5.9
CiteScore
5.9
Impact Factor
Volume 48 Issue 5
May  2021
Turn off MathJax
Article Contents
Article Navigation >  Journal of Genetics and Genomics  > 2021  >  48(5): 347-360

The advancements, challenges, and future implications of the CRISPR/Cas9 system in swine research

doi: 10.1016/j.jgg.2021.03.015
  •  

    a Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education & Key Lab of Swine Genetics and Breeding of Ministry of Agriculture and Rural Affairs, Huazhong Agricultural University, Wuhan 430070, PR China;

  •  

    b Animal and Human Health Program, Biosciences, International Livestock Research Institute (ILRI), P.O. Box 30709, Nairobi 00100, Kenya;

  •  

    c Key Laboratory of Pig Molecular Quantitative Genetics of Anhui Academy of Agricultural Sciences, Livestock and Poultry Epidemic Diseases Research Center of Anhui Province, Anhui Provincial Key Laboratory of Livestock and Poultry Product Safety Engineering, Institute of Animal Husbandry and Veterinary Medicine, Anhui Academy of Agricultural Sciences, Hefei 230031, PR China;

  •  

    d The Cooperative Innovation Center for Sustainable Pig Production, Huazhong Agricultural University, Wuhan 430070, PR China;

  •  

    e Lingnan Guangdong Laboratory of Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518124, PR China

Funds:

This work was supported by the National Transgenic Project of China (2016ZX08006003-004 and 2018ZX08009-26B), the NSFC Major Research Plan-Major Scientific Problems of African Swine Fever virus (31941008), the Fundamental Research Funds for the Central Universities (2662018JC002), the IDRC Livestock Vaccine Innovation Fund (109212-001), the CGIAR Research Program on Livestock, and Natural Science Foundation of Anhui Province (2008085QC138).

