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The localization of LAP2β during pronuclear formation in bovine oocytes after fertilization or activation

Published online by Cambridge University Press:  01 May 2006

Mamiko Isaji
Affiliation:
Department of Bioresource and Agrobiosciences, Graduate School of Science and Technology, Kobe University, Kobe 657-8501, Japan.
Hisataka Iwata
Affiliation:
Department of Animal Science, Tokyo University of Agriculture, Funako 1737, Atugi, 246-0034, Japan.
Hiroshi Harayama
Affiliation:
Department of Bioresource and Agrobiosciences, Graduate School of Science and Technology, Kobe University, Kobe 657-8501, Japan.
Masashi Miyake*
Affiliation:
Department of Bioresource and Agrobiosciences, Graduate School of Science and Technology, Kobe University, Kobe 657-8501, Japan.
*
All correspondence to: M. Miyake, Department of Bioresource and Agrobiosciences, Graduate School of Science and Technology, Kobe University, Kobe 657-8501, Japan. e-mail: miyake@kobe-u.ac.jp

Summary

We have shown that the assembly of lamin-associated polypeptide (LAP) 2β was detected surrounding the chromatin mass around the time of extrusion of the second polar body (PB) in some fertilized oocytes, but not in most activated oocytes, by using A23187 and cycloheximide (CaA + CH). Here, we immunohistologically analysed the correlation between LAP2β assembly and chromatin condensation in fertilized and activated oocytes during the second meiosis. In bovine cumulus cells, the onset of LAP2β assembly was observed around anaphase chromosomes with strongly phosphorylated histone H3. No LAP2β assembled around the chromosomes in the first and second polar bodies and the alternative oocyte chromatin (oCh) if histone H3 was phosphorylated. Only histone H3 of oCh was completely dephosphorylated during the telophase II/G1 transition (Tel II/G1), and then LAP2β assembled around only the oCh without phosphorylated histone H3. In the oocytes activated by CaA + CH, LAP2β did not assemble around the condensed oCh during the Tel II/G1 transition, although their histone H3 dephosphorylation occurred rather rapidly compared with that of the fertilized oocytes. The patterns of histone H3 dephosphorylation and LAP2β assembly in oocytes activated by CaA alone showed greater similarity to those in fertilized oocytes than to those in oocytes activated by CaA + CH. These results show that LAP2β assembles around only oCh after complete dephosphorylation of histone H3 after fertilization and activation using CaA alone, and that the timing of histone H3 dephosphorylation and LAP2β assembly in these oocytes is different from that of somatic cells. The results also indicate that CH treatment inhibits LAP2β assembly around oCh but not histone H3 dephosphorylation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

