Skip to main content
Log in

Non-random positioning of chromosomes in human sperm nuclei

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

In human spermatozoa, the arrangement of chromosomes is non-random. Characteristic features are association of centromeres in the interior chromocenter and peripheral location of telomeres. In this paper, we have investigated the highest level of order in DNA packing in sperm – absolute and relative intranuclear chromosome positioning. Asymmetrical nuclear shape, existence of a defined spatial marker, and the haploid complement of chromosomes facilitated an experimental approach using in situ hybridization. Our results showed the tendency for non-random intranuclear location of individual chromosome territories. Moreover, centromeres demonstrated specific intranuclear position, and were located within a limited area of nuclear volume. Additionally, the relative positions of centromeres were non-random; some were found in close proximity, while other pairs showed significantly greater intercentromere distances. Therefore, a unique and specific adherence may exist between chromosomes in sperm. The observed chromosome order is discussed in relation to sperm nuclei decondensation, and reactivation during fertilization.

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

  • Allison DC, Nestor AL (1999) Evidence for a relatively random array of human chromosomes on the mitotic ring. J Cell Biol 145: 1-14.

    Article  PubMed  CAS  Google Scholar 

  • Ashley T (1979) Specific end-to-end attachment of chromosomes in Ornithogalum virens. J Cell Sci 38: 357-367.

    PubMed  CAS  Google Scholar 

  • Balhorn R (1982) A model for the structure of chromatin in mammalian sperm. J Cell Biol 93: 298-305.

    Article  PubMed  CAS  Google Scholar 

  • Bickmore WA, Chubb JR (2003) Chromosome position: now, where was I? Curr Biol 13: 357-359.

    Article  Google Scholar 

  • Bojanowski K, Maniotis AJ, Plisov S, Larsen AK, Ingber DE (1998) DNA topoisomerase II can drive changes in higher order chromosome architecture without enzymatically modifying DNA. J Cell Biochem 69: 127-142.

    Article  PubMed  CAS  Google Scholar 

  • Boyle S, Gilchrist S, Bridger JM, Mahy NL, Ellis JA, Bickmore WA (2001). The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum Mol Genet 10: 211-219.

    Article  PubMed  CAS  Google Scholar 

  • Blobel G (1985) Gene gating: a hypothesis. Proc Natl Acad Sci USA 82: 8527-8529.

    Article  PubMed  CAS  Google Scholar 

  • Cockell M, Gasser SM (1999) Nuclear compartments and gene regulation. Curr Opin Genet Dev 9: 199-205.

    Article  PubMed  CAS  Google Scholar 

  • Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2: 292-301.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145: 1119-1131.

    Article  PubMed  CAS  Google Scholar 

  • Dozortsev D, Coleman A, Nagy P, et al. (2000) Nucleoli in a pronuclei-stage mouse embryo are represented by major satellite DNA of interconnecting chromosomes. Fertil Steril 73: 366-371.

    Article  PubMed  CAS  Google Scholar 

  • Dundr M, Misteli T (2001) Functional architecture in the cell nucleus. Biochem J 356: 297-310.

    Article  PubMed  CAS  Google Scholar 

  • Francastel C, Walters MC, Groudine M, Martin DI (1999) A functional enhancer suppresses silencing of a transgene and prevents its localization close to centromeric heterochromatin. Cell 99: 259-269.

    Article  PubMed  CAS  Google Scholar 

  • Gasser SM (2002) Visualizing chromatin dynamics in interphase nuclei. Science 296: 1412-1416.

    Article  PubMed  CAS  Google Scholar 

  • Geraedts JP, Pearson PL (1975) Spatial distribution of chromosomes 1 and Y in human spermatozoa. J. Reprod Fertil 45: 515-417.

    Article  PubMed  CAS  Google Scholar 

  • Greaves IK, Rens W, Ferguson-Smith MA, Griffin D, Marshall-Graves JA (2003) Conservation of chromosome arrangement and position of the X in mammalian sperm suggests functional significance. Chromosome Res 11: 503-512.

    Article  PubMed  CAS  Google Scholar 

  • Gurevitch M, Amiel A, Ben-Zion M, Fejgin M, Bartoov B (2001) Acrocentric centromere organization within the chromocenter of the human sperm nucleus. Mol Reprod Dev 60: 507-516.

