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Organization of the X and Y chromosomes in human, chimpanzee and mouse pachytene nuclei using molecular cytogenetics and three-dimensional confocal analyses

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Abstract

We used multicolour fluorescence in-situ hybridization on air-dried pachytene nuclei to analyse the structural and functional domains of the sex vesicle (SV) in human, chimpanzee and mouse. The same technology associated with 3-dimensional analysis was then performed on human and mouse pachytene nuclei from cytospin preparations and tissue cryosections. The human and the chimpanzee SVs were very similar, with a consistently small size and a high degree of condensation. The mouse SV was most often seen to be large and poorly condensed, although it did undergo progressive condensation during pachynema. These results suggest that the condensation of the sex chromosomes is not a prerequisite for the formation of the mouse SV, and that a different specific mechanism could be responsible for its formation. We also found that the X and Y chromosomes are organized into two separate and non-entangled chromatin domains in the SV of the three species. In each species, telomeres of the X and Y chromosomes remain clustered in a small area of the SV, even those without a pseudoautosomal region. The possible mechanisms involved in the organization of the sex chromosomes and in SV formation are discussed.

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References

  • Ariel M, Robinson E, McCarrey JR, Cedar H (1995) Gamete-specific methylation correlates with imprinting of the murine Xist gene. Nat Genet 9: 312–315.

    Google Scholar 

  • Armstrong SJ, Kirkham AJ, Hultén MA (1994) XY chromosome behaviour in the germ line of the human male: a FISH analysis of spatial orientation, chromatin condensation and pairing. Chromosome Res 2: 445–452.

    Google Scholar 

  • Ayoub N, Richler C, Wahrman J (1997) Xist RNA is associated with the transcriptionally inactive XY body in mammalian male meiosis. Chromosoma 106: 1–10.

    Google Scholar 

  • Bishop CE (1992) The mouse Y chromosome. Mamm Genome 3 Spec No: S289–S293.

    Google Scholar 

  • Bonhomme F, Guénet JL (1989) The wild mouse and its relative. In Lyon MF, Searle AG, eds., Genetic Variants and Strains of the Laboratory Mouse, 2nd edn. Oxford: Oxford University Press, pp 649–662.

    Google Scholar 

  • Burgoyne PS (1982) Genetic homology and crossing over in the X and Y chromosomes of mammals. Hum Genet 61: 85–90.

    Google Scholar 

  • Chandley AC, Goetz P, Hargreave TB, Joseph AM, Speed RM (1984) On the nature and extent of XY pairing at meiotic prophase in man. Cytogenet Cell Genet 38: 241–247.

    Google Scholar 

  • Disteche CM, Tantravahi U, Gandy S, Eisenhard M, Adler D, Kunkel LM (1985) Isolation and characterization of two repetitive DNA fragments located near the centromere of the mouse X chromosome. Cytogenet Cell Genet 39: 262–268.

    Google Scholar 

  • Graves JAM, Wakefield MJ, Toder R (1998) The origin and evolution of the pseudoautosomal regions of human sex chromosomes. Hum Mol Genet 7: 1991–1996.

    Google Scholar 

  • Heard E, Mongelard F, Arnaud D, Avner P (1999) Xist yeast artificial chromosome transgenes function as X-inactivation centers only in multicopy arrays and not as single copies. Mol Cell Biol 19: 3156–3166.

    Google Scholar 

  • Koshland D, Strunnikov A (1996) Mitotic chromosome condensation. Annu Rev Cell Dev Biol 12: 305–3333.

    Google Scholar 

  • Kralewski M, Novello A, Bennavente R (1997) A novel Mr 77,000 protein of the XY body of mammalian spermatocytes: its localization in normal animals and in Searle's translocation carriers. Chromosoma 106: 160–167.

    Google Scholar 

  • Kvalov K, Galvagni F, Brown WRA (1994) The sequence organization of the long arm pseudoautosomal region of the human sex chromosomes. Hum Mol Genet 3: 771–778.

    Google Scholar 

  • Lansdorp PM, Verwoerd NP, van de Rijke FM et al. (1996) Heterogeneity in telomere length of human chromosomes. Hum Mol Genet 5: 685–691.

    Google Scholar 

  • Lee JT, Jaenisch R (1997) The epigenetic control of mammalian X-chromosome. Curr Opin Genet Dev 7: 274–280.

    Google Scholar 

  • Lengauer C, Green ED, Cremer T (1992) Fluorescence in situ hybridization of YAC clones after alu-PCR amplification. Genomics 13: 826–828.

    Google Scholar 

  • Luciani JM, Morazzani MR, Stahl A (1975) Identification of pachytene bivalents in human male meiosis using G-banding technique. Chromosoma 52: 275–282.

    Google Scholar 

  • McCarrey J, Dilworth DD (1992) Expression of Xist in mouse germ cells correlates with X-chromosome inactivation. Nat Genet 2: 200–203.

    Google Scholar 

  • McKee BD, Handel MA (1993) Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102: 71–80.

    Google Scholar 

  • Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R (1997) Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Devel 11: 156–166.