  • Received Date: 2020-12-28
  • Revised Date: 2021-03-10
  • Accepted Date: 2021-03-13
  • Publish Date: 2021-05-20
    Abstract
  • Clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (CRISPR/Cas9) genome editing technology has dramatically influenced swine research by enabling the production of high-quality disease-resistant pig breeds, thus improving yields. In addition, CRISPR/Cas9 has been used extensively in pigs as one of the tools in biomedical research. In this review, we present the advancements of the CRISPR/Cas9 system in swine research, such as animal breeding, vaccine development, xenotransplantation, and disease modeling. We also highlight the current challenges and some potential applications of the CRISPR/Cas9 technologies.
    • FullText(HTML)
  • loading
    • References(163)
  • Aird, E.J., Lovendahl, K.N., St, M.A., Harris, R.S., Gordon, W.R., 2018. Increasing Cas9-mediated homology-directed repair efficiency through covalent tethering of DNA repair template. Commun. Biol. 1, 54.
    Berg, F., Gustafson, U., Andersson, L., 2006. The uncoupling protein 1 gene (UCP1) is disrupted in the pig lineage:a genetic explanation for poor thermoregulation in piglets. PLoS Genet. 2, e129.
    Bhaya, D., Davison, M., Barrangou, R., 2011. CRISPR-cas systems in bacteria and archaea:versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45, 273-297.
    Bi, Y., Hua, Z., Liu, X., Hua, W., Ren, H., Xiao, H., Zhang, L., Li, L., Wang, Z., Laible, G., et al., 2016. Isozygous and selectable marker-free MSTN knockout cloned pigs generated by the combined use of CRISPR/Cas9 and Cre/LoxP. Sci. Rep. 6, 31729.
    Borca, M.V., Holinka, L.G., Berggren, K.A., Gladue, D.P., 2018. CRISPR-Cas9, a tool to efficiently increase the development of recombinant African swine fever viruses. Sci. Rep. 8, 3154.
    Burkard, C., Opriessnig, T., Mileham, A.J., Stadejek, T., Ait-Ali, T., Lillico, S.G., Whitelaw, C., Archibald, A.L., 2018. Pigs lacking the scavenger receptor cysteinerich domain 5 of CD163 are resistant to porcine reproductive and respiratory syndrome virus 1 infection. J. Virol. 92, e00415-e00418.
    Butler, J.R., Martens, G.R., Estrada, J.L., Reyes, L.M., Ladowski, J.M., Galli, C., Perota, A., Cunningham, C.M., Tector, M., Joseph, T.A., 2016a. Silencing porcine genes significantly reduces human-anti-pig cytotoxicity profiles:an alternative to direct complement regulation. Transgenic Res. 25, 751-759.
    Butler, J.R., Wang, Z., Martens, G.R., Ladowski, J.M., Li, P., Tector, M., Tector, A.J., 2016b. Modified glycan models of pig-to-human xenotransplantation do not enhance the human-anti-pig T cell response. Transpl. Immunol. 35, 47-51.
    Calvert, J.G., Slade, D.E., Shields, S.L., Jolie, R., Mannan, R.M., Ankenbauer, R.G., Welch, S.K., 2007. CD163 expression confers susceptibility to porcine reproductive and respiratory syndrome viruses. J. Virol. 81, 7371-7379.
    Capecchi, M.R., 1989. Altering the genome by homologous recombination. Science 244, 1288-1292.
    Carey, K., Ryu, J., Uh, K., Lengi, A.J., Clark-Deener, S., Corl, B.A., Lee, K., 2019. Frequency of off-targeting in genome edited pigs produced via direct injection of the CRISPR/Cas9 system into developing embryos. BMC Biotechnol. 19, 25.
    Chattha, K.S., Roth, J.A., Saif, L.J., 2015. Strategies for design and application of enteric viral vaccines. Annu. Rev. Anim. Biosci. 3, 375-395.
    Chen, J., An, B., Yu, B., Peng, X., Yuan, H., Yang, Q., Chen, X., Yu, T., Wang, L., Zhang, X., et al., 2020a. CRISPR/Cas9-mediated knockin of human factor IX into swine factor IX locus effectively alleviates bleeding in hemophilia B pigs. Haematologica 106, 829-837.
    Chen, J., Wang, H., Bai, J., Liu, W., Liu, X., Yu, D., Feng, T., Sun, Z., Zhang, L., Ma, L., et al., 2019a. 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.
    Chen, K., Wang, Y., Zhang, R., Zhang, H., Gao, C., 2019b. CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu. Rev. Plant Biol. 70, 667-697.
    Chen, L., Magliano, D.J., Zimmet, P.Z., 2011. The worldwide epidemiology of type 2 diabetes mellitus-present and future perspectives. Nat. Rev. Endocrinol. 8, 228-236.
    Chen, W., Zhao, D., He, X., Liu, R., Wang, Z., Zhang, X., Li, F., Shan, D., Chen, H., Zhang, J., et al., 2020b. A seven-gene-deleted African swine fever virus is safe and effective as a live attenuated vaccine in pigs. Sci. China Life Sci. 63, 623-634.
    Chin, K.C., Cresswell, P., 2001. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc. Natl. Acad. Sci. U. S. A. 98, 15125-15130.
    Cho, B., Kim, S.J., Lee, E., Ahn, S.M., Lee, J.S., Ji, D., Lee, K., Kang, J., 2018. Generation of insulin-deficient piglets by disrupting INS gene using CRISPR/Cas9 system. Transgenic Res. 27, 289-300.
    Choe, Y.J., Jee, Y., Takashima, Y., Lee, J.K., 2020. Japanese encephalitis in the Western Pacific region:implication from the Republic of Korea. Vaccine 38, 2760-2763.
