hPSC gene editing for cardiac disease therapy.
CRISPR/Cas9
Cardiovascular disease
Genome editing
TALEN
ZFN
hiPSC
Journal
Pflugers Archiv : European journal of physiology
ISSN: 1432-2013
Titre abrégé: Pflugers Arch
Pays: Germany
ID NLM: 0154720
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
received:
20
05
2022
accepted:
18
09
2022
revised:
09
08
2022
pubmed:
28
9
2022
medline:
18
10
2022
entrez:
27
9
2022
Statut:
ppublish
Résumé
Cardiovascular diseases (CVDs) are the leading cause of mortality worldwide. However, the lack of human cardiomyocytes with proper genetic backgrounds limits the study of disease mechanisms. Human pluripotent stem cell-derived cardiomyocytes (hPSC-CMs) have significantly advanced the study of these conditions. Moreover, hPSC-CMs made it easy to study CVDs using genome-editing techniques. This article discusses the applications of these techniques in hPSC for studying CVDs. Recently, several genome-editing systems have been used to modify hPSCs, including zinc finger nucleases, transcription activator-like effector nucleases, and clustered regularly interspaced short palindromic repeat-associated protein 9 (CRISPR/Cas9). We focused on the recent advancement of genome editing in hPSCs, which dramatically improved the efficiency of the cell-based mechanism study and therapy for cardiac diseases.
Identifiants
pubmed: 36163402
doi: 10.1007/s00424-022-02751-2
pii: 10.1007/s00424-022-02751-2
doi:
Substances chimiques
Transcription Activator-Like Effector Nucleases
EC 3.1.-
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1123-1132Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, Chen PJ, Wilson C, Newby GA, Raguram A, Liu DR (2019) Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576:149–157. https://doi.org/10.1038/s41586-019-1711-4
doi: 10.1038/s41586-019-1711-4
pubmed: 31634902
pmcid: 6907074
Bultmann S, Morbitzer R, Schmidt CS, 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 40:5368–5377. https://doi.org/10.1093/nar/gks199
doi: 10.1093/nar/gks199
pubmed: 22387464
pmcid: 3384321
Chadwick AC, Musunuru K (2017) Genome editing for the study of cardiovascular diseases. Curr Cardiol Rep 19:22. https://doi.org/10.1007/s11886-017-0830-5
doi: 10.1007/s11886-017-0830-5
pubmed: 28220462
pmcid: 5969527
Chang L, Zhang J, Tseng YH, Xie CQ, Ilany J, Brüning JC, Sun Z, Zhu X, Cui T, Youker KA, Yang Q, Day SM, Kahn CR, Chen YE (2007) Rad GTPase deficiency leads to cardiac hypertrophy. Circulation 116(25):2976–2983. https://doi.org/10.1161/CIRCULATIONAHA.107.707257
doi: 10.1161/CIRCULATIONAHA.107.707257
pubmed: 18056528
pmcid: 4207362
Christidi E, Huang HM, Brunham LR (2018) CRISPR/Cas9-mediated genome editing in human stem cell-derived cardiomyocytes: applications for cardiovascular disease modeling and cardiotoxicity screening. Drug Discov Today Technol 28:13–21. https://doi.org/10.1016/j.ddtec.2018.06.002
doi: 10.1016/j.ddtec.2018.06.002
pubmed: 30205876
Das J, Bhatia P, Singh A (2019) CRISP points on establishing CRISPR-Cas9 in vitro culture experiments in a resource constraint haematology oncology research lab. Indian journal of hematology & blood transfusion: an official journal of Indian Society of Hematology and Blood Transfusion 35(2):208–214. https://doi.org/10.1007/s12288-018-1008-z
doi: 10.1007/s12288-018-1008-z
Den Hartogh SC, Passier R (2016) Concise review: fluorescent reporters in human pluripotent stem cells: contributions to cardiac differentiation and their applications in cardiac disease and toxicity. Stem Cells 34:13–26. https://doi.org/10.1002/stem.2196
doi: 10.1002/stem.2196
DeWeirdt PC, Sangree AK, Hanna RE et al (2020) Genetic screens in isogenic mammalian cell lines without single cell cloning. Nat Commun 11:752. https://doi.org/10.1038/s41467-020-14620-6
doi: 10.1038/s41467-020-14620-6
pubmed: 32029722
pmcid: 7005275
Gaj T, Gersbach CA, Barbas CF (2013) 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405. https://doi.org/10.1016/j.tibtech.2013.04.004
doi: 10.1016/j.tibtech.2013.04.004
