Targeted gene correction minimally impacts whole-genome mutational load in human-disease-specific induced pluripotent stem cell clones

Cell Stem Cell

Volumn 15, Issue 1, 2014, Pages 31-36

  Suzuki, Keiichiro ^a   Yu, Chang ^b   Qu, Jing ^c   Li, Mo ^a   Yao, Xiaotian ^b   Yuan, Tingting ^c   Goebl, April ^a   Tang, Senwei ^b,d   Ren, Ruotong ^c   Aizawa, Emi ^a   Zhang, Fan ^b,e   Xu, Xiuling ^c   Soligalla, Rupa Devi ^a   Chen, Feng ^b   Kim, Jessica ^a   Kim, Na Young ^a   Liao, Hsin Kai ^a   Benner, Chris ^a   Esteban, Concepcion Rodriguez ^a   Jin, Yabin ^b   Liu, Guang Hui ^c,f,g   Li, Yingrui ^b   Izpisua Belmonte, Juan Carlos ^a   more..

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b BGI SHENZHEN   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

^d CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^e UNIVERSITY OF MICHIGAN   (United States)

^f Center for Age related Diseases (CAD)   (China)

^g BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ENDONUCLEASE;

ARTICLE; CELL CLONE; CELL CULTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; GENOME; HUMAN; HUMAN CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; TARGETED GENE REPAIR; ADENOVIRIDAE; CRISPR CAS SYSTEM; DNA REPAIR; DNA SEQUENCE; GENE THERAPY; GENE VECTOR; GENETICS; HEK293 CELL LINE; METABOLISM; MUTATION; PHYSIOLOGY; REGENERATIVE MEDICINE; CHROMOSOME; CPG ISLAND; DNA END JOINING REPAIR; EXPRESSION VECTOR; GENE TARGETING; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENETIC MANIPULATION; HYBRID; INDEL MUTATION; MUTATION RATE; POINT MUTATION; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION;

ADENOVIRIDAE; CLONE CELLS; CRISPR-CAS SYSTEMS; DNA REPAIR; ENDONUCLEASES; GENETIC THERAPY; GENETIC VECTORS; GENOME; HEK293 CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MUTATION; REGENERATIVE MEDICINE; SEQUENCE ANALYSIS, DNA;

EID: 84903942097     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.06.016     Document Type: Article

References (35)

