Skip to main content
Log in

Dynamic relocation of telomere complexes in mouse meiotic chromosomes

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Telomeric DNA repeats as well as different specific proteins such as TRF1 and Rap1 associate in functional telomere complexes found at chromosome ends. Using spreading techniques, the presence of TRF1 and Rap1 has been reported at mammalian meiotic telomeres during prophase I. In the present study, we have analysed, by fluorescence in-situ hybridization and immunofluorescence, the appearance and location of telomere complexes during both male mouse meiotic divisions. Additionally, we have studied their relationship with different centromere/kinetochore proteins and the synaptonemal complex protein SCP3. Our results show that telomere complexes are not located at condensed meiotic chromosome tips. Therefore, a change in chromosome structure may occur from pachytene up to metaphase I involving the dynamic relocation of telomere complexes in condensed chromosomes. Moreover, we have found that proximal telomere complexes are relocated internally to kinetochores from metaphase I up to anaphase II. We discuss the functional significance of the location of telomere complexes into internal domains of condensed meiotic chromosomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alsheimer M, Benavente R (1996) Change of karyoskeleton during mammalian spermatogenesis: expression pattern of nuclear lamin C2 and its regulation. Exp Cell Res 228: 181–188.

    Article  PubMed  CAS  Google Scholar 

  • Bianchi A, Smith S, Chong L, Elias P, de Lange T (1997) TRF1 is a dimer and bends telomeric DNA. EMBO J 16: 1785–1794.

    Article  PubMed  CAS  Google Scholar 

  • Blackburn EK (2001) Switching and signaling at the telomere. Cell 106: 661–673.

    Article  PubMed  CAS  Google Scholar 

  • Broccoli D, Chong L, Oelmann S et al. (1997) Comparison of the human and mouse genes encoding the telomeric protein, TRF1: chromosomal localization, expression and conserved protein domains. Hum Mol Genet 6: 69–76.

    Article  PubMed  CAS  Google Scholar 

  • Cooke CA, Schaar B, Yen TJ, Earnshaw WC (1997) Localization of CENP-E in the fibrous corona and outer plate of mammalian kinetochores from prometaphase through anaphase. Chromosoma 106: 446–455.

    Article  PubMed  CAS  Google Scholar 

  • Cuñado N, Santos JL (1998) A method for fluorescence in situ hybridization against synaptonemal complex-associated chromatin of plant meiocytes. Exp Cell Res 239: 179–182.

    Article  PubMed  Google Scholar 

  • Cuñado N, Garrido-Ramos MA, de la Herrán R, Ruíz Rejón C, Ruíz Rejón M, Santos JL (2000) Organization of repetitive DNA sequences at pachytene chromosomes of gilthead seabream Sparus auratus (Pisces, Perciformes). Chromosome Res 8: 67–72.

    Article  PubMed  Google Scholar 

  • Dernburg AF, Sedat JW, Cande WZ, Bass HW (1995) Cytology of telomeres. In: Blackburn EH. and Greider CW., <nt>eds.</nt> Telomeres. Plainview, New York: Cold Spring Harbor Laboratory Press, pp 295–338.

    Google Scholar 

  • Franco S, Alsheimer M, Herrera E, Benavente R, Blasco MA (2002) Mammalian meiotic telomeres: composition and ultrastructure in telomerase-deficient mice. Eur J Cell Biol 81: 335–340.

    Article  PubMed  Google Scholar 

  • Garagna S, Zuccotti M, Capanna E, Redi CA (2002) Highresolution organization of mouse telomeric and pericentromeric DNA. Cytogenet Genome Res 96: 125–129.

    Article  PubMed  CAS  Google Scholar 

  • Heng HHQ, Chamberlain JW, Shi XM, Spyropoulos B, Tsui LC, Moens PB (1996) Regulation of meiotic chromatin loop size by chromosomal position. Proc Natl Acad Sci USA 93: 2795–2800.

    Article  PubMed  CAS  Google Scholar 

  • Kipling D, Ackford HE, Taylor BA, Cooke HJ (1991) Mouse minor satellite DNA genetically maps to the centromere and is physically linked to the proximal telomere. Genomics 11: 235–241.

