logo

SCIENCE CHINA Life Sciences, Volume 60, Issue 5: 447-457(2017) https://doi.org/10.1007/s11427-017-9032-4

CRISPR/Cas9-mediated correction of human genetic disease

More info
  • ReceivedFeb 12, 2017
  • AcceptedMar 5, 2017
  • PublishedMay 3, 2017

Abstract

The clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated (Cas) protein 9 system (CRISPR/Cas9) provides a powerful tool for targeted genetic editing. Directed by programmable sequence-specific RNAs, this system introduces cleavage and double-stranded breaks at target sites precisely. Compared to previously developed targeted nucleases, the CRISPR/Cas9 system demonstrates several promising advantages, including simplicity, high specificity, and efficiency. Several broad genome-editing studies with the CRISPR/Cas9 system in different species in vivo and ex vivo have indicated its strong potential, raising hopes for therapeutic genome editing in clinical settings. Taking advantage of non-homologous end-joining (NHEJ) and homology directed repair (HDR)-mediated DNA repair, several studies have recently reported the use of CRISPR/Cas9 to successfully correct disease-causing alleles ranging from single base mutations to large insertions. In this review, we summarize and discuss recent preclinical studies involving the CRISPR/Cas9-mediated correction of human genetic diseases.


Funded by

National Natural Science Foundation(NSFC81502677,NSFC81602699,NSFC81123003)

National Key Research and Development Program of China(2016YFA0201402)

Key Technologies R & D program of Sichuan Province(2015FZ0040)


Acknowledgment

This work was supported by the National Natural Science Foundation (NSFC81502677, NSFC81602699, NSFC81123003), the National Key Research and Development Program of China (2016YFA0201402), and the Key Technologies R & D program of Sichuan Province (2015FZ0040).


Interest statement

The author(s) declare that they have no conflict of interest.


References

[1] Aartsma-Rus A., Kaman W.E., Weij R., den Dunnen J.T., van Ommen G.J.B., van Deutekom J.C.T.. Exploring the frontiers of therapeutic exon skipping for Duchenne muscular dystrophy by double targeting within one or multiple exons. Mol Ther, 2006, 14: 401-407 CrossRef PubMed Google Scholar

[2] Aartsma-Rus A., Fokkema I., Verschuuren J., Ginjaar I., van Deutekom J., van Ommen G.J., den Dunnen J.T.. Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Hum Mutat, 2009, 30: 293-299 CrossRef PubMed Google Scholar

[3] Aoki Y., Yokota T., Nagata T., Nakamura A., Tanihata J., Saito T., Duguez S.M.R., Nagaraju K., Hoffman E.P., Partridge T., Takeda S.. Bodywide skipping of exons 45–55 in dystrophic mdx52 mice by systemic antisense delivery. Proc Natl Acad Sci USA, 2012, 109: 13763-13768 CrossRef PubMed ADS Google Scholar

[4] Asokan A., Schaffer D.V., Jude Samulski R.. The AAV vector toolkit: poised at the clinical crossroads. Mol Ther, 2012, 20: 699-708 CrossRef PubMed Google Scholar

[5] Avior Y., Sagi I., Benvenisty N.. Pluripotent stem cells in disease modelling and drug discovery. Nat Rev Mol Cell Biol, 2016, 17: 170-182 CrossRef PubMed Google Scholar

[6] Azuma H., Paulk N., Ranade A., Dorrell C., Al-Dhalimy M., Ellis E., Strom S., Kay M.A., Finegold M., Grompe M.. Robust expansion of human hepatocytes in Fah−/−/Rag2−/−/Il2rg−/− mice. Nat Biotechnol, 2007, 25: 903-910 CrossRef PubMed Google Scholar

[7] Bamshad M.J., Ng S.B., Bigham A.W., Tabor H.K., Emond M.J., Nickerson D.A., Shendure J.. Exome sequencing as a tool for Mendelian disease gene discovery. Nat Rev Genet, 2011, 12: 745-755 CrossRef PubMed Google Scholar

[8] Bassuk A.G., Zheng A., Li Y., Tsang S.H., Mahajan V.B.. Precision medicine: genetic repair of retinitis pigmentosa in patient-derived stem cells. Sci Rep, 2016, 6: 19969 CrossRef PubMed ADS Google Scholar

