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A study of meiotic pairing, nondisjunction and germ cell death in laboratory mice carrying Robertsonian translocations

Published online by Cambridge University Press:  14 April 2009

C. A. Everett
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford 0X1 3PS Department of Obstetrics and Gynaecology, Centre for Reproductive Biology, University of Edinburgh, 37 Chalmers Street, Edinburgh EH3 9EW. Tel. 0131 229 2575. Fax. 0131 229 2408. E-mail Clare.Everett@ed.ac.uk
J. B. Searle
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford 0X1 3PS Department of Biology, University of York, PO Box 373, York YO1 5YW, UK. Tel. 01904 4329 7. Fax. 01904 432860. E-mail JBS3@unix.york.ac.uk
B. M. N. Wallace
Affiliation:
School of Biological Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT. Tel. 0121 414 5917. Fax. 0121 414 5925 E-mail B.M.N.Wallace@bham.ac.uk
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Frequencies of anaphase I nondisjunction, germ cell death and pairing abnormalities at pachytene were assessed in male mice singly heterozygous and homozygous for the Robertsonian (Rb) translocations: Rb (1.3)lBnr, Rb(ll. 13)4Bnr and Rb(10. ll)8Bnr. Rb homozygotes showed low frequencies of nondisjunction but substantial germ cell death. This germ cell death could not be attributed to problems at pachytene as Rb homozygotes showed no increase in pairing abnormalities over the (C3H/HeH×1O1/H)F1 controls. Instead genie factors are involved. Rb heterozygotes showed substantial frequencies of nondisjunction and even greater germ cell death than found in the homozygotes. Pachytene pairing abnormalities were observed and it appears that these, together with genie factors, cause physiological perturbation of meiocytes, thereby promoting germ cell death, with nondisjunction of the trivalent as a sublethal response.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

