Long-term culture of chicken primordial germ cells isolated from embryonic blood and production of germline chimaeric chickens

Animal Reproduction Science

Volumn 153, Issue , 2015, Pages 50-61

  Naito, Mitsuru ^a   Harumi, Takashi ^a   Kuwana, Takashi ^b  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b International Institute of Avian Conservation Science   (United Arab Emirates)

Author keywords

Chicken; Culture; Embryo; Germline chimaera; Primordial germ cell

Indexed keywords

GALLUS GALLUS;

ANIMAL; BLOOD CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CHICK EMBRYO; CHICKEN; CHIMERA; CYTOLOGY; FEMALE; GERM CELL; MALE; PRIMARY CELL CULTURE; PROCEDURES; VETERINARY;

ANIMALS; BLOOD CELLS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHICK EMBRYO; CHICKENS; CHIMERA; FEMALE; GERM CELLS; MALE; PRIMARY CELL CULTURE;

EID: 84921327333     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2014.12.003     Document Type: Article

References (50)

1. Aige-Gil V., Simkiss K. Sterilising embryos for transgenic chimaeras. Br. Poult. Sci. 1991, 32:427-438.
2. Bresler M., Behnam J., Luke G., Simkiss K. Manipulations of germ-cell populations in the gonad of the fowl. Br. Poult. Sci. 1994, 35:241-247.
3. Carsience R.S., Clark M.E., Verrinder Gibbins A.M., Etches R.J. Germline chimeric chickens from dispersed donor blastodermal cells and compromised recipient embryos. Development 1993, 117:669-675.
4. Choi J.W., Lee E.Y., Shin J.H., Zheng Y., Cho B.W., Kim J.K., Han J.Y. Identification of breed-specific DNA polymorphisms for a simple and unambiguous screening system in germline chimeric chickens. J. Exp. Zool. 2007, 307A:241-248.
5. Choi J.W., Kim S., Kim T.M., Kim Y.M., Seo H.W., Park T.S., Jeong J.W., Song G., Han J.Y. Basic fibroblast growth factor activates Mek/Erk cell signaling pathway and stimulates the proliferation of chicken primordial germ cells. PLoS ONE 2010, 5(9):e12968. 10.1371/journal.pone.0012968.
6. Clinton M., Haines L., Belloir B., McBride D. Sexing chick embryos: a rapid and simple protocol. Br. Poult. Sci. 2001, 42:134-138.
7. Eyal-Giladi H., Kochav S. 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. 1976, 49:321-337.
8. Freshney R.I. Culture of Animal Cells 1987, 245-256. Alan R Liss, New York. second ed.
9. Glover J.D., McGrew M.J. Primordial germ cell technologies for avian germplasm cryopreservation and investigating germ cell development. J. Poult. Sci. 2012, 49:155-162.
10. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. J. Morphol. 1951, 8:49-92.
11. Kang S.J., Choi J.W., Kim S.Y., Park K., Kim T.M., Lee Y.M., Kim H., Lim J.M., Han J.Y. Reproduction of wild birds via interspecies germ cell transplantation. Biol. Reprod. 2008, 79:931-937.
12. Kerje S., Sharma P., Gunnarsson U., Kim H., Bagchi S., Fredriksson R., Schutz K., Jensen P., von Heijine G., Okimoto R., Andersson L. The Dominant white, Dun and Smoky color variants in chicken are associated with insertion/deletion polymorphisms in the PMEL17 gene. Genetics 2004, 168:1507-1518.
13. Kuwana T. Migration of avian primordial germ cells toward the gonadal anlage. Dev. Growth Differ. 1993, 35:237-243.
14. Kuwana T., Hashimoto K., Nakanishi A., Yasuda Y., Tajima A., Naito M. Long-term culture of avian embryonic cells in vitro. Int. J. Dev. Biol. 1996, 40:1061-1064.
15. Li H.C., Kagami H., Matsui K., Ono T. Restriction of proliferation of primordial germ cells by the irradiation of Japanese quail embryos with soft X-rays. Comp. Biochem. Physiol. A 2001, 130:133-140.
