Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-12-01T01:51:25.288Z Has data issue: false hasContentIssue false

The differential staining pattern of the X chromosome in the embryonic and extraembryonic tissues of postimplantation homozygous tetraploid mouse embryos

Published online by Cambridge University Press:  14 April 2009

S. Webb
Affiliation:
Department of Anatomy, University Medical School, Teviot Place, Edinburgh EH8 9AG, U.K.
T. J. de Vries
Affiliation:
Department of Anatomy, University Medical School, Teviot Place, Edinburgh EH8 9AG, U.K.
M. H. Kaufman*
Affiliation:
Department of Anatomy, University Medical School, Teviot Place, Edinburgh EH8 9AG, U.K.
*
* Corresponding author.
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.

(C57BL × CBA)F1 hybrid female mice were mated with hemizygous Rb(X.2)2Ad males to distinguish the paternal X chromosome. Homozygous tetraploids were produced by blastomere fusion at the 2-cell stage, and 161 of these were transferred to recipients and analysed on the 10th day of gestation. 59 implants contained resorptions and 76 contained either an embryo and/or extraembryonic membranes. 38 (20, XXXX and 18, XXYY) were analysed to investigate their X-inactivation pattern. Embryonic and yolk sac endodermally- and mesodermally-derived samples were analysed by G-banding and by Kanda analysis. In the XX and XY controls, the predicted pattern of X-inactivation was observed, though 12·2% of metaphases in the XX series displayed no X-inactivation. In the XY series the Y chromosome was seen in a high proportion of metaphases.

In the XXXX tetraploids, 8 cell lineages were recognized with regard to their X-inactivation pattern, though most belonged to the following 3 categories: (XmXm)XpXp, Xm(XmXp)Xp and XmXm(XpXp). The other categories were only rarely encountered. In the embryonic and mesodermally-derived tissue the ratio of these groups was close to 1:2:1, whereas in the endodermally-derived tissue it was 1:4·11:4·88, due to preferential paternal X-inactivation. A significant but small proportion of all 3 tissues analysed displayed no evidence of X-inactivation. Indirect evidence suggests that this represents a genuine group because of the high efficiency of the Kanda staining. The presence of the Xm(XmXp)Xp category is consistent with the expectation that X-inactivation occurs randomly in 2 of the 4 X chromosomes present. The presence of small numbers of preparations with no evidence of X-inactivation and other unexpected categories suggests that these are probably selected against during development.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

