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Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis

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.

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References

  1. 1

    Graham, C. F. Biol. Rev. 49, 399–422 (1974).

    CAS  Article  Google Scholar 

  2. 2

    Hoppe, P. C. & Illmensee, K. Proc. natn. Acad. Sci. U.S.A. 74, 5657–5661 (1977).

    ADS  CAS  Article  Google Scholar 

  3. 3

    Hoppe, P. C. & Illmensee, K. Proc. natn. Acad. Sci. U.S.A. 79, 1912–1916 (1982).

    ADS  CAS  Article  Google Scholar 

  4. 4

    Surani, M. A. H. & Barton, S. C. Science 222, 1034–1036 (1983).

    ADS  CAS  Article  Google Scholar 

  5. 5

    Modlinski, J. A. J. Embryol. exp. Morph. 60, 153–161 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6

    Markert, C. L. J. Hered. 73, 390–397 (1982).

    CAS  Article  Google Scholar 

  7. 7

    Kaufman, M. H., Barton, S. C. & Surani, M. A. H. Nature 265, 53–55 (1977).

    ADS  CAS  Article  Google Scholar 

  8. 8

    Surani, M. A. H., Barton, S. C. & Kaufman, M. H. Nature 270, 601–603 (1977).

    ADS  CAS  Article  Google Scholar 

  9. 9

    Sawicki, J. A., Magnuson, T. & Epstein, C. J. Nature 294, 450–451 (1981).

    ADS  CAS  Article  Google Scholar 

  10. 10

    West, J. D., Frels, W. I., Chapman, V. M. & Papaioannou, V. E. Cell 12, 873–882 (1977).

    CAS  Article  Google Scholar 

  11. 11

    Takagi, N., Wake, N. & Sasaki, M. Cytogenet. Cell Genet. 20, 240–248 (1978).

    CAS  Article  Google Scholar 

  12. 12

    Harper, M. I., Fosten, M. & Monk, M. J. Embryol. exp. Morph. 67, 127–135 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    Endo, S. & Takagi, N. Jap. J. Genet. 56, 349–356 (1981).

    CAS  Article  Google Scholar 

  14. 14

    Rastan, S., Kaufman, M. H., Handyside, A. H. & Lyon, M. F. Nature 288, 172–173 (1980).

    ADS  CAS  Article  Google Scholar 

  15. 15

    Wakasugi, N. J. Reprod. Fert. 41, 85–96 (1974).

    CAS  Article  Google Scholar 

  16. 16

    Stevens, L. C. Symp. Soc. dev. Biol. 33, 93–106 (1975).

    Google Scholar 

  17. 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  Google Scholar 

  18. 18

    Stevens, L. C., Varnum, D. S. & Eicher, E. M. Nature 269, 515–517 (1977).

    ADS  CAS  Article  Google Scholar 

  19. 19

    Whittingham, D. G. & Wales, R. G. Aust. J. biol. Sci. 22, 1065–1072 (1969).

    CAS  Article  Google Scholar 

  20. 20

    Cuthbertson, K. S. R. J. exp. Zool. 226, 311–314 (1983).

    CAS  Article  Google Scholar 

  21. 21

    Whittingham, D. G. J. Reprod. Fert. Suppl. 14, 7–21 (1971).

    CAS  Google Scholar 

  22. 22

    Barton, S. C. & Surani, M. A. H. Expl Cell Res. 146, 187–191 (1983).

    CAS  Article  Google Scholar 

  23. 23

    McGrath, J. & Solter, D. Science 220, 1300–1302 (1983).

    ADS  CAS  Article  Google Scholar 

  24. 24

    Neff, J. M. & Enders, J. F. Proc. Soc. exp. Biol. Med. 127, 260–271 (1968).

    CAS  Article  Google Scholar 

  25. 25

    Giles, R. E. & Ruddle, F. H. In Vitro 9, 103–108 (1973).

    CAS  Article  Google Scholar 

  26. 26

    Graham, C. F. Acta endocr. Suppl. 153, 154–167 (1971).

    CAS  Article  Google Scholar 

  27. 27

    Chapman, V. M., Whitten, W. K. & Ruddle, F. H. Devl Biol. 26, 153–161 (1971).

    CAS  Article  Google Scholar 

  28. 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 

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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

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