    Article  PubMed  CAS  Google Scholar 

  • Haaf T (2001) The battle of the sexes after fertilization: behaviour of paternal and maternal chromosomes in the early mammalian embryo. Chromosome Res 9: 263-271.

    Article  PubMed  CAS  Google Scholar 

  • Haaf T, Ward DC (1995) Higher order nuclear structure in mammalian sperm revealed by in situ hybridization and extended chromatin fibers. Exp Cell Res 219: 604-611.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Heslop-Harrison JS (1996) Comparative analysis of plant genome architecture. Symp Soc Exp Biol 50: 17-23.

    PubMed  CAS  Google Scholar 

  • Hoyer-Fender S, Singh PB, Motzkus D (2000) The murine heterochromatin protein M31 is associated with the chromocenter in round spermatids and is a component of mature spermatozoa. Exp Cell Res 254: 72-79.

    Article  PubMed  CAS  Google Scholar 

  • Jennings C, Powell D (1995) Genome organization in the murine sperm nucleus. Zygote 3: 123-131.

    PubMed  CAS  Google Scholar 

  • Joffe BI, Solovei IV, Macgregor HC (1998) Ordered arrangement and rearrangement of chromosomes during spermatogenesis in two species of planarians (Plathelminthes). Chromosoma 107: 173-183.

    Article  PubMed  CAS  Google Scholar 

  • Leitch AR, Brown JK, Mosgoller W, Schwarzacher T, Heslop-Harrison JS (1994) The spatial localization of homologous chromosomes in human fibroblasts at mitosis. Hum Genet 93: 275-280.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Maniotis AJ, Bojanowski K, Ingber DE (1997) Mechanical continuity and reversible chromosome disassembly within intact genomes removed from living cells. J Cell Biochem 65: 114-130.

    Article  PubMed  CAS  Google Scholar 

  • Marshall WF (2002) Order and disorder in the nucleus. Curr Biol 12: 185-192.

    Article  Google Scholar 

  • Marshall WF, Straight A, Marko JF, et al. (1997) Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol 7: 930-939.

    Article  PubMed  CAS  Google Scholar 

  • McLay DW, Clarke HJ (2003) Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125: 625-633.

    Article  PubMed  CAS  Google Scholar 

  • Meyer-Ficca M, Muller-Navia J, Scherthan H (1998) Clustering of pericentromeres initiates in step 9 of spermiogenesis of the rat (Rattus norvegicus) and contributes to a well defined genome architecture in the sperm nucleus. J Cell Sci 111: 1363-1370.

    PubMed  CAS  Google Scholar 

  • Nagele R, Freeman T, McMorrow L, Lee HY (1995) Precise spatial positioning of chromosomes during prometaphase: evidence for chromosomal order. Science 270: 1831-1835.

    PubMed  CAS  Google Scholar 

  • Nagele RG, Freeman T, Fazekas J, Lee KM, Thomson Z, Lee HY (1998) Chromosome spatial order in human cells: evidence for early origin and faithful propagation. Chromosoma 107: 330-338.

    Article  PubMed  CAS  Google Scholar 

  • Nagele RG, Freeman T, McMorrow L, Thomson Z, Kitson-Wind K, Lee H (1999) Chromosomes exhibit preferential positioning in nuclei of quiescent human cells. J Cell Sci 112: 525-535.

    PubMed  CAS  Google Scholar 

  • Oud JL, Mans A, Brakenhoff GJ, van Der Voort HT, van Spronsen EA, Nanninga N (1989) Three-dimensional chromosome arrangement of Crepis capillaris in mitotic prophase and anaphase as studied by confocal scanning laser microscopy. J Cell Sci 92: 329-339.

    PubMed  Google Scholar 

  • Parada L, Misteli T (2002) Chromosome positioning in the interphase nucleus. Trends Cell Biol 12: 425-432.

    Article  PubMed  CAS  Google Scholar 

  • Powell D, Cran DG, Jennings C, Jones R (1990) Spatial organization of repetitive DNA sequences in the bovine sperm nucleus. J Cell Sci 97: 185-191.

