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Genetic manipulation in chickens

Published online by Cambridge University Press:  18 September 2007

M. Naito
M. Naito
Affiliation:
National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan, e-mail: mnaito@affrc.go.jp
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Abstract

Development of chicken embryo culture techniques provides precise methods for the manipulation of early chicken embryos and has made it possible to analyse the results of themanipulation in hatched chickens. Various attempts have been made to introduce exogenous DNA into the chicken germline, but an efficient method for producing transgenic chickensby non-viral methods has not yet been devised. Since the system for producing germline cimaeric chickens has been established by the transfer of primordial germ cells isolated from early stage embryos, manipulation of primordial germ cells seems to be one of the mostpromising methods for genetic manipulation in chickens.

Keywords

blastodermembryo manipulationgermline chimaeraprimordial germ celltransgenesis
Type
Reviews
Information
World's Poultry Science Journal , Volume 59 , Issue 3 , September 2003 , pp. 361 - 371
Copyright
Copyright © Cambridge University Press 2003

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References

Abinawanto, , Zhang, C., Saito, N., Matsuda, Y. and Shimada, K. (1998) Identification of sperm-bearing female-specific chromosome in the sex-reversed chicken. Journal of Experimental Zoology 280: 65–72.3.0.CO;2-F>CrossRefGoogle ScholarPubMed
Bacon, L.D., Zajchowski, L., Clark, M.E. and Etches, R.J. (2002) Identification and evaluation of major histocompatibility complex antigens in chicken chimeras and their relationship to germline transmission. Poultry Science 81: 1427–1438.CrossRefGoogle ScholarPubMed
Brazolot, C.L., Petitte, J.N., Etches, R.J. and Verrinder Gibbins, A.M. (1991) Efficient transfection of chicken cells by lipofection, and introduction of transfected blastodermal cells into the embryo. Molecular Reproduction and Development 30: 304–312.CrossRefGoogle ScholarPubMed
Carsience, R.S., Clark, M.E., Verrinder Gibbins, A.M. and Etches, R.J. (1993) Germline chimeric chickens from dispersed donor blastodermal cells and compromised recipient embryos. Development 117: 669–675.CrossRefGoogle ScholarPubMed
Chang, I.K., Jeong, D.K., Hong, Y.H., Park, T.S., Moon, Y.K., Ohno, T. and Han, J.Y. (1997). Production of germline chimeric chickens by transfer of cultured primordial germ cells. Cell Biology International 21: 495–499.CrossRefGoogle ScholarPubMed
Chang, K., Qian, J., Jiang, M.-S., Liu, Y.-H, Wu, M.-C., Chen, C.-D., Lai, C.-K., Lo, H.-L., Hsiao, C.-T., Brown, L., Bolen, J. Jr., Huang, H.-I., Ho, P.-Y., Shih, P.-Y., Yao, C.-W., Lin, W.-J., Chen, C.-H., Wu, F.-Y., Lin, Y.-J., Xu, J. and Wang, K. (2002) Effective generation of transgenic pigs and mice by linker based sperm-mediated gene transfer. BioMed Central Biotechnology 2: 5 (manuscript PDF).Google ScholarPubMed
Clinton, M. (1994) A rapid protocol for sexing chick embryos (Gallus g. domesticus). Animal Genetics 25: 361–362.CrossRefGoogle ScholarPubMed
Clinton, M., Haines, L., Belloir, B. and Mcbride, D. (2001) Sexing chick embryos: a rapid and simple protocol. British Poultry Science 42: 134–138.CrossRefGoogle ScholarPubMed
Etches, R.J., Carsience, R.S., Fraser, R.M., Clark, M.E., Toner, A. and Verrinder Gibbins, A.M. (1993) Avian chimeras and their use in manipulation of the avian genome. Poultry Science 72: 882–889.CrossRefGoogle Scholar
