Applications of CRISPR/CAS9 Technology in Mice and Livestock Genome Editing: Current Research

Maj, Dorota; Górka, Klaudiusz

doi:10.2478/aoas-2024-0078

Abstract

Clustered regulatory interspaced short palindromic repeats/CRISPR-associated protein 9 (CRISPR/Cas9) technology is a novel and one of the most promising gene editing methods. Here we review the current research on the use of CRISPR/Cas9 technology to edit the genomes of mice, rabbits, pigs, sheep, goats, and cattle, as well as current obstacles and perspectives that may arise thanks to this technology. CRISPR/Cas9 has an advantage over other gene editing methods because of its simple design and the ease of modifying multiple target sites (multiplexing). This technology allows for the creation of in vitro and in vivo models of many diseases, which may contribute to the development of new drugs and effective therapies. CRISPR/Cas9 can also revolutionize the meat, dairy, leather, and fur industries by genetically modifying animals to obtain different products.

References

Bae S., Park J., Kim J.S. (2014). CAS-OFFinder: A fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases. Bioinformatics, 30: 1473–1475.
Search in Google Scholar Back to article
Bailly J., Del Rossi N., Runtz L., Li J.J., Park D.W., Scherrer G., Tanti A., Birling M.C., Darcq E., Kieffer B.L. (2020). Targeting morphine-responsive neurons: Generation of a knock-in mouse line expressing cre recombinase from the mu-opioid receptor gene locus. eNeuro, 7: ENEURO.0433-19.2020.
Search in Google Scholar Back to article
Barrangou R., Fremaux C., Deveau Hélène Richards M., Boyaval P., Moineau S., Romero D. A., Horvath P. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315: 1709–1712.
Search in Google Scholar Back to article
Beckermann T.M., Welch R.C., Williams F.M., Mortlock D.P., Sha F., Ikizler T.A., Woodard L.E., Wilson M.H. (2020). CRISPR/Cas9 engineering of albino cystinuria type A mice. Genesis, 58: e23357.
Search in Google Scholar Back to article
Bevacqua R.J., Fernandez-Martín R., Savy V., Canel N.G., Gismondi M.I., Kues W.A., Carlson D.F., Fahrenkrug S.C., Niemann H., Taboga O.A., Ferraris S., Salamone D.F. (2016). Efficient edition of the bovine PRNP prion gene in somatic cells and IVF embryos using the CRISPR/Cas9 system. Theriogenology, 86: 1886–1896.
Search in Google Scholar Back to article
Biswas P., Anand U., Ghorai M., Pandey D.K., Jha N.K., Behl T., Kumar M., Chauhan R., Shekhawat M.S., Dey A. (2022). Unraveling the promise and limitations of CRISPR/CAS system in natural product research: Approaches and challenges. Biotechnol. J., 17: 2100507.
Search in Google Scholar Back to article
Bowling S., Sritharan D., Osorio F.G., Nguyen M., Cheung P., Rodriguez-Fraticelli A., Patel S., Yuan W.C., Fujiwara Y., Li B.E., Orkin S.H., Hormoz S., Camargo F.D. (2020). An engineered CRISPRCas9 mouse line for simultaneous readout of lineage histories and gene expression profiles in single cells. Cell, 181: 1410–1422.
Search in Google Scholar Back to article
Burkard C., Opriessnig T., Mileham A.J., Stadejek T., Ait-Ali T., Lillico S.G., Whitelaw C.B., Archibald A.L. (2018). Pigs lacking the scavenger receptor cysteine-rich domain 5 of CD163 are resistant to porcine reproductive and respiratory syndrome virus 1 infection. J. Virol., 92: 00415–18.
Search in Google Scholar Back to article
Cancellieri S., Canver M.C., Bombieri N., Giugno R., Pinello L. (2019). CRISPRitz: rapid, high-throughput and variant-aware in silico off-target site identification for CRISPR genome editing. Bioinformatics, 36: 2001–2008.
Search in Google Scholar Back to article
Chen B., Gilbert L.A., Cimini B.A., Schnitzbauer J., Zhang W., Li G.W., Park, J., Blackburn E.H., Weissman J.S., Qi L.S., Huang B. (2013). Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell, 155: 1479–1491.
Search in Google Scholar Back to article
Chen J., Wang, H., Bai J., Liu W., Liu X., Yu D., Feng T., Sun Z., Zhang L., Ma L., Hu Y., Zou Y., Tan T., Zhong J., Hu M., Bai X., Pan D., Xing Y., Zhao Y., Tian K., Hu X., Li N. (2019). Generation of pigs resistant to highly pathogenic-porcine reproductive and respiratory syndrome virus through gene editing of CD163. Int. J. Biol. Sci., 15: 481–492.
Search in Google Scholar Back to article
Chen J., An B., Yu B., Peng X., Yuan H., Yang Q., Chen X., Yu T., Wang L., Zhang X., Wang H., Zou X., Pang D., Ouyang H., Tang X. (2020). CRISPR/Cas9-mediated knockin of human factor IX into swine factor IX locus effectively alleviates bleeding in hemophilia B pigs. Haematologica, 106: 829–837.
