Stalk cell differentiation by cells from migrating slugs of Dictyostelium discoideum: special properties of tip cells
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1 /. Embryol. exp. Morph. Vol. 42, pp , Printed in Great Britain Company of Biologists Limited 1977 Stalk cell differentiation by cells from migrating slugs of Dictyostelium discoideum: special properties of tip cells By C. D. TOWN 1 AND E. STANFORD 1 From the Imperial Cancer Research Fund, Mill Hill Laboratories, London SUMMARY When fragments of migrating slugs of D. discoideum are disaggregated and spread on agar containing 1 ITIM cyclic AMP, cells from all parts of the slug form stalk cells with high efficiency. When cyclic AMP is not added to the agar, normal fruiting of dissociated slug cells can be prevented by overlaying them with cellophane. Under these conditions only cells from the anterior 10% of the slug (the 'tip') give rise to appreciable numbers of stalk cells, all other cells remaining amoeboid. By separating distinct cell populations with cellophane we have shown that tip cells can induce cells from other parts of the slug to differentiate into stalk cells. The ability of tips to induce stalk cells is independent of tip age, but the proportion of cells induced depends both on the age of the slug and the part of the slug from which they are derived. The proportion induced is greater in older slugs than in newly formed ones, and in the older slugs is greater in the cells from fronts than from backs. The active substance released by the tip cells may be cyclic AMP. INTRODUCTION Cytological and biochemical differences can be detected between cells comprising approximately the front one third and the rear two thirds of the migrating slug of D. discoideum (Bonner, Chiquoine & Kolderie, 1955; Krivanek, 1956; Newell, Ellingson & Sussman, 1969; Hayashi & Takeuchi, 1976). Under normal conditions, the cells from the front third of the slug become stalk cells in the mature fruiting body, while the remainder become spores (Raper, 1940). Fragments from any part of the slug can regulate to produce normally proportioned fruiting bodies, given sufficient time. However, if fragments are induced to fruit immediately after cutting, those derived from the front part produce fruit with disproportionately large stalks, indicating a degree of commitment of front cells to become stalk cells (Raper, 1940; Bonner & Slifkin, 1949; Sampson, 1976). The apical region or 'tip' corresponding to about the first 10 % of the slug has 1 Authors' address: Imperial Cancer Research Fund, Mill Hill Laboratories, Burtonhole Lane, London, NW7 IAD, U.K.
2 106 C. D. TOWN AND E. STANFORD long been recognized as having unique, organizer-like properties (Raper, 1940) and is often morphologically distinct (Loomis, 1975). There is evidence that it acts as the receptive and directive centre of migration (Raper, 1940; Poff & Loomis, 1973) and may be a source of chemotactic signals (Bonner, 1949; Rubin & Robertson, 1975) which are probably cyclic AMP (Rubin, 1976). It also specifies anterior-posterior polarity, and is absolutely required for all development of aggregates (Gerisch, 1960; Farnsworth, 1973). There exists some gradient down the slug reflected both in the time taken to form a new tip following removal of the original one (Farnsworth, 1973; Sampson, 1976) and in the ability of the cut surface at a particular point to inhibit secondary axis formation (Durston, 1976). We have recently demonstrated efficient induction of stalk cell differentiation when vegetative amoebae of strain V12 M2 are plated at high cell density in the presence of cyclic AMP (1-5 HIM) (Town, Gross & Kay, 1976). Cells spread at high density in the absence of cyclic AMP can be prevented from normal development and fruiting by an overlay of cellophane. Under these conditions, the cells aggregate via streams in the usual way but apparently proceed no further; no stalk cell differentiation is seen. The evidence for cell commitment in the slug (Raper, 1940; Bonner & Slifkin, 1949; Sampson, 1976) made it of interest to use the same technique to examine the behaviour of cells taken from the fronts and rears of slugs and spread on agar with and without cyclic AMP. We have found that the ability to form stalk cells in the absence of exogenous cyclic AMP is largely confined to the tip region and that tip cells are able to induce cells from other parts of