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Fine Structure of Centrosome Complex and Its Connection with Cell Nucleus in the Slime Mould, Physarum Polycephalum

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Fine Structure of Centrosome Complex and Its Connection with Cell Nucleus in the Slime Mould, Physarum Polycephalum _??_1992 The Japan Mendel society Cytologia 57: 515 -523 , 1992 Fine Structure of Centrosome Complex and its Connection with Cell Nucleus in the Slime Mould, Physarum polycephalum T. Ohta, S. Kawano and T. Kuroiwa Department of Biology , Faculty of Science, University of Tokyo, Hongo, Tokyo 113, Japan Accepted September 30, 1992 Nuclear migration plays a fundamental role in many developmental processes in both higher and lower eukaryotes (for review see Meindl 1983, Raff and Glover 1989). This migra tion is also observed during the amoebo-flagellate transformation of the slime mould , Physarum spp. (Schuster 1965, Aldrich 1968, Goodman 1980, Uyeda and Furuya 1985). The cell nucleus is located at the center of the cell in amoeba cells but at the cell periphery , bound tightly to the b ase of flagella in swarm cells . During the amoebo-flagellate transformation of P. polycephalum, the cell nucleus first forms a sharp projection in the direction of movement . The amoeba cell then transforms into a comma-shaped swarm cell with flagella . The centrosome is first located on the tip of the projected cell nucleus and always moves ahead of it. This centrosome migra tion was shown to play an essential role in cell-nuclear migration during the amoebo-flagellate transformation (Ohta et al. 1991). Nuclear migration mediated by the centrosome has also been observed druing the embryogenesis of Drosophila (Zolakar and Erk 1976, Raff and Glover 1989). Since nuclear migration was shown to be mediated by the centrosome, the centrosome would be expected to be strongly connected to the cell nucleus (Ohta et al. 1991). In most eukaryotes, the centrosome can be found in close proximity to cell nucleus. To maintain this spatial relationship, some type of connecting structure should exist universally between the centrosome and the cell nucleus. Since the centrosome functions as a microtubule organizing center (MTOC) (McIntosh 1983, Wheatley 1982) and several microtubules have indeed been observed to run between the centrosome and the cell nucleus, microtubules are generally believed to function as the connecting structure which anchor the centrosome. In P. polycephalum it has been suggested that a structure called mtoc, which is the microtubule organizing center as sociated with one of the two centrioles, is connected to the cell nucleus through microtubules (Wright et al. 1979, 1980a). However, both anchorage of the centrosome to the cell nucleus and cell-nuclear migration mediated by the centrosome were observed even after destruction of microtubules with a specific inhibitor, nocodazole (Ohta et al. 1991). This result suggests the presence of some connecting structure other than microtubules between the centrosome and the cell nucleus in P. polycephalum. Electron micrography with thin sections of intact amoeba cell is not suitable for observing fine details of electron opaque material near the centrosome, since cytoplasm around the cen trioles is stained uniformly by the conventional staining method. It is well known that cellular structures, such as the cytoskeleton, centrioles or microtubules, are conserved after treatment with some detergents. The different concentrations of NaCl were also expected to gradually destroy the bond between proteins so that debris of the cytoplasm would be removed while stubborn cytoskeletal structures would remain intact. Therefore, to remove the cytoplasm Correspondence and requests for reprints: T. Ohta, Department of Biology, Faculty of Science, Uni versity of Tokyo, Hongo, Tokyo 113, Japan. 516 T. Ohta, S. Kawano and T. Kuroiwa Cytologia 57 near the centrosome, we treated amoeba cells of P. polycephalum histochemically with Triton X-100 and NaCl, and analyzed the fine structure of the centrosome and its connection with the cell nucleus using light and electron microscopy. Ca2+ was added to depolymerize micro tubules. It was shown that structures observed by Wright et al. (1979, 1980a), namely, mtoc, link, ppks (para-posterior kinetosomal structure) and extension, composed a single structural unit together with structures newly found in our observation, crown and lattice. In this report we observed the fine structure of the connection and showed that it is maintained even after microtubules are depolymerized by Ca2+. Materials and methods The amoeba strain NG15 (Kawano et al. 1987) of Physarum polycephalum was used. Amoebae were prepared as described in the previous paper (Ohta et al. 1991). For the per meabilization of amoebae, an equal volume of double-strength permeabilization solution (0.2 % Triton X-100, 4mM MgCl2, 0-1000mM NaCl, 2mM EGTA or 4mM CaCl2) was added to the suspension of amoebae in 10mM KPB. After 1 min, the suspension was fixed either with 3.7 % formaldehyde for 10 min (fluorescence staining) or with 2.0 % glutaraldehyde for 1 hour (electron microscopy). Double-fluorescence staining of microtubules and DNA was conducted as described in the previous paper (Ohta et al. 1991). Triton permeabilized cells were prepared for whole mount electron microscopy by a modification of the method of Miller et al. (1970), originally used for studies of DNA transcription. 