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Inheritance of a meiotic abnormality that causes the ovulation of primary oocytes and the production of digynic triploid mice

Published online by Cambridge University Press:  14 April 2009

John D. West ,
Sheila Webb  and
Matthew H. Kaufman
John D. West*
Affiliation:
Department of Obstetrics and Gynaecology, University of Edinburgh, Centre for Reproductive Biology, 37 Chalmers Street, Edinburgh EH3 9EW, UK
Sheila Webb
Affiliation:
Department of Anatomy, Medical School, University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, UK
Matthew H. Kaufman
Affiliation:
Department of Anatomy, Medical School, University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, UK
*
* Corresponding author.
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Previous studies have demonstrated that the LT/SvKau strain of mice ovulates a high proportion of oocytes as diploid primary oocytes rather than secondary oocytes. These ovulated primary oocytes are arrested at meiotic metaphase I but may be fertilized to produce digynic triploid embryos. In the present study, 40·4% of eggs analysed from LT/SvKau females were ovulated as primary oocytes, compared to 1·2% from control C57BL/Ws strain mothers. These two inbred strains were intercrossed to produce eight sets of Fl, F2 and backcross females and the frequency of triploidy was investigated. The results are compatible with segregation of a co-dominant, autosomal gene that has a major influence on the incidence of triploidy. We suggest that the provisional gene symbol Poo (primary oocyte ovulation) be assigned to this gene, with alleles Pool (the ‘mutant’ allele present in the LT/SvKau strain) and Poob (the normal allele present in C57BL/Ws mice). Poo is incompletely penetrant and has variable expressivity because the proportion of oocytes ovulated as primary oocytes by LT/SvKau mice was variable and, in some cases, nil. In putative Pool/Poob heterozygotes the frequency of ovulated primary oocytes was increased only marginally (from 1·2% to 66%) by the presence of one copy of the Pool allele, but this increase was found consistently (in two reciprocal Fl crosses) and was statistically significant. No evidence was found for tight genetic linkage between Poo and two Mendelian loci (brown on chromosome 4 and glucose phosphate isomerase on chromosome 7), that were segregating in the crosses. The Pool mutant in the LT/SvKau strain of mice provides a valuable resource to study the cell and molecular biology of mammalian oocyte maturation and the control of meiosis.

Type
Research Article
Information
Genetics Research , Volume 62 , Issue 3 , December 1993 , pp. 183 - 193
Copyright
Copyright © Cambridge University Press 1993

