Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

An X-chromosome linked locus contributes to abnormal placental development in mouse interspecific hybrids

Nature Genetics volume 12, pages 398–403 (1996)Cite this article

Abstract

Interspecific hybridization between closely related species is commonly associated with decreased fertility or viability of F1 hybrids. Thus, in mouse interspecific hybrids, several different hybrid sterility genes that impair gametogenesis of the male hybrids have been described. We describe a novel effect in hybrids between different mouse species that manifests itself in abnormal growth of the placenta. Opposite phenotypes, that is, placental hypotrophy versus hypertrophy, are observed in reciprocal crosses and backcrosses. The severity of the phenotype, which is mainly caused by abnormal development of the spongiotrophoblast, is influenced by the sex of the conceptus. In general, placental hypertrophy is associated with increased fetal growth. Hypotrophy of the placenta frequently leads to growth impairment or death of the fetus. One of the major genetic determinants of placental growth maps to the proximal part of the mouse X chromosome.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Coyne, J.A. Genetics and speciation. Nature 355, 511–515 (1992).

    Article  CAS  Google Scholar 

  2. Wu, C. & Palopoli, M.F. Genetics of postmating reproductive isolation in animals. Annu. Rev. Genet. 27, 283–308 (1994).

    Article  Google Scholar 

  3. Haldane, J.B.S. Sex-ratio and unisexual sterility in hybrid animals. J. Genet. 12, 101–109 (1922).

    Article  Google Scholar 

  4. Britton, J., Pasteur, N. & Thaler, L. Les souris du Midi de la France: caractérisation génétique de deux groupes de populations sympatriques. C. R. Acad. Sci. Paris 283, 515–518 (1976).

    CAS  Google Scholar 

  5. Bonhomme, F. Evolutionary relationships in the genus Mus . in The Wild Mouse in Immunology (eds. Potter, M., Nadeau, J.H. & Cancro, M.P.) 19–34 (Springer-Verlag, Berlin, 1986).

    Chapter  Google Scholar 

  6. Festetics, A. Ährenmaushügel in Österreich. Z. Säugetierkunde 26, 112–125 (1961).

    Google Scholar 

  7. Bonhomme, F., Catalan, J., Gerasimov, S., Orsini, P. & Thaler, L. Le complexe d'espèces du genre Mus en Europe Centrale et Orientale. I. Génétique. Z. Säugetierkunde. 48, 78–85 (1983).

    Google Scholar 

  8. Bonhomme, F., Martin, S. & Thaler, L. Hybridization between Mus musculus L and Mus spretus Lataste under laboratory conditions. Experientia 34, 1140–1141 (1978).

    Article  CAS  Google Scholar 

  9. Guénet, J.-L., Nagamine, C., Simon-Chazottes, D., Montagutelli, X. & Bonhomme, F. Hst-3: an X-linked hybrid sterility gene. Genet. Res. Camb. 56, 163–165 (1990).

    Article  Google Scholar 

  10. Biddle, F.G. Segregation distortion of X-linked marker genes in interspecific crosses between Mus musculus and Mus spretus . Genome 29, 389–392 (1987).

    Article  CAS  Google Scholar 

  11. Eicher, E.M., Lee, B.K., Washburn, L.L., Hale, D.W. & King, T.R. Telomere-related markers for the pseudoautosomal region of the mouse genome. Proc. Natl. Acad. Sci. USA 89, 2160–2164 (1992).

    Article  CAS  Google Scholar 

  12. Rowe, L.B. et al. Maps from two interspecific backcross DNA panels available as a community genetic mapping resource. Mam. Genome. 5, 253–274 (1994).

    Article  CAS  Google Scholar 

  13. Lescisin, K.R., Varmuza, S. & Rossant, J. Isolation and characterization of a novel trophoblast-specific cDNA in the mouse. Genes Dev. 2, 1639–1646 (1989).

    Article  Google Scholar 

  14. Rudert, F., Saunders, A.M., Rebstock, S., Thompson, J.A. & Zimmermann, W. Characterization of murine carcinoembryonic antigen gene family members. Mam. Genome. 3, 262–273 (1992).

    Article  CAS  Google Scholar 

  15. Takagi, N. & Sasaki, M. Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256, 640–642 (1975).

    Article  CAS  Google Scholar 

  16. West, J.D., Frels, W.I., Chapman, V.M. & Papaioannou, V.E. Preferential expression of the maternally derived X chromosome in the mouse yolk sac. Cell 12, 873–882 (1977).

