Characterisation and germline transmission of cultured avian primordial germ cells

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Macdonald, Joni ^a   Glover, James D ^a   Taylor, Lorna ^a   Sang, Helen M ^a   McGrew, Michael J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; STAGE SPECIFIC EMBRYO ANTIGEN 1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; BENZAMIDE DERIVATIVE; DIPHENYLAMINE; DRUG DERIVATIVE; GREEN FLUORESCENT PROTEIN; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL LINEAGE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; FOWL; GAMETE; GONAD; MEIOSIS; NONHUMAN; PRIMORDIAL GERM CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEXUAL DEVELOPMENT; ANIMAL; CELL CULTURE; CHICK EMBRYO; CYTOLOGY; DRUG EFFECT; EMBRYONIC STEM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GERM CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; METABOLISM; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL;

AVES; GALLUS GALLUS; MAMMALIA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BENZAMIDES; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; CHICK EMBRYO; DIPHENYLAMINE; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MAP KINASE SIGNALING SYSTEM; MEIOSIS; PHOSPHATIDYLINOSITOL 3-KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78649758522     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015518     Document Type: Article

References (67)

1. Petitte JN, Karagenç L, Ginsburg M (1997) The origin of the avian germ line and transgenesis in birds. Poult Sci 76: 1084-1092.
2. 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.
3. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88: 49-92.
4. Nieuwkoop PD, Sutasurya LA (1979) Primordal Germ Cells in the Chordates. Cambridge: Cambridge University Press.
5. Surani MA, Durcova-Hills G, Hajkova P, Hayashi K, Tee WW (2008) Germ line, stem cells, and epigenetic reprogramming. Cold Spring Harb Symp Quant Biol 73: 9-15.
6. Matsui Y, Zsebo K, Hogan BL (1992) Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70: 841-847.
7. Resnick JL, Bixler LS, Cheng L, Donovan PJ (1992) Long-term proliferation of mouse primordial germ cells in culture. Nature 359: 550-551.
8. Durcova-Hills G, Surani A (2008) Reprogramming primordial germ cells (PGC) to embryonic germ (EG) cells. In: Curr Protoc Stem Cell Biol 20, Chapter 1:Unit1A.3.
9. Donovan PJ (1998) The germ cell-the mother of all stem cells. Int J Dev Biol 42: 1043-50.
10. Park TS, Han JY (2000) Derivation and characterization of pluripotent embryonic germ cells in chicken. Mol Reprod Dev 56: 475-482.
11. Jung JG, Kim DK, Park TS, Lee SD, Lim JM, et al. (2005) Development of novel markers for the characterization of chicken primordial germ cells. Stem Cells 23: 689-698.
12. van de Lavoir MC, Diamond JH, Leighton PA, Mather-Love C, Heyer BS, et al. (2006) Germline transmission of genetically modified primordial germ cells. Nature 441: 766-769.
13. Sang H (2006) Transgenesis sunny-side up. Nat Biotechnol 24: 955-956.
14. McGrew MJ (2010) Avian specific Transgenesis. Encyclopaedia of Sustainability Science and Technology Springer, Heidelberg. In press.
15. Blesbois E, Seigneurin F, Grasseau I, Limouzin C, Besnard J, et al. (2007) Semen cryopreservation for ex situ management of genetic diversity in chicken: creation of the French avian cryobank. Poult Sci 86: 555-564.
16. Petitte JN, Liu G, Yang Z (2004) Avianpluripotentstem cells. Mech Dev 121: 1159-1168.
17. Pain B, Clark M E, Shen M, Nakazawa H, Sakurai M, et al. (1996) Long-term in vitro culture and characterisation of avian embryonic stem cells with multiple morphogenetic potentialities. Development 122: 2339-2348.
18. van de Lavoir MC, Mather-Love C, Leighton P, Diamond JH, Heyer BS, et al. (2006) High-grade transgenic somatic chimeras from chicken embryonic stem cells. Mech Dev 123: 31-41.
19. Fulton JE (2006) Avian genetic stock preservation: an industry perspective. Poult Sci 85: 227-231.
20. McGrew MJ, Sherman A, Lillico SG, Ellard FM, Radcliffe PA, et al. (2008) Localised axial progenitor cell populations in the avian tail bud are not committed to a posterior Hox identity. Development 135: 2289-2299.
21. Clinton M, Haines L, Belloir B, McBride D (2001) Sexing chick embryos: a rapid and simple protocol. Br Poult Sci 42: 134-138.