    Chojnacka-Puchta, L., Sawicka, D., 2020. CRISPR/Cas9 gene editing in a chicken model:current approaches and applications. J. Appl. Genet. 61, 221-229.
    Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A., et al., 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823.
    Cooper, C.A., Challagulla, A., Jenkins, K.A., Wise, T.G., O'Neil, T.E., Morris, K.R., Tizard, M.L., Doran, T.J., 2017. Generation of gene edited birds in one generation using sperm transfection assisted gene editing (STAGE). Transgenic Res. 26, 331-347.
    Cromwell, C.R., Sung, K., Park, J., Krysler, A.R., Jovel, J., Kim, S.K., Hubbard, B.P., 2018. Incorporation of bridged nucleic acids into CRISPR RNAs improves Cas9 endonuclease specificity. Nat. Commun. 9, 1448.
    Cwynar, P., Stojkov, J., Wlazlak, K., 2019. African swine fever status in Europe. Viruses 11, 310.
    Devaux, C.A., 2012. Emerging and re-emerging viruses:a global challenge illustrated by Chikungunya virus outbreaks. World J. Virol. 1, 11-22.
    Eichner, J.E., Dunn, S.T., Perveen, G., Thompson, D.M., Stewart, K.E., Stroehla, B.C., 2002. Apolipoprotein E polymorphism and cardiovascular disease:a HuGE review. Am. J. Epidemiol. 155, 487-495.
    Fang, B., Ren, X., Wang, Y., Li, Z., Zhao, L., Zhang, M., Li, C., Zhang, Z., Chen, L., Li, X., et al., 2018. Apolipoprotein E deficiency accelerates atherosclerosis development in miniature pigs. Dis. Model. Mech. 11, dmm036632.
    Fernbach, P.M., Light, N., Scott, S.E., Inbar, Y., Rozin, P., 2019. Extreme opponents of genetically modified foods know the least but think they know the most. Nat. Hum. Behav. 3, 251-256.
    Fischer, K., Kind, A., Schnieke, A., 2018. Assembling multiple xenoprotective transgenes in pigs. Xenotransplantation 25, e12431.
    Fischer, K., Rieblinger, B., Hein, R., Sfriso, R., Zuber, J., Fischer, A., Klinger, B., Liang, W., Flisikowski, K., Kurome, M., et al., 2020. Viable pigs after simultaneous inactivation of porcine MHC class I and three xenoreactive antigen genes GGTA1, CMAH and B4GALNT2. Xenotransplantation 27, e12560.
    Freije, C.A., Myhrvold, C., Boehm, C.K., Lin, A.E., Welch, N.L., Carter, A., Metsky, H.C., Luo, C.Y., Abudayyeh, O.O., Gootenberg, J.S., et al., 2019. Programmable inhibition and detection of RNA viruses using Cas13. Mol. Cell. 76, 826-837. e11.
    Fung, R.K., Kerridge, I.H., 2016. Gene editing advance re-ignites debate on the merits and risks of animal to human transplantation. Intern. Med. J. 46, 1017-1022.
    Gao, H., Zhao, C., Xiang, X., Li, Y., Zhao, Y., Li, Z., Pan, D., Dai, Y., Hara, H., Cooper, D.K., et al., 2017. Production of alpha1,3-galactosyltransferase and cytidine monophosphate-N-acetylneuraminic acid hydroxylase gene doubledeficient pigs by CRISPR/Cas9 and handmade cloning. J. Reprod. Dev. 63, 17-26.
    Gao, M., Zhang, B., He, Y., Yang, Q., Deng, L., Zhu, Y., Lai, E., Wang, M., Wang, L., Yang, G., et al., 2019. Efficient generation of an Fah/Rag2 dual-gene knockout porcine cell line using CRISPR/Cas9 and adenovirus. DNA Cell Biol. 38, 314-321.
    Garas, L.C., Murray, J.D., Maga, E.A., 2015. Genetically engineered livestock:ethical use for food and medical models. Annu. Rev. Anim. Biosci. 3, 559-575.
    Golovan, S.P., Meidinger, R.G., Ajakaiye, A., Cottrill, M., Wiederkehr, M.Z., Barney, D.J., Plante, C., Pollard, J.W., Fan, M.Z., Hayes, M.A., et al., 2001. Pigs expressing salivary phytase produce low-phosphorus manure. Nat. Biotechnol. 19, 741-745.
    Guo, C., Wang, M., Zhu, Z., He, S., Liu, H., Liu, X., Shi, X., Tang, T., Yu, P., Zeng, J., et al., 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, 1846.
    Hackett, P.B., 2020. Regulatory issues for genetically modified animals. Front. Agr. Sci. Eng. 7, 188.
    Hai, T., Guo, W., Yao, J., Cao, C., Luo, A., Qi, M., Wang, X., Wang, X., Huang, J., Zhang, Y., et al., 2017. Creation of miniature pig model of human Waardenburg syndrome type 2A by ENU mutagenesis. Hum. Genet. 136, 1463-1475.
    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.
    Han, H.A., Pang, J.K.S., Soh, B., 2020. Mitigating off-target effects in CRISPR/Cas9-mediated in vivo gene editing. J. Mol. Med. 98, 615-632.
    He, Z., Shi, X., Du, B., Qin, Y., Cong, P., Chen, Y., 2015. Highly efficient enrichment of porcine cells with deletions induced by CRISPR/Cas9 using dual fluorescence selection. J. Biotechnol. 214, 69-74.
    Horvath, P., Barrangou, R., 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327, 167-170.
    Hou, L., Shi, J., Cao, L., Xu, G., Hu, C., Wang, C., 2017. Pig has no uncoupling protein 1. Biochem. Biophys. Res. Commun. 487, 795-800.
    Hryhorowicz, M., Grzeskowiak, B., Mazurkiewicz, N., Sledzinski, P., Lipinski, D., Slomski, R., 2019. Improved delivery of CRISPR/Cas9 system using magnetic nanoparticles into porcine fibroblast. Mol. Biotechnol. 61, 173-180.
    Hsu, P.D., Lander, E.S., Zhang, F., 2014. Development and applications of CRISPRCas9 for genome engineering. Cell 157, 1262-1278.
