm from human induced pluripotent stem cells. Hepatology 2010;51:329-35. https://doi.org/10.1002/hep.23335
  31. Okita K, Ichisaka T, Yamanaka S. Generation of germlinecompetent induced pluripotent stem cells. Nature 2007;448:313-7. https://doi.org/10.1038/nature05934
  32. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 2008;26:101-6. https://doi.org/10.1038/nbt1374
  33. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, Thomson JA. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009;324:797-801. https://doi.org/10.1126/science.1172482
  34. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K. Induced pluripotent stem cells generated without viral integration. Science 2008;322:945-9. https://doi.org/10.1126/science.1162494
  35. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad Ser B Phys Biol Sci 2009;85:348-62. https://doi.org/10.2183/pjab.85.348
  36. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science 2008;322:949-53. https://doi.org/10.1126/science.1164270
  37. Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, Woltjen K. Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 2009;458:771-5. https://doi.org/10.1038/nature07864
  38. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hamalainen R, Cowling R, Wang W, Liu P, Gertsenstein M, Kaji K, Sung HK, Nagy A. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 2009;458:766-70. https://doi.org/10.1038/nature07863
  39. Sommer CA, Stadtfeld M, Murphy GJ, Hochedlinger K, Kotton DN, Mostoslavsky G. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 2009;27:543-9. https://doi.org/10.1634/stemcells.2008-1075
  40. Zhou H, Wu S, Joo JY, Zhu S, Han DW, Lin T, Trauger S, Bien G, Yao S, Zhu Y, Siuzdak G, Scholer HR, Duan L, Ding S. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009;4:381-4. https://doi.org/10.1016/j.stem.2009.04.005
  41. Huangfu D, Maehr R, Guo W, Eijkelenboom A, Snitow M, Chen AE, Melton DA. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 2008;26:795-7. https://doi.org/10.1038/nbt1418
  42. Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F, Ebina W, Mandal PK, Smith ZD, Meissner A, Daley GQ, Brack AS, Collins JJ, Cowan C, Schlaeger TM, Rossi DJ. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010;7:618-30. https://doi.org/10.1016/j.stem.2010.08.012
  43. Anokye-Danso F, Trivedi CM, Juhr D, Gupta M, Cui Z, Tian Y, Zhang Y, Yang W, Gruber PJ, Epstein JA, Morrisey EE. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 2011;8:376-88. https://doi.org/10.1016/j.stem.2011.03.001
  44. Hanna J, Saha K, Pando B, van Zon J, Lengner CJ, Creyghton MP, van Oudenaarden A, Jaenisch R. Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 2009;462:595-601. https://doi.org/10.1038/nature08592
  45. Miura K, Okada Y, Aoi T, Okada A, Takahashi K, Okita K, Nakagawa M, Koyanagi M, Tanabe K, Ohnuki M, Ogawa D, Ikeda E, Okano H, Yamanaka S. Variation in the safety of induced pluripotent stem cell lines. Nat Biotechnol 2009;27:743-5. https://doi.org/10.1038/nbt.1554
  46. Kim K, Doi A, Wen B, Ng K, Zhao R, Cahan P, Kim J, Aryee MJ, Ji H, Ehrlich LI, Yabuuchi A, Takeuchi A, Cunniff KC, Hongguang H, McKinney-Freeman S, Naveiras O, Yoon TJ, Irizarry RA, Jung N, Seita J, Hanna J, Murakami P, Jaenisch R, Weissleder R, Orkin SH, Weissman IL, Feinberg AP, Daley GQ. Epigenetic memory in induced pluripotent stem cells. Nature 2010;467:285-90. https://doi.org/10.1038/nature09342