Search in Google Scholar Back to article
Chen P.R., Rowland R.R.R., Stoian A.M., Petrovan V., Sheahan M., Ganta C., Cino-Ozuna G., Kim D.Y., Dunleavey J.M., Whitworth K.M., Samuel M.S. (2022). Disruption of anthrax toxin receptor 1 in pigs leads to a rare disease phenotype and protection from senecavirus A infection. Sci. Rep., 12: 5009.
Search in Google Scholar Back to article
Cho B., Kim S.J., Lee E.J., Ahn S.M., Lee J.S., Ji D.Y., Lee K., Kang J.T. (2018). Generation of insulin-deficient piglets by disrupting INS gene using CRISPR/Cas9 system. Transgenic. Res., 27: 289–300.
Search in Google Scholar Back to article
Czarnek M., Bereta J. (2016). The CRISPR-cas system – from bacterial immunity to genome engineering. Postep. Hig. Med. Dosw., 70: 901–916.
Search in Google Scholar Back to article
Dave J., Raad N., Mittal N., Zhang L., Fargnoli A., Oh J.G., Savoia M.E., Hansen J., Fava M., Yin X., Theofilatos K. (2022). Gene editing reverses arrhythmia susceptibility in humanized PLN-R14del mice: modelling a European cardiomyopathy with global impact. Cardiovasc. Res., 118: 3140–50.
Search in Google Scholar Back to article
Ding Q., Strong A., Patel K.M., Ng S.L., Gosis B.S., Regan S.N., Cowan C.A., Rader D.J., Musunuru K. (2014). Permanent alteration of PCSK9 with in vivo CRISPR-Cas9 genome editing. Circ. Res.,115: 488–492.
Search in Google Scholar Back to article
Fan Z., Perisse I.V., Cotton C.U., Regouski M., Meng Q., Domb C., Van Wettere A.J., Wang Z., Harris A., White K.L., Polejaeva I.A. (2018). A sheep model of cystic fibrosis generated by CRISPR/ Cas9 disruption of the CFTR gene. JCI Insight, 3: e123529.
Search in Google Scholar Back to article
Fischer K., Rieblinger B., Hein R., Sfriso R., Zuber J., Fischer A., Klinger B., Liang W., Flisikowski K., Kurome M., Zakhartchenko V., Kessler B., Wolf E., Rieben R., Schwinzer R., Kind A., Schnieke A. (2019). Viable pigs after simultaneous inactivation of porcine MHC class I and three xenoreactive antigen genes GGTA1, CMAH and B4GALNT2. Xenotransplantation, 27: e12560.
Search in Google Scholar Back to article
Fu Y., Foden J.A., Khayter C., Maeder M.L., Reyon D., Joung J.K., Sander J.D. (2013). High-frequency off-target mutagenesis induced by CRISPR-cas nucleases in human cells. Nat. Biotechnol., 31: 822–826.
Search in Google Scholar Back to article
Gaj T, Ojala D.S, Ekman F.K, Byrne L.C, Limsirichai P, Schaffer D.V. (2017). In vivo genome editing improves motor function and extends survival in a mouse model of ALS. Sci. Adv. 3: eaar3952.
Search in Google Scholar Back to article
Gao Y., Wu H., Wang Y., Liu X., Chen L., Li Q., Cui C., Liu X., Zhang J., Zhang Y. (2017). Single Cas9 nickase induced generation of NRAMP1 knockin cattle with reduced off-target effects. Genome Biol., 18: 13.
Search in Google Scholar Back to article
Gilbert L.A., Larson M.H., Morsut L., Liu Z., Brar G.A., Torres S.E., Stern-Ginossar N., Brandman O., Whitehead E.H., Doudna J.A., Lim W.A. (2013). CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 154: 442–451.
Search in Google Scholar Back to article
Gim G.M., Eom K.H., Kwon D.H., Jung D.J., Kim D.H., Yi J.K., Ha J.J., Lee J.H., Lee S.B., Son W.J., Yum S.Y., Lee W.W., Jang G. (2023). Generation of double knockout cattle via CRISPR-Cas9 ribonucleoprotein (RNP) electroporation. J. Anim. Sci. Biotechnol., 14: 103.
Search in Google Scholar Back to article
Guo C., Wang M., Zhu Z., He S., Liu H., Liu X., Shi X., Tang T., Yu P., Zeng J., Yang L., Cao Y., Chen Y., Liu X., He Z. (2019). Highly efficient generation of pigs harboring a partial deletion of the CD163 SRCR5 domain, which are fully resistant to porcine reproductive and respiratory syndrome virus 2 infection. Front. Immunol., 10: 2019.01846.
Search in Google Scholar Back to article
Hai T., Teng F., Guo R., Li W., Zhou Q. (2014). One-step generation of knockout pigs by zygote injection of CRISPR/Cas System. Cell Res., 24: 372–375.
Search in Google Scholar Back to article
Hall B., Cho A., Limaye A., Cho K., Khillan J., Kulkarni A.B. (2018). Genome editing in mice using CRISPR/Cas9 technology. Curr. Protoc. Cell Biol., 81: e57.