    Huang, L., Hua, Z., Xiao, H., Cheng, Y., Xu, K., Gao, Q., Xia, Y., Liu, Y., Zhang, X., Zheng, X., et al., 2017. CRISPR/Cas9-mediated ApoE-/- and LDLR-/- double gene knockout in pigs elevates serum LDL-C and TC levels. Oncotarget 8, 37751-37760.
    Hubner, A., Petersen, B., Keil, G.M., Niemann, H., Mettenleiter, T.C., Fuchs, W., 2018. Efficient inhibition of African swine fever virus replication by CRISPR/Cas9 targeting of the viral p30 gene (CP204L). Sci. Rep. 8, 1449.
    Jonas, E., de Koning, D.J., 2015. Genomic selection needs to be carefully assessed to meet specific requirements in livestock breeding programs. Front. Genet. 6, 49.
    Josefsberg, J.O., Buckland, B., 2012. Vaccine process technology. Biotechnol. Bioeng. 109, 1443-1460.
    Joung, J., Konermann, S., Gootenberg, J.S., Abudayyeh, O.O., Platt, R.J., Brigham, M.D., Sanjana, N.E., Zhang, F., 2017. Genome-scale CRISPR-Cas9 knockout and transcriptional activation screening. Nat. Protoc. 12, 828-863.
    Juillerat, A., Dubois, G., Valton, J., Thomas, S., Stella, S., Marechal, A., Langevin, S., Benomari, N., Bertonati, C., Silva, G.H., et al., 2014. Comprehensive analysis of the specificity of transcription activator-like effector nucleases. Nucleic Acids Res. 42, 5390-5402.
    Kang, J.T., Ryu, J., Cho, B., Lee, E.J., Yun, Y.J., Ahn, S., Lee, J., Ji, D.Y., Lee, K., Park, K.W., 2016. Generation of RUNX3 knockout pigs using CRISPR/Cas9-mediated gene targeting. Reprod. Domest. Anim. 51, 970-978.
    Kappes, M.A., Faaberg, K.S., 2015. PRRSV structure, replication and recombination:origin of phenotype and genotype diversity. Virology 479-480, 475-486.
    Kim, Y.G., 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.
    Kopecky, J., Clarke, G., Enerbäck, S., Spiegelman, B., Kozak, L.P., 1995. Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J. Clin. Invest. 96, 2914-2923.
    Lema, M.A., 2019. Regulatory aspects of gene editing in Argentina. Transgenic Res. 28, 147-150.
    Li, W., Lu, R., He, Q., 2017a. Aminopeptidase N is not required for porcine epidemic diarrhea virus cell entry. Virus Res. 235, 6-13.
    Li, C., Zhang, R., Meng, X., Chen, S., Zong, Y., Lu, C., Qiu, J., Chen, Y., Li, J., Gao, C., 2020a. Targeted, random mutagenesis of plant genes with dual cytosine and adenine base. Nat. Biotechnol. 38, 875-882.
    Li, G., Zhang, X., Wang, H., Mo, J., Zhong, C., Shi, J., Zhou, R., Li, Z., Yang, H., Wu, Z., et al., 2020b. CRISPR/Cas9-mediated integration of large transgene into pig CEP112 locus. G3-Genes. Genom. Genet. 10, 467-473.
    Li, J., Fang, K., Rong, Z., Li, X., Ren, X., Ma, H., Chen, H., Li, X., Qian, P., 2020c. Comparison of gE/gI-and TK/gE/gI-gene-deleted pseudorabies virus vaccines mediated by CRISPR/Cas9 and Cre/Lox systems. Viruses 12, 369.
    Li, L., Meng, H., Zou, Q., Zhang, J., Cai, L., Yang, B., Weng, J., Lai, L., Yang, H., Gao, Y., 2019. Establishment of gene-edited pigs expressing human bloodcoagulation factor VII and albumin for bioartificial liver use. J. Gastroenterol. Hepatol. 34, 1851-1859.
    Li, W., Mao, L., Cao, Y., Zhou, B., Yang, L., Han, L., Hao, F., Lin, T., Zhang, W., Jiang, J., 2017b. Porcine viperin protein inhibits the replication of classical swine fever virus (CSFV) in vitro. Virol. J. 14, 202.
    Liang, X., Sun, L., Yu, T., Pan, Y., Wang, D., Hu, X., Fu, Z., He, Q., Cao, G., 2016. A CRISPR/Cas9 and Cre/Lox system-based express vaccine development strategy against re-emerging Pseudorabies virus. Sci. Rep. 6, 19176.
    Lim, C., Gapinske, M., Brooks, A.K., Woods, W.S., Powell, J.E., Zeballos, C.M., Winter, J., Perez-Pinera, P., Gaj, T., 2020. Treatment of a mouse model of ALS by in vivo base editing. Mol. Ther. 28, 1177-1189.
    Lin, J., Cao, C., Tao, C., Ye, R., Dong, M., Zheng, Q., Wang, C., Jiang, X., Qin, G., Yan, C., et al., 2017. Cold adaptation in pigs depends on UCP3 in beige adipocytes. J. Mol. Cell Biol. 9, 364-375.
    Liu, Q., Cheng, X., Liu, G., Li, B., Liu, X., 2020a. Deep learning improves the ability of sgRNA off-target propensity prediction. BMC Bioinf. 21, 51.
    Liu, R.L.W.Z., Yang, X.L.M.W., He, D.M.X.L., 2020b. Precise editing of myostatin signal peptide by CRISPR/Cas9 increases the muscle mass of Liang Guang Small Spotted pigs. Transgenic Res. 1, 149-163.
    Liu, X., Liu, X., Liu, H., Liu, H., Wang, M., Wang, M., Li, R., Li, R., Zeng, J., Zeng, J., et al., 2019. Disruption of the ZBED6 binding site in intron 3 of IGF2 by CRISPR/Cas9 leads to enhanced muscle development in Liang Guang Small Spotted pigs. Transgenic Res. 28, 141-150.
    Llobat, L., 2020. Embryo gene expression in pig pregnancy. Reprod. Domest. Anim. 55, 523-529.
    Luo, L., Wang, S., Zhu, L., Fan, B., Liu, T., Wang, L., Zhao, P., Dang, Y., Sun, P., Chen, J., et al., 2019. Aminopeptidase N-null neonatal piglets are protected from transmissible gastroenteritis virus but not porcine epidemic diarrhea virus. Sci. Rep. 9, 13186.