[9] Beckmann J.S., Estivill X., Antonarakis S.E.. Copy number variants and genetic traits: closer to the resolution of phenotypic to genotypic variability. Nat Rev Genet, 2007, 8: 639-646 CrossRef PubMed Google Scholar

[10] Blasco R.B., Karaca E., Ambrogio C., Cheong T.C., Karayol E., Minero V.G., Voena C., Chiarle R.. Simple and rapid in vivo generation of chromosomal rearrangements using CRISPR/Cas9 technology. Cell Rep, 2014, 9: 1219-1227 CrossRef PubMed Google Scholar

[11] Bondeson M.L., Dahl N., Malmgren H., Kleijer W.J., Tönnesen T., Carlberg B.M., Pettersson U.. Inversion of the IDS gene resulting from recombination with IDS-related sequences in a common cause of the Hunter syndrome. Hum Mol Genet, 1995, 4: 615-621 CrossRef Google Scholar

[12] Carbery I.D., Ji D., Harrington A., Brown V., Weinstein E.J., Liaw L., Cui X.. Targeted genome modification in mice using zinc-finger nucleases. Genets, 2010, 186: 451-459 CrossRef PubMed Google Scholar

[13] Chang C.W., Lai Y.S., Westin E., Khodadadi-Jamayran A., Pawlik K.M., Lamb Jr. L.S., Goldman F.D., Townes T.M.. Modeling human severe combined immunodeficiency and correction by CRISPR/Cas9-enhanced gene targeting. Cell Rep, 2015, 12: 1668-1677 CrossRef PubMed Google Scholar

[14] Chang N., Sun C., Gao L., Zhu D., Xu X., Zhu X., Xiong J.W., Xi J.J.. Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos. Cell Res, 2013, 23: 465-472 CrossRef PubMed Google Scholar

[15] Chen F., Pruett-Miller S.M., Huang Y., Gjoka M., Duda K., Taunton J., Collingwood T.N., Frodin M., Davis G.D.. High-frequency genome editing using ssDNA oligonucleotides with zinc-finger nucleases. Nat Meth, 2011, 8: 753-755 CrossRef PubMed Google Scholar

[16] Cheng S.H., Gregory R.J., Marshall J., Paul S., Souza D.W., White G.A., O’Riordan C.R., Smith A.E.. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell, 1990, 63: 827-834 CrossRef Google Scholar

[17] Chen Z.G., Zhang Y.A.. Cell therapy for macular degeneration—first phase I/II pluripotent stem cell-based clinical trial shows promise. Sci China Life Sci, 2015, 58: 119-120 CrossRef PubMed Google Scholar

[18] Cho S.W., Kim S., Kim J.M., Kim J.S.. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol, 2013, 31: 230-232 CrossRef PubMed Google Scholar

[19] Choi P.S., Meyerson M.. Targeted genomic rearrangements using CRISPR/Cas technology. Nat Commun, 2014, 5: 3728 CrossRef PubMed ADS Google Scholar

[20] Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A., Zhang F.. Multiplex genome engineering using CRISPR/Cas systems. Science, 2013, 339: 819-823 CrossRef PubMed ADS Google Scholar

[21] Davidoff A.M., Gray J.T., Ng C.Y.C., Zhang Y., Zhou J., Spence Y., Bakar Y., Nathwani A.C.. Comparison of the ability of adeno-associated viral vectors pseudotyped with serotype 2, 5, and 8 capsid proteins to mediate efficient transduction of the liver in murine and nonhuman primate models. Mol Ther, 2005, 11: 875-888 CrossRef PubMed Google Scholar

[22] Dickinson D.J., Ward J.D., Reiner D.J., Goldstein B.. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Meth, 2013, 10: 1028-1034 CrossRef PubMed Google Scholar

[23] Ding Q., Strong A., Patel K.M., Ng S.L., Gosis B.S., Regan S.N., Cowan C.A., Rader D.J., Musunuru K.. Permanent alteration of PCSK9 with in vivo CRISPR-Cas9 genome editing. Circul Res, 2014, 115: 488-492 CrossRef PubMed Google Scholar