Search in Google Scholar Back to article
Han H., Ma Y., Wang T., Lian L., Tian X., Hu R., Deng S., Li K., Wang F., Li N., Liu G., Zhao Y., Lian Z. (2014). One-step generation of myostatin gene knockout sheep via the CRISPR/Cas9 system. Front. Agric. Sci. Eng., 1: 2.
Search in Google Scholar Back to article
Hao F., Yan W., Li X., Wang H., Wang Y., Hu X., Liu X., Liang H., Liu D. (2018). Generation of cashmere goats carrying an EDAR gene mutant using CRISPR-Cas9-mediated genome editing. Int. J. Biol. Sci., 14: 427–436.
Search in Google Scholar Back to article
Heo Y.T., Quan X., Xu Y.N., Baek S., Choi H., Kim N.H., Kim J. (2015). CRISPR/Cas9 nuclease-mediated gene knock-in in bovine-induced pluripotent cells. Stem Cells Dev., 24: 393–402.
Search in Google Scholar Back to article
Hryhorowicz M., Lipiński D., Zeyland J., Słomski R. (2016). CRISPR/Cas9 immune system as a tool for genome engineering. Arch. Immunol. Ther. Exp., 65: 233–240.
Search in Google Scholar Back to article
Hu X., Hao F., Li X., Xun Z., Gao Y., Ren B., Cang M., Liang H., Liu D. (2021). Generation of VEGF knock-in Cashmere goat via the CRISPR/Cas9 system. Int. J. Biol. Sci., 17: 1026–1040.
Search in Google Scholar Back to article
Huang L., Luo J., Song N., Gao W., Zhu L., Yao W. (2022). CRISPR/ Cas9-mediated knockout of mir-130b affects mono- and polyun-saturated fatty acid content via PPARG-PGC1α axis in goat mam-mary epithelial cells. Int. J. Mol. Sci., 23: 3640.
Search in Google Scholar Back to article
Ikeda M., Matsuyama S., Akagi S., Ohkoshi K., Nakamura S., Minabe S., Kimura K., Hosoe M. (2017). Correction of a disease mutation using CRISPR/Cas9-assisted genome editing in Japanese Black cattle. Sci. Rep., 7: 1470.
Search in Google Scholar Back to article
Ishii T. (2017). Genome-edited livestock: Ethics and social acceptance. Anim. Front., 7: 24–32.
Search in Google Scholar Back to article
Islam M.A., Rony S.A,, Rahman M.B., Cinar M.U., Villena J., Uddin M.J., Kitazawa H. (2020). Improvement of disease resistance in livestock: Application of immunogenomics and CRISPR/Cas9 technology. Animals, 10: 2236.
Search in Google Scholar Back to article
Jacquin A.L., Odom D.T., Lukk M. (2019). Crisflash: Open-source software to generate CRISPR guide RNAS against genomes annotated with individual variation. Bioinformatics, 35: 3146–3147.
Search in Google Scholar Back to article
Jiang W., Bikard D., Cox D., Zhang F., Marraffini L.A. (2013). RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol., 31: 233–239.
Search in Google Scholar Back to article
Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpen-tier E. (2012). A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science, 337: 816–821. Jivanji S., Harland C., Cole S., Brophy B, Garrick D., Snell R., Littlejohn M., Laible G. (2021). The genomes of precision edited cloned calves show no evidence for off-target events or increased de novo mutagenesis. BMC Genom., 22: 457.
Search in Google Scholar Back to article
Kalds P., Zhou S., Cai B., Liu J., Wang Y., Petersen B., Sonstegard T., Wang X., Chen Y. (2019). Sheep and goat genome engineering: From random transgenesis to the CRISPR era. Front. Genet., 10: 2019.00750.
Search in Google Scholar Back to article
Kalds P., Gao Y., Zhou S., Cai B., Huang X., Wang X., Chen Y. (2020). Redesigning small ruminant genomes with CRISPR toolkit: Overview and perspectives. Theriogenology, 147: 25–33.
Search in Google Scholar Back to article
Khadempar S., Familghadakchi S., Motlagh R.A., Farahani N., Dashtiahangar M., Rezaei H., Gheibi Hayat S.M. (2019). CRISPR–Cas9 in genome editing: Its function and medical applications. J. Cell. Physiol., 234: 5751–5761.
Search in Google Scholar Back to article
Kim D.E., Lee J.H., Ji K.B., Park K.S., Kil T.Y., Koo O., Kim M.K. (2022). Generation of genome-edited dogs by somatic cell nuclear transfer. BMC Biotechnol., 22: 19.
Search in Google Scholar Back to article
Kim E.C., Zhang J., Tang A.Y., Bolton E.C., Rhodes J.S., Christian-Hinman C.A., Chung H.J. (2021). Spontaneous seizure and memory loss in mice expressing an epileptic encephalopathy variant in the calmodulin-binding domain of K_v7.2. P. Natl A. Sci., 118: e2021265118.
Search in Google Scholar Back to article
Kim H., Kim J.S. (2014). A guide to genome engineering with programmable nucleases. Nat. Rev. Genet., 15: 321–334.