Etches, R.J., Clark, M.E., Toner, A., Liu, G. and Verrinder Gibbins, A.M. (1996) Contributions to somatic and germline lineages of chicken blastodermal cells maintained in culture. Molecular Reproductionand Development 45: 291–298.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Etches, R.J., Clark, M.E., Zajchowski, L., Speksnijder, G., Verrinder Gibbins, A.M., Kino, K., Pain, B. and Samarut, J. (1997) Manipulation of blastodermal cells. Poultry Science 76: 1075–1083.CrossRefGoogle ScholarPubMed
Eyal-Giladi, H. and 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. Developmental Biology 49: 321–337.CrossRefGoogle Scholar
Fraser, R.A., Carsience, R.S., Clark, M.E., Etches, R.J. and Verrinder Gibbins, A.M. (1993) Efficient incorporation of transfected blastodermal cells into chimeric chicken embryos. International Journal of Developmental Biology 37: 381–385.Google ScholarPubMed
Ginsburg, M. (1994) Primordial germ cell formation in birds. In Ciba Foundation Symposium 182, Germline Development (Marsh, J. and Goode, J., Eds) John Wiley and Sons, Chahester, UK. pp. 52–67.Google Scholar
Hamburger, V. and Hamilton, H.L. (1951) A series of normalages in the development of the chick embryo. Journal of Morphology 8: 49–92.CrossRefGoogle Scholar
Han, J.Y., Park, T.S., Hong, Y.H., Jeong, D.K., Kim, J.N., Kim, K.D. and Lim, J.M. (2002) Production of germline chimeras by transfer of chicken gonadal primordial germ cells maintained in vitro for an extended period. Theriogenology 58: 1531–1539.CrossRefGoogle ScholarPubMed
Harvey, A.J., Speksnijder, G., Baugh, L.R., Morris, J.A. and Ivarie, R. (2002a) Consistent production of transgenic chickens using replication-deficient retroviral vectors and high-throughput screening procedures. Poultry Science 81: 202–212.CrossRefGoogle ScholarPubMed
Harvey, A.J., Speksnijder, G., Baugh, L.R., Morris, J.A. and Ivarie, R. (2002b) Expression of exogenous protein in the egg white of transgenic chickens. Nature Biotechnology 19: 396–399.CrossRefGoogle Scholar
Hong, Y.H., Moon, Y.K., Jeong, D.K. and Han, J.Y. (1998) Improved transfection efficiency of chicken gonadal primordial germ cells for the production of transgenic poultry. Transgenic Research 7: 247–252.CrossRefGoogle ScholarPubMed
Ivarie, R. (2003) Avian transgenesis: Progress towards the promises. Trends in Biotechnology 21: 14–19.CrossRefGoogle Scholar
Jeong, D.K. and Han, J.Y. (2002) Migration activity of chicken gonadal primordial germ cells (gPGCs) and post-transfer localization of lacZ-translected gPGCs in the embryonic gonads. Asian-Australasian Journal of Animal Sciences 15: 1227–1231.CrossRefGoogle Scholar
Kagami, H. (2002) Developmental genetic analysis of the avian primordial germ cells and the application for production of chimeric chickens. Journal of Poultry Science 39: 131–139.CrossRefGoogle Scholar
Kagami, H., Clark, M.E., Verrinder Gibbins, A.M. and Etches, R.J. (1995) Sexual differentiation of chimeric chickens containing ZZ and ZW cells in the germ-line. Molecular Reproduction and Development 42: 379–387.CrossRefGoogle Scholar
Kagami, H., Tagami, T., Matsubara, Y., Harumi, T., Hanada, H., Maruyama, K., Sakurai, M., Kuwana, T. and 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 offspringin the chicken. Molecular Reproduction and Development 48: 501–510.3.0.CO;2-W>CrossRefGoogle Scholar
Kagami, H., Iwata, J., Yasuda, J. and Ono, T. (2002) Strain preference in donor and recipient for production of W-bearing sperm in mixed-sex germline chimeric chickens. Comparative Biochemistry and Physiology Part A 131: 287–292.CrossRefGoogle ScholarPubMed
Kagami, H., Yasuda, J., Tagami, T., Naito, M., Matsubara, Y., Harumi, T., Noguchi, T., Yamamoto, Y., Takahashi, T., Matsuyama, J., Komatsu, H. and Ono, T. (2003) Effect of the strain combination of the donor and recipient on the production efficiency of W-bearing sperm in mixed-sex germline chimeric chickens. Animal ScienceJournal 73: 453–456.Google Scholar