    Maga, E.A., Shoemaker, C.F., Rowe, J.D., BonDurant, R.H., Anderson, G.B., Murray, J.D., 2006. Production and processing of milk from transgenic goats expressing human lysozyme in the mammary gland. J. Dairy Sci. 89, 518-524.
    Manghwar, H., Li, B., Ding, X., Hussain, A., Lindsey, K., Zhang, X., Jin, S., 2020. CRISPR/Cas systems in genome editing:methodologies and tools for sgRNA design, off-target evaluation, and strategies to mitigate off-target effects. Adv. Sci. 7, 1902312.
    Matson, A.W., Hosny, N., Swanson, Z.A., Hering, B.J., Burlak, C., 2019. Optimizing sgRNA length to improve target specificity and efficiency for the GGTA1 gene using the CRISPR/Cas9 gene editing system. PLoS One 14, e0226107.
    McGaugh, S., Schwartz, T.S., 2017. Here and there, but not everywhere:repeated loss of uncoupling protein 1 in amniotes. Biol. Lett. 13, 20160749.
    Mettenleiter, T.C., 1995. Progress in the development of vaccines against Aujeszky's disease. Tierarztl. Prax. 23, 570-574.
    Meyer, A.E., Pfeiffer, C.A., Brooks, K.E., Spate, L.D., Benne, J.A., Cecil, R., Samuel, M.S., Murphy, C.N., Behura, S., McLean, M.K., et al., 2019. New perspective on conceptus estrogens in maternal recognition and pregnancy establishment in the pigdagger. Biol. Reprod. 101, 148-161.
    Miller, J.C., Tan, S., Qiao, G., Barlow, K.A., Wang, J., Xia, D.F., Meng, X., Paschon, D.E., Leung, E., Hinkley, S.J., et al., 2011. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143-148.
    Moalic, Y., Blanchard, Y., Felix, H., Jestin, A., 2006. Porcine endogenous retrovirus integration sites in the human genome:features in common with those of murine leukemia virus. J. Virol. 80, 10980-10988.
    Moennig, V., 2015. The control of classical swine fever in wild boar. Front. Microbiol. 6, 1211.
    Muller, T., Batza, H.J., Schluter, H., Conraths, F.J., Mettenleiter, T.C., 2003. Eradication of Aujeszky's disease in Germany. J. Vet. Med. B. Infect. Dis. Vet. Public. Health. 50, 207-213.
    Nasr, N., Maddocks, S., Turville, S.G., Harman, A.N., Woolger, N., Helbig, K.J., Wilkinson, J., Bye, C.R., Wright, T.K., Rambukwelle, D., et al., 2012. HIV-1 infection of human macrophages directly induces viperin which inhibits viral production. Blood 120, 778-788.
    Neumann, E.J., Kliebenstein, J.B., Johnson, C.D., Mabry, J.W., Bush, E.J., Seitzinger, A.H., Green, A.L., Zimmerman, J.J., 2005. Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J. Am. Vet. Med. Assoc. 227, 385-392.
    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, e106718.
    Niemann, H., Petersen, B., 2016. The production of multi-transgenic pigs:update and perspectives for xenotransplantation. Transgenic Res. 25, 361-374.
    Nishio, K., Tanihara, F., Nguyen, T.V., Kunihara, T., Nii, M., Hirata, M., Takemoto, T., Otoi, T., 2018. Effects of voltage strength during electroporation on the development and quality of in vitro-produced porcine embryos. Reprod. Domest. Anim. 53, 313-318.
    Niu, D., Wei, H.J., Lin, L., George, H., Wang, T., Lee, I.H., Zhao, H.Y., Wang, Y., Kan, Y., Shrock, E., et al., 2017. Inactivation of porcine endogenous retrovirus in pigs using CRISPR-Cas9. Science 357, 1303-1307.
    Oh, J.N., Choi, K.H., Lee, C.K., 2018. Multi-resistance strategy for viral diseases and in vitro short hairpin RNA verification method in pigs. Asian-Australas. J. Anim. Sci. 31, 489-498.
    Pan, J., Tao, C., Cao, C., Zheng, Q., Lam, S.M., Shui, G., Liu, X., Li, K., Zhao, J., Wang, Y., 2019. Adipose lipidomics and RNA-Seq analysis revealed the enhanced mitochondrial function in UCP1 knock-in pigs. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1864, 1375-1383.
    Patience, C., Takeuchi, Y., Weiss, R.A., 1997. Infection of human cells by an endogenous retrovirus of pigs. Nat. Med. 3, 282-286.
    Pattanayak, V., Ramirez, C.L., Joung, J.K., Liu, D.R., 2011. Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat. Methods 8, 765-770.
    Piotrowski-Daspit, A.S., Glazer, P.M., Saltzman, W.M., 2018. Delivery technologies for genome editing. Nat. Rev. Drug Discov. 7, 24-32.
    Price, A.A., Sampson, T.R., Ratner, H.K., Grakoui, A., Weiss, D.S., 2015. Cas9-mediated targeting of viral RNA in eukaryotic cells. Proc. Natl. Acad. Sci. U. S. A. 112, 6164-6169.
    Proudfoot, C., Carlson, D.F., Huddart, R., Long, C.R., Pryor, J.H., King, T.J., Lillico, S.G., Mileham, A.J., McLaren, D.G., Whitelaw, C.B., et al., 2015. Genome edited sheep and cattle. Transgenic Res. 24, 147-153.
    Ramirez, C.L., Foley, J.E., Wright, D.A., Muller-Lerch, F., Rahman, S.H., Cornu, T.I., Winfrey, R.J., Sander, J.D., Fu, F., Townsend, J.A., et al., 2008. Unexpected failure rates for modular assembly of engineered zinc fingers. Nat. Methods 5, 374-375.
    Ran, F.A., Hsu, P.D., Wright, J., Agarwala, V., Scott, D.A., Zhang, F., 2013. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308.
    Ren, J., Wang, H., Zhou, L., Ge, X., Guo, X., Han, J., Yang, H., 2020. Glycoproteins C and D of PRV Strain HB1201 contribute individually to the escape from BarthaK61 vaccine-induced immunity. Front. Microbiol. 11, 323.
