Chromosome Research

, Volume 11, Issue 5, pp 503–512 | Cite as

Conservation of chromosome arrangement and position of the X in mammalian sperm suggests functional significance

  • Ian K. Greaves
  • Willem Rens
  • Malcolm A. Ferguson-Smith
  • Darren Griffin
  • Jennifer A. Marshall Graves
Article

Abstract

We used chromosome painting to show directly that chromosomes occupy fixed positions in the nuclei of mammal but not chicken sperm. We found that the positions of homologous chromosomes are conserved in sperm of two marsupial species that diverged 50–60 million years ago. We also discovered that the X chromosome lies in the region that makes first contact with the egg in marsupial and monotreme mammals, as well as eutherians, and suggest that this position may be related to its propensity for inactivation, and its high rate of loss from ICSI embryos. We propose that nuclear architecture in sperm is important for spatial chromatin differentiation and normal development of the fertilized egg, and evolved along with mammal-specific regulatory systems such as X inactivation and genomic imprinting.

chicken chromatin chromosome painting Eutheria imprinting marsupial sperm X-inactivation 

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References

  1. Barr ML, Bertram EG (1949) A morphological distinction between neurons oft he male and female, and the behaviour oft he nucleolar satellite during accelerated nucleoprotein synthesis. Nature 163: 676-677.PubMedGoogle Scholar
  2. Borden J, Manuelidis L (1988) Movement oft he X chromosome in epilepsy. Science 242: 1687-1691.PubMedGoogle Scholar
  3. Boyle S, Gilchrist S, Bridger JM, Mahy NL, Ellis JA, Bickmore WA (2001) The spatial organization ofhu man chromosomes within the nuclei ofno rmal and emerin-mutant cells. Hum Mol Genet 10: 211-219.PubMedCrossRefGoogle Scholar
  4. Breed WG (1994) How does sperm meet egg? in a marsupial. Reprod Fertil Dev 6: 485-506.PubMedCrossRefGoogle Scholar
  5. Bridger JM, Boyle S, Kill IR, Bickmore WA (2000) Re-modelling ofnu clear architecture in quiescent and senescent human ¢broblasts. Curr Biol 10: 149-152.PubMedCrossRefGoogle Scholar
  6. Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, Fisher AG (1997) Association oft ranscriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 91: 845-854.PubMedCrossRefGoogle Scholar
  7. Comings DE (1968) The rationale for an ordered arrangement of chromatin in the interphase nucleus. Am J Hum Genet 20: 440-460.PubMedGoogle Scholar
  8. Cremer M, von Hase J, Volm T et al. (2001) Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells. Chromosome Res 9: 541-567.PubMedCrossRefGoogle Scholar
  9. Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA (1999) Differences in the localization and morphology ofch romosomes in the human nucleus. J Cell Biol 145: 1119-1131.PubMedCrossRefGoogle Scholar
  10. De Leo AA, Guedelha N, Toder R et al. (1999) Comparative chromosome painting between marsupial orders: relationships with a 2n=14 ancestral marsupial karyotype. Chromosome Res 7: 509-517.PubMedCrossRefGoogle Scholar
  11. Douglas LT (1965) Evidence for tandem arrangement of chrommosomal elements in spermatid nuclei oft he chinese hamster. Genetica 36: 59-64.PubMedCrossRefGoogle Scholar
  12. Ellegren H (2002) Dosage compensation: do birds do it as well? Trends Genet 18: 25-28.PubMedCrossRefGoogle Scholar
  13. Francastel C Schubeler D, Martin DI, Groudine M (2000) Nuclear compartmentalization and gene activity. Nat Rev Mol Cell Biol 1: 137-143.PubMedCrossRefGoogle Scholar
  14. Gardiner-Garden M, Ballesteros M, Gordon M, Tam PP (1998). Histone-and protamine-DNA association: conservation ofd ifferent patterns within the beta-globin domain in human sperm. Mol Cell Biol 18: 3350-3356.PubMedGoogle Scholar
  15. Gatewood JM, Cook GR, Balhorn R, Bradbury EM, Schmid CW (1987) Sequence-speci¢c packaging ofD NA in human sperm chromatin. Science 236: 962-964.PubMedGoogle Scholar
  16. Greaves IK, Svartman M, Wake¢eld M et al. (2001) Chromosomal painting detects non-random chromosome arrangement in dasyurid marsupial sperm. Chromosome Res 9: 251-259.PubMedCrossRefGoogle Scholar
  17. Haaf T (2001) The battle of the sexes after fertilization: behaviour ofpa ternal and maternal chromosomes in the early mammalian embryo. Chromosome Res 9: 263-271.PubMedCrossRefGoogle Scholar
  18. Habermann FA, Cremer M, Walter J et al. (2001) Arrangements ofm acro-and microchromosomes in chicken cells. Chromosome Res 9: 569-584.PubMedCrossRefGoogle Scholar
  19. Hazzouri M, Rousseaux S, Mongelard F et al. (2000) Genome organization in the human sperm nucleus studied by FISH and confocal microscopy. Mol Reprod Dev 55: 307-315.PubMedCrossRefGoogle Scholar
  20. Hewitson L, Simerly C, Dominko T, Schatten G (2000) Cellular and molecular events after in vitro fertilization and intracytoplasmic sperm injection. Theriogenology 53: 95104.CrossRefGoogle Scholar
  21. Hughes-Schrader S (1946) A new type ofs permatogenesis in iceryine coccids with linear alignment ofc hromosomes in the sperm.J Morphol 78: 43-84.CrossRefGoogle Scholar
