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Decondensation of Sperm Chromatin

In vertebrates, sperm decondensation follows variations on the theme seen in the echinoderms. In the frog Xenopus, the sperm DNA is condensed through its interaction with a protein assembly, composed of one molecule each, of histone H3; histone H4; and sperm-specific proteins X and Y. The oocyte cytoplasm contains histones H2A and H2B complexed with the protein nucleoplasmin. This nucleoplasmin has a greater affinity for the X and Y proteins than it does for histones H2A and H2B, and it trades the histones for the X and Y proteins (Figure 1; Philpott and Leno, 1992). This restores the normal chromatin conformation to the male pronuclear DNA. Soon afterward, new membranous vesicles aggregate along the periphery of the chromatin mass and connect with the fragments of the old envelope that have been carried on the ends of the sperm chromosomes.

Figure 1
Figure 1   Schematic model illustrating the remodeling of sperm chromatin during decondensation. Sperm chromatin is tightly bound through a complex of histones H3, H4, and sperm-specific proteins X and Y. Oocyte nucleoplasmin binds a dimer of histones H2A and H2B and trades them for the X-Y dimer. The resulting chromatin forms the characteristic nucleosome structure containing histones H2A, H2B, H3, and H4, and approximately 200 base pairs of DNA. (After Philpott and Leno, 1992.)

Nucleoplasmin is an example of a newly discovered functional class of molecules called molecular chaperones. Molecular chaperones are proteins that interact transiently and noncovalently with other proteins and influence their folding, assembly, or localization. Other examples are the E. coli protein groEL and its partner groES, which have been shown to facilitate the folding of several other proteinsin the bacterium. Homologs of these E. coli proteins, called "chaperonins," occur in mitochondria and chloroplasts, and they are thought to facilitate the folding and assembly of organellar proteins. In vertebrates, a cytoplasmic homolog called TCP-1, plays a role in spermatogenesis in mice (Laskey et al., 1978; Kubota et al., 1994).

In mammals, the sperm nucleus contains a unique structure, the nuclear annulus. The DNA of the sperm nucleus appears to be anchored to this annulus. The DNA has been compacted by the replacement of the nuclear histones by sperm-specific protamines during spermatogenesis. The compacted DNA forms a toroid shaped "doughnut" of tightly coiled chromatin loops that is held in place by disulfide bonds, formed by the oxidation of sulfhydryl groups present on the protamines (Figure 2; Calvin and Bedford, 1971; Ward and Coffey, 1991; Ward, 1993). This is much tighter than the normal solenoid loops typical of somatic cell nuclei. The decondensation of the DNA utilizes glutathione to reduce the protamine disulfide bonds (Perreault et al., 1984; 1988). As the links are cleaved, the "doughnut" loops unfold and enable egg factors to decondense the chromatin and form the male pronucleus (Zirkin et al., 1989).

Figure 2
Figure 2   Equivalent levels of DNA packaging in somatic cells (left) and sperm cells (right). In somatic cells, DNA is compacted into solenoids with about 6 nucleosomes per turn, and they are attached to the nuclear matrix at intervals of about 60,000 base pairs. Active genes tend to be associated with the nuclear matrix. In the sperm nucleus, protamines bind to the DNA, neutralizing its negative charge, and coiling the complex into tight circles. These circles collapse into a "doughnut shaped structure." Each doughnut represents one DNA loop attached to the nuclear matrix. (From Ward, 1993).

Literature Cited

Calvin, H. I. and Bedford, J. M. 1971. Formation of disulfide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis. J. Reprod. Fertil. [Suppl.] 13: 65o75.

Kubota, H., Hynes, G., Carne, A., Ashworth, A., and Willison, K. (1994). Identification Of Six Tcp-1-Related Genes Encoding Divergent Subunits Of The Tcp-1-Containing Chaperonin. Current Biology 4 : 89-99.

Laskey, R. A., Honda, B. M., Mills, A. D., and Finch, J. T. (1978). Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275 : 416-418.

Perreault, S. D., Wolff, R. A., and Zirkin, B. R. 1984. The role of disulfide bond reduction during mammalian sperm decondensation in vivo. Devel. Biol. 125: 181-186.

Perreault, S. D., Barbee, R. R., and Slott, V. L. 1988. Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Devel. Biol. 125: 181-186.

Philpott, A. and Leno, G. H. 1992. Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell 69: 759-767.

Ward, W. S. 1993. Deoxyribonucleic acid loop domain tertiary structure in mammalian spermatozoa. Biol. Reprod. 48: 1193-1201.

Ward, W. S. and Coffey, D. S. 1991. DNA packaging and organization in the mammalian spermatozoa: comparison with somatic cells. Biol. Reprod. 44: 569-574.

Zirkin, B. R., Perreault, S. D., and Naish, S. J. 1989. Formation and function of the pronucleus during mammalian fertilization. In The Molecular Biology of Fertilization (H. Schatten and G. Schatten, eds.), Academic Press, San Diego. pp. 91-114.


Portions of this review were submitted by Dr. Harry Roy, Professor of Biology, Rensselaer Polytechnic Institute Troy, New York, 12180-3590.

First posted: Mar 26, 2003
Last edit: Mar 26, 2003 by morse

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