Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-26T15:06:21.688Z Has data issue: false hasContentIssue false
  • English
  • Français

The relationship between position and expression of genes on the kangaroo X chromosome suggests a tissue-specific spread of inactivation from a single control site

Published online by Cambridge University Press:  14 April 2009

Jennifer A. Marshall Graves  and
Garey W. Dawson
Jennifer A. Marshall Graves*
Affiliation:
Department of Genetics and Human Variation, La Trobe University, Bundoora, Victoria 3083, Australia
Garey W. Dawson
Affiliation:
Department of Genetics and Human Variation, La Trobe University, Bundoora, Victoria 3083, Australia
*
* 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.

In marsupials, X chromosome inactivation is paternal and incomplete. The tissue-specific pattern of inactivation of X-linked loci (G6PD, PGK, GLA) has been attributed to a piecemeal inactivation of different regions of the X. We here propose an alternative hypothesis, in which inactivation of the marsupial X is a chromosome-wide event, but is differentially regulated in different tissues. This hypothesis was suggested by the relationship between the positions and activity of genes on the kangaroo paternal X. In the absence of an HPRT polymorphism, we have used somatic cell hybridization to assess the activity of the paternal HPRT allele in lymphocytes and fibroblasts. The absence of the paternal X, and of the paternal forms of G6PD or PGK, from 33 cell hybrids made by fusing HPRT-deficient rodent cells with lymphocytes or fibroblasts of heterozygous females, suggests that the HPRT gene on the paternal X is inactive in both tissues and therefore not selectable. Since HPRT is located medially on the Xq near GLA, which shares the same characteristics of activity, we suggest that the locus-specific and tissue-specific patterns of activity result from a differential spread of inactivation from a single control locus, located near HPRT and GLA, outwards in both directions to G6PD and PGK. The nucleolus organizer region on the short arm does not seem to be part of the inactivated unit.

Type
Research Article
Information
Genetics Research , Volume 51 , Issue 2 , April 1988 , pp. 103 - 109
Copyright
Copyright © Cambridge University Press 1988

