Human germline editing: Insights to future clinical treatment of diseases

References

[1] Abou-El-Enein M, Cathomen T, Ivics Z, June CH, Renner M, Schneider CK, Bauer G (2017) Human genome editing in the clinic: new challenges in regulatory benefit-risk assessment. Cell Stem Cell 21:427–430

[2] Abrahimi P, Chang WG, Kluger MS, Qyang Y, Tellides G, Saltzman WM, Pober JS (2015) Efficient gene disruption in cultured primary human endothelial cells by CRISPR/Cas9. Circ Res 117:121–128

[3] Adikusuma F, Piltz S, Corbett MA, Turvey M, McColl SR, Helbig KJ, Beard MR, Hughes J, Pomerantz RT, Thomas PQ (2018) Large deletions induced by Cas9 cleavage. Nature 560:E8–E9

[4] Cao J, Wu L, Zhang SM, Lu M, Cheung WK, Cai W, Gale M, Xu Q, Yan Q (2016) An easy and efficient inducible CRISPR/Cas9 platform with improved specificity for multiple gene targeting. Nucleic Acids Res 44:e149

[5] Chapman JR, Taylor MR, Boulton SJ (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47:497–510

[6] Chen Y, Wang Z, Ni H, Xu Y, Chen Q, Jiang L (2017) CRISPR/Cas9-mediated base-editing system efficiently generates gain-of-function mutations in Arabidopsis. Sci China Life Sci 60:520–523

[7] Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA (2013) Multiplex genome engineering using CRISPR/Cas systems. Science (NY, NY) 339:819–823

[8] Cornu TI, Mussolino C, Cathomen T (2017) Refining strategies to translate genome editing to the clinic. Nat Med 23:415–423

[9] Corrigan-Curay J, O’Reilly M, Kohn DB, Cannon PM, Bao G, Bushman FD, Carroll D, Cathomen T, Joung JK, Roth D (2015) Genome editing technologies: defining a path to clinic. Mol Ther J Am Soc Gene Ther 23:796–806

[10] Eggan K, Rode A, Jentsch I, Samuel C, Hennek T, Tintrup H, Zevnik B, Erwin J, Loring J, Jackson-Grusby L (2002) Male and female mice derived from the same embryonic stem cell clone by tetraploid embryo complementation. Nat Biotechnol 20:455–459

[11] Egli D, Zuccaro MV, Kosicki M, Church GM, Bradley A, Jasin M (2018) Inter-homologue repair in fertilized human eggs? Nature 560:E5–E7

[12] Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR (2018) Publisher Correction: programmable base editing of A*T to G*C in genomic DNA without DNA cleavage. Nature 559:E8

[13] Haapaniemi E, Botla S, Persson J, Schmierer B, Taipale J (2018) CRISPR-Cas9 genome editing induces a p53-mediated DNA damage response. Nat Med 24:927–930

[14] Heyer WD, Ehmsen KT, Liu J (2010) Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44:113–139

[15] Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–1278

[16] Iyer V, Boroviak K, Thomas M, Doe B, Riva L, Ryder E, Adams DJ (2018) No unexpected CRISPR-Cas9 off-target activity revealed by trio sequencing of gene-edited mice. PLoS Genet 14: e1007503

[17] Kang X, He W, Huang Y, Yu Q, Chen Y, Gao X, Sun X, Fan Y (2016) Introducing precise genetic modifications into human 3PN embryos by CRISPR/Cas-mediated genome editing. J Assist Reprod Genet 33:581–588

[18] Kim K, Ryu SM, Kim ST, Baek G, Kim D, Lim K, Chung E, Kim S, Kim JS (2017a) Highly efficient RNA-guided base editing in mouse embryos. Nat Biotechnol 35:435–437

[19] Kim YB, Komor AC, Levy JM, Packer MS, Zhao KT, Liu DR (2017b) Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nat Biotechnol 35:371–376

[20] Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533:420–424

[21] Komor AC, Zhao KT, Packer MS, Gaudelli NM, Waterbury AL, Koblan LW, Kim YB, Badran AH, Liu DR (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

[22] Kosicki M, Tomberg K, Bradley A (2018) Repair of double-strand breaks induced by CRISPR-Cas9 leads to large deletions and complex rearrangements. Nat Biotechnol 36:765–771

[23] Li G, Liu Y, Zeng Y, Li J, Wang L, Yang G, Chen D, Shang X, Chen J, Huang X (2017a) Highly efficient and precise base editing in discarded human tripronuclear embryos. Protein Cell 8:776–779

[24] Li L, Song L, Liu X, Yang X, Li X, He T, Wang N, Yang S, Yu C, Yin T (2017b) Artificial virus delivers CRISPR-Cas9 system for genome editing of cells in mice. ACS Nano 11:95–111

[25] Li TD, Feng GH, Li YF, Wang M, Mao JJ, Wang JQ, Li X, Wang XP, Qu B, Wang LY (2017c) Rat embryonic stem cells produce fertile offspring through tetraploid complementation. Proc Natl Acad Sci USA 114:11974–11979