Karagenc, L., Cinnamon, Y., Ginsburg, M. and Petitte, J.N. (1996) Origin of primordial germ cells in the prestreak chick embryo. Developmental Genetics 19: 290–301.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Klein, S. and Ellendorff, F. (1998) Analysis of chicken embryonic development after removal of blastodermal cells for sexing. British Poultry Science 39: 482–487.CrossRefGoogle ScholarPubMed
Klein, S. and Ellendorff, F. (2000) Localization of XhoI repetitive sequences on the autosomes in addition to the W chromosome in chickens and its relevance for sex diagnosis. Animal Genetics 31: 104–109.CrossRefGoogle Scholar
Kuwana, T. (1993) Migration of avian primordial germ cells toward the gonadal anlage. Development Growth and Differentiation 35: 237–243.CrossRefGoogle ScholarPubMed
Li, Y., Behnam, J. and Simkiss, K. (1995) Ballistic transfection of avian primordial germ cells in ovo. Transgenic Research 4:CrossRefGoogle ScholarPubMed
Love, J., Gribbin, C., Mather, C. and Sang, H. (1994) Transgenic birds by DNA microinjection. Bio/technology 12: 60–63.Google ScholarPubMed
Mizuno, S., Saitoh, Y., Nomura, O., Kunita, R., Ohtomo, K., Nishimori, K., Ono, H. and Saitoh, H. (1993) Sex-specific DNA sequence in galliformes and their application to the study of sex differentiation. In Manipulation of the Avian Genome (Etches, R.J. and Verrinder Gibbins, A.M., Eds) CRC Press, Boca Raton, USA. pp. 257–274.Google Scholar
Mozdziak, P.E., Borwornpinyo, S., Mccoy, D. W. and Petitte, J.N. (2003) Development of transgenic chickens expressing bacterial β-galactosidase. Developmental Dynamics 226: 439–445.CrossRefGoogle ScholarPubMed
Muramatsu, T., Mizutani, Y., Ohmori, Y. and Okumura, J. (1997) Comparison of three nonviral transfection methods for foreign gene expression in early chicken embryos in ovo. Biochemical and Biophysical Communications 230: 376–380.CrossRefGoogle ScholarPubMed
Muramatsu, T., Nakamura, A. and Park, H.-M. (1998) In vivo electroporation: a powerful and convenient means of nonviral gene transfer to tissues of living animals (Review). International Journal of Molecular Medicine 1: 55–62.Google Scholar
Naito, M. (1997) The microinjection of DNA into early chicken embryo. In transgenic animals: Generation and use (Houdebine, L.M., Ed) Harwood Academic Publishers. The Netherlands. pp. 69–73.Google Scholar
Naito, M. (1998) Manipulation of primordial germ cells for avian transgenesis. AgBiotech News and Information 10: 397–404.Google Scholar
Naito, M. (2003a) Cryopreservation of avian germline cells and subsequent production of viable offspring. Journal of Poultry Science 40: 1–12.CrossRefGoogle Scholar
Naito, M. (2003b) Development of avian embryo manipulation techniques and their application to germ cell manipulation. Animal Science Journal 74: 157–168.CrossRefGoogle Scholar
Naito, M. and Perry, M.M. (1989). Development in culture of the chick embryo from cleavage to hatch. British Poultry Science 30: 251–256.CrossRefGoogle ScholarPubMed
Naito, M., Nirasawa, K. and Oishi, T. (1990) Development in culture of the chick embryo from fertilized ovum to hatching. Journal of experimental Zoology 254: 322–326.CrossRefGoogle ScholarPubMed
Naito, M., Agata, K., Otsuka, K., Kino, K., Ohta, M., Hirose, K., Perry, M.M. and Eguchi, G. (1991a). Embryonic expression of βactin-lacZ hybrid gene injected into the fertilized ovum of the domestic fowl. International Journal of Developmental Biology 35: 69–75.Google ScholarPubMed
