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Patterns in Dictyostelium Discoideum: the Role of Myosin II in the Transition from the Unicellular to the Multicellular Phase

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Patterns in Dictyostelium Discoideum: the Role of Myosin II in the Transition from the Unicellular to the Multicellular Phase Journal of Cell Science 104, 457-466 (1993) 457 Printed in Great Britain © The Company of Biologists Limited 1993 Patterns in Dictyostelium discoideum: the role of myosin II in the transition from the unicellular to the multicellular phase Susannah Eliott1, Gregory H. Joss1, Annamma Spudich2 and Keith L. Williams1 1School of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia 2Department of Cell Biology, Stanford University School of Medicine, Stanford, California 94305, USA SUMMARY Dictyostelium discoideum amoebae which lack the elongation, cells within the mutant mound eventually myosin II gene are motile and aggregate to form rudi- cease translocation altogether as the terminal shape of mentary mounds, but do not undergo further morpho- the mound is reached and only intracellular particle logical development (Manstein et al., 1989). Here we use movement is observed. Scanning electron micrographs scanning electron microscopy, light microscopy, show that the surface of the wild-type mound consists immunofluorescence and computer analysis of time- of flattened cells which fit neatly together. The myosin lapse video films to study how D. discoideum myosin null null cell mound has an uneven surface, the orientation cells of strains HS2205 and HS2206 aggregate. Myosin of the cells is chaotic and no tip is formed. This is con- null cells are sufficiently coordinated in their move- sistent with the results of synergy experiments in which ments to form two-dimensional aggregation streams, myosin null cells were absent from the tips of chimeric although mutant cells within streams lack the elongated HS2205/AX2 slugs and pre-culminates. Immunofluores- shape and parallel orientation of wild-type strains. In cence microscopy using prespore and spore cell mark- the wild-type, cell movements are coordinated, cells ers reveals that a prestalk/prespore pattern forms usually joining streams that spiral inwards and upwards within the mutant mound but that terminal spore differ- as the mound extends into the standing papilla. In the entiation is incomplete. These results are discussed in aggregates of mutant strains, cell movements are relation to the role of myosin II in aggregation and mor- chaotic, only occasionally forming short-term spirals phogenesis. that rotate at less than half the speed of wild-type spi- rals and frequently change direction. Unlike the situa- Key words: myosin II, morphogenesis, Dictyostelium tion in the wild-type where spirals continue with mound development, cytoskeleton INTRODUCTION (Williams et al., 1986; De Lozanne and Spudich, 1987; Eliott et al., 1991). D. discoideum is a soil amoeba that can Animal morphogenesis involves precisely timed cell differ- exist as single cells or as a structured multicellular aggre- entiation and cell migrations. For co-ordinated cell move- gate, depending on the stage of the asexual lifecycle. Mol- ments to occur during morphogenesis, cells must be able ecular genetic techniques involving the use of homologous to respond to extracellular signals and alter their shape and recombination have made it possible to construct myosin II movements accordingly. There is increasing evidence that null cells from which the myosin heavy chain gene has been the cytoskeleton is involved in many aspects of morpho- excised (Manstein et al., 1989). Though the mutant amoe- genesis including cell migration, cytodifferentiation and bae are able to migrate on a surface and aggregate to form developmental gene expression (Ben-Ze’ev, 1991, for rudimentary mounds, further development is blocked; these review). We are interested specifically in the role of myosin cells are unable to form the organized multicellular ‘slug’ II in animal morphogenesis. Actin and myosin II form a or mature fruiting body (Knecht and Loomis, 1987; De contractile unit that is thought to be involved in the fold- Lozanne and Spudich, 1987; Wessels et al., 1988; Peters et ing of epithelial cell sheets during gastrulation in chick (Lee al., 1988). This implies an important role for myosin II in et al., 1983) and Drososphila embryos (Young et al., 1991; tissue formation. The timing of developmental gene see also Odell et al., 1981) and the compaction of the mouse expression in the mutant is apparently normal (Knecht and morula (Sobel, 1983, 1984). Loomis, 1988), indicating that the block in morphogenesis We use the cellular slime mould, Dictyostelium dis - is due to a spatial or mechanical abnormality. coideum, to study the cytoskeleton and cell-cell interactions Using immunofluorescence techniques, it has been shown during development of a simple three-dimensional tissue that the myosin II protein is distributed unevenly in cells 458 S. Eliott and others of D. discoideum wild-type slugs, being concentrated in the 1987, 1988; De Lozanne and Spudich, 