Transgenic chickens

Development Growth and Differentiation

Volumn 55, Issue 1, 2013, Pages 207-216

  Nishijima, Ken Ichi ^a   Iijima, Shinji ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

Embryonic stem cell; Gene silencing; Primordial germ cell; Retroviral vector; Transgenic chicken

Indexed keywords

COMPLEMENTARY DNA; GAG PROTEIN; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 11; INTERLEUKIN 6; LENTIVIRUS VECTOR; NUCLEOPROTEIN; RETROVIRUS VECTOR; SOMATOMEDIN; STEM CELL FACTOR; VIRUS ENVELOPE PROTEIN;

BIOLOGICAL ACTIVITY; BLASTODERM; CELL CULTURE; CELL CYCLE M PHASE; CHICKEN; CHROMOSOME ANALYSIS; CPG ISLAND; DEVELOPMENTAL STAGE; DNA METHYLATION; DNA SYNTHESIS; EGG YOLK; EMBRYO CELL; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; EXON; GAMETE; GENE SILENCING; GENETIC TRANSFECTION; HOST CELL; IN VITRO STUDY; LENTIVIRINAE; LONG TERMINAL REPEAT; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; OOCYTE; PRIMORDIAL GERM CELL; REVIEW; SEXUAL MATURATION; SPERMATOGONIUM; TRANSCRIPTION INITIATION SITE; TRANSGENE; TRANSGENICS; VIRION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELLS, CULTURED; CHICKENS; EMBRYONIC STEM CELLS; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; MALE; OOCYTES; RETROVIRIDAE; SPERMATOGONIA; TRANSFECTION; VIRUS REPLICATION;

GALLUS GALLUS; MAMMALIA;

EID: 84872159409     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/dgd.12032     Document Type: Review

References (98)

1. Beumer, K., Bhattacharyya, G., Bibikova, M., Trautman, J. K. & Carroll, D. 2006. Efficient gene targeting in Drosophila with zinc-finger nucleases. Genetics 172, 2391-2403.
2. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A. & Bonas, U. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509-1512.
3. Bosselman, R. A., Hsu, R. Y., Boggs, T., Hu, S., Bruszewski, J., Ou, S., Kozar, L., Martin, F., Green, C., Jacobsen, F., Nicolson, M., Schultz, J. A., Semon, K. M., Rishell, W. & Stewart, R. G. 1989. Germline transmission of exogenous genes in the chicken. Science 243, 533-535.
4. Carsience, R. S., Clark, M. E., Verrinder Gibbins, A. M. & Etches, R. J. 1993. Germline chimeric chickens from dispersed donor blastodermal cells and compromised recipient embryos. Development 117, 669-675.
5. Cermak, T., Doyle, E. L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J. A., Somia, N. V., Bogdanove, A. J. & Voytas, D. F. 2011. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82.
6. Chapman, S. C., Lawson, A., Macarthur, W. C. & Wiese, R. J. 2005. Ubiquitous GFP expression in transgenic chickens using a lentiviral vector. Development 132, 935-940.
7. Cui, X., Ji, D., Fisher, D. A., Wu, Y., Briner, D. M. & Weinstein, E. J. 2011. Targeted integration in rat and mouse embryos with zinc-finger nucleases. Nat. Biotechnol. 29, 64-67.
8. Etches, R. J. 1995. Physiology of reproduction: the female. In Poultry Production (ed. Hunton P.), pp. 221-241. Elsevier, Amsterdam.
9. Etches, R. J. 2006. The hard cell(s) of avian transgenesis. Transgenic Res. 15, 521-526.
10. Etches, R. J., Clark, M. E., Toner, A., Liu, G. & Gibbins, A. M. 1996. Contributions to somatic and germline lineages of chicken blastodermal cells maintained in culture. Mol. Reprod. Dev. 45, 291-298.
