Generation of B Cell-Deficient Pigs by Highly Efficient CRISPR/Cas9-Mediated Gene Targeting

Journal of Genetics and Genomics

Volumn 42, Issue 8, 2015, Pages 437-444

  Chen, Fengjiao ^a   Wang, Ying ^a   Yuan, Yilin ^a   Zhang, Wei ^a   Ren, Zijian ^a   Jin, Yong ^a   Liu, Xiaorui ^a   Xiong, Qiang ^a   Chen, Qin ^a   Zhang, Manling ^a   Li, Xiaokang ^a   Zhao, Lihua ^a   Li, Ze ^a   Wu, Zhaoqiang ^a   Zhang, Yanfei ^a   Hu, Feifei ^a   Huang, Juan ^a   Li, Rongfeng ^a   Dai, Yifan ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

B cell deficiency; CRISPR Cas9 system; IgM heavy chain; Pig genome editing; Somatic cell nuclear transfer

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOGLOBULIN MU CHAIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CD3+ T LYMPHOCYTE; CRISPR CAS SYSTEM; EMBRYO TRANSFER; FETUS; FIBROBLAST; FRAMESHIFT MUTATION; GENE INACTIVATION; GENE MUTATION; GENE TARGETING; GENETIC TRANSFECTION; GENOTYPE; HOMOLOGOUS RECOMBINATION; LYMPHOCYTE SUBPOPULATION; MALE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PIG; PIGLET; PROTEIN EXPRESSION; SOMATIC CELL; ANIMAL; CELL NUCLEUS TRANSPLANTATION; CYTOLOGY; GENETIC ENGINEERING; GENETICS; METABOLISM; PHENOTYPE; PRIMARY CELL CULTURE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; B-LYMPHOCYTES; CRISPR-CAS SYSTEMS; FETUS; FIBROBLASTS; GENE TARGETING; GENETIC ENGINEERING; IMMUNOGLOBULIN M; MALE; NUCLEAR TRANSFER TECHNIQUES; PHENOTYPE; PRIMARY CELL CULTURE; SWINE;

EID: 84940574829     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2015.05.002     Document Type: Article

References (38)

