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X inactivation in mammalian testis is correlated with inactive X–specific transcription

Abstract

X chromosome inactivation occurs twice during the mammalian life cycle. In females one of the two X chromosomes of somatic nuclei is inactive, while in males the solitary X chromosome is inactivated during germ cell development. Despite the different properties of the inactivated chromosomes of females and males, the molecular initiation of inactivation may be the same. X inactive–specific transcripts, XIST, are produced from somatic inactivated X chromosomes. We demonstrate here the existence of XIST transcripts in testes of man and mouse. Inactivation of X chromosomes in males, as in females, may thus be mediated through XIST. Conceivably, the silencing of X–linked genes is the price paid for the evolution of successful mechanisms of chromosomal sex determination.

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References

  1. Solari, A.J. The behavior of the XY pair in mammals. Int. Rev. Cytol. 38, 273–317 (1974).

    Article  CAS  Google Scholar 

  2. Davies, K. The essence of inactivity. Nature 349, 15–16 (1991).

    Article  CAS  Google Scholar 

  3. Martin, G.R. X-Chromosome inactivation in mammals. Cell 29, 721–724 (1982).

    Article  CAS  Google Scholar 

  4. Gartler, S.M. & Riggs, A.D. Mammalian X-chromosome inactivation. Ann. Rev. Genet. 17, 155–190 (1983).

    Article  CAS  Google Scholar 

  5. Lifschytz, E. & Lindsley, D.L. The role of X-chromosome inactivation during spermatogenesis. Proc. natn. Acad. Sci. U.S.A. 69, 182–186 (1972).

    Article  CAS  Google Scholar 

  6. Rosenmann, A. et al. Meiotic association between the XY chromosmes and unpaired autosomal elements as a cause of human male sterility. Cytogenet. Cell Genet. 39, 19–29 (1985).

    Article  CAS  Google Scholar 

  7. Richler, C., Uliel, E., Kerem, B. & Wahrman, J. Regions of active chromatin conformation in ‘inactive’ male meiotic sex chromosomes of the mouse. Chromosoma 95, 167–170 (1987).

    Article  CAS  Google Scholar 

  8. Monesi, V. Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse. Chromosoma 17, 11–21 (1965).

    Article  CAS  Google Scholar 

  9. Brown, C.J. et al. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349, 38–44 (1991).

    Article  CAS  Google Scholar 

  10. Brockdorff, N. et al. Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 351, 329–331 (1991).

    Article  CAS  Google Scholar 

  11. Borsani, G. et al. Characterization of a murine gene expressed from the inactive X chromosome. Nature 351, 325–329 (1991).

    Article  CAS  Google Scholar 

  12. Chelly, J., Concordet, J., Kaplan, J. & Kahn, A. Illegitimate transcription: Transcription of any gene in any cell type. Proc. natn. Acad. Sci. U.S.A. 86, 2617–2621 (1989).

    Article  CAS  Google Scholar 

  13. Singer-Sam, J., Robinson, M.O., Bellvé, A.R., Simon, M.I. & Riggs, A.D. Measurement by quantitative PCR of changes in HPRT, PGK-1, PGK-2, APRT, MTase, and Zfy gene transcripts during mouse spermatogenesis. Nucl. Acids Res. 18, 1255–1259 (1990).

    Article  CAS  Google Scholar 

  14. Hotta, Y. & Chandley, A.C. Activities of X-linked enzymes in spermatocytes of mice rendered sterile by chromosomal alterations. Gamete Res. 6, 65–72 (1982).

    Article  CAS  Google Scholar 

  15. Tres, L.L. & Kierszenbaum, A.L. Meiotic chromosomes of mouse spermatocytes: Identification of bivalents, lampbrush organization, and transcription activities, in Bioregulators of Reproduction (eds Jagiello, G. & Vogel, H.J.) 229–256 (Academic Press, New York, 1981).

    Chapter  Google Scholar 

  16. Venolia, L. & Gartler, S.M. Comparison of transformation efficiency of human active and inactive X-chromosomal DNA. Nature 302, 82–83 (1983).

