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The Position of the Microtubule-Organizing Center In Proc. Nati. Acad. Sci. USA Vol. 88, pp. 8367-8371, October 1991 Cell Biology The position of the microtubule-organizing center in directionally migrating fibroblasts depends on the nature of the substratum KARIN SCHUTZE*t, ANDREW MANIOTIS*t, AND MANFRED SCHLIWA*t* *Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720; and tInstitute for Cell Biology, University of Munich, Schillerstrasse 42, 8000 Munich 2, Federal Republic of Germany Communicated by Keith R. Porter, June 3, 1991 ABSTRACT Immunofluorescence and confocal micros- We have used a convenient assay for determining direc- copy were used to monitor the positioning of microtubule- tional migration of large numbers of cells that does not organizing centers (MTOCs) during directional migration of require constant observation of each individual cell. The chicken embryo fibroblasts on planar substrata and within assay is based on the fact that cells of small aggregates, or three-dimensional collagen gels. Homologous assay conditions plaques, move radially from the plaque during the initial based on the radial emigration of cells from cell aggregates stages of migration. The advantage of this assay is that it can were used in both cases. Whereas =70% of the cells migrating be applied to cells on both planar and three-dimensional directionally on glass and at least 60% on other planar sub- substrata. We compared MTOC positioning during the radial strata have their MTOCs anterior to the nucleus, MTOCs are migration of cells on glass and within a three-dimensional randomly distributed around the nucleus in cells within colla- collagen environment. We find that, in contrast to two- gen gels. The anterior location of the MTOC in cells on glass dimensional substrata, cells in collagen gels have a random is attained gradually during the first 4 hr of directional position of the MTOC relative to the nucleus during direc- migration. Cells on oriented planar substrata, manufactured tional movement. by photolithographic etching of narrow parallel grooves into the glass surface, also have a random position of the MTOC, MATERIALS AND although the cells themselves assume a highly polarized cell METHODS shape parallel to the grooves. This environment mimics the Chicken embryo fibroblasts (CEFs) of day 9-12 embryos partial orientation of the collagen fibers produced by the (kindly provided by S. Martin, University of California, tractive forces of the cells within collagen networks. These Berkeley) were prepared and cultured as described (18). Rat findings demonstrate a difference in MTOC positioning be- tail collagen (kindly provided by S. Nandi, University of tween Jibroblasts on planar substrata and within a quasi- California, Berkeley) was used as described (19). For the natural environment. preparation ofcell aggregates, primary cultures ofCEFs were allowed to grow to confluency for =3 days. Regions of high Microtubules play important roles in the life of a eukaryotic cell density were separated from the rest of the monolayer cell. Originating from the centrosome, the cell's microtubule- with a glass needle, collected with a Pasteur pipette, and organizing center (MTOC), they are involved in cell division, either placed directly onto coverslips or mixed with an equal intracellular transport, the development and maintenance of amount of neutralized collagen. About 30 ,ul of the collagen cell asymmetry, and cell migration (1). An involvement in the gel/cell aggregate mixture was carefully spread onto a 12-mm expression of a locomotory phenotype is revealed in the coverslip with a sterilized strip of parafilm. For immunoflu- experimental observation that microtubule depolymerization orescence microscopy, cells were processed as described impairs cell locomotion (e.g., see refs. 2 and 3), and the (20). Cells in gels were lysed for 2 min with 2% Triton X-100 morphological finding that, in certain migrating cells, the in PHEM buffer (21) and fixed with 1% glutaraldehyde in MTOC is located ahead of the nucleus and behind the PHEM buffer containing 2% Triton X-100. For best results, advancing lamellipodium (4-6). This intriguing correlation antibody incubations were carried out overnight at room was interpreted to mean that MTOC reorientation to the front temperature. A Bio-Rad MRC 600 laser scanning microscope of the cell not only accompanies the onset of cell migration was used for the visualization of some cells embedded within but actually "may play a role in determining the direction of collagen gels but turned out to be impractical for determining cell movement" (ref. 4; for reviews, see refs. 7-9). MTOC position in large numbers ofcells. Much ofthe scoring Fibroblasts cultured on glass or plastic substrata have of MTOC positions was done independently by three differ- served as important models for some of these studies (3, 5, ent people and was done directly on the fluorescence micro- 10). However, the advantage oftwo-dimensional