Hostname: page-component-7479d7b7d-qlrfm Total loading time: 0 Render date: 2024-07-09T08:22:20.008Z Has data issue: false hasContentIssue false

Use of triple tissue blastocyst reconstitution to study the development of diploid parthenogenetic primitive ectoderm in combination with fertilization-derived trophectoderm and primitive endoderm

Published online by Cambridge University Press:  14 April 2009

R. L. Gardner*
Affiliation:
Imperial Cancer Research Fund, Developmental Biology Unit, Department of Zoology, South Parks Road, Oxford, OX1 3PS
S. C. Barton
Affiliation:
Department of Molecular Embryology, AFRC Institute of Animal Physiology and Genetics Research, Cambridge Research Station, Babraham Hall, Cambridge, CB2 4AT
M. A. H. Surani
Affiliation:
Department of Molecular Embryology, AFRC Institute of Animal Physiology and Genetics Research, Cambridge Research Station, Babraham Hall, Cambridge, CB2 4AT
*
Corresponding author.

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Diploid mouse conceptuses lacking a paternal genome can form morphologically normal but small fetuses of up to 25 somites, but they invariably fail to develop beyond mid-gestation. Such conceptuses differ from normal most notably in the poor development of extra-embryonic tissues which are largely of trophectodermal and primitive endodermal origin. However, it is not clear whether the demise of diploid parthenogenetic (P) or gynogenetic (G) conceptuses is attributable entirely to the defective development of these two tissues or whether differentiation of the primitive ectoderm, the precursor of the foetus, extra-embryonic mesoderm and amnion, is also impaired by the absence of a paternal genome. Therefore, a new blastocyst reconstitution technique was used which enabled primitive ectoderm from P blastocysts to be combined with primitive endoderm and trophectoderm from fertilization-derived (F) blastocysts. One third of the ‘triple tissue’ reconstituted blastocysts that implanted yielded foetuses. However, all foetuses recovered on the llth or 12th day of gestation were small and, with one exception, either obviously retarded or arrested in development. The exception was a living 44 somite specimen which is the most advanced P foetus yet recorded. Foetuses were invariably degenerating in conceptuses recovered on the 13th day. In contrast, at least 16% of control reconstituted blastocysts with primitive ectoderm as well as primitive endoderm and trophectoderm of F origin developed normally on the 13th day of gestation or to term. Hence, the presence of a paternal genome seems to be essential for normal differentiation of all 3 primary tissues of the mouse blastocyst.

The P foetuses that developed from reconstituted blastocysts were so closely invested by their membranes that they often showed abnormal flexure of the posterior region of the body. Several also showed a deficiency of allantoic tissue. Therefore, the possibility that the defect in development of P primitive ectoderms resided in their extra-embryonic tissues was investigated by analysing a series of chimaeras produced by injecting them into intact F blastocysts. The foregoing anomalies were not discernible even when P cells made a large contribution to the extra-embryonic mesoderm or amnion plus umbilical cord. Furthermore, selection against P cells was no greater in extra-embryonic derivatives of the primitive ectoderm than in the foetus itself.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