    Roura, E., Koopmans, S.J., Lalles, J.P., Le Huerou-Luron, I., de Jager, N., Schuurman, T., Val-Laillet, D., 2016. Critical review evaluating the pig as a model for human nutritional physiology. Nutr. Res. Rev. 29, 60-90.
    Rousseau, B.A., Hou, Z., Gramelspacher, M.J., Zhang, Y., 2018. Programmable RNA cleavage and recognition by a natural CRISPR-Cas9 system from neisseria meningitidis. Mol. Cell. 69, 906-914. e4.
    Ruan, J., Xu, J., Chen-Tsai, R.Y., Li, K., 2017. Genome editing in livestock:are we ready for a revolution in animal breeding industry? Transgenic Res. 26, 715-726.
    Rudin, N., Haber, J.E., 1988. Efficient repair of HO-induced chromosomal breaks in Saccharomyces cerevisiae by recombination between flanking homologous sequences. Mol. Cell Biol. 8, 3918-3928.
    Rui, Y., Wilson, D.R., Green, J.J., 2019. Non-viral delivery to enable genome editing. Trends Biotechnol. 37, 281-293.
    Ryu, J., Prather, R.S., Lee, K., 2018. Use of gene-editing technology to introduce targeted modifications in pigs. J. Anim. Sci. Biotechnol. 9, 5.
    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.
    Schneider, J.W., Oommen, S., Qureshi, M.Y., Goetsch, S.C., Pease, D.R., Sundsbak, R.S., Guo, W., Sun, M., Sun, H., Kuroyanagi, H., et al., 2020. Dysregulated ribonucleoprotein granules promote cardiomyopathy in RBM20 geneedited pigs. Nat. Med. 26, 1788-1800.
    Schultheiss, H.P., Fairweather, D., Caforio, A., Escher, F., Hershberger, R.E., Lipshultz, S.E., Liu, P.P., Matsumori, A., Mazzanti, A., McMurray, J., et al., 2019. Dilated cardiomyopathy. Nat. Rev. Dis. Primers. 5, 33.
    Shalem, O., Sanjana, N.E., Zhang, F., 2015. High-throughput functional genomics using CRISPR-Cas9. Nat. Rev. Genet. 16, 299-311.
    Sharma, V., Kaushik, S., Kumar, R., Yadav, J.P., Kaushik, S., 2019. Emerging trends of Nipah virus:a review. Rev. Med. Virol. 29, e2010.
    Sheets, T.P., Park, C.H., Park, K.E., Powell, A., Donovan, D.M., Telugu, B.P., 2016. Somatic cell nuclear transfer followed by CRIPSR/Cas9 microinjection results in highly efficient genome editing in cloned pigs. Int. J. Mol. Sci. 17, 2031.
    Shen, Z., Wang, G., Yang, Y., Shi, J., Fang, L., Li, F., Xiao, S., Fu, Z.F., Peng, G., 2019. A conserved region of nonstructural protein 1 from alphacoronaviruses inhibits host gene expression and is critical for viral virulence. J. Biol. Chem. 294, 13606-13618.
    Song, R., Wang, Y., Wang, Y., Zhao, J., 2020. Base editing in pigs for precision breeding. Front. Agr. Sci. Eng. 7, 161.
    Stoian, A., Rowland, R., Petrovan, V., Sheahan, M., Samuel, M.S., Whitworth, K.M., Wells, K.D., Zhang, J., Beaton, B., Cigan, M., et al., 2020. The use of cells from ANPEP knockout pigs to evaluate the role of aminopeptidase N (APN) as a receptor for porcine deltacoronavirus (PDCoV). Virology 541, 136-140.
    Tanihara, F., Hirata, M., Nguyen, N.T., LE, Q.A., Hirano, T., Otoi, T., 2019a. Effects of concentration of CRISPR/Cas9 components on genetic mosaicism in cytoplasmic microinjected porcine embryos. J. Reprod. Dev. 65, 209-214.
    Tanihara, F., Hirata, M., Nguyen, N.T., Le, Q.A., Hirano, T., Takemoto, T., Nakai, M., Fuchimoto, D.I., Otoi, T., 2018. Generation of a TP53-modified porcine cancer model by CRISPR/Cas9-mediated gene modification in porcine zygotes via electroporation. PLoS One 13, e0206360.
    Tanihara, F., Hirata, M., Nguyen, N.T., Le, Q.A., Wittayarat, M., Fahrudin, M., Hirano, T., Otoi, T., 2019b. Generation of CD163-edited pig via electroporation of the CRISPR/Cas9 system into porcine in vitro-fertilized zygotes. Anim. Biotechnol. 1-8.
    Tanihara, F., Hirata, M., Nguyen, N.T., Le, Q.A., Hirano, T., Takemoto, T., Nakai, M., Fuchimoto, D.I., Otoi, T., 2019c. Generation of PDX-1 mutant porcine blastocysts by introducing CRISPR/Cas9-system into porcine zygotes via electroporation. Anim. Sci. J. 90, 55-61.
    Tanihara, F., Hirata, M., Thi, N.N., Anh, L.Q., Hirano, T., Otoi, T., 2020. Generation of viable PDX1 gene-edited founder pigs as providers of nonmosaics. Mol. Reprod. Dev. 87, 471-481.
    Tao, D., Liu, J., Nie, X., Xu, B., Tran-Thi, T.N., Niu, L., Liu, X., Ruan, J., Lan, X., Peng, G., et al., 2020. Application of CRISPR-Cas12a enhanced fluorescence assay coupled with nucleic acid amplification for the sensitive detection of African swine fever virus. ACS Synth. Biol. 9, 2339-2350.
    Thygesen, P., 2019. Clarifying the regulation of genome editing in Australia:situation for genetically modified organisms. Transgenic Res. 28, 151-159.
    Tu, C.F., Chuang, C.K., Hsiao, K.H., Chen, C.H., Chen, C.M., Peng, S.H., Su, Y.H., Chiou, M.T., Yen, C.H., Hung, S.W., et al., 2019. Lessening of porcine epidemic diarrhoea virus susceptibility in piglets after editing of the CMP-Nglycolylneuraminic acid hydroxylase gene with CRISPR/Cas9 to nullify N-glycolylneuraminic acid expression. PLoS One 14, e0217236.