    PubMed  CAS  Google Scholar 

  • Saifitdinova AF, Derjusheva SE, Malykh AG, Zhurov VG, Andreeva TF, Gaginskaya ER (2001) Centromeric tandem repeat from the chaffinch genome: isolation and molecular characterization. Genome 44: 96-103.

    Article  PubMed  CAS  Google Scholar 

  • Sbracia M, Baldi M, Cao D, et al. (2002) Preferential location of sex chromosomes, their aneuploidy in human sperm, and their role in determining sex chromosome aneuploidy in embryos after ICSI. Hum Reprod 17: 320-324.

    Article  PubMed  CAS  Google Scholar 

  • Solovei IV, Joffe BI, Hori T, Thomson P, Mizuno S, Macgregor HC (1998) Unordered arrangement of chromosomes in the nuclei of chicken spermatozoa. Chromosoma 107: 184-188.

    Article  PubMed  CAS  Google Scholar 

  • Sun HB, Yokota H (1999) Correlated positioning of homologous chromosomes in daughter fibroblast cells. Chromosome Res 7: 603-610.

    Article  PubMed  CAS  Google Scholar 

  • Sun HB, Shen J, Yokota H (2000) Size-dependent positioning of human chromosomes in interphase nuclei. Biophys J 79: 184-190.

    Article  PubMed  CAS  Google Scholar 

  • Tanabe H, Habermann FA, Solovei I, Cremer M, Cremer T (2002) Non-random radial arrangements of interphase chromosome territories: evolutionary considerations and functional implications. Mutat Res 504: 37-45.

    PubMed  CAS  Google Scholar 

  • Terada Y, Luetjens CM, Sutovsky P, Schatten G (2000) Atypical decondensation of the sperm nucleus, delayed replication of the male genome, and sex chromosome positioning following intracytoplasmic human sperm injection (ICSI) into golden hamster eggs: does ICSI itself introduce chromosomal anomalies? Fertil Steril 74: 454-460.

    Article  PubMed  CAS  Google Scholar 

  • Tilgen N, Guttenbach M, Schmid M (2001) Heterochromatin is not an adequate explanation for close proximity of interphase chromosomes 1-Y, 9-Y, and 16-Y in human spermatozoa. Exp Cell Res 265: 283-287.

    Article  PubMed  CAS  Google Scholar 

  • Ward WS, Zalensky AO (1996) The unique, complex organization of the transcriptionally silent sperm chromatin. Crit Rev Eukaryot Gene Expr 6: 139-147.

    PubMed  CAS  Google Scholar 

  • Watson JM, Meyne J, Graves JA (1996) Ordered tandem arrangement of chromosomes in the sperm heads of monotreme mammals. Proc Natl Acad Sci USA 93: 10200-10205.

    Article  PubMed  CAS  Google Scholar 

  • Wouters-Tyrou D, Martinage A, Chevaillier P, Sautiere P (1998) Nuclear basic proteins in spermiogenesis. Biochimie 80: 117-128.

    Article  PubMed  CAS  Google Scholar 

  • Zalensky AO, Breneman JW, Zalenskaya IA, Brinkley BR, Bradbury EM (1993) Organization of centromeres in the decondensed nuclei of mature human sperm. Chromosoma 102: 509-518.

    Article  PubMed  CAS  Google Scholar 

  • Zalensky AO, Allen MJ, Kobayashi, A, Zalenskaya IA, Bradbury EM (1995) Well-defined genome architecture in the human sperm nucleus. Chromosoma 103: 577-590.

    PubMed  CAS  Google Scholar 

  • Zalensky AO, Tomilin NV, Zalenskaya IA, Teplitz RL, Bradbury EM (1997) Telomere-telomere interactions and candidate telomere binding protein(s) in mammalian sperm cells. Exp Cell Res 232: 29-41.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrei O. Zalensky.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zalenskaya, I.A., Zalensky, A.O. Non-random positioning of chromosomes in human sperm nuclei. Chromosome Res 12, 163–173 (2004). https://doi.org/10.1023/B:CHRO.0000013166.04629.97

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:CHRO.0000013166.04629.97

Navigation