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Insights into X chromosome inactivation from studies of species variation, DNA methylation and replication, and vice versa

Published online by Cambridge University Press:  14 April 2009

Barbara R. Migeon
Barbara R. Migeon
Affiliation:
Department of Pediatrics and The Center for Medical Genetics, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21210, USA
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I am indebted to Mary Lyon as her X-inactivation hypothesis stimulated my mentor, Barton Childs, and in turn, myself, to think about the consequences of X-inactivation in heterozygous females. I often reread her original papers setting forth the single active X hypothesis, and still marvel at the concise and compelling exposition of the hypothesis and the logical predictions which seemed prophetic at my first reading, and have survived the test of time.

My contribution to this Festschrift reviews evidence derived from studies of DNA methylation, species variation and DNA replication that reveals an important role for methylated CpG islands and suggests a role for late DNA replication in propagating X inactivation from one cell to its progeny. These studies also show that X inactivation is a powerful research tool for identifying the factors which program and maintain developmental processes.

Type
Research Article
Information
Genetics Research , Volume 56 , Issue 2-3 , October 1990 , pp. 91 - 98
Copyright
Copyright © Cambridge University Press 1990

References

Barton, S. C., Surani, M. A. H. & Norris, M. L. (1984). Role of paternal and maternal genomes in mouse development. Nature 311, 374–376.CrossRefGoogle ScholarPubMed
Beggs, A. H. & Migeon, B. R. (1989). Studies of chromatin loop structure of the human X chromosome: relevance to X inactivation and CpG clusters. Molecular & Cellular Biology 9, 2322–2331.Google Scholar
Bird, A. P. (1986). CpG-rich islands and the function of DNA methylation. Nature 321, 209–213.CrossRefGoogle ScholarPubMed
Brown, C. J. & Willard, H. F. (1989). Non-inactivation of a Selectable Human X-linked Gene that Complements a Murine Temperature-sensitive Cell Cycle Defect. The American Journal of Human Genetics 45, 592–598.Google Scholar
Cattanach, B. M. & Kirk, M. (1985). Differential activity of maternally and paternally derived chromosome regions in mice. Nature 315, 496–498.CrossRefGoogle ScholarPubMed
Chapman, V. M. (1985). X chromosome regulation in female mammals, in Genetic Manipulation of the Early Mammalian Embryo, (edited by Constantini, F. & Jaenisch, R.) Banbury Report 20, 11–19.Google Scholar
Cooper, D. W., VandeBerg, J. L., Sharman, G. B. & Poole, W. E. (1971). Phosphoglycerate kinase polymorphism in kangaroos provides further evidence of paternal X inactivation. Nature New Biology 230, 155–157.CrossRefGoogle ScholarPubMed
Cooper, D. N. & Youssoufian, H. (1988). The CpG dinucleotide and human genetic disease. Human Genetics 78, 151–155.Google Scholar
Driscoll, D. J. & Migeon, B. R. (1989). Evidence for lack of DNA methylation in human fetal germ cells: Relevance to parental chromosome imprinting and CpG mutation. The American Journal of Human Genetics 45, A111.Google Scholar
Driscoll, D. J. & Migeon, B. R. (1990). Sex difference in methylation of single copy genes in human meiotic germ cells: Implications for X chromosome inactivation, parental imprinting and origin of CpG mutations. Somatic Cell and Molecular Genetics 16, 267–282.Google Scholar
Frels, W. I., Rossant, J. & Chapman, V. M. (1980). Maternal X chromosome expression in mouse chorionic ectoderm. Developmental Genetics 1, 124–132.Google Scholar
Gartler, S. M., Andina, R. & Gant, N. (1975). Ontogeny of X-chromosome inactivation in the female germ line. Experimental Cell Research 91, 454–457.CrossRefGoogle ScholarPubMed
Gartler, S. M. & Riggs, A. D. (1983). Mammalian X chromosome inactivation. Annual Review of Genetics 17, 155–170.CrossRefGoogle ScholarPubMed