Search in Google Scholar Back to article
Koonin E.V., Makarova K.S., Zhang F. (2017). Diversity, classification and evolution of CRISPR-Cas systems. Curr. Opin. Microbiol., 37: 67–78.
Search in Google Scholar Back to article
Laible G., Cole S.A., Brophy B.J., Wei J., Leath S., Jivanji S., Littlejohn M.D., Wells D.N. (2021). Holstein Friesian dairy cattle edited for diluted coat color as a potential adaptation to climate change. BMC Genom., 22: 856.
Search in Google Scholar Back to article
Ledford H., Callaway E. (2020). Pioneers of revolutionary CRISPR gene editing win Chemistry Nobel. Nature, 586: 346–347.
Search in Google Scholar Back to article
Lee B., Lee K., Panda S., Gonzales-Rojas R., Chong A., Bugay V., Park H. M., Brenner R., Murthy N., Lee H. Y. (2018). Nanoparticle delivery of CRISPR into the brain rescues a mouse model of fragile X syndrome from exaggerated repetitive behaviours. Nat. Biomed. Eng., 2: 497–507.
Search in Google Scholar Back to article
Li G., Zhang X., Wang H., Mo J., Zhong C., Shi J., Zhou R., Li Z., Yang H., Wu Z., Liu D. (2020). CRISPR/Cas9-mediated integration of large transgene into pig CEP112 locus. G3-Genes Genom. Genet., 10: 467–473.
Search in Google Scholar Back to article
Li H., Li, Z., Xiao N., Su X., Zhao S., Zhang Y., Cui K., Liu Q., Shi D. (2019 a). Site-specific integration of rotavirus VP6 gene in rabbit β-casein locus by CRISPR/Cas9 system. In Vitro Cell. Dev. Biol. Anim., 55: 586–597.
Search in Google Scholar Back to article
Li X., Hao F., Hu X., Wang H., Dai B., Wang X., Liang H., Cang M., Liu D. (2019 b). Generation of TΒ4 knock-in Cashmere goat using CRISPR/Cas9. Int. J. Biol. Sci., 15: 1743–1754.
Search in Google Scholar Back to article
Listgarten J., Weinstein M., Kleinstiver B.P., Sousa A.A., Joung J.K., Crawford J., Gao K., Hoang L., Elibol M., Doench J.G., Fusi N. (2018). Prediction of off-target activities for the end-to-end design of CRISPR guide RNAs. Nat. Biomed. Eng., 2: 38–47.
Search in Google Scholar Back to article
Liu Z., Dong H., Cui Y., Cong L., Zhang D. (2020). Application of different types of CRISPR/Cas-based systems in bacteria. Microb. Cell Factories, 19: 172.
Search in Google Scholar Back to article
Ma T., Tao J., Yang M., He C., Tian X., Zhang X., Zhang J., Deng S., Feng J., Zhang Z., Wang J., Ji P., Song Y., He P., Han H., Fu J., Lian Z., Liu G. (2017). An AANAT/ASMT transgenic animal model constructed with CRISPR/Cas9 system serving as the mammary gland bioreactor to produce melatonin-enriched milk in sheep. J. Pineal Res., 63: 12406.
Search in Google Scholar Back to article
Ma Y., Zhang L., Huang X. (2014). Genome modification by CRISPR/ Cas9. FEBS J., 281: 5186–5193.
Search in Google Scholar Back to article
Martin F., Sánchez-Hernández S., Gutiérrez-Guerrero A., Pinedo-Gomez J., Benabdellah K. (2016). Biased and unbiased methods for the detection of off-target cleavage by CRISPR/Cas9: An overview. Int. J. Mol. Sci., 17: 1507.
Search in Google Scholar Back to article
McKenna A., Shendure J. (2018). FlashFry: A fast and flexible tool for large-scale CRISPR target design. BMC Biol., 16: 74. Menchaca A., dos Santos-Neto P.C., Souza-Neves M., Cuadro F., Mulet A.P., Tesson L., Chenouard V., Guiffès A., Heslan J.M., Gantier M., Anegón I., Crispo M. (2020). Otoferlin gene editing in sheep via CRISPR-assisted SSODN-mediated homology directed repair. Sci. Rep., 10: 5995.
Search in Google Scholar Back to article
Naeem M., Majeed S., Hoque M.Z., Ahmad I. (2020). Latest developed strategies to minimize the off-target effects in CRISPR-cas-mediated genome editing. Cells, 9: 1608.
Search in Google Scholar Back to article
Nelson C.E., Hakim C.C., Ousterout D.G., Thakore P.I., Moreb E.A., Ruth M., Rivera R.M., Madhavan S., Pan X.F., Ran A., Gersbach C.A. (2016). In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science, 351: 403–407.
Search in Google Scholar Back to article
Nguyen X.X., Sanderson M., Helke K., Feghali-Bostwick C. (2021). Phenotypic characterization of transgenic mice expressing human IGFBP-5. Int. J. Mol. Sci., 22: 335.