    Tu, Z., Yang, W., Yan, S., Guo, X., Li, X.J., 2015. CRISPR/Cas9:a powerful genetic engineering tool for establishing large animal models of neurodegenerative diseases. Mol. Neurodegener. 10, 35.
    Van Gorp, H., Van Breedam, W., Delputte, P.L., Nauwynck, H.J., 2008. Sialoadhesin and CD163 join forces during entry of the porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 89, 2943.
    Vilahur, G., Padro, T., Badimon, L., 2011. Atherosclerosis and thrombosis:insights from large animal models. J. Biomed. Biotechnol. 2011, 907575.
    Waltz, E., 2016. GM salmon declared fit for dinner plates. Nat. Biotechnol. 34, 7-8.
    Wang, R.G., Ruan, M., Zhang, R.J., Chen, L., Li, X.X., Fang, B., Li, C., Ren, X.Y., Liu, J.Y., Xiong, Q., et al., 2018. Antigenicity of tissues and organs from GGTA1/CMAH/beta4GalNT2 triple gene knockout pigs. J. Biomed. Res. 33, 235-243.
    Wang, H., Shen, L., Chen, J., Liu, X., Tan, T., Hu, Y., Bai, X., Li, Y., Tian, K., Li, N., et al., 2019a. Deletion of CD163 exon 7 confers resistance to highly pathogenic porcine reproductive and respiratory viruses on pigs. Int. J. Biol. Sci. 15, 1993-2005.
    Wang, J., Liu, M., Zhao, L., Li, Y., Zhang, M., Jin, Y., Xiong, Q., Liu, X., Zhang, L., Jiang, H., et al., 2019b. Disabling of nephrogenesis in porcine embryos via CRISPR/Cas9-mediated SIX1 and SIX4 gene targeting. Xenotransplantation 26, e12484.
    Wang, K., Ouyang, H., Xie, Z., Yao, C., Guo, N., Li, M., Jiao, H., Pang, D., 2015. Efficient generation of myostatin mutations in pigs using the CRISPR/Cas9 system. Sci. Rep. 5, 16623.
    Wang, X., Cao, C., Huang, J., Yao, J., Hai, T., Zheng, Q., Wang, X., Zhang, H., Qin, G., Cheng, J., et al., 2016. One-step generation of triple gene-targeted pigs using CRISPR/Cas9 system. Sci. Rep. 6, 20620.
    Wang, K., Tang, X., Xie, Z., Zou, X., Li, M., Yuan, H., Guo, N., Ouyang, H., Jiao, H., Pang, D., 2017. CRISPR/Cas9-mediated knockout of myostatin in Chinese indigenous Erhualian pigs. Transgenic Res. 26, 799-805.
    Wells, K.D., Bardot, R., Whitworth, K.M., Trible, B.R., Fang, Y., Mileham, A., Kerrigan, M.A., Samuel, M.S., Prather, R.S., Rowland, R., 2017. Replacement of porcine CD163 scavenger receptor cysteine-rich domain 5 with a CD163-Like homolog confers resistance of pigs to genotype 1 but not genotype 2 porcine reproductive and respiratory syndrome virus. J. Virol. 91 e01521-16.
    Whitworth, K.M., Benne, J.A., Spate, L.D., Murphy, S.L., Samuel, M.S., Murphy, C.N., Richt, J.A., Walters, E., Prather, R.S., Wells, K.D., 2017. Zygote injection of CRISPR/Cas9 RNA successfully modifies the target gene without delaying blastocyst development or altering the sex ratio in pigs. Transgenic Res. 26, 97-107.
    Whitworth, K.M., Lee, K., Benne, J.A., Beaton, B.P., Spate, L.D., Murphy, S.L., Samuel, M.S., Mao, J., O'Gorman, C., Walters, E.M., et al., 2014. Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitroderived oocytes and embryos1. Biol. Reprod. 91, 78.
    Whitworth, K.M., Rowland, R., Petrovan, V., Sheahan, M., Cino-Ozuna, A.G., Fang, Y., Hesse, R., Mileham, A., Samuel, M.S., Wells, K.D., et al., 2019. Resistance to coronavirus infection in amino peptidase N-deficient pigs. Transgenic Res. 28, 21-32.
    Whitworth, K.M., Rowland, R.R., Ewen, C.L., Trible, B.R., Kerrigan, M.A., CinoOzuna, A.G., Samuel, M.S., Lightner, J.E., McLaren, D.G., Mileham, A.J., et al., 2016. Gene-edited pigs are protected from porcine reproductive and respiratory syndrome virus. Nat. Biotechnol. 34, 20-22.
    Whyte, J.J., Meyer, A.E., Spate, L.D., Benne, J.A., Cecil, R., Samuel, M.S., Murphy, C.N., Prather, R.S., Geisert, R.D., 2018. Inactivation of porcine interleukin-1beta results in failure of rapid conceptus elongation. Proc. Natl. Acad. Sci. U. S. A. 115, 307-312.
    Xiang, G., Ren, J., Hai, T., Fu, R., Yu, D., Wang, J., Li, W., Wang, H., Zhou, Q., 2018. Editing porcine IGF2 regulatory element improved meat production in Chinese Bama pigs. Cell. Mol. Life Sci. 75, 4619-4628.
    Xie, Z., Jiao, H., Xiao, H., Jiang, Y., Liu, Z., Qi, C., Zhao, D., Jiao, S., Yu, T., Tang, X., et al., 2020. Generation of pRSAD2 gene knock-in pig via CRISPR/Cas9 technology. Antivir. Res. 174, 104696.
    Xie, Z., Pang, D., Yuan, H., Jiao, H., Lu, C., Wang, K., Yang, Q., Li, M., Chen, X., Yu, T., et al., 2018. Genetically modified pigs are protected from classical swine fever virus. PLoS Pathog. 14, e1007193.
    Xu, A., Qin, C., Lang, Y., Wang, M., Lin, M., Li, C., Zhang, R., Tang, J., 2015. A simple and rapid approach to manipulate pseudorabies virus genome by CRISPR/Cas9 system. Biotechnol. Lett. 37, 1265-1272.
    Xu, C.L., Ruan, M., Mahajan, V.B., Tsang, S.H., 2019. Viral delivery systems for CRISPR. Viruses 11, 28.
    Xu, K., Zhou, Y., Mu, Y., Liu, Z., Hou, S., Xiong, Y., Fang, L., Ge, C., Wei, Y., Zhang, X., et al., 2020. 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.