Goldman, M. A. (1988). The chromatin domain as a unit of gene regulation. Bioessays 9, 50–55.CrossRefGoogle ScholarPubMed
Goldman, M. A., Holmquist, G. P., Gray, M. C., Caston, L. A. & Nag, A. (1984). Replication timing of genes and middle repetitive sequences. Science 224, 686–692.Google Scholar
Goldman, M. A., Stokes, K. R., Idzerda, R. L., McKnight, G. S., Hammer, R. E., Brinster, R. L. & Gartler, S. M. (1987). A chicken transferrin gene on the X chromosome of transgenic mice escapes X chromosome inactivation. Science 236, 593–595.CrossRefGoogle ScholarPubMed
Goodfellow, P. N., Pym, B., Pritchard, C., Ellis, N., Palmer, M., Smith, M. & Goodfellow, P. J. (1988). MIC2: a human pseudoautosomal gene. Philosophical Transactions of the Royal Society of London B 322, 145–154.Google ScholarPubMed
Grant, S. G. & Chapman, V. M. (1988). Mechanisms of X-Chromosome Regulation. Annual Review of Genetics 22, 199–233.CrossRefGoogle ScholarPubMed
Gutierrez, A. G., Christensen, A. C., Manning, J. E. & Lucchesi, J. C. (1989). Cloning and Dosage compensation of the 6-phosphogluconate dehydrogenase gene (Pdg + ) of Drosophila melanogaster. Developmental Genetics 10, 155–161.CrossRefGoogle Scholar
Handel, M. A. (1987). Genetic control of spermatogenesis. In Results and Problems in Cell Differentiation (ed. Hennig, W., vol. 15, pp. 1–62, Berlin, Springer-Verlag.Google Scholar
Hannibal, M., Ruta, Cullen C., Kaslow, D. C., Davies, K. E. & Migeon, B. R. (1986). Evidence that sex differences in methylation of the ornithine transcarbamylase locus on the X chromosome are not functional. The American Journal of Human Genetics 39, A 201.Google Scholar
Harrison, K. B. (1988). X Chromosome inactivation is isolated human cytotrophoblast. The American Journal of Human Genetics 43, A 130.Google Scholar
Holliday, R. & Pugh, J. E. (1975). DNA modification mechanisms and gene activity during development. Science 187, 226–232.Google Scholar
Holmquist, G. P. (1987). Role of replication time in the control of tissue-specific expression. American Journal Human Genetics 40, 151–173.Google Scholar
Johnston, P. G. & Robinson, E. S. (1985). Glucose-6-phosphate dehydrogenase expression in heterozygous kangaroo embryos and extra-embryonic membranes. Genetical Research 45, 205–208.CrossRefGoogle ScholarPubMed
Johnston, P. G. & Robinson, E. S. (1987). X chromosome inactivation in female embryos of a marsupial mouse (Antechinus stuartii). Chromosoma (Berlin) 95, 419–423.CrossRefGoogle ScholarPubMed
Johnston, P. G., Sharman, G. B., James, E. A. & Cooper, D. W. (1978). Studies on metatherian sex chromosomes. VII. Glucose-6-phosphate dehydrogenase expression in tissues and cultured fibroblasts of kangaroos. Australian Journal Biological Science 31, 415–424.Google Scholar
Kahan, B. & DeMars, R. (1975). Localized derepression on the human inactive X chromosome in mouse-human cell hybrids. Proceedings National Academy Science USA 72, 1510–1514.CrossRefGoogle ScholarPubMed
Kaslow, D. C. & Migeon, B. R. (1987). DNA methylation stabilizes X chromosome inactivation in eutherians, but not in marsupials: evidence for multi-step maintenance of mammalian X dosage compensation. Proceedings National Academy Science USA 84, 6210–6214.Google Scholar
Keith, D. H., Singer-Sam, J. & Riggs, A. D. (1986). Active X chromosome DNA is unmethylated at eight CCGG sites clustered in a guanine-plus-rich island at the 5′ end of the gene for phosphoglycerate kinase. Molecular & Cellular Biology 6, 4122–4125.Google Scholar
Kratzer, P. G. & Chapman, V. M. (1981). X chromosome reactivation in oocytes of MUS caroli. Proceedings National Academy Science USA 78, 3093–3097.CrossRefGoogle ScholarPubMed
Krumlauf, R., Chapman, V. M., Hammer, R. E., Brinster, R. & Tilghman, S. M. (1986). Differential expression of fetoprotein genes on the inactive X chromosome in extraembryonic and somatic tissues of a transgenic mouse line. Nature 319, 224–226.Google Scholar