surfaces for scope because the ability to focus through the preparations microscopic observation is counterbalanced by the disadvan- facilitates the determination of MTOC position, particularly tage that these conditions are clearly unrepresentative of a in gels. In some experiments, MTOC position was also fibroblast's natural environment, a three-dimensional colla- determined by the regrowth of small microtubule asters after gen network (11, 12). Observations on fibroblasts in hydrated depolymerization at 0C. For each cell migrating from a cell collagen gels in vitro and in situ demonstrate a number of aggregate in a radial fashion, the position of the MTOC differences in morphology and behavior from their counter- relative to the nucleus was recorded in a schematic drawing parts on planar substrata (e.g., see refs. 11, and 13-17). It (for an example, see Fig. 4). In this way, a complete record would seem important to ascertain that findings on cells of MTOC position in all the cells analyzed under all exper- cultured on planar substrata apply to cells in a more natural imental conditions was compiled. environment as well, particularly with respect to the question Glass slides with a series of parallel grooves of different of MTOC positioning during cell migration. depth and pitch (width) were prepared by a photolithographic The publication costs of this article were defrayed in part by page charge Abbreviations: MTOC, microtubule-organizing center; CEF, payment. This article must therefore be hereby marked "advertisement" chicken embryo fibroblast. in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed at t. 8367 Downloaded by guest on September 27, 2021 8368 Cell Biology: Schfitze et A Proc. Natl. Acad. Sci. USA 88 (1991) FIG. 1. Time course of CEF emigration from cell aggregates (plaques) on a glass surface (a-c) and within a three-dimensional collagen gel (d-f). The numbers in each micrograph represent time (in hr) after plating. (a-c, x135; d-f, x90.) process in the Microfabrication Facility ofthe Department of in gels keep moving radially for at least 50 hr, even after losing Electrical Engineering and Computer Sciences (University of contact with the plaque. Video recordings show that the California, Berkeley). The steps in the preparation process overall movement of cells is smooth and continuous in both consist of computerized design of a mask with the desired cases, although advances of the leading edge may be inter- grating pattern, coating of the glass surface with photoresist, rupted by brief phases of retraction, particularly in collagen exposure to UV light through the mask, development of the gels. The average speed ofmovement during emigration from photoactivated glass slide, and etching to the desired groove a plaque is 0.21 + 0.08 um/min (n = 128) for cells on glass depth. The groove depths used here ranged from 2 to 5 um. and 0.16 + 0.05 ,&m/min (n = 241) within a collagen gel. In In most ofour experiments, slides with a groove depth of2-3 both conditions, an intact microtubule system is required for ,um were used. migration since disassembly of microtubules by nocodazole (5 tzg/ml) severely reduces (glass) or completely inhibits (gels) cell movement. Immunofluorescence microscopy con- RESULTS firms the complete absence of microtubules in both cases Comparison of Plaques on Glass and Within Coflagen Gels. (data not shown). The behavior and morphology of fibroblasts on glass and MTOC Position. Immunofluorescence and laser scanning within three-dimensional hydrated collagen gels have been confocal microscopy were used to determine the position of described (e.g., see refs. 11-15) and need not be repeated the MTOC during the peak phase of radial migration, when here. Only some features specifically pertaining to the plaque cells had moved approximately one cell length away from the assay shall briefly be mentioned. Plaques on two-dimensional plaque. This phase was between 4 and 6 hr after plating substrata adhere quickly (within 20 min). The leading edges plaques on glass and between 15 and 25 hr after embedding ofcells emerge from the plaque perimeter after =30 min, and plaques within a collagen gel (Fig. 3). On glass, >70%o of the cells move out radially with broad, flat lamellipodia typical cells have the MTOC positioned anterior to the middle ofthe for fibroblasts (Fig. 1 a-c). After 5-8 hr, cells that had lost nucleus (Table 1). In cells moving away from gel-embedded contact with the plaque begin to move in directions other than plaques, the MTOC has a random position relative to the radial. Plaques embedded within three-dimensional collagen nucleus, with -45% located anterior to the nuclear midline. gels usually show a refractory period of several hours before The MTOC distributions in cells of one population on glass cells emerge. During this period, radial alignment ofcollagen and one population within a collagen gel are shown in Fig. 4. fibers in the vicinity ofthe plaque becomes visible.
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