DEVELOPMENTAL GENETICS 11:32%332 (1990)

Actin-Associated Proteins in Dictyostelium discoideum ELIZABETH J . LUNA AND JOHN S. CONDEELIS Cell Biology Group, Worcester Foundation for Experimental Biology, Shrewsbury, Massachusetts (E.J.L.), and Department of Anatomy and Structural Biology, Albert Einstein College of Medicine, Bronx, New York (J.S.C.)

ends [Hartmann et al., 1989; Schleicher et al., 19841. Filament cutting proteins, such a s D. discoideum severin [Brown et al., 1982; Yamamoto et al., 19821, may be thought of a s overly-zealous capping proteins. In the presence of micromolar calcium ions, severin fragments actin filaments and then binds to the increased numbers of barbed filament ends (Fig. 1)[Giffard et al., 1984; Yamamoto et al., 19821. A second class of actin-binding proteins interacts with the sides of actin filaments. Bundling proteins, which are usually relatively small, cross-link actin filaments into highly organized, parallel arrays (for instance, see Furukawa and Fechheimer, 19901. At least Key words: Cellular slime molds, cytoskeleton, three actin-bundling proteins are present in D. discoiactin-binding proteins, review deum (Fig. 1); two (p30a and p30b) have apparent molecular masses of 30,000 daltons on SDS-gels and one (APB-50) electrophoreses with a n apparent Mr of INTRODUCTION 50,000. p30a is a calcium-sensitive actin cross-linking During the last decade, there has been a n explosion protein that bundles actin filaments in the absence of detailed knowledge about the proteins involved in ( [ C a + + ]= lo-' M), but not in the presence, of microDictyostelium chemotaxis and adhesion. The molecular molar-free calcium ions [Fechheimer and Taylor, basis for the recognition of extracellular CAMP and 19841. p30b [Brown, 19851, and ABP-50 [Condeelis et many of the biochemical processes in the signal trans- al., 1990; Demma et al., 19901 are calcium-insensitive duction pathway have been elucidated (for instance, actin bundling proteins that are immunologically dissee sections on Signal Transduction and Gene Regula- tinct from p30a. p30a [Fechheimer, 1987; Johns et al., tion in Volume 12, Nos. 112). The active site of gp80, a 19881 and ABP-50 [Demma et al., 19901 also are assoprotein responsible for one of the major developmen- ciated with actin bundles in filopodia and other orgatally regulated cell-cell adhesion mechanisms, has nized arrays of actin filaments in vivo. Dictyostelium been localized to a peptide of just 8 residues [Kamboj et alpha-actinin is a calcium- and pH-regulated actin al., 1989; Siu and Kamboj, 19901. Finally, many of the cross-linking protein with a n in vitro filament buncytoskeletal proteins involved in cellular responses to dling activity that is disrupted by micromolar concenchemotactic and adhesive stimuli have been described trations of free calcium ions or by pH's >7 [Condeelis in detail. In Dictyostelium, components of the actin- and Vahey, 1982; Fechheimer et al., 19821. In vivo, albased cytoskeleton are involved in the cell responses, pha-actinin is found in patches throughout the cytoe.g., pseudopod extension, t h a t follow stimulation by plasm and in the hyaline cytoplasm of pseudopods cell contact or chemotactic factors [Condeelis et al., [Brier et al., 1983; Carboni and Condeelis, 19851, local19901. The effects of many of these proteins on actin izations suggestive of incorporation into actin strucfilament structure in vitro are schematized in Figure 1. One class of these actin-associated proteins are proteins that bind to a n end of the actin filament. Capping proteins, such a s the heterodimeric cap 32/34 [see Hartmann et al., 19901 bind to the so-called barbed end of Received for publication May 1, 1990; accepted July 27, 1990. the actin filament, the preferred end for filament elongation. Cap 32/34 binding to actin, which is indepen- Address reprint requests to Elizabeth J. Luna, Worcester Foundation dent of the presence of calcium ions, inhibits filament for Experimental Biology, 222 Maple Avenue, Shrewsbury, MA elongation by blocking monomer addition to the barbed 01545. The cellular slime mold DictyABSTRACT ostelium discoideum is becoming the premier system for the explication of the biochemical and cellular events that occur during motile processes. Proteins associated with the actin cytoskeleton, in particular, appear to play key roles in cellular responses to many external stimuli. This review summarizes our present understanding of the actinassociated proteins in Dictyostelium, including their in vitro activities and their structural and/or functional analogues in mammalian cells.