1. Aigner B., Renner S., Kessler B., Klymiuk N., Kurome M., Wünsch A., Wolf E. Transgenic pigs as models for translational biomedical research. J. Mol. Med. 2010, 88:653-664.
2. Bassett A.R., Liu J.L. CRISPR/Cas9 and genome editing in Drosophila. J. Genet. Genomics 2014, 41:7-19.
3. Butler J.E., Sun J.S., Navarro P. The swine Ig heavy chain locus has a single JH and no identifiable IgD. Int. Immunol. 1996, 8:1897-1904.
4. Carter D.B., Lai L., Park K.W., Samuel M., Lattimer J.C., Jordan K.R., Estes D.M., Besch-Williford C., Prather R.S. Phenotyping of transgenic cloned piglets. Cloning Stem Cells 2002, 4:131-145.
5. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
6. Eguchi-Ogawa T., Wertz N., Sun X.Z., Puimi F., Uenishi H., Wells K., Chardon P., Tobin G.J., Butler J.E. Antibody repertoire development in fetal and neonatal piglets. XI. The relationship of variable heavy chain gene usage and the genomic organization of the variable heavy chain locus. J. Immunol. 2010, 184:3734-3742.
7. Fu Y., Foden J.A., Khayter C., Maeder M.L., Reyon D., Joung J.K., Sander J.D. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 2013, 31:822-826.
8. Green L., Hardy M., Maynard-Currie C., Tsuda H., Louie D., Mendez M., Abderrahim H., Noguchi M., Smith D., Zeng Y. Antigen-specific human monoclonal antibodies from mice engineered with human Ig heavy and light chain YACs. Nat. Genet. 1994, 7:13-21.
9. Hai T., Teng F., Guo R., Li W., Zhou Q. One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res. 2014, 24:372-375.
10. Hsu P.D., Scott D.A., Weinstein J.A., Ran F.A., Konermann S., Agarwala V., Li Y., Fine E.J., Wu X., Shalem O. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 2013, 31:827-832.
11. Jakobovits A., Vergara G.J., Kennedy J.L., Hales J.F., McGuinness R.P., Casentini-Borocz D.E., Brenner D.G., Otten G.R. Analysis of homozygous mutant chimeric mice: deletion of the immunoglobulin heavy-chain joining region blocks B-cell development and antibody production. Proc. Natl. Acad. Sci. USA 1993, 90:2551-2555.
12. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337:816-821.
13. Jung D., Giallourakis C., Mostoslavsky R., Alt F.W. Mechanism and control of V (D) J recombination at the immunoglobulin heavy chain locus. Annu. Rev. Immunol. 2006, 24:541-570.
14. Kitamura D., Roes J., Kühn R., Rajewsky K. AB cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 1991, 350:423-426.
15. Kuroiwa Y., Kasinathan P., Choi Y.J., Naeem R., Tomizuka K., Sullivan E.J., Knott J.G., Duteau A., Goldsby R.A., Osborne B.A. Cloned transchromosomic calves producing human immunoglobulin. Nat. Biotechnol. 2002, 20:889-894.
16. Kuroiwa Y., Kasinathan P., Sathiyaseelan T., Jiao J.A., Matsushita H., Sathiyaseelan J., Wu H., Mellquist J., Hammitt M., Koster J. Antigen-specific human polyclonal antibodies from hyperimmunized cattle. Nat. Biotechnol. 2009, 27:173-181.
17. Lai L., Kang J.X., Li R., Wang J., Witt W.T., Yong H.Y., Hao Y., Wax D.M., Murphy C.N., Rieke A. Generation of cloned transgenic pigs rich in omega-3 fatty acids. Nat. Biotechnol. 2006, 24:435-436.
18. Li D., Qiu Z., Shao Y., Chen Y., Guan Y., Liu M., Li Y., Gao N., Wang L., Lu X. Heritable gene targeting in the mouse and rat using a CRISPR-Cas system. Nat. Biotechnol. 2013, 31:681-683.
19. 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.
20. Lonberg N. Human antibodies from transgenic animals. Nat. Biotechnol. 2005, 23:1117-1125.
21. Lonberg N., Taylor L.D., Harding F.A., Trounstine M., Higgins K.M., Schramm S.R., Kuo C.C., Mashayekh R., Wymore K., McCabe J.G., Munoz-O'Regan D., O'Donnell S.L., Lapachet E.S.G., Bengoechea T., Fishwild D.M., Carmack C.E., Kay R.M., Huszar D. Antigen-specific human antibodies from mice comprising four distinct genetic modifications. Nature 1994, 368:856-859.
22. Ma Y., Zhang X., Shen B., Lu Y., Chen W., Ma J., Bai L., Huang X., Zhang L. Generating rats with conditional alleles using CRISPR/Cas9. Cell Res. 2014, 24:122-125.
23. Mendicino M., Ramsoondar J., Phelps C., Vaught T., Ball S., LeRoith T., Monahan J., Chen S., Dandro A., Boone J. Generation of antibody-and B cell-deficient pigs by targeted disruption of the J-region gene segment of the heavy chain locus. Transgenic Res. 2011, 20:625-641.
24. Niu Y., Shen B., Cui Y., Chen Y., Wang J., Wang L., Kang Y., Zhao X., Si W., Li W. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 2014, 156:836-843.
25. Pattanayak V., Lin S., Guilinger J.P., Ma E., Doudna J.A., Liu D.R. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 2013, 31:839-843.
26. Ramsoondar J., Mendicino M., Phelps C., Vaught T., Ball S., Monahan J., Chen S., Dandro A., Boone J., Jobst P. Targeted disruption of the porcine immunoglobulin kappa light chain locus. Transgenic Res. 2011, 20:643-653.
27. Randall T.D., Carragher D.M., Rangel-Moreno J. Development of secondary lymphoid organs. Annu. Rev. Immunol. 2008, 26:627-650.
28. Rogers C.S., Stoltz D.A., Meyerholz D.K., Ostedgaard L.S., Rokhlina T., Taft P.J., Rogan M.P., Pezzulo A.A., Karp P.H., Itani O.A. Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 2008, 321:1837-1841.
29. Shen B., Zhang J., Wu H., Wang J., Ma K., Li Z., Zhang X., Zhang P., Huang X. Generation of gene-modified mice via Cas9/RNA-mediated gene targeting. Cell Res. 2013, 23:720-723.
30. Tan W., Carlson D.F., Lancto C.A., Garbe J.R., Webster D.A., Hackett P.B., Fahrenkrug S.C. Efficient nonmeiotic allele introgression in livestock using custom endonucleases. Proc. Natl. Acad. Sci. USA 2013, 110:16526-16531.
31. Tesson L., Usal C., Ménoret S., Leung E., Niles B.J., Remy S., Santiago Y., Vincent A.I., Meng X., Zhang L. Knockout rats generated by embryo microinjection of TALENs. Nat. Biotechnol. 2011, 29:695-696.
32. Tomizuka K., Shinohara T., Yoshida H., Uejima H., Ohguma A., Tanaka S., Sato K., Oshimura M., Ishida I. Double trans-chromosomic mice: maintenance of two individual human chromosome fragments containing Ig heavy and κ loci and expression of fully human antibodies. Proc. Natl. Acad. Sci. USA 2000, 97:722-727.
33. 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.
34. Wei C., Liu J., Yu Z., Zhang B., Gao G., Jiao R. TALEN or Cas9-rapid, efficient and specific choices for genome modifications. J. Genet. Genomics 2013, 40:281-289.
35. 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., Murphy C.N., Driver J., Mileham A., McLaren D., Wells K.D., Prather R.S. Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos. Biol. Reprod. 2014, 91:1-13.
36. Wiedenheft B., Sternberg S.H., Doudna J.A. RNA-guided genetic silencing systems in bacteria and archaea. Nature 2012, 482:331-338.
37. Yel L., Minegishi Y., Coustan-Smith E., Buckley R.H., Trübel H., Pachman L.M., Kitchingman G.R., Campana D., Rohrer J., Conley M.E. Mutations in the mu heavy-chain gene in patients with agammaglobulinemia. N. Engl. J. Med. 1996, 335:1486-1493.
38. Zhou X., Xin J., Fan N., Zou Q., Huang J., Ouyang Z., Zhao Y., Zhao B., Liu Z., Lai S., Yi X., Guo L., Esteban M.A., Zeng Y., Yang H., Lai L. Generation of CRISPR/Cas9-mediated gene-targeted pigs via somatic cell nuclear transfer. Cell. Mol. Life Sci. 2015, 72:1175-1184.