11. Eyal-Giladi, H., Ginsburg, M. & Farbarov, A. 1981. Avian primordial germ cells are of epiblastic origin. J. Embryol. Exp. Morphol. 65, 139-147.
12. Eyal-Giladi, H. & Kochav, S. 1976. From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick I. General morphology. Dev. Biol. 49, 321-337.
13. Furuta, H. & Fujihara, N. 1999. Proliferation of exogenously injected primordial germ cells (PGCs) into busulfan-treated chicken embryos. Asian J. Androl. 1, 187-190.
14. Harel-Markowitz, E., Gurevich, M., Shore, L. S., Katz, A., Stram, Y. & Shemesh, M. 2009. Use of sperm plasmid DNA lipofection combined with REMI (restriction enzyme-mediated insertion) for production of transgenic chickens expressing eGFP (enhanced green fluorescent protein) or human follicle-stimulating hormone. Biol. Reprod. 80, 1046-1052.
15. Harvey, A. J., Speksnijder, G., Baugh, L. R., Morris, J. A. & Ivarie, R. 2002a. Consistent production of transgenic chickens using replication-deficient retroviral vectors and high-throughput screening procedures. Poult. Sci. 81, 202-212.
16. Harvey, A. J., Speksnijder, G., Baugh, L. R., Morris, J. A. & Ivarie, R. 2002b. Expression of exogenous protein in the egg white of transgenic chickens. Nat. Biotechnol. 20, 396-399.
17. Hockemeyer, D., Wang, H. Y., Kiani, S., Lai, C. S., Gao, Q., Cassady, J. P., Cost, G. J., Zhang, L., Santiago, Y., Miller, J. C., Zeitler, B., Cherone, J. M., Meng, X. D., Hinkley, S. J., Rebar, E. J., Gregory, P. D., Urnov, F. D. & Jaenisch, R. 2011. Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol. 29, 731-734.
18. Horiuchi, H., Tategaki, A., Yamashita, Y., Hisamatsu, H., Ogawa, M., Noguchi, T., Aosasa, M., Kawashima, T., Akita, S., Nishimichi, N., Mitsui, N., Furusawa, S. & Matsuda, H. 2004. Chicken leukemia inhibitory factor maintains chicken embryonic stem cells in the undifferentiated state. J. Biol. Chem. 279, 24514-24520.
19. Howarth, B. 1995. Physiology of reproduction: the male. In Poultry Production (ed. Hunton P.), pp. 243-270. Elsevier, Amsterdam.
20. Ivarie, R. 2003. Avian transgenesis: progress towards the promise. Trends Biotechnol. 21, 14-19.
21. Jahner, D., Stuhlmann, H., Stewart, C. L., Harbers, K., Lohler, J., Simon, I. & Jaenisch, R. 1982. De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature 298, 623-628.
22. Kagami, H., Tagami, T., Matsubara, Y., Harumi, T., Hanada, H., Maruyama, K., Sakurai, M., Kuwana, T. & Naito, M. 1997. The developmental origin of primordial germ cells and the transmission of the donor-derived gametes in mixed-sex germline chimeras to the offspring in the chicken. Mol. Reprod. Dev. 48, 501-510.
23. Kalina, J., Senigl, F., Micakova, A., Mucksova, J., Blazkova, J., Yan, H., Poplstein, M., Hejnar, J. & Trefil, P. 2007. Retrovirus-mediated in vitro gene transfer into chicken male germ line cells. Reproduction 134, 445-453.
24. Kamihira, M., Ono, K., Esaka, K., Nishijima, K., Kigaku, R., Komatsu, H., Yamashita, T., Kyogoku, K. & Iijima, S. 2005. High-level expression of single-chain Fv-Fc fusion protein in serum and egg white of genetically manipulated chickens by using a retroviral vector. J. Virol. 79, 10864-10874.
