Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis (original) (raw)

Nature volume 308, pages 548–550 (1984)Cite this article

Abstract

It has been suggested that the failure of parthenogenetic mouse embryos to develop to term is primarily due to their aberrant cytoplasm and homozygosity leading to the expression of recessive lethal genes1. The reported birth of homozygous gynogenetic (male pronucleus removed from egg after fertilization) mice and of animals following transplantation of nuclei from parthenogenetic embryos to enucleated fertilized eggs2,3, is indicative of abnormal cytoplasm and not an abnormal genotype of the activated eggs. However, we4 and others5,6 have been unable to obtain such homozygous mice. We investigated this problem further by using reconstituted heterozygous eggs, with haploid parthenogenetic eggs as recipients for a male or female pronucleus. We report here that the eggs which receive a male pronucleus develop to term but those with two female pronuclei develop only poorly after implantation. Therefore, the cytoplasm of activated eggs is fully competent to support development to term but not if the genome is entirely of maternal origin. We propose that specific imprinting of the genome occurs during gametogenesis so that the presence of both a male and a female pronucleus is essential in an egg for full-term development. The paternal imprinting of the genome appears necessary for the normal development of the extraembryonic membranes and the trophoblast.

This is a preview of subscription content, access via your institution

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

Similar content being viewed by others

References

  1. Graham, C. F. Biol. Rev. 49, 399–422 (1974).
    Article CAS PubMed Google Scholar
  2. Hoppe, P. C. & Illmensee, K. Proc. natn. Acad. Sci. U.S.A. 74, 5657–5661 (1977).
    Article ADS CAS Google Scholar
  3. Hoppe, P. C. & Illmensee, K. Proc. natn. Acad. Sci. U.S.A. 79, 1912–1916 (1982).
    Article ADS CAS Google Scholar
  4. Surani, M. A. H. & Barton, S. C. Science 222, 1034–1036 (1983).
    Article ADS CAS PubMed Google Scholar
  5. Modlinski, J. A. J. Embryol. exp. Morph. 60, 153–161 (1980).
    CAS PubMed Google Scholar
  6. Markert, C. L. J. Hered. 73, 390–397 (1982).
    Article CAS PubMed Google Scholar
  7. Kaufman, M. H., Barton, S. C. & Surani, M. A. H. Nature 265, 53–55 (1977).
    Article ADS CAS PubMed Google Scholar
  8. Surani, M. A. H., Barton, S. C. & Kaufman, M. H. Nature 270, 601–603 (1977).
    Article ADS CAS PubMed Google Scholar
  9. Sawicki, J. A., Magnuson, T. & Epstein, C. J. Nature 294, 450–451 (1981).
    Article ADS CAS PubMed Google Scholar
  10. West, J. D., Frels, W. I., Chapman, V. M. & Papaioannou, V. E. Cell 12, 873–882 (1977).
    Article CAS PubMed Google Scholar
  11. Takagi, N., Wake, N. & Sasaki, M. Cytogenet. Cell Genet. 20, 240–248 (1978).
    Article CAS PubMed Google Scholar
  12. Harper, M. I., Fosten, M. & Monk, M. J. Embryol. exp. Morph. 67, 127–135 (1982).
    CAS PubMed Google Scholar
  13. Endo, S. & Takagi, N. Jap. J. Genet. 56, 349–356 (1981).
    Article CAS Google Scholar
  14. Rastan, S., Kaufman, M. H., Handyside, A. H. & Lyon, M. F. Nature 288, 172–173 (1980).
    Article ADS CAS PubMed Google Scholar
  15. Wakasugi, N. J. Reprod. Fert. 41, 85–96 (1974).
    Article CAS Google Scholar
  16. Stevens, L. C. Symp. Soc. dev. Biol. 33, 93–106 (1975).
    Google Scholar
  17. Iles, S. A., McBurney, M. W., Bramwell, S. R., Deussen, Z. A. & Graham, C. F. J. Embryol. exp. Morph. 34, 387–405 (1975).
    CAS PubMed Google Scholar
  18. Stevens, L. C., Varnum, D. S. & Eicher, E. M. Nature 269, 515–517 (1977).
    Article ADS CAS PubMed Google Scholar
  19. Whittingham, D. G. & Wales, R. G. Aust. J. biol. Sci. 22, 1065–1072 (1969).
    Article CAS PubMed Google Scholar
  20. Cuthbertson, K. S. R. J. exp. Zool. 226, 311–314 (1983).
    Article CAS PubMed Google Scholar
  21. Whittingham, D. G. J. Reprod. Fert. Suppl. 14, 7–21 (1971).
    CAS Google Scholar
  22. Barton, S. C. & Surani, M. A. H. Expl Cell Res. 146, 187–191 (1983).
    Article CAS Google Scholar
  23. McGrath, J. & Solter, D. Science 220, 1300–1302 (1983).
    Article ADS CAS PubMed Google Scholar
  24. Neff, J. M. & Enders, J. F. Proc. Soc. exp. Biol. Med. 127, 260–271 (1968).
    Article CAS PubMed Google Scholar
  25. Giles, R. E. & Ruddle, F. H. In Vitro 9, 103–108 (1973).
    Article CAS PubMed Google Scholar
  26. Graham, C. F. Acta endocr. Suppl. 153, 154–167 (1971).
    Article CAS Google Scholar
  27. Chapman, V. M., Whitten, W. K. & Ruddle, F. H. Devl Biol. 26, 153–161 (1971).
    Article CAS Google Scholar
  28. Markert, C. L. & Seidel, G. E. in New Technologies in Animal Breeding (eds Brackett, B. G., Seidel, G. E. & Seidel, S. M.) 181–199 (Academic, New York, 1981).
    Google Scholar

Download references

Author information

Authors and Affiliations

  1. AFRC Institute of Animal Physiology, 307 Huntingdon Road, Cambridge, CB3 0JQ, UK
    M. A. H. Surani, S. C. Barton & M. L. Norris

Authors

  1. M. A. H. Surani
    You can also search for this author inPubMed Google Scholar
  2. S. C. Barton
    You can also search for this author inPubMed Google Scholar
  3. M. L. Norris
    You can also search for this author inPubMed Google Scholar

Rights and permissions

About this article

Cite this article

Surani, M., Barton, S. & Norris, M. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis.Nature 308, 548–550 (1984). https://doi.org/10.1038/308548a0

Download citation

This article is cited by