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.
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.
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.
Blackburn EK (2001) Switching and signaling at the telomere. Cell 106: 661–673.
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.
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.
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.
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.
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.
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.
Garagna S, Zuccotti M, Capanna E, Redi CA (2002) Highresolution organization of mouse telomeric and pericentromeric DNA. Cytogenet Genome Res 96: 125–129.
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.
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.
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.
Li B, Oestreich S, de Lange T (2000) Identification of human Rap1: Implications for telomere evolution. Cell 101: 471–483.
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.
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.
Moens PB, Pearlman RE (1990) Telomere and centromere DNA are associated with the cores of meiotic prophase chromosomes. Chromosoma 100: 8–14.
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.
Page J, Suja JA, Santos JL, Rufas JS (1998) Squash procedure for protein immunolocalization in meiotic cells. Chromosome Res 6: 639–642.
Parra MT, Page J, Yen TJ et al. (2002) Expression and behaviour of CENP-E at kinetochores during mouse spermatogenesis. Chromosoma 111: 53–61.
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.
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.
Petronczki M, Siomos MF, Nasmyth K (2003) Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 21: 423–440.
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.
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.
Smith S, de Lange T (1997) TRF1, a mammalian telomeric protein. Trends Genet 13: 21–26.
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.
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.
Viera A, Parra MT, Rufas JS, Suja JA (2002) Size heterogeneity of telomeric DNA in mouse meiotic chromosomes. Cytogenet Genome Res 28: 221–224.
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.
Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32: 619–697.
Author information
Authors and Affiliations
Rights 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
Issue Date:
DOI: https://doi.org/10.1023/B:CHRO.0000005781.71466.da