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Decrease in CD9 content and reorganization of microvilli may contribute to the oolemma block to sperm penetration during fertilization of mouse oocyte

Published online by Cambridge University Press:  26 November 2009

Eliza Żyłkiewicz ,
Julita Nowakowska  and
Marek Maleszewski
Eliza Żyłkiewicz
Affiliation:
Department of Embryology, Institute of Zoology, Faculty of Biology, University of Warsaw, Poland.
Julita Nowakowska
Affiliation:
Laboratory of Electron and Confocal Microscopy, Faculty of Biology, University of Warsaw, Poland.
Marek Maleszewski*
Affiliation:
Department of Embryology, Institute of Zoology, University of Warsaw, Miecznikowa 1, 02–096 Warszawa, Poland. Department of Embryology, Institute of Zoology, Faculty of Biology, University of Warsaw, Poland.
*
All correspondence to: Department of Embryology, Institute of Zoology, University of Warsaw, Miecznikowa 1, 02–096 Warszawa, Poland. Fax: +48 22 55 41 210. e-mail: [email protected]
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Summary

Tetraspanin CD9 is the only protein of the oocyte membrane (oolemma) known to be required for the fusion of gametes during fertilization in the mouse. Using electron microscopy and immunostaining we examined the differences in localization of CD9 between ovulated oocytes, zygotes and parthenogenetically activated eggs (parthenogenotes). Changes in ultrastructure of oolemma, which take place in oocytes after fertilization or artificial activation, were also assessed. We demonstrated that after fertilization the level of CD9 present on microvilli of zygote was two times lower than its level on the oolemma of the oocyte. In addition, we showed that the distribution of microvilli is less uniform in the zygotes than in the unfertilized oocytes. We propose that the changes of microvilli distribution and their CD9 content are responsible for the development of the oocyte membrane block to sperm penetration.

Keywords

Block to polyspermyElectron microscopyFertilizationGamete fusion
Type
Research Article
Information
Zygote , Volume 18 , Issue 3 , August 2010 , pp. 195 - 201
Copyright
Copyright © Cambridge University Press 2009

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References

Borsuk, E. & Tarkowski, A.K. (1989). Transformation of sperm nuclei into male pronuclei in nucleate and anucleate fragments of parthenogenetic mouse eggs. Gamete Res. 24, 471–481.CrossRefGoogle ScholarPubMed
Bronson, R. (1998). Is the oocyte a non-professional phagocyte? Hum. Reprod. Update 4, 763–775.CrossRefGoogle ScholarPubMed
Byrd, W. & Belisle, B.W. (1985). Microvillar elongation following parthenogenetic activation of sea urchin eggs. Exp. Cell Res. 159, 211–223.CrossRefGoogle ScholarPubMed
Chen, M.S., Tung, K.S., Coonrod, S.A., Takahashi, Y., Bigler, D., Chang, A., Yamashita, Y., Kincade, P.W., Herr, J.C. & White, J.M. (1999). Role of the integrin-associated protein CD9 in binding between sperm ADAM 2 and the egg integrin alpha6beta1: implications for murine fertilization. Proc. Natl. Acad. Sci. USA 96, 11830–11835.CrossRefGoogle ScholarPubMed
Cline, C.A., Schatten, H., Balczon, R. & Schatten, G. (1983). Actin-mediated surface motility during sea urchin fertilization. Cell Motil. 3, 513–524.CrossRefGoogle ScholarPubMed
Close, B., Banister, K., Baumans, V., Bernoth, E.M., Bromage, N., Bunyan, J., Erhardt, W., Flecknell, P., Gregory, N., Hackbarth, H., Morton, D. & Warwick, C. (1996). Recommendations for euthanasia of experimental animals. Part 1: DGXI of the European Commission. Lab. Anim. 30, 293–316.Google Scholar
Close, B., Banister, K., Baumans, V., Bernoth, E. M., Bromage, N., Bunyan, J., Erhardt, W., Flecknell, P., Gregory, N., Hackbarth, H., Morton, D. & Warwick, C. (1997). Recommendations for euthanasia of experimental animals: Part 2. DGXT of the European Commission. Lab. Anim. 31, 1–32.Google Scholar
Cuthbertson, K.S. (1983). Parthenogenetic activation of mouse oocytes in vitro with ethanol and benzyl alcohol. J. Exp. Zool. 226, 311–314.CrossRefGoogle ScholarPubMed
Dale, B., Tosti, E. & Iaccarino, M. (1995). Is the plasma membrane of the human oocyte reorganised following fertilisation and early cleavage? Zygote 3, 31–36.CrossRefGoogle ScholarPubMed
Fulton, B.P. & Whittingham, D.G. (1978). Activation of mammalian oocytes by intracellular injection of calcium. Nature 273, 149–151.CrossRefGoogle ScholarPubMed
Gardner, A.J. & Evans, J.P. (2006). Mammalian membrane block to polyspermy: new insights into how mammalian eggs prevent fertilisation by multiple sperm. Reprod. Fertil. Dev. 18, 53–61.CrossRefGoogle ScholarPubMed
Horvath, P.M., Kellom, T., Caulfield, J. & Boldt, J. (1993). Mechanistic studies of the plasma membrane block to polyspermy in mouse eggs. Mol. Reprod. Dev. 34, 65–72.CrossRefGoogle ScholarPubMed
Johnson, M.H., Eager, D., Muggleton-Harris, A. & Grave, H.M. (1975). Mosaicism in organisation concanavalin A receptors on surface membrane of mouse egg. Nature 257, 321–322.CrossRefGoogle ScholarPubMed
Kaji, K., Oda, S., Shikano, T., Ohnuki, T., Uematsu, Y., Sakagami, J., Tada, N., Miyazaki, S. & Kudo, A. (2000). The gamete fusion process is defective in eggs of CD9-deficient mice. Nat. Genet. 24, 279–282.CrossRefGoogle ScholarPubMed
Komar, A. (1982). Fertilization of parthenogenetically activate mouse eggs. I. Behaviour of sperm nuclei in the cytoplasm of parthenogenetically activated eggs. Exp. Cell Res. 139, 361–367.CrossRefGoogle ScholarPubMed
Komorowski, S., Szczepanska, K. & Maleszewski, M. (2003). Distinct mechanisms underlie sperm-induced and protease-induced oolemma block to sperm penetration. Int. J. Dev. Biol. 47, 65–69.Google ScholarPubMed
Komorowski, S., Baranowska, B. & Maleszewski, M. (2006). CD9 protein appears on growing mouse oocytes at the time when they develop the ability to fuse with spermatozoa. Zygote 14, 1–5.CrossRefGoogle ScholarPubMed
Le Naour, F., Rubinstein, E., Jasmin, C., Prenant, M. & Boucheix, C. (2000). Severely reduced female fertility in CD9-deficient mice. Science 287, 319–321.CrossRefGoogle ScholarPubMed
Longo, F.J. (1987). Actin-plasma membrane associations in mouse eggs and oocytes. J. Exp. Zool. 243, 299–309.CrossRefGoogle ScholarPubMed
Longo, F.J. (1997). Fertilization. Chapman & Hall, London, Weinham, New York, Tokyo, Melbourne, Madras.Google Scholar
Maleszewski, M. (1992). Behavior of sperm nuclei incorporated into parthenogenetic mouse eggs prior to the first cleavage division. Mol. Reprod. Dev. 33, 215–221.CrossRefGoogle Scholar
Maleszewski, M. & Bielak, A. (1993). Sperm penetration in parthenogenetic mouse embryos triggers a plasma membrane block to polyspermy. Zygote 1, 237–242.CrossRefGoogle ScholarPubMed
Maleszewski, M., Kimura, Y. & Yanagimachi, R. (1996). Sperm membrane incorporation into oolemma contributes to the oolemma block to sperm penetration: evidence based on intracytoplasmic sperm injection experiments in the mouse. Mol. Reprod. Dev. 44, 256–259.3.0.CO;2-0>CrossRefGoogle Scholar
Maluchnik, D. & Borsuk, E. (1994). Sperm entry into fertilised mouse eggs. Zygote 2, 129–131.CrossRefGoogle ScholarPubMed
McAvey, B.A., Wortzman, G.B., Williams, C.J. & Evans, J.P. (2002). Involvement of calcium signaling and the actin cytoskeleton in the membrane block to polyspermy in mouse eggs. Biol. Reprod. 67, 1342–1352.CrossRefGoogle ScholarPubMed
Miyado, K., Yamada, G., Yamada, S., Hasuwa, H., Nakamura, Y., Ryu, F., Suzuki, K., Kosai, K., Inoue, K., Ogura, A., Okabe, M. & Mekada, E. (2000). Requirement of CD9 on the egg plasma membrane for fertilization. Science 287, 321–324.CrossRefGoogle ScholarPubMed
Nicolson, G.L., Yanagimachi, R. & Yanagimachi, H. (1975). Ultrastructural localization of lectin-binding sites on the zonae pellucidae and plasma membranes of mammalian eggs. J. Cell Biol. 66, 263–274.CrossRefGoogle ScholarPubMed
Nicosia, S.V., Wolf, D.P. & Inoue, M. (1977). Cortical granule distribution and cell surface characteristics in mouse eggs. Dev. Biol. 57, 56–74.CrossRefGoogle ScholarPubMed
Pyrzynska, B., Maleszewski, M. & Maluchnik, D. (1996). Mouse oocytes penetrated by sperm at GV or GVBD stage lose the ability to fuse with additional spermatozoa. Zygote 4, 123–128.CrossRefGoogle ScholarPubMed
Runge, K.E., Evans, J.E., He, Z.Y., Gupta, S., McDonald, K.L., Stahlberg, H., Primakoff, P. & Myles, D.G. (2007). Oocyte CD9 is enriched on the microvillar membrane and required for normal microvillar shape and distribution. Dev. Biol. 304, 317–325.CrossRefGoogle ScholarPubMed
Sala-Valdes, M., Ursa, A., Charrin, S., Rubinstein, E., Hemler, M.E., Sanchez-Madrid, F. & Yanez-Mo, M. (2006). EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrin–radixin–moesin proteins. J. Biol. Chem. 281, 19665–19675.CrossRefGoogle Scholar
Santella, L., Alikani, M., Talansky, B.E., Cohen, J. & Dale, B. (1992). Is the human oocyte plasma membrane polarized? Hum. Reprod. 7, 999–1003.CrossRefGoogle ScholarPubMed
Sato, K. (1979). Polyspermy-preventing mechanisms in mouse eggs fertilized in vitro. J. Exp. Zool. 210, 353–359.CrossRefGoogle ScholarPubMed
Shalgi, R. & Phillips, D. (1980). Mechanics of sperm entry in cycling hamsters. J. Ultrastruct. Res. 71, 154–161.CrossRefGoogle ScholarPubMed
Swann, K., Saunders, C.M., Rogers, N.T. & Lai, F.A. (2006). PLCzeta(zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin. Cell. Dev. Biol. 17, 264–273.CrossRefGoogle ScholarPubMed
Szollosi, D. (1962). Cortical granules: a general feature of mammalian eggs? J. Reprod. Fertil. 4, 223–224.Google Scholar
Tilney, L.G. & Jaffe, L.A. (1980). Actin, microvilli, and the fertilization cone of sea urchin eggs. J. Cell Biol. 87, 771–782.CrossRefGoogle ScholarPubMed
Wabik-Sliz, B. & Kujat, R. (1979). The surface of mouse oocytes from two inbred strains differing in efficiency of fertilization, as revealed by scanning electron microscopy. Biol. Reprod. 20, 405–408.CrossRefGoogle ScholarPubMed
Wassarman, P.M. (1990). Regulation of mammalian fertilization by zona pellucida glycoproteins. J. Reprod. Fertil. Suppl. 42, 79–87.Google ScholarPubMed
Wilson, N.F. & Snell, W.J. (1998). Microvilli and cell–cell fusion during fertilization. Trends Cell Biol. 8, 93–96.CrossRefGoogle ScholarPubMed
Wolf, D.P. (1978). The block to sperm penetration in zonal-free mouse eggs. Dev. Biol. 64, 1–10.CrossRefGoogle ScholarPubMed
Wortzman, G.B. & Evans, J.P. (2005). Membrane and cortical abnormalities in post-ovulatory aged eggs: analysis of fertilizability and establishment of the membrane block to polyspermy. Mol. Hum. Reprod. 11, 1–9.CrossRefGoogle ScholarPubMed
Wortzman-Show, G.B., Kurokawa, M., Fissore, R.A. & Evans, J.P. (2007). Calcium and sperm components in the establishment of the membrane block to polyspermy: studies of ICSI and activation with sperm factor. Mol. Hum. Reprod. 13, 557–565.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1994). Mammalian fertilization. In The Physiology of Reproduction, 2nd edn (Knobil, E. & Neill, J. eds). Raven Press, New York, pp. 189–317.Google Scholar
Yanagimachi, R. & Noda, Y.D. (1970). Ultrastructural changes in the hamster sperm head during fertilization. J. Ultrastruct. Res. 31, 465–485.CrossRefGoogle ScholarPubMed
Ziyyat, A., Rubinstein, E., Monier-Gavelle, F., Barraud, V., Kulski, O., Prenant, M., Boucheix, C., Bomsel, M. & Wolf, J.P. (2006). CD9 controls the formation of clusters that contain tetraspanins and the integrin alpha 6 beta 1, which are involved in human and mouse gamete fusion. J. Cell Sci. 119, 416–424.CrossRefGoogle ScholarPubMed