[24] Filareto A., Parker S., Darabi R., Borges L., Iacovino M., Schaaf T., Mayerhofer T., Chamberlain J.S., Ervasti J.M., McIvor R.S., Kyba M., Perlingeiro R.C.R.. An ex vivo gene therapy approach to treat muscular dystrophy using inducible pluripotent stem cells. Nat Commun, 2013, 4: 1549 CrossRef PubMed ADS Google Scholar

[25] Flynn R., Grundmann A., Renz P., Hänseler W., James W.S., Cowley S.A., Moore M.D.. CRISPR-mediated genotypic and phenotypic correction of a chronic granulomatous disease mutation in human iPS cells. Exp Hematol, 2015, 43: 838-848.e3 CrossRef PubMed Google Scholar

[26] Frazer K.A., Murray S.S., Schork N.J., Topol E.J.. Human genetic variation and its contribution to complex traits. Nat Rev Genet, 2009, 10: 241-251 CrossRef PubMed Google Scholar

[27] Friedland A.E., Tzur Y.B., Esvelt K.M., Colaiácovo M.P., Church G.M., Calarco J.A.. Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Meth, 2013, 10: 741-743 CrossRef PubMed Google Scholar

[28] Gao X.. Model animals and their applications. Sci China Life Sci, 2015, 58: 319-320 CrossRef PubMed Google Scholar

[29] Gilissen C., Hoischen A., Brunner H.G., Veltman J.A.. Unlocking Mendelian disease using exome sequencing. Genome Biol, 2011, 12: 228 CrossRef PubMed Google Scholar

[30] Graw J., Brackmann H.H., Oldenburg J., Schneppenheim R., Spannagl M., Schwaab R.. Haemophilia A: from mutation analysis to new therapies. Nat Rev Genet, 2005, 6: 488-501 CrossRef PubMed Google Scholar

[31] Hanna J., Wernig M., Markoulaki S., Sun C.W., Meissner A., Cassady J.P., Beard C., Brambrink T., Wu L.C., Townes T.M., Jaenisch R.. Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science, 2007, 318: 1920-1923 CrossRef PubMed ADS Google Scholar

[32] Hoffman E.P., Brown Jr. R.H., Kunkel L.M.. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell, 1987, 51: 919-928 CrossRef Google Scholar

[33] Huang X., Wang Y., Yan W., Smith C., Ye Z., Wang J., Gao Y., Mendelsohn L., Cheng L.. Production of gene-corrected adult beta globin protein in human erythrocytes differentiated from patient iPSCs after genome editing of the sickle point mutation. Stem Cells, 2015, 33: 1470-1479 CrossRef PubMed Google Scholar

[34] Huertas P.. DNA resection in eukaryotes: deciding how to fix the break. Nat Struct Mol Biol, 2010, 17: 11-16 CrossRef PubMed Google Scholar

[35] Hwang W.Y., Fu Y., Reyon D., Maeder M.L., Tsai S.Q., Sander J.D., Peterson R.T., Yeh J.R.J., Joung J.K.. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol, 2013, 31: 227-229 CrossRef PubMed Google Scholar

[36] Inagaki K., Fuess S., Storm T.A., Gibson G.A., Mctiernan C.F., Kay M.A., Nakai H.. Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol Ther, 2006, 14: 45-53 CrossRef PubMed Google Scholar

[37] Jao L.E., Wente S.R., Chen W.. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci USA, 2013, 110: 13904-13909 CrossRef PubMed ADS Google Scholar

[38] Jinek M., East A., Cheng A., Lin S., Ma E., Doudna J.. RNA-programmed genome editing in human cells. eLife, 2013, 2: e00471 CrossRef PubMed Google Scholar

[39] Kay M.A., Manno C.S., Ragni M.V., Larson P.J., Couto L.B., McClelland A., Glader B., Chew A.J., Tai S.J., Herzog R.W., Arruda V., Johnson F., Scallan C., Skarsgard E., Flake A.W., High K.A.. Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat Genet, 2000, 24: 257-261 CrossRef PubMed Google Scholar

[40] Kimbrel E.A., Lanza R.. Current status of pluripotent stem cells: moving the first therapies to the clinic. Nat Rev Drug Discov, 2015, 14: 681-692 CrossRef PubMed Google Scholar