Naito, M., Watanabe, M., Kinutani, M., Nirasawa, K. and Oishi, T. (1991b) Production of quail-chick chimaeras by blastodermcell transfer. British Poultry Science 32: 79–86.CrossRefGoogle ScholarPubMed
Naito, M., Nirasawa, K. and Oishi, T. (1992) Preservation of quail blastoderm cells in liquid nitrogen. British Poultry Science 33: 449–453.CrossRefGoogle ScholarPubMed
Naito, M., Sasaki, E., Ohtaki, M. and Sakurai, M. (1994a). Introduction of exogenous DNA into somatic and germ cells of chickens bymicroinjection into the germinal disc of fertilized ova. Molecular Reproduction and Development 37: 167–171.CrossRefGoogle ScholarPubMed
Naito, M., Tajima, A., Yasuda, Y. and Kuwana, T. (1994b) Production of germline chimeric chickens, with high transmission rate of donor-derived gametes, produced by transfer of primordial germ cells. Molecular Reproduction and Development 39: 153–161.CrossRefGoogle ScholarPubMed
Naito, M., Tajima, A., Tagami, T., Yasuda, Y. and Kuwana, T. (1994c) Preservation of chick primordial germ cells in liquid nitrogen and subsequent production of viable offspring. Journal of Reproduction and Fertility 102: 321–325.CrossRefGoogle ScholarPubMed
Naito, M., Nirasawa, K. and Oishi, T. (1995) An in vitro culture method for chick embryos obtained from the anterior portion of the magnum of oviduct. British Poultry Science 36: 161–164.CrossRefGoogle Scholar
Naito, M., Sakurai, M. and Kuwana, T. (1998a) Expression of exogenous DNA in the gonads of chimaeric chicken embryos produced by transfer of primordial germ cells transfected in vitro and subsequent fate of the introducedDNA. Journal of reproduction and Fertility 113: 137–143.CrossRefGoogle Scholar
Naito, M., Tajima, A., Yasuda, Y. and Kuwana, T. (1998b) Donor primordial germ cell-derived offspring from recipient germline chimaeric chickens: absence of long term immune rejection and effects sex ratios. British Poultry Science 39: 20–23.CrossRefGoogle ScholarPubMed
Naito, M., Matsubara, Y., Harumi, T., Tagami, T., Kagami, H., Sakurai, M. and Kuwana, T. (1999). Differentiation of donor primordial germ cells into functional gametes in the gonads mixed-sex germline chimaeric chickens produced by transfer of primordial germ cells isolated embryonic blood. Journal of Reproduction and Fertility 117: 291–298.CrossRefGoogle ScholarPubMed
Naito, M., Matsubara, Y., Harumi, T., Tagami, T., Sakurai, M. and Kuwana, T. (2000a) Foreign gene expression in the gonads of chimaeric chicken embryos by transfer of primordial germ transfected in vitro by lipofection for 24 hours. Animal Science Journal 71: 308–311.Google Scholar
Naito, M., Sano, A., Tagami, T., Harumi, T. and Matsubara, Y. (2000b). Efficient transfection chicken blastoderms in vivo by lipofection and electroporation using green fluorescent protein gene as a marker. Animal Science Journal 71: 377–385.Google Scholar
Naito, M., Sano, A., Matsubara, Y., Harumi, T., Tagami, T., Sakurai, M. and Kuwana, T. (2001a) Localization of primordial germ cells or their precursors in stage X blastoderm of chickens and thier ability to differentiate into functional gametes in opposite-sex recipient gonads. Reproduction 121: 547–552.CrossRefGoogle ScholarPubMed
Naito, M., Sano, A., Matsubara, Y., Harumi, T., Tagami, T., Sakurai, M. and Kuwana, T. (2001b) Fate of donor blastodermal cells derived from the central disc, marginal zone and area opaca transferred into the recipient embryos. Journal of Poultry Science 38: 58–61.CrossRefGoogle Scholar
Naito, M., Sano, A., Tagami, T., Harumi, T., Matsubara, Y. and Kuwana, T. (2001c) Effect mytomycin C treatment on feeder cells and the proliferation of cultured primordial germ cells isolated embryonic blood. Journal of Poultry Science 38: 343–347.CrossRefGoogle Scholar
