Skip to main content
SpringerLink
Log in

Isolation and characterization of a bovine visceral endoderm cell line derived from a parthenogenetic blastocyst

  • Articles
  • Cell and Tissue Models
  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Summary

A cell line, BPE-1, was derived from a parthegogenetic 8-d in vitro-produced bovine blastocyst that produced a cell outgrowth on STO feeder cells. The BPE-1 cells resembled visceral endoderm previously cultured from blastocysts produced by in vitro fertilization (IVF). Analysis of the BPE-1 cells demonstrated that they produced serum proteins and were negative for interferon-tau production (a marker of trophectoderm). Transmission electron microscopy revealed that the cells were a polarized epithelium connected by complex junctions resembling tight junctions in conjunction with desmosomes. Rough endoplasmic reticulum was prominent within the cells as were lipid vacuoles. Immunocytochemistry indicated the BPE-1 cells had robust microtubule networks. These cells have been growth for over 2 yr for multiple passages at 1∶10 or 1∶20 split ratios on STO feeder cells. The BPE-1 cell line presumably arose from embryonic cells that became diploid soon after parthenogenetic activation and development of the early embryo. However, metaphase spreads prepared at passage 41 indicated that the cell population had a hypodiploid (2n=60) unimodal chromosome content with a mode of 53 and a median and mean of 52. The cell line will be of interest for functional comparisons with bovine endoderm cell lines derived from IVF and nuclear transfer embryos.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adamson, E. D.; Strickland, S.; Tu, M., et al. A teratocarcinoma-derived endoderm stem cell line (1H5) that can differentiate into extra-embryonic endoderm cell types. Differentiation 29:68–76; 1985.

    Article  PubMed  CAS  Google Scholar 

  • Beckman, D. A.; Lloyd, J. B.; Brent, R. L. Investigations into mechanisms of amino acid supply to the rat embryo using whole-embryo culture. Int. J. Dev. Biol. 41:315–318; 1997.

    PubMed  CAS  Google Scholar 

  • Boediono, A.; Suzuki, T. Pregnancies after transfer of aggregated parthenogenetic bovine activated oocytes. Theriogenology 41:166; 1994.

    Article  Google Scholar 

  • Carlson, B. M. Patten's foundations of embryology. New York, NY: McGraw-Hill; 1981:197–200.

    Google Scholar 

  • Cezar, G. G.; Bartolomei, M. S.; Forsberg, E. J., et al. Genome-wide epigenetic alterations in cloned bovine fetuses. Biol. Reprod. 68:1009–1014; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Chang, M. C. Development of bovine blastocyst with a note on implantation. Anat. Rec. 113:43–161; 1952.

    Article  Google Scholar 

  • De La Fuente, R.; King W. A. Developmental consequences of karyokinesis without cytokinesis during the first mitotic cell cycle of bovine parthenotes. Biol. Reprod. 58:952–962; 1998.

    Article  Google Scholar 

  • De Sousa, P. A.; King, T.; Harkness, L., et al. Evaluation of gestional deficiencies in cloned sheep fetuses and placentae. Biol. Reprod. 65: 23–30; 2001.

    Article  PubMed  Google Scholar 

  • Freshney, R. I. Culture of animal cells. 3rd ed. New York, NY: Wiley-Liss; 1994;12; 254.

    Google Scholar 

  • Fukui, Y.; Sawai K.; Furudate, M., et al. Parthenogenetic development of bovine oocytes treated with ethanol and cytochalasin B after in vitro maturation. Mol. Reprod. Dev. 33:357–362; 1992.

    Article  PubMed  CAS  Google Scholar 

  • Hagemann, L. J.; Peterson, A. J.; Weilert, L. L., et al. In vitro and early development of sheep gynogenones and putative androgenones. Mol. Reprod. Dev. 50:154–162; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Hashizume, K.; Ishiwata, H.; Kizaki, K., et al. Implantation and placental development in somatic cell clone recipient cows. Cloning Stem Cells 4:197–209; 2002.

    Article  PubMed  CAS  Google Scholar 

  • Hill, J. R.; Burghardt, R. C.; Jones, K., et al. Evidence for placental abnormalities as the major cause of mortality in first-trimester somatic cell cloned bovine fetuses. Biol. Reprod. 63:1787–1794; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Humphreys, D.; Eggan, K.; Akutsu, H., et al. Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc. Natl. Acad. Sci. USA 99:12889–12894; 2002.

