|
|
|
Human germline editing: Insights to future clinical treatment of diseases |
Yanni Li1, Xiang Jin Kang1, Jeremy Kah Sheng Pang2, Boon Seng Soh1,2, Yang Yu3( ), Yong Fan1( ) |
1. Key Laboratory for Major Obstetric Diseases of Guangdong Province, Center of Reproductive Medicine, The Third Affiliated Hospital of Guangzhou Medical University, Guangzhou 510150, China 2. Disease Modeling and Therapeutics Laboratory, A*STAR Institute of Molecular and Cell Biology, 61 Biopolis Drive Proteos, Singapore 138673, Singapore 3. Center of Reproductive Medicine, Department of Obstetrics and Gynecology, Peking University Third Hospital, Beijing 100191, China |
|
|
|
|
|
|
Corresponding Author(s):
Yang Yu,Yong Fan
|
|
Issue Date: 25 July 2019
|
|
| 1 |
M Abou-El-Enein, T Cathomen, Z Ivics, CH June, M Renner, CK Schneider, G Bauer (2017) Human genome editing in the clinic: new challenges in regulatory benefit-risk assessment. Cell Stem Cell 21:427–430
https://doi.org/10.1016/j.stem.2017.09.007
|
| 2 |
P Abrahimi, WG Chang, MS Kluger, Y Qyang, G Tellides, WM Saltzman, JS Pober (2015) Efficient gene disruption in cultured primary human endothelial cells by CRISPR/Cas9. Circ Res 117:121–128
https://doi.org/10.1161/CIRCRESAHA.117.306290
|
| 3 |
F Adikusuma, S Piltz, MA Corbett, M Turvey, SR McColl, KJ Helbig, MR Beard, J Hughes, RT Pomerantz, PQ Thomas (2018) Large deletions induced by Cas9 cleavage. Nature 560:E8–E9
https://doi.org/10.1038/s41586-018-0380-z
|
| 4 |
J Cao, L Wu, SM Zhang, M Lu, WK Cheung, W Cai, M Gale, Q Xu, Q Yan (2016) An easy and efficient inducible CRISPR/Cas9 platform with improved specificity for multiple gene targeting. Nucleic Acids Res 44:e149
https://doi.org/10.1093/nar/gkw660
|
| 5 |
JR Chapman, MR Taylor, SJ Boulton (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47:497–510
https://doi.org/10.1016/j.molcel.2012.07.029
|
| 6 |
Y Chen, Z Wang, H Ni, Y Xu, Q Chen, L Jiang (2017) CRISPR/Cas9-mediated base-editing system efficiently generates gain-of-function mutations in Arabidopsis. Sci China Life Sci 60:520–523
https://doi.org/10.1007/s11427-017-9021-5
|
| 7 |
L Cong, FA Ran, D Cox, S Lin, R Barretto, N Habib, PD Hsu, X Wu, W Jiang, LA Marraffiniet al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science (NY, NY) 339:819–823
https://doi.org/10.1126/science.1231143
|
| 8 |
TI Cornu, C Mussolino, T Cathomen (2017) Refining strategies to translate genome editing to the clinic. Nat Med 23:415–423
https://doi.org/10.1038/nm.4313
|
| 9 |
J Corrigan-Curay, M O’Reilly, DB Kohn, PM Cannon, G Bao, FD Bushman, D Carroll, T Cathomen, JK Joung, D Rothet al. (2015) Genome editing technologies: defining a path to clinic. Mol Ther J Am Soc Gene Ther 23:796–806
https://doi.org/10.1038/mt.2015.54
|
| 10 |
K Eggan, A Rode, I Jentsch, C Samuel, T Hennek, H Tintrup, B Zevnik, J Erwin, J Loring, L Jackson-Grusbyet al. (2002) Male and female mice derived from the same embryonic stem cell clone by tetraploid embryo complementation. Nat Biotechnol 20:455–459
https://doi.org/10.1038/nbt0502-455
|
| 11 |
D Egli, MV Zuccaro, M Kosicki, GM Church, A Bradley, M Jasin (2018) Inter-homologue repair in fertilized human eggs? Nature 560:E5–E7
https://doi.org/10.1038/s41586-018-0379-5
|
| 12 |