pubmed: 23664777
pmcid: 3694601
Gao Y, Wu S, Pan J, Zhang K, Li X, Xu Y, Jin C, He X, Shi J, Ma L, Wu F (2021) CRISPR/Cas9-edited triple-fusion reporter gene imaging of dynamics and function of transplanted human urinary-induced pluripotent stem cell-derived cardiomyocytes. Eur J Nucl Med Mol Imaging 48:708–720. https://doi.org/10.1007/s00259-020-05087-0
doi: 10.1007/s00259-020-05087-0
pubmed: 33216174
Gehrke JM, Cervantes O, Clement MK, Wu Y, Zeng J, Bauer DE, Pinello L, Joung JK (2018) An APOBEC3A-Cas9 base editor with minimized bystander and off-target activities. Nat Biotechnol 36:977–982. https://doi.org/10.1038/nbt.4199
doi: 10.1038/nbt.4199
pubmed: 30059493
pmcid: 6181770
Guo R, Wan F, Morimatsu M, Xu Q, Feng T, Yang H, Gong Y, Ma S, Chang Y, Zhang S, Jiang Y (2021) Cell sheet formation enhances the therapeutic effects of human umbilical cord mesenchymal stem cells on myocardial infarction as a bioactive material. Bioactive materials 6:2999–3012. https://doi.org/10.1016/j.bioactmat.2021.01.036
doi: 10.1016/j.bioactmat.2021.01.036
pubmed: 33732969
pmcid: 7941025
Hernandez MJ, Christman KL (2017) Designing acellular injectable biomaterial therapeutics for treating myocardial infarction and peripheral artery disease. JACC Basic Transl Sci 2:212–226. https://doi.org/10.1016/j.jacbts.2016.11.008
doi: 10.1016/j.jacbts.2016.11.008
pubmed: 29057375
pmcid: 5646282
Hinson JT, Chopra A, Nafissi N, Polacheck WJ, Benson CC, Swist S, Gorham J, Yang L, Schafer S, Sheng CC, Haghighi A (2015) Titin mutations in iPS cells define sarcomere insufficiency as a cause of dilated cardiomyopathy. Science 349:982–986. https://doi.org/10.1126/science.aaa5458
doi: 10.1126/science.aaa5458
pubmed: 26315439
pmcid: 4618316
Jankele R, Svoboda P (2014) TAL effectors: tools for DNA targeting. Brief Funct Genomics 13:409–419. https://doi.org/10.1093/bfgp/elu013
doi: 10.1093/bfgp/elu013
pubmed: 24907364
pmcid: 4168661
Jeziorowska D, Korniat A, Salem JE, Fish K, Hulot JS (2015) Generating patient-specific induced pluripotent stem cells-derived cardiomyocytes for the treatment of cardiac diseases. Expert opinion on biological therapy 15(10): pp.1399–1409. https://doi.org/10.1517/14712598.2015.1064109
Jinek M, Jiang F, Taylor DW, Sternberg SH, Kaya E, Ma E., Anders C, Hauer M, Zhou K, Lin S, Kaplan M, lavarone AT, Charpentier E, Nogales E, Doudna JA (2014) Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science 343(6176).
Karakikes I, Termglinchan V, Cepeda DA, Lee J, Diecke S, Hendel A, Itzhaki I, Ameen M, Shrestha R, Wu H, Ma N (2017) A comprehensive TALEN-based knockout library for generating human-induced pluripotent stem cell–based models for cardiovascular diseases. Circ Res 120:1561–1571. https://doi.org/10.1161/CIRCRESAHA.116.309948
doi: 10.1161/CIRCRESAHA.116.309948
pubmed: 28246128
pmcid: 5429194
Kaur B, Perea-Gil I, Karakikes I (2018) Recent progress in genome editing approaches for inherited cardiovascular diseases. Curr Cardiol Rep 20:58. https://doi.org/10.1007/s11886-018-0998-3
doi: 10.1007/s11886-018-0998-3
pubmed: 29860642
Kim Y, Kweon J, Kim A, Chon JK, Yoo JY, Kim HJ, Kim S, Lee C, Jeong E, Chung E, Kim D, Lee MS, Go EM, Song HJ, Kim H, Cho N, Bang D, Kim S, Kim JS (2013) A library of TAL effector nucleases spanning the human genome. Nat Biotechnol 31:251–258. https://doi.org/10.1038/nbt.2517
doi: 10.1038/nbt.2517
pubmed: 23417094
Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A 93:1156–1160. https://doi.org/10.1073/pnas.93.3.1156
doi: 10.1073/pnas.93.3.1156
pubmed: 8577732
pmcid: 40048
Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK et al (2007) Cardiomyocytes derived from human embryonic stem cells in prosurvival factors enhance function of infarcted rat hearts. Nat Biotechnol 25(9):1015–1024
doi: 10.1038/nbt1327
Lan F, Lee AS, Liang P, Sanchez-Freire V, Nguyen PK, Wang L, Han L, Yen M, Wang Y, Sun N, Abilez OJ (2013) Abnormal calcium handling properties underlie familial hypertrophic cardiomyopathy pathology in patient-specific induced pluripotent stem cells. Cell Stem Cell 12(1):101–113