  47. Polo JM, Liu S, Figueroa ME, Kulalert W, Eminli S, Tan KY, Apostolou E, Stadtfeld M, Li Y, Shioda T, Natesan S, Wagers AJ, Melnick A, Evans T, Hochedlinger K. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol 2010;28:848-55. https://doi.org/10.1038/nbt.1667
  48. Marchetto MC, Yeo GW, Kainohana O, Marsala M, Gage FH, Muotri AR. Transcriptional signature and memory retention of human-induced pluripotent stem cells. PLoS One 2009;4:e7076. https://doi.org/10.1371/journal.pone.0007076
  49. Loh YH, Hartung O, Li H, Guo C, Sahalie JM, Manos PD, Urbach A, Heffiner GC, Grskovic M, Vigneault F, Lensch MW, Park IH, Agarwal S, Church GM, Collins JJ, Irion S, Daley GQ. Reprogramming of T cells from human peripheral blood. Cell Stem Cell 2010;7:15-9 https://doi.org/10.1016/j.stem.2010.06.004
  50. Staerk J, Dawlaty MM, Gao Q, Maetzel D, Hanna J, Sommer CA, Mostoslavsky G, Jaenisch R. Reprogramming of human peripheral blood cells to induced pluripotent stem cells. Cell Stem Cell 2010;7:20-4. https://doi.org/10.1016/j.stem.2010.06.002
  51. Kunisato A, Wakatsuki M, Shinba H, Ota T, Ishida I, Nagao K. Direct generation of induced pluripotent stem cells from human nonmobilized blood. Stem Cells Dev 2011;20:159-68. https://doi.org/10.1089/scd.2010.0063
  52. Seki T, Yuasa S, Oda M, Egashira T, Yae K, Kusumoto D, Nakata H, Tohyama S, Hashimoto H, Kodaira M, Okada Y, Seimiya H, Fusaki N, Hasegawa M, Fukuda K. Generation of induced pluripotent stem cells from human terminally differentiated circulating T cells. Cell Stem Cell 2010;7:11-4. https://doi.org/10.1016/j.stem.2010.06.003
  53. Brown ME, Rondon E, Rajesh D, Mack A, Lewis R, Feng X, Zitur LJ, Learish RD, Nuwaysir EF. Derivation of induced pluripotent stem cells from human peripheral blood T lymphocytes. PLoS One 2010;5:e11373. https://doi.org/10.1371/journal.pone.0011373
  54. Haase A, Olmer R, Schwanke K, Wunderlich S, Merkert S, Hess C, Zweigerdt R, Gruh I, Meyer J, Wagner S, Maier LS, Han DW, Glage S, Miller K, Fischer P, Scholer HR, Martin U. Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell 2009;5:434-41. https://doi.org/10.1016/j.stem.2009.08.021
  55. Eminli S, Foudi A, Stadtfeld M, Maherali N, Ahfeldt T, Mostoslavsky G, Hock H, Hochedlinger K. Diff erentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nat Genet 2009;41:968-76. https://doi.org/10.1038/ng.428
  56. Giorgetti A, Montserrat N, Aasen T, Gonzalez F, Rodriguez- Piza I, Vassena R, Raya A, Boue S, Barrero MJ, Corbella BA, Torrabadella M, Veiga A, Izpisua Belmonte JC. Generation of induced pluripotent stem cells from human cord blood using OCT4 and SOX2. Cell Stem Cell 2009;5:353-7. https://doi.org/10.1016/j.stem.2009.09.008
  57. Panopoulos AD, Ruiz S, Yi F, Herrerias A, Batchelder EM, Izpisua Belmonte JC. Rapid and highly efficient generation of induced pluripotent stem cells from human umbilical vein endothelial cells. PLoS One 2011;6:e19743. https://doi.org/10.1371/journal.pone.0019743
  58. Sugii S, Kida Y, Kawamura T, Suzuki J, Vassena R, Yin YQ, Lutz MK, Burggren WT, Izpisua Belmonte JC, Evans RM. Human and mouse adipose-derived cells support feeder-independent induction of pluripotent stem cells. Proc Natl Acad Sci U S A 2010;107:3558-63. https://doi.org/10.1073/pnas.0910172106
  59. Aoki T, Ohnishi H, Oda Y, Tadokoro M, Sasao M, Kato H, Hattori K, Ohgushi H. Generation of induced pluripotent stem cells from human adipose-derived stem cells without c-MYC. Tissue Eng Part A 2010;16:2197-206. https://doi.org/10.1089/ten.tea.2009.0747