References

Anderegg, C. & Markert, C. L. (1986). Successful rescue of microsurgically produced homozygous uniparental mouse embryos via production of aggregation chimaeras. Proceedings of the National Academy of Science U.S.A. 83, 65096513.CrossRefGoogle Scholar
Barton, S. C., Surani, M. A. H. & Norris, M. L. (1984). Role of paternal and maternal genomes in mouse development. Nature 311, 374376.Google Scholar
Barton, S. C., Adams, C. A., Norris, M. L. & Surani, M. A. H. (1985). Development of gynogenetic and parthenogenetic inner cell mass and trophectoderm tissues in reconstituted blastocysts in the mouse. Journal of Embryology and experimental Morphology 90, 267285.Google ScholarPubMed
Cattanach, B. M. (1986). Parental origin effects in mice. Journal of Embryology and experimental Morphology 97, Suppl., 137150.Google ScholarPubMed
Champlin, A. K., Dorr, D. L. & Gates, A. H. (1973). Determining the stage of the estrous cycle in the mouse by the appearance of the vagina. Biology of Reproduction 8, 491494.Google Scholar
Clarke, H. J., Varmuza, S., Prideaux, V. R. & Rossant, J. (1988). The developmental potential of parthenogenetically derived cells in chimaeric mouse embryos: implications for action of imprinted genes. Development 104, 175182.Google Scholar
Cockroft, D. L. & Gardner, R. L. (1987). Clonal analysis of the developmental potential of 6th and 7th day visceral endoderm cells in the mouse. Development 101, 143155.Google Scholar
Cuthbertson, K. S. R. (1983). Parthenogenetic activation of mouse oocyte in vitro with ethanol and benzyl alcohol. Journal of experimental Zoology 226, 311314.Google Scholar
Dyban, A. P. & Baranov, V. S. (1987). Cytogenetics of Mammalian Embryonic Development. Clarendon Press, Oxford.Google Scholar
Eicher, E. M. & Washburn, L. L. (1978). Assignment of genes to regions of mouse chromosomes. Proceedings of the national Academy of Science U.S.A. 75, 946950.CrossRefGoogle ScholarPubMed
Epstein, C. J. (1986). The Consequences of Chromosome Imbalance: Principles, Mechanisms and Models. Cambridge University Press, Cambridge.Google Scholar
Fundele, R., Norris, M. L., Barton, S. C., Reik, W. & Surani, M. A. H. (1989). Systematic elimination of path-enogenetic cells in mouse chimaeras. Development 106, 2935.CrossRefGoogle Scholar
Fundele, R. H., Morris, M. L., Barton, S. C., Fehlau, M., Howlett, S. K., Mills, W. E. & Surani, M. A. (1990). Temporal and spatial selection against parthenogenetic cells during development of foetal chimaeras. Development 108, 203211.CrossRefGoogle Scholar
Gardner, R. L. (1978). Production of chimeras by injecting cells or tissue into the blastocyst. In Methods in Mammalian Reproduction (ed. Daniel, J. C.), pp. 137165. Academic Press, New York.CrossRefGoogle Scholar
Gardner, R. L. (1985 a). Clonal analysis of early mammalian development. Philosophical Transactions of the Royal Society B 312, 163178.Google ScholarPubMed
Gardner, R. L. (1985 b). Regeneration of endoderm from primitive ectoderm in the mouse embryo: Fact or artifact? Journal of Embryology and experimental Morphology 88, 303326.Google Scholar
Gardner, R. L. (1988 a). Cell fate in the developing embryo. In Fetal and Neonatal Development - Research in Perinatal Medicine VII (ed. Jones, C. T.), pp. 1023. Perinatology Press, New York.Google Scholar
Gardner, R. L. (1988 b). Embryo transfer and manipulation. In New Developments in Biosciences: Their Implications for Laboratory Animal Science (ed. Beynen, A. C. and Solleveld, H. A.), pp. 147162. Martinus Nijhoff, Dordrecht.CrossRefGoogle Scholar
Gardner, R. L. & Beddington, R. S. P. (1988). Multi-lineage ‘stem’ cells in the mammalian embryo. Journal of Cell Science Suppl. 10, 1127.CrossRefGoogle ScholarPubMed
Gardner, R. L., Papaioannou, V. E. & Barton, S. C. (1973). Origin of the ectoplacental cone and secondary giant cells in mouse blastocysts reconstituted from isolated trophoblast and inner cell mass. Journal of Embryology and experimental Morphology 30, 561572.Google ScholarPubMed
Kaufman, M. H. (1982). The chromosome complement of single pronuclear haploid mouse embryos following activation by alcohol. Journal of Embryology and experimental Morphology 71, 139154.Google Scholar
Kaufman, M. H. (1983). Early Mammalian Development: Parthenogenetic Studies. Cambridge University Press, Cambridge.Google Scholar
McGrath, J. & Solter, D. (1983). Nuclear transplantation in the mouse embryo by microsurgery and cell fusion. Science 220, 13001303.CrossRefGoogle ScholarPubMed
McGrath, J. & Solter, D. (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179183.Google Scholar
