Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-23T07:28:38.088Z Has data issue: false hasContentIssue false

X-chromosome activity in female mouse embryos heterozygous for Pgk-1 and Searle's translocation, T(X; 16) 16H

Published online by Cambridge University Press:  14 April 2009

A. McMahon
Affiliation:
MRC Mammalian Development Unit, Wolfson House (University College London), 4 Stephenson Way, London NW1 2HE, England
M. Monk
Affiliation:
MRC Mammalian Development Unit, Wolfson House (University College London), 4 Stephenson Way, London NW1 2HE, England
Rights & Permissions [Opens in a new window]

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.

To investigate whether the preferential expression of genes on the translocated X chromosome in female mice carrying the X-autosome translocation T(X; 16)16H (Searle's translocation) is due to non-random inactivation or to cell selection, we examined tissues of mouse embryos heterozygous for the X-linked gene coding for phosphoglycerate kinase (Pgk-1). From the cross T16H Pgk-lb/+ Pgk-lb ♀ × +Pgk-la / Y ♂, embryos expressing both isozymic forms of PGK-1 in the epiblast, and only the maternally inherited Pgk-lb allele in extra-embryonic tissues, were assumed to be chromosomally balanced, heterozygous female embryos carrying the Searle's translocation (like the mother). The normal X chromosome in this cross carries a high-expression Xcec locus. At 6 days post-coitum (p.c.) both isozymes were equally expressed in the epiblast as expected if both X chromosomes are active, but by 7 days p.c. the PGK-1B contribution was significantly less than 50%, suggesting that X inactivation has occurred with a bias towards inactivation of the translocated X chromosome carrying the lower-expression Xce allele. By 8 days p.c. the situation was the reverse, with a Pgk-lb contribution of significantly more than 50%, and by 12½ days p.c. no Pgk-la expression could be detected. We interpret the dramatic change in isozy me expression between 7 and 8 days p.c. as indicating rapid selection against cells that had inactivated the translocated 16X chromosome. Two 7-day p.c. embryos unexpectedly showed equal expression of both Pgk-1 alleles in both embryonic and extra-embryonic tissues; these were presumably chromosomally unbalanced embryos which had inherited from the mother both an active translocated 16X chromosome carrying Pgk-lb and an active normal X chromosome carrying Pgk-la.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1983

