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Sperm nuclear envelope: breakdown of intrinsic envelope and de novo formation in hamster oocytes or eggs

Published online by Cambridge University Press:  26 September 2008

Noriko Usui ,
Atsuo Ogura ,
Yasuyuki Kimura  and
Ryuzo Yanagimachi
Noriko Usui*
Affiliation:
Department of Anatomy, Teikyo University School of Medicine, TokyoJapan.
Atsuo Ogura
Affiliation:
Department of Anatomy and Reprodutive Biology, University of Hawaii School of Medicine, Honolulu Hawaii, USA.
Yasuyuki Kimura
Affiliation:
Department of Anatomy and Reprodutive Biology, University of Hawaii School of Medicine, Honolulu Hawaii, USA.
Ryuzo Yanagimachi
Affiliation:
Department of Anatomy and Reprodutive Biology, University of Hawaii School of Medicine, Honolulu Hawaii, USA.
*
Dr Noriko Usui, Department of Antomy, Teikyo University School of Medicine, 2-11-1, Kaga, Itabashi-ku, Tokyo 173, Japan. Tel: +81-03-3964-1211 ext.2107. Fax: +81-03-3964-8415.
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Summary

During fertilisation of a fully mature oocyte, the sperm intrinsic nuclear envelope (SINE) disappears soon after sperm-oocyte fusion. A new nuclear envelope appears around the decondensed sperm chromatin when the oocyte reaches telophase II. Whether the SINE persists or rapidly disappears after sperm entery into immature oocytes or fertilised eggs has been controversial. Nuclear envelopes have been demonstrated around the sperm chromatin, which cannot be decondensed within the ooplasm of these oocytes or eggs, but whether these envelopes are persisting SINEs or newly formed envelopes has been apoint of dispute. To resolve this issue, the fate of the germinal vesicle stage(GV oocytes) or fertilised eggs at the pronuclear stage(PN eggs). The SINEs disappeared quikly within these oocytes or eggs, like those within maturing or mature oocytes, suggesting that the envelops around the sperm chromatin must be newly formed after SINE breakdown. To obtain further evidence, a detergent-treated, SINE-free sperm nucleus was injected into a PN egg. A new envelope appeared around the still-condensed or partially decondensed sperm chromatin within 3h after injection. Thus, disassembly of the SINE within ooplasm, unlike that of nuclear envelopes of other cells at prophase, is independent of the cell cycle stage of the oocyte or egg, whereas the ability of the ooplasm to assemble the new envelope is restricted to certain periods of the cycle. i.e. early prophase and telophase during meiosis and interphase, periods when active M-phase Promoting factor (MPF) is absent from the ooplasm.

Keywords

Cell cycleHamsterMPFNuclearenvelopeOoplasm
Type
Article
Information
Zygote , Volume 5 , Issue 1 , February 1997 , pp. 35 - 46
Copyright
Copyright © Cambridge University Press 1997