References

Air, G. M., Thompson, E. O. P., Richardson, B. J. & Sharman, G. B. (1971). Amino acid sequences of kangaroo myoglobulin and haemoglobin, and the date of marsupial–eutherian divergence. Nature 229, 391–394.CrossRefGoogle Scholar
Cattanach, B. M. (1975). Control of chromosome inactivation. Annual Review of Genetics 9, 1–18.CrossRefGoogle ScholarPubMed
Cooper, D. W., Johnston, P. G., Murtagh, C. E., Sharman, G. B., VandeBerg, J. L. & Poole, W. E. (1975). Sex linked isozymes and sex chromosome evolution and inactivation in Australian marsupials and monotremes. In Isozymes, III Developmental Biology, (ed. Markert, C. L.), pp. 559–573. New York: Academic Press.Google Scholar
Cooper, D. W., Edwards, C., James, E., Sharman, G. B., VandeBerg, J. L. & Graves, J. A. M. (1977). Studies on metatherian sex chromosomes VI. A third state of an X-linked gene: partial activity for the paternally derived Pgk-A allele in cultured fibroblasts of Macropus giganteus and M. parryi. Australian Journal of Biological Sciences 30; 431–443.CrossRefGoogle Scholar
Cooper, D. W., Woolley, P. A., Maynes, G. M., Sherman, F. S. & Poole, W. E. (1983). Studies on metatherian sex chromosomes. XII. Sex-linked inheritance and probable paternal X-inactivation of α-galactosidase A in Australian marsupials. Australian Journal of Biological Sciences 36, 511–517.CrossRefGoogle ScholarPubMed
Dawson, G. W. & Graves, J. A. M. (1984). Gene mapping in marsupials and monotremes. I. The chromosomes of rodent-marsupial (Macropus) cell hybrids, and gene assignments to the X chromosome of the grey kangaroo. Chromosoma 91, 20–27.CrossRefGoogle Scholar
Dawson, G. W. & Graves, J. A. M. (1986). Gene mapping in marsupials and monotremes. III. Assignment of four genes to the X chromosome of the wallaroo and the euro (Macropus robustus). Cytogenetics and Cell Genetics 42, 80–84.Google Scholar
Dobrovic, A. & Graves, J. A. M. (1986). Gene mapping in marsupials and monotremes. II. Assignments to the X chromosome of dasyurid marsupials. Cytogenetics and Cell Genetics 41, 9–13.CrossRefGoogle Scholar
Donald, J. A. & Hope, R. M. (1981). Mapping a marsupial X chromosome using kangaroo–mouse somatic cell hybrids. Cytogenetics and Cell Genetics 29, 127–137.CrossRefGoogle ScholarPubMed
Goodpasture, C. & Bloom, S. E. (1975). Visualization of the nucleolus organizer regions in mammalian chromosomes using silver staining. Chromosoma 53, 37–50.CrossRefGoogle ScholarPubMed
Graves, J. A. M. (1983). Inactivation and reactivation of the mammalian X chromosome – on the threshold of molecular biology. In Development in Mammals, vol. 5, (ed. M. H. Johnson), pp. 251–295.Google Scholar
Graves, J. A. M., Chew, G. K., Cooper, D. W. & Johnston, P. G. (1979). Marsupial–mouse cell hybrids containing fragments of the marsupial X chromosome. Somatic Cell Genetics 5, 481–489.CrossRefGoogle ScholarPubMed
Hayman, D. L. & Rofe, R. H. (1977). Marsupial sex chromosomes. In Reproduction and Evolution, ed. Calaby, J. H. and Tyndale-Biscoe, C. H.. Canberra: Australian Academy of Science.Google Scholar
Hope, R. M. & Graves, J. A. M. (1978). Fusion and hybridization of marsupial and eutherian cells. V. Development of selective systems. Australian Journal of Biological Science 31, 293–301.CrossRefGoogle ScholarPubMed
Lyon, M. F. (1961). Gene action in the X chromosome of the mouse (Mus musculus L.). Nature 190, 372–373.Google Scholar
Migeon, B. R., Shapiro, L. J., Norum, R. A., Mohandas, T. & Axelman, J. (1982). Differential expression of steroid sulphatase locus on active and inactive human X chromosomes. Nature 299, 838–840.CrossRefGoogle Scholar
Migeon, B. R., Wolf, S. F., Axelman, J., Kaslow, D. C. & Schmidt, M. (1985). Incomplete X chromosome dosage compensation in chorionic villi of human placenta. Proceedings of the National Academy of Sciences, USA 82, 3390–3394.CrossRefGoogle ScholarPubMed
Miller, O. J., Miller, D. A., Dev, V. G., Tantravahi, R. & Croce, C. M. (1976). Expression of human and suppression of mouse nucleolus organizer activity in mouse–human somatic cell hybrids. Proceedings of the National Academy of Sciences, USA 73, 4531–4535.CrossRefGoogle ScholarPubMed
Robins, A. J., Hayman, D. L. & Wells, J. R. E. (1984). Ribosomal gene reiteration in a marsupial species with an X-linked nucleolar organizer. Australian Journal of Biological Science 37, 211–216.CrossRefGoogle Scholar
Russell, L. B. (1963). Mammalian X chromosome action: inactivation limited in spread and region of origin. Science 140, 976.Google Scholar
Samollow, P. B., Ford, A. L. & VandeBerg, J. L. (1987). X-linked gene expression in the Virginia opossum: differences between the paternally derived Gpd and Pgk-A loci. Genetics 115, 185–195.CrossRefGoogle ScholarPubMed
Szybalski, W., Szybalska, E. H. & Ragni, G. (1962). Genetic studies with human cell lines. National Cancer Institute Monogaph 7, 75–89.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, 240–248.CrossRefGoogle ScholarPubMed
Therman, E., Sarto, G. E., Palmer, C. G., Kallio, H. & Denniston, C. (1979). Position of the human X inactivation centre on Xq-Human Genetics 50, 59–64.Google Scholar
VandeBerg, J. L., Cooper, D. W. & Sharman, G. B. (1977). Studies on metatherian sex chromosomes, V. Activity of the paternally derived allele at the X-linked Pgk-A locus in some tissues of the kangaroos Macropus giganteus and M. parryi. Australian Journal of Biological Science 30, 421–430.CrossRefGoogle Scholar
VandeBerg, J. L., Robinson, E. S., Samollow, P. B. & Johnston, P. G. (1987). X linked gene expression and X chromosome inactivation: marsupials, mouse and man compared. In Isozymes: Current Topics in Biological and Medical Research 15, 225–253.Google Scholar
Wrigley, J. M. & Graves, J. A. M. (1988). Sex chromosome homology and incomplete, tissue-specific X inactivation suggests that monotremes represent an intermediate stage of mammalian sex chromosome evolution. J. Heredity (In the Press.)CrossRefGoogle Scholar