[26] Liang P, Xu Y, Zhang X, Ding C, Huang R, Zhang Z, Lv J, Xie X, Chen Y, Li Y (2015) CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes. Protein Cell 6:363–372

[27] Liang P, Ding C, Sun H, Xie X, Xu Y, Zhang X, Sun Y, Xiong Y, Ma W, Liu Y (2017a) Correction of beta-thalassemia mutant by base editor in human embryos. Protein Cell 8:811–822

[28] Liang P, Sun H, Sun Y, Zhang X, Xie X, Zhang J, Zhang Z, Chen Y, Ding C, Xiong Y (2017b) Effective gene editing by highfidelity base editor 2 in mouse zygotes. Protein Cell 8:601–611

[29] Liu H, Chen Y, Niu Y, Zhang K, Kang Y, Ge W, Liu X, Zhao E, Wang C, Lin S (2014) TALEN-mediated gene mutagenesis in rhesus and cynomolgus monkeys. Cell Stem Cell 14:323–328

[30] Lu Y, Zhu JK (2017) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol Plant 10:523–525

[31] Ma H, Marti-Gutierrez N, Park SW, Wu J, Lee Y, Suzuki K, Koski A, Ji D, Hayama T, Ahmed R (2017) Correction of a pathogenic gene mutation in human embryos. Nature 548:413–419

[32] Ma H, Marti-Gutierrez N, Park SW, Wu J, Hayama T, Darby H, Van Dyken C, Li Y, Koski A, Liang D (2018) Ma et al. reply. Nature 560:E10–E23

[33] Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826

[34] Nelson CE, Hakim CH, Ousterout DG, Thakore PI, Moreb EA, Castellanos Rivera RM, Madhavan S, Pan X, Ran FA, Yan WX (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351:403–407

[35] Niu Y, Shen B, Cui Y, Chen Y, Wang J, Wang L, Kang Y, Zhao X, Si W, Li W (2014) Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156:836–843

[36] Noel S, Lee SA, Sadasivam M, Hamad ARA, Rabb H (2018) KEAP1 editing using CRISPR/Cas9 for therapeutic NRF2 activation in primary human T lymphocytes. J Immunol 200:1929–1936

[37] Ormond KE, Mortlock DP, Scholes DT, Bombard Y, Brody LC, Faucett WA, Garrison NA, Hercher L, Isasi R, Middleton A (2017) Human germline genome editing. Am J Hum Genet 101:167–176

[38] Pei D, Beier DW, Levy-Lahad E, Marchant G, Rossant J, Izpisua Belmonte JC, Lovell-Badge R, Jaenisch R, Charo A, Baltimore D (2017) Human embryo editing: opportunities and importance of transnational cooperation. Cell Stem Cell 21:423–426

[39] Sato M, Koriyama M, Watanabe S, Ohtsuka M, Sakurai T, Inada E, Saitoh I, Nakamura S, Miyoshi K (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

[40] Savic N, Ringnalda FC, Lindsay H, Berk C, Bargsten K, Li Y, Neri D, Robinson MD, Ciaudo C, Hall J (2018) Covalent linkage of the DNA repair template to the CRISPR-Cas9 nuclease enhances homology-directed repair. eLife.

[41] Schwank G, Koo BK, Sasselli V, Dekkers JF, Heo I, Demircan T, Sasaki N, Boymans S, Cuppen E, van der Ent CK (2013) Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell 13:653–658

[42] Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelson T, Heckl D, Ebert BL, Root DE, Doench JG (2014) Genomescale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87

[43] Shen B, Zhang W, Zhang J, Zhou J, Wang J, Chen L, Wang L, Hodgkins A, Iyer V, Huang X (2014) Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat Methods 11:399–402

[44] Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F (2016) Rationally engineered Cas9 nucleases with improved specificity. Science 351:84–88

[45] Tang L, Zeng Y, Du H, Gong M, Peng J, Zhang B, Lei M, Zhao F, Wang W, Li X (2017) CRISPR/Cas9-mediated gene editing in human zygotes using Cas9 protein. Mol Genet Genomics 292:525–533

[46] 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

[47] Wilde JJ, Aida T, Wienisch M, Zhang Q, Qi P, Feng G (2018) RAD51 enhances zygotic interhomolog repair. bioRxiv.

[48] Wu Y, Liang D, Wang Y, Bai M, Tang W, Bao S, Yan Z, Li D, Li J (2013) Correction of a genetic disease in mouse via use of CRISPR-Cas9. Cell Stem Cell 13:659–662

[49] Zeng Y, Li J, Li G, Huang S, Yu W, Zhang Y, Chen D, Chen J, Liu J, Huang X (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.

[50] Zhou C, Zhang M, Wei Y, Sun Y, Sun Y, Pan H, Yao N, Zhong W, Li Y, Li W (2017) Highly efficient base editing in human tripronuclear zygotes. Protein Cell 8:772–775

[51] Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35:438–440

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