[41] Li H.L., Fujimoto N., Sasakawa N., Shirai S., Ohkame T., Sakuma T., Tanaka M., Amano N., Watanabe A., Sakurai H., Yamamoto T., Yamanaka S., Hotta A.. Precise correction of the dystrophin gene in Duchenne muscular dystrophy patient induced pluripotent stem cells by TALEN and CRISPR-Cas9. Stem Cell Rep, 2015, 4: 143-154 CrossRef PubMed Google Scholar

[42] Li W., Teng F., Li T., Zhou Q.. Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nat Biotechnol, 2013, 31: 684-686 CrossRef PubMed Google Scholar

[43] Lisowski L., Dane A.P., Chu K., Zhang Y., Cunningham S.C., Wilson E.M., Nygaard S., Grompe M., Alexander I.E., Kay M.A.. Selection and evaluation of clinically relevant AAV variants in a xenograft liver model. Nature, 2014, 506: 382-386 CrossRef PubMed ADS Google Scholar

[44] Long C., McAnally J.R., Shelton J.M., Mireault A.A., Bassel-Duby R., Olson E.N.. Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA. Science, 2014, 345: 1184-1188 CrossRef PubMed ADS Google Scholar

[45] Lu Q.L., Yokota T., Takeda S., Garcia L., Muntoni F., Partridge T.. The status of exon skipping as a therapeutic approach to Duchenne muscular dystrophy. Mol Ther, 2011, 19: 9-15 CrossRef PubMed Google Scholar

[46] Maddalo D., Manchado E., Concepcion C.P., Bonetti C., Vidigal J.A., Han Y.C., Ogrodowski P., Crippa A., Rekhtman N., de Stanchina E., Lowe S.W., Ventura A.. In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system. Nature, 2014, 516: 423-427 CrossRef PubMed ADS Google Scholar

[47] Mali P., Esvelt K.M., Church G.M.. Cas9 as a versatile tool for engineering biology. Nat Meth, 2013a, 10: 957-963 CrossRef PubMed Google Scholar

[48] Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M.. RNA-guided human genome engineering via Cas9. Science, 2013b, 339: 823-826 CrossRef PubMed ADS Google Scholar

[49] Manno C.S., Pierce G.F., Arruda V.R., Glader B., Ragni M., Rasko J.J., Rasko J., Ozelo M.C., Hoots K., Blatt P., Konkle B., Dake M., Kaye R., Razavi M., Zajko A., Zehnder J., Rustagi P.K., Nakai H., Chew A., Leonard D., Wright J.F., Lessard R.R., Sommer J.M., Tigges M., Sabatino D., Luk A., Jiang H., Mingozzi F., Couto L., Ertl H.C., High K.A., Kay M.A.. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med, 2006, 12: 342-347 CrossRef PubMed Google Scholar

[50] Mingozzi F., High K.A.. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet, 2011, 12: 341-355 CrossRef PubMed Google Scholar

[51] Morrissey D.V., Lockridge J.A., Shaw L., Blanchard K., Jensen K., Breen W., Hartsough K., Machemer L., Radka S., Jadhav V., Vaish N., Zinnen S., Vargeese C., Bowman K., Shaffer C.S., Jeffs L.B., Judge A., MacLachlan I., Polisky B.. Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat Biotechnol, 2005, 23: 1002-1007 CrossRef PubMed Google Scholar

[52] Mukherjee S., Thrasher A.J.. iPSCs: unstable origins?. Mol Ther, 2011, 19: 1188-1190 CrossRef PubMed Google Scholar

[53] Nathwani A.C., Gray J.T., Ng C.Y.C., Zhou J., Spence Y., Waddington S.N., Tuddenham E.G.D., Kemball-Cook G., McIntosh J., Boon-Spijker M., Mertens K., Davidoff A.M.. Self-complementary adeno-associated virus vectors containing a novel liver-specific human factor IX expression cassette enable highly efficient transduction of murine and nonhuman primate liver. Blood, 2006, 107: 2653-2661 CrossRef PubMed Google Scholar

