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The Actin Cytoskeleton of Dictyostelium: a Story Told by Mutants

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The Actin Cytoskeleton of Dictyostelium: a Story Told by Mutants Journal of Cell Science 113, 759-766 (2000) 759 Printed in Great Britain © The Company of Biologists Limited 2000 JCS0731 COMMENTARY The actin cytoskeleton of Dictyostelium: a story told by mutants Angelika A. Noegel1,* and Michael Schleicher2 1Institut für Biochemie I, Medizinische Fakultät, Universität zu Köln, Joseph-Stelzmann-Str. 52, 50931 Köln, Germany 2Adolf-Butenandt-Institut für Zellbiologie, Ludwig-Maximilians-Universität, Schillerstr. 42, 80336 München, Germany *Author for correspondence (e-mail: [email protected]) Published on WWW 14 February 2000 SUMMARY Actin-binding proteins are effectors of cell signalling and development. Furthermore, the studies have identified coordinators of cellular behaviour. Research on the several cellular and developmental stages that are Dictyostelium actin cytoskeleton has focused both on the particularly sensitive to an unbalanced cytoskeleton. In elucidation of the function of bona fide actin-binding addition, use of GFP fusion proteins is revealing the spatial proteins as well as on proteins involved in signalling to the and temporal dynamics of interactions between actin- cytoskeleton. A major part of this work is concerned with associated proteins and the cytoskeleton. the analysis of Dictyostelium mutants. The results derived from these investigations have added to our understanding Key words: Actin binding protein, Cell signalling, Chemotaxis, of the role of the actin cytoskeleton in growth and Morphogenesis, GFP fusion protein INTRODUCTION antisense strategies, restriction-enzyme-mediated integration (REMI), transposon-tagging-like mutagenesis, and expression The actin cytoskeleton of a cell is required for cell-shape of GFP fusion proteins. The 34-Mb genome is carried on six changes, cell motility and chemotaxis, as well as for chromosomes. The Dictyostelium genome project (see cytokinesis, intracellular transport processes, development and http://www.uni-koeln.de/dictyostelium/) should be completed signal transduction. It is composed of actin and associated by 2002; however, information on more than 90% of the genes proteins. Their interactions are highly dynamic, and constant is already available. reorganization of the actin network is required for it to perform Dictyostelium is therefore a valuable and convenient its functions. experimental system for studies of the role of the actin Dictyostelium has been a model system for the analysis of cytoskeleton in cell motility, chemotaxis, signal transduction, the actin cytoskeleton for some time now, and research in this development and differentiation. Here, we highlight new field has contributed to a general understanding of the structure developments in three areas: (1) cytoskeletal dynamics at leading and function of cytoskeletal proteins (for reviews see Schleicher fronts, where experiments with GFP fusion proteins provided and Noegel, 1992; Noegel and Luna, 1995). Dictyostelium has spectacular data on chemotaxis, cell movement, phagocytosis several features that make it especially well suited to studies of and pinocytosis (Maniak et al., 1995; Parent et al., 1998); (2) the the actin cytoskeleton. It is a unicellular amoeba that lives as a roles of actin and actin-binding proteins as effectors of cell natural phagocyte and feeds on yeast and bacteria. When cells signalling; (3) coordination of cellular behaviour by actin and starve, development is initiated, and cells aggregate by actin-binding proteins, where the genome project aided the chemotaxis in response to relayed cAMP signals. Once the identification of new components that reveal additional roles for amoebae have aggregated, they form a multicellular organism the actin cytoskeleton. Moreover, we try to give an update on that in its slug form can migrate towards light and orient in a components of the actin cytoskeleton and putative regulatory thermotactic gradient. During development, cells differentiate components, and their impact on cell biology – as taken from into spore and stalk cells and, finally, a fruiting body is mutant analysis (Table 1). Structural analyses of cytoskeletal constructed. In the laboratory this program is completed within proteins have also made significant contributions; these studies, 24 hours. Multicellularity requires specific cell interactions, however, are beyond the scope of this Commentary. extracellular signals and the corresponding receptors, as well as various signal transduction pathways. Dictyostelium is haploid. This facilitates isolation of mutants DYNAMIC EVENTS AT LEADING FRONTS but makes it difficult to study essential genes. A wide spectrum of molecular genetic techniques is available, including gene Components of the signal