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References

de la Barre, A.E., Gerson, V., Gout, S., Creaven, M., Allis, C.D. & Dimitrov, S. (2000). Core histone N-termini play an essential role in mitotic chromosome condensation. EMBO J. 19, 379–91.Google Scholar
Bodoor, K., Shaikh, S., Salina, D., Raharjo, W.H., Bastos, R., Lohka, M. & Burke, B. (1999). Sequential recruitment of NPC proteins to the nuclear periphery at the end of mitosis. J. Cell Sci. 112, 2253–64.CrossRefGoogle Scholar
Collas, P. (1999). Sequential PKC- and Cdc2-mediated phosphorylation events elicit zebrafish nuclear envelope disassembly. J. Cell Sci. 112, 977–87.CrossRefGoogle ScholarPubMed
Dechat, T., Gotzmann, J., Stockinger, A., Harris, C.A., Talle, M.A., Siekierka, J.J. & Foisner, R. (1998). Detergent-salt resistance of LAP2alpha in interphase nuclei and phosphorylation-dependent association with chromosomes early in nuclear assembly implies functions in nuclear structure dynamics. EMBO J. 17, 4887–902.CrossRefGoogle ScholarPubMed
Foisner, R. (1997). Dynamic organization of intermediate filaments and associated proteins during the cell cycle. Bioessays 19, 297305.CrossRefGoogle ScholarPubMed
Foisner, R. & Gerace, L. (1993). Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73, 1267–79.CrossRefGoogle ScholarPubMed
Furukawa, K. (1999). LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2- chromatin interaction. J. Cell Sci. 112, 2485–92.CrossRefGoogle ScholarPubMed
Furukawa, K., Pante, N., Aebi, U. & Gerace, L. (1995). Cloning of a cDNA for amino-associated polypeptide 2 (LAP2) and identification of regions that specify targeting to the nuclear envelope. EMBO J. 14, 1626–36.CrossRefGoogle Scholar
Furukawa, K., Fritze, C.E. & Gerace, L. (1998). The major nuclear envelope targeting domain of LAP2 coincides with its lamin binding region but is distinct from its chromatin interaction domain. J. Biol. Chem. 273, 4213–19.CrossRefGoogle ScholarPubMed
Giet, R. & Glover, D.M. (2001). Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152, 669–82.CrossRefGoogle ScholarPubMed
Goto, H., Tomono, Y., Ajiro, K., Kosako, H., Fujita, M., Sakurai, M., Okawa, K., Iwamatsu, A., Okigaki, T., Takahashi, T. & Inagaki, M. (1999). Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274, 25543–9.CrossRefGoogle ScholarPubMed
Gotzmann, J. & Foisner, R. (1999). Lamins and lamin-binding proteins in functional chromatin organization. Crit. Rev. Eukaryotic Gene Expression 9, 257–65.CrossRefGoogle ScholarPubMed
Gruenbaum, Y., Wilson, K.L., Harel, A., Goldberg, M. & Cohen, M. (2000). Review: nuclear lamins – structural proteins with fundamental functions. J. Struct. Biol. 129, 313–23.CrossRefGoogle ScholarPubMed
Hendzel, M.J., Wei, Y., Mancini, M.A., Van Hooser, A., Ranalli, T., Brinkley, B.R., Bazett-Jones, D.P. & Allis, C.D. (1997). Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348–60.Google Scholar
Hozak, P., Sasseville, A.M., Raymond, Y. & Cook, P.R. (1995). Lamin proteins form an internal nucleoskeleton as well as a peripheral lamina in human cells. J. Cell Sci. 108, 635–44.CrossRefGoogle ScholarPubMed
Hsu, J.Y., Sun, Z.W., Li, X., Reuben, M., Tatchell, K., Bishop, D.K., Grushcow, J.M., Brame, C.J., Caldwell, J.A., Hunt, D.F., Lin, R., Smith, M.M. & Allis, C.D. (2000). Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102, 279–91.CrossRefGoogle ScholarPubMed
Isaji, M., Iwata, H., Harayama, H. & Miyake, M. (2004). The localization of LAP2β in bovine oocytes after in vitro activation and fertilization. Zygote 12, 8193.CrossRefGoogle ScholarPubMed
Lenart, P. & Ellenberg, J. (2003). Nuclear envelope dynamics in oocytes: from germinal vesicle breakdown to mitosis. Curr. Opin. Cell Biol. 15, 8895.CrossRefGoogle ScholarPubMed
Maison, C., Pyrpasopoulou, A., Theodoropoulos, P.A. & Georgatos, S.D. (1997). The inner nuclear membrane protein LAP1 forms a native complex with B-type lamins and partitions with spindle-associated mitotic vesicles. EMBO J. 16, 4839–50.CrossRefGoogle ScholarPubMed
Moir, R.D., Yoon, M., Khuon, S. & Goldman, R.D. (2000). Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J. Cell Biol. 151, 1155–68.CrossRefGoogle ScholarPubMed
Murnion, M.E., Adams, R.R., Callister, D.M., Allis, C.D., Earnshaw, W.C. & Swedlow, J.R. (2001). Chromatin-associated protein phosphatase 1 regulates aurora-B and histone H3 phosphorylation. J. Biol. Chem. 276, 26656–65.CrossRefGoogle ScholarPubMed
Nickerson, J. (2001). Experimental observations of a nuclear matrix. J. Cell Sci. 114, 463–74.CrossRefGoogle ScholarPubMed
Prigent, C. & Dimitrov, S. (2003). Phosphorylation of Serine 10 in histone H3: what for?. J. Cell Sci. 116, 3677–85.CrossRefGoogle Scholar
Sauve, D.M., Anderson, H.J., Ray, J.M., James, W.M. & Roberge, M. (1999). Phosphorylation-induced rearrangement of the histone H3 NH2-terminal domain during mitotic chromosome condensation. J. Cell Biol. 145, 225–35.CrossRefGoogle ScholarPubMed
Scrittori, L., Hans, F., Angelov, D., Charra, M., Prigent, C. & Dimitrov, S. (2001). pEg2 aurora-A kinase, histone H3 phosphorylation, and chromosome assembly in. Xenopus egg extract. J. Biol. Chem. 276, 30002–10.CrossRefGoogle ScholarPubMed
Steen, R.L. & Collas, P. (2001). Mistargeting of B-type lamins at the end of mitosis: implications on cell survival and regulation of lamins A/C expression. J. Cell Biol. 153, 621–6.CrossRefGoogle ScholarPubMed
Steen, R.L., Martins, S.B., Tasken, K. & Collas, P. (2000). Recruitment of protein phosphatase 1 to the nuclear envelope by A-kinase anchoring protein AKAP149 is a prerequisite for nuclear lamina assembly. J. Cell Biol. 150, 1251–62.CrossRefGoogle Scholar
Stuurman, N., Heins, S. & Aebi, U. (1998). Nuclear lamins: their structure, assembly, and interactions. J. Struct. Biol. 122, 4266.CrossRefGoogle ScholarPubMed
Sugiyama, K., Sugiura, K., Hara, T., Sugimoto, K., Shima, H., Honda, K., Furukawa, K., Yamashita, S. & Urano, T. (2002). Aurora-B associated protein phosphatases as negative regulators of kinase activation. Oncogene 21, 3103–11.Google Scholar
Van Hooser, A., Goodrich, D.W., Allis, C.D., Brinkley, B.R. & Mancini, M.A. (1998). Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J. Cell Sci. 111, 3497–506.CrossRefGoogle Scholar
Wei, T., Lanlan, Y., Josephine, B., Gorovsky, M.A. & Allis, C.D. (1999). Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97, 99109.CrossRefGoogle ScholarPubMed
Ye, Q. & Worman, H.J. (1994). Primary structure analysis and lamin B and DNA binding of human LBR, an integral protein of the nuclear envelope inner membrane. J. Biol. Chem. 269, 11306–11.CrossRefGoogle ScholarPubMed
Zheng, R., Ghirlando, R., Lee, M.S., Mizuuchi, K., Krause, M. & Craigie, R. (2000). Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleoprotein complex. Proc. Natl. Acad. Sci. USA 97, 89979002.CrossRefGoogle Scholar