Search in Google Scholar Back to article
Ni W., Qiao J., Hu S., Zhao X., Regouski M., Yang M., Polejaeva I.A., Chen C. (2014). Efficient gene knockout in goats using CRISPR/ Cas9 system. PLoS ONE, 9: 0106718.
Search in Google Scholar Back to article
Nidhi S., Anand U., Oleksak P., Tripathi P., Lal J.A., Thomas G., Kuca K., Tripathi V. (2021). Novel CRISPR–Cas systems: An updated review of the current achievements, applications, and future research perspectives. Int. J. Mol. Sci., 22: 3327.
Search in Google Scholar Back to article
Nishimasu H., Ran F.A., Hsu P.D., Konermann S., Shehata S.I., Dohmae N., Ishitani R., Zhang F., Nureki O. (2014). Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell, 156: 935–949.
Search in Google Scholar Back to article
Niu D., Wei H.J., Lin L., George H., Wang T., Lee I.H., Zhao H.Y., Wang Y., Kan Y., Shrock E., Lesha E., Wang G., Luo Y., Qing Y., Jiao D., Zhao H., Zhou X., Wang S., Wei H., Güell M., Church G.M., Yang L. (2017). Inactivation of porcine endogenous retrovirus in pigs using CRISPR-Cas9. Science, 357: 1303–1307.
Search in Google Scholar Back to article
Pan X., Philippen L., Lahiri S.K., Lee C., Park S.H., Word T.A., Li N., Jarrett K.E., Gupta R., Reynolds J.O., Lin J. (2018). In vivo Ryr2 editing corrects catecholaminergic polymorphic ventricular tachycardia. Circ. Res., 123: 953–963.
Search in Google Scholar Back to article
Park H., Kim J. (2022). Activation of melatonin receptor 1 by crispr-Cas9 activator ameliorates cognitive deficits in an Alzheimer’s disease mouse model. J. Pineal Res., 72: e12787.
Search in Google Scholar Back to article
Park K.E., Kaucher A.V., Powell A., Waqas M.S., Sandmaier S.E., Oatley M.J., Park C.H., Tibary A., Donovan D.M., Blomberg L.A., Lillico S.G., Whitelaw C.B., Mileham A., Telugu B.P., Oatley J.M. (2017). Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene Sci. Rep., 7: 40176.
Search in Google Scholar Back to article
Popova J., Bets V., Kozhevnikova E. (2023). Perspectives in genome-editing techniques for livestock. Animals, 13: 2580.
Search in Google Scholar Back to article
Ren J., Yu D., Fu R., An P., Sun R., Wang Z., Guo R., Li H., Zhang Y., Li Z., Yang Y. G., Li W., Hai T., Hu Z. (2020). IL2RG-deficient minipigs generated via CRISPR/Cas9 technology support the growth of human melanoma-derived tumours. Cell Prolif., 53: e12863.
Search in Google Scholar Back to article
Rieblinger B., Sid S., Duda D., Bozoglu T., Klinger R., Schlickenrieder A., Lengyel K., Flisikowski K., Flisikowska T, Simm N., Grodziecki A., Perleberg C., Bähr A., Carrier L., Kurome M., Zakhartchenko V., Kessler B., Wolf E., Kettler L., Luksch H., Hagag I.T., Wise D., Kaufman J., Kaufer B.B., Kupatt C., Schnieke A., Schusser B. (2021). Cas9-expressing chickens and pigs as resources for genome editing in livestock. PNAS, 118: e2022562118.
Search in Google Scholar Back to article
Romanowska K., Ostapowicz J., Golusiński W. (2022). Application of CRISPR/Cas9 technology in cancer treatment. Lett. Oncol. Sci., 18: 92–98.
Search in Google Scholar Back to article
Rutten M.G.S., Derks T.G.J., Huijkman N.C.A., Bos T., Kloosterhuis N.J., van de Kolk Kees C.W.A., Wolters J.C., Koster M.H., Bongiovanni L., Thomas R.E., de Bruin A., van de Sluis B., Oosterveer M.H. (2021). Modeling phenotypic heterogeneity of glycogen storage disease type 1a liver disease in mice by somatic CRISPR/CRISPR-associated protein 9–mediated gene editing. Hepatology, 74: 2491–2507.
Search in Google Scholar Back to article
Schmid-Burgk J.L., Höning K., Thomas S., Ebert T.S., Hornung V. (2016). CRISPaint allows modular base-specific gene tagging using a ligase-4-dependent mechanism. Nat. Commun., 7: 12338.
Search in Google Scholar Back to article
Schultz-Bergin M. (2018). Is CRISPR an ethical game changer? J. Agric. Environ. Ethics, 31: 219–238.
Search in Google Scholar Back to article
Shan Q., Wang Y., Li, J., Zhang Y., Chen K., Liang Z., Zhang K., Liu J., Xi J.J., Qiu J.L., Gao C. (2013). Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol., 31: 686–688.
Search in Google Scholar Back to article
Shen B., Zhang J., Wu H., Wang J., Ma K., Li Z., Zhang X., Zhang P., Huang X. (2013). Generation of gene-modified mice via Cas9/ RNA-mediated gene targeting. Cell Res., 23: 720–723.