[54] Nathwani A.C., Tuddenham E.G.D., Rangarajan S., Rosales C., McIntosh J., Linch D.C., Chowdary P., Riddell A., Pie A.J., Harrington C., O'Beirne J., Smith K., Pasi J., Glader B., Rustagi P., Ng C.Y.C., Kay M.A., Zhou J., Spence Y., Morton C.L., Allay J., Coleman J., Sleep S., Cunningham J.M., Srivastava D., Basner-Tschakarjan E., Mingozzi F., High K.A., Gray J.T., Reiss U.M., Nienhuis A.W., Davidoff A.M.. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med, 2011, 365: 2357-2365 CrossRef PubMed Google Scholar

[55] Nikiforova M.N., Stringer J.R., Blough R., Medvedovic M., Fagin J.A., Nikiforov Y.E.. Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science, 2000, 290: 138-141 CrossRef ADS Google Scholar

[56] Okada T., Takeda S.. Current challenges and future directions in recombinant AAV-mediated gene therapy of Duchenne muscular dystrophy. Pharmaceuticals, 2013, 6: 813-836 CrossRef PubMed Google Scholar

[57] Olivares E.C., Hollis R.P., Chalberg T.W., Meuse L., Kay M.A., Calos M.P.. Site-specific genomic integration produces therapeutic factor IX levels in mice. Nat Biotech, 2002, 20: 1124-1128 CrossRef PubMed Google Scholar

[58] Ott J., Kamatani Y., Lathrop M.. Family-based designs for genome-wide association studies. Nat Rev Genet, 2011, 12: 465-474 CrossRef PubMed Google Scholar

[59] Ousterout D.G., Kabadi A.M., Thakore P.I., Majoros W.H., Reddy T.E., Gersbach C.A.. Multiplex CRISPR/Cas9-based genome editing for correction of dystrophin mutations that cause Duchenne muscular dystrophy. Nat Commun, 2015, 6: 6244 CrossRef PubMed ADS Google Scholar

[60] Park C.Y., Kim D.H., Son J.S., Sung J.J., Lee J., Bae S., Kim J.H., Kim D.W., Kim J.S.. Functional correction of large factor VIII gene chromosomal inversions in hemophilia A patient-derived iPSCs using CRISPR-Cas9. Cell Stem Cell, 2015, 17: 213-220 CrossRef PubMed Google Scholar

[61] Park I.H., Arora N., Huo H., Maherali N., Ahfeldt T., Shimamura A., Lensch M.W., Cowan C., Hochedlinger K., Daley G.Q.. Disease-specific induced pluripotent stem cells. Cell, 2008, 134: 877-886 CrossRef PubMed Google Scholar

[62] Paulk N.K., Wursthorn K., Wang Z., Finegold M.J., Kay M.A., Grompe M.. Adeno-associated virus gene repair corrects a mouse model of hereditary tyrosinemia in vivo. Hepatology, 2010, 51: 1200-1208 CrossRef PubMed Google Scholar

[63] Pichavant C., Aartsma-Rus A., Clemens P.R., Davies K.E., Dickson G., Takeda S., Wilton S.D., Wolff J.A., Wooddell C.I., Xiao X., Tremblay J.P.. Current status of pharmaceutical and genetic therapeutic approaches to treat DMD. Mol Ther, 2011, 19: 830-840 CrossRef PubMed Google Scholar

[64] Piras B.A., Drury J.E., Morton C.L., Spence Y., Lockey T.D., Nathwani A.C., Davidoff A.M., Meagher M.M.. Distribution of AAV8 particles in cell lysates and culture media changes with time and is dependent on the recombinant vector. Mol Ther Methods Clin Dev, 2016, 3: 16015 CrossRef PubMed Google Scholar

[65] Pirazzoli V., Nebhan C., Song X., Wurtz A., Walther Z., Cai G., Zhao Z., Jia P., de Stanchina E., Shapiro E.M., Gale M., Yin R., Horn L., Carbone D.P., Stephens P.J., Miller V., Gettinger S., Pao W., Politi K.. Acquired resistance of EGFR-mutant lung adenocarcinomas to afatinib plus cetuximab is associated with activation of mTORC1. Cell Rep, 2014, 7: 999-1008 CrossRef PubMed Google Scholar