NM Gaudelli, AC Komor, HA Rees, MS Packer, AH Badran, DI Bryson, DR Liu (2018) Publisher Correction: programmable base editing of A*T to G*C in genomic DNA without DNA cleavage. Nature 559:E8
https://doi.org/10.1038/s41586-018-0070-x
|
| 13 |
E Haapaniemi, S Botla, J Persson, B Schmierer, J Taipale (2018) CRISPR-Cas9 genome editing induces a p53-mediated DNA damage response. Nat Med 24:927–930
https://doi.org/10.1038/s41591-018-0049-z
|
| 14 |
WD Heyer, KT Ehmsen, J Liu (2010) Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44:113–139
https://doi.org/10.1146/annurev-genet-051710-150955
|
| 15 |
PD Hsu, ES Lander, F Zhang (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–1278
https://doi.org/10.1016/j.cell.2014.05.010
|
| 16 |
V Iyer, K Boroviak, M Thomas, B Doe, L Riva, E Ryder, DJ Adams (2018) No unexpected CRISPR-Cas9 off-target activity revealed by trio sequencing of gene-edited mice. PLoS Genet 14: e1007503
https://doi.org/10.1371/journal.pgen.1007503
|
| 17 |
X Kang, W He, Y Huang, Q Yu, Y Chen, X Gao, X Sun, Y Fan (2016) Introducing precise genetic modifications into human 3PN embryos by CRISPR/Cas-mediated genome editing. J Assist Reprod Genet 33:581–588
https://doi.org/10.1007/s10815-016-0710-8
|
| 18 |
K Kim, SM Ryu, ST Kim, G Baek, D Kim, K Lim, E Chung, S Kim, JS Kim (2017a) Highly efficient RNA-guided base editing in mouse embryos. Nat Biotechnol 35:435–437
https://doi.org/10.1038/nbt.3816
|
| 19 |
YB Kim, AC Komor, JM Levy, MS Packer, KT Zhao, DR Liu (2017b) Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nat Biotechnol 35:371–376
https://doi.org/10.1038/nbt.3803
|
| 20 |
AC Komor, YB Kim, MS Packer, JA Zuris, DR Liu (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533:420–424
https://doi.org/10.1038/nature17946
|
| 21 |
AC Komor, KT Zhao, MS Packer, NM Gaudelli, AL Waterbury, LW Koblan, YB Kim, AH Badran, DR Liu (2017) Improved base excision repair inhibition and bacteriophage Mu Gam protein yields C:G-to-T:A base editors with higher efficiency and product purity. Sci Adv 3:eaao4774
https://doi.org/10.1126/sciadv.aao4774
|
| 22 |
M Kosicki, K Tomberg, A Bradley (2018) Repair of double-strand breaks induced by CRISPR-Cas9 leads to large deletions and complex rearrangements. Nat Biotechnol 36:765–771
https://doi.org/10.1038/nbt.4192
|
| 23 |
G Li, Y Liu, Y Zeng, J Li, L Wang, G Yang, D Chen, X Shang, J Chen, X Huanget al. (2017a) Highly efficient and precise base editing in discarded human tripronuclear embryos. Protein Cell 8:776–779
https://doi.org/10.1007/s13238-017-0458-7
|
| 24 |
L Li, L Song, X Liu, X Yang, X Li, T He, N Wang, S Yang, C Yu, T Yinet al. (2017b) Artificial virus delivers CRISPR-Cas9 system for genome editing of cells in mice. ACS Nano 11:95–111
https://doi.org/10.1021/acsnano.6b04261
|
| 25 |
TD Li, GH Feng, YF Li, M Wang, JJ Mao, JQ Wang, X Li, XP Wang, B Qu, LY Wanget al. (2017c) Rat embryonic stem cells produce fertile offspring through tetraploid complementation. Proc Natl Acad Sci USA 114:11974–11979
https://doi.org/10.1073/pnas.1708710114
|
| 26 |
P Liang, Y Xu, X Zhang, C Ding, R Huang, Z Zhang, J Lv, X Xie, Y Chen, Y Liet al. (2015) CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes. Protein Cell 6:363–372