16. Liu C., Khazanehdari K.A., Baskar V., Saleem S., Kinne J., Wernery U., Chang I.K. Production of chicken progeny (Gallus gallus domesticus) from interspecies germline chimeric duck (Anas domesticus) by primordial germ cell transfer. Biol. Reprod. 2012, 86:101-108.
17. Macdonald J., Glover J.D., Taylor L., Sang H.M., McGrew M.J. Characterisation and germline transmission of cultured avian primordial germ cells. PLoS ONE 2010, 5(11):e15518. 10.1371/journal.pone.0015518.
18. Macdonald J., Taylor L., Sherman A., Kawakami K., Takahashi Y., Sang H.M., McGrew M.J. Efficient genetic modification and germ-line transmission of primordial germ cells using piggyBac and Tol2 transposons. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(23):E1466-E1472.
19. Matsui Y., Tokitake Y. Primordial germ cells contain subpopulations that have greater ability to develop into pluripotential stem cells. Dev. Growth Differ. 2009, 51:657-667.
20. Miyahara D., Mori T., Makino R., Nakamura Y., Oishi I., Ono T., Nirasawa K., Tagami T., Kagami H. Culture conditions for maintain propagation, long-term survival and germline transmission of chicken primordial germ cell-like cells. J. Poult. Sci. 2014, 51:87-95.
21. Naito M. Genetic manipulation in chickens. World's Poult. Sci. J. 2003, 59:375-385.
22. Naito M. Embryo manipulation in chickens. J. Poult. Sci. 2015, 52:7-14.
23. Naito M., Nirasawa K., Oishi T. Development in culture of the chick embryo from fertilized ovum to hatching. J. Exp. Zool. 1990, 254:322-326.
24. Naito M., Watanabe M., Kinutani M., Nirasawa K., Oishi T. Production of quail-chick chimaeras by blastoderm cell transfer. Br. Poult. Sci. 1991, 32:79-86.
25. Naito M., Tajima A., Yasuda Y., Kuwana T. Production of germline chimeric chickens with high transmission rate of donor-derived gametes, produced by transfer of primordial germ cells. Mol. Reprod. Dev. 1994, 39:153-161.
26. Naito M., Tajima A., Tagami T., Yasuda Y., Kuwana T. Preservation of chick primordial germ cells in liquid nitrogen and subsequent production of viable offspring. J. Reprod. Fertil. 1994, 102:321-325.
27. Naito M., Tajima A., Yasuda Y., Kuwana T. Donor primordial germ cell-derived offspring from recipient germline chimaeric chickens: absence of long term immune rejection and effects on sex ratios. Br. Poult. Sci. 1998, 39:20-23.
28. Naito M., Sakurai M., Kuwana T. 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 introduced DNA. J. Reprod. Fertil. 1998, 113:137-143.
29. Naito M., Matsubara Y., Harumi T., Tagami T., Kagami H., Sakurai M., Kuwana T. 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. 1999, 117:291-298.
30. Naito M., Sano A., Harumi T., Matsubara Y., Kuwana T. Migration of primordial germ cells isolated from embryonic blood into the gonads after transfer to stage X blastoderms and detection of germline chimaerism by PCR. Br. Poult. Sci. 2004, 45:762-768.
31. Naito M., Minematsu T., Harumi T., Kuwana T. Intense expression of GFP gene in gonads of chicken embryos by transfecting circulating primordial germ cells in vitro and in vivo. J. Poult. Sci. 2007, 44:416-425.
32. Naito M., Harumi T., Kuwana T. Long term in vitro culture of chicken primordial germ cells isolated from embryonic blood and incorporation into germline of recipient embryo. J. Poult. Sci. 2010, 47:57-64.