22. De Miguel MP, Cheng L, Holland EC, Federspiel MJ, Donovan PJ (2002) Dissection of the c-Kit signaling pathway in mouse primordial germ cells by retroviral-mediated gene transfer. Proc Natl Acad Sci USA 99: 10458-63.
23. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, et al. (2008) The ground state of embryonic stem cell self-renewal. Nature 453: 519-23.
24. Henrique D, Adam J, Myat A, Chitnis A, Lewis J, et al. (1995) Expression of a Delta homologue in prospective neurons in the chick. Nature 375: 787-790.
25. Lavial F, Acloque H, Bertocchini F, Macleod DJ, Boast S, et al. (2007) The Oct4 homologue PouV and Nanog regulate pluripotency in chicken embryonic stem cells. Development 134: 3549-3563.
26. Perry MM (1988) A complete culture system for the chick embryo. Nature 331: 70-72.
27. McGrew MJ, Sherman AS, Ellard FM, Lillico SG, Gilhooley HJ, et al. (2004) Efficient production of germline transgenic chickens using lentiviral vectors. EMBO Rep 5: 728-733.
28. Petitte JN In:, Handbook of Stem Cells. Lanza R, et al. (2004) Burlington, Massachusetts: Elsevier Academic Press. pp 471-477.
29. Fujimoto T, Ninomyiya T, Ukeshima A (1976) Observation of the primordial germ cells in blood samples from the chick embryo. Dev Biol 49: 278-282.
30. Feng H, Sandlow JI, Sandra A (1998) The c-kit receptor and its possible signaling transduction pathway in mouse spermatozoa. Mol Reprod Dev 49: 317-26.
31. Dolci S, Williams DE, Ernst MK, Resnick JL, Brannan CI, et al. (1991) Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature 352: 807-809.
32. Godin I, Deed R, Cooke J, Zsebo K, Dexter M, et al. (1991) Effects of the steel gene product on mouse primordial germ cells in culture. Nature 352: 809-811.
33. Matsui Y, Toksoz D, Nishikawa S, Nishikawa S, Williams D, et al. (1991) Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture. Nature 353: 750-752.
34. Thompson N, Lyons J (2005) Recent progress in targeting the Raf/MEK/ERK pathway with inhibitors in cancer drug discovery. Curr Opin Pharmacol 5: 350-356.
35. Takeuchi Y, Molyneaux K, Runyan C, Schaible K, Wylie C (2005) The roles of FGF signaling in germ cell migration in the mouse. Development 132: 5399-5409.
36. Hay B, Jan LY, Jan YN (1988) A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATPdependent helicases. Cell 55: 577-587.
37. Youngren KK, Coveney D, Peng X, Bhattacharya C, Schmidt LS, et al. (2005) The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 435: 360-364.
38. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Takamatsu K, Chuma S, et al. (2010) MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev 24: 887-892.
39. Aramaki S, Kubota K, Soh T, Yamauchi N, Hattori MA (2009) Chicken dead end homologue protein is a nucleoprotein of germ cells including primordial germ cells. J Reprod Dev 55: 214-218.
40. Yamaguchi S, Kimura H, Tada M, Nakatsuji N, Tada T (2005) Nanog expression in mouse germ cell development. Gene Expr Patterns 5: 639-646.
41. Durcova-Hills G, Tang F, Doody G, Tooze R, Surani MA (2008) Reprogramming primordial germ cells into pluripotent stem cells. PLoS ONE 3: e3531.
42. Hirning U, Schmid P, Schulz WA, Rettenberger G, Hameister H (1991) A comparative analysis of N-myc and c-myc expression and cellular proliferation in mouse organogenesis. Mech Dev 33: 119-25.
43. Ehlermann J, Pfisterer P, Schorle H (2003) Dynamic expression of Krüppel-like factor 4 (Klf4), a target of transcription factor AP-2alpha during murine midembryogenesis. Anat Rec A Discov Mol Cell Evol Biol 273: 677-680.
44. Antin PB, Pier M, Sesepasara T, Yatskievych TA, Darnell DK (2010) Embryonic expression of the chicken Krü ppel-like (KLF) transcription factor gene family. Dev Dyn 239: 1879-1887.
45. Fujimoto T, Miyayama Y, Fuyuta M (1977) The origin, migration and fine morphology of human primordial germ cells. The Anat Rec 188: 315-329.