transduction pathway inactivation by homologous recombination, gene replacement, Chemotaxis in Dictyostelium requires a cAMP receptor and 760 A. A. Noegel and M. Schleicher Table 1. Mutants in bona fide actin-binding proteins and in components that might be involved in regulation of the actin cytoskeleton Protein Exp. approach Phenotype References α-actinin Knock-out Reduced resistance to shear stress; growth defect under different osmotic conditions; Eichinger et al., 1996; in combination with gelation factor: development arrested at mound stage; small Witke et al., 1992; cell size, motility defect, orientation defect, sensitivity to osmotic shock Rivero et al., 1996a Akt/PKB Knock-out Aberrant chemotaxis, polarisation defect, aggregation-minus at low cell densities Meili et al., 1999 34-kDa bundling protein Knock-out Reduced growth rate at low temperatures, persistence of motility increased Rivero et al., 1996b Calmodulin Antisense Cytokinesis Liu et al., 1992 CAP/ASP56 Knock-out Cell morphology altered, cytokinesis defect, endocytosis defect, reduced motility, Noegel et al., 1999 delay in development Capping protein Antisense Reduced motility; Hug et al., 1995 (cap 32/34) overexpression increased motility, cytoskeletal architecture altered Clathrin heavy chain Knock-out Pinocytosis, cell type differentiation, cytokinesis O’Halloran and Anderson, 1992; Niswonger and O’Halloran, 1997a,b Cofilin Overexpression Stimulation of actin bundling, membrane ruffles, cell movement, reorganises actin Aizawa et al., 1996 into bundles that, in concert with DAip1, contract in a myosin independent way in and 1999 response to hyperosmotic stress Coronin Knock-out Cytokinesis defect, phagocytosis defect, motility defect de Hostos et al., 1993; Maniak et al., 1995 Cortexillin I Knock-out Developmental arrest in Polysphondylium Fey and Cox, 1999 Cortexillin I and II Knock-out Cell shape altered, cytokinesis defect Faix et al., 1996 DAip1 Knock-out Impaired growth, endocytosis, phagocytosis and movement, slight cytokinesis defect Konzok et al., 1999 DdLim Overexpression Formation of large lamella, increased ruffling, multinucleated cells Prassler et al., 1998 DdMEK1 Knock-out Chemotaxis defect, aggregation defect, small aggregates formed Ma et al., 1997 DGAP1 Knock-out F-actin level increased; Faix et al., 1998 overexpressor cellular projections suppressed, speed of motility reduced Discoidin Conventional mutant No elongated morphology Alexander et al., 1992 ERK1 Antisense, knock-out Essential for vegetative growth, morphogenesis and cell-type differentiation; Gaskins et al., 1994 overexpression abnormal expression from slug stage on, abnormal morphogenesis in combination and 1996 with PTP2 ko GEF (aimless) Knock-out Chemotaxis defect, aggregation defective Insall et al., 1996 Gelation factor (ABP120) Knock-out Actin cross-linking affected, cytoskeletal structure altered, pseudopod number and Cox et al., 1996; size altered, cell motility, chemotaxis and phagocytosis impaired; phototaxis defect Fisher et al., 1997 G-protein β subunit Knock-out Aggregation minus, chemotaxis defect, phagocytosis defect, no transient actin Lilly et al., 1993; polymeristaion upon stimulation by chemoattractant Peracino et al., 1998 GRP125 Knock-out Phototaxis defect Stocker et al., 1999 Hisactophilin I and II Knock-out Resistance of cells to acidification reduced; Stoeckelhuber et al., overexpression of hisII resistance of cells to acidification increased 1996 IQGAP Knock-out Completion of cytokinesis affected Adachi et al., 1997 Myosin I (A,B, C) Knock-out Multiple knock-outs: fluid phase endocytosis impaired, membrane internalisation Novak et al., 1995; overexpression impaired, rearrangement of cortical actin-rich structures impaired, cortical tension Jung, G. et al., 1996; reduced; overexpressors: cell velocity reduced, delay in aggregation Novak and Titus, 1997; Dai et al., 1999 Myosin II heavy chain Knock-out Cortical motile activities impaired, cytokinesis defect, development arrested at De Lozanne and antisense mound stage Spudich, 1987; Knecht and Loomis, 1987; Fukui et al., 1990 Myosin II heavy chain Knock-out Partial defects in myosin localization; Kolman et al., 1996 kinase overexpression growth in suspension reduced, size increased, multinuclearity, arrest at mound stage Myosin essential light Antisense Increased cell size, multinuclearity, developmental arrest Pollenz et al., 1992 chain (ELC) Myosin regulatory light Knock-out Increased cell size, multinuclearity, developmental arrest Chen et al., 1994 chain (RLC) Myosin VII Knock-out Phagocytosis reduced by 80% Titus, 1999 PAKa Knock-out Cytokinesis in suspension defect, formation of lateral pseudopods not suppressed, Chung and Firtel, 1999 direction of cell movement impaired, myosin II assembly defect PI3 kinases Knock-out Macropinocytosis defect, deficits in certain F-actin-enriched
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