References

REFERENCES

Bücher, T., Bender, W., Fundele, R., Hofner, H. & Linke, I. (1980). Quantitative evaluation of electrophoretic allo- and isozyme patterns. FEBS Letters 115, 319324.CrossRefGoogle ScholarPubMed
Cattanach, B. M. (1970). Controlling elements in the mouse X-chromosome. III. Influence upon both parts of an X divided by rearrangement. Genetical Research 16, 293301.CrossRefGoogle Scholar
Cohen, M. M. & Rattazzi, M. C. (1971). Cytological and biochemical correlation of late X-chromosome replication and gene inactivation in the mule. Proceedings of the National Academy of Sciences, U.S.A. 68, 544548.CrossRefGoogle ScholarPubMed
Disteche, C. M., Eicher, E. M. & Latt, S. A. (1979). Late replication in an X-autosome translocation in the mouse: correlation with genetic inactivation and evidence for selective effects during embryogenesis. Proceedings of the National Academy of Sciences, U.S.A. 76, 52345238.CrossRefGoogle Scholar
Disteche, C. M., Eicher, E. M. & Latt, S. A. (1981). Late replication patterns in adult and embryonic mice carrying Searle's X-autosome translocation. Experimental Cell Research 133, 357362.CrossRefGoogle ScholarPubMed
Eicher, E. M., Nesbitt, M. N. & Francke, V. (1972). Cytological identification of the chromosomes involved in Searle's translocation and the location of the centromere in the X-chromosome of the mouse. Genetics 71, 643648.CrossRefGoogle ScholarPubMed
Gustavsson, I., Fraccaro, M., Tiepolo, L. & Lindsten, J. (1968). Presumptive X-autosome translocation in a cow: preferential inactivation of the normal X-chromosome. Nature (London) 218, 183185.CrossRefGoogle Scholar
Hagemeijer, J., Hoovers, E. M., Smit, E. & Bootsma, D. (1977). Replication pattern of the X-chromosomes in three X-autosomal translocations. Cytogenetics and Cellular Genetics 18, 333348.CrossRefGoogle ScholarPubMed
Harper, M., Fosten, M. & Monk, M. (1982). Preferential paternal X-inactivation in extra-embryonic tissues of early mouse embryos. Journal of Embryology and Experimental Morphology. (In the Press.)Google Scholar
Johnston, P. G. (1981). X chromosome activity in female germ cells of mice heterozygous for Searle's translocation T(X;16)16H. Genetical Research 37, 317322.CrossRefGoogle ScholarPubMed
Johnston, P. G. & Cattanach, B. M. (1981). Controlling elements in the mouse. IV. Evidence of non-random X-inactivation. Genetical Research 37, 151160.CrossRefGoogle ScholarPubMed
Laurent, C., Biemont, M.-CL. & Dutrillaux, B. (1975). Sur quatre nouveaux cas de translocation du chromosome X chez l'homme. Humangenetik 26, 3546.Google Scholar
Leisti, J. T., Kaback, M. M. & Rimoin, D. L. (1975). Human X-autosome translocations: differential inactivation of the X-chromosome in a kindred with an X-9 translocation. American Journal of Human Genetics 27, 441453.Google Scholar
Levak-Švajger, B., Švajger, A. & Škreb, N. (1969). Separation of germ-layers in presomite rat embryos. Experientia 25, 13111312.CrossRefGoogle Scholar
Lyon, M. F. (1961). Gene action in the X-chromosome of the mouse, Mus musculus. Nature (London) 190, 372373.CrossRefGoogle ScholarPubMed
Lyon, M. F. (1966 a). Order of loci on the Jf-chromosome of the mouse. Genetical Research 7, 130133.CrossRefGoogle ScholarPubMed
Lyon, M. F. (1966 b). Lack of evidence that inactivation of the mouse X-chromosome is incomplete. Genetical Research 8, 197203.CrossRefGoogle ScholarPubMed
Lyon, M. F., Searle, A. G., Ford, C. E. & Ohno, S. (1964). A mouse translocation suppressing sex-linked variegation. Cytogenetics 3, 306323.CrossRefGoogle ScholarPubMed
McMahon, A. (1981). Cell differentiation and X-chromosome activity in the definitive germ -layers and the germ-line of the mouse. Ph.D. Thesis, University of London.Google Scholar
McMahon, A., Fosten, M. & Monk, M. (1981). Random X-chromosome inactivation in female primordial germ cells in the mouse. Journal of Embryology and Experimental Morphology 64, 251258.Google ScholarPubMed
McMahon, A., Fosten, M. & Monk, M. (1982). X chromosome inactivation mosaicism in the three germ layers and the germ line of the mouse embryo. Journal of Embryology and Experimental Morphology. (In press.)Google Scholar
Monk, M. & Harper, M. (1979). Sequential X-chromosome inactivation coupled with cellular differentiation in early mouse embryos. Nature (London) 281, 311313.CrossRefGoogle ScholarPubMed
Nielsen, J. T. & Chapman, V. M. (1977). Electrophoretic variation for X-chromosome-linked phosphoglycerate kinase (PGK-1) in the mouse. Genetics 87, 319325.CrossRefGoogle ScholarPubMed
Ohno, S. (1967). Three different consequences of X-autosome translocation. In Sex Chromosomes and Sex Linked Genes, pp. 123135. New York: Springer Verlag.CrossRefGoogle Scholar
Ohno, S. & Cattanach, B. M. (1962). Cytological study of an X-autosome translocation in Mus musculus. Cytogenetics 1, 129140.CrossRefGoogle ScholarPubMed
Ohno, S. & Lyon, M. F. (1965). Cytological study of Searle's X-autosome translocation in Mus musculus. Chromosomu (Berlin) 16, 90100.CrossRefGoogle ScholarPubMed
Rastan, S., Kaufman, M. H., Handyside, A. H. & Lyon, M. F. (1980). X-chromosome inactivation in extra-embryonic membranes of diploid parthenogenetic mouse embryos demonstrated by differential staining. Nature 288, 172173.CrossRefGoogle ScholarPubMed
Russell, L. B. (1963). Mammalian X-chromosome action: inactivation limited in spread and in region of origin. Science 140, 976978.CrossRefGoogle ScholarPubMed
Russell, L. B. & Montgomery, C. S. (1970). Comparative studies on X-autosome translocations in the mouse. II. Inactivation of autosomal loci, segregation and mapping of autosomal breakpoints in five T(X);l)'s. Genetics 64, 281312.CrossRefGoogle Scholar
Russell, L. B. & Cacheiro, N. L. A. (1978). The use of mouse X-autosome translocations in the study of X-inactivation pathways and nonrandomness. In Genetic Mosaics and Chimaeras in Mammals, Basic Life Science, vol. 12 (ed. Russell, L. B.). New York: Plenum Press.CrossRefGoogle Scholar
Searle, A. G. (1962). Is sex-linked Tabby really recessive in the mouse? Heredity 17, 297.Google Scholar
Snow, M. H. L. & Tam, P. P. L. (1979). Is compensatory growth a complicating factor in mouse teratology? Nature (London) 279, 555557.CrossRefGoogle ScholarPubMed
Takagi, N. (1980). Primary and secondary non-random X-chromosome inactivation in early female mouse embryos carrying Searle's translocation T(X; 16)16H. Chromosomu (Berlin) 81, 439459.CrossRefGoogle Scholar
Thelen, T. H., Abrams, D. J. & Fisch, R. O. (1971). Multiple abnormalities due to possible genetic inactivation in an X-autosome translocation. American Journal of Human Genetics 23, 410418.Google Scholar
Therman, E. & Pätau, K. (1974). Abnormal X-chromosomes in man: origin, behaviour and effects. Humangenetik 25, 116.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. I., 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
Whittingham, D. G. & Wales, R. G. (1969). Storage of two cell mouse embryos in vitro. Australian Journal of Biological Science 22, 10651068.CrossRefGoogle ScholarPubMed