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References

Barros, C. (1987). Sperm chromatin decondensation after fertilization. Microsc. Electr. Biol. Cell. 11, 15–25.Google ScholarPubMed
Barros, C.. Franklin, L.E. (1968). Behavior of the gamete membranes during sperm entry into the mammalian egg. J. Cell Biol. 37, c13–c18.CrossRefGoogle ScholarPubMed
Barros, C. & Rhim, A. (1980). Unpacking of the spermatozoal nucleus at fertilization. Arch. Biol. Med. Exp. 13, 325–34.Google Scholar
Bedford, J.M. (1972). An electron microscopic study of sperm penetration into the rabbit egg after natural mating. AM. J. Anat. 133, 213–54.CrossRefGoogle ScholarPubMed
Berrios, M.. & Bedford, J.M. (1979). Oocyte maturation: aberrant postfusion responses of the rabbit primary oocyte to penetrating spermatoza. J. Cell Sci. 39, 1–12.CrossRefGoogle Scholar
Chatot, C.L., Ziomeck, C.A.. Bavister, B.D., Lewis, J.L. & Torres, I. (1989). An improved culture madium supports development of random-bred 1-cell embryos in vitro. J. Reprot. Fertil. 86, 679–88.CrossRefGoogle ScholarPubMed
Clarke, H.J. (1992). Nuclear and chromatin composition of mammalian gametes and early embryos. Biochem. Cell Biol. 70, 856–66.CrossRefGoogle ScholarPubMed
Crozet, N. (1988). Fine structure of sheep fertilization in vitro. Gamet Res. 19, 291–303.CrossRefGoogle ScholarPubMed
Fawcett, D.W.(1977). The structure of the spermatozoon. In Frontiers in Reprodution and Fertility Control, ed. Koblinsky, G., pp. 353–78. Cambrige MA: MIT Press.Google Scholar
Franke, W.W.(1970). On the university of nuclear pore complex structure. Z. Zellforsch. Mikrosk. Anat. 105, 405–29.CrossRefGoogle Scholar
Franke, W.W., Scheer, U., Krohne, G.. & Jarasch, E.-D. (1981). The nuclear envelope and the architecture of the nuclear periphery J. Cell Biol. 91, 39s–50s.CrossRefGoogle ScholarPubMed
Fulka, J. Jr, Jung, T. & Moor, R.M. (1992). The fall of biological maturation promoting factor (MPF) and histone H1 kinase activity during anaphase and telophase in mouse oocytes. Mol. Reprod. Dev. 32, 378–82.CrossRefGoogle ScholarPubMed
Guraya, S.S.. & Sidhu, K.S. 1975. Histochemical localization of hydrolytic enzymes in the buffalo spermatozoa. Acta Histochem. 54, 307–12Google ScholarPubMed
Hashimoto, N. & Kishimoto, T. (1988). Regulation of meiotic metaphase by a cytoplsamic maturation-promoting factor during mouse oocyte maturation. Dev. biol. 126, 242–52.CrossRefGoogle Scholar
Jedlicki, A., Barros, C., Salgado, A.M. & Herrera, E. (1986). Effects of in vivo oocyte aging on sperm chromatin decondensation in the golden hamster. Gamete Res. 14, 347–54.CrossRefGoogle Scholar
Kann, M.-L., Feinberg, J.. Rainteau, D., Dadoune, J.-P., Weinman, S. & Fouquet, J.-P. (1991). Localization of calmodulin in perinuclear strutures of spermatids and spermatozoa: a comparison of six mammalin species. Anat. Rec. 230,481–8.CrossRefGoogle Scholar
Kimura, Y. & Yanagimachi, R. (1995). Intracytoplasmic sperm injection in the mouse Biol. Reprod. 25, 709–20.CrossRefGoogle Scholar
Kishimoto, T. (1988). Regulation of metaphase by meturation-promoting factor. Dev. Growth Differ. 30, 105–15.CrossRefGoogle ScholarPubMed
Kishimto, T. & Kanatani, H. (1976). Cytoplasmic factor responsible for germinal vesicle breakdown and meiotic maturation in starfish oocytes. Nature 260, 321–2.CrossRefGoogle Scholar
Lohka, M.J. (1989). Mitotic control by metaphase-Promothing factor and cdc proteins. J. Cell Sci. 92, 131–5.CrossRefGoogle ScholarPubMed
Longo, F.J..,Krohne, G. & Franke, W.W. (1987). Basic proteins of the perinuclear theca of mammalian spermatozoa and spermatides: a novel class of cytoskeletal elements J. Cell Biol. 105,1105–20.CrossRefGoogle ScholarPubMed
Maleszewski, M. (1992). Behavior of sperm nuclei incorporated into parthenogenetic mouse eggs prir to the first cleavage division Mol. Reprod. Dev 33,215–21.CrossRefGoogle Scholar
Maleszewski, M. (1995). Sperm nuclei entering parthenogenetically activated mouse oocytes before the first mitosis transform into pronuclei: an ultrastructural study Anat. Rec 243,516–18.CrossRefGoogle ScholarPubMed
Masuri, Y. (1992). Towards understanding the control of the division cycle in animal cells. Biochem. Cell Biol. 70, 920–45.CrossRefGoogle Scholar
Masui, Y. & Clarke, H.J. (1979). Oocyte maturation Int. Rev. Cytol 57, 185–282.CrossRefGoogle ScholarPubMed
Newport, J. (1987). Nuclear reconstitution in vitro: stages of assembly around protein-free Dna. Cell 48,205–17.CrossRefGoogle ScholarPubMed
