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Relationship between the parental origin of the X chromosomes, embryonic cell lineage and X chromosome expression in mice

Published online by Cambridge University Press:  14 April 2009

Virginia E. Papaioannou
Affiliation:
Sir William Dunn School of Pathology, South Parks Road, Oxford 0X1 3RE, U.K.
John D. West
Affiliation:
Sir William Dunn School of Pathology, South Parks Road, Oxford 0X1 3RE, U.K.
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Summary

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The electrophoretic variants of the X-chromosome-linked enzyme phosphoglycerate kinase (PGK-1) have been used to investigate the randomness of X chromosome expression in the fetus and various extra-embryonic membranes of the mouse conceptus. The amnion shows essentially random expression of the maternally derived X chromosome (Xm) and the paternally derived X chromosome (Xp). The parietal endoderm, however, shows exclusive or preferential expression of Xm. The results support the idea that the randomness of X chromosome expression is correlated with embryonic cell lineage such that Xm is preferentially (perhaps exclusively) expressed in derivatives of the primitive endoderm and trophectoderm but that Xm and Xp are randomly expressed in the derivatives of the primitive ectoderm.

Experiments involving ovary transplants, embryo transfers or crosses with heterozygous mothers confirm previous findings that Xm is preferentially expressed regardless of the X chromosome expressed in the reproductive tract. Additional experiments show that the preferentially expressed X chromosome in the parietal endoderm and visceral yolk sac endoderm of a normal XmXp conceptus is always Xm regardless of grand-parental origin of Xm and regardless of whether the mother is a normal XX female or an XO female. Xp is, however, expressed in these tissues hi XpO female conceptuses. It is argued that a form of chromosome imprinting occurs at each generation to mark Xm and Xp as different and that this difference influences the choice of which X chromosomes are expressed in each cell lineage.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1981

References

REFERENCES

Beutler, E. (1969). Electrophoresis of phosphoglycerate kinase. Biochemical Genetics 3, 189195.CrossRefGoogle ScholarPubMed
Brown, S. W. & Chandra, H. S. (1973). Inactivation system of the mammalian X chromosome. Proceedings of the National Academy of Sciences, USA 70, 195199.CrossRefGoogle ScholarPubMed
Cattanach, B. M. (1975). Control of chromosome inactivation. Annual Review of Genetics 9, 118.CrossRefGoogle ScholarPubMed
Cooper, D. W. (1971). Directed genetic change model for X chromosome inactivation in eutherian mammals. Nature 230, 292294.CrossRefGoogle ScholarPubMed
Cooper, D. W., VandeBerg, J. L., Sharman, G. B. & Poole, W. E. (1971). Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X-inactivation. Nature New Biology 230, 155157.CrossRefGoogle ScholarPubMed
Evans, E. P. & Phillips, R. J. S. (1975). Inversion heterozygosity and the origin of XO daughters of Bpa/ + female mice. Nature 256, 4041.CrossRefGoogle ScholarPubMed
Frels, W. I. & Chapman, V. M. (1979). Paternal X chromosome expression in extraembryonic membranes of XO mice. Journal of Experimental Zoology 210, 553560.CrossRefGoogle ScholarPubMed
Frels, W. I. & Chapman, V. M. (1980). Expression of the maternally derived X chromosome in the mural trophoblast of the mouse. Journal of Embryology and Experimental Morphology 56, 179190.Google ScholarPubMed
Frels, W. I., Rossant, J. & Chapman, V. M. (1979). Maternal X chromosome expression in mouse chorionic ectoderm. Developmental Genetics 1, 123132.CrossRefGoogle Scholar
Gardner, R. L. & Papaioannou, V. E. (1975). Differentiation in the trophectoderm and inner cell mass. In The Early Development of Mammals, Second Symposium of the British Society for Developmental Biology (ed. Balls, M. and Wild, A. E.), pp. 107ð132. Cambridge University Press.Google Scholar
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
Harris, H. & Hopkinson, D. A. (1976). Handbook of Enzyme Electrophoresis in Human Genetics. Amsterdam: North-Holland.Google Scholar
Kaufman, M. H., Guc-Cubrilo, M. & Lyon, M. F. (1978). X chromosome inactivation in diploid parthenogenetic mouse embryos. Nature 271, 547549.CrossRefGoogle ScholarPubMed
Levak-Švajger, B., Švajger, A. & Škreb, N. (1969). Separation of germ layers in presomite rat embryos. Experientia 25, 13111312.CrossRefGoogle Scholar
Lyon, M. F. (1977). Chairman's address. In Reproduction and Evolution. Proceedings of the 4th Symposium on Comparative Biology of Reproduction, pp. 9598. Australian Academy of Science.Google Scholar
McLaren, A. & Michie, D. (1956). Studies on the transfer of fertilized mouse eggs to uterine foster-mothers. 1. Factors affecting the implantation and survival of native and transferred eggs. Journal of Experimental Biology 33, 394416.CrossRefGoogle Scholar
Monk, M. & Harper, M. I. (1979). Sequential X chromosome inactivation coupled with cellular differentiation in early mouse embryos. Nature 281, 311313.CrossRefGoogle ScholarPubMed
Nielsen, J. T. & Chapman, V. M. (1977). Electrophoretic variation for sex-linked phosphoglycerate kinase (PGK-1) in the mouse. Genetics 87, 319325.CrossRefGoogle Scholar
Takagi, N. (1978). Preferential inactivation of the paternally derived X chromosome in mice. In Genetic Mosaics and Chimeras in Mammals (ed. Russell, L. B.), pp. 341360. Basic Life Sciences, volume 12. New York: Plenum Press.CrossRefGoogle Scholar
Takagi, N. & Sasaki, M. (1975). Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256, 640642.CrossRefGoogle ScholarPubMed
Vickers, A. D. (1967). Amniotic sex chromatin and foetal sexing in the mouse. Journal of Reproduction and Fertility 14, 503505.CrossRefGoogle ScholarPubMed
West, J. D. & Chapman, V. M. (1978). Variation for X chromosome expression in mice detected by electrophoresis of phosphoglycerate kinase. Genetical Research 32, 91102.CrossRefGoogle ScholarPubMed
West, J. D., Frels, W. L., Chapman, V. M. & Papaioannou, V. E. (1977). Preferential expression of the maternally derived X chromosome in the mouse yolk sac. Cell 12, 873882.CrossRefGoogle ScholarPubMed
West, J. D., Papaioannou, V. E., Fuels, W. I. & Chapman, V. M. (1978). Preferential expression of the maternally derived X chromosome in extraembryonic tissues of the mouse. In Genetic Mosaics and Chimeras in Mammals (ed. Russell, L. B.), pp. 361377. Basic Life Sciences, volume 12. New York: Plenum Press.CrossRefGoogle Scholar
Whittingham, D. G. & Wales, R. G. (1969). Storage of two-cell mouse embryos in vitro. Australian Journal of Biological Sciences 22, 10651068.CrossRefGoogle ScholarPubMed