Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-23T00:03:35.773Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression of three t-complex genes, Tcp-1, D17Leh117c3, and D17Leh66, in purified murine spermatogenic cell populations

Published online by Cambridge University Press:  14 April 2009

K. R. Willison ,
G. Hynes ,
P. Davies ,
A. Goldsborough  and
V. A. Lewis
K. R. Willison
Affiliation:
Institute of Cancer Research, Chester Beany Laboratories, Fulham Road, London SW3 6JB, U.K.
G. Hynes
Affiliation:
Institute of Cancer Research, Chester Beany Laboratories, Fulham Road, London SW3 6JB, U.K.
P. Davies
Affiliation:
Institute of Cancer Research, Chester Beany Laboratories, Fulham Road, London SW3 6JB, U.K.
A. Goldsborough
Affiliation:
Institute of Cancer Research, Chester Beany Laboratories, Fulham Road, London SW3 6JB, U.K.
V. A. Lewis
Affiliation:
Institute of Cancer Research, Chester Beany Laboratories, Fulham Road, London SW3 6JB, U.K.
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Transmission ratio distortion (TRD) is a property of the complete t-haplotype which results in the preferential transmission of the t-haplotype chromosome from heterozygous t/+ males to the majority of the progeny. Available data suggest that in t/+ males, a dysfunction of the wild-type sperm within the female reproductive tract is responsible for the observed deviation from Mendelian segregation ratios. Genetically, Lyon has shown that multiple loci within the t-complex are required for maximum levels of TRD. These loci include multiple t-complex distorters (Teds) which act upon a single t-complex responder (Ter). Testis-expressed genes have been cloned which map to the same subregions of the t-complex as the Teds and Ter and are thus considered candidate genes for the products of these loci. To begin to understand how the products of these loci biochemically control TRD, the expression of three TRD-candidate genes (Tcp-1, D17Leh117c3, and D17Leh66) has been determined in populations of spermatocytes and differentiated spermatids purified to near homogeneity by unit gravity sedimentation. Fractions covering the entire gradient were analysed resulting in a more accurate picture of the precise timing of expression than previously reported. Transcription of all three genes was up-regulated in pachytene primary spermatocytes and persisted at stable levels through the haploid spermatid stages. Significantly, only levels of mRNA encoded by D17Leh66, the candidate gene for Tcr, increased from early round to elongating-stage spermatids. If this pattern of expression does, in fact, represent Tcr, these data provide the first direct evidence that wild-type and t-haplotype Tcr elements could be differentially expressed in haploid spermatids.

Type
Research Article
Information
Genetics Research , Volume 56 , Issue 2-3 , October 1990 , pp. 193 - 201
Copyright
Copyright © Cambridge University Press 1990