    Article  CAS  Google Scholar 

  • Inoue, K.; Kodha, T.; Lee, J., et al. Faithful expression of imprinted genes in cloned mice. Science 295:297;2002.

    Article  PubMed  CAS  Google Scholar 

  • Janzen, R. G.; Mably, E. R.; Tamaoki, T., et al. Synthesis of alpha-fetoprotein by the pre-implantation and post-implantation bovine embryo. J. Reprod. Fertil. 65:105–110; 1982.

    Article  PubMed  CAS  Google Scholar 

  • Kadokawa, Y.; Kato, Y.; Eguchi, G. Cell lineage analysis of the primitive and visceral endoderm of mouse embryos cultured in vitro. Cell Differ. 21: 69–76; 1987.

    Article  PubMed  CAS  Google Scholar 

  • Kaufman, M. H.; Robertson, E. J.; Handyside, A. H., et al. Establishment of pluripotential cell lines from haploid mouse embryos. J. Embryol. Exp. Morphol. 73:249–261; 1983.

    PubMed  CAS  Google Scholar 

  • Kharroubi, A. B.; Piras, G.; Stewart, C. L. DNA demethylation reactivates a subset of imprinted genes in uniparental mouse embryonic fibroblasts. J. Biol. Chem. 276:8674–8680; 2001.

    Article  PubMed  Google Scholar 

  • Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277:680–685; 1970.

    Article  Google Scholar 

  • Loi, P.; Ledda, S.; Fulka, J., Jr., et al. Development of parthenogenetic and cloned ovine embryos: effect of activation protocols. Biol. Reprod. 58:1177–1187; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Mamaeva, S. E. Karyotypic evolution of cells in culture: a new concept. Int. Rev. Cytol. 178:1–40; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Mossman, H. W. Vertebrate fetal membranes. New Brunswick, NJ: Rutgers University Press; 1987:279–291.

    Google Scholar 

  • Mummery, C. L.; van Achterberg, T. A. E.; van den Eijnden-van Raaji, A. J. M., et al. Visceral-endoderm-like cell lines induce differentiation of murine P19 embryonal carcinoma cells. Differentiation 46:51–60; 1991.

    Article  PubMed  CAS  Google Scholar 

  • Niimi, G.; Usuda, N.; Shinzato, M., et al. A light and electron microscopic study of the mouse visceral yolk sac endodermal cells in the middle and late embryonic periods, showing the possibility of definitive erythropoiesis. Ann. Anat. 184: 425–429; 2002.

    Article  PubMed  Google Scholar 

  • Pera, M. F.; Blasco-Lafita, M. J.; Mills, J. Cultured stem-cells from human testicular teratomas: the nature of human embryonal carcinoma, and its comparison with two types of yolk-sac carcinoma. Int. J. Cancer 40: 334–343; 1987.

    Article  PubMed  CAS  Google Scholar 

  • Robet, R. M.; Imakawa, K.; Niwano, Y., et al. Interferon production by the preimplanation show embryo. J. Interferon Res. 9:175–187; 1989.

    Google Scholar 

  • Rüsse, I.; Sinowatz, F.; Hunter, L., et al. Development of the yolk sac of ruminants (sheep and cattle), Anat. Histol. Embryol. 21:324–347; 1992.

    PubMed  Google Scholar 

  • Santos, F.; Zakhartchenko, V.; Stojkovic, M., et al. Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr. Biol. 13:1116–1121; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Shi, W. K.; Hopkins, B.; Thompson, S., et al. Synthesis of apolipoproteins, alphafoetoprotein, albumin, and transferrin by the human foetal yolk sac and other foetal organs. J. Embryol. Exp. Morphol. 85:191–206; 1985.

    PubMed  CAS  Google Scholar 

  • Starling, D.; Duncan, R.; Lloyd, J. B. The role of microtubules in pinocytosis. Inhibition of fluid-phase pinocytosis in rat visceral yolk sac by mitoclasic and related agents. Cell Biol. Int. Rep. 7:593–602; 1983.