https://doi.org/10.1007/s13238-015-0153-5
|
| 27 |
P Liang, C Ding, H Sun, X Xie, Y Xu, X Zhang, Y Sun, Y Xiong, W Ma, Y Liuet al. (2017a) Correction of beta-thalassemia mutant by base editor in human embryos. Protein Cell 8:811–822
https://doi.org/10.1007/s13238-017-0475-6
|
| 28 |
P Liang, H Sun, Y Sun, X Zhang, X Xie, J Zhang, Z Zhang, Y Chen, C Ding, Y Xionget al. (2017b) Effective gene editing by highfidelity base editor 2 in mouse zygotes. Protein Cell 8:601–611
https://doi.org/10.1007/s13238-017-0418-2
|
| 29 |
H Liu, Y Chen, Y Niu, K Zhang, Y Kang, W Ge, X Liu, E Zhao, C Wang, S Linet al. (2014) TALEN-mediated gene mutagenesis in rhesus and cynomolgus monkeys. Cell Stem Cell 14:323–328
https://doi.org/10.1016/j.stem.2014.01.018
|
| 30 |
Y Lu, JK Zhu (2017) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol Plant 10:523–525
https://doi.org/10.1016/j.molp.2016.11.013
|
| 31 |
H Ma, N Marti-Gutierrez, SW Park, J Wu, Y Lee, K Suzuki, A Koski, D Ji, T Hayama, R Ahmedet al. (2017) Correction of a pathogenic gene mutation in human embryos. Nature 548:413–419
https://doi.org/10.1038/nature23305
|
| 32 |
H Ma, N Marti-Gutierrez, SW Park, J Wu, T Hayama, H Darby, C Van Dyken, Y Li, A Koski, D Lianget al. (2018) Ma et al. reply. Nature 560:E10–E23
https://doi.org/10.1038/s41586-018-0381-y
|
| 33 |
P Mali, L Yang, KM Esvelt, J Aach, M Guell, JE DiCarlo, JE Norville, GM Church (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826
https://doi.org/10.1126/science.1232033
|
| 34 |
CE Nelson, CH Hakim, DG Ousterout, PI Thakore, EA Moreb, RM Castellanos Rivera, S Madhavan, X Pan, FA Ran, WX Yanet al. (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351:403–407
https://doi.org/10.1126/science.aad5143
|
| 35 |
Y Niu, B Shen, Y Cui, Y Chen, J Wang, L Wang, Y Kang, X Zhao, W Si, W Liet al. (2014) Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156:836–843
https://doi.org/10.1016/j.cell.2014.01.027
|
| 36 |
S Noel, SA Lee, M Sadasivam, ARA Hamad, H Rabb (2018) KEAP1 editing using CRISPR/Cas9 for therapeutic NRF2 activation in primary human T lymphocytes. J Immunol 200:1929–1936
https://doi.org/10.4049/jimmunol.1700812
|
| 37 |
KE Ormond, DP Mortlock, DT Scholes, Y Bombard, LC Brody, WA Faucett, NA Garrison, L Hercher, R Isasi, A Middletonet al. (2017) Human germline genome editing. Am J Hum Genet 101:167–176
https://doi.org/10.1016/j.ajhg.2017.06.012
|
| 38 |
D Pei, DW Beier, E Levy-Lahad, G Marchant, J Rossant, JC Izpisua Belmonte, R Lovell-Badge, R Jaenisch, A Charo, D Baltimore (2017) Human embryo editing: opportunities and importance of transnational cooperation. Cell Stem Cell 21:423–426
https://doi.org/10.1016/j.stem.2017.09.010
|
| 39 |
M Sato, M Koriyama, S Watanabe, M Ohtsuka, T Sakurai, E Inada, I Saitoh, S Nakamura, K Miyoshi (2015) Direct injection of CRISPR/Cas9-related mRNA into cytoplasm of parthenogenetically activated porcine oocytes causes frequent mosaicism for Indel mutations. Int J Mol Sci 16:17838–17856
https://doi.org/10.3390/ijms160817838
|
| 40 |
N Savic, FC Ringnalda, H Lindsay, C Berk, K Bargsten, Y Li, D Neri, MD Robinson, C Ciaudo, J Hallet al. (2018) Covalent linkage of the DNA repair template to the CRISPR-Cas9 nuclease enhances homology-directed repair. eLife.