46. De Felici M, Scaldaferri ML, Lobascio M, Iona S, Nazzicone V, et al. (2004) Experimental approaches to the study of primordial germ cell lineage and proliferation. Hum Reprod Update 10: 197-206.
47. Spiegelman M, Bennett D (1973) A light- and electron-microscopic study of primordial germ cells in the early mouse embryo. J Embryol Exp Morphol 30: 97-118.
48. Bielañska-Osuchowska Z (2006) Oogenesis in pig ovaries during the prenatal period: ultrastructure and morphometry. Reprod Biol 6: 161-193.
49. Mozdziak PE, Angerman-Stewart J, Rushton B, Pardue SL, Petitte JN (2005) Isolation of chicken primordial germ cells using fluorescence-activated cell sorting. Poult Sci 84: 594-600.
50. Marani E, van Oers JW, Tetteroo PA, Poelmann RE, van der Veeken J, et al. (1986) Stage specific embryonic carbohydrate surface antigens of primordial germ cells in mouse embryos: FAL (SSEA-1) and globoside (SSEA-3). Acta Morphol Neerl Scand; 24: 103-110.
51. Karagenç L, Cinnamon Y, Ginsburg M, Petitte JN (1996) Origin of primordial germ cells in the prestreak chick embryo. Dev Genet 19: 290-301.
52. Aravin AA, van der Heijden GW, Castañeda J, Vagin VV, Hannon GJ, et al. (2009) Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet 5: e1000764.
53. Kedde M, Strasser MJ, Boldajipour B, Oude Vrielink JA, et al. (2007) RNAbinding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131: 1273-86.
54. Slanchev K, Stebler J, Goudarzi M, Cojocaru V, Weidinger G, et al. (2009) Control of Dead end localization and activity-implications for the function of the protein in antagonizing miRNA function. Mech Dev 126: 270-277.
55. Farini D, Scaldaferri ML, Iona S, La Sala G, De Felici M (2005) Growth factors sustain primordial germ cell survival, proliferation and entering into meiosis in the absence of somatic cells. Dev Biol 285: 49-56.
56. Kimura T, Tomooka M, Yamano N, Murayama K, Matoba S, et al. (2008) AKT signaling promotes derivation of embryonic germ cells from primordial germ cells. Development 135: 869-879.
57. Goel S, Fujihara M, Tsuchiya K, Takagi Y, Minami N, et al. (2009) Multipotential ability of primitive germ cells from neonatal pig testis cultured in vitro. Reprod Fertil Dev 21: 696-708.
58. Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317.
59. Hill DJ, Crace CJ, Nissley SP, Morrell D, Holder AT, et al. (1985) Fetal rat myoblasts release both rat somatomedin-C (SM-C)/insulin-like growth factor I (IGF I) and multiplication-stimulating activity in vitro: partial characterization and biological activity of myoblast-derived SM-C/IGF I. Endocrinology 117: 2061-72.
60. Smith AG, Heath JK, Donaldson DD, Wong GG, Moreau J, et al. (1988) Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 336: 688-690.
61. Zsebo KM, Wypych J, McNiece IK, Lu HS, Smith KA, et al. (1990) Identification, purification, and biological characterization of hematopoietic stem cell factor from buffalo rat liver-conditioned medium. Cell 63: 195-201.
62. Wandzioch E, Edling CE, Palmer RH, Carlsson L, Hallberg B (2004) Activation of the MAP kinase pathway by c-Kit is PI-3 kinase dependent in hematopoietic progenitor/stem cell lines. Blood 104: 51-57.
63. Ong SH, Hadari YR, Gotoh N, Guy GR, Schlessinger J, et al. (2001) Stimulation of phosphatidylinositol 3-kinase by fibroblast growth factor receptors is mediated by coordinated recruitment of multiple docking proteins. Proc Natl Acad Sci USA 98: 6074-6079.
64. Kocer A, Reichmann J, Best D, Adams IR (2009) Germ cell sex determination in mammals. Mol Hum Reprod 15: 205-213.
65. Ford CE, Evans EP, Burtenshaw MD, Clegg HM, Tuffrey M, et al. (1975) A functional 'sex-reversed' oocyte in the mouse. Proc R Soc Lond B Biol Sci 190: 187-197.
66. Palmer SJ, Burgoyne PS (1991) In situ analysis of fetal, prepubertal and adult XX-XY chimaeric mouse testes: Sertoli cells are predominantly, but not exclusively, XY. Development 112: 265-268.
67. Naito M, Matsubara Y, Harumi T, Tagami T, Kagami H, et al. (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.