the slug to differentiate into stalk cells. MATERIALS AND METHODS Dictyostelium discoideum strain V12 M2 was used. Cells were grown for 24 h at 22 C in association with K. aerogenes on SM agar (KH 2 PO 4, 2-25 g; K 2 HPO 4, 0-67 g; MgSO 4.7H 2 O, 0-5 g; Difco yeast extract, 0-5 g; Difco Bacto peptone, 5-0 g; glucose 5-0 g; Difco Bacto agar, 15-0 g; per litre water). They were then freed of bacteria by one wash in KK 2 buffer (KH 2 PO 4, 2-25 g; K 2 HPO 4, 0-67 g; MgSO 4.7H 2 O, 0-5 g; per litre water, ph 6-1) and three washes in distilled water. Washed cells were resuspended at 2 x 10 8 cells/ml in distilled water and 50 ju\ volumes were dispensed in lines ~ 4 cm long on 9 cm diameter agar plates (1-5% (w/v) Difco Bacto agar in distilled water). The plates were incubated in a humid atmosphere at 22 C under unidirectional illumination. Slugs formed after ~ 16 h and continued to migrate towards the light for up to 5 days. Sections were cut using a microspatula. To examine stalk cell differentiation at high cell density, three fragments each of one or more type were transferred to small squares of cellophane (325P; British Cellophane Ltd.) and gently dispersed with a platinum loop. These squares were then transferred to agar with
3 Stalk cell differentiation in Dictyostelium 107 or without cyclic AMP, so that the cell layer was sandwiched between the agar and cellophane. For observation at low cell density, fragments of each type were pooled and disaggregated by trituration in 1 % Bonner's salt solution. Cells were then spread on agar with or without cyclic AMP and examined for stalk cells after 2-3 days incubation at 22 C as described previously (Town et at. 1976). RESULTS (a) Stalk cell differentiation in disaggregated fronts and rears of slugs The frequencies of differentiation of cells plated at high density (where the cells are predominantly in contact) in the absence or presence of 1 mm cyclic AMP are shown in Fig. 1. In the absence of cyclic AMP, cells from the rears of slugs gave very few stalk cells, regardless of slug age (Fig. 1 a). In cells from the fronts of slugs, however, the proportion of stalk cells rose from 20 % for cells from day-0 slugs to about 50 % for older slugs. The difference between fronts and rears is highly significant (P < 001) except on day 0 (005 > P > 002). In the presence of 1 mm cyclic AMP, cells from both fronts and rears of slugs were induced to form stalk cells (Fig. 1 b). For the pooled data (all time points) the average frequencies of differentiation for cells from fronts and rears are (mean ± standard error of the mean) and 37-1 ±8-3 respectively. These frequencies are significantly different (0-002 > P > 0001). However, it is not possible to say from these data whether this average difference reflects a difference at all slug ages, or is due mainly to a decline in inducibility of cells from the rears of slugs at later times. (b) The role of the tip A second series of experiments was performed some time later using more refined dissection techniques. The principal object of these was to examine the possible role of the tip in the differentiation of front quarter cells reported above, following a suggestion by Dr Marilyn Monk. In these experiments the tip region was treated as a separate entity and the differentiation of various fragments was examined either alone or in a number of combinations. The results obtained for differentiation in the absence of cyclic AMP are shown in Table 1. Columns (a) and (b) contain the new data for the front and rear fragments, corresponding to those used in the first series of experiments, and are quantitatively similar to those in Fig. 1. The effect of the tip can be seen in subsequent columns. Column (c) shows that when tip cells alone are taken, a rather higher proportion of stalk cells is formed than when intact front quarters are used. Moreover, front quarters from which the tip has been removed (fragment 1, column d) yield a very low frequency of stalk cells, comparable to rear quarters. Mixtures of tips and fragment-1 or fragment-4 cells gave rise to considerable