20-50 ƒÊl of sample suspension was sedimented at 1,000 g for 10 min directly onto carbon-coated grids. The grids were then negatively stained with 3 phosphotungstic acid, pH 7.0. Triton permeabilized cells in the presence of Call were pro cessed for thin section electron microscopy. After permeabilization, the cell suspension was pre-fixed by 2.0 % glutaraldehyde in 25mM sodium cacodylate buffer, pH 7.2, for 2 hour, post fixed in 1.0 % osmium tetroxide in 25mM sodium cacodylate buffer, pH 7.2, for 2 hours and then stained in 1 % uranyl acetate solution for 2 hours at room temperature. The sample was dehydrated with graded ethanol and embedded in Spurr's epoxy resin. Ultra-thin sections were contrasted successively with 2 % uranyl acetate and Reynolds' lead nitrate. Alternatively, amoeba cells were briefly exposed to 8 % osmium tetroxide vapor and treated as above there after. Results An electron micrograph of the amoeba cell of P. polycephalum is shown in Fig. 1. The centrosome is located next to the cell nucleus, and a round-shaped electron opaque mtoc can be observed between the centriole and the cell nucleus. In this electron micrograph, the mtoc appears to be directly connected to the outer membrane of the cell nucleus without intervening microtubules. This suggests that microtubules are not involved in this connection. How ever, a conventional thin-section technique such as in Fig. 1, does not produce a clear enough image of the region around the mtoc to demonstrate this possibility . To analyze the fine details of the perimeter of the centrosome, and especially the space between the cell nucleus and mtoc, we used Triton X-100 and different concentrations of NaCl to remove obstructive cytoplasm around the centrosome and the cell nucleus. The effects of 100mM and 1000mM NaCl on the amoeba cells permeabilized with Triton X-100 were ex amined by light and electron microscopy . In this lysis solution, we always used 2mM EGTA to exclude Ca2+ ion which depolymerizes microtubules. The treated cells were stained with 1992 Centro some Is Connected to Cell Nucleus 517 DAPI, anti-tubulin antibody and observed under fluorescence microscope equipped with phase-contrast (Fig. 2). Cells fixed with formaldehyde without treatment with NaCl and Triton X-100 were also observed as control. Control cells retained their cyto plasm and cellular microtubules. Mito chondrial nuclei (nucleoids) could still be observed around the cell nuclei (Fig. 2a, b, c). With 100mM NaCl, microtubular flu orescence was mostly degraded (Fig. 2e). Mitochondrial nuclear fluorescence was lost from around cell nucleus (Fig. 2f). In the phase contrast image, a filamentous appen dage could be seen extruding from the cell nucleus (Fig. 2d) and microtubular fluores cence originated from this structure. No sign of cytoplasm other than this appendage was visible under this condition. With 1000 mM NaCl, the amoeba cell nucleus became dispersed (Fig. 2g, i). The phase contrast image showed two black dots with a short tail and microtubular fluorescence was ob Fig. 1. Electron micorgraph of thin-sectioned amoeba cell showing the connection between the served as paired dots (Fig. 2h), correspond cell nucleus and the centrosome. The outer mem ingly, which indicates that these paired dots brane of the cell nucleus and mtoc of the centro represent centrioles visible at light microsco some seem to be directly connected to each other (indicated by arrows). Microtubules are barely pic level. distinguishable. N; cell nucleus, M; mtoc, L; link, AC; anterior centriole. Bar indicates 200 nm. Fig. 2. Effect of NaCl on Triton X-100-treated amoeba cell. Cells were observed under phase contrast light microscope (a, d, g) after staining with anti-tubulin antibody (b, e, h), DAPI (c, f, i). Control cells (a, b, c) were treated in the absence of NaCl. Cells were first treated with Triton X -100 and EGTA in the presence of 100mM (d, e, f) or 1000mM (g, h, i) NaCl. Arrowheads in dicate the location of the centrosome. Bar indicates 2 ƒÊm. 518 T. Ohta, S. Kawano and T. Kuroiwa Cytologia 57 These treated amoeba cells were examined by whole mount electron microscopy (Fig. 3). The cell-nuclear appendage and microtubules were now visible in detail because the obscuring cytoplasm had been degraded with 100mM NaCl (Fig. 3a). Two components of the cell nuclear appendage which had been revealed by light microscopy, i.e., two dots and a short tail, were confirmed to be centrioles and a filamentous structure composed of two parallel filaments, Fig. 3. Whole-mounted, negative-stained electron micrographs showing the effect of NaCl on amoebae. Amoebae were treated with Triton X-100 and EGTA in the presence of 100mM (a) or 1000mM (b) NaCl. M; mtoc, L; link, AC; anterior centriole, PC; posterior centriole, Cr; crown, P; para-posterior kinetosomal structure, E; extension, 4; microtubular array 4, Lt; lattice and N; cell nucleus.
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