Naito, M., Sano, A., Tagami, T., Harumi, T., Matsubara, Y. and Kuwana, T. (2002) Efficient gene transfer into earlychicken embryos by electroporation of stage X blastoderms in vivo, applying electric pulses vertically to the blastoderm layer. Journal of Poultry Science 39: 292–301.CrossRefGoogle Scholar
Naito, M., Sano, A., Kawashima, T., Nakamichi, H., Harumi, T., Matsubara, Y. and Kuwana, T. (2003) A simplemethod for sexing chicken embryos at stage X. Journal of Poultry Science 40, 226–230.CrossRefGoogle Scholar
Naito, M. and Kuwana, T. (2003) Production of chimeric chickens. In Germ Cells, Methods in Molecular Medicine (Schatten, H., Ed) Humana Press, Totowa, NJ. (in press).Google Scholar
Ochiai, H., Park, H.-M., Nakamura, A., Sasaki, R., Okumura, J.-I. and Muramatsu, T. (1998) Synthesis of human erythropoietin in vivo in the oviduct of laying hens by localized in vivo gene transfer using electroporation. Poultry Science 77: 299–302.CrossRefGoogle ScholarPubMed
Pain, B., Clark, M.E., Shen, M., Nakazawa, H., Sakurai, M., Samarut, J. and Etches, R.J. (1996) Long-term in vitro culture and characterisation of avian embryonic stem cells with multiple morphogenetic potentialities. Development 122: 2339–2348,CrossRefGoogle ScholarPubMed
Pain, B., Chenevier, P. and Samarut, J. (1999) Chicken embryonic stem cells and transgenic strategies. Cells Tissues and Organs 165: 212–219.CrossRefGoogle ScholarPubMed
Park, T.S. and Han, J.Y. (2000) Derivation and characterization of pluripotent embryonic germ cells in chicken.Molecular Reproduction and Development 56: 475–482.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Perry, M.M. (1988) A complete culture system for the chick embryo. Nature 331: 70–72.CrossRefGoogle ScholarPubMed
Perry, M., Morrice, D., Hettle, S. and Sang, H. (1991) Expression of exogenous DNA during the early development of the chick embryo. Roux'ives of Developmental Biology 200: 312–319.CrossRefGoogle ScholarPubMed
Petitte, J.N., Clark, M.E., Liu, G., Verrinder Gibbins, A.M. and Etches, R.J. (1990) Production of somatic and germline chimeras in the chicken by transfer of early blastodermal cells. Development 108: 185–189.CrossRefGoogle ScholarPubMed
Petitte, J.N., Brazolot, C.L., Clark, M.E., Liu, G., Verrinder Gibbins, A.M. and Etches, R.J. (1993 ) Accessing the genome of the chicken using germ-line chimeras. In manipulation of the avian genome(Etches, R.J. and Verrinder Gibbins, A.M. Eds) CRC Press, Boca Raton. pp.81–101.Google Scholar
Petitte, J.N. (2002) The avian germline and strategies for the production of transgenic chickens. Journal of Poultry Science 39: 205–228.CrossRefGoogle Scholar
Sang, H. and Perry, M.M. (1989). Episomal replication of cloned DNA injected into the fertilized ovum of the hen, callns domesticus. Molecular Reproduction and Development 1: 98–106.CrossRefGoogle ScholarPubMed
Sano, A., Tagami, T., Harumi, T., Matsubara, Y. and Naito, M. (2003) Introduction of exogenous DNA into gonads of chicken embryos by lipofection and electroporation of stage X blastoderms in vivo. British Poultry Science 44: 36–39.CrossRefGoogle Scholar
Sherman, A., Dawson, A., Mather, C., Gilhooley, H., Li, Y., Mitchell, R., Finnegan, D. and Sang, H. (1998) Transposition of the Drosophila element mariner into the chicken germ line. Nature Biotechnology 16: 1050–1053.CrossRefGoogle ScholarPubMed
Simkiss, K., Luke, G. and Behnam, J. (1996) Femalechromosomes in cockerel ejaculates. Proceedings of the Royal Society of London B 263: 1245–1249.Google ScholarPubMed
Speksnijder, G.J., Etches, R.J. and Verrinder Gibbins, A.M. (1999) Germline chimeric chickens from FACS-sorted donor cells. Molecular Reproduction and Development 52: 33–42.3.0.CO;2-G>CrossRefGoogle Scholar