25. Kodama, D., Nishimiya, D., Nishijima, K., Okino, Y., Inayoshi, Y., Kojima, Y., Ono, K., Motono, M., Miyake, K., Kawabe, Y., Kyogoku, K., Yamashita, T., Kamihira, M. & Iijima, S. 2012. Chicken oviduct-specific expression of transgene by a hybrid ovalbumin enhancer and the Tet expression system. J. Biosci. Bioeng. 113, 146-153.
26. Koo, B. C., Kwon, M. S., Choi, B. R., Kim, J. H., Cho, S. K., Sohn, S. H., Cho, E. J., Lee, H. T., Chang, W., Jeon, I., Park, J. K., Park, J. B. & Kim, T. 2006. Production of germline transgenic chickens expressing enhanced green fluorescent protein using a MoMLV-based retrovirus vector. FASEB J. 20, 2251-2260.
27. Koo, B. C., Kwon, M. S., Lee, H., Kim, M., Kim, D., Roh, J. Y., Park, Y. Y., Cui, X. S., Kim, N. H., Byun, S. J. & Kim, T. 2010. Tetracycline-dependent expression of the human erythropoietin gene in transgenic chickens. Transgenic Res. 19, 437-447.
28. Kumar, M., Keller, B., Makalou, N. & Sutton, R. E. 2001. Systematic determination of the packaging limit of lentiviral vectors. Hum. Gene Ther. 12, 1893-1905.
29. Kwon, M. S., Koo, B. C., Choi, B. R., Park, Y. Y., Lee, Y. M., Suh, H. S., Park, Y. S., Lee, H. T., Kim, J. H., Roh, J. Y., Kim, N. H. & Kim, T. 2008. Generation of transgenic chickens that produce bioactive human granulocyte-colony stimulating factor. Mol. Reprod. Dev. 75, 1120-1126.
30. Kwon, M. S., Koo, B. C., Roh, J. Y., Kim, M., Kim, J. H. & Kim, T. 2011. Production of transgenic chickens expressing a tetracycline-inducible GFP gene. Biochem. Biophys. Res. Commun. 410, 890-894.
31. Lavial, F., Acloque, H., Bachelard, E., Nieto, M. A., Samarut, J. & Pain, B. 2009. Ectopic expression of Cvh (chicken Vasa homologue) mediates the reprogramming of chicken embryonic stem cells to a germ cell fate. Dev. Biol. 330, 73-82.
32. Lavial, F. & Pain, B. 2010. Chicken embryonic stem cells as a non-mammalian embryonic stem cell model. Dev. Growth Differ. 52, 101-114.
33. Lee, S. H., Gupta, M. K., Han, D. W., Han, S. Y., Uhm, S. J., Kim, T. & Lee, H. T. 2007. Development of transgenic chickens expressing human parathormone under the control of a ubiquitous promoter by using a retrovirus vector system. Poult. Sci. 86, 2221-2227.
34. Lee, Y. M., Jung, J. G., Kim, J. N., Park, T. S., Kim, T. M., Shin, S. S., Kang, D. K., Lim, J. M. & Han, J. Y. 2006. A testis-mediated germline chimera production based on transfer of chicken testicular cells directly into heterologous testes. Biol. Reprod. 75, 380-386.
35. Lei, Y. N., Lee, C. L., Joo, K. I., Zarzar, J., Liu, Y. R., Dai, B. B., Fox, V. & Wang, P. 2011. Gene editing of human embryonic stem cells via an engineered baculoviral vector carrying zinc-finger nucleases. Mol. Ther. 19, 942-950.
36. Leighton, P. A., van de Lavoir, M. C., Diamond, J. H., Xia, C. & Etches, R. J. 2008. Genetic modification of primordial germ cells by gene trapping, gene targeting, and phiC31 integrase. Mol. Reprod. Dev. 75, 1163-1175.
37. Lewinski, M. K., Yamashita, M., Emerman, M., Ciuffi, A., Marshall, H., Crawford, G., Collins, F., Shinn, P., Leipzig, J., Hannenhalli, S., Berry, C. C., Ecker, J. R. & Bushman, F. D. 2006. Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog. 2, 611-622.