References

Braden, A. W. H. (1958). Influence of mating time on the segregation ratio of alleles at the T Locus in the house mouse. Nature 181, 786–787.CrossRefGoogle Scholar
Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156–159.CrossRefGoogle ScholarPubMed
Clermont, Y. (1972). Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiological Reviews 52, 198–236.CrossRefGoogle ScholarPubMed
Dudley, K., Potter, J., Lyon, M. F. & Willison, K. R. (1984). Analysis of male sterile mutations in the mouse using haploid stage expressed cDNA probes. Nucleic Acids Research 12, 4281–4293.CrossRefGoogle ScholarPubMed
Fawcett, D. W. (1975). The mammalian spermatozoon. Developmental Biology 44, 394–436.CrossRefGoogle ScholarPubMed
Feinberg, A. P. & Vogelstein, B. (1984). A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Analytical Biochemistry 137, 266–267.Google ScholarPubMed
Gizang-Ginsberg, E. & Wolgemuth, D. J. (1985). Localization of mRNAs in mouse testes by in situ hybridization: Distribution of alpha tubulin and developmental stage specificity of pro-opimelanocortin transcripts. Developmental Biology 111, 293–305.CrossRefGoogle Scholar
Gummere, G. R., McCormick, P. J. & Bennett, D. (1986). The influence of genetic background and the homologous chromosome 17 on t haplotype transmission ratio distortion in mice. Genetics 114, 235–245.CrossRefGoogle Scholar
Haffner, R. & Willison, K. (1987). In situ hybridization to messenger RNA in tissue sections. In Mammalian Development - A Practical Approach. Editor: Monk, M. Publisher: IRL Press, Oxford, pp. 199–215.Google Scholar
Hammer, M. F., Schimenti, J. & Silver, L. M. (1989). Evolution of mouse chromosome 17 and the origin of inversions associated with t-haplotypes. Proceedings of the National Academy of Sciences USA 86, 3261–3265.CrossRefGoogle ScholarPubMed
Hecht, N. B. (1986). Regulation of gene expression during mammalian spermatogenesis. In Experimental Approaches to Mammalian Embryonic Development. Ed: Rossant, J. and Pederson, R. A. Publisher: Cambridge University Press, Cambridge, pp. 151–193.Google Scholar
Kleene, K. C., Distel, R. J. & Hecht, N. B. (1983). cDNA clones encoding cytoplasmic poly(A)+RNAs which first appear at detectable levels in haploid phases of spermatogenesis in the mouse. Developmental Biology 98, 455–464.CrossRefGoogle ScholarPubMed
Kleene, K. C., Distel, R. J. & Hecht, N. B. (1985). The nucleotide sequence of a cDNA clone encoding mouse protamine I. Biochemistry 24, 719–722.CrossRefGoogle Scholar
Lyon, M. (1984). Transmission ratio distortion in mouse t-haplotypes is due to multiple distorter genes acting on a responder locus. Cell 37, 621–628.CrossRefGoogle ScholarPubMed
Lyon, M. (1986). Male sterility of the mouse t-complex is due to homozygosity of the distorter genes. Cell 44, 357–363.CrossRefGoogle ScholarPubMed
Lyon, M. (1990). Search for differences among t-haplotypes in distorter and responder genes. Genetical Research 55, 13–19.CrossRefGoogle ScholarPubMed
McGrath, J. & Hillman, N. (1980). The in vitro transmission frequency of the t12 mutation in the mouse. Journal of Embryology and Experimental Morphology 60, 141–151.Google ScholarPubMed
Meijer, D., Hermans, A., von Lindern, M., van Agthoven, T., de Klein, A., Mackenbach, P., Grootegoed, A., Talarico, D., Della, Valle G. & Grosveld, G. (1987). Molecular characterization of the testis-specific c-abl mRNA in mouse. EMBO Journal 6, 4041–4048.CrossRefGoogle Scholar
Olds-Clarke, P. (1983). The nonprogressive motility of sperm populations from mice with tw32 haplotype. Journal of Andrology 4, 136–143.CrossRefGoogle ScholarPubMed
Olds-Clarke, P. & McCabe, S. (1981). Genetic background affects expression of t-haplotype in mouse sperm. Genetical Research 40, 249–254.CrossRefGoogle Scholar
Olds-Clarke, P. & Peitz, B. (1985). Fertility of sperm from t / + mice: evidence that + bearing sperm are dysfunctional. Genetical Research 47, 49–52.CrossRefGoogle Scholar