1987). HS2205 mounds cortex of peripheral and anterior cells, and evenly through- were fixed after all streams had either collected into the mounds out the cytoplasm in the inner posterior cells (Eliott et al., or begun to break up (between 17 and 19 h depending on initial 1991). This distribution corresponds with the prestalk-pre- cell density). For comparison, tipless aggregates of AX2 cells were spore pattern, a finding that is consistent with prestalk cells developed as described above and fixed after 7 h development. providing the major motive force for slug movement All mounds were vapour fixed in 1% (v/v) glutaraldehyde and 2.5% (w/v) paraformaldehyde in starvation buffer (25 mM MES, (Inouye and Takeuchi, 1980; Williams et al., 1986; Voet et 2 mM MgSO4, 0.2 mM CaCl2, pH 6.8) for approximately 2 h. al., 1984; Yumura, 1992). Cells at the periphery of the slug After fixation, plastic replicas were made of the mounds using are polarised with respect to myosin II, resembling indi- Exaflex hydrophobic dental impression material (Kerr) as vidual motile amoebae. We suggest that these cells have a described by Williams and Green (1988) for plant meristems. This specialised role in the morphogenesis and migration of the technique requires minimal fixation and handling of tissue and whole organism. thus reduces artefacts due to conventional preparation for SEM. Here we study the aggregation and development of two The replicas were coated with gold and viewed under a Philips myosin null mutant strains, HS2205 and HS2206, in order 505 scanning electron microscope. to elucidate the role of myosin II in normal D. discoideum development. We show that cells lacking myosin II are able Time-lapse videomicroscopy and computer to form aggregation streams that appear similar to wildtype analysis strains on casual observation. However, cell shape is abnor- For video observation and analysis of cell movements during mal in both streams and mounds. Myosin null cells do not aggregation, cells were filmed using a low-light-sensitive camera undergo the coordinated spiralling movements observed for (Mintron, CCD, MTV-1801CB) attached to a Zeiss OPM1 micro- scope fitted with a f100 or f150 mm lens and recorded on a wild-type cells as they approach the aggregation centre. National time-lapse cassette recorder, NV-8051. Myosin null cell Although coordinated movement is absent in mutant streams and aggregates were filmed for 2 to 8 h periods within a mounds, a distinctive prespore pattern is established. time frame of 12 to 24 h after plating. AX2 and AX3 streams and Mutant mounds are unable to form tips and, when mixed aggregates were filmed for 30 min to 5 h periods within a time with wild-type cells, are absent from the tips of chimeric frame of 5 to 12 h after plating. slugs and preculminates, suggesting that myosin II may be Speed of spiral motion (min per revolution) in aggregation involved in the process of tip formation (a factor that may mounds was determined from time lapse video segments by mea- be crucial in the inability of myosin null cells alone to suring the amount of time taken for a number of cells in the outer progress morphologically beyond the mound stage). third of a rotating aggregate to move 1/4 or 1/2 way around the circumference of the mound. For computer analysis, images taken at 10 s intervals using the above microscope and camera were stored directly in a 386 com- MATERIALS AND METHODS puter using a Matrox PIP(1024) image board. Cell movements were tracked using a program which maps individually selected Strains and development of cells points through consecutive frames (Breen et al., unpublished data). For light, immunofluorescence and scanning electron microscopy This program measures flow of identifiable features rather than (SEM) and synergy experiments, the D. discoideum myosin null delineating the cells and tracking them individually. Cell-cell mutants, HS2205 and HS2206 (Manstein et al., 1989) and two boundaries and intracellular vesicles were chosen as points to be wild-type axenic strains, AX3 (Loomis, 1969) and AX2 (Watts tracked because they could be easily seen and tracked for several and Ashworth, 1970), were used. Amoebae were grown on slime minutes. mould nutrient agar (SM) with Klebsiella aerogenes. To develop aggregates, cells were collected from a lawn of K. aerogenes, Immunofluorescence washed three times in Bonner’s salts solution and 2-25 ml drops 6 6 HS2206 amoebae (prepared as described above) were allowed to at a density of between 2 ´ 10 and 4 ´ 10 cells/ml were pipet- develop for 19, 23, 30 and 65 h at 21(±1)˚C before fixing in 2.5% ted onto water agar (1% Noble agar in distilled water with 250 (w/v) paraformaldehyde in PBS (0.15 M potassium phosphate; mg/ml dihydrostreptomycin sulphate) which formed thin (i.e. 2.75 0.9% (w/v) NaCl, pH 7.2) for 15 h at room temperature. Mounds ml agar: for filming and photography) or thick (i.e. 30 ml agar: were then encased in molten water agar and cubes bearing 1 to 4 for scanning electron and immunofluorescence microscopy) layers mounds were washed in PBS overnight at 4˚C.
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