doi: 10.1016/j.stem.2012.10.010
Lee EJ, Choi EK, Kang SK, Kim GH, Park JY, Kang HJ, Lee SW, Kim KH, Kwon JS, Lee KH, Ahn Y (2012) N-cadherin determines individual variations in the therapeutic efficacy of human umbilical cord blood-derived mesenchymal stem cells in a rat model of myocardial infarction. Mol Ther 20:155–167. https://doi.org/10.1038/mt.2011.202
doi: 10.1038/mt.2011.202
pubmed: 22068423
Lee HK, Willi M, Miller SM, Kim S, Liu C, Liu DR, Hennighausen L (2018) Targeting fidelity of adenine and cytosine base editors in mouse embryos. Nat Commun 9:4804. https://doi.org/10.1038/s41467-018-07322-7
doi: 10.1038/s41467-018-07322-7
pubmed: 30442934
pmcid: 6238002
Li X, Lu WJ, Li YN, Wu F, Bai R, Ma S, Dong T, Zhang H, Lee AS, Wang Y, Lan F (2019) MLP-deficient human pluripotent stem cell derived cardiomyocytes develop hypertrophic cardiomyopathy and heart failure phenotypes due to abnormal calcium handling. Cell Death Dis 10:1–15. https://doi.org/10.1038/s41419-019-1826-4)
doi: 10.1038/s41419-019-1826-4)
Li Y.N, Chang Y, Li X, Li X, Gao J, Zhou Y, Wu F, Bai R, Dong T, Ma S, Zhang S (2020) RAD-deficient human cardiomyocytes develop hypertrophic cardiomyopathy phenotypes due to calcium dysregulation. Frontiers in cell and developmental biology 8. https://doi.org/10.3389/fcell.2020.585879 .
Li H, Yang Y, Hong W et al (2020) Applications of genome editing technology in the targeted therapy of human diseases: mechanisms, advances and prospects. Sig Transduct Target Ther 5:1. https://doi.org/10.1038/s41392-019-0089-y
doi: 10.1038/s41392-019-0089-y
Lian X, Zhang J, Azarin SM, Zhu K, Hazeltine LB, Bao X, Hsiao C, Kamp TJ, Palecek SP (2013) Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat Protoc 8:162–175. https://doi.org/10.1038/nprot.2012.150
doi: 10.1038/nprot.2012.150
pubmed: 23257984
Limpitikul WB, Dick IE, Joshi-Mukherjee R, Overgaard MT, George AL Jr, Yue DT (2014) Calmodulin mutations associated with long QT syndrome prevent inactivation of cardiac L-type Ca (2+) currents and promote proarrhythmic behavior in ventricular myocytes. J Mol Cell Cardiol 74:115–124. https://doi.org/10.1016/j.yjmcc.2014.04.022
doi: 10.1016/j.yjmcc.2014.04.022
pubmed: 24816216
pmcid: 4262253
Lin Q, Zong Y, Xue C, Wang S, Jin S, Zhu Z, Wang Y, Anzalone AV, Raguram A, Doman JL, Liu DR (2020) Prime genome editing in rice and wheat. Nat Biotechnol 38:582–585
doi: 10.1038/s41587-020-0455-x
Liu GH, Qu J, Suzuki K, Nivet E, Li M, Montserrat N, Yi F, Xu X, Ruiz S, Zhang W, Wagner U, Kim A, Ren B, Li Y, Goebl A, Kim J, Soligalla RD, Dubova I, Thompson J, Yates J 3rd, Esteban CR, Sancho-Martinez I, Izpisua Belmonte JC (2012) Progressive degeneration of human neural stem cells caused by pathogenic LRRK2. Nature 491:603–607. https://doi.org/10.1038/nature11557
doi: 10.1038/nature11557
pubmed: 23075850
pmcid: 3504651
Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C (2010) Executive summary: heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 121:948–954. https://doi.org/10.1161/circulationaha.109.192666
doi: 10.1161/circulationaha.109.192666
pubmed: 20177011
Lombardo A, Cesana D, Genovese P et al (2011) Site-specific integration and tailoring of cassette design for sustainable gene transfer. Nat Methods 8:861–869. https://doi.org/10.1038/nmeth.1674)
doi: 10.1038/nmeth.1674)
pubmed: 21857672
Ma D, Liu F (2015) Genome editing and its applications in model organisms. Genomics Proteomics Bioinformatics 13:336–344. https://doi.org/10.1016/j.gpb.2015.12.001
doi: 10.1016/j.gpb.2015.12.001
pubmed: 26762955
Matsa E, Ahrens JH, Wu JC (2016) Human induced pluripotent stem cells as a platform for personalized and precision cardiovascular medicine. Physiol Rev 96:1093–1126. https://doi.org/10.1152/physrev.00036.2015
doi: 10.1152/physrev.00036.2015
pubmed: 27335446
pmcid: 6345246
Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:882–887. https://doi.org/10.1038/42264
doi: 10.1038/42264
pubmed: 9278050