1. I.A. Adzhubei, S. Schmidt, L. Peshkin, V.E. Ramensky, A. Gerasimova, P. Bork, A.S. Kondrashov, and S.R. Sunyaev A method and server for predicting damaging missense mutations Nat. Methods 7 2010 248 249
2. L. Cheng, N.F. Hansen, L. Zhao, Y. Du, C. Zou, F.X. Donovan, B.K. Chou, G. Zhou, S. Li, S.N. Dowey NISC Comparative Sequencing Program Low incidence of DNA sequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression Cell Stem Cell 10 2012 337 344
3. S. Corti, M. Nizzardo, C. Simone, M. Falcone, M. Nardini, D. Ronchi, C. Donadoni, S. Salani, G. Riboldi, and F. Magri et al. Genetic correction of human induced pluripotent stem cells from patients with spinal muscular atrophy Sci. Transl. Med. 4 2012 165ra162
4. Q. Ding, Y.K. Lee, E.A. Schaefer, D.T. Peters, A. Veres, K. Kim, N. Kuperwasser, D.L. Motola, T.B. Meissner, and W.T. Hendriks et al. A TALEN genome-editing system for generating human stem cell-based disease models Cell Stem Cell 12 2013 238 251
5. Q. Ding, S.N. Regan, Y. Xia, L.A. Oostrom, C.A. Cowan, and K. Musunuru Enhanced efficiency of human pluripotent stem cell genome editing through replacing TALENs with CRISPRs Cell Stem Cell 12 2013 393 394
6. H. Fong, C. Wang, J. Knoferle, D. Walker, M.E. Balestra, L.M. Tong, L. Leung, K.L. Ring, W.W. Seeley, and A. Karydas et al. Genetic correction of tauopathy phenotypes in neurons derived from human induced pluripotent stem cells Stem Cell Reports 1 2013 226 234
7. S.A. Forbes, G. Bhamra, S. Bamford, E. Dawson, C. Kok, J. Clements, A. Menzies, J.W. Teague, P.A. Futreal, and M.R. Stratton The Catalogue of Somatic Mutations in Cancer (COSMIC) Curr. Protoc. Hum. Genet. Chapter 10 2008 Unit 10 11
8. R. Gabriel, A. Lombardo, A. Arens, J.C. Miller, P. Genovese, C. Kaeppel, A. Nowrouzi, C.C. Bartholomae, J. Wang, and G. Friedman et al. An unbiased genome-wide analysis of zinc-finger nuclease specificity Nat. Biotechnol. 29 2011 816 823
9. D.B. Goldstein, A. Allen, J. Keebler, E.H. Margulies, S. Petrou, S. Petrovski, and S. Sunyaev Sequencing studies in human genetics: design and interpretation Nat. Rev. Genet. 14 2013 460 470
10. J.P. Guilinger, V. Pattanayak, D. Reyon, S.Q. Tsai, J.D. Sander, J.K. Joung, and D.R. Liu Broad specificity profiling of TALENs results in engineered nucleases with improved DNA-cleavage specificity Nat. Methods 11 2014 429 435
11. G. Ha, A. Roth, D. Lai, A. Bashashati, J. Ding, R. Goya, R. Giuliany, J. Rosner, A. Oloumi, and K. Shumansky et al. Integrative analysis of genome-wide loss of heterozygosity and monoallelic expression at nucleotide resolution reveals disrupted pathways in triple-negative breast cancer Genome Res. 22 2012 1995 2007
12. A. Hendel, E.J. Kildebeck, E.J. Fine, J.T. Clark, N. Punjya, V. Sebastiano, G. Bao, and M.H. Porteus Quantifying genome-editing outcomes at endogenous loci with SMRT sequencing Cell Reports 7 2014 293 305
13. D. Hockemeyer, F. Soldner, C. Beard, Q. Gao, M. Mitalipova, R.C. DeKelver, G.E. Katibah, R. Amora, E.A. Boydston, and B. Zeitler et al. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases Nat. Biotechnol. 27 2009 851 857
14. S.L. Holbeck, and J.N. Strathern A role for REV3 in mutagenesis during double-strand break repair in Saccharomyces cerevisiae Genetics 147 1997 1017 1024
15. Z. Hou, Y. Zhang, N.E. Propson, S.E. Howden, L.F. Chu, E.J. Sontheimer, and J.A. Thomson Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis Proc. Natl. Acad. Sci. USA 110 2013 15644 15649
16. J. Ji, S.H. Ng, V. Sharma, D. Neculai, S. Hussein, M. Sam, Q. Trinh, G.M. Church, J.D. McPherson, A. Nagy, and N.N. Batada Elevated coding mutation rate during the reprogramming of human somatic cells into induced pluripotent stem cells Stem Cells 30 2012 435 440
17. M. Li, K. Suzuki, J. Qu, P. Saini, I. Dubova, F. Yi, J. Lee, I. Sancho-Martinez, G.H. Liu, and J.C. Izpisua Belmonte Efficient correction of hemoglobinopathy-causing mutations by homologous recombination in integration-free patient iPSCs Cell Res. 21 2011 1740 1744