33. Naito M., Harumi T., Kuwana T. In vitro culture of testicular and ovarian gonocytes obtained from 19-day incubated chicken embryos and subsequent colonization into gonads of recipient embryos. J. Poult. Sci. 2011, 48:112-118.
34. Naito M., Harumi T., Kuwana T. Expression of GFP gene in cultured PGCs isolated from embryonic blood and incorporation into gonads of recipient embryos. J. Poult. Sci. 2012, 49:116-123.
35. Nakamichi H., Sano A., Harumi T., Matsubara Y., Tajima A., Kosugiyama M., Naito M. Effects of soft X-ray irradiation to stage X blastoderm on restriction of proliferation of primordial germ cells in early chicken embryos. J. Poult. Sci. 2006, 43:394-400.
36. Nakamura Y., Usui F., Atsumi Y., Otomo A., Teshima A., Ono T., Takeda K., Nirasawa K., Kagami H., Tagami T. Effects of busulfan sustained-release emulsion on depletion and repopulation of primordial germ cells in early chicken embryos. J. Poult. Sci. 2009, 46:127-135.
37. Nakamura Y., Usui F., Ono T., Takeda K., Nirasawa K., Kagami H., Tagami T. Germline replacement by transfer of primordial germ cells into partially sterilized embryos in the chicken. Biol. Reprod. 2010, 83:130-137.
38. Park T.S., Han J.Y. PiggyBac transposition into primordial germ cells is an efficient tool for transgenesis in chickens. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:9337-9341.
39. Park T.S., Han J.Y. Conservation of migration and differentiation circuits in primordial germ cells between avian species. J. Reprod. Dev. 2013, 59:252-257.
40. Perry M.M. A complete culture system for the chick embryo. Nature 1988, 331:70-72.
41. Raynaud G. Reproductive capacity and offspring of chickens submitted to transfer of primordial germ cells during embryonic life. Roux's Arch. Dev. Biol. 1976, 179:85-110.
42. Song Y., D'Costa S., Pardue S.L., Petitte J.N. Production of germline chimeric chickens following the administration of a busulfan emulsion. Mol. Reprod. Dev. 2005, 70:438-444.
43. Tajima A., Naito M., Yasuda Y., Kuwana T. Production of germ line chimera by transfer of primordial germ cells in domestic chicken (Gallus domesticus). Theriogenology 1993, 40:509-519.
44. Tajima A., Naito M., Yasuda Y., Kuwana T. Production of germ-line chimeras by transfer of cryopreserved gonadal primordial germ cells (gPGCs) in chicken. J. Exp. Zool. 1998, 280:265-267.
45. Tajima A., Hayashi H., Kamizumi A., Ogura J., Kuwana T., Chikamune T. Study on the concentration of circulating primordial germ cells (cPGCs) in early chick embryos. J. Exp. Zool. 1999, 284:759-764.
46. Tsunekawa N., Naito M., Sakai Y., Nishida T., Noce T. Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 2000, 127:2741-2750.
47. 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. Germline transmission of genetically modified primordial germ cells. Nature 2006, 441:766-769.
48. 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. Interspecific germline transmission of cultured primordial germ cells. PLoS ONE 2012, 7(5):e35664. 10.1371/journal.pone.0035664.
49. Wernery U., Liu C., Baskar V., Guerineche Z., Khazanehdari K.A., Saleem S., Kinne J., Wernery R., Griffin D.K., Chang I.K. Primordial germ cell-mediated chimera technology produces viable pure-line Houbara Bustard offspring: potential for repopulating an endangered species. PLoS ONE 2010, 5(12):e15824. 10.1371/journal.pone.0015824.
50. Zhao D.F., Kuwana T. Purification of avian circulating primordial germ cells by Nycodenz density gradient centrifugation. Br. Poult. Sci. 2003, 44:30-35.