Lester, S. C., Korn, N. J. & DeMars, R. (1982). Derepression of genes on the human inactive X chromosome: evidence for differences in locus specific rates of derepression and rates of active and inactive genes after DNA-mediated transformation. Somatic Cell Genetics 8, 265–284.Google Scholar
Liskay, R. M. & Evans, R. J. (1980). Inactive X chromosome DNA does not function in DNA-mediated cell transformation for the hypoxanthine phosphoribosyl transferase gene. Proceedings National Academy Science USA 77, 4895–4898.Google Scholar
Lock, L. F., Takagi, N. & Martin, G. R. (1987). Methylation of the HPRT gene on the inactive X occurs after chromosome inactivation. Cell 48, 39–46.CrossRefGoogle ScholarPubMed
Lucchesi, J. C. & Manning, J. E. (1987). Gene dosage compensation in Drosophila Melanogaster. Advances in Genetics 24, 371–429.CrossRefGoogle ScholarPubMed
Lyon, M. F. (1989). X-chromosome inactivation as a system of dosage compensation to regulate gene expression. Progress in Nucleic Acid Research & Molecular Biology 36, 119–130.CrossRefGoogle ScholarPubMed
Lyon, M. F. & Rastan, S. (1984). Parental source of chromosome imprinting and its relevance for X chromosome inactivation. Differentiation 26, 63–67.Google Scholar
McCarrey, J. & Thomas, K. (1987). Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326, 501–505.Google Scholar
Migeon, B. R., Axelman, J. & Beggs, A. (1988). Effect of ageing on expression and reactivation of the human X-linked Hprt locus. Nature 335, 93–96.CrossRefGoogle Scholar
Migeon, B. R., Jan de Beur, S. & Axelman, J. (1989). Frequent Derepression of G6Pd and HPRT on the Marsupial Inactive X Chromosome Associated with Cell Proliferation in Vitro. Experimental Cell Research 182, 596–609.Google Scholar
Migeon, B. R., Schmidt, M., Axelman, J. & Ruta, Cullen C. (1986). Complete reactivation of X chromosomes from human chorionic villi with a switch to early DNA replication. Proceedings National Academy Science USA 83, 2182–2186.Google Scholar
Migeon, B. R., Shapiro, L. J., Norum, R. A., Mohandas, T., Axelman, J. & Dabora, R. L. (1982 a). Differential expression of the steroid sulfatase locus on the active and inactive human X chromosome. Nature 299, 838–840.CrossRefGoogle ScholarPubMed
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 National Academy Science USA 82, 3390–3394.Google Scholar
Migeon, B. R., Wolf, S. F., Mareni, C. & Axelman, J. (1982 b). Derepression with decreased expression of the G6PD locus on the inactive X chromosome in normal human cells. Cell 29, 595–600.Google Scholar
Mohandas, T., Geller, R. L., Yen, P. H., Rosendorff, J., Bernstein, R., Yoshida, A. & Shapiro, L. J. (1987). Cytogenetic and molecular studies on a recombinant human X chromosome: Implications for the spreading of X chromosome inactivation. Proceedings of the National Academy of Sciences USA 84, 5954–4958.CrossRefGoogle ScholarPubMed
Mohandas, T. T., Sparkes, R. S., Bishop, D. F., Desnick, R. J. & Shapiro, L. J. (1984). Frequency of reactivation and variability in expression of X-linked enzyme loci. The American Journal of Human Genetics 36, 916–925.Google ScholarPubMed
Mohandas, T., Sparkes, R. S. & Shapiro, L. J. (1981). Reactivation of an inactive human X chromosome: evidence for X inactivation by DNA methylation. Science 211, 393–396.CrossRefGoogle ScholarPubMed
Monk, M., Boubelik, M. & Lehnert, S. (1987). Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99, 371–382.Google Scholar
Monk, M. & Harper, M. I. (1979). Sequential X chromosome inactivation coupled with cellular differentiation in early embryos. Nature 281, 311–313.CrossRefGoogle Scholar
Mullins, L. J., Veres, G., Caskey, C. T. & Chapman, V. (1987). Differential methylation of the ornithine carbamoyl transferase gene on active and inactive X chromosomes. Molecular & Cellular Biology 7, 3916–3922.Google Scholar