4 108 C. D. TOWN AND E. STANFORD (a) NocAMP 80 - J tt. 100 (b)\ 1 ITIMCAMP 80 8 J 60 -I 1 40 ( I Slug age (days) Fig. 1. Stalk cell differentiation in high density cell populations derived from front and rear quarters of slugs of various ages, (a) No cyclic AMP, (b) with 1 mm cyclic AMP. Fronts, ; rears, O Data are shown as meanls.e. of the mean, with three or four independent determinations per point. Points with no error bars are single determinations. For clarity, some data points have been offset with respect to the abscissa. numbers of stalk cells (Table 1, columns (e) and (/)). The fact that the yield was significantly greater in the former than in the latter mixture (P < 0-01 for pooled data) suggested that the stalk cells formed in such mixtures might not derive only from the tip cells. In order to examine this possibility, cells from the tip and regions 1 or 4 were separately spread on cellophane squares which were then placed one over the other in pairs, on agar. In this way, the two cell populations were separated by a layer of cellophane and stalk cell differentiation was scored in each population separately. The results presented in Table 2 show that: (a) tip cells are able to induce stalk cell differentiation in cells of fragments 1 or 4 across a cellophane membrane, (b) the inducing 'power' of tip cells is similar whether they are derived from day-0 or day-2 slugs, (c) the inducibility (or
5 Stalk cell differentiation in Dictyostelium 109 Table 1. Stalk cell formation by different slug fragments or combinations of fragments in the absence of exogenous cyclic AMP Day 0 Day 1 Day 2 Day 3 Mean of all <data (a) T.I 7-2±l ± ± ± ±2-8 (b) ± ± ± ± ±O-7 (c) T 15-2 ± ± ± ± ±3-1 (d) 1 0* 3-5f 2 2±0 9 2t 1 7±0 6 (e) T+l 50±l ± ± ±2-4 ll-0±l-5 CO T ±0-5 ll-8± ± ± ±1-2 (g) T ± ± ± ± ±1-2 (h) ± ± ± ± ±0-9 The following nomenclature is used to describe the different combinations of cells examined: T = tip (first 10% of slug length), 1 = front quarter minus tip (i.e. from 10 to 25% of slug length), 4 = rear quarter minus a small 'tail' (i.e. from 75-95% of slug length), T.I = first quarter including tip (i.e. from 0 to 25% of slug length), T + l = tip mixed with section 1 from a different slug, T + 4 = tip plus section 4 from another slug, T.I = whole slug, = tipless slug. Data are given ±S.E. of the mean. * Six determinations. t Two determinations. Table 2. Induction of stalk cell differentiation in fragments 1 and 4 by tip cells For most experiments, slugs were prepared so that slugs of two different ages (day 0 and day 2) were available on the same day. Fragments T, 1, and 4 were cut as defined in Table 1 and disaggregated on cellophane squares. These were laid one over the other in pairwise combinations so that it was possible to examine the effect of slug age both on the potency of the tip as an inducing source, and on the sensitivity of the responding population (derived from fragment 1 or 4). Inducers 1 1 None Tips, day 0 Tips, day 2 Tips, day ± ±2-3 Responders Day 0 Day 2 Day 3 3-3±O ± ± ± ± ± ± ± ± O±l-5 The yields of stalk cells in the layers of tip cells overlaying a test population were comparable to those observed with tip cells alone (column (c), Table 1). 12 responsiveness) of cells from both fragments 1 and 4 is higher in day-2 slugs than in day-0 slugs {P < in each case), (d) as already suggested by the results in Table 1, at least with older slugs (day 2 and 3), more cells from fragment 1 are induced than from fragment 4. This difference is significant at the 1 % level when all the data for 2- and 3-day-old slugs are pooled ( (n = 14) for fragment 1, 14-1 ± 2-0 (n = 13) for fragment 4). Differentiation of the same fragments and combinations of fragments as in EMB 42
6 110 C. D. TOWN AND E. STANFORD 50 - (a) No camp (b) 1 mm camp > / ' / \ / 30- c/i 7J H n. \ 1 Tl' \ J^ I \ 1 \ \\ b Slug age (days) Fig. 2. Stalk cell differentiation in low density cell populations. Details as for Fig. 1. Table 1 was also examined in the presence of 1 mm cyclic AMP. Similar proportions of stalk cells (~ 50 %) were seen in all the cases, irrespective of the age or origin of the slug fragments. The difference between the response of fronts and rears was much smaller than in the first series of experiments (Fig. 1) and was not significant. (c) Differentiation at low cell density Stalk cell differentiation was also examined in cells disaggregated from the fronts and rears of slugs and plated as isolated cells at ~5 x 10 3 cells/cm 2, a cell density much lower than that used above. Vegetative cells plated at this density give no stalk cells in the absence of cyclic AMP and % stalk cells with 1 mm cyclic AMP (Town et ah 1976). The results for disaggregated slug cells are shown in Fig. 2.