    Google Scholar 

  • Metzler-Guillemain C, Mignon C, Depetris D, Guichaoua MR, Mattei MG (1999) Bivalent 15 regularly associates with the sex vesicle in normal male meiosis. Chromosome Res 7: 369–378.

    Google Scholar 

  • Mitchell MJ (2000) Spermatogenesis and the mouse Y chromosome: specialisation out of decay. In: Results and Problems in Cell Differentiation. Berlin Heidelberg: Springer-Verlag, p 28.

    Google Scholar 

  • Morton NE (1991) Parameters of the human genome. Proc Natl Acad Sci USA 88: 7474–7476.

    Google Scholar 

  • Motzkus D, Singh PB, Hoyer-Fender S (1999) M31, a murine homolog of drosophila HP1, is concentrated in the XY body during spermatogenesis. Cytogenet Cell Genet 86: 83–88.

    Google Scholar 

  • Parazza F, Humbert C, Usson Y (1993) Method for 3D volumetric analysis of intranuclear fluorescence distribution in confocal microscopy. Comput Med Imag Graph 17: 189–200.

    Google Scholar 

  • Parazza F, Bertin E, Wozniak Z, Usson Y (1995) Analysis of the spatial distribution of the AgNOR proteins in cell nuclei using simultaneous confocal scanning laser fluorescence and transmitted light microscopy. J Microsc 178: 251–260.

    Google Scholar 

  • Parraga M, Del Mazo J (2000) XYbp, a novel RING-finger protein, is a component of the XY body of spermatocytes and centrosomes. Mech Dev 90: 95–101.

    Google Scholar 

  • Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83: 2934–2938.

    Google Scholar 

  • Popp S, Scholl HP, Loos P et al. (1990) Distribution of chromosome 18 and X centric heterochromatin in the interphase nucleus of cultured human cells. Exp Cell Res 189: 1–12.

    Google Scholar 

  • Rettenberger G, Zimmermann W, Klett C, Zechner U, Hameister H (1995) Mapping of murine YACs containing the genes Cea2 and Cea4 after B1–PCR amplification and FISH analysis. Chromosome Res 3: 473–478.

    Google Scholar 

  • Richler C, Soreq H, Wahrman J (1992) X inactivation in mammalian testis is correlated with inactive X-specific transcription. Nat Genet 2: 192–195.

    Google Scholar 

  • Richler C, Uliel E, Kerem BS, Wahrman J (1987) Regions of active chromatin conformation in ``inactive'' male meiotic sex chromosomes in the mouse. Chromosoma 95: 167–170.

    Google Scholar 

  • Salido EC, Yen PH, Mohandas TK, Shapiro LJ (1992) Expression of the X-inactivation-associated gene Xist during spermatogenesis. Nat Genet 2: 196–199.

    Google Scholar 

  • Salido EC, Li XM, Yen PH, Martin N, Mohandas TK, Shapiro LJ (1996) Cloning and expression of the mouse pseudoautosomal steroid sulphatase gene (Sts). Nat Genet 13: 83–86.

    Google Scholar 

  • Schmid M, Haaf T (1984) DistamycinA/DAPI bands and the effects of 5–azacytine on the chromosomes of the chimpanzee, Pan troglodytes. Cytogenet Cell Genet 38: 192–199.

    Google Scholar 

  • Schnedl W, Dev VG, Trantravahi R, Miller DA, Erlanger BF, Miller OJ (1975) 5–Methylcytosine in heterochromatic regions of chromosomes: chimpanzee and gorilla compared to human. Chromosoma 52: 59–66.

    Google Scholar 

  • Sharp P (1982) Sex chromosome pairing during male meiosis in marsupials. Chromosoma 86: 27–42.

    Google Scholar 

  • Sherthan H, Weich S, Schwegler H, Heyting C, Härle M, Cremer T (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134: 1109–1125.

    Google Scholar 

  • Smith A, Benavente R (1992) Meiosis-specific protein selectively associated with sex chromosomes of rat pachytene spermatocytes. Proc Natl Acad Sci USA 89: 6938–6942.

    Google Scholar 

  • Solari AJ (1969). The evolution of the ultrastructure of the sex chromosomes (sex vesicle) during meiotic prophase in mouse spermatocytes. J Ultrastruct Res 27: 289–305.

    Google Scholar 

  • Solari AJ (1974) The behaviour of the XY pair in mammals. Int Rev Cytol 38: 273–317.

    Google Scholar 

  • Solari AJ (1980) Synaptonemal complexes and associated structures in microspread human spermatocytes. Chromosoma 81: 315–337

    Google Scholar 

  • Solari AJ (1989) Sex chromosome pairing and fertility in the heterogametic sex of mammals and birds. In: Gillies CB, ed. Fertility and Chromosome Pairing. Recent Studies in Plants and Animals. Boca Raton, Florida: CRC Press, pp 77–107.

    Google Scholar 

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Metzler-Guillemain, C., Usson, Y., Mignon, C. et al. Organization of the X and Y chromosomes in human, chimpanzee and mouse pachytene nuclei using molecular cytogenetics and three-dimensional confocal analyses. Chromosome Res 8, 571–584 (2000). https://doi.org/10.1023/A:1009277722579

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