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DNA loop domains in mammalian spermatozoa

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Abstract

The highly condensed and tightly packaged DNA of hamster spermatozoa was found to be organized into topologically constrained DNA loop domains attached at their bases to a nuclear matrix. The loop domains of the sperm nuclei differed from somatic cell loop domains from the same animal in two aspects. Sperm loop domains were 60% smaller than somatic cell loop domains, with an average DNA length of 46±7 kb in sperm as compared with 16±11 kb in brain. Secondly, unlike virtually all somatic cell DNA known which is negatively supercoiled, sperm DNA was devoid of detectable supercoiling. The presence of the loop domain structure in the highly condensed DNA of mammalian spermatozoa suggests that this motif is a fundamental aspect of eukaryotic DNA organization.

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References

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

    Google Scholar 

  • Bedford JM, Calvin HI (1974) The occurrence and possible functional significance of -S-S-crosslinks in sperm heads, with particular reference to eutherian mammals. J Exp Zool 188:137–155

    Google Scholar 

  • Bellve AR (1982) Biogenesis of the mammalian spermatozoon. In: Amann RP, Seidel GE (eds) Prospects for sexing mammalian sperm. Colorado Associated University Press, Boulder, pp 69–102

    Google Scholar 

  • Berezney R, Coffey DS (1974) Identification of a nuclear protein matrix. Biochem Biophys Res Commun 60:1410–1417

    Google Scholar 

  • Buongiorno-Nardelli M, Micheli G, Carri MT, Marrilley M (1982) A relationship between replicon size and supercoiled loop domains in the eukaryotic genome. Nature 298:100–102

    Google Scholar 

  • Carri MT, Micheli G, Graziano E, Pace T, Buongiorno-Nardelli M (1986) The relationship between chromosomal origins of replication and the nuclear matrix during the cell cycle. Exp Cell Res 164:426–436

    Google Scholar 

  • Chang TSK, Zirkin BR (1978) Proteolytic degradation of protamine during thiol-induced nuclear decondensation in rabbit spermatozoa. J Exp Zool 204:283–289

    Google Scholar 

  • Cockerill PN, Garrard WT (1986) Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell 44:273–282

    Google Scholar 

  • Coelingh JP, Rozijn TH (1975) Comparative studies on the basic nuclear proteins in mammalian and other spermatozoa. In: Duckett JG, Racey PA (eds) The biology of the male gamete. Academic Press, London, pp 245–256

    Google Scholar 

  • Cook PR, Brazell JA, Jost E (1976) Characterization of nuclear structures containing superhelical DNA. J Cell Sci 22:303–324

    Google Scholar 

  • Dooher GB, Bennett D (1973) Fine structural observations on the development of the sperm head in the mouse. Am J Anat 136:339–362

    Google Scholar 

  • Earnshaw WC, Laemmli UK (1983) Architecture of metaphase chromosomes and chromosome scaffolds. J Cell Biol 96:84–93

    Google Scholar 

  • Finch JT, Klug A (1976) Solenoid model for superstructure in chromatin. Proc Natl Acad Sci USA 73:1897–1901

    Google Scholar 

  • Flickinger RA, Givens R, Pine S, Sepanik P (1986) Factors controlling the size of DNA loops in frog embryos and Friend erythroleukemia cells. Cell Differ 19:59–71

    Google Scholar 

  • Gatewood JM, Cook GR, Balhorn R, Bradbury EM, Schmid CW (1987) Sequence-specific packaging of DNA in human sperm chromatin. Science 236:962–964

    Google Scholar 

  • Hyodo M, Flickinger RA (1973) Replicon growth rates during DNA replication in developing frog embryos. Biochim Biophys Acta 299:29–33

    Google Scholar 

  • Kierszenbaum AL, Tres LL (1978) The packaging unit: a basic structural feature for the condensation for late cricket spermatid nuclei. J Cell Sci 33:265–283

    Google Scholar 

  • Liu LF (1983) DNA topoisomerases — enzymes that catalyze the breaking and rejoining of DNA. CRC Crit Rev Biochem 15:1–24