38. Li, T., Huang, S., Zhao, X. F., Wright, D. A., Carpenter, S., Spalding, M. H., Weeks, D. P. & Yang, B. 2011. Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res. 39, 6315-6325.
39. Lillico, S. G., Sherman, A., McGrew, M. J., Robertson, C. D., Smith, J., Haslam, C., Barnard, P., Radcliffe, P. A., Mitrophanous, K. A., Elliot, E. A. & Sang, H. M. 2007. Oviduct-specific expression of two therapeutic proteins in transgenic hens. Proc. Natl Acad. Sci. USA 104, 1771-1776.
40. Lim, J. M., Kwon, H. M., Kim, D. K., Kim, J. N., Park, T. S., Ono, T. & Han, J. Y. 2006. Selective decrease of chick embryonic primordial germ cells in vivo and in vitro by soft X-ray irradiation. Anim. Reprod. Sci. 95, 67-74.
41. Love, J., Gribbin, C., Mather, C. & Sang, H. 1994. Transgenic birds by DNA microinjection. Bio-Technology 12, 60-63.
42. Macdonald, J., Glover, J. D., Taylor, L., Sang, H. M. & McGrew, M. J. 2010. Characterisation and germline transmission of cultured avian primordial germ cells. PLoS ONE 5, e15518.
43. Macdonald, J., Taylor, L., Sherman, A., Kawakami, K., Takahashi, Y., Sang, H. M. & Mcgrew, M. J. 2012. Efficient genetic modification and germ-line transmission of primordial germ cells using piggyBac and Tol2 transposons. Proc. Natl Acad. Sci. USA 109, E1466-E1472.
44. Mahfouz, M. M., Li, L. X., Shamimuzzaman, M., Wibowo, A., Fang, X. Y. & Zhu, J. K. 2011. De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc. Natl Acad. Sci. USA 108, 2623-2628.
45. McGrew, M. J., Sherman, A., Ellard, F. M., Lillico, S. G., Gilhooley, H. J., Kingsman, A. J., Mitrophanous, K. A. & Sang, H. 2004. Efficient production of germline transgenic chickens using lentiviral vectors. EMBO Rep. 5, 728-733.
46. Meng, X. D., Noyes, M. B., Zhu, L. H. J., Lawson, N. D. & Wolfe, S. A. 2008. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat. Biotechnol. 26, 695-701.
47. 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., Dulay, G. P., Hua, K. L., Ankoudinova, I., Cost, G. J., Urnov, F. D., Zhang, H. S., Holmes, M. C., Zhang, L., Gregory, P. D. & Rebar, E. J. 2011. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143-148.
48. Minczuk, M., Papworth, M. A., Miller, J. C., Murphy, M. P. & Klug, A. 2008. Development of a single-chain, quasi-dimeric zinc-finger nuclease for the selective degradation of mutated human mitochondrial DNA. Nucleic Acids Res. 36, 3926-3938.
49. Mitchell, R. S., Beitzel, B. F., Schroder, A. R. W., Shinn, P., Chen, H. M., Berry, C. C., Ecker, J. R. & Bushman, F. D. 2004. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol. 2, 1127-1137.
50. Mizuarai, S., Ono, K., Yamaguchi, K., Nishijima, K., Kamihira, M. & Iijima, S. 2001. Production of transgenic quails with high frequency of germ-line transmission using VSV-G pseudotyped retroviral vector. Biochem. Biophys. Res. Commun. 286, 456-463.
51. Moscou, M. J. & Bogdanove, A. J. 2009. A simple cipher governs DNA recognition by TAL effectors. Science 326, 1501.
52. Motono, M., Ohashi, T., Nishijima, K. & Iijima, S. 2008. Analysis of chicken primordial germ cells. Cytotechnology 57, 199-205.