  60. Oda Y, Yoshimura Y, Ohnishi H, Tadokoro M, Katsube Y, Sasao M, Kubo Y, Hattori K, Saito S, Horimoto K, Yuba S, Ohgushi H. Induction of pluripotent stem cells from human third molar mesenchymal stromal cells. J Biol Chem 2010;285:29270-8. https://doi.org/10.1074/jbc.M109.055889
  61. Song B, Niclis JC, Alikhan MA, Sakkal S, Sylvain A, Kerr PG, Laslett AL, Bernard CA, Ricardo SD. Generation of induced pluripotent stem cells from kidney mesangial cells. J Am Soc Nephrol 2011;22:1213-20. https://doi.org/10.1681/ASN.2010101022
  62. Aasen T, Raya A, Barrero MJ, Garreta E, Consiglio A, Gonzalez F, Vassena R, Bilic J, Pekarik V, Tiscornia G, Edel M, Boue S, Izpisua Belmonte JC. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 2008;26:1276-84. https://doi.org/10.1038/nbt.1503
  63. Kim JB, Greber B, Arauzo-Bravo MJ, Meyer J, Park KI, Zaehres H, Scholer HR. Direct reprogramming of human neural stem cells by OCT4. Nature 2009;461:649-53. https://doi.org/10.1038/nature08436
  64. Utikal J, Maherali N, Kulalert W, Hochedlinger K. Sox2 is dispensible for the reprogramming of melanocytes and melanoma cells into induced pluripotent stem cells. J Cell Sci 2009;122(Pt 19):3502-10. https://doi.org/10.1242/jcs.054783
  65. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 2007;1:39-49. https://doi.org/10.1016/j.stem.2007.05.012
  66. Moretti A, Bellin M, Welling A, Jung CB, Lam JT, Bott-Flugel L, Dorn T, Goedel A, Hohnke C, Hofmann F, Seyfarth M, Sinnecker D, Schomig A, Laugwitz KL. Patient-specific induced pluripotent stem-cell models for long QT syndrome. N Engl J Med 2010;363:1397-409. https://doi.org/10.1056/NEJMoa0908679
  67. Seifinejad A, Tabebordbar M, Baharvand H, Boyer LA, Salekdeh GH. Progress and promise towards safe induced pluripotent stem cells for therapy. Stem Cell Rev 2010;6:297-306. https://doi.org/10.1007/s12015-010-9121-x
  68. Maehr R, Chen S, Snitow M, Ludwig T, Yagasaki L, Goland R, Leibel RL, Melton DA. Generation of pluripotent stem cells from patients with type 1 diabetes. Proc Natl Acad Sci U S A 2009;106:15768-73. https://doi.org/10.1073/pnas.0906894106
  69. Si-Tayeb K, Noto FK, Nagaoka M, Li J, Battle MA, Duris C, North PE, Dalton S, Duncan SA. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 2010;51:297-305. https://doi.org/10.1002/hep.23354
  70. Stadtfeld M, Hochedlinger K. Induced pluripotency: history, mechanisms, and applications. Genes Dev 2010;24:2239-63. https://doi.org/10.1101/gad.1963910
  71. Rubin LL. Stem cells and drug discovery: the beginning of a new era? Cell 2008;132:549-52. https://doi.org/10.1016/j.cell.2008.02.010
  72. Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, Croft GF, Saphier G, Leibel R, Goland R, Wichterle H, Henderson CE, Eggan K. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008;321:1218-21. https://doi.org/10.1126/science.1158799
  73. Yang J, Cai J, Zhang Y, Wang X, Li W, Xu J, Li F, Guo X, Deng K, Zhong M, Chen Y, Lai L, Pei D, Esteban MA. Induced pluripotent stem cells can be used to model the genomic imprinting disorder Prader-Willi syndrome. J Biol Chem 2010;285:40303-11. https://doi.org/10.1074/jbc.M110.183392
  74. Th omas KR, Folger KR, Capecchi MR. High frequency targeting of genes to specific sites in the mammalian genome. Cell 1986;44:419-28. https://doi.org/10.1016/0092-8674(86)90463-0
  75. Khan IF, Hirata RK, Wang PR, Li Y, Kho J, Nelson A, Huo Y, Zavaljevski M, Ware C, Russell DW. Engineering of human pluripotent stem cells by AAV-mediated gene targeting. Mol Ther 2010;18:1192-9. https://doi.org/10.1038/mt.2010.55