Nurse, P. (1990). Universal control mechism regulating on set of M-phase. Nature 344, 503–8.CrossRefGoogle Scholar
Oko, R. & Morales, C.R. (1994). A novel testicular protein, with sequence similarities to a family of lipid binding proteins, is a mojor component of the rat sperm perinuclear theca Dev. Biol 166, 235–54.CrossRefGoogle Scholar
Oison, G.E..& Winfrey, V.P. (1988). Characterization of postacrosomal sheath of bovine spermatozoa Gamet Res 20,329–42.Google Scholar
ookata, K., Hisanaga, S., Okano, T., Tachibana, K. & Kishimoto, T. (1992). Relocation and distinct subcellular localization of p34cdc2.cyclin B complex at meiosis reintiation in starfish oocytes. EMBO J. 11, 1763–72.CrossRefGoogle Scholar
Ōura, C.. & Toshimori, K. 1990. Ultrastructural studies on the fertilization of mammalian gametes. Int. Rev. Cytol. 122, 105–51.CrossRefGoogle ScholarPubMed
Perreault, S.D., Wolff, R.A. & Zirkin, B.R. 1984. The role of disulfide bond redution during mammalian sperm nuclear decondensation in vitro. Dev. Biol. 101, 160–7.CrossRefGoogle Scholar
Peter, M., Nakagawa, J., Dorée, M., Labbé, J.C. & Nigg, E.A. 1990. In vitro disassembly of the nuclear lamina and M Phase-specific phospharylation of lamins by cdc2 kinase. Cell. 61,591–602.CrossRefGoogle Scholar
Ponce, R.H., Yanagimachi, R.Urch, U.A., Yamagata, T. & Ito, M. 1993. Retention of hamster oolemma fusibility with spermatozoa after various enzyme treaments: a search for the molecules involved in sperm-egg fusion. Zygote. 1, 163–71.CrossRefGoogle Scholar
Sato, A.. & Yanagimachi, R. 1972. Transplantation of preimplantation hamster embryos. J. Reprod. Fertil. 30, 329–32.CrossRefGoogle ScholarPubMed
Schatten, G., Maul, G.G., Schatten, H.Chaly, N., Simerly, C., Balczon, R. & Brown, D.L. 1985. Nuclear lamins and peripheral nuclear antigens during fertilization and embryogenesis in mice and sea urchins. Proc. Natl. Acad. Sci. USA, 82 4727–31.CrossRefGoogle ScholarPubMed
Szöllösi, D., Szöllösi, M.S., Czolowska, R.. & Tarkowski, A.K. 1990. Sperm penetration into immature mouse oocytes and nuclear changes during maturation: an EM study. Biol. Cell. 69, 53–64.CrossRefGoogle ScholarPubMed
Szöllösi, M.S., Borsuk, E. & Szöllösi, D. 1994. Relationship between sperm nucleus remodelling and cell cycle prograssion of fragment of mouse parthenogenotes. Mol. Reprod. Dev. 37, 146–56.CrossRefGoogle Scholar
Teichman, R.J. & Bernstein, M.H. 1971. Fine structure localizations of acid phosphatase in rabbit and bull sperm heads. J. Reprod. Fertil. 27, 243–8.CrossRefGoogle ScholarPubMed
Tuomikoski, T., Felix, M.-A., Dorée, M. & Gruenberg, J. 1989. Inhibition of endocytic vesicle fusion in vitro by the cell-cycle control protein kinase cdc2. Nature. 342, 942–5.CrossRefGoogle ScholarPubMed
Usui, N. 1976. Eletron microscopic studies of hamster sperm nuclei incorporated into maturing oocytes (in Japanese). J. Tokyo Women's med. Call. 46, 467–80.Google Scholar
Usui, N. 1996. Morphological differences in nuclear materials released from hamster sperm heads at an early stage of incorporation into immature oocytes or fertilized eggs. Mol. Reprod. Dev. 44, 132–40.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Usui, N.. & Yanagimachi, R. 1976. Behavior of hamster sperm nuclei incorporated into and early development. J. Ultra struct. Res. 57, 276–88.CrossRefGoogle ScholarPubMed
Ward, G.E. & Kirschner, M.W. 1990. Identification of cell cycle-regulated phosphorylation sites on nuclear lamin c. Cell. 61, 561–77.CrossRefGoogle ScholarPubMed
Watanabe, N., Hunt, T.Ikawa, Y. & Sagata, N. 1991. Independent inctivetion of MPF and cytostatic factor (MOS) upon fertilization of Xenopus eggs. Nature 352, 247–8CrossRefGoogle ScholarPubMed
Yanagimachi, R. 1981. Mechanism of fertilization in mammals. In Fertilization and Embryomic Development in Vitro. Mastroianni, L. & Biggers, J.D.81–182. New YOrk: Plenum Press.CrossRefGoogle Scholar
Yanagimachio, R. 1988. Sperm-egg fusion. in Current Topics in Membranes and Transport, ed Duzgunes, N. & F., Bronner 32. PP 3–43San Diego. Acamamic Press.Google Scholar
Yanagimachi, R. 1994. Mammalian fertilization. In The Physiology of Reproduction 2nd edn, Knobil, E & Neill, J.D. pp 178–317. New York: Raven PressGoogle Scholar
Yanagimachio, R. & Noda, Y.D. 1970.Electron microscope studies of sperm incorporation into the golden hamster egg.Am. J. Anat. 128, 429–63.CrossRefGoogle Scholar