  22. In'tVeld P, Brandenberg H, Verhoeff A, Dhont M, Los F (1995) Sex chrommosomal abnormalities and intracytoplasmic sperm injection. Lancet 346: 773.CrossRefGoogle Scholar
  23. Kirsch JAW, Lapointe FJ, Springer M (1996) DNA-hybridization studies ofm arsupials and their implications formetatherianclassi¢cation. AustJZool 45:221-280.Google Scholar
  24. Kozubek S, Lukasova E, Mareckova A et al. (1999) The topological organization ofc hromosomes 9 and 22 in cell nuclei has a determinative role in the induction oft (9,22) translocations and in the pathogenesis oft (9,22) leukemias. Chromosoma 108: 426-435.PubMedCrossRefGoogle Scholar
  25. Lichter P, Cremer T, Borden J, Manuelidis L, Ward DC (1988) Delineation ofin dividual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum Genet 80: 224-234.PubMedCrossRefGoogle Scholar
  26. Lin M, Jones RC (2000) Spermiogenesis and spermiation in a monotreme mammal, the platypus, Ornithorhynchus anatinus.J Anat 196: 217-232.PubMedCrossRefGoogle Scholar
  27. Luetjens CM, Payne C, Schatten G (1999) Non-random chromosome positioning in human sperm and sex chromosome anomalies following intracytoplasmic sperm injection. Lancet 353: 1240.PubMedCrossRefGoogle Scholar
  28. Macgregor HC, Walker MH (1973) The arrangement of chromosomes in nuclei ofsp erm from Plethodontid salamanders. Chromosoma 40: 243-262.CrossRefGoogle Scholar
  29. Manuelidis L, Borden J (1988) Reproducible compartmentalization ofin dividual chromosome domains in human CNS cells revealed by in situ hybridization and threedimensional reconstruction. Chromosoma 96: 397-410.PubMedCrossRefGoogle Scholar
  30. Meyer-Ficca M, Muller-Navia J, Scherthan H(1998) Clustering ofpe ricentromeres initiates in step 9 ofsp ermiogenesis of the rat (Rattus norvegicus) and contributes to a well de¢ned genome architecture in the sperm nucleus. J Cell Sci 111: 1363-1370.PubMedGoogle Scholar
  31. Nagele RG, Freeman T, McMorrow L, Thomson Z, Kitson-Wind K, Lee H (1999) Chromosomes exhibit preferential positioning in nuclei ofq uiescent human cells. J Cell Sci 112: 525-535.PubMedGoogle Scholar
  32. Nogami M, Nogami O, Kagotani K et al. (2000) Intranuclear arrangement ofh uman chromosome 12 correlates to large-scale replication domains. Chromosoma 108: 514-522.PubMedCrossRefGoogle Scholar
  33. Oliva R, Dixon GH (1991) Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog Nucleic Acid Res Mol Biol 40: 25-94.PubMedCrossRefGoogle Scholar
  34. Rens W, O'Brien PCM, Yang F, Graves JAM, Ferguson-Smith MA (1999) Karyotypic relationships between four distantly related marsupials revealed by reciprocal chromosome painting. Chromosome Res 7: 461-474.PubMedCrossRefGoogle Scholar
  35. Rofe R, Hayman D (1985) G-banding evidence for a conserved complement in the Marsupialia. Cytogenet Cell Genet 39: 40-50.PubMedCrossRefGoogle Scholar
  36. Solovei IV, Joffe BI, Hori T, Thomson P, Mizuno S, Macgregor HC (1998) Unordered arrangement ofc hromosomes in the nuclei ofc hicken spermatozoa. Chromosoma 107: 184-188.PubMedCrossRefGoogle Scholar
  37. Tanabe H, Muller S, Neusser M et al. (2002) Evolutionary conservation ofc hromosome territory arrangements in cell nuclei from higher primates. Proc Natl Acad Sci USA 99: 4424-4429.PubMedCrossRefGoogle Scholar
  38. Taylor AH (1964) The arrangement ofc hromosomes in the mature sperm ofg rasshopper. J Cell Biol 21: 286289.CrossRefGoogle Scholar
  39. Terada Y, Luetjens CM, Sutovsky P, Schatten G (2000) Atypical decondensation oft he sperm nucleus delayed replication oft he male genome and sex chromosome positioning following intracytoplasmic human sperm injection (ICSI) into golden hamster eggs: does ICSI itselfin troduce chromosomal anomalies? Fertil Steril 74: 454-460.PubMedCrossRefGoogle Scholar
  40. Watson JM, Meyne J, Graves JA (1996) Ordered tandem arrangement ofc hromosomes in the sperm heads of monotreme mammals. Proc Natl Acad Sci USA 93: 10200-10205.PubMedCrossRefGoogle Scholar
  41. Wrigley JM, Graves JA (1988) Karyotypic conservation in the mammalian order monotremata (subclass Prototheria). Chromosoma 96: 231-247.PubMedCrossRefGoogle Scholar
  42. Zechner U, Wilda M, Kehrer-Sawatzki H, Vogel W, Fundele R, Hameister H (2001) A high density of X-linked genes for general cognitive ability: a run-away process shaping human evolution? Trends Genet 17: 697-701.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Ian K. Greaves
    • 1
    • 2
  • Willem Rens
    • 3
  • Malcolm A. Ferguson-Smith
    • 3
  • Darren Griffin
    • 4
  • Jennifer A. Marshall Graves
    • 1
    • 2
  1. 1.Research School of Biological SciencesThe Australian National UniversityCanberraAustralia
  2. 2.Department of GeneticsLaTrobe University, BundooraVictoriaAustralia
  3. 3.Department of Clinical Veterinary MedicineCambridge UniversityCambridgeUK
  4. 4.Department of Biological SciencesBrunel UniversityUxbridge, MiddlesexUK

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