    Google Scholar 

  • Liu LF, Wang JC (1975) On the degree of unwinding of the DNA helix by ethidium II. Studies by electron microscopy. Biochim Biophys Acta 395:405–412

    Google Scholar 

  • Livolant F (1984) Cholesteric organization of DNA in the stallion sperm head. Tissue Cell 16:535–555

    Google Scholar 

  • Loir M, Lanneau M (1984) Structural function of the basic nuclear proteins in ram spermatids. J Ultrastruct Res 86:262–276

    Google Scholar 

  • Longo FJ, Krohne F, Franke WW (1987) Basic protein of the perinuclear theca of mammalian spermatozoa and spermatids: a novel class of cytoskeletal elements. J Cell Biol 105:1105–1120

    Google Scholar 

  • McGhee JD, Felsenfeld F (1980) Nucleosome structure. Annu Rev Biochem 49:1115–11156

    Google Scholar 

  • Nelson WG, Pienta KJ, Barrack ER, Coffey DS (1986) The role of the nuclear matrix in the organization and function of DNA. Annu Rev Biophys Chem 15:457–475

    Google Scholar 

  • O'Brien DA, Bellve AR (1980) Protein constituents of the mouse spermatozoon I. An electrophoretic characterization. Dev Biol 75:386–404

    Google Scholar 

  • O'Brien DA, Bellve AR (1983) The mammalian spermatozoon: structure and temporal assembly. In: Hartmann JF (ed) Mechanism and control of animal fertilization. Academic Press, New York, pp 55–137

    Google Scholar 

  • Pienta KJ, Coffey DS (1984) A structural analysis of the role of the nuclear matrix and DNA loops in the organization of the nucleus and chromosome. J Cell Sci Suppl 1: 123–135

    Google Scholar 

  • Pogany GC, Corzett M, Weston S, Balhorn R (1981) DNA and protein content of mouse sperm: implication regarding sperm chromatin structure. Exp Cell Res 136:127–136

    Google Scholar 

  • Risley MS, Einheber S, Bumcrot DA (1986) Changes in DNA topology during spermatogenesis. Chromosoma 94:217–227

    Google Scholar 

  • Robinson SI, Nelkin BD, Vogelstein B (1982) The ovalbumin gene is associated with the nuclear matrix of chicken oviduct cells. Cell 28:99–106

    Google Scholar 

  • Rodman TC, Pruslin FH (1985) Proteins of demembraned mouse sperm heads. J Biol Chem 260:5654–5659

    Google Scholar 

  • Sipski ML, Wagner TE (1977) The total structure and organization of chromosomal fibers in eutherian sperm nuclei. Biol Reprod Fertil 16:428–440

    Google Scholar 

  • Tsanev R, Avramova Z (1981) Nonprotamine nucleoprotein ultrastructures in mature ram sperm nuclei. Eur J Cell Biol 24:139–145

    Google Scholar 

  • Van der Velden HMW, van Willigen G, Wetzels RHW, Wanka F (1984) Attachment of origins of replication to the nuclear matrix and the chromosomal scaffold. FEBS Lett 171:13–16

    Google Scholar 

  • Vogelstein B, Pardoll DM, Coffey DS (1980) Supercoiled loops and eucaryotic DNA replication. Cell 22:79–85

    Google Scholar 

  • Warren AC, Cook PR (1978) Supercoiling of DNA and nuclear conformation during the cell-cycle. J Cell Sci 30:211–226

    Google Scholar 

  • Watson JD, Crick FHC (1953) Molecular structure of nucleic acids. Nature 171:737–738

    Google Scholar 

  • Wyrobek AJ, Meistrich ML, Furrer R, Bruce WR (1976) Physical characteristics of mouse sperm nuclei. Biophys J 16:811–825

    Google Scholar 

  • Zirkin BR, Soucek DA, Chang TSK (1982) Sperm nuclear packing and regulation during spermatogenesis and fertilization. Johns Hopkins Med J 151:101–112

    Google Scholar 

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Ward, W.S., Partin, A.W. & Coffey, D.S. DNA loop domains in mammalian spermatozoa. Chromosoma 98, 153–159 (1989). https://doi.org/10.1007/BF00329678

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  • DOI: https://doi.org/10.1007/BF00329678

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