Search in Google Scholar Back to article
Skrzyszowska M., Samiec M. (2021). Generating cloned goats by somatic cell nuclear transfer – molecular determinants and application to transgenics and biomedicine. Int. J. Mol. Sci., 22: 7490.
Search in Google Scholar Back to article
Song J., Zhang J., Xu J., Garcia-Barrio M., Chen Y.E., Yang D. (2021). Genome engineering technologies in rabbits. J. Biomed. Res., 35: 135–147.
Search in Google Scholar Back to article
Song Y., Xu Y., Liang M., Zhang Y., Chen M., Deng J., Li Z. (2018). CRISPR/Cas9-mediated mosaic mutation of SRY gene induces hermaphroditism in rabbits. Biosci. Rep., 38: BSR20171490.
Search in Google Scholar Back to article
Stemmer M., Thumberger T., del Sol Keyer M., Wittbrodt J., Mateo J.L. (2015). CCTop: An intuitive, flexible and reliable CRISPR/ Cas9 target prediction tool. PLoS One, 10: e0176619.
Search in Google Scholar Back to article
Sui T., Yuan L., Liu H., Chen M., Deng J., Wang Y., Li Z., Lai L. (2016). CRISPR/Cas9-mediated mutation of PHEX in rabbit recapitulates human X-linked hypophosphatemia (XLH). Hum. Mol. Genet., 25: 2661–2671
Search in Google Scholar Back to article
Sui T., Lau Y. S., Liu D., Liu T., Xu L., Gao Y., Lai L., Li Z., Han R. (2018 a). A novel rabbit model of Duchenne muscular dystrophy generated by CRISPR/Cas9. Dise. Model. Mech., 11: dmm032201.
Search in Google Scholar Back to article
Sui T., Xu L., Lau Y. S., Liu D., Liu T., Gao Y., Lai L., Han R., Li Z. (2018 b). Development of muscular dystrophy in a CRISPR-engineered mutant rabbit model with frame-disrupting ANO5 mutations. Cell Death Dis., 9: 609.
Search in Google Scholar Back to article
Sui T., Liu D., Liu T., Deng J., Chen M., Xu Y., Song Y., Ouyang H., Lai L., Li Z. (2019). LMNA-mutated rabbits: A model of premature aging syndrome with muscular dystrophy and dilated cardiomyopathy. Aging Dis., 10: 102.
Search in Google Scholar Back to article
Tanihara F., Hirata M., Thi Nguyen N., Anh Le Q., Hirano T., Otoi T. (2020). Generation of viable PDX1 gene-edited founder pigs as providers of nonmosaics. Mol. Reprod. Dev., 87: 471–481.
Search in Google Scholar Back to article
Tian H., Niu H., Luo J., Yao W., Chen X., Wu J., Geng Y., Gao W., Lei A., Gao Z., Tian X., Zhao X., Shi H., Li C., Hua J. (2022). Knockout of stearoyl-COA desaturase 1 decreased milk fat and unsaturated fatty acid contents of the GOAT model generated by CRISPR/Cas9. J. Agric. Food Chem., 70: 4030–4043.
Search in Google Scholar Back to article
Tiruneh G., Medhin M., Chekol Abebe E., Sisay T., Berhane N., Bekele T., Asmamaw Dejenie T. (2021). Current applications and future perspectives of CRISPR-Cas9 for the treatment of lung cancer. Biologics, 15: 199–204.
Search in Google Scholar Back to article
Vera L. N., Schuh R.S., Fachel F.N., Poletto E., Piovesan E., Kubaski F., Couto E., Brum B., Rodrigues G., Souza H., Giugliani R., Matte U., Baldo G., Teixeira H.F. (2022). Brain and visceral gene editing of mucopolysaccharidosis I mice by nasal delivery of the CRISPR/Cas9 system. J. Gene Med., 24: e3410.
Search in Google Scholar Back to article
Vilarino M., Rashid S.T., Suchy F.P., McNabb B.R., van der Meulen T., Fine E.J., Ahsan S.D., Mursaliyev N., Sebastiano V., Diab S.S., Huising M.O., Nakauchi H., Ross P.J. (2017). CRISPR/Cas9 microinjection in oocytes disables pancreas development in sheep. Sci. Rep., 7: 17472.
Search in Google Scholar Back to article
Wang H., Yang H., Shivalila C.S., Dawlaty M.M., Cheng A.W., 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.
Search in Google Scholar Back to article
Wang H., Shen L., Chen J., Liu X., Tan T., Hu Y., Bai X., Li Y., Tian K., Li N., Hu X. (2019). Deletion of CD163 exon 7 confers resistance to highly pathogenic porcine reproductive and respiratory viruses on pigs. Int. J. Biol. Sci., 15: 1993–2005.
Search in Google Scholar Back to article
Wang S.W., Gao C., Zheng Y.M., Yi L., Lu J.C., Huang X.Y., Cai J.B., Zhang P.F., Cui Y.H., Ke A.W. (2022). Current applications and future perspective of CRISPR/Cas9 gene editing in cancer. Mol. Cancer, 21: 57.