    Yan, S., Tu, Z., Liu, Z., Fan, N., Yang, H., Yang, S., Yang, W., Zhao, Y., Ouyang, Z., Lai, C., et al., 2018. A Huntingtin knockin pig model recapitulates features of selective neurodegeneration in Huntington's disease. Cell 173, 989-1002. e13.
    Yang, L., Güell, M., Niu, D., George, H., Lesha, E., Grishin, D., Aach, J., Shrock, E., Xu, W., Poci, J., et al., 2015. Genome-wide inactivation of porcine endogenous retroviruses (PERVs). Science 350, 1101-1104.
    Yang, S., Li, X., Li, K., Fan, B., Tang, Z., 2014. A genome-wide scan for signatures of selection in Chinese indigenous and commercial pig breeds. BMC Genet. 15, 7.
    Yao, J., Zeng, H., Zhang, M., Wei, Q., Wang, Y., Yang, H., Lu, Y., Li, R., Xiong, Q., Zhang, L., et al., 2019. OSBPL2-disrupted pigs recapitulate dual features of human hearing loss and hypercholesterolaemia. J. Genet. Genomics. 46, 379-387.
    Yue, Y., Xu, W., Kan, Y., Zhao, H., Zhou, Y., Song, X., Wu, J., Xiong, J., Goswami, D., Yang, M., et al., 2020. Extensive germline genome engineering in pigs. Nat. Biomed. Eng. 5, 134-143.
    Yugo, D.M., Heffron, C.L., Ryu, J., Uh, K., Subramaniam, S., Matzinger, S.R., Overend, C., Cao, D., Kenney, S.P., Sooryanarain, H., et al., 2018. Infection dynamics of hepatitis E virus in wild-type and immunoglobulin heavy chain knockout jh -/- gnotobiotic piglets. J. Virol. 92, e01208e-01218.
    Zarei, A., Razban, V., Hosseini, S.E., Tabei, S.M.B., 2019. Creating cell and animal models of human disease by genome editing using CRISPR/Cas9. J. Gene Med. 21 e3082-n/a.
    Zhan, T., Rindtorff, N., Betge, J., Ebert, M.P., Boutros, M., 2019. CRISPR/Cas9 for cancer research and therapy. Semin. Cancer. Biol. 55, 106-119.
    Zhang, R., Wang, Y., Chen, L., Wang, R., Li, C., Li, X., Fang, B., Ren, X., Ruan, M., Liu, J., et al., 2018. Reducing immunoreactivity of porcine bioprosthetic heart valves by genetically-deleting three major glycan antigens, GGTA1/beta4GalNT2/CMAH. Acta Biomater. 72, 196-205.
    Zhang, B., Wang, C., Zhang, Y., Jiang, Y., Qin, Y., Pang, D., Zhang, G., Liu, H., Xie, Z., Yuan, H., et al., 2020. A CRISPR-engineered swine model of COL2A1 deficiency recapitulates altered earlyskeletaldevelopmentaldefects in humans. Bone 137, 115450.
    Zhang, Y., Xi, Q., Ding, J., Cai, W., Meng, F., Zhou, J., Li, H., Jiang, Q., Shu, G., Wang, S., et al., 2012. Production of transgenic pigs mediated by pseudotyped lentivirus and sperm. PLoS One 7, e35335.
    Zhao, C., Liu, H., Xiao, T., Wang, Z., Nie, X., Li, X., Qian, P., Qin, L., Han, X., Zhang, J., et al., 2020. CRISPR screening of porcine sgRNA library identifies host factors associated with Japanese encephalitis virus replication. Nat. Commun. 11, 5178.
    Zhao, C., Wang, Y., Nie, X., Han, X., Liu, H., Li, G., Yang, G., Ruan, J., Ma, Y., Li, X., et al., 2019. Evaluation of the effects of sequence length and microsatellite instability on single-guide RNA activity and specificity. Int. J. Biol. Sci. 15, 2641-2653.
    Zhao, C., Zheng, X., Qu, W., Li, G., Li, X., Miao, Y.L., Han, X., Liu, X., Li, Z., Ma, Y., et al., 2017. CRISPR-offinder:a CRISPR guide RNA design and off-target searching tool for user-defined protospacer adjacent motif. Int. J. Biol. Sci. 13, 1470-1478.
    Zheng, Q., Lin, J., Huang, J., Zhang, H., Zhang, R., Zhang, X., Cao, C., Hambly, C., Qin, G., Yao, J., et al., 2017. Reconstitution of UCP1 using CRISPR/Cas9 in the white adipose tissue of pigs decreases fat deposition and improves thermogenic capacity. Proc. Natl. Acad. Sci. U. S. A. 114, E9474-E9482.
    Zhou, X., Xin, J., Fan, N., Zou, Q., Huang, J., Ouyang, Z., Zhao, Y., Zhao, B., Liu, Z., Lai, S., et al., 2015. Generation of CRISPR/Cas9-mediated gene-targeted pigs via somatic cell nuclear transfer. Cell. Mol. Life Sci. 72, 1175-1184.
    Zhu, X.X., Zhong, Y.Z., Ge, Y.W., Lu, K.H., Lu, S.S., 2018. CRISPR/Cas9-mediated generation of Guangxi Bama minipigs harboring three mutations in alphasynuclein causing Parkinson's disease. Sci. Rep. 8, 12420.
    Zou, X., Ouyang, H., Yu, T., Chen, X., Pang, D., Tang, X., Chen, C., 2019. Preparation of a new type 2 diabetic miniature pig model via the CRISPR/Cas9 system. Cell Death Dis. 10, 823.
    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.
    Zuo, E., Sun, Y., Wei, W., Yuan, T., Ying, W., Sun, H., Yuan, L., Steinmetz, L.M., Li, Y., Yang, H., 2019. Cytosine base editor generates substantial off-target singlenucleotide variants in mouse embryos. Science 364, 289-292.
    • Relative Articles
    • Supplements(0)
    • Cited By
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索
    Get Citation
    PDF

    Article Metrics

    Article views (234) PDF downloads (19) Cited by ()
    Proportional views
    Related

    Editorial Office

    Journal of Genetics and Genomics

    京ICP备09063187号-7

    No.1, West Beichen Road, Chaoyang District, Beijing 100101, P.R.China

    +86-10-64806528+86-10-64807786jgg@genetics.ac.cn

    Supported by: Beijing Renhe Information Technology Co. Ltd  

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return