53. Motono, M., Yamada, Y., Hattori, Y., Nakagawa, R., Nishijima, K. & Iijima, S. 2010. Production of transgenic chickens from purified primordial germ cells infected with a lentiviral vector. J. Biosci. Bioeng. 109, 315-321.
54. Mozdziak, P. E., Borwornpinyo, S., Mccoy, D. W. & Petitte, J. N. 2003. Development of transgenic chickens expressing bacterial beta-galactosidase. Dev. Dyn. 226, 439-445.
55. Mozdziak, P. E., Wysocki, R., Angerman-Stewart, J., Pardue, S. L. & Petitte, J. N. 2006. Production of chick germline chimeras from fluorescence-activated cell-sorted gonocytes. Poult. Sci. 85, 1764-1768.
56. Mussolino, C., Morbitzer, R., Lutge, F., Dannemann, N., Lahaye, T. & Cathomen, T. 2011. A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res. 39, 9283-9293.
57. Naito, M., Matsubara, Y., Harumi, T., Tagami, T., Kagami, H., Sakurai, M. & Kuwana, T. 1999. Differentiation of donor primordial germ cells into functional gametes in the gonads of mixed-sex germline chimaeric chickens produced by transfer of primordial germ cells isolated from embryonic blood. J. Reprod. Fertil. 117, 291-298.
58. Naito, M., Sakurai, M. & Kuwana, T. 1998. Expression of exogenous DNA in the gonads of chimaeric chicken embryos produced by transfer of primordial germ cell transfected in vitro and subsequent fate of the introduced DNA. J. Reprod. Fertil. 113, 137-143.
59. Nakamura, Y., Usui, F., Atsumi, Y., Otomo, A., Teshima, A., Ono, T., Takeda, K., Nirasawa, K., Kagami, H. & Tagami, T. 2009. Effects of busulfan sustained-release emulsion on depletion and repopulation of primordial germ cells in early chicken embryos. J. Poult. Sci. 46, 127-135.
60. Naldini, L., Blomer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F. H., Verma, I. M. & Trono, D. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267.
61. Oishi, I. 2010. Improvement of transfection efficiency in cultured chicken primordial germ cells by percoll density gradient centrifugation. Biosci. Biotechnol. Biochem. 74, 2426-2430.
62. Pain, B., Clark, M. E., Shen, M., Nakazawa, H., Sakurai, M., Samarut, J. & Etches, R. J. 1996. Long-term in vitro culture and characterisation of avian embryonic stem cells with multiple morphogenetic potentialities. Development 122, 2339-2348.
63. Park, S. H., Kim, J. N., Park, T. S., Lee, S. D., Kim, T. H., Han, B. K. & Han, J. Y. 2010. CpG methylation modulates tissue-specific expression of a transgene in chickens. Theriogenology 74, 805-816.
64. Park, T. S. & Han, J. Y. 2012. piggyBac transposition into primordial germ cells is an efficient tool for transgenesis in chickens. Proc. Natl Acad. Sci. USA 109, 9337-9341.
65. Petitte, J. N. & Mozdziak, P. E. 2007. The incredible, edible, and therapeutic egg. Proc. Natl Acad. Sci. USA 104, 1739-1740.
66. Porteus, M. H. 2006. Mammalian gene targeting with designed zinc finger nucleases. Mol. Ther. 13, 438-446.
67. Pruett-Miller, S. M., Connelly, J. P., Maeder, M. L., Joung, J. K. & Porteus, M. H. 2008. Comparison of zinc finger nucleases for use in gene targeting in mammalian cells. Mol. Ther. 16, 707-717.
68. Rapp, J. C., Harvey, A. J., Speksnijder, G. L., Hu, W. & Ivarie, R. 2003. Biologically active human interferon α-2b produced in the egg white of transgenic hens. Transgenic Res. 12, 569-575.