Razin, A. & Riggs, A. D. (1980). DNA methylation and gene function. Science 210, 604–610.Google Scholar
Riggs, A. D. (1989). DNA methylation and Cell Memory. Cell Biophysics 15, 1–13.CrossRefGoogle ScholarPubMed
Ruta Cullen, C., Hubberman, P., Kaslow, D. C. & Migeon, B. R. (1986). Comparison of Factor IX methylation on human active and inactive X chromosomes: Implications for X inactivation and transcription of tissue-specific genes. EMBO Journal 9, 2223–2229.CrossRefGoogle Scholar
Sager, R. & Kitchin, R. (1975). Selective silencing of eukaryotic DNA. Science 189, 426–433.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.Google Scholar
Sanford, J. P., Chapman, V. M. & Rossant, J. (1985). DNA methylation in extra-embryonic lineages of mammals. Trends in Genetics 3, 89–93.Google Scholar
Sanford, J. P., Clark, H. J., Chapman, V. M. & Rossant, J. (1987). Differences in DNA methylation during oogenesis and spermatogenesis and their persistence during early embryogenesis in the mouse. Genes & Development 1, 1039–1046.CrossRefGoogle ScholarPubMed
Schmidt, M. & Migeon, B. R. (1990). Asynchronous replication of homologous loci on human active and inactive X chromosomes. Proceedings National Academy Science USA (in the press).CrossRefGoogle Scholar
Schmidt, M., Wolf, S. F. & Migeon, B. R. (1985). Evidence for a relationship between DNA methylation and DNA replication from studies of the 5-azacytidine, reactivated allocyclic X chromosome. Experimental Cell Research 158, 301–310.CrossRefGoogle ScholarPubMed
Schneider-Gadicke, A., Beer-Romero, P., Brown, L. G., Nussbaum, R. & Page, D. C. (1989). The ZFX gene on the human X chromosome escapes X inactivation and is closely related to ZFY, the putative sex determinant on the Y chromosome. Cell 57, 1247–1258.Google Scholar
Takagi, N. & Sasaki, M. (1975). Preferential inactivation of the paternally derived X chromosome in the extra-embryonic membranes of the mouse. Nature 256, 640–642.Google Scholar
Takagi, N., Yoshida, M. A., Sugawara, O. & Sasaki, M. (1983). Reversal of X-inactivation in female mouse somatic cells hybridized with murine teratocarcinoma stem cells in vitro. Cell 34, 1053–1062.Google Scholar
Toniolo, D., Martini, G., Migeon, B. R. & Dono, R. (1988). Expression of the G6PD locus on the human X chromosome is associated with demethylation of three CpG clusters within 100 kb of DNA. EMBO Journal 7, 401–406.Google Scholar
Venolia, L. & Gartler, S. M. (1983). Transformation of Hprt with sperm DNA. Somatic Cell Genetics 9, 617–627.Google Scholar
Warcham, K. A., Lyon, M. F., Glenister, P. H. & Williams, E. D. (1987). Age-related reactivation of an X-linked gene. Nature 327, 725–727.Google Scholar
Wolf, S. F., Dintzis, S., Toniolo, D., Persico, G., Lunnen, K., Axelman, J. & Migeon, B. R. (1984 a). Complete concordance between glucose-6-phosphate dehydrogenase activity and hypomethylation of 3′CpG clusters: implications for X chromosome dosage compensation. Nucleic Acids Research 12, 9333–9348.CrossRefGoogle Scholar
Wolf, S. F., Jolly, D. J., Lunnen, K. D., Friedmann, T. & Migeon, B. R. (1984 b). Methylation of the HPRT locus on the human X: implications for X inactivation. Proceedings National Academy Science USA 81, 2806–2810.CrossRefGoogle Scholar
Wolf, S. F. & Migeon, B. R. (1982). Studies of X-chromosome DNA methylation in normal human cells. Nature 295, 667–671.Google Scholar
Wolf, S. F. & Migeon, B. R. (1985). Clusters of CpG dinucleotides implicated by control elements of housekeeping genes. Nature 314, 467–469.CrossRefGoogle ScholarPubMed
Wolffe, A. P. & Brown, D. D. (1986). DNA replication in vitro erases a Xenopus 5S RNA transcription complex. Cell 47, 217–227.CrossRefGoogle Scholar
Yen, P. H., Patel, P., Chinault, A. C., Mohandas, T. & Shapiro, L. J. (1984). Differential methylation of hypoxanthine phosphoribosyltransferase genes on active and inactive human X-chromosomes. Proceedings National Academy Science USA 81, 1759–1763.Google Scholar