[66] Platt R.J., Chen S., Zhou Y., Yim M.J., Swiech L., Kempton H.R., Dahlman J.E., Parnas O., Eisenhaure T.M., Jovanovic M., Graham D.B., Jhunjhunwala S., Heidenreich M., Xavier R.J., Langer R., Anderson D.G., Hacohen N., Regev A., Feng G., Sharp P.A., Zhang F.. CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell, 2014, 159: 440-455 CrossRef PubMed Google Scholar

[67] Porteus M.H., Dann C.T.. Genome editing of the germline: broadening the discussion. Mol Ther, 2015, 23: 980-982 CrossRef PubMed Google Scholar

[68] Ran F.A., Cong L., Yan W.X., Scott D.A., Gootenberg J.S., Kriz A.J., Zetsche B., Shalem O., Wu X., Makarova K.S., Koonin E.V., Sharp P.A., Zhang F.. In vivo genome editing using Staphylococcus aureus Cas9. Nature, 2015, 520: 186-191 CrossRef PubMed ADS Google Scholar

[69] Raya A., Rodríguez-Pizà I., Guenechea G., Vassena R., Navarro S., Barrero M.J., Consiglio A., Castellà M., Río P., Sleep E., González F., Tiscornia G., Garreta E., Aasen T., Veiga A., Verma I.M., Surrallés J., Bueren J., Izpisúa Belmonte J.C.. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature, 2009, 460: 53-59 CrossRef PubMed ADS Google Scholar

[70] Robinton D.A., Daley G.Q.. The promise of induced pluripotent stem cells in research and therapy. Nature, 2012, 481: 295-305 CrossRef PubMed ADS Google Scholar

[71] Savić N., Schwank G.. Advances in therapeutic CRISPR/Cas9 genome editing. Transl Res, 2016, 168: 15-21 CrossRef PubMed Google Scholar

[72] Schwank G., Koo B.K., Sasselli V., Dekkers J.F., Heo I., Demircan T., Sasaki N., Boymans S., Cuppen E., van der Ent C.K., Nieuwenhuis E.E.S., Beekman J.M., Clevers H.. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell, 2013, 13: 653-658 CrossRef PubMed Google Scholar

[73] Sebestyén M.G., Budker V.G., Budker T., Subbotin V.M., Zhang G., Monahan S.D., Lewis D.L., Wong S.C., Hagstrom J.E., Wolff J.A.. Mechanism of plasmid delivery by hydrodynamic tail vein injection. I. Hepatocyte uptake of various molecules. J Gene Med, 2006, 8: 852-873 CrossRef PubMed Google Scholar

[74] Sharpless N.E., Depinho R.A.. The mighty mouse: genetically engineered mouse models in cancer drug development. Nat Rev Drug Discov, 2006, 5: 741-754 CrossRef PubMed Google Scholar

[75] Shinmyo Y., Tanaka S., Tsunoda S., Hosomichi K., Tajima A., Kawasaki H.. CRISPR/Cas9-mediated gene knockout in the mouse brain using in utero electroporation. Sci Rep, 2016, 6: 20611 CrossRef PubMed ADS Google Scholar

[76] Smith K.R.. Gene therapy: the potential applicability of gene transfer technology to the human germline. Int J Med Sci, 2004, 1: 76-91 CrossRef Google Scholar

[77] Song B., Fan Y., He W., Zhu D., Niu X., Wang D., Ou Z., Luo M., Sun X.. Improved hematopoietic differentiation efficiency of gene-corrected beta-thalassemia induced pluripotent stem cells by CRISPR/Cas9 system. Stem Cells Dev, 2015, 24: 1053-1065 CrossRef PubMed Google Scholar

[78] Suda T., Liu D.. Hydrodynamic gene delivery: its principles and applications. Mol Ther, 2007, 15: 2063-2069 CrossRef PubMed Google Scholar

[79] Swiech L., Heidenreich M., Banerjee A., Habib N., Li Y., Trombetta J., Sur M., Zhang F.. In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat Biotechnol, 2015, 33: 102-106 CrossRef PubMed Google Scholar

[80] Takahashi K., Yamanaka S.. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 2006, 126: 663-676 CrossRef PubMed Google Scholar

[81] Trounson A., DeWitt N.D.. Pluripotent stem cells progressing to the clinic. Nat Rev Mol Cell Biol, 2016, 17: 194-200 CrossRef PubMed Google Scholar