Squires, E.J. and Drake, D. (1997) Transgenic chickens by liposonie-sperm-mediated gene transfer. in: transgenic animals: generation and use (HoudebineL.M., D L.M., D) Harwood Academic Publishers, The Netherlands. pp. 95–99.Google Scholar
Sugihara, K., Park, H.-M. and Muramatsu, T. (2000a) Foreign gene expression by in vivo gene electroporation in the quail testis. Comparative Biochemistry and Physiology Part B 125: 47–52.CrossRefGoogle ScholarPubMed
Sugihara, K., Park, H.-M. and Muramatsu, T. (2000b) In vivo gene electroporation confers strong transient expression of foreign genes in the chicken testis. Poultry Science 79: 1116–1119.CrossRefGoogle ScholarPubMed
Tagami, T., Matsubara, Y., Hanada, H. and Naito, M. (1997) Differentiation of female chicken primordial germ cells into spermatozoa in male gonads. Development Growth and Differentiation 39: 267–271.CrossRefGoogle ScholarPubMed
Tajima, A. (2002) Production of germ-line chimeras and their application in domestic chicken.Avian and Poultry Biology Reviews 13: 15–30.CrossRefGoogle Scholar
Tajima, A., Naito, M., Yasuda, Y. and Kuwana, T. (1993) Production of germ line chimera by transfer of primordial germ cells in domestic chicken (Gallus domesticus). Theriogenology 40: 509–519.CrossRefGoogle ScholarPubMed
Tajima, A., Naito, M., Yasuda, Y. and Kuwana, T. (1998) Production of germ-line chimeras by transfer of cryopreserved gonadal primordial germ cells (gPGCs) in chicken. Journal of Experimental Zoology 280: 265–267.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Tajima, A., Barbato, G.F., Kuwana, T. and Hammerstedt, R.H. (2003) Conservation of a genetically selected broiler line (42l) using cryopreserved circulating primordial germ cells (PGCs) isolated by filtration method. Journal of Poultry Science 40: 53–61.CrossRefGoogle Scholar
Tanaka, K., Wada, T., Koga, O., Nishio, Y. and Hertelendy, F. (1994) Chick production by in vitro fertilization of the fowlovum. Journal Reproduction and Fertility 100: 447–449.CrossRefGoogle Scholar
Tsunekawa, N., Naito, M., Sakai, Y., Nishida, T. and Noce, T. (2000) Isolation of chicken vasa homolog gene and tracing theorigin of primordial germ cells. Development 127: 2741–2750.CrossRefGoogle Scholar
Watanabe, M., Kinutani, M., Naito, M., Ochi, O. and Takashima, Y. (1992) Distribution analysis of transferred donor cells in avian blastodermal chimeras. Development 114: 331–338.CrossRefGoogle ScholarPubMed
Watanabe, M., Naito, M., Sasaki, E., Sakurai, M., Kuwana, T. and Oishi, T. (1994) Liposome-mediated DNA transfer into chicken primordial germ cells in vivo. Molecular Reproduction and Development 38: 268–274.CrossRefGoogle ScholarPubMed
Wei, Q., Croy, B.A. and Etches, R.J. (2001) Selection of genetically modified blastoderrnal cells by magnetic-activated cell sorting. Poultry Science 80: 1671–1678.CrossRefGoogle ScholarPubMed
Wentworth, A.L. and Wentworth, B.C. (2000) The avian primordial germ cell … an enigma of germline evolution, development and immortality. Avian and Poultry Biology Reviews 11: 173–282.Google Scholar
Yasuda, Y., Tajima, A., Fujimoto, T. and Kuwana, T. (1992) A method to obtain avian germ-line chimaeras using isolated primordial germ cells. Journal of Reproduction and Fertility 96: 521–528.CrossRefGoogle ScholarPubMed
Zaijchowski, L.D. and Etches, R.J. (2000) Transgenic chickens: past, present and future. Avian and Poultry Biology Reviews 11: 63–80.Google Scholar
Zhao, D.-F., Yamashita, H., Matsuzaki, M., Takano, T., Abe, S.-I., Naito, M. and Kuwana, T. (2003) Genetic factors affect the number of circulating primordial germ cells in early chick embryos. Journal of Poultry Science 40: 101–113.CrossRefGoogle Scholar