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Chromosome Research

, Volume 3, Issue 7, pp 399–409 | Cite as

Loss of telomeric sites in the chromosomes ofMus musculus domesticus (Rodentia: Muridae) during Robertsonian rearrangements

  • Indrajit Nanda
  • Sonja Schneider-Rasp
  • Heinz Winking
  • Michael Schmid
Article

Abstract

Mouse chromosomes possessing multiple Robertsonian rearrangements (Rb chromosomes) have been examined using fluorescencein situ hybridization with the telomeric consensus sequence (TTAGGG)n. No hybridization signals were detected at the primary constriction of Rb chromosomes. This observation leads us to conclude that the formation of Rb chromosomes in the mouse is invariably associated with the loss of telomeric regions. More significantly, a further alteration in regions flanking the primary constrictions was observed after hybridizing with a minor satellite DNA probe to Rb chromosomes. It seems likely that the breakpoints required for a Robertsonian process do not include telomeric sites exclusively but extend to the adjacent pericentromeric regions of the original acrocentric chromosomes. In contrast to previous reports, these observations demonstrate the elimination of substantial amounts of chromosomal DNA during the formation of mouse Rb chromosomes.

Key words

minor satellite DNA Mus Robertsonian rearrangements telomeres Y chromosome 

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References

  1. Ashley T, Ward DC (1993) A ‘hot spot’ of recombination coincides with an interstitial telomeric sequence in the Armenian hamster.Cytogenet Cell Genet 62: 169–171.Google Scholar
  2. Baker RJ, Bickham JW (1986) Speciation by monobrachial centric fusions.Proc Natl Acad Sci USA 83: 8245–8248.Google Scholar
  3. Belkhir K, Britton-Davidian J, Konig B (1991) De nouvelles populations robertsoniennes de souris (Mus musculus domesticus) au nord des Alpes.Genome 34: 658–660.Google Scholar
  4. Blin N, Stafford DW (1976) A general method for isolation of high molecular weight DNA from eukaryotes.Nucleic Acids Res 3: 2303–2308.Google Scholar
  5. Broccoli D, Miller OJ, Miller D (1990) Relationship of mouse minor satellite DNA to centromere activity.Cytogenet Cell Genet 54: 182–186.Google Scholar
  6. Capanna E (1982) Robertsonian numerical variation in animal speciation:Mus musculus, an emblematic model. In: Barigozzi C, ed.Mechanisms of Speciation. New York: Alan R Liss, pp 155–177.Google Scholar
  7. Capanna E, Gropp A, Winking H, Noack G, Civitelli MV (1976) Robertsonian metacentrics in the mouse.Chromosoma 58: 341–353.Google Scholar
  8. Carpenter ATC (1987) Gene conversion, recombination nodules, and the initiation of meiotic synapsis.BioEssays 6: 232–236.Google Scholar
  9. Comings DE, Avelino E (1972) DNA loss during Robertsonian fusion in studies of the Tobacco mouse.Nature New Biol 237: 199.Google Scholar
  10. Comings DE, Okada TA (1970) Whole-mount electron microscopy of the centromeric region of metacentric and telocentric mammalian chromosomes.Cytogenetics 9: 436–449.Google Scholar
  11. Eicher EM, Lee BK, Washburn LL, Hale DW, King TR (1992) Telomere-related markers for the pseudoautosomal region of the mouse genome.Proc Natl Acad Sci USA 89: 2160–2164.Google Scholar
  12. Elder FFB, Hsu TC (1988) Tandem fusion in the evolution of mammalian chromosomes. In: Daniel A, ed.The Cytogenetics of Mammalian Autosomal Rearrangements. New York: Alan R Liss, pp 481–506.Google Scholar
  13. Elliott RW, Yen C-H (1991) DNA variants with telomere probe enable genetic mapping of ends of mouse chromosomes.Mammalian Genome 1: 118–122.Google Scholar
  14. Garagna S, Redi CA, Capanna Eet al. (1993) Genome distribution, chromosomal allocation and organization of the major and minor satellite DNAs in 11 species and subspecies of the genusMus.Cytogenet Cell Genet 64: 247–255.Google Scholar
  15. Gropp A, Tettenborn U, Lehmann E (1970) Chromosomenvariation vom Robertsonschen Typus bei der TabakmausM. poschiavinus und ihren hybriden mit der laboratoriumsmaus.Cytogenetics 9: 9–23.Google Scholar
  16. Gropp A, Winking H, Zech L, Müller HJ (1972) Robertsonian chromosomal variation and identification of metacentric chromosomes in feral mice.Chromosoma 39: 265–288.Google Scholar
  17. Guttenbach M, Schmid M (1990) Determination of Y chromosome aneuploidy in human sperm nuclei by nonradioactivein situ hybridization.Am J Hum Genet 46: 553–558.Google Scholar
  18. Hastie ND, Allshire RC (1989) Human telomeres: fusion and interstitial sites.Trends Genet 5: 326–331.Google Scholar
  19. Holmquist G, Dancis BM (1980) A general model of karyotype evolution.Genetica 52/53: 151–163.Google Scholar
  20. Hsu TC, Patton JL (1969) Bone marrow preparations for chromosome studies. In: Benrischke K, ed.Comparative Mammalian Cytogenetics. Berlin: Springer, pp 454–460.Google Scholar