7 Stalk cell differentiation in Dictyostelium 111 In the absence of cyclic AMP, cells from the rears of slugs gave rise to only a very small proportion of stalk cells (Fig. 2 a) and this number remained approximately constant with slug age. In cells from slug fronts, which include tip cells, the frequency of stalk cell differentiation was higher, and showed a considerable increase with slug age, rising from ~3 % on day 0 to ~ 40 % on day 3. The maximum frequency observed (40 % at day 3) was comparable to that seen in the high density preparation from old slug fronts (Fig. 1 a). It therefore appears that tip cells from old slugs can exert their influence over distances of up to 100 /*m, and that isolated cells of this age can respond as efficiently as cells at high density. In the presence of 1 HIM cyclic AMP, cells from fronts and rears of slugs differentiated into stalk cells with comparable efficiencies (fronts 34-4±60, rears 36-2 ± 7-4). These values are slightly higher than those observed previously for vegetative cells at this density (Town et al. 1976). DISCUSSION These results demonstrate two new properties of cells from the tips (anterior 10 %) of migrating slugs of Dictyostelium discoideum. Firstly, a substantial proportion of tip cells spread on agar under cellophane will differentiate into stalk cells without exogenous cyclic AMP. This proportion increases with slug age from 15 % for day-0 slugs to 40 % for day-2 to day-3 slugs. We cannot say whether this increase occurs uniformly throughout a constant 'tip region' or whether it represents a spreading back of this tip property as the slugs age, in a manner similar to that described for the pre-stalk enzyme alkaline phosphatase (Bonner et al. 1955; Krivanek, 1956). Secondly, tip cells release a dialysable factor which induces stalk cell differentiation in cells from other parts of the slug. The 'strength' of the inducing factor does not vary with slug age, but the responsiveness of cells to the factor is greater in older slugs. In addition, cells from the fronts of old slugs are more responsive to the inducing stimulus than those from the rear. Since 1 mm exogenous cyclic AMP similarly induces stalk cell differentiation in cells from any part of the slug, the dialysable inducing factor released by the tip is probably either cyclic AMP or some other substance capable of elevating the intracellular level of cyclic AMP. Exogenous cyclic AMP concentrations greater than 10~ 4 M are required to cause appreciable stalk cell differentiation, even at low cell density where there is relatively little hydrolysis (unpublished observations). It is unlikely that the number of tip cells used in the trans-cellophane induction experiments (~3 x 10 4 cells) could produce steady cyclic AMP concentrations of this magnitude, and even less likely that isolated tip cells could do this at ranges of up to ~ 100 jum. It is therefore likely that some kind of periodic signalling and signal amplification is occurring. It has previously been reported that slug tips are sources of chemotactic 8-2
8 112 C. D. TOWN AND E. STANFORD signals (Bonner, 1949; Rubin & Robertson, 1975; Rubin, 1976) and that they may also contain higher levels of cyclic AMP than the rest of the slug (Pan, Bonner, Wedner & Parker, 1974; Brenner, 1977). However, even if it should be true that the substance released by tip cells and inducing stalk cell formation under our conditions is cyclic AMP, it would be unwise to assume that this result has a direct bearing on the mechanism of pattern formation. Thus we know that exposure of a dense preparation of washed cells of various species to high concentrations of cyclic AMP results in their virtually quantitative conversion to stalk cells, and never to spores (Town et a/. 