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Metaphase and Anaphase in the Artificially Induced Monopolar Spindle

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Metaphase and Anaphase in the Artificially Induced Monopolar Spindle Proc. Natl. Acad. Sci. USA Vol. 91, pp. 3921-3925, April 1994 Cell Biology Metaphase and anaphase in the artificially induced monopolar spindle (mitosis/chromosome movement/mitotic spindle/sea urchin egg) KoHnI ITO*, MICHITAKA MASUDAt, KEIGI FUJIWARAt, HIROSHI HAYASHI*, AND HIDEMI SATOf *Sugashima Marine Biological Laboratory, School of Science, Nagoya University, Toba, Mie 517, Japan; tDepartment of Structural Analysis, National Cardiovascular Center Research Institute, Suita, Osaka 565, Japan; and *School of Science, Nagoya University, Nagoya 464, Japan Communicated by Daniel Mazia, January 3, 1994 ABSTRACT By using monopolar spindles artificially in- and a period clearly defined as metaphase was not observed duced in sea urchin embryos, we exmied whether or not the (5, 6, 11). Leslie (12) produced an extra half-spindle exper- presence of two opposing poles was an indispensable condition imentally from one pole of a bipolar spindle in fertilized sea for keeping chromosomes at a fixed distance from the pole at urchin eggs. Statistical analyses using fixed cells showed that metaphase and for the anaphase chromosome movement. the average chromosome-to-pole distance in the metaphase Chromosomes were stained with Hoechst dye 33342 and their extra half-spindle was identical to that in the metaphase behavior was followed in the monopolar and the control bipolar bipolar spindle. Monopolar spindles were also produced in a spindles. In the monopolar spindle, chromosomes were first temperature-sensitive mutant line of Syrian hamster cells arranged on a curved metaphase plate and then spread on a (13). Electron microscope studies of these cells showed that part of the Imaginary surface of a sphere whose center was the chromosomes lined up in a metaphase-like position in the monopole. The estimated chromosome-to-pole distance was monopolar spindle. However, since chromosome movement similar to that of bipolar spindies at metaphase and remained was not followed in living cells in either of these studies, an fixed until chromosomes started to move toward the pole. The oscillatory chromosome movement similar to that in newt average duration of metaphase in the monopolar spindle was 6 lung cells could not be ruled out. times longer than that in the bipolar spindle. The poleward Monopolar spindles can be artificially induced in sea urchin movement of chromosomes in the monopolar spindle was embryo cells (14) and have been extensively characterized: similar to the anaphase A (chromosome-to-pole movement) in one cell has one centrosome consisting of a pair ofcentrioles the bipolar spindle with respect to the velocity, duration, (15); the single pole organizes chromosomes in a quasi- distance, and synchronization ofmigration. These results show metaphase arrangement in which one kinetochore facing the that even half of the normal spindle has capacities for the pole is connected to the pole by a bundle of microtubules, arrangement of chromosomes at metaphase and for the whereas its sister kinetochore facing away from the pole is anaphase A chromosome movement. Based on these results, we free from microtubule contact (16). In spite of these detailed were able to exclude some existing theories of metaphase, such morphological data, chromosome movement in the mono- as the one based on the balance offorces between the two poles. polar spindle has not been convincingly described, because it is difficult to identify chromosomes in monopolar spindles in There are several hypotheses on the mechanism for the living sea urchin blastomeres with a Nomarski or a phase- arrangement of chromosomes on the metaphase plate. Per- contrast microscope. The same problem also makes it diffi- haps, the most conventional view (hypothesis A) states that cult to determine whether or not a stable metaphase exists in the balance between two poleward forces at the oppositely the monopolar spindle. oriented kinetochores keeps paired sister chromatids at the To overcome these difficulties, we stained chromosomes midpoint between two poles (1-3). Another hypothesis (hy- in artificially induced sea urchin monopolar spindles with pothesis B) is that the chromosomes are confined to the Hoechst dye 33342 and observed chromosome behavior in equatorial boundary of a spindle because this is the equilib- living cells. Our analysis has shown that a period definable as rium position between the poleward force at the kinetochore metaphase exists, indicating that the balance offorces due to and the resistance of the relatively solid half-spindle to the the presence oftwo opposite poles as proposed by hypothesis further advance of the chromosomes to the pole (4). Instead A is not