Musunuru K, Sheikh F, Gupta RM, Houser SR, Maher KO, Milan DJ, Terzic A, Wu JC (2018) Induced pluripotent stem cells for cardiovascular disease modeling and precision medicine: a scientific statement from the American Heart Association. Circulation Genomic and Precision Medicine 11(1):43. https://doi.org/10.1161/HCG.0000000000000043
doi: 10.1161/HCG.0000000000000043
Nguyen Q, Lim KRQ, Yokota T (2020) Genome editing for the understanding and treatment of inherited cardiomyopathies. Int J Mol Sci 21:733. https://doi.org/10.3390/ijms21030733
doi: 10.3390/ijms21030733
pmcid: 7036815
Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S (2008) Generation of mouse induced pluripotent stem cells without viral vectors. Science 322:949–953. https://doi.org/10.1126/science.1164270
doi: 10.1126/science.1164270
pubmed: 18845712
Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, Lerou PH, Lensch MW, Daley GQ (2008) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451:141–146. https://doi.org/10.1038/nature06534
doi: 10.1038/nature06534
pubmed: 18157115
Qi T, Wu F, Xie Y, Gao S, Li M, Pu J, Li D, Lan F, Wang Y (2020) Base editing mediated generation of point mutations into human pluripotent stem cells for modeling disease. Frontiers in cell and developmental biology 8:1029. https://doi.org/10.3389/fcell.2020.590581
doi: 10.3389/fcell.2020.590581
Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18:399–404. https://doi.org/10.1038/74447
doi: 10.1038/74447
pubmed: 10748519
Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD, Joung JK (2012) FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 30:460–465. https://doi.org/10.1038/nbt.2170
doi: 10.1038/nbt.2170
pubmed: 22484455
pmcid: 3558947
Ronaldson-Bouchard K, Ma SP, Yeager K, Chen T, Song L, Sirabella D, Morikawa K, Teles D, Yazawa M, Vunjak-Novakovic G (2018) Advanced maturation of human cardiac tissue grown from pluripotent stem cells. Nature 556(7700):239–243. https://doi.org/10.1038/s41586-018-0016-3
doi: 10.1038/s41586-018-0016-3
pubmed: 29618819
pmcid: 5895513
Rosenthal N (1987) Identification of regulatory elements of cloned genes with functional assays. Methods Enzymol 152:704–720. https://doi.org/10.1016/0076-6879(87)52075-4
doi: 10.1016/0076-6879(87)52075-4
pubmed: 2889129
Shin J, Chen J, Solnica-Krezel L (2014) Efficient homologous recombination-mediated genome engineering in zebrafish using TALE nucleases. Development 141:3807–3818. https://doi.org/10.1242/dev.108019.93
doi: 10.1242/dev.108019.93
pubmed: 25249466
pmcid: 4197590
Shinnawi R, Shaheen N, Huber I, Shiti A, Arbel G, Gepstein A, Ballan N, Setter N, Tijsen AJ, Borggrefe M, Gepstein L (2019) Modeling reentry in the short QT syndrome with human-induced pluripotent stem cell–derived cardiac cell sheets. J Am Coll Cardiol 73(18):2310–2324. https://doi.org/10.1016/j.jacc.2019.02.055
doi: 10.1016/j.jacc.2019.02.055
pubmed: 31072576
Simon CS, Zhang L, Wu T, Cai W, Saiz N, Nowotschin S, Cai CL, Hadjantonakis AK (2018) A Gata4 nuclear GFP transcriptional reporter to study endoderm and cardiac development in the mouse. Biol Open 7(12):036517. https://doi.org/10.1242/bio.036517
doi: 10.1242/bio.036517
Strong A, Musunuru K (2017) Genome editing in cardiovascular diseases. Nat Rev Cardiol 14(1):11. https://doi.org/10.1038/nrcardio.2016.139
doi: 10.1038/nrcardio.2016.139
pubmed: 27609628
Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872. https://doi.org/10.1016/j.cell.2007.11.019
doi: 10.1016/j.cell.2007.11.019
pubmed: 18035408
Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676. https://doi.org/10.1016/j.cell.2006.07.024
doi: 10.1016/j.cell.2006.07.024
pubmed: 16904174
Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147. https://doi.org/10.1126/science.282.5391.1145
doi: 10.1126/science.282.5391.1145
pubmed: 9804556
Tohyama S, Fukuda K (2016) Future treatment of heart failure using human iPSC-derived cardiomyocytes. Etiology and Morphogenesis of Congenital Heart Disease pp.25–31. https://doi.org/10.1007/978-4-431-54628-3_4 .
Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67:509–544. https://doi.org/10.1146/annurev.biochem.67.1.509
doi: 10.1146/annurev.biochem.67.1.509
pubmed: 9759496
Wang G, McCain ML, Yang L, He A, Pasqualini FS, Agarwal A, Yuan H, Jiang D, Zhang D, Zangi L, Geva J (2014) Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat Med 20:616–623. https://doi.org/10.1038/nm.3545
doi: 10.1038/nm.3545
pubmed: 24813252
pmcid: 4172922
Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–918. https://doi.org/10.1016/j.cell.2013.04.025
doi: 10.1016/j.cell.2013.04.025
pubmed: 23643243
pmcid: 3969854
Wang Y, Zhang WY, Hu S, Lan F, Lee AS, Huber B, Lisowski L, Liang P, Huang M, De Almeida PE, Won JH (2012) Genome editing of human embryonic stem cells and induced pluripotent stem cells with zinc finger nucleases for cellular imaging. Circ Res 111:1494–1503. https://doi.org/10.1161/CIRCRESAHA.112.274969
doi: 10.1161/CIRCRESAHA.112.274969
pubmed: 22967807
pmcid: 3518748
Wang Z, Su X, Ashraf M, Kim IM, Weintraub NL, Jiang M, Tang Y (2018) Regenerative therapy for cardiomyopathies. J Cardiovasc Transl Res 11:357–365. https://doi.org/10.1007/s12265-018-9807
doi: 10.1007/s12265-018-9807
pubmed: 29744805
pmcid: 6226381
Wu H, Wang Y, Zhang Y, Yang M, Lv J, Liu J, Zhang Y (2015) TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis. Proc Natl Acad Sci U S A 112(13):E1530–E1539. https://doi.org/10.1073/pnas.1421587112
doi: 10.1073/pnas.1421587112
pubmed: 25733846
pmcid: 4386332
Yong SB, Chung JY, Song Y, Kim YH (2018) Recent challenges and advances in genetically-engineered cell therapy. J Pharm Investig 48:199–208. https://doi.org/10.1007/s40005-017-0381-1
doi: 10.1007/s40005-017-0381-1
pubmed: 30680249
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 (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920. https://doi.org/10.1126/science.1151526
doi: 10.1126/science.1151526
pubmed: 18029452
Zimmermann M, Murina O, Reijns M, Agathanggelou A, Challis R, Tarnauskaitė Ž, Muir M, Fluteau A, Aregger M, McEwan A, Yuan W, Clarke M, Lambros MB, Paneesha S, Moss P, Chandrashekhar M, Angers S, Moffat J, Brunton VG, Hart T, Durocher D (2018) CRISPR screens identify genomic ribonucleotides as a source of PARP-trapping lesions. Nature 559(7713):285–289. https://doi.org/10.1038/s41586-018-0291-z)
doi: 10.1038/s41586-018-0291-z)
pubmed: 29973717
pmcid: 6071917
Zu Y, Tong X, Wang Z, Liu D, Pan R, Li Z, Hu Y, Luo Z, Huang P, Wu Q, Zhu Z, Zhang B, Lin S (2013) TALEN-mediated precise genome modification by homologous recombination in zebrafish. Nat Methods 10:329–331. https://doi.org/10.1038/nmeth.2374
doi: 10.1038/nmeth.2374
pubmed: 23435258