1976; Hohl, Honegger, Traub & Markwalder, 1977). However, since no conditions have yet been found that elicit spore formation in vitro, there can be no certainty that it is the cyclic AMP that determines the choice of one pathway rather than the other. It is equally possible that in the intact slug the tip signal is a relayed cyclic AMP signal (somewhat as it is during aggregation) and that this signalling is required for gene expression in both pathways of differentiation, the choice of pathway being determined by other, unknown, factor(s). We thank Dr Julian Gross for much helpful advice and encouragement. REFERENCES BONNER, J. T., CHIQUOINE, A. D. & KOLDERIE, M. Q. (1955). A histochemical study of differentiation in the cellular slime molds. /. exp. Zool. 130, BONNER, J. T. (1949). The demonstration of acrasin in the later stages of development of the slime mold Dictyostelium discoideum. J. exp. Zool. 119, BONNER, J. T. & SLIFKIN, M. K. (1949). A study of the control of differentiation: the proportion of stalk and spore cells in the slime mold Dictyostelium discoideum. Am. J. Bot. 36, BRENNER, M. (1977). Cyclic AMP gradient in migrating pseudoplasmodia of the cellular slime mold Dictyostelium discoideum. J. biol. Chem. 252, DURSTON, A. J. (1976). Tip formation is regulated by an inhibitory gradient in the Dictyostelium discoideum slug. Nature, Lond. 263, FARNSWORTH, P. (1973). Morphogenesis in the cellular slime mould Dictyostelium discoideum: the formation and regulation of aggregate tips and the specification of developmental axes. /. Embryol. exp. Morph. 29, GERISCH, G. (1960). Zellfunktionen und Zellfunktionswechsel in der Entwicklung von Dictyostelium discoideum. I. Zellagglutination und lnduktion der Fruchtkorperpolaritat. Wilhelm Roux Arch EntwMech. Org. 152, HAYASHI, M. & TAKEUCHI, I. (1976). Quantitative studies on cell differentiation during morphogenesis of the cellular slime mold Dictyostelium discoideum. Devi Biol. 50, HOHL, H. R., HONEGGER, R., TRAUB, F. & MARKWALDER, M. (1977). Influence of camp on cell differentiation and morphogenesis in Polysphondylium. In Proceedings of the EMBO. Workshop: 'Development and Differentiation in the Cellular Slime Moulds' 1 (ed. P. Cappuccinelli) Amsterdam: Elsevier/North Holland, pp KRIVANEK, J. O. (1956). Alkaline phosphatase activity in the developing slime mold, Dictyostelium discoideum Raper. J. exp. Zool. 133, LOOMIS, W. F. (1975). Polarity and Pattern in Dictyostelium. In Developmental Biology (ed. D. McMahon & C. F. Fox). ICN-UCLA Symposia on Molecular and Cellular Biology, vol. 2, pp Menlo Park, California: W. A. Benjamin, Inc.
9 Stalk cell differentiation in Dictyostelium 113 NEWELL, P. C, ELLINGSON, J. S. & SUSSMAN, M. (1969). Synchrony of enzyme accumulation in a population of differentiating slime mold cells. Biochim. biophys. Acta 111, PAN, P., BONNER, J. T., WEDNER, H. J. & PARKER, C. W. (1974). Immunofluoresence evidence for the distribution of cyclic AMP in cells and cell masses of the cellular slime molds. Proc. natn. Acad. Set, U.S.A. 71, POFF, K. L. & LOOMIS, W. F., Jr. (1973). Control of phototactic migration in Dictyostelium cliseoideum. Expl Cell Res. 82, RAPER, K. B. (1940). Pseudoplasmodium formation and organisation in Dictyostelium discoideum. J. Elisha Mitchell Sci. Soc. 56, RUBIN, J. & ROBERTSON, A. (1975). The tip of Dictyostelium discoideum pseudoplasmodium as an organizer. /. Embryol. exp. Morph. 33, RUBIN, J. (1976). The signal from fruiting body tips and conus tips of Dictyostelium discoideum. J. Embryol. exp. Morph. 36, SAMPSON, J. (1976). Cell patterning in migrating slugs of Dictyostelium discoideum. J. Embryol. exp. Morph. 36, TOWN, C. D., GROSS, J. D. & KAY, R. R. (1976). Cell differentiation without morphogenesis in Dictyostelium discoideum. Nature, Lond. 262, (Received 7 October 1976, revised 21 July 1977)
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