  21. Hsu TC, Pathak S, Chen TR (1975) The possibility of latent centromeres and a proposed nomenclature system for total chromosome and whole arm translocations.Cytogenet Cell Genet 15: 41–49.Google Scholar
  22. Ijdo JW, Baldini A, Ward DC, Reeders ST, Wells RA (1991) Origin of human chromosome 2: An ancestral telomere-telomere fusion.Proc Natl Acad Sci USA 88: 9051–9055.Google Scholar
  23. John B, Freeman M (1975) Causes and consequences of Robertsonian exchange.Chromosoma 52: 123–136.Google Scholar
  24. 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.Google Scholar
  25. Matthew R (1965) Cytogenetic mechanism and speciations of mammals.In vitro 1: 1–11.Google Scholar
  26. Meyne J, Ratliff RL, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG)n among vertebrates.Proc Natl Acad Sci USA 89: 7049–7053.Google Scholar
  27. Meyne J, Baker RJ, Hobart HHet al. (1990) Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes.Chromosoma 99: 3–10.Google Scholar
  28. Miller OJ, Miller DA, Tantravahi R, Dev VG (1978) Nucleolus organizer activity and the origin of Robertsonian translocation.Cytogenet Cell Genet 20: 40–50.Google Scholar
  29. Moyzis RK, Buckingham JM, Cram LSet 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.Google Scholar
  30. Narayanswami S, Doggett NA, Clark LM, Hildebrand CE, Weier H-U, Hamkalo BA (1992) Cytological and molecular characterization of centromeres inMus domesticus andMus spretus.Mammalian Genome 2: 186–194.Google Scholar
  31. Park VM, Gustashaw KM, Wathen TM (1992) The presence of interstitial telomeric sequences in constitutional chromosome abnormalities.Am J Hum Genet 50: 914–923.Google Scholar
  32. Pluta AF, Zakian VA (1989) Recombination occurs during telomere formation in yeast.Nature 337: 429–433.Google Scholar
  33. Redi CA, Garagna S, Mazzini S, Winking H (1986) Pericentromeric heterochromatin and A-T contents during Robertsonian fusion in the house mouse.Chromosoma 94: 31–35.Google Scholar
  34. Redi CA, Garagna G, Zuccotti M (1990) Robertsonian chromosome formation and fixation: the genomic scenario.Biol J Linn Soc 41: 235–255.Google Scholar
  35. Reimann N, Rogalla P, Kazmierczak Bet al. (1994) Evidence that metacentric and submetacentric chromosomes in canine tumors can result from telomeric fusions.Cytogenet Cell Genet 67: 81–85.Google Scholar
  36. Robertson WRB (1916) Chromosome studies. I. Taxonomic relationships shown in the chromosomes of tettigidae and acrididae: V-shaped chromosomes and their significance in acrididae, locustidae, and gryllidae: chromosomes and variation.J Morphol 27: 179–331.Google Scholar
  37. Rossi E, Floridia G, Casali Met al. (1993) Types, stability, and phenotype consequences of chromosome rearrangements leading to interstitial telomeric sequences.J Med Genet 30: 926–931.Google Scholar
  38. Seabright M (1971) A rapid banding technique for human chromosomes.Lancet ii: 971–972.Google Scholar
  39. Scherthan H (1990) Localization of the repetitive telomeric sequence (TTAGGG)n in two muntjac species and implications for their karyotypic evolution.Cytogenet Cell Genet 53: 115–117.Google Scholar
  40. Schmid M, Feichtinger W, Nanda Iet al. (1994) An extraordinary low diploid chromosome number in the reptileGonatodes taniae (Sauria, Gekonidae) J Hered 85: 255–260.Google Scholar
  41. Schubert I, Schriever-Schwemmer G, Werner T, Adler I-D (1992) Telomeric signals in Robertsonian fusion and fission chromosomes: implication for the origin of pseudoaneuploidy.Cytogenet Cell Genet 59: 6–9.Google Scholar
  42. Starling JA, Maule J, Hastie ND, Allshire RC (1990) Extensive telomere repeat arrays in mouse are hypervariable.Nucleic Acids Res 18: 6881–6888.Google Scholar
  43. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin.Exp Cell Res 75: 304–306.Google Scholar
  44. Tucker PK, Lee BK, Lundrigan BL, Eicher EM (1992) Geographic origin of the Y chromosomes in ‘old’ inbred strains of mice.Mammalian Genome 3: 254–261.Google Scholar
  45. White MJD (1973)Animal Cytology and Evolution. Cambridge: Cambridge University Press.Google Scholar
  46. Winking H, Beatrica D, Bulfield G (1988) Robertsonian karyotype variation in the European house mouse,Mus musculus: survey of present knowledge and new observations.Z Säugetierkunde 53: 148–161.Google Scholar
  47. Wong AKC, Rattner JB (1988) Sequence organization and cytological localization of the minor satellite of mouse.Nucleic Acids Res 16: 11645–11661.Google Scholar
  48. Wong AKC, Biddle FG, Rattner JB (1990) The chromosomal distribution of the major and minor satellite is not conserved in the genusMus.Chromosoma 99: 190–195.Google Scholar

Copyright information

© Rapid Communications of Oxford Ltd 1995

Authors and Affiliations

  • Indrajit Nanda
    • 1
  • Sonja Schneider-Rasp
    • 1
  • Heinz Winking
    • 2
  • Michael Schmid
    • 1
  1. 1.the Department of Human GeneticsUniversity of WürzburgWürzburgGermany
  2. 2.the Institute of BiologyUniversity of LübeckGermany

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