References

Abercrombie, M., (1946). Estimation of nuclear population from microtome sections. Anatomical Record 94, 239247.Google Scholar
Baker, B. S., Carpenter, A. T. C., Esposito, M. S., Esposito, R. E., & Sandier, L., (1976). The genetic control of meiosis. Annual Reviews of Genetics 10, 53134.CrossRefGoogle ScholarPubMed
Bauchau, V., (1990). Phylogenetic analysis of the distribution of chromosomal races of Mus musculus domesticus Rutty in Europe. Biological Journal of the Linnean Society 41, 171192.CrossRefGoogle Scholar
Beatty, R. A., Lim, M.-C., & Coulter, V. J., (1975). A quantitative study of the second meiotic metaphase in male mice (Mus musculus). Cytogenetics and Cell Genetics 15, 256275.Google Scholar
de Boer, P., (1986). Chromosomal causes of fertility reduction in mammals. In Chemical Mutagens (ed. de Serres, F. J.), 10, pp. 427467. New York: Plenum.Google Scholar
Burgoyne, P. S., & Baker, T. G., (1984). Meiotic pairing and gametogenic failure. In Controlling Events in Meiosis. 38th Symposium of the Society for Experimental Biology (ed. Evans, C. W., and Dickinson, M. G.), pp. 349362. Cambridge: Company of Biologists.Google Scholar
Capanna, E., Gropp, A., Winking, H., Noack, G., & Cristaldi, M., (1976). Robertsonian metacentrics in the mouse. Chromosoma 58, 341353.Google Scholar
Cattanach, B. M., & Beechey, C. V., (1990). Chromosome imprinting phenomena in mice and indications in man. Chromosomes Today 10, 135148.Google Scholar
Cattanach, B. M., & Moseley, H., (1973). Nondisjunction and reduced fertility caused by tobacco mouse metacentric chromosomes. Cytogenetics and Cell Genetics 12,264–287.Google Scholar
Committee on Standardised Nomenclature for Mice (1972). Standard karyotype of the mouse, Mus musculus. Journal of Heredity 63, 6972.Google Scholar
Eichenlaub-Ritter, U., (1994). Mechanisms of nondisjunction in mammalian meiosis. Current Topics in Developmental Biology 29, 281323.Google Scholar
Evans, E. P., (1976). Male sterility and double heterozygosity for Robertsonian translocation in the mouse. Chromosomes Today 5, 7581.Google Scholar
Evans, E. P., Breckon, G., & Ford, C. E., (1964). An air drying method for meiotic preparations from mammalian testes. Cytogenetics 3, 289294.CrossRefGoogle ScholarPubMed
Everett, C. A., & Searle, J. B., (1995). Pattern and frequency of nocodazole induced meiotic nondisjunction in oocytes of mice carrying the ‘tobacco mouse’ metacentric Rb(16·17)7Bnr. Genetical Research 66, 3543.Google Scholar
Ford, C. E., & Evans, E. P., (1973). Robertsonian translocations in mice: segregational irregularities in male heterozygotes and zygotic unbalance. Chromosomes Today 8, 117127.Google Scholar
Forejt, J., (1982). X-Y involvement in male sterility caused by autosome translocations — a hypothesis. In Genetic Control of Gamete Production and Function (ed. Crosignani, P. G., Rubin, B. L., and Fraccaro, M.), pp. 135151. Academic Press.Google Scholar
Garagna, S., Redi, C. A., Zuccotti, M., Britton-Davidian, J., & Winking, H., (1990). Kinetics of oogenesis in mice heterozygous for Robertsonian translocations. Differentiation 42, 167171.CrossRefGoogle Scholar
Gropp, A., Giers, D., & Kolbus, U., (1974). Trisomy in the fetal backcross progeny of male and female metacentric heterozygotes in the mouse. Cytogenetics and Cell Genetics 13, 511535.Google Scholar
Gropp, A., & Winking, H., (1981). Robertsonian translocations: cytology, meiosis, segregational patterns and biological consequences of heterozygosity. Symposia of the Zoological Society of London 47, 141181.Google Scholar
Gropp, A., Winking, H., & Redi, C. A., (1982). Consequences of Robertsonian heterozygosity segregational impairment of fertility versus male limited sterility. In Genetic Control of Gamete Production and Function (ed. Crosignani, P. G., Rubin, B. L., & Fraccaro, M.), pp. 155–134. Academic Press.Google Scholar
Hultén, M. A., Saadallah, N., Wallace, B. M. N., & Creasy, M. R., (1985). Meiotic studies in man. In Human Cytogenetics: A Practical Approach (ed. Rooney, D. E., and Czepulkowski, B. H.), pp. 163196. Oxford: IRL Press.Google Scholar
King, M., (1993). Species Evolution: the Role of Chromosome Change. Cambridge: Cambridge University Press.Google Scholar
Kodama, Y., Yoshida, M. C., & Sasaki, M., (1980). An improved silver-staining technique for nucleolus organizer regions by using nylon cloth. Japanese Journal of Human Genetics 25, 229233.Google ScholarPubMed
LeBlond, C. P., & Clermont, Y., (1952). Spermiogenesis of rat, mouse, hamster and guinea-pig as revealed by the ‘periodic acid-fuchsin sulphurous acid’ technique. American Journal of Anatomy 90, 167215.Google Scholar
Mahadevaiah, S. K., Setterfield, L. A., & Mittwoch, U., (1990). Pachytene pairing and sperm counts in mice with single Robertsonian translocations and monobrachial compounds. Cytogenetics and Cell Genetics 53, 2631.CrossRefGoogle ScholarPubMed
Miklos, G. L. G., (1974). Sex chromosome pairing and male fertility. Cytogenetics and Cell Genetics 13, 558577.Google Scholar
Moses, M. J., (1977). Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). I. Morphology of the autosomal complement in spread preparations. Chromosoma 60, 99125.Google Scholar
Oakberg, E. F., (1956). A description of spermatogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. American Journal of Anatomy 99, 391413.CrossRefGoogle ScholarPubMed
Ratomponirina, C., Andrianivo, J., & Rumpler, Y., (1982). Spermatogenesis in several intra- and interspecific hybrids of the lemur (Lemur). Journal of Reproduction and Fertility 66, 717721.Google Scholar
Redi, C. A., & Capanna, E., (1988). Robertsonian heterozygotes in the house mouse and the fate of their germ cells. In The Cytogenetics of Mammalian Autosomal Rearrangements (ed. Daniel, A.), pp. 315359. New York: Liss.Google Scholar
Redi, C. A., Garagna, S., Hilscher, B., & Winking, H., (1985). The effects of some Robertsonian chromosome combinations on the seminiferous epithelium of the mouse. Journal of Embryology and Experimental Morphology 85, 119.Google ScholarPubMed
Said, K., Saad, A., Auffray, J.-C., & Britton-Davidian, J., (1993). Fertility estimates in the Tunisian acrocentric and Robertsonian populations of the house mouse and their chromosomal hybrids. Heredity 71, 532538.Google Scholar
Searle, A. G., (1989). Chromosomal variants. Numerical variants and structural rearrangements. In Genetic Variants and Strains of the Laboratory Mouse, 2nd edition (ed. Lyon, M. F., and Searle, A. G.), pp. 582616. Oxford: Oxford University Press.Google Scholar
Searle, J. B., (1993). Chromosomal hybrid zones in eutherian mammals. In Hybrid Zones and the Evolutionary Process (ed. Harrison, R.G.), pp. 309352. New York: Oxford University Press.CrossRefGoogle Scholar
Shire, J. G. M., & Bartke, A., (1972). Strain differences in testicular weight and spermatogenesis with special reference to C57BL/10J and DBA/2J mice. Journal of Endocrinology 55, 163171.Google Scholar
Tettenborn, U., & Gropp, A., (1970). Meiotic nondisjunction in mice and mouse hybrids. Cytogenetics 9, 272283.CrossRefGoogle ScholarPubMed
Wallace, B. M. N., Searle, J. B., & Everett, C. A., (1992). Male meiosis and gametogenesis in wild house mice (Mus musculus domesticus) from a chromosomal hybrid zone: a comparison between ‘simple’ Robertsonian heterozygotes and homozygotes. Cytogenetics and Cell Genetics 61, 211220.Google Scholar
Winking, H., (1986). Some aspects of Robertsonian karyotype variation in European wild mice. Current Topics in Microbiology and Immunology 127, 6874. Berlin, Heidelberg: Springer Verlag.Google Scholar
Winking, H., & Gropp, A., (1976). Meiotic nondisjunction of metacentric heterozygotes in oocytes versus spermatocytes. In Ovulation in the Human (ed. Crosignani, P. G., and Mitchell, D. R.), pp. 4756. Academic Press.Google Scholar