    Article  PubMed  CAS  Google Scholar 

  • Lammers JH, Offenberg HH, van Aalderen M, Vink AC, Dietrich AJ, Heyting C (1994) The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol 14: 1137–1146.

    PubMed  CAS  Google Scholar 

  • Li B, Oestreich S, de Lange T (2000) Identification of human Rap1: Implications for telomere evolution. Cell 101: 471–483.

    Article  PubMed  CAS  Google Scholar 

  • Lombillo VA, Nislow C, Yen TJ, Gelfand VI, McIntosh JR (1995) Antibodies to the kinesin motor domain and CENP-E inhibit microtubule depolymerization-dependent motion of chromosomes in vitro. J Cell Biol 128: 107–115.

    Article  PubMed  CAS  Google Scholar 

  • Meyne J, Baker RJ, Hobart HH et al. (1990) Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99: 3–10.

    Article  PubMed  CAS  Google Scholar 

  • Moens PB, Pearlman RE (1990) Telomere and centromere DNA are associated with the cores of meiotic prophase chromosomes. Chromosoma 100: 8–14.

    Article  PubMed  CAS  Google Scholar 

  • Moyzis RK, Buckingham JM, Cram LS et al. (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci USA 85: 6622–6626.

    Article  PubMed  CAS  Google Scholar 

  • Page J, Suja JA, Santos JL, Rufas JS (1998) Squash procedure for protein immunolocalization in meiotic cells. Chromosome Res 6: 639–642.

    Article  PubMed  CAS  Google Scholar 

  • Parra MT, Page J, Yen TJ et al. (2002) Expression and behaviour of CENP-E at kinetochores during mouse spermatogenesis. Chromosoma 111: 53–61.

    Article  PubMed  CAS  Google Scholar 

  • Parra MT, Viera A, Gómez R et al. (2003) Dynamic relocalization of the chromosomal passenger complex proteins inner centromere protein (INCENP) and aurora-B kinasa during male mouse meiosis. J Cell Sci 116: 961–974.

    Article  PubMed  CAS  Google Scholar 

  • Peters AHFM, Plug AW, van Vugt MJ, de Boer P (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germ line. Chromosome Res 5: 66–68.

    Article  PubMed  CAS  Google Scholar 

  • Petronczki M, Siomos MF, Nasmyth K (2003) Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 21: 423–440.

    Article  Google Scholar 

  • Scherthan 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.

    Article  PubMed  CAS  Google Scholar 

  • Scherthan H, Jerratsch M, Li B et al. (2000) Mammalian meiotic telomeres: protein composition and redistribution in relation to nuclear pores. Mol Biol Cell 11: 4189–4203.

    PubMed  CAS  Google Scholar 

  • Smith S, de Lange T (1997) TRF1, a mammalian telomeric protein. Trends Genet 13: 21–26.

    Article  PubMed  CAS  Google Scholar 

  • Steinmüller J, Schleiermacher E, Scherthan H (1993) Direct detection of repetitive, whole chromosome paint and telomere DNA probes by immunogold electron microscopy. Chromosome Res 1: 45–51.

    Article  PubMed  Google Scholar 

  • Valdivia MM, Figueroa J, Iglesias C, Ortiz M (1998) A novel centromere monospecific serum to a human autoepitope on the histone H3-like protein CENP-A. FEBS Lett 23: 5–9.

    Article  Google Scholar 

  • Viera A, Parra MT, Rufas JS, Suja JA (2002) Size heterogeneity of telomeric DNA in mouse meiotic chromosomes. Cytogenet Genome Res 28: 221–224.

    Article  CAS  Google Scholar 

  • Warburton PE, Cooke CA, Bourassa S et al. (1997) Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr Biol 7: 901–904.

    Article  PubMed  CAS  Google Scholar 

  • Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32: 619–697.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Viera, A., Parra, M.T., Page, J. et al. Dynamic relocation of telomere complexes in mouse meiotic chromosomes. Chromosome Res 11, 797–807 (2003). https://doi.org/10.1023/B:CHRO.0000005781.71466.da

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:CHRO.0000005781.71466.da

Navigation