69. Reynaud, G. 1976. Localization study of primordial germ-cells in embryos of Japanese quail by means of ultraviolet-irradiation. Comptes Rendus Hebdomadaires Des Seances De L Academie Des Sciences Serie D 282, 1195-1198.
70. Rudolph, N. S. 1999. Biopharmaceutical production in transgenic livestock. Trends Biotechnol. 17, 367-374.
71. Salter, D. W., Smith, E. J., Hughes, S. H., Wright, S. E., Fadly, A. M., Witter, R. L. & Crittenden, L. B. 1986. Gene insertion into the chicken germ line by retroviruses. Poult. Sci. 65, 1445-1458.
72. Salter, D. W., Smith, E. J., Hughes, S. H., Wright, S. E. & Crittenden, L. B. 1987. Transgenic chickens: insertion of retroviral genes into the chicken germ line. Virology 157, 236-240.
73. Sang, H. 1994. Transgenic chickens - methods and potential applications. Trends Biotechnol. 12, 415-420.
74. Sang, H. 2004. Prospects for transgenesis in the chick. Mech. Dev. 121, 1179-1186.
75. Sato, Y., Poynter, G., Huss, D., Filla, M. B., Czirok, A., Rongish, B. J., Little, C. D., Fraser, S. E. & Lansford, R. 2010. Dynamic analysis of vascular morphogenesis using transgenic quail embryos. PLoS ONE 5, e12674.
76. Schlegel, R., Tralka, T. S., Willingham, M. C. & Pastan, I. 1983. Inhibition of VSV binding and infectivity by phosphatidylserine: is phosphatidylserine a VSV-binding site? Cell 32, 639-646.
77. Scott, B. B. & Lois, C. 2005. Generation of tissue-specific transgenic birds with lentiviral vectors. Proc. Natl Acad. Sci. USA 102, 16443-16447.
78. Sherman, A., Dawson, A., Mather, C., Gilhooley, H., Li, Y., Mitchell, R., Finnegan, D. & Sang, H. 1998. Transposition of the Drosophila element mariner into the chicken germ line. Nat. Biotechnol. 16, 1050-1053.
79. Shin, S. S., Kim, T. M., Kim, S. Y., Kim, T. W., Seo, H. W., Lee, S. K., Kwon, S. C., Lee, G. S., Kim, H., Lim, J. M. & Han, J. Y. 2008. Generation of transgenic quail through germ cell-mediated germline transmission. FASEB J. 22, 2435-2444.
80. Simkiss, K. 1991. Primordial germ cells and the scope for genetic manipulation using embryos. In Avian Incubation (ed. T. S.), Butterworth-Heinemann, London 125-136.
81. Smith, K. & Spadafora, C. 2005. Sperm-mediated gene transfer: applications and implications. BioEssays 27, 551-562.
82. Stebler, J., Spieler, D., Slanchev, K., Molyneaux, K. A., Richter, U., Cojocaru, V., Tarabykin, V., Wylie, C., Kessel, M. & Raz, E. 2004. Primordial germ cell migration in the chick and mouse embryo: the role of the chemokine SDF-1/CXCL12. Dev. Biol. 272, 351-361.
83. Suzuki, Y. & Craigie, R. 2007. The road to chromatin - nuclear entry of retroviruses. Nat. Rev. Microbiol. 5, 187-196.
84. Tagami, T. & Kagami, H. 1998. Developmental origin of avian primordial germ cells and its unique differentiation in the gonads of mixed-sex chimeras. Mol. Reprod. Dev. 50, 370-376.
85. Thoraval, P., Afanassieff, M., Cosset, F. L., Lasserre, F., Verdier, G., Coudert, F. & Dambrine, G. 1995. Germline transmission of exogenous genes in chickens using helper-free ecotropic avian leukosis virus-based vectors. Transgenic Res. 4, 369-377.
86. Tsunekawa, N., Naito, M., Sakai, Y., Nishida, T. & Noce, T. 2000. Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127, 2741-2750.