    Article  CAS  Google Scholar 

  17. Sobis, H., Verstuyf, A. & Vandeputte, M. Histochemical differences inexpression of X-linked glucose-6-phosphate dehydrogenase between ectoderm- and endoderm-derived embryonic and extra-embryonic tissues. J. Histochem. Cytochem. 39, 569–574 (1991).

    Article  CAS  Google Scholar 

  18. McLaren, A. Genetic and environmental effects on foetal and placental growth in mice. J. Reprod. Fert. 9, 79–98 (1965).

    Article  CAS  Google Scholar 

  19. Lyon, M.F. Gene action in the X-chromosome of the mouse (Mus musculus). Nature 190, 372–373 (1961).

    Article  CAS  Google Scholar 

  20. Nielsen, J.T. & Chapman, V.M. Electrophoretic variation for X-chromosome-linked phosphoglycerate kinase (PGK-1) in the mouse. Biochem. Genet. 21, 487–496 (1977).

    Google Scholar 

  21. Tan, S.S., Williams, E.A. & Tam, P.P.L. X-chromosome inactivation occurs at different times in different tissues of the post-implantation mouse embryo. Nature Genet. 3, 170–174 (1993).

    Article  CAS  Google Scholar 

  22. Rogers, J.F. & Dawson, W.D. Foetal and placental size in a Peromyscus species cross. J. Reprod. Fert. 21, 255–262 (1970).

    Article  CAS  Google Scholar 

  23. Catzeflis, F.M., Dickerman, A.W., Michaux, J. & Kirsch, J.A.W. DNA hybridization and rodent phylogeny. in Mammal Phytogeny: Vol.2: Placentals. (eds. Szalay, F.S., Novacek, M.J. & McKenna, M.C.) 159–172 (Springer-Verlag, Berlin, New York, 1993).

    Chapter  Google Scholar 

  24. Allen, W.R., Skidmore, J.A., Stewart, F. & Antczak, D.F. Effects of fetal genotype and uterine environment on placental development in equids. J. Reprod. Fert. 97, 55–60 (1993).

    Article  Google Scholar 

  25. Haig, D. Genetic conflicts in human pregnancy Quart. Rev. Biol. 68, 495–532 (1993).

    Article  CAS  Google Scholar 

  26. Moore, T., Hurst, L.D. & Reik, W. Genetic conflict and evolution of mammalian X-chromosome inactivation. Dev. Genet. 17, 206–211 (1995).

    Article  CAS  Google Scholar 

  27. Schmid, P., Schulz, W.A. & Hameister, H. Dynamic expression pattern of the myc protooncogene in midgestation mouse embryos. Science 243, 226–229 (1989).

    Article  CAS  Google Scholar 

  28. Lyon, M.F. & Kirby, M.C. Mouse chromosome atlas. Mouse Genome 93, 23–66 (1995).

    Google Scholar 

  29. Dietrich, W.F. et al. A genetic map of the mouse with 4,006 simple sequence length polymorphisms. Nature Genet. 7, 220–245 (1994).

    Article  CAS  Google Scholar 

  30. Copeland, N.G. et al. A genetic linkage map of the mouse: current applications and future prospects. Science 262, 57–66 (1993).

    Article  CAS  Google Scholar 

  31. Supplemented by additional markers. in Whitehead Institute/MIT Center for Genome Research, Genetic Map of the Mouse, Database Release 9, February 7 (1995).

  32. Saiki, R.K. et al. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239, 487–491 (1988).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Abteilung Medizinische Genetik der Universität Ulm, Albert-Einstein-Attee 11, D-89069, Ulm, Germany

    Ulrich Zechner & Horst Hameister

  2. Institut für Biologie III der Universität Freiburg, Schänzlestraße 1, D-79104, Freiburg, Germany

    Matthias Reule & Reinald Fundele

  3. Laboratoire Génome et Populations, Université de Montpellier II, F-34095, Montpettier, France

    Annie Orth & François Bonhomme

  4. Unité de Génétique des Mammifères, Institut Pasteur, 25 rue du Docteur Roux, 75724, Paris, Cedex 15, France

    Bärbel Strack & Jean-Louis Guénet

Authors
  1. Ulrich Zechner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthias Reule
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Annie Orth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. François Bonhomme
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bärbel Strack
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jean-Louis Guénet
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Horst Hameister
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Reinald Fundele
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zechner, U., Reule, M., Orth, A. et al. An X-chromosome linked locus contributes to abnormal placental development in mouse interspecific hybrids. Nat Genet 12, 398–403 (1996). https://doi.org/10.1038/ng0496-398

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng0496-398

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing