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Nuclear envelope removal/maintenance determines the structural and functional remodelling of embryonic red blood cell nuclei in activated mouse oocytes

Published online by Cambridge University Press:  15 January 2010

Daniel Szöllösi ,
Renata Czołowska ,
Ewa Borsuk ,
Maria S. Szöllösi  and
Pascale Debey
Daniel Szöllösi
Affiliation:
INRA, Jouy-en-Josas, France, University of Warsaw, Poland, IBPC, Paris and Muséum National d'Histoire Naturelle, Paris, France
Renata Czołowska*
Affiliation:
INRA, Jouy-en-Josas, France, University of Warsaw, Poland, IBPC, Paris and Muséum National d'Histoire Naturelle, Paris, France
Ewa Borsuk
Affiliation:
INRA, Jouy-en-Josas, France, University of Warsaw, Poland, IBPC, Paris and Muséum National d'Histoire Naturelle, Paris, France
Maria S. Szöllösi
Affiliation:
INRA, Jouy-en-Josas, France, University of Warsaw, Poland, IBPC, Paris and Muséum National d'Histoire Naturelle, Paris, France
Pascale Debey
Affiliation:
INRA, Jouy-en-Josas, France, University of Warsaw, Poland, IBPC, Paris and Muséum National d'Histoire Naturelle, Paris, France
*
Renata Czołowska, Department of Embryology, University of Warsaw, Krakowskie Przedmiescie 26/28, 00-927 Warsaw 64, Poland. Telephone: +48 22 6 20 03 81 (ext. 475). Fax: +48 22 8 26 86 24. e-mail: [email protected].
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Summary

Nuclei of embryonic red blood cells (e-RBC) from 12-day mouse fetuses are arrested in Go phase of the cell cycle and have low transcriptional activity. These nuclei were transferred with help of polyethylene glycol (PEG)-mediated fusion to parthenogenetically activated mouse oocytes and heterokaryons were analysed for nuclear structure and transcriptional activity. If fusion proceeded 25–45 min after oocyte activation, e-RBC nuclei were induced to nuclear envelope breakdown and partial chromatin condensation, followed by formation of nuclei structurally identical with pronuclei. These ‘pronuclei’, similar to egg (female) pronuclei, remained transcriptionally silent over several hours of in vitro culture. If fusion was performed 1 h or later (up to 7 h) after activation, the nuclear envelope of e-RBC nuclei remained intact and nuclear remodelling was less spectacular (slight chromatin decondensation, formation of nucleolus precursor bodies). These nuclei, however, reinforced polymerase-II-dependent transcription within a few hours of in vitro culture. Our present experiments, together with our previous work, demonstrate that nuclear envelope breakdown/maintenance are critical events for nuclear remodelling in activated mouse oocytes and that somatic dormant nuclei can be stimulated to renew transcription at a time when the female pronucleus remains transcriptionally silent.

Keywords

HeterokaryonsMouse oocyteNuclear remodellingRed blood cell nucleiTranscription
Type
Research Article
Information
Zygote , Volume 6 , Issue 1 , February 1998 , pp. 65 - 73
Copyright
Copyright © Cambridge University Press 1998

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References

Aoki, F., Worrad, D.M. & Schultz, R.M. (1997). Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 181, 296–307.CrossRefGoogle ScholarPubMed
Borsuk, E., Szöllösi, M.S., Besombes, D. & Debey, P. (1996). Fusion with activated mouse oocytes modulates the transcriptional activity of introduced somatic cell nuclei. Exp. Cell Res. 225, 93–101.CrossRefGoogle ScholarPubMed
Bouniol, C., Nguyen, E. & Debey, P. (1995). Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp. Cell Res. 218, 57–62.CrossRefGoogle ScholarPubMed
Bruno, J., Reich, N. & Lucas, J.J. (1981). Globin synthesis in hybrid cells constructed by transplantation of dormant avian erythrocyte nuclei into enucleated fibroblasts. Mol. Cell Biol. 1, 1163–76.Google ScholarPubMed
Campbell, K.H.S., McWhir, J., Ritchie, W.A. & Wilmut, I. (1996). Sheep cloned by nuclear transfer from a cultured cell line. Nature 380, 64–6.CrossRefGoogle ScholarPubMed
Claussen, C.P. (1985). Cell organelles involved in hemoglobin biosynthesis in vertebrates. Fortsch. Zool. 30, 397–400.Google Scholar
Cuthbertson, K.S.R. (1983). Parthenogenetic activation of mouse oocytes in vitro with ethanol and benzyl alcohol. J. Exp. Zool. 226, 311–14.CrossRefGoogle ScholarPubMed
Czolowska, R., Szöllösi, D. & Szöllösi, M.S. (1992). Changes in embryonic 8-cell nuclei transferred by means of cell fusion to mouse eggs. Int. J. Dev. Biol. 36, 543–53.Google ScholarPubMed
Derenzini, M., Farabegoli, F., Pession, A. & Novello, F. (1987). Spatial redistribution of ribosomal chromatin in the fibrillar centres of human circulating lymphocytes after stimulation of transcription. Exp. Cell Res. 170, 31–41.CrossRefGoogle ScholarPubMed
DiBerardino, M.A. & Hoffner-Orr, N. (1992). Genomie potential of erythroid and leucocytic cells of Rana pipiens analyzed by nuclear transfer into diplotene and maturing oocytes. Differentiation 50, 1–13.Google Scholar
Fulton, B.P. & Whittingham, D.G. (1978). Activation of mammalian oocytes by intracellular injection of calcium. Nature 273, 149–51.Google Scholar
Halleck, M.S., Schlegel, R.A. & Rose, K.M. (1989). Cyto-plasmic to nuclear translocation of RNA polymerase I is required for lipopolisaccharide-induced nucleolar RNA synthesis and subsequent DNA synthesis in murine B lymphocytes, J. Cell Sci. 92, 101–9.CrossRefGoogle Scholar
Harris, J.R. (1986). Blood cell nuclei: the structure and function of lymphoid and erythroid nuclei. Int. Rev. Cytol. 102, 53–168.Google Scholar
Hernandez-Verdun, D. & Bouteille, M. (1979). Nucleologenesis in chick erythrocyte nuclei reactivated by cell fusion. J. Ultrastruct. Res. 69, 164–79.CrossRefGoogle ScholarPubMed
Hozák, P., Novák, J.T. & Smetana, K. (1989). Three-dimensional reconstructions of nucleolus-organizing regions in PHA-stimulated human lymphocytes. Biol. Cell 66, 225–33.Google ScholarPubMed
King, W.A., Shepherd, D.L., Plante, L., Lavoir, M.-C., Looney, C.R. & Barnes, F.L. (1996). Nucleolar and mitochondrial morphology in bovine embryos reconstructed by nuclear transfer. Mol. Repród. Dev. 44, 499–506.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Kopeĉný, V., Fléchon, J-E., Camous, S. & Fulka, J. Jr (1989). Nucleologenesis and the onset of transcription in the eight-cell bovine embryo: fine-structural autoradiographie study. Mol. Repród. Dev. 1, 79–90.CrossRefGoogle Scholar
Kovach, J.S., Marks, P.A., Russell, E.S. & Epier, H. (1967). Erythroid cell development in fetal mice: ultrastructural characteristics and hemoglobin synthesis, J. Mol. Biol. 25, 131–2.CrossRefGoogle ScholarPubMed
Linder, S., Zuckerman, S.H. & Ringertz, N.R. (1981). Reactivation of chicken erythrocyte nuclei in heterokaryons results in expression of adult chicken globin genes. Proc. Nati. Acad. Sci. USA 78, 6286–9.CrossRefGoogle ScholarPubMed
Nasr-Esfahani, M., Johnson, M.H. & Aitken, R.J. (1990). The effect of iron and iron chelators on the in vitro block to development of the mouse preimplantation embryo: BAT6 a new medium for improved culture of the mouse embryos in vitro. Hum. Reprod. 5, 997–1003.CrossRefGoogle ScholarPubMed
Ochs, R.L. & Smetana, K. (1989). Fibrillar center distribution in nucleoli of PHA-stimulated human lymphocytes. Exp. Cell Res. 184, 552–7.CrossRefGoogle ScholarPubMed
Rifkind, R.A., Bank, A. & Marks, P.A. (1974). Erythropoiesis. In The Red Blood Cell, ed. Mac, D., Surgenor, N., vol. 1, pp. 51–89. New York: Academic Press.CrossRefGoogle Scholar
Scheer, U., Lanfranchi, G., Rose, K.M., Franke, W.W. & Ringertz, N.R. (1983). Migration of rat RNA polymerase into chick erythrocyte nuclei undergoing reactivation in chick-rat heterokaryons. J. Cell Biol. 97, 1641–3.CrossRefGoogle ScholarPubMed
Setterfield, G., Hall, R., Bladon, T., Little, J. & Kaplan, J.G. (1983). Changes in structure and composition of lymphocyte nuclei during mitogenic stimulation, J. Ultrastruct. Res. 82, 264–82.CrossRefGoogle ScholarPubMed
Szöllösi, M.S. & Szöllösi, D. (1988). ‘Blebbing’ of the nuclear envelope of mouse zygotes, early embryos and hybrid cells, J. Cell Sci. 91, 257–67.CrossRefGoogle ScholarPubMed
Szöllösi, D., Czolowska, R., Soltyńska, M.S. & Tarkowski, A.K. (1986a); Ultrastructure of cell fusion and premature chromosome condensation (PCC) of thymocyte nuclei in metaphase II mouse oocytes. Biol. Cell 56, 239–50.CrossRefGoogle ScholarPubMed
Szöllösi, D., Czolowska, R., Soltyńska, M.S. & Tarkowski, A.K. (1986b). Remodelling of thymocyte nuclei in activated mouse oocytes: an ultrastructural study. Eur. J. Cell Biol. 42, 140–51.Google ScholarPubMed
Szöllösi, D., Czolowska, R., Szöllösi, M.S. & Tarkowski, A.K. (1988). Remodelling of mouse thymocyte nuclei depends on the time of their transfer into activated, homologous oocytes. J. Cell Sci. 91, 603–13.CrossRefGoogle ScholarPubMed
Szöllösi, M.S., Kubiak, J.Z., Debey, P. de, Pennard, H., Szöllösi, D. & Maro, H. (1993). Inhibition of protein kinases by 6-dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J. Cell Sci. 104, 861–72.Google Scholar
Takeuchi, I.K. & Takeuchi, Y.K. (1986). Ultrastructural localization of Ag-NOR proteins in full- grown oocytes and preimplantation embryos of mice. J. Electron Microsc. 35, 280–7.Google Scholar
Tarkowski, A.K. & Wróblewska, J. (1967). Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage, J. Embryol. Exp. Morphol. 18, 155–80.Google Scholar
Telford, N.A., Watson, A.J. & Schultz, G.A. (1990). Transition from a maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Repród. Dev. 26, 90–100.CrossRefGoogle ScholarPubMed
Wansink, D.G., Schul, W., van der Kraan, I., van Steensel, B., van Driel, R. & de Jong, L. (1993). Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus, J. Cell Biol. 122, 283–93.Google Scholar
Weber, M., Kubiak, J.Z., Arlinghaus, R.B., Pines, J. & Maro, B. (1991). c-mos proto-oncogene product is partly degraded after release from meiotic arrest and persists during interphase in mouse zygotes. Dev. Biol. 148, 393–7.CrossRefGoogle ScholarPubMed
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J. & Campbell, K.H.S. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–3.CrossRefGoogle ScholarPubMed