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In Dictyostelium Downloaded from genesdev.cshlp.org on October 7, 2021 - Published by Cold Spring Harbor Laboratory Press REVIEW Integration of signaling information in controlling, cell-fate decisions in Dictyostelium Richard A. Firtel Department of Biology, Center for Molecular Genetics, University of California, San Diego, La Jolla, California 92093-0634 USA Over the last few years, a combination of genetic, mo- cisions in Dictyostelium and their relationship to devel- lecular, and biochemical approaches has led to signifi- opmental decisions in other organisms. cant new insights into the regulation of development in Dictyostelium and has uncovered new pathways that Formation of the multicellular organism may also control developmental decisions in other sys- tems. In Dictyostelium, the vegetative growth and the Multicellular development is initiated several hours af- multicellular developmental portions of the life cycle are ter removal of the food source, when a small number of separated; wild-type Dictyostelium strains are haploid, cells within the population emit an extracellular pulse of and multicellular development, which is initiated by cAMP. Cells respond by chemotaxis toward the signal starvation, takes place in the absence of cell division. and activation of adenylyl cyclase (AC) to produce more Thus, many genes that are essential for the multicellular cAMP, which is secreted/released (Devreotes 1994). Cy- phase have no effect on growth, facilitating genetic anal- clic AMP binding to receptors on outlying cells relays ysis of gene products essential for multicellular develop- the signal, whereas binding to additional receptors on ment. The general developmental program of Dictyoste- the activated cell amplifies the signal. Like receptor-cou- lium is depicted in Figure 1. pled pathways in other systems, the responses are tran- Dictyostelium is an ideal organism for studying how sient; they adapt within 1-2 min, and the cells regain signaling pathways are integrated to control morphogen- responsiveness to cAMP in 5--6 min. About 20--30 pulses esis and gene regulation, and much of the recent progress (cycles of activation and adaptation of the pathways) are in understanding the control of multicellular develop- required for an aggregation domain to produce a mound. ment in Dictyostelium is a result of linking the various In addition to regulating the relay of the cAMP signal components into regulatory networks. The identifica- and chemotaxis, the cAMP pulses also induce expression tion and functional analysis of stage and cell-type-spe- of genes required for aggregation (pulse-induced genes), cific G proteins, serpentine (G protein-coupled) recep- as described below. tors, the transcription factor GBF (G-box-binding factor), Adaptation of the aggregation responses is crucial be- MAP (_r!aitogen-activated protein) kinases, PKA (protein cause this provides directionality to the chemotactic _kinase A_), GSK-3 (glycogen synthase _kinase-3)(the latter movement toward the aggregation center. The rapid ad- two control cell-fate decisions in Drosophila), and other aptation ensures that cells respond only to cAMP from signaling molecules common to all eukaryotes have pro- the direction of the aggregation center and not to cAMP vided basic, new insights into control of these processes secreted by outlying cells (Tomchik and Devreotes 1981; in Dictyostelium and other systems. In addition, novel Van Haastert et al. 1987). As long as cAMP is present, the pathways have been identified that are regulated by ex- pathways remain adapted. To remove extracellular tracellular cAMP functioning through serpentine recep- cAMP, aggregation-stage Dictyostelium cells express an tors to activate distinctly different developmental path- extracellular phosphodiesterase (PDE}, which rapidly hy- ways, depending on whether the cells perceive a pulsa- drolyzes the extracellular cAMP (Franke and Kessin tile or sustained signal. This has led to an initial 1992). The level of active PDE is tightly regulated both at understanding of how signaling and transcriptional the level of transcription and via a phosphodiesterase events are integrated to control developmental timing inhibitor (PDI, which binds to and inhibits the PDE), and how cell-type specification is regulated by these fac- because high levels of PDE would interfere with diffu- tors and extracellular morphogens. sion of cAMP to adjacent cells and low levels would This review examines these recent findings and de- result in the sustained presence of cAMP and prolonged scribes how they have led to a new understanding of the adaptation. High levels of cAMP stimulate PDE expres- molecular mechanisms regulating the developmental de- sion and inhibit the expression of PDI, whereas low lev- GENES & DEVELOPMENT 9:1427-1444 91995 by Cold Spring Harbor Laboratory Press ISSN 0890-9369/95 $5.00 1427 Downloaded from genesdev.cshlp.org on October 7, 2021 - Published by Cold Spring Harbor Laboratory Press Firtel Figure 1. The developmental cycle is shown. The first panel shows spore germi- nation. A dark-field image of an aggrega- tion domain is shown at 6 hr. Developing mounds are seen at 8 hr and 10 hr, and a tipped aggregate at 12 hr. At 14 hr, a finger has formed that falls over to become the slug (16 hr). Culmination ensues at 18 hr, and a mature fruiting body is formed by 24 hr. The developmental phases are shown with the periodicity of cAMP production. (Bottom) The developmental kinetics of gene expression, emphasizing the tran- scriptional changes at the time of mound formation. At the initiation of develop- ment by starvation, a set of genes are in- duced that are then repressed by pulses of cAMP. These pulses induce another set of genes (pulse-induced genes) that play es- sential roles during aggregation. As the mound forms, these pulse-induced genes are repressed and the developmental cascade leading to cell-type differentiation is initiated by the induction of GBF followed by the postaggregative or primary-response genes and the cell-type-specific genes. (See text for details.) els of cAMP stimulate PDI expression (Franke and has the same predicted structure as mammalian ACs Kessin 1992). The regulatory gene products discussed in (Pitt et al. 1992; Tang and Gilman 1992) and is thought this review are described in Table 1. to be directly regulated by the G~t subunit rather than a specific G~ subunit. Several lines of evidence support this conclusion. In vivo, cAMP activation of AC requires A series of integrated signaling pathways G~2, whereas in vitro, AC can be activated in g~2 but regulates aggregation not gf~ null cells by GTP~S (Kesbeke et al. 1988; Kuma- gai et al. 1991; Wu et al. 1995). Overexpression of G~2 Analysis of the signaling pathways that regulate aggre- suppresses the activation of AC but stimulates the acti- gation in Dictyostelium provides general insight into eu- vation of GC (Okaichi et al. 1992). At least two other karyotic receptor-regulated pathways, including chemo- components are required for AC activation in Dictyo- taxis in mammalian cells (Devreotes and Zigmond stelium: the MAP kinase ERK2 and a cytosolic protein, 1988). cAMP binds to classic serpentine cell-surface re- CRAC (Lilly and Devreotes 1994; Segall et al. 1995). ceptors (cAMP receptors or cARs) that couple to the het- CRAC has a pleckstrin domain, suggesting that it inter- erotrimeric G protein containing the G~ subunit Ga2 acts with another protein, possibly the G[~ subunit (In- (Fig. 2). Three second-messenger pathways are activated: sall et al. 1994a; Touhara et al. 1994). MAP kinases are guanylyl cyclase (GC), phospholipase C (PLC), and AC known to be activated through both receptor tyrosine (Devreotes 1994). AC activity peaks at -90 sec and then kinases and G protein-coupled receptors (Davis 1993; adapts, whereas GC and PLC peak and adapt more rap- Errede and Levin 1993; Blumer and Johnson 1994) but idly (10 and 7 sec, respectively). Continuous fluxes of have not been known previously to be required for the cAMP cause a single, transient activation of these path- activation of AC. ways, followed by the eventual down-regulation of the Activation of GC and production of cGMP have been receptors. Analysis of null strains indicates that the re- linked to chemotaxis and the membrane-associated ceptor and the G protein are essential for these responses polymerization of actin and myosin, similar to pathways in vivo (Kumagai et al. 1989, 1991; Kesbeke et al. 1990; mediating chemotaxis in mammalian cells (McRobbie Sun and Devreotes 1991; Wu et al. 1995). cAR1, the most and Newell 1984; Devreotes and Zigmond 1988; Liu et abundant cAR during aggregation, has a high affinity for al. 1993). Mutations affecting the GC/cGMP pathway cAMP and is able to respond to the low concentrations of result in cells that are not capable of chemotaxis or that cAMP present during the early stages (Johnson et al. show altered chemotaxis but activate AC normally 1992; Insall et al. 1994b). cAR3, a lower affinity cAR, can (Newell and Liu 1992; Kuwayama et al. 1993). The gene replace cAR1; however, higher concentrations of cAMP encoding PLC has been disrupted, but there is no devel- are required to activate the responses (Insall et al. 1994a). opmental phenotype, suggesting that PLC activity is not This indicates that multiple cARs couple to G~2 and can required for aggregation or other stages in development regulate the same signaling pathways. (Drayer et al. 1994). For a more detailed analysis, the The activation of AC is regulated via a fairly
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