Mullen, R. J. & Whitten, W. K. (1971). Relationship of genotype and degree of chimerism in coat color to sex ratios and gametogenesis in chimeric mice. Journal of experimental Zoology 178, 165176.CrossRefGoogle ScholarPubMed
Nagy, A., Paldi, A., Dezso, L., Varga, L. & Magyar, A. (1987). Prenatal fate of parthenogenetic cells in mouse aggregation chimaeras. Development 101, 6771.CrossRefGoogle ScholarPubMed
Nagy, A., Sass, M. & Markkula, M. (1989). Systematic nonuniform distribution of parthenogenetic cells in adult mouse chimaeras. Development 106, 321324.Google Scholar
Nichols, J. & Gardner, R. L. (1984). Heterogeneous differentiation of external cells in individual isolated early mouse inner cell masses in culture. Journal of Embryology and experimental Morphology 80, 225240.Google ScholarPubMed
Otani, H., Yokoyama, M., Nozawa-Kimura, S., Tanaka, O. & Katsuki, M. (1987). Pluripotency of homozygousdiploid mouse embryos in chimaeras. Development, Growth and Differentiation 29, 373380.Google Scholar
Paldi, A., Nagy, A., Markkula, M., Barna, I. & Dezso, L. (1989). Postnatal development of parthenogenetic fertilized mouse aggregation chimeras. Development 105, 115118.CrossRefGoogle ScholarPubMed
Papaioannou, V. E. (1982). Lineage analysis of inner cell mass and trophectoderm using microsurgically reconstituted blastocysts. Journal of Embryology and experimental Morphology 80, 225240.Google Scholar
Reik, W., Collick, A., Norris, M. L., Barton, S. C. & Surani, M. A. H. (1987). Genomic imprinting determines methylation of parental alleles in transgenic mice. Nature 328, 4851.CrossRefGoogle ScholarPubMed
Sapienza, C., Peterson, A. C., Rossant, J. & Balling, R. (1987). Degree of methylation of transgenes is dependent on gamete of origin. Nature 328, 5154.CrossRefGoogle ScholarPubMed
Stanners, C. P., Eliceiri, G. L. & Green, H. (1971). Two types of ribosome in mouse-hamster hybrid cells. Nature, New Biology 230, 5254.Google ScholarPubMed
Stevens, L. C. (1978). Totipotent cells of parthenogenetic origin in a chimeric mouse. Nature 276, 266267.CrossRefGoogle Scholar
Stevens, L. C., Varnum, D. S. & Eicher, E. M. (1977). Viable chimaeras produced from normal and parthenogenetic mouse embryos. Nature 269, 515517.Google Scholar
Surani, M. A. H. & Barton, S. C. (1983). Development of gynogenetic eggs in the mouse: implications for parthenogenetic embryos. Science 222, 10341035.CrossRefGoogle ScholarPubMed
Surani, M. A. H., Barton, S. C. & Kaufman, M. H. (1977). Development to term of chimaeras between diploid parthenogenetic and fertilized embryos. Nature 270, 601603.Google Scholar
Surani, M. A. H., Barton, S. C. & Norris, M. L. (1984). Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308, 548550.Google Scholar
Surani, M. A. H., Barton, S. C. & Norris, M. L. (1987). Influence of parental chromosomes on spatial specificity in androgenetic parthenogenetic chimaeras in the mouse. Nature 326, 395397.CrossRefGoogle ScholarPubMed
Surani, M. A., Barton, S. C., Hewlett, S. K. & Norris, M. L. (1988). Influence of chromosomal determinants on development of androgenetic and parthenogenetic cells. Development 103, 171178.CrossRefGoogle ScholarPubMed
Surani, M. A., Allen, N. D., Barton, S. C., Fundele, R., Howlett, S. K., Norris, M. L. & Reik, W. (1990). Developmental consequences of imprinting of parental chromosomes by DNA methylation. Philosophical Transactions of the Royal Society London B 326, 313327.Google ScholarPubMed
Swain, J. L., Stewart, T. A. & Leder, P. (1987). Parental legacy determines methylation and expression of an autosomal transgene: A molecular mechanism for parental imprinting. Cell 50, 719727.Google Scholar
Thomson, J. A. & Solter, D. (1988). The developmental fate of androgenetic, parthenogenetic, and gynogenetic cells in chimaeric gastrulating mouse embryos. Genes and Development 2, 13441351.CrossRefGoogle Scholar
Thomson, J. A. & Solter, D. (1989). Chimaeras between parthenogenetic or androgenetic blastomeres and normal embryos: allocation to the inner cell mass and trophectoderm. Developmental Biology 131, 580583.CrossRefGoogle ScholarPubMed
Tsunoda, Y., Yasui, T., Nakamura, K., Uchida, T. & Sugie, T. (1986). Effect of cutting the zona pellucida on the pronuclear transplantation in mice. Journal of experimental Zoology 240, 119125.Google Scholar
West, J. D. (1982). X chromosome expression during mouse embryogenesis. In Genetic Control of Gamete Production and function (ed. Crosignani, P. G. and Rubin, B. L.), pp. 4991. Academic Press, New York.Google Scholar
Whittingham, D. G. & Wales, R. G. (1969). Storage of two cell mouse embryos in vitro. Australian Journal of Biological Science 22, 10651068.CrossRefGoogle ScholarPubMed