18. M. Li, K. Suzuki, N.Y. Kim, G.H. Liu, and J.C. Izpisua Belmonte A cut above the rest: targeted genome editing technologies in human pluripotent stem cells J. Biol. Chem. 289 2014 4594 4599
19. G.H. Liu, B.Z. Barkho, S. Ruiz, D. Diep, J. Qu, S.L. Yang, A.D. Panopoulos, K. Suzuki, L. Kurian, and C. Walsh et al. Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome Nature 472 2011 221 225
20. G.H. Liu, K. Suzuki, J. Qu, I. Sancho-Martinez, F. Yi, M. Li, S. Kumar, E. Nivet, J. Kim, and R.D. Soligalla et al. Targeted gene correction of laminopathy-associated LMNA mutations in patient-specific iPSCs Cell Stem Cell 8 2011 688 694
21. G.H. Liu, J. Qu, K. Suzuki, E. Nivet, M. Li, N. Montserrat, F. Yi, X. Xu, S. Ruiz, and W. Zhang et al. Progressive degeneration of human neural stem cells caused by pathogenic LRRK2 Nature 491 2012 603 607
22. H. Liu, Y. Chen, Y. Niu, K. Zhang, Y. Kang, W. Ge, X. Liu, E. Zhao, C. Wang, and S. Lin et al. TALEN-mediated gene mutagenesis in rhesus and cynomolgus monkeys Cell Stem Cell 14 2014 323 328
23. A. Lombardo, P. Genovese, C.M. Beausejour, S. Colleoni, Y.L. Lee, K.A. Kim, D. Ando, F.D. Urnov, C. Galli, and P.D. Gregory et al. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery Nat. Biotechnol. 25 2007 1298 1306
24. Y. Miyaoka, A.H. Chan, L.M. Judge, J. Yoo, M. Huang, T.D. Nguyen, P.P. Lizarraga, P.L. So, and B.R. Conklin Isolation of single-base genome-edited human iPS cells without antibiotic selection Nat. Methods 11 2014 291 293
25. V. Pattanayak, C.L. Ramirez, J.K. Joung, and D.R. Liu Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection Nat. Methods 8 2011 765 770
26. A.J. Rattray, B.K. Shafer, C.B. McGill, and J.N. Strathern The roles of REV3 and RAD57 in double-strand-break-repair-induced mutagenesis of Saccharomyces cerevisiae Genetics 162 2002 1063 1077
27. P. Reinhardt, B. Schmid, L.F. Burbulla, D.C. Schöndorf, L. Wagner, M. Glatza, S. Höing, G. Hargus, S.A. Heck, and A. Dhingra et al. Genetic correction of a LRRK2 mutation in human iPSCs links parkinsonian neurodegeneration to ERK-dependent changes in gene expression Cell Stem Cell 12 2013 354 367
28. L.H. Sanders, J. Laganière, O. Cooper, S.K. Mak, B.J. Vu, Y.A. Huang, D.E. Paschon, M. Vangipuram, R. Sundararajan, and F.D. Urnov et al. LRRK2 mutations cause mitochondrial DNA damage in iPSC-derived neural cells from Parkinson's disease patients: reversal by gene correction Neurobiol. Dis. 62 2014 381 386
29. F. Soldner, J. Laganière, A.W. Cheng, D. Hockemeyer, Q. Gao, R. Alagappan, V. Khurana, L.I. Golbe, R.H. Myers, and S. Lindquist et al. Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations Cell 146 2011 318 331
30. J.N. Strathern, B.K. Shafer, and C.B. McGill DNA synthesis errors associated with double-strand-break repair Genetics 140 1995 965 972
31. M. Sugiura, Y. Kasama, R. Araki, Y. Hoki, M. Sunayama, M. Uda, M. Nakamura, S. Ando, and M. Abe Induced Pluripotent Stem Cell Generation- Associated Point Mutations Arise during the Initial Stages of the Conversion of These Cells Stem Cell Reports 2 2014 52 63
32. J. Wang, C.G. Mullighan, J. Easton, S. Roberts, S.L. Heatley, J. Ma, M.C. Rusch, K. Chen, C.C. Harris, and L. Ding et al. CREST maps somatic structural variation in cancer genomes with base-pair resolution Nat. Methods 8 2011 652 654
33. M.A. Young, D.E. Larson, C.W. Sun, D.R. George, L. Ding, C.A. Miller, L. Lin, K.M. Pawlik, K. Chen, and X. Fan et al. Background mutations in parental cells account for most of the genetic heterogeneity of induced pluripotent stem cells Cell Stem Cell 10 2012 570 582
34. K. Yusa, S.T. Rashid, H. Strick-Marchand, I. Varela, P.Q. Liu, D.E. Paschon, E. Miranda, A. Ordóñez, N.R. Hannan, and F.J. Rouhani et al. Targeted gene correction of α1-antitrypsin deficiency in induced pluripotent stem cells Nature 478 2011 391 394
35. J. Zou, M.L. Maeder, P. Mali, S.M. Pruett-Miller, S. Thibodeau-Beganny, B.K. Chou, G. Chen, Z. Ye, I.H. Park, and G.Q. Daley et al. Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells Cell Stem Cell 5 2009 97 110