Search in Google Scholar Back to article
Wang X., Niu Y., Zhou J., Zhu H., Ma B., Yu H., Yan H., Hua J., Huang X., Qu L., Chen Y. (2018). CRISPR/Cas9-mediated MSTN disruption and heritable mutagenesis in goats causes increased body mass. Anim. Genet., 49: 43–51.
Search in Google Scholar Back to article
Whitworth K.M., Rowland R.R., Ewen C.L., Trible B.R., Kerrigan M.A., Cino-Ozuna A.G., Samuel M.S., Lightner J.E., McLaren D.G., Mileham A.J., Wells K.D., Prather R.S. (2016). Gene-edited pigs are protected from porcine reproductive and respiratory syndrome virus. Nat. Biotechnol., 34: 20–22.
Search in Google Scholar Back to article
Whitworth K.M., Rowland R.R., Petrovan V., Sheahan M., Cino-Ozuna A.G., Fang Y., Hesse R., Mileham A., Samuel M.S., Wells K.D., Prather R.S. (2019). Resistance to coronavirus infection in amino peptidase N-deficient pigs. Transgenic Res., 28: 21–32.
Search in Google Scholar Back to article
Williams B.O., Warman M.L. (2017). CRISPR/Cas9 technologies. J. Bone Miner. Res., 32: 883–888.
Search in Google Scholar Back to article
Williams D.K., Pinzón C., Huggins S., Pryor J.H., Falck A., Herman F., Oldeschulte J., Chavez M.B., Foster B.L., White S.H., Westhusin M.E., Suva L.J., Long C.R., Gaddy D. (2018). Genetic engineering a large animal model of human hypophosphatasia in sheep. Sci. Rep., 8: 16945.
Search in Google Scholar Back to article
Workman A.M., Heaton M.P., Vander Ley B.L., Webster D.A., Sherry L., Bostrom J.R., Larson S.,, Kalbfleisch T.S., Harhay G.P., Jobman E.E., Carlson D.F. (2023). First gene-edited calf with reduced susceptibility to a major viral pathogen. PNAS Nexus, 2: pgad125.
Search in Google Scholar Back to article
Wu Y., Zhang J., Peng B., Tian D., Zhang D., Li Y., Feng X., Liu J., Li J., Zhang T., Liu X. (2019). Generating viable mice with heritable embryonically lethal mutations using the CRISPR-Cas9 system in two-cell embryos. Nat. Commun., 10: 2883.
Search in Google Scholar Back to article
Xie C., Zhang Y.P., Song L., Luo J., Qi W., Hu J., Lu D., Yang Z., Zhang J., Xiao J., Zhou B. (2016). Genome editing with CRISPR/ Cas9 in postnatal mice corrects PRKAG2 cardiac syndrome. Cell Res., 26: 1099–111.
Search in Google Scholar Back to article
Xu K., Zhou Y., Mu Y., Liu Z., Hou S., Xiong Y., Fang L., Ge C., Wei Y., Zhang X., Xu C. (2020 a). CD163 and pAPN double-knockout pigs are resistant to PRRSV and TGEV and exhibit decreased susceptibility to PDCoV while maintaining normal production performance. Elife, 9: e57132.
Search in Google Scholar Back to article
Xu Y., Liu H., Pan H., Wang X., Zhang Y., Yao B., Li N., Lai L., Li Z. (2020 b). CRISPR/Cas9-mediated disruption of fibroblast growth factor 5 in rabbits results in a systemic long hair phenotype by prolonging anagen. Genes, 11: 297.
Search in Google Scholar Back to article
Yan S., Tu Z., Liu Z., Fan N., Yang H., Yang S., Yang W., Zhao Y., Ouyang Z., Lai C., Yang H., Li L., Liu Q., Shi H., Xu G., Zhao H., Wei H., Pei Z., Li S., Li X.J. (2018). A huntingtin knockin pig model recapitulates features of selective neurodegeneration in Huntington’s disease. Cell, 173: 989–1002.
Search in Google Scholar Back to article
Yang D., Xu J., Zhu T., Fan J., Lai L., Zhang J., Chen Y.E. (2014). Effective gene targeting in rabbits using RNA-guided Cas9 nucleases. J. Mol. Cell Biol., 6: 97–99.
Search in Google Scholar Back to article
Yang H., Zhang J., Zhang X., Shi J., Pan Y., Zhou R., Li G., Li Z., Cai G., Wu Z. (2018). CD163 knockout pigs are fully resistant to highly pathogenic porcine reproductive and respiratory syndrome virus. Antiviral Res., 151: 63–70.
Search in Google Scholar Back to article
You W., Li M., Qi Y., Wang Y., Chen Y., Liu Y., Li Y., Ouyang H., Pang P. (2021). CRISPR/Cas9-mediated specific integration of Fat-1 and IGF-1 at the pRosa26 locus. Genes (Basel), 12: 1027.
Search in Google Scholar Back to article
Yu W., Mookherjee S., Chaitankar V., Hiriyanna S., Kim J.W., Brooks M., Ataeijannati Y., Sun X., Dong L., Li T., Swaroop A. (2017). Nrl knockdown by AAV-delivered CRISPR/Cas9 prevents retinal degeneration in mice. Nat Commun., 8: 14716.