References

Bartels, I., Jenderny, J. & Hansmann, I. (1984). Control of meiosis by somatic cells in mice: Inheritance of the meiosis I error ‘diploidy’ and nondisjunction in sensitive NMRI/Han oocytes ovulated from chimaeras. Cell Differentiation 15, 189–194.CrossRefGoogle Scholar
Beermann, F., Jenderny, J., Hummler, E. & Hansmann, I. (1987). Inheritance of a meiosis I error expressed in mouse oocytes and modulated by a maternal factor. Genetical Research 49, 239–243.CrossRefGoogle ScholarPubMed
Dandoy, F., De Maeyer-Guignard, J. & De Maeyer, E. (1989). Linkage analysis of the murine mos proto-oncogene on chromosome 4. Genomics 4, 546–551.CrossRefGoogle ScholarPubMed
Eppig, J. J. (1978). Granulosa cell deficient follicles. Occurrence, structure and relationship to ovarian teratocar-cinogenesis in strain LT/Sv mice. Differentiation 12, 111–120.CrossRefGoogle ScholarPubMed
Eppig, J. J. & Downs, S. M. (1984). Chemical signals that regulate mammalian oocyte maturation. Biology of Reproduction 30, 1–11.CrossRefGoogle ScholarPubMed
Eppig, J. J., Kozak, L. P., Eicher, E. M. & Stevens, L. C. (1977). Ovarian teratomas in mice are derived from oocytes that have completed the first meiotic division. Nature 269, 517–518.CrossRefGoogle ScholarPubMed
Hansmann, I. & El-Nahass, E. (1979). Incidence of nondisjunction in mouse oocytes. Cytogenetics and Cell Genetics 24, 115–121.CrossRefGoogle ScholarPubMed
Hansmann, I., Bartels, I., Beermann, F., Caspari, D., Hummler, E. & Theuring, F. (1985). Mechanisms of nondisjunction: facts and perspectives. In Aneuploidy: Aetiology and Mechanisms (ed. Dellarco, V. L., Votek, P. E., Hollaender, A., Brinkley, B. R., Hook, E. B. and Moses, M. J.), pp. 417–432. New York: Plenum.CrossRefGoogle Scholar
Jenderny, J., Düls, C., Probeck, H. D., Richter, P., Schulz, H. & Hansmann, I. (1980). Genetically determined diploidy in mouse oocytes. European Journal of Cell Biology 22, 23.Google Scholar
Justice, M. J., Siracusa, L. D., Gilbert, D. J., Heisterkamp, N., Groffen, J., Chada, K., Silan, C. M., Copeland, N. G. & Jenkins, N. A. (1990). A genetic linkage map of mouse chromosome 10: localization of eighteen molecular markers using a single interspecific backcross. Genetics 125, 855–866.CrossRefGoogle ScholarPubMed
Kanki, J. P. & Donoghue, D. J. (1991). Progression from meiosis I to meiosis II in Xenopus oocytes requires de novo translation of the mosxe protooncogene. Proceedings of the National Academy of Sciences, USA 88, 5794–5798.CrossRefGoogle Scholar
Kaufman, M. H. & Howlett, S. K. (1986). The ovulation and activation of primary and secondary oocytes in LT/Sv strain mice. Gamete Research 14, 255–264.CrossRefGoogle Scholar
Linder, D., McCaw, B. K. & Hecht, F. (1975). Partheno-genetic origin of benign ovarian teratomas. New England Journal of Medicine 292, 63–66.CrossRefGoogle Scholar
Linder, D. & Power, J. (1970). Further evidence for post-meiotic origin of teratomas in the human female. Annals of Human Genetics 34, 21–30.CrossRefGoogle ScholarPubMed
Murray, A. W. & Kirschner, M. W. (1989). Cyclin synthesis drives the early embryonic cell cycle. Nature 339, 275–280.CrossRefGoogle ScholarPubMed
Murray, A. W., Solomon, M. J. & Kirschner, M. W. (1989). The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339, 280–286.CrossRefGoogle ScholarPubMed
O'Keefe, S. J., Wolfes, H., Kiessling, A. A. & Cooper, G. M. (1989). Microinjection of antisense c-mos oligonucleotides prevents meiosis II in the maturing mouse egg. Proceedings of the National Academy of Sciences, USA 86, 7038–7042.CrossRefGoogle Scholar
O'Neill, G. T. & Kaufman, M. H. (1987). Ovulation and fertilization of primary and secondary oocytes in LT/Sv strain mice. Gamete Research 18, 27–36.CrossRefGoogle ScholarPubMed
Peters, J. & Cocking, Y. (1993). Mouse gene list. Mouse Genome 91, 156–249.Google Scholar
Sagata, N., Watanabe, N., Vande Woude, G. F. & Ikawa, Y. (1989). The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs. Nature 342, 512–518.CrossRefGoogle ScholarPubMed
Sakaguchi, A. Y., Martinez, L., Lalley, P. A., Sylvia, V. L., Hans, E. S., Killary, A. M. & Ghosh Choudhury, G. (1991). Chromosome mapping in mouse of genes that regulate the eukaryotic cell cycle. Cytogenetics and Cell Genetics 58 (Human Gene Mapping 11th London Conference, p. 2138, abstract 27428).Google Scholar
Speirs, S. & Kaufman, M. H. (1988). Effect of exogenous hormones on the ovulation of primary and secondary oocytes in LT/Sv strain mice. Gamete Research 21, 179–184.CrossRefGoogle ScholarPubMed
Speirs, S. & Kaufman, M. H. (1990). Effect of maternal age on the incidence of digynic triploidy in LT/Sv strain mice: implications for the ovulation of primary and secondary oocytes in this strain. Journal of Experimental Zoology 253, 83–87.CrossRefGoogle ScholarPubMed
Takagi, N. (1970). High incidence of triploid embryos associated with artificial polyovulation in mice. Chromosome Information Service no. 11, p. 32.Google Scholar
Takagi, N. & Oshimura, M. (1973). Developmental fate of triploid mouse embryos induced by superovulation. Chromosome Information Service no. 14, p. 36.Google Scholar
Takagi, N. & Sasaki, M. (1976). Digynic triploidy after superovulation in mice. Nature 264, 278–281.CrossRefGoogle ScholarPubMed
Tarkowski, A. K. (1966). An air-drying method for chromosome preparations from mouse eggs. Cytogenetics 5, 394–400.CrossRefGoogle Scholar
Watanabe, N., Vande Woude, G. F., Ikawa, Y. & Sagata, N. (1989). Specific proteolysis of the c-mos protooncogene product by calpain on fertilization of Xenopus eggs. Nature 342, 505–511.CrossRefGoogle ScholarPubMed
West, J. D. & Fisher, G. (1984). A new allele of the Gpi-It temporal gene that regulates the expression of glucose phosphate isomerase in mouse oocytes. Genetical Research 44, 169–181.CrossRefGoogle Scholar
Whittingham, D. G. (1971). Culture of mouse ova. Journal of Reproduction and Fertility (Supplement 14), 7–21.Google Scholar
Yew, N., Mellini, M. L. & Vande Woude, G. V. (1992). Meiotic initiation by the mos protein in Xenopus. Nature 355, 649–652.CrossRefGoogle ScholarPubMed
Yew, N., Strobel, M. & Vande Woude, G. V. (1993). Mos and the cell cycle: the molecular bases of the transformed phenotype. Current Opinions in Genetics and Development 3, 19–25.CrossRefGoogle Scholar