    Article  PubMed  CAS  Google Scholar 

  • Surani, M. A. H.; Barton, S. C. Development of gynogenetic eggs in the mouse: implications for parthenogenetic embryos. Science 222:1034–1036; 1983.

    Article  PubMed  CAS  Google Scholar 

  • Surani, M. A. H., Kothary, R., Allen, N. D., et al. Genome imprinting and development in the mouse. Development (Suppl.):89–98; 1990.

  • Susko-Parrish, J. L.; Leibfried-Rutledge, M. L.; Northey, D. L., et al. Inhibition of protein kinases after an induced calcium transient causes transition of bovine oocytes to embryonic cycles without meiotic completion. Dev. Biol. 166:729–739; 1994.

    Article  PubMed  CAS  Google Scholar 

  • Tada, T.; Takagi, N. Early development and X-chromosome inactivation in mouse parthenogenetic embryos. Mol. Reprod. Dev. 31:20–27; 1992.

    Article  PubMed  CAS  Google Scholar 

  • Talbot, N. C.; Caperna, T. J.; Edwards, J. L., et al. Bovine blastocyst-derived trophectoderm and endoderm cell cultures: interferon-tau and transferrin expression as respective in vitro markers. Biol. Reprod. 62:235–247; 2000a.

    Article  PubMed  CAS  Google Scholar 

  • Talbot, N. C.; Garrett, W. M.; Caperna, T. J. 2003. Analysis of the expression of aquaporin-1 and-9 in pig liver tissue: comparison with rat liver tissue. Cells Tissues Organs 174:17–28; 2003.

    Article  CAS  Google Scholar 

  • Talbot, N. C.; Powell, A.; Garrett, W., et al. Ultrastructural and karyotypic examination of in vitro produced bovine embryos developed in the sheep uterus. Tissue Cell 32: 9–27; 2000b.

    Article  PubMed  CAS  Google Scholar 

  • Talbot, N. C.; Powell, A. M.; Rexroad, C. E., Jr In vitro pluripotency of epiblasts derived from bovine blastocysts. Mol. Reprod. Dev. 42: 35–52; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Talbot, N. C.; Rexroad, C. E., Jr.; Pursel, V. G., et al. Culturing the epiblast cells of the pig blastocyst. In Vitro Cell. Dev. Biol. 29A:543–554; 1993.

    CAS  Google Scholar 

  • Walter, G.; Intek, A.; Wobus, A. M., et al. Serological characterization of a pluripotent mouse embryonal stem cell line, two transformed derivatives, and an endoderm-like cell line. Cell Differ. 15:147–151; 1984.

    Article  PubMed  CAS  Google Scholar 

  • Winger, Q. A., De La Fuente, R.; King, W. A., et al. Bovine parthenogenesis is characterized by abnormal chromosomal complements: implications for maternal and paternal co-dependence during early bovine development. Dev. Genet. 21:160–166; 1997.

    Article  PubMed  CAS  Google Scholar 

  • Young, M. F.; Klein, N. W. Synthesis of serum proteins by cultures of chick embryo yolk sac endodermal cells. Dev. Biol. 100: 50–58; 1983.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Agricultural Research Service, Animal and Natural Resources Institute, Biotechnology and Germplasm Laboratory, U.S. Department of Agriculture, 20705, Beltsville, Maryland

    Neil C. Talbot, Anne M. Powell, Ann Le Blomberg & Wesley M. Garrett

  2. Growth Biology Laboratory, Beltsville Agricultural Research Center, 20705, Beltsville, Maryland

    Thomas J. Caperna

  3. Department of Animal Sciences, University of Florida, 32611-0910, Gainesville, Florida

    Alan D. Ealy

Authors
  1. Neil C. Talbot
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas J. Caperna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anne M. Powell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alan D. Ealy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ann Le Blomberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wesley M. Garrett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Neil C. Talbot.

Additional information

Disclaimer: Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Talbot, N.C., Caperna, T.J., Powell, A.M. et al. Isolation and characterization of a bovine visceral endoderm cell line derived from a parthenogenetic blastocyst. In Vitro Cell.Dev.Biol.-Animal 41, 130–141 (2005). https://doi.org/10.1290/040901.1

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1290/040901.1

Key words

Search

Navigation