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Well-defined genome architecture in the human sperm nucleus

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Abstract

Using fluorescence in situ hybridization, conventional epifluorescence microscopy, and laser scanning confocal microscopy followed by three-dimensional reconstruction we describe a well-defined higher order packaging of the human genome in the sperm cell nucleus. This was determined by the spatial localization of centromere and telomere regions of all chromosomes and supported by localization of subtelomere sequences of chromosome 3 and the entire chromosome 2. The nuclear architecture in the human sperm is characterized by the clustering of the 23 centromeres into a compact chromocenter positioned well inside the nucleus. The ends of the chromosomes are exposed to the nuclear periphery where both the subtelomere and the telomere sequences of the chromosome arms are joined into dimers. Thus chromosomes in the human sperm nucleus are looped into a hairpin-like configuration. The biological implications of this nuclear architecture in spermatogenesis and male pronuclear formation following fertilization are discussed.

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References

  • AgardDA, SedatJW (1983) Three-dimensional architecture of a polytene nucleus. Nature 302:676–681

    Google Scholar 

  • AllenMJ, LeeC, LeeIVJD, PoganyGC, BaloochM, SieckhausWJ, BalhornR (1993) Atomic force microscopy of mammalian sperm chromatin. Chromosoma 102:623–630

    Google Scholar 

  • BalhornR (1989) Mammalian protamines: Structure and molecular interactions. In: AdolfKW (ed) Molecular biology of chromosome function. Springer-Verlag, New York, pp 366–395

    Google Scholar 

  • BilliaF, DeBoniH (1991) Localization of centromere satellite and telomeric DNA sequences in dorsal root ganglion neurons in vitro. J Cell Sci 100:219–226

    Google Scholar 

  • BoveriKT (1888) Die Befructung und Teilung des Eles von Ascaris megalocephalia. Zellen studies. Fisher, Jene

    Google Scholar 

  • BrinkleyBR, BrennerSL, HallJM, ToussonA, BalczonRD, ValdiviaMM (1986) Arrangements of kinetochores in mouse cells during meiosis and spermatogenesis. Chromosoma 94:309–317

    Google Scholar 

  • ChikashigeY, DingD-Q, FunabikiH, HaraguchiT, MashikoS, YanagidaM, HiraokaY (1994) Telomere-led premeiotic chromosome movement in fission yeast. Science 264:270–273

    Google Scholar 

  • ComingsDE (1980) Arrangement of the chromatin in the nucleus. Hum Genet 60:46–56

    Google Scholar 

  • CoonenE, PietersMHEC, DumoulinJCM, MeyerH, EversJLH, RamaekersFCS, GeraedtsJPM (1991) Nonisotopic in situ hybridization as a method for nondisjunction studies in human spermatozoa. Mol Reprod Dev 28:18–22

    Google Scholar 

  • CourtensJ-L, BiggiogeraM, RothfieldNF, BurnierM, FakanS (1992) Migration of centromere proteins in rabbit spermatids. Mol Reprod Dev 32:369–377

    Google Scholar 

  • deLangeT (1992) Human telomeres are attached to the nuclear matrix. EMBO J 11:717–724

    Google Scholar 

  • EmmerichP, LoosP, JanchA, HopmanAHN, WiegantJ, HigginsMJ, WhiteBN, PloegM, CremerC, CremerT (1989) Double in situ hybridization in combination with digital image analysis: A new approach to study interphase chromosome topography. Exp Cell Res 181:126–140

    Google Scholar 

  • FawcettDW, AndersonWA, PhillipsDM (1971) Morphogenetic factors influencing the shape of the sperm head. Dev Biol 26:220–251

    Google Scholar 

  • GarrardWT (1990) Chromosomal loop organization in eukaryotic genomes. In: EcksteinF, LilleyDM (eds) Nucleic acids molecular biology. Springer-Verlag, Heidelberg, Berlin, pp 163–175

    Google Scholar 

  • GusseM, SautierreP, BelaicheD, MartinageA, RouxC, DadouneJ-P, ChevaillierP (1986) Purification and characterization of nuclear basic proteins of human sperm. Biochim Biophys Acta 884:124–134