indispensable for the establishment of metaphase. of a physical boundary, hypothesis C postulates that each Our study has suggested that the astral ejection force acting chromosome arm is subjected to an ejection force generated on chromosome arms as proposed by hypothesis C is not a by astral microtubules to balance the poleward force at the significant force at metaphase. As the mechanism for estab- kinetochore (5-7). A newer idea (hypothesis D) is that lishing the metaphase chromosome arrangement, our results chromosomes are kept at the metaphase plate by the regu- are compatible with hypotheses B and D. In addition, lation of microtubule-based motors located at the kineto- anaphase chromosome movement, which was indistinguish- chore (8-10). able from anaphase A in bipolar spindles, was observed in the A monopolar spindle is an interesting in vivo system for monopolar spindle, indicating that the monopolar spindle investigating how chromosomes become arranged at a fixed also possessed the complete machinery required for the distance from the pole during metaphase. Chromosomes in a anaphase A chromosome movement. monopolar spindle cannot attain a metaphase position by the balance oftwo opposing forces as proposed by hypothesis A, but they may do so by the mechanism proposed by hypoth- MATERIALS AND METHODS esis B, C or D. In monopolar spindles of cultured newt lung Induction ofMonopolar Spindles. Monopolar spindles were cells, chromosomes oscillate toward and away from the pole induced in sea urchin eggs as described by Mazia et al. (14). In brief, fertilized eggs of the sea urchin (Hemicentrotus The publication costs ofthis article were defrayed in part by page charge pulcherrimus) and the sand dollar (Clypeaster japonicus) payment. This article must therefore be hereby marked "advertisement" were immersed in artificial seawater (Jamarin U, Osaka) in accordance with 18 U.S.C. §1734 solely to indicate this fact. containing 0.1 M 2-mercaptoethanol at prometaphase-to- 3921 Downloaded by guest on September 30, 2021 3922 Cell Biology: Ito et al. Proc. Natl. Acad. Sci. USA 91 (1994) metaphase of the first division and were kept immersed until Immunofluorescence Microscopy. Blastomeres having the control eggs completed the second division. They were monopolar spindles were fixed by incubation with 0.1% then washed several times with artificial seawater to remove glutaraldehyde and 2% formaldehyde in microtubule- 2-mercaptoethanol. Each egg formed a tetrapolar spindle and stabilizing medium [10 mM EGTA/0.55 mM MgCl2/25% divided into four daughter cells (1:4 division). Each daughter (wt/vol) glycerol/1% (wt/vol) Nonidet P-40/0.5 mM phenyl- cell reformed the nucleus and went into the next cell cycle, methanesulfonyl fluoride/25 mM Mes; pHl 6.8 (18)] for 20 during which a monopolar spindle was formed. In some cells, min. Microtubules were indirectly immunostained with rab- one of the furrows failed, so that they divided into three bit anti-tubulin antiserum raised against vinblastine-induced daughter cells (1:3 division). In this case, one cell had a sea urchin tubulin crystals (19) and followed by fluorescein- bipolar spindle and the other two cells had monopolar spin- conjugated affimity-purified goat anti-rabbit IgG (Cappel). dles. The induction ofmonopolar spindles was ascertained by Chromosomes were counterstained with propidium iodide at using a supersensitive polarizing microscope (17) manufac- 0.1 pg/ml. An Olympus confocal laser scanning microscope tured by Nikon Engineering. (LSM-GB200) was used to obtain optical sections of the Observation of Chromosome Movement. After 2-mercapto- monopolar spindle. Three-dimensional images were con- ethanol treatment, cells were immersed in artificial seawater structed by using a computer program developed by S. Hanai with Hoechst 33342 at 5-10 pg/ml. Embryos stained with the (Department of Vascular Physiology, National Cardiovascu- fluorescent dye developed normally at least to the hatching lar Center Research Institute, Osaka). stage. Chromosome movement was observed by using an Olympus BH-2 epifluorescence microscope equipped with a RESULTS 100-W mercury lamp, a standard UV filter set (excitation, 365-nm band pass; emission, 435-nm long pass) and a x40 Prometaphase in Monopolar Spindles. We observed chro- oil-immersion objective lens (na, 1.0). A neutral density filter mosome movement in both monopolar and control, bipolar (ND8) and a heat-cut filter were used to minimize photo- spindles in living sea urchin embryo cells which were stained bleaching and cell damage. Fluorescence images were col- with Hoechst 33342. Immediately after the breakdown ofthe lected by a SIT camera (C-1000-12, Hamamatsu Photonics, nuclear envelope, fluorescent chromosomes were seen to be frames an scattered inside the spherical region where the nucleus had Hamamatsu, Japan), averaged over
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