https://doi.org/10.7554/eLife.33761.001
|
| 41 |
G Schwank, BK Koo, V Sasselli, JF Dekkers, I Heo, T Demircan, N Sasaki, S Boymans, E Cuppen, CK van der Entet al. (2013) Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell 13:653–658
https://doi.org/10.1016/j.stem.2013.11.002
|
| 42 |
O Shalem, NE Sanjana, E Hartenian, X Shi, DA Scott, T Mikkelson, D Heckl, BL Ebert, DE Root, JG Doenchet al. (2014) Genomescale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87
https://doi.org/10.1126/science.1247005
|
| 43 |
B Shen, W Zhang, J Zhang, J Zhou, J Wang, L Chen, L Wang, A Hodgkins, V Iyer, X Huanget al. (2014) Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat Methods 11:399–402
https://doi.org/10.1038/nmeth.2857
|
| 44 |
IM Slaymaker, L Gao, B Zetsche, DA Scott, WX Yan, F Zhang (2016) Rationally engineered Cas9 nucleases with improved specificity. Science 351:84–88
https://doi.org/10.1126/science.aad5227
|
| 45 |
L Tang, Y Zeng, H Du, M Gong, J Peng, B Zhang, M Lei, F Zhao, W Wang, X Liet al. (2017) CRISPR/Cas9-mediated gene editing in human zygotes using Cas9 protein. Mol Genet Genomics 292:525–533
https://doi.org/10.1007/s00438-017-1299-z
|
| 46 |
H Wang, H Yang, CS Shivalila, MM Dawlaty, AW Cheng, F Zhang, R Jaenisch (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
|
| 47 |
JJ Wilde, T Aida, M Wienisch, Q Zhang, P Qi, G Feng (2018) RAD51 enhances zygotic interhomolog repair. bioRxiv.
https://doi.org/10.1101/263699
|
| 48 |
Y Wu, D Liang, Y Wang, M Bai, W Tang, S Bao, Z Yan, D Li, J Li (2013) Correction of a genetic disease in mouse via use of CRISPR-Cas9. Cell Stem Cell 13:659–662
https://doi.org/10.1016/j.stem.2013.10.016
|
| 49 |
Y Zeng, J Li, G Li, S Huang, W Yu, Y Zhang, D Chen, J Chen, J Liu, X Huang (2018) Correction of the Marfan syndrome pathogenic FBN1 mutation by base editing in human cells and heterozygous embryos. Mol Ther J Am Soc Gene Ther.
https://doi.org/10.1016/j.ymthe.2018.08.007
|
| 50 |
C Zhou, M Zhang, Y Wei, Y Sun, Y Sun, H Pan, N Yao, W Zhong, Y Li, W Liet al. (2017) Highly efficient base editing in human tripronuclear zygotes. Protein Cell 8:772–775
https://doi.org/10.1007/s13238-017-0459-6
|
| 51 |
Y Zong, Y Wang, C Li, R Zhang, K Chen, Y Ran, JL Qiu, D Wang, C Gao (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35:438–440
https://doi.org/10.1038/nbt.3811
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|