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Cell Division and the Mitotic Spindle'

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Cell Division and the Mitotic Spindle' Cell Division and the Mitotic Spindle' SHINYA INOUE The study of cell division spans the past full century . Lately, by Schrader [6]) . Chromosomes were pulled toward the spindle the field has blossomed, and exciting advances have been poles, via their kinetochores," by shortening of a traction fiber made, especially at the molecular and fine-structural levels . or the chromosomal spindle fiber. In addition, chromosomes Downloaded from http://rupress.org/jcb/article-pdf/91/3/131s/1075457/131s.pdf by guest on 28 September 2021 Yet as we commemorate the centennial of Flemming's discov- were "pushed" apart by the pole-to-pole lengthening of the ery' of "indirect" cell division, or mitosis, many basic questions central spindle to which the chromosomal fibers were an- still remain unanswered or incompletely explained . chored . The notion of a musclelike contraction for poleward The first half-century of study on cell division is synthesized chromosome motion had been propounded by Flemming in in Wilson's (2) classic treatise "The Cell in Development and 1879 (1) and earlier workers, and questioned by Wilson (2) as Heredity ."' While laying a solid foundation for the cytology of not being consistent with the "dynamic nature of the cytoplas- the dividing cell and the genetic and developmental signifi- mic fibrillae" observed in living cells. As to the dual mecha- cance of mitosis and meiosis, Wilson (Chapter IX) also directs nism, Ris (8), in working with living grasshopper spermato- our attention to an important viewpoint regarding the struc- cytes, was able to inhibit the pole-to-pole elongation without tural basis of cell function . Thus he quotes Brdcke : affecting chromosome-to-pole movement by exposing the cells "We must therefore ascribe to living cells, beyond the mo- to a solution containing a few tenths of a percent chloral lecular structure of the organic compounds that they contain, hydrate . still another structure of different type of complication ; and it Yet the nagging doubt, expressed by Wilson (e .g ., pages 178- is this which we call by the name of organization ." 198 in reference 2) and others regarding the physical nature of It is this aspect of the dividing cell, its organization, especially the "achromatic" fibrous machinery of the mitotic spindle, in its dynamic attributes, that I shall stress in this briefhistorical which was believed to be responsible for chromosome move- sketch . In particular, I shall focus on the organization of the ment, had not abated. Rather, the problems were compounded ephemeral mitotic spindle, which emerges cyclically at each by the late 1940s despite, and partly because of, the wealth of cell division . With it, the replicated, condensed chromosomes studies that had been made on carefully fixed and stained cells are separated and positioned forinclusion into the (two) daugh- and by the deductions drawn from observations of living cell ter cells. behavior (6) . In that atmosphere it was first necessary to learn whether the mitotic figures seen in fixed cells in fact repre- The Mitotic Spindle sented, in living cells, a physically integral body capable of moving chromosomes or exerting force enough to deform cell As we entered the early 1950s, evidence pointed to two shape . mechanisms ofanaphase chromosome movement (summarized ISOLATION OF THE MITOTIC SPINDLE : In1952,Ma- zia and Dan [9] succeeded in developing a ' Dedicated to Professor Kenneth W. Cooper, University of California, method for the mass Riverside, whose continued friendship and advice have added im- isolation of "mitotic apparatuses," thereby identifying the mi- mensely to my work . totic spindle, chromosomes, and asters as a coherent physical z Translated and reproduced in 1965 . J. Cell Biol. 25(1 ; part 2) :1-69 . body separable from the rest of the cell (Fig . 1) . Although there Flemming saw that the nucleus did not divide directly into two, but were earlier reports of expelling the spindle out of an intact formed chromatin threads (hence mitosis) . The condensed chromatin cell (e .g ., Foot and Strobell [10] from earthworm eggs), the threads, or chromosomes, were moved apart and placed into two new pioneering work of Mazia and Dan finally opened the way for cells by a transient, fibrillar achromatic apparatus, the "nuclear sp~- the mass isolation and characterization of the mitotic appara- r dle" (1) formed from the hyaline kinoplasm . tus . That same year, Carlson (11), in an extensive micromanip- 'Wilson's work is complemented in the botanical realm by Sharp (3) . ulation study on living grasshopper neuroblasts, demonstrated Belai (4) provides a thorough, thought-provoking examination of the integrity and mechanical achromatic