Perey, B., Clermont, Y. & LeBlond, C. P. (1961). The wave of the seminiferous epithelium in the rat. The American Journal of Anatomy 108, 47–77.CrossRefGoogle Scholar
Peschon, J. J., Behringer, R. R., Brinster, R. L. & Palmiter, R. D. (1987). Spermatid-specific expression of protamine 1 in transgenic mice. Proceedings of the National Academy of Sciences USA 84, 5316–5319.CrossRefGoogle ScholarPubMed
Rappold, G. A., Stubbs, L., Labeit, S., Crkvenjakov, R. B. & Lehrach, H. (1987). Identification of a testis-specific gene from the mouse t–complex next to a CpG-rich island. EMBO Journal 6, 1975–1980.CrossRefGoogle ScholarPubMed
Romrell, L. J., Bellve, A. R. & Fawcett, D. W. (1976). Separation of mouse spermatogenic cells by sedimentation velocity. Developmental Biology 49, 119–131.CrossRefGoogle ScholarPubMed
Sanchez, E. R. & Erickson, R. P. (1985). Expression of the Tcp-1 locus of the mouse during early embryogenesis. Journal of Embryology and Experimental Morphology 89, 113–122.Google ScholarPubMed
Schimenti, J., Cebra-Thomas, J. A., Decker, C. L., Islam, S. D., Pilder, S. H. & Silver, L. M. (1988). A candidate gene family for the mouse t complex responder (ter) locus responsible for haploid effects on sperm function. Cell 55, 71–78.CrossRefGoogle Scholar
Shackelford, G. M. & Varmus, H. E. (1987). Expression of the proto-oncogene int-1 is restricted to postmeiotic male germ cells and the neural tube of mid-gestational embryos. Cell 50, 89–95.CrossRefGoogle Scholar
Silver, L. M. (1989). Gene dosage effects on transmission ratio distortion and fertility in mice that carry t–haplotypes. Genetical Research 54, 221–225.CrossRefGoogle ScholarPubMed
Silver, L. M., Artzt, K. & Bennett, D. (1979). A major testicular cell protein specified by a mouse T/t complex gene. Cell 17, 275–284.CrossRefGoogle Scholar
Silver, L. (1985). Mouse t haplotypes. Annual Reviews of Genetics 19, 179–208.CrossRefGoogle ScholarPubMed
Silver, L. M., Kleene, K. C., Distel, R. J. & Hecht, N. B. (1987). Synthesis of mouse t–complex proteins during haploid stages of spermatogenesis. Developmental Biology 119, 605–608.CrossRefGoogle ScholarPubMed
Silver, L. M. & Olds-Clarke, P. (1984). Transmission ratio distortion of mouse t haplotypes is not a consequence of wild-type sperm degeneration. Developmental Biology 105, 250–252.CrossRefGoogle Scholar
Silver, L. M. & Remis, D. (1987). Five of the nine genetically defined regions of mouse t–haplotypes are involved in transmission ratio distortion. Genetical Research 49, 51–56.CrossRefGoogle ScholarPubMed
Simanis, V. & Lane, D. P. (1985). An immunoaffinity purification procedure for SV40 large T antigen. Virology 144, 88–100.CrossRefGoogle ScholarPubMed
Stern, L., Kleene, K. C., Gold, B. & Hecht, N. B. (1983). Gene expression during mammalian spermatogenesis III. Changes in populations of mRNA during spermiogenesis. Experimental Cell Research 143, 247–255.CrossRefGoogle ScholarPubMed
Thomas, P. S. (1980). Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proceeding of the National Academy of Sciences USA 77, 5201–5205.CrossRefGoogle ScholarPubMed
Willison, K. & Ashworth, A. (1987). Mammalian spermatogenic gene expression. Trends in Genetics 3, 351–355.CrossRefGoogle Scholar
Willison, K. R., Dudley, K. & Potter, J. (1986). Molecular cloning and sequence analysis of a haploid expressed gene encoding t-complex polypeptide 1. Cell 44, 727–738.CrossRefGoogle ScholarPubMed
Willison, K., Lewis, V., Zuckerman, K. S., Cordell, J., Dean, C., Miller, K., Lyon, M. F. & Marsh, M. (1989). The t-complex polypeptide-1 (TCP-1) is associated with the cytoplasmic aspect of Golgi membranes. Cell 57, 621–632.CrossRefGoogle ScholarPubMed
Wolgemuth, D. J., Ginzang-Ginsberg, E., Engelmyer, E., Gavin, B. J. & Ponzetto, C. (1985). Separation of mouse testis cells on a Celsep apparatus and their usefulness as a source of high molecular weight DNA or RNA. Gamete Research 12, 1–10.CrossRefGoogle ScholarPubMed