[82] Veltman J.A., Brunner H.G.. De novo mutations in human genetic disease. Nat Rev Genet, 2012, 13: 565-575 CrossRef PubMed Google Scholar

[83] Wang H., Yang H., Shivalila C.S., Dawlaty M.M., Cheng A.W., Zhang F., Jaenisch R.. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell, 2013, 153: 910-918 CrossRef PubMed Google Scholar

[84] Weiner A., Zauberman N., Minsky A.. Recombinational DNA repair in a cellular context: a search for the homology search. Nat Rev Micro, 2009, 7: 748-755 CrossRef PubMed Google Scholar

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

[86] Xie F., Ye L., Chang J.C., Beyer A.I., Wang J., Muench M.O., Kan Y.W.. Seamless gene correction of β-thalassemia mutations in patient-specific iPSCs using CRISPR/Cas9 and piggyBac. Genome Res, 2014, 24: 1526-1533 CrossRef PubMed Google Scholar

[87] Xu L., Park K.H., Zhao L., Xu J., El Refaey M., Gao Y., Zhu H., Ma J., Han R.. CRISPR-mediated genome editing restores dystrophin expression and function in mdx mice. Mol Ther, 2016, 24: 564-569 CrossRef PubMed Google Scholar

[88] Yang H., Wang H., Shivalila C.S., Cheng A.W., Shi L., Jaenisch R.. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell, 2013, 154: 1370-1379 CrossRef PubMed Google Scholar

[89] Yang Y., Wang L., Bell P., McMenamin D., He Z., White J., Yu H., Xu C., Morizono H., Musunuru K., Batshaw M.L., Wilson J.M.. A dual AAV system enables the Cas9-mediated correction of a metabolic liver disease in newborn mice. Nat Biotechnol, 2016a, 34: 334-338 CrossRef PubMed Google Scholar

[90] Yang Y., Zhang X., Yi L., Hou Z., Chen J., Kou X., Zhao Y., Wang H., Sun X.F., Jiang C., Wang Y., Gao S.. Naïve induced pluripotent stem cells generated from β-thalassemia fibroblasts allow efficient gene correction with CRISPR/Cas9. Stem Cell Transl Med, 2016b, 5: 8-19 CrossRef PubMed Google Scholar

[91] Yin H., Xue W., Chen S., Bogorad R.L., Benedetti E., Grompe M., Koteliansky V., Sharp P.A., Jacks T., Anderson D.G.. Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat Biotechnol, 2014, 32: 551-553 CrossRef PubMed Google Scholar

[92] Yoshimi K., Kaneko T., Voigt B., Mashimo T.. Allele-specific genome editing and correction of disease-associated phenotypes in rats using the CRISPR-Cas platform. Nat Commun, 2014, 5: 4240 CrossRef PubMed ADS Google Scholar

[93] Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., Nie J., Jonsdottir G.A., Ruotti V., Stewart R., Slukvin I.I., Thomson J.A.. Induced pluripotent stem cell lines derived from human somatic cells. Science, 2007, 318: 1917-1920 CrossRef PubMed ADS Google Scholar

[94] Yu Z., Ren M., Wang Z., Zhang B., Rong Y.S., Jiao R., Gao G.. Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila. Genets, 2013, 195: 289-291 CrossRef PubMed Google Scholar

[95] Zhang D., Li J.F.. DNA-guided genome editing tool. Sci China Life Sci, 2016, 59: 740-741 CrossRef PubMed Google Scholar

[96] Zhang D., Li Z., Yan B., Li J.F.. A novel RNA-guided RNA-targeting CRISPR tool. Sci China Life Sci, 2016, 59: 854-856 CrossRef PubMed Google Scholar

[97] Zhang X., Wang S.. From the first human gene-editing to the birth of three-parent baby. Sci China Life Sci, 2016, 59: 1341-1342 CrossRef PubMed Google Scholar

[98] Zincarelli C., Soltys S., Rengo G., Rabinowitz J.E.. Analysis of AAV serotypes 1–9 mediated gene expression and tropism in mice after systemic injection. Mol Ther, 2008, 16: 1073-1080 CrossRef PubMed Google Scholar

Copyright 2019 Science China Press Co., Ltd. 《中国科学》杂志社有限责任公司 版权所有

京ICP备18024590号-1