  76. Khan IF, Hirata RK, Russell DW. AAV-mediated gene targeting methods for human cells. Nat Protoc 2011;6:482-501. https://doi.org/10.1038/nprot.2011.301
  77. Jang JH, Koerber JT, Kim JS, Asuri P, Vazin T, Bartel M, Keung A, Kwon I, Park KI, Schaffer DV. An evolved adeno-associated viral variant enhances gene delivery and gene targeting in neural stem cells. Mol Ther 2011;19:667-75. https://doi.org/10.1038/mt.2010.287
  78. Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD. Genome editing with engineered zinc finger nucleases. Nat Rev Genet 2010;11:636-46. https://doi.org/10.1038/nrg2842
  79. Kim YG, Cha J, Chandrasegaran S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A 1996;93:1156-60. https://doi.org/10.1073/pnas.93.3.1156
  80. Miller JC, Holmes MC, Wang J, Guschin DY, Lee YL, Rupniewski I, Beausejour CM, Waite AJ, Wang NS, Kim KA, Gregory PD, Pabo CO, Rebar EJ. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 2007;25:778-85. https://doi.org/10.1038/nbt1319
  81. Doyon Y, Vo TD, Mendel MC, Greenberg SG, Wang J, Xia DF, Miller JC, Urnov FD, Gregory PD, Holmes MC. Enhancing zinc-finger nuclease activity with improved obligate heterodimeric architectures. Nat Methods 2011;8:74-9. https://doi.org/10.1038/nmeth.1539
  82. Collin J, Lako M. Concise review: putting a fi nger on stem cell biology: zinc finger nuclease-driven targeted genetic editing in human pluripotent stem cells. Stem Cells 2011;29:1021-33. https://doi.org/10.1002/stem.658
  83. Lombardo A, Genovese P, Beausejour CM, Colleoni S, Lee YL, Kim KA, Ando D, Urnov FD, Galli C, Gregory PD, Holmes MC, Naldini L. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 2007;25:1298-306. https://doi.org/10.1038/nbt1353
  84. Benabdallah BF, Allard E, Yao S, Friedman G, Gregory PD, Eliopoulos N, Fradette J, Spees JL, Haddad E, Homes MC, Beausejour CM. Targeted gene edition to human mesenchmal stromal cells as a cell-based plasma-soluble protein delivery platform. Cytotherapy 2010;12:394-9. https://doi.org/10.3109/14653240903583803
  85. Zou J, Maeder ML, Mali P, Pruett-Miller SM, Thibodeau- Beganny S, Chou BK, Chen G, Ye Z, Park IH, Daley GQ, Porteus MH, Joung JK, Cheng L. Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 2009;5:97-110. https://doi.org/10.1016/j.stem.2009.05.023
  86. Vogel G. Stem cells. Diseases in a dish take off. Science 2010;330:1172-3. https://doi.org/10.1126/science.330.6008.1172
  87. Soldner F, Laganiere J, Cheng AW, Hockemeyer D, Gao Q, Alagappan R, Khurana V, Golbe LI, Myers RH, Lindquist S, Zhang L, Guschin D, Fong LK, Vu BJ, Meng X, Urnov FD, Rebar EJ, Gregory PD, Zhang HS, Jaenisch R. Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 2011;146:318-31. https://doi.org/10.1016/j.cell.2011.06.019
  88. Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, DeKelver RC, Katibah GE, Amora R, Boydston EA, Zeitler B, Meng X, Miller JC, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol 2009;27:851-7. https://doi.org/10.1038/nbt.1562
  89. DeKelver RC, Choi VM, Moehle EA, Paschon DE, Hockemeyer D, Meijsing SH, Sancak Y, Cui X, Steine EJ, Miller JC, Tam P, Bartsevich VV, Meng X, Rupniewski I, Gopalan SM, Sun HC, Pitz KJ, Rock JM, Zhang L, Davis GD, Rebar EJ, Cheeseman IM, Yamamoto KR, Sabatini DM, Jaenisch R, Gregory PD, Urnov FD. Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease-driven transgenesis into a safe harbor locus in the human genome. Genome Res 2010;20:1133-42. https://doi.org/10.1101/gr.106773.110

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