References

Adler, I. D.Johannisson, R. & Winking, H. (1989). The influence of the Robertsonian translocation Rb(X.2)2Ad on anaphase I non-disjunction in male laboratory mice. Genetical Research 53, 7786.CrossRefGoogle Scholar
Boué, J.Boué, A. & Lazar, P. (1975). The epidemiology of human spontaneous abortions with chromosomal anomalies. In Aging Gametes: Their Biology and Pathology (ed. Blandau, R. J.), pp. 330348. Basel: Karger, S..Google Scholar
Dyban, A. P. & Baranov, V. S. (1987). Cytogenetics of Mammalian Embryonic Development. Oxford: Clarendon Press.Google Scholar
Eglitis, M. A. (1980). Formation of tetraploid mouse blastocysts following blastomere fusion with polyethylene glycol. Journal of Experimental Zoology 213, 309313.Google Scholar
Eglitis, M. A. & Wiley, L. M. (1981). Tetraploidy and early development, effects on Cellularity timing and embryonic metabolism. Journal of Embryology and Experimental Morphology 66, 91108.Google Scholar
Endo, S.Takagi, N. & Sasaki, M. (1982). The late replicating X chromosome in digynous mouse triploid embryos. Developmenta Genetics 3, 165176.Google Scholar
Evans, E. P.Burtenshaw, M. D. & Ford, C. E. (1972). Chromosomes of mouse embryos and newborn young, preparations from membranes and tail tips. Stain Technology 47, 229234.Google Scholar
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 Scholar
Frels, W. I.Rossant, J. & Chapman, V. M. (1979). Maternal X chromosome expression in mouse chorionic ectoderm. Cellularity Genetics 1, 123132.Google Scholar
Golbus, M. S.Bachman, R.Wiltse, S. & Hall, B. D. (1976). Tetraploidy in a newborn infant. Journal of Medical Genetics 13, 329332.CrossRefGoogle Scholar
Graham, C. F. (1971). Virus assisted fusion of embryonic cells. Ada Endocrinologica, Suppl. 153, 154165.Google ScholarPubMed
Harper, M. I.Fosten, M. & Monk, M. (1982). Preferential paternal X-inactivation in extra-embryonic tissues of early mouse embryos. Journal of Embryology and Experimental Morphology 67, 127135.Google Scholar
Hassold, T.Chen, N.Funkhouser, J.Jooss, T.Manuel, B.Matsuura, J.Matsuyama, A.Wilson, C.Yamane, J. A. & Jacobs, P. A. (1980). A cytogenetic study of 1000 spontaneous abortions. Annals of Human Genetics 44, 151178.Google Scholar
Kanda, N. (1973). A new differential technique for staining the heteropycnotic X-chromosome in female mice. Experimental Cell Research 80, 463–167.Google Scholar
Kaufman, M. H. (1991). Histochemical identification of primordial germ cells and differentiation of the gonads in homozygous tetraploid mouse embryos. Journal of Anatomy 179, 169181.Google Scholar
Kaufman, M. H. (1992). Postcranial morphological features of homozygous tetraploid mouse embryos. Journal of Anatomy (in the press).Google Scholar
Kaufman, M. H. & Webb, S. (1990). Postimplantation development of tetraploid mouse embryos produced by electrofusion. Development 110, 11211132.Google Scholar
Kubiak, J. Z. & Tarkowski, A. K. (1985). Electrofusion of mouse blastomeres. Experimental Cell Research 157, 561566.Google Scholar
Levak-Svajger, B.Svajger, A. & Skreb, N. (1969). Separation of germ layers in presomite rat embryos. Experientia 25, 13111313.Google Scholar
Lin, C. CDe Braekeleer, N. & Jamro, H. (1985). Cytogenetic studies in spontaneous abortions: the Calgary experience. Canadian Journal of Genetics and Cytology 27, 565570.Google Scholar
Lyon, M. F. (1961). Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190 372373.Google Scholar
Lyon, M. F. (1962). X-chromosome inactivation and Cellularity patterns in mammals. Biological Reviews 47, 135.CrossRefGoogle Scholar
Monk, M. (1978). Biochemical studies on mammalian X chromosome activity. In Development in Mammals, Vol. 3 (ed. Johnson, M. H.) pp. 189224. Amsterdam: North-Holland.Google Scholar
Monk, M. (1981). A stem-line model for cellular and chromosomal differentiation in early mouse development. Differentiation 19, 7176.Google Scholar
Monk, M. & Harper, M. I. (1979). Sequential X chromosome inactivation coupled with cellular differentiation in early mouse embryos. Nature 281, 311313.Google Scholar
O'Neill, G. T.Speirs, S. & Kaufman, M. H. (1990). Sexchromosome constitution of postimplantation tetraploid mouse embryos. Cytogenetics and Cell Genetics 53, 191195.Google Scholar
Ozil, J. & Modliński, J. A. (1986). Effects of electric field on fusion rate and survival of 2-cell rabbit embryos. Journal of Embryology and Experimental Morphology 96, 211228.Google ScholarPubMed
Pajares, I. L.Delicado, A.Diaz de Bustamente, A.Pellicer, A.Pinel, I.Pardo, M. & Martin, M. (1990). Tetraploidy in a liveborn infant. Journal of Medical Genetics 27, 782783.CrossRefGoogle Scholar
Quinn, P.Barros, C. & Whittingham, D. G. (1982). Preservation of hamster oocytes to assay the fertilizing capacity of human spermatozoa. Journal of Reproduction and Fertility 66, 161168.CrossRefGoogle ScholarPubMed
Pitt, D.Leversha, M.Sinfield, C.Campbell, P.Anderson, R.Bryan, D. & Rogers, J. (1981). Tetraploidy in a liveborn infant with spina bifida and other anomalies. Journal of Medical Genetics 18, 309311.Google Scholar
Rastan, S.Kaufman, M. H.Handyside, A. H. & Lyon, M. F. (1980). X-chromosome inactivation in extraembryonic membranes of diploid parthenogenetic mouse embryos demonstrated by differential staining. Nature 288, 172173.Google Scholar
Sheppard, D. M.Fisher, R. A.Lawler, S. D. & Povey, S. (1982). Tetraploid conceptus with three paternal contributions. Human Genetics 62, 371374.Google Scholar
Snow, M. H. L. (1973). Tetraploid mouse embryos produced by cytochalasin B during cleavage. Nature 244, 513515.Google Scholar
Snow, M. H. L. (1975). Embryonic development of tetraploid mice during the second half of gestation. Journal of Embryology and Experimental Morphology 34, 707721.Google Scholar
Snow, M. H. L. (1976). The immediate postimplantation development of tetraploid mouse blastocysts. Journal of Embryology and Experimental Morphology 35, 8186.Google Scholar
Speirs, S.Cross, J. M. & Kaufman, M. H. (1990). The pattern of X-chromosome inactivation in the embryonic and extra-embryonic tissues of post-implantation digynic triploid LT/Sv strain mouse embryos. Genetical Research 56, 107114.Google Scholar
Speirs, S. & Kaufman, M. H. (1989). Analysis of the sex chromosome constitution of digynic triploid mouse embryos. Cytogenetics and Cell Genetics 52, 151153.Google Scholar
Surti, U. (1987). Genetic concepts and techniques. In Gestational Trophoblastic Disease (ed. Szulman, A. E. and Buchsbaum, H. J.), pp. 111121. Berlin: Springer.Google Scholar
Surti, U.Szulman, A. E.Wagner, K.Leppert, M. & O'Brien, S. J. (1986). Tetraploid partial hydatidiform moles: two cases with a triple paternal contribution and a 92.XXXY karyotype. Human Genetics 72, 1521.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.Google Scholar
Takagi, N.Wake, N. & Sasaki, M. (1978). Cytologic evidence for preferential inactivation of the paternally derived X chromosome in XX mouse blastocysts. Cytogenetics and Cell Genetics 20, 240248.Google Scholar
Tarkowski, A. K.Witkowska, A. & Opas, J. (1977). Development of cytochalasin B-induced tetraploid and diploid/tetraploid mosaic mouse embryos. Journal of Embryology and Experimental Morphology 41, 4764.Google 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.Google Scholar
Whittingham, D. G. (1971). Culture of mouse ova. Journal of Reproduction and Fertility, Supplement 14 721.Google ScholarPubMed
Wilson, G. N.Vekemans, M. J. J. & Kaplan, P. (1988). MCA/MR syndrome in a female infant with tetraploidy mosaicism: review of the human polyploid phenotype. American Journal of Medical Genetics 30, 953961.Google Scholar