    Google Scholar 

  • GuttenbachM, SchmidM (1991) Non-isotopic detection of chromosome 1 in human meiosis and demonstration of disomic sperm nuclei. Hum Genet 87:261–265

    Google Scholar 

  • HaafT, GrunenbergH, SchmidM (1990) Paired arrangements of nonhomologous centromeres during vertebrate spermatogenesis. Exp Cell Res 187:157–161

    Google Scholar 

  • HadlaczkyGY, WentM, RingertzNR (1986) Direct evidence for the non-random localization of mammalian chromosomes in the interphase nucleus. Exp Cell Res 167:1–15

    Google Scholar 

  • HanTL, WebbGC, FlahertySP, CorrellA, MatthewsCD, FordJH (1992) Detection of chromosome 17- and X-bearing human spermatozoa using fluorescence in situ hybridization. Mol Reprod Dev 33:189–194

    Google Scholar 

  • HillikerAJ, AppelsR (1989) The arrangement of interphase chromosomes: Structural and functional aspects. Exp Cell Res 185:297–318

    Google Scholar 

  • HiraokaY, AgardDA, SedatJW (1990) Temporal and spatial coordination of chromosome movement, spindle formation and nuclear envelope breakdown during prometaphase in Drosophila melanogaster embryos. J Cell Biol 111:2815–2828

    Google Scholar 

  • HolmesJM, MartinRH (1993) Aneuploidy detection in human sperm nuclei using chromosome specific probes in in situ hybridization. Hum Genet 91:20–24

    Google Scholar 

  • HudNV, AllenMJ, DowningKH, LeeJ, BalhornR (1993) Identification of the elemental packing unit of DNA in mammalian sperm cells by atomic force microscopy. Biophys Biochem Res Commun 193:1347–1354

    Google Scholar 

  • KaplanFS, MurrayJ, SilvesterJE, GonzalezIL, O'ConnorJP, DoeringJL, MuenkeM, EmanuelBS, ZasloffMA (1993) The topographic organization of repetitive DNA in the human nucleolus. Genomics 15:123–132

    Google Scholar 

  • LaemmliUK, KasE, PoljakL, AdachiY (1992) Scaffold-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr Op Genet Dev 2:275–285

    Google Scholar 

  • LichterP, CremerT, BordenJ, ManuelidisL, WardDC (1988) Delineation of individual human chromosomes in metaphase and interphase cells by in situ hybridization using recombinant DNA libraries. Hum Genet 80:304–312

    Google Scholar 

  • LichterP, BoyleAL, CremerT, WardDC (1991) Analysis of genes and chromosomes by nonisotopic in situ hybridization. GATA 8:24–55

    Google Scholar 

  • MajlofL, ForsgrenP-O (1993) Confocal microscopy: Important considerations for accurate imaging. Methods Cell Biol 38:79–97

    Google Scholar 

  • ManuelidisL (1984) Different central nervous system cell types display distinct and non-random arrangements of satellite DNA sequences. Proc Natl Acad Sci USA 81:3121–3127

    Google Scholar 

  • ManuelidisL (1990) A view of interphase chromosomes. Science 250:1533–1540

    Google Scholar 

  • ManuelidisL, BordenJ (1988) Reproducible compartmentalization of individual chromosome domains in human CNS cells revealed by in situ hybridization and three-dimensional reconstruction. Chromosoma 96:397–410

    Google Scholar 

  • MathogD, HochotrasserM, GruenbaumY, SaumweberH, SedatJ (1984) Characteristic folding pattern of polytene chromosomes in Drosophila salivary gland nuclei. Nature 308:414–421

    Google Scholar 

  • McNeilJA, JohnsonCV, CarterKC, SingerRH, LawrenceJB (1991) Localization DNA and RNA within nuclei and chromosomes by fluorescence in situ hybridization. GATA 8:41–58

    Google Scholar 

  • MoensPB, PearlmanRE (1989) Satellite DNA I in chromatin loops of rat pachytene chromosomes and in spermatids. Chromosoma 98:287–294

    Google Scholar 

  • NelsonWG, PientaKJ, BarrackER, CoffeyDS (1986) The role of nuclear matrix in the organization and function of DNA. Annu Rev Biophys Chem 15:457–475

