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.
Similar content being viewed by others
References
Balhorn R (1982) A model for the structure of chromatin in mammalian sperm. J Cell Biol 93:298–305
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
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
Berezney R, Coffey DS (1974) Identification of a nuclear protein matrix. Biochem Biophys Res Commun 60:1410–1417
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
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
Chang TSK, Zirkin BR (1978) Proteolytic degradation of protamine during thiol-induced nuclear decondensation in rabbit spermatozoa. J Exp Zool 204:283–289
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
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
Cook PR, Brazell JA, Jost E (1976) Characterization of nuclear structures containing superhelical DNA. J Cell Sci 22:303–324
Dooher GB, Bennett D (1973) Fine structural observations on the development of the sperm head in the mouse. Am J Anat 136:339–362
Earnshaw WC, Laemmli UK (1983) Architecture of metaphase chromosomes and chromosome scaffolds. J Cell Biol 96:84–93
Finch JT, Klug A (1976) Solenoid model for superstructure in chromatin. Proc Natl Acad Sci USA 73:1897–1901
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
Gatewood JM, Cook GR, Balhorn R, Bradbury EM, Schmid CW (1987) Sequence-specific packaging of DNA in human sperm chromatin. Science 236:962–964
Hyodo M, Flickinger RA (1973) Replicon growth rates during DNA replication in developing frog embryos. Biochim Biophys Acta 299:29–33
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
Liu LF (1983) DNA topoisomerases — enzymes that catalyze the breaking and rejoining of DNA. CRC Crit Rev Biochem 15:1–24
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
Livolant F (1984) Cholesteric organization of DNA in the stallion sperm head. Tissue Cell 16:535–555
Loir M, Lanneau M (1984) Structural function of the basic nuclear proteins in ram spermatids. J Ultrastruct Res 86:262–276
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
McGhee JD, Felsenfeld F (1980) Nucleosome structure. Annu Rev Biochem 49:1115–11156
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
O'Brien DA, Bellve AR (1980) Protein constituents of the mouse spermatozoon I. An electrophoretic characterization. Dev Biol 75:386–404
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
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
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
Risley MS, Einheber S, Bumcrot DA (1986) Changes in DNA topology during spermatogenesis. Chromosoma 94:217–227
Robinson SI, Nelkin BD, Vogelstein B (1982) The ovalbumin gene is associated with the nuclear matrix of chicken oviduct cells. Cell 28:99–106
Rodman TC, Pruslin FH (1985) Proteins of demembraned mouse sperm heads. J Biol Chem 260:5654–5659
Sipski ML, Wagner TE (1977) The total structure and organization of chromosomal fibers in eutherian sperm nuclei. Biol Reprod Fertil 16:428–440
Tsanev R, Avramova Z (1981) Nonprotamine nucleoprotein ultrastructures in mature ram sperm nuclei. Eur J Cell Biol 24:139–145
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
Vogelstein B, Pardoll DM, Coffey DS (1980) Supercoiled loops and eucaryotic DNA replication. Cell 22:79–85
Warren AC, Cook PR (1978) Supercoiling of DNA and nuclear conformation during the cell-cycle. J Cell Sci 30:211–226
Watson JD, Crick FHC (1953) Molecular structure of nucleic acids. Nature 171:737–738
Wyrobek AJ, Meistrich ML, Furrer R, Bruce WR (1976) Physical characteristics of mouse sperm nuclei. Biophys J 16:811–825
Zirkin BR, Soucek DA, Chang TSK (1982) Sperm nuclear packing and regulation during spermatogenesis and fertilization. Johns Hopkins Med J 151:101–112
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00329678