    Article  CAS  Google Scholar 

  17. Venolia, L., Cooper, D.W., O'Brien, D.A., Millette, C.F. & Gartler, S.M. Transformation of the Hprt gene with DNA from spermatogenic cells. Implications for the evolution of X chromosome inactivation. Chromosoma 90, 185–189 (1984).

    Article  CAS  Google Scholar 

  18. Richler, C., Uliel, E., Rosenmann, A. & Wahrman, J. Chromosomally derived sterile mice have a ‘fertile’ active XY chromatin conformation but no XY body. Chromosoma 97, 465–474 (1989).

    Article  CAS  Google Scholar 

  19. Chandley, A.C. & McBeath, S. DNase I hypersensitive sites along the XY bivalent at meiosis in man include the XpYp pairing region. Cytogenet. Cell Genet. 44, 22–31 (1987).

    Article  CAS  Google Scholar 

  20. Weisbrod, S. Active chromatin. Nature 297, 289–295 (1982).

    Article  CAS  Google Scholar 

  21. Kerem, B., Goitein, R., Richler, C., Marcus, M. & Cedar, H. In situ nick-translation distinguishes between active and inactive X chromosomes. Nature 304, 88–90 (1983).

    Article  CAS  Google Scholar 

  22. Driscoll, D.J. & Migeon, B.R. 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 molec. Genet. 16, 267–282 (1990).

    Article  CAS  Google Scholar 

  23. Henderson, S.A. RNA synthesis during male meiosis and spermiogenesis. Chromosoma 15, 345–366 (1964).

    Article  CAS  Google Scholar 

  24. Messthaler, H. & Traut, W. Phases of sex chromosome inactivation in Oncopeltus fasciatus and Pyrrhocoris apterus (Insecta, Heteroptera). Caryologia 28, 501–510 (1975).

    Article  Google Scholar 

  25. Scarbrough, K., Hattman, S. & Nur, U. Relationship of DNA methylation level to the presence of heterochromatin in mealybugs. Molec. cell Biol. 4, 599–603 (1984).

    Article  CAS  Google Scholar 

  26. Hanna-Alava, A. The premeiotic stages of spermatogenesis. Ad. Genet. 13, 157–226 (1965).

    Article  Google Scholar 

  27. Jablonka, E. & Lamb, M.J. Meiotic pairing constraints and the activity of sex chromosomes. J. theor. Biol. 133, 23–36 (1988).

    Article  CAS  Google Scholar 

  28. Hotta, Y., Chandley, A.C., Stern, H., Searle, A.G. & Beechey, C.V. A disruption of pachytene DNA metabolism in male mice with chromosomally-derived sterility. Chromosoma 73, 287–300 (1979).

    Article  CAS  Google Scholar 

  29. Cao, L., Alani, E. & Kleckner, N. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61, 1089–1101 (1990).

    Article  CAS  Google Scholar 

  30. Lyon, M.F. X-Chromosome inactivation as a system of gene dosage compensation to regulate gene expression. Prog. Nucl. Acid Res. molec. Biol. 36, 119–130 (1989).

    Article  CAS  Google Scholar 

  31. Nur, U. Undercondensation and localized euchromatinization of the X chromosome in the grasshopper Melanoplus femur-rubrum. Chromosoma 82, 353–365 (1981).

    Article  CAS  Google Scholar 

  32. Kim, E., Waters, S.H., Hake, L.E. & Hecht, N.B. Identification and developmental expression of a smooth-muscle γ-actin in postmeiotic male germ cells of mice. Molec. cell Biol. 9, 1875–1881 (1989).

    Article  CAS  Google Scholar 

  33. Winship, P.R. An improved method for directly sequencing PCR amplified material using dimethyl sulphoxide. Nucl. Acids Res. 17, 1266 (1989).

    Article  CAS  Google Scholar 

  34. Fletcher, J.M. Light microscope analysis of meiotic prophase chromosomes by silver staining. Chromosoma 72, 241–248 (1979).

    Article  CAS  Google Scholar 

  35. Editorial. Congenital bilateral absence of the vas deferens and cystic fibrosis. Lancet 339, 1328–1329 (1992).

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Richler, C., Soreq, H. & Wahrman, J. X inactivation in mammalian testis is correlated with inactive X–specific transcription. Nat Genet 2, 192–195 (1992). https://doi.org/10.1038/ng1192-192

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