    Google Scholar 

  • PocciaD (1989) Reactivation and remodeling of the sperm nucleus following fertilization. In: SchattenH, SchattenG (eds) The molecular biology of fertilization, Academic Press, San Diego, pp 115–136

    Google Scholar 

  • PowellD, CranDC, JenningsC, JonesR (1990) Spatial organization of repetitive DNA sequences in the bovine sperm nucleus. J Cell Sci 97:185–191

    Google Scholar 

  • RablC (1885) Morphologisches Jahrbuch, Berlin

    Google Scholar 

  • RawlingsDJ, ShawPJ (1990) Localization of ribosomal and telomeric DNA sequences in intact plant nuclei by in situ hybridization and three dimensional reconstruction. J Microsc 157:83–89

    Google Scholar 

  • SteinmullerJ, SchleiermacherE, ScherthanH (1993) Direct detection of repetitive, whole chromosome and telomere DNA probes by immunogold electron microscopy. Chromosome Res 1:45–51

    Google Scholar 

  • VillepoteauB (1992) Heparin increases chromatin accessibility by binding to the trypsin sensitive basic residues in histones. Biochem J 288:953–958

    Google Scholar 

  • Vourc'hC, TaruscioD, BoyleAL, WardDC (1993) Cell cycle dependent distribution of telomeres, centromeres and chromosome-specific subsatellite domain in the interphase nucleus of mouse lymphocytes. Exp Cell Res 205:142–151

    Google Scholar 

  • WalkerCL, CargileCB, FloyKM, DelannoyM, MigeonBR (1991) The Barr body is a looped X chromosome formed by telomere association. Proc Natl Acad Sci USA 88:6191–6195

    Google Scholar 

  • WardWS (1993) Deoxyribonucleic acid loop domain tertiary structure in mammalian spermatozoa. Biol Reprod 48:1193–1201

    Google Scholar 

  • WeierH-U, ZitzelsbergHF GrayJW (1991) Non-isotopic labeling of murine heterochromatin in situ by hybridization with in vitro-synthesized biotinylated gamma (major) satellite DNA. BioTechniques 10:498–505

    Google Scholar 

  • WilliamsBJ, BallingerCA, MalterHE, BishopF, TuckerM, ZwingmanTA, HassoldTJ (1993) Non-disjunction in human sperm: results of fluorescence in situ hybridization studies using two and three probes. Hum Mol Genet 11:1929–1936

    Google Scholar 

  • WyrobeckAJ, AlhbornT, BalhornR, StankerL, PinkelD (1990) Fluorescent in situ hybridization to Y chromosomes in decondensed human sperm nuclei. Mol Reprod Dev 27:200–208

    Google Scholar 

  • ZakianVA (1989) Structure and function of telomeres. Annu Rev Genet 23:579–604

    Google Scholar 

  • ZalenskyAO, BrenemanJW, ZalenskayaIA, BrinkleyBR, BradburyEM (1993) Organization of centromeres in the decondensed nuclei of mature human sperm. Chromosoma 102:509–518

    Google Scholar 

  • ZirkinBR, PerreaultSD, NaishSJ (1989) Formation and function of the male pronucleus during mammalian fertilization. In: SchattenH, SchattenG (eds) The molecular biology of fertilization. Academic Press, San Diego, pp 91–114

    Google Scholar 

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Authors and Affiliations

  1. Department of Biological Chemistry, University of California at Davis, 95616, Davis, CA, USA

    A. O. Zalensky, M. J. Allen, I. A. Zalenskaya & E. M. Bradbury

  2. Biology and Biotechnology Research Program, Lawrence Livermore National Laboratory, 94550, Livermore, CA, USA

    M. J. Allen, A. Kobayashi & R. Balhorn

  3. Los Alamos National Laboratory, 87545, Los Alamos, NM, USA

    E. M. Bradbury

Authors
  1. A. O. Zalensky
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  2. M. J. Allen
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  3. A. Kobayashi
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  4. I. A. Zalenskaya
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  5. R. Balhorn
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  6. E. M. Bradbury
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Zalensky, A.O., Allen, M.J., Kobayashi, A. et al. Well-defined genome architecture in the human sperm nucleus. Chromosoma 103, 577–590 (1995). https://doi.org/10.1007/BF00357684

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  • DOI: https://doi.org/10.1007/BF00357684

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