Search in Google Scholar Back to article
Yuan M., Zhang J., Gao Y., Yuan Z., Zhu Z., Wei Y., Wu T., Han J., Zhang Y. (2021). HMEJ-based safe-harbor genome editing enables efficient generation of cattle with increased resistance to tuberculosis. J. Biol. Chem., 296: 100497.
Search in Google Scholar Back to article
Yue Y., Xu W., Kan Y., Zhao H.-Y., Zhou Y., Song X., Wu J., Xiong J., Goswami D., Yang M., Lamriben L. (2021). Extensive germline genome engineering in pigs. Nat. Biomed. Eng., 5: 134–143. Zhang T., Li J. Z., Wang T., Zhao F., Sui T. (2021). No apparent p53 activation in CRISPR-engineered gene-edited rabbits. J. Cell. Mol. Med., 25: 10313–10317.
Search in Google Scholar Back to article
Zhang X., Li W., Liu C., Peng X., Lin J., He S., Li X., Han B., Zhang N., Wu Y., Chen L., Wang L., MaYila Huang J., Liu M. (2017). Alteration of sheep coat color pattern by disruption of ASIP gene via CRISPR Cas9. Sci. Rep., 7: 8149.
Search in Google Scholar Back to article
Zhang X.H., Tee L.Y., Wang X.G., Huang Q.S., Yang S.H. (2015). Off-target effects in CRISPR/Cas9-mediated genome engineering. Mol. Ther. Nucleic. Acids, 4: e264.
Search in Google Scholar Back to article
Zhang Y., Yang J., Yao H., Zhang Z., Song Y. (2022). CRISPR/Cas9-mediated deletion of Fam83h induces defective tooth mineralization and hair development in rabbits. J. Cell. Mol. Med., 26: 5670–5679.
Search in Google Scholar Back to article
Zhang Y., Bassel-Duby Y., Olson E.N. (2023). CRISPR-Cas9 correction of Duchenne muscular dystrophy in mice by a self-complementary AAV delivery system. Methods Mol. Biol., 2587: 411–425.
Search in Google Scholar Back to article
Zhao H., Li Y., He L., Pu W., Yu W., Li Y., Wu Y.T., Xu C., Wei Y., Ding Q., Song B.L., Huang H., Zhou B. (2020). In vivo Aav-CRISPR/Cas9–mediated gene editing ameliorates atherosclerosis in familial hypercholesterolemia. Circulation, 141: 67–79.
Search in Google Scholar Back to article
Zhao Y., Yang L., Su G., Wei Z., Liu X., Song L., Hai C., Wu D., Hao Z., Wu Y., Zhang L., Bai C., Li G. (2022). Growth traits and sperm proteomics analyses of myostatin gene-edited Chinese yellow cattle. Life, 12: 627.
Search in Google Scholar Back to article
Zheng Q., Lin J., Huang J., Zhang H., Zhang R., Zhang X., Cao C., Hambly C., Qin G., Yao J., Song R. (2017). Reconstitution of UCP1 using CRISPR/Cas9 in the white adipose tissue of pigs decreases fat deposition and improves thermogenic capacity. PNAS, 114: E9474–E9482.
Search in Google Scholar Back to article
Zhou J., Yan Q., Tang C., Liao Y., Zhang Q., Wang X., Zhou X., Lai L., Zou Q. (2020). Development of a rabbit model of Wiskott-Aldrich syndrome. FASEB J., 35: e22126.
Search in Google Scholar Back to article
Zhou W., Wan Y., Guo R., Deng M., Deng K., Wang Z., Zhang Y., Wang F. (2017). Generation of beta-lactoglobulin knock-out goats using CRISPR/Cas9. PLoS One, 12: 0186056.
Search in Google Scholar Back to article
Zhu X.X., Zhan Q.M., Wei Y.Y., Yan A.F., Feng J., Liu L., Lu S.S., Tang D.S. (2020). CRISPR/Cas9-mediated MSTN disruption accelerates the growth of Chinese Bama pigs. Reprod. Domest. Anim., 55: 1314–1327.
Search in Google Scholar Back to article
Zou Y., Li Z., Zou Y., Hao H., Li N., Li Q. (2018). An FBXO40 knockout generated by CRISPR/Cas9 causes muscle hypertrophy in pigs without detectable pathological effects Biochem. Biophys. Res. Commun., 498: 940–945.
Search in Google Scholar Back to article
Zuckermann M., Hovestadt V., Knobbe-Thomsen C.B., Zapatka M., Northcott P.A., Schramm K., Belic J., Jones D.T.W., Tschida B., Moriarity B., Largaespada D., Roussel M.F., Korshunov A., Reifenberger G., Pfister S.M., Lichter P., Kawauchi D., Gronych J. (2015). Somatic CRISPR/Cas9-mediated tumour suppressor disruption enables versatile brain tumour modeling. Nat Commun., 6: 7391.
Search in Google Scholar Back to article

Applications of CRISPR/CAS9 Technology in Mice and Livestock Genome Editing: Current Research

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