87. Tzfira, T., Weinthal, D., Marton, I., Zeevi, V., Zuker, A. & Vainstein, A. 2012. Genome modifications in plant cells by custom-made restriction enzymes. Plant Biotechnol. J. 10, 373-389.
88. Urnov, F. D., Rebar, E. J., Holmes, M. C., Zhang, H. S. & Gregory, P. D. 2010. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646.
89. van de Lavoir, M. C., Collarini, E. J., Leighton, P. A., Fesler, J., Lu, D. R., Harriman, W. D., Thiyagasundaram, T. S. & Etches, R. J. 2012. Interspecific germline transmission of cultured primordial germ cells. PLoS ONE 7, e35664.
90. van de Lavoir, M. C., Diamond, J. H., Leighton, P. A., Mather-Love, C., Heyer, B. S., Bradshaw, R., Kerchner, A., Hooi, L. T., Gessaro, T. M., Swanberg, S. E., Delany, M. E. & Etches, R. J. 2006a. Germline transmission of genetically modified primordial germ cells. Nature 441, 766-769.
91. van de Lavoir, M. C., Mather-Love, C., Leighton, P., Diamond, J. H., Heyer, B. S., Roberts, R., Zhu, L., Winters-Digiacinto, P., Kerchner, A., Gessaro, T., Swanberg, S., Delany, M. E. & Etches, R. J. 2006b. High-grade transgenic somatic chimeras from chicken embryonic stem cells. Mech. Dev. 123, 31-41.
92. Vick, L., Li, Y. & Simkiss, K. 1993. Transgenic birds from transformed primordial germ cells. Proc. Biol. Sci. 251, 179-182.
93. Wood, A. J., Lo, T. W., Zeitler, B., Pickle, C. S., Ralston, E. J., Lee, A. H., Amora, R., Miller, J. C., Leung, E., Meng, X. D., Zhang, L., Rebar, E. J., Gregory, P. D., Urnov, F. D. & Meyer, B. J. 2011. Targeted genome editing across species using ZFNs and TALENs. Science 333, 307.
94. Wu, X. L., Li, Y., Crise, B. & Burgess, S. M. 2003. Transcription start regions in the human genome are favored targets for MLV integration. Science 300, 1749-1751.
95. Yasuda, Y., Tajima, A., Fujimoto, T. & Kuwana, T. 1992. A method to obtain avian germ-line chimaeras using isolated primordial germ cells. J. Reprod. Fertil. 96, 521-528.
96. Young, J. J., Cherone, J. M., Doyon, Y., Ankoudinova, I., Faraji, F. M., Lee, A. H., Ngo, C., Guschin, D. Y., Paschon, D. E., Miller, J. C., Zhang, L., Rebar, E. J., Gregory, P. D., Urnov, F. D., Harland, R. M. & Zeitler, B. 2011. Efficient targeted gene disruption in the soma and germ line of the frog Xenopus tropicalis using engineered zinc-finger nucleases. Proc. Natl Acad. Sci. USA 108, 7052-7057.
97. Zhao, D. F. & Kuwana, T. 2003. Purification of avian circulating primordial germ cells by Nycodenz density gradient centrifugation. Br. Poult. Sci. 44, 30-35.
98. Zhu, L., van de Lavoir, M. C., Albanese, J., Beenhouwer, D. O., Cardarelli, P. M., Cuison, S., Deng, D. F., Deshpande, S., Diamond, J. H., Green, L., Halk, E. L., Heyer, B. S., Kay, R. M., Kerchner, A., Leighton, P. A., Mather, C. M., Morrison, S. L., Nikolov, Z. L., Passmore, D. B., Pradas-Monne, A., Preston, B. T., Rangan, V. S., Shi, M., Srinivasan, M., White, S. G., Winters-Digiacinto, P., Wong, S., Zhou, W. & Etches, R. J. 2005. Production of human monoclonal antibody in eggs of chimeric chickens. Nat. Biotechnol. 23, 1159-1169.