Derivation and characterization of pluripotent embryonic germ cells in chicken

Embryonic germ (EG) cell lines established from primordial germ cells (PGCs) are undifferentiated and pluripotent stem cells. To date, EG cells with proven germ‐line transmission have been completely established only in the mouse with embryonic stem (ES) cells. We isolated PGCs from 5.5‐day‐old (stage 28) chicken embryonic gonads and established a putative chicken EG cell line with EG culture medium supplemented with stem cell factor (SCF), leukemia inhibitory factor (LIF), basic fibroblast growth factor (bFGF), interleukin‐11 (IL‐11), and insulin‐like growth factor‐I (IGF‐I). These cells grew continuously for ten passages (4 months) on a feeder layer of mitotically active chicken embryonic fibroblasts. After several passages, these cells were characterized by screening with the periodic acid‐Schiff reaction, anti‐SSEA‐1 antibody, and a proliferation assay. The chicken EG cells maintained characteristics of gonadal PGCs and undifferentiated stem cells. When cultured in suspension, the chicken EG cells successfully formed an embryoid body and differentiated into a variety of cell types. The chicken EG cells were injected into stage X blastodermal layer and produced chimeric chickens with various differentiated tissues derived from the EG cells. Chicken EG cells will be useful for the production of transgenic chickens and for studies of germ cell differentiation and genomic imprinting. Mol. Reprod. Dev. 56:475–482, 2000. © 2000 Wiley‐Liss, Inc.

[1]  C. Brannan,et al.  Requirement for mast cell growth factor for primordial germ cell survival in culture , 1991, Nature.

[2]  K. Zsebo,et al.  Effects of the steel gene product on mouse primordial germ cells in culture , 1991, Nature.

[3]  D. Solter,et al.  Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[4]  P. Donovan,et al.  Growth factor regulation of mouse primordial germ cell development. , 1994, Current topics in developmental biology.

[5]  Y. Chebloune,et al.  Use of retroviral vectors to introduce and express the beta-galactosidase marker gene in cultured chicken primordial germ cells. , 1994, Developmental biology.

[6]  R. Foote,et al.  Pluripotency of cultured rabbit inner cell mass cells detected by isozyme analysis and eye pigmentation of fetuses following injection into blastocysts or morulae , 1993, Molecular reproduction and development.

[7]  A. Yoshiki,et al.  Germ line chimera produced by transfer of cultured chick primordial germ cells. , 1995, Cell biology international.

[8]  S. Akira,et al.  Cytokine signal transduction , 1994, Cell.

[9]  Charles H. Swift.  Origin and early history of the primordial germ‐cells in the chick , 1914 .

[10]  J. Thomson,et al.  Embryonic stem cell lines derived from human blastocysts. , 1998, Science.

[11]  S. Nishikawa,et al.  Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture , 1991, Nature.

[12]  M. Wheeler,et al.  Development and validation of swine embryonic stem cells: a review. , 1994, Reproduction, fertility, and development.

[13]  M. Kaufman,et al.  Establishment in culture of pluripotential cells from mouse embryos , 1981, Nature.

[14]  T. Doetschman,et al.  Myosin heavy chain gene expression in mouse embryoid bodies. An in vitro developmental study. , 1991, The Journal of biological chemistry.

[15]  A. Bradley,et al.  Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines , 1984, Nature.

[16]  V. Hamburger,et al.  A series of normal stages in the development of the chick embryo. 1951. , 2012, Developmental dynamics : an official publication of the American Association of Anatomists.

[17]  S Kochav,et al.  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. , 1976, Developmental biology.

[18]  J. Piedrahita,et al.  Advances in the generation of transgenic pigs via embryo-derived and primordial germ cell-derived cells. , 2020, Journal of reproduction and fertility. Supplement.

[19]  R. Cherny,et al.  Strategies for the isolation and characterization of bovine embryonic stem cells. , 1994, Reproduction, fertility, and development.

[20]  D. B. Meyer,et al.  THE MIGRATION OF PRIMORDIAL GERM CELLS IN THE CHICK EMBRYO. , 1964, Developmental biology.

[21]  J. Samarut,et al.  Long-term in vitro culture and characterisation of avian embryonic stem cells with multiple morphogenetic potentialities. , 1996, Development.

[22]  K. Yoshinaga,et al.  Scanning and transmission electron microscopic observations of chick primordial germ cells with special reference to the extravasation in their migration course. , 1991, Journal of electron microscopy.

[23]  W. Swartz.  Acid and alkaline phosphatase activity in migrating primordial germ cells of the early chick embryo , 1982, The Anatomical record.

[24]  A. Tajima,et al.  Proliferation of chick primordial germ cells cultured on stroma cells from the germinal ridge. , 1995, Cell biology international.

[25]  D. Barlow,et al.  Mouse embryonic germ (EG) cell lines: transmission through the germline and differences in the methylation imprint of insulin-like growth factor 2 receptor (Igf2r) gene compared with embryonic stem (ES) cell lines. , 1994, Development.

[26]  N. Nakatsuji,et al.  Functional requirement of gp130-mediated signaling for growth and survival of mouse primordial germ cells in vitro and derivation of embryonic germ (EG) cells. , 1996, Development.

[27]  N. First,et al.  Systems for production of calves from cultured bovine embryonic cells. , 1994, Reproduction, fertility, and development.

[28]  Y. Ando,et al.  Ultrastructural Evidence that Chick Primordial Germ Cells Leave the Blood‐Vascular System Prior to Migrating to the Gonadal Anlagen , 1983 .

[29]  C. Dehay,et al.  In vitro differentiation of embryonic stem cells into glial cells and functional neurons. , 1995, Journal of cell science.

[30]  P. Donovan,et al.  Long-term proliferation of mouse primordial germ cells in culture , 1992, Nature.

[31]  R Kemler,et al.  The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. , 1985, Journal of embryology and experimental morphology.

[32]  H. Holzhausen,et al.  Characterization of a pluripotent stem cell line derived from a mouse embryo. , 1984, Experimental cell research.

[33]  A. Gutiérrez-Adán,et al.  Isolation of pluripotent stem cells from cultured porcine primordial germ cells. , 1997 .

[34]  B. Hogan,et al.  Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture , 1992, Cell.

[35]  Y. Hong,et al.  PRODUCTION OF GERMLINE CHIMERIC CHICKENS BY TRANSFER OF CULTURED PRIMORDIAL GERM CELLS , 1997, Cell biology international.

[36]  J. Nichols,et al.  Maintenance of the pluripotential phenotype of embryonic stem cells through direct activation of gp130 signalling pathways , 1994, Mechanisms of Development.

[37]  Peter J. Donovan,et al.  Derivation of pluripotent stem cells from cultured human primordial germ cells , 1998 .

[38]  F. Bazer,et al.  Generation of transgenic porcine chimeras using primordial germ cell-derived colonies. , 1998, Biology of reproduction.

[39]  T. Doetschman,et al.  Establishment of hamster blastocyst-derived embryonic stem (ES) cells. , 1988, Developmental biology.