spindle components and varying patterns of mitosis in anisotropy of the metaphase spindle, as well as the protists . Morgan (5) illustrates and raises penetrating questions regard- "liquefaction" of the spindle mid-zone ing the role of cell division in embryonic development and gene observed during anaphase . expression . "Chromosomes commonly possess a single spindle fiber attachment s. INOUE Marine Biological Laboratory, Woods Hole, Massachusetts, point, or kinetochore. Some chromosomes have, or behave as though and Department of Biology, University of Pennsylvania, Philadelphia, they have, diffuse kinetochores along the length of their chromosomes Pennsylvania (6, 7) . They are called holokinetic chromosomes . THE JOURNAL OF CELL BIOLOGY " VOLUME 91 NO . 3 PT . 2 DECEMBER 1981 131s-147s C The Rockefeller University Press " 0021-9525/81/12/131s/17 $1 .00 131s Downloaded from http://rupress.org/jcb/article-pdf/91/3/131s/1075457/131s.pdf by guest on 28 September 2021 FIGURE 1 Mitotic spindle in metaphase isolated from the egg of a sea urchin, Lytechinus variegatus. (Left) Observed with a rectified polarizing microscope, spindle fibers and astral rays appear in light or dark contrast depending on their orientation . The weak birefringence (measuring a few nanometers in retardation) of the fibers produces the sharp contrast observed . Microtubular bundles are responsible for the (positive form) birefringence of the fibers . Chromosomes display little birefringence and appear as gray bodies at the equator of the spindle. (Right) The same spindle in Nomarsky differential interference contrast . Chromosomes show prominently . The microtubules in these clean spindles (isolated in a new medium devised by Salmon) depolymerize when exposed to submicromoiarconcentrations of calcium ions once glycerol is removed from the isolation medium . In these isolates, which lack vesicular components, the chromosomal fibers shorten as they are depolymerized by micromolar concentrations of calcium ions. Unpublished figures, courtesy of Dr . E . D . Salmon, University of North Carolina . Bar, 10 Am . Many improvements were made on the basic isolation tech- tion) as a single cell progressed through prometaphase, meta- nique of Mazia and Dan. In particular, the work of Kane (12) phase, anaphase, and telophase . Each interpreted the obser- that identified the pH and solute conditions (in effect, water vations in molecular terms, variously biased by the paradigm activity) needed for mitotic apparatus isolation, helped shed adopted . light on the basic physicochemical parameters that delineated By 1953, I was able to demonstrate clearly with the polarizing the functioning cytoplasm . On the other hand, early attempts microscope (19) that "there is fibrous structure in living cells at defining the chemical makeup of the mitotic spindle were which in conformation is very close to what the cytologists less successful . In retrospect, that is not so surprising because have long observed in well-fixed preparations . There are con- the fibers of the spindle and aster are immersed in (and spun tinuous fibers, chromosomal fibers, and astral rays" (6). Cou- out from) the hyaline cytoplasm that permeates the cell. Large pled with Cleveland et al . (20) and Cooper's (21) earlier cytoplasmic granules are excluded from the spindle, but ribo- observations of fibrous structures in the spindles of certain somes and some membranes are not. Yolk and other granules other living cells, the issue of the "reality" of spindle fibers also adhered to earlier isolates . seemed to be settled . SPINDLE FIBERS I NV I VO : Whereas the isolated mitotic Whereas these earlier studies vividly displayed some dy- apparatus exhibited a physical coherence and clearly displayed namic changes ofspindle birefringence in living cells, changes spindle fibers, such fibers could have arisen by fixing or which should reflect events taking place at the molecular level overstabilizing the cell, as was suggested by many investigators during cell division, a clearer outlook depended on better (see 6) . Pollister (13), for example, argued that astral rays were optical resolution and broader experience gained through ob- not fibers in the living cell but rather were channels offlow of servations and experimental manipulations of cells in division . oriented molecules belonging to the hyaloplasm. Our own With progressive improvements in the resolution and sensitivity work, which paralleled that of Mazia and Dan, focused on the of the polarizing microscope, culminating in the introduction development of sensitive polarized light microscopy, with of "rectified" optics (22), clearer images of individual spindle which we hoped to study directly in living cells the nature of fibers were obtained, and the birefringence distribution within the anisotropically arrayed
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