0 1990 WILEY-LISS, INC.

ACTIN-ASSOCIATED PROTEINS IN DICTYOSTELIUM

329

Sequeitezng Proteins

I End-on Membrane Attachment (P247)

@.

0 . : 0 .

'

0

Capping Proteins (Cap 32/34)

G-actin

@

8

@ /

+ ca++

Lateral Membrane Attachment

@ +-

Severing (Severin) Proteins

(Ponticulin, ABP-240?, ABP-220?, histactophilin?)

Actin Filaments

Bundling Proteins (p30a - Ca't p30b, ABP-50) Membrane-bound Motors (Myosin I)

4-

4+

MgATP

Contractile Proteins

(Myosin II)

Cross-linking Proteins (ABP-240, ABP-220, ABP-120,a -actinin - Ca++)

Fig. 1. Schematic diagram summarizing the effects on actin structure produced by actin-binding proteins known to be present in D.discoideum.

tures (Fig. 1).Other D. discoideum cytoplasmic proteins exhibiting cortical cytoplasmic localizations and the ability to cross-link actin filaments in vitro include ABP-120 [Condeelis et al., 1981, 1982; Ogihara et al., 19881 and ABP-240 [Hock and Condeelis, 19871. D. discoideum amebae contain at least two types of myosin. The two-headed myosin (myosin 11) is structurally similar to conventional muscle myosin; it is a hexamer, consisting of a pair of 210,000-dalton heavy chains and two 18,000-dalton and two 16,000-dalton light chains [Clarke and Spudich, 19741. Myosin II's actin-activated ATPase activity is potentiated by phosphorylation of the 18,000-dalton light chain [Griffith et al., 19871. Phosphorylation of the heavy chain controls the assembly of this protein into short bipolar filaments capable of interacting with two or more actin filaments [Kuczmarski and Spudich, 1980; Kuczmarski, 1986; C6te and Bukiejko, 19871. By immunofluorescence microscopy, myosin I1 is localized throughout the cytoplasm and cortex of rounded cells, at the pos-

terior of polarized amebae, and i n the cleavage furrow of dividing cells [Fukui et al., 1989; Fukui and Yumura, 1986; Rubino et al., 1984; Yumura et al., 19841. Upon chemotactic stimulation, developed amebae exhibit a transient translocation of myosin I1 to the region of the cortex immediately subjacent to the plasma membrane [Nachmias et al., 1989; Yumura and Fukui, 19851. Electron microscopic localizations of myosin filaments support the cortical localization of myosin I1 [Clarke and Baron, 19871 and suggest that this protein is associated with cytoplasmic vesicles [Ogihara et al., 19881. Myosin I1 association with vesicles is supported by the observation that a myosin I1 null mutant exhibits a depressed rate of vesicle movement a s well as slower rates of cellular translocation (see Sol1 et al., 1990). Gene deletion studies indicate that myosin I1 is required for proper cytokinesis, capping of cell surface receptors, efficient chemotaxis, and morphogenetic changes occurring late in development (reviewed in Spudich, 1989).

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LUNA AND CONDEELIS

D. discoideum myosin I is a single-headed myosin that contains only one heavy chain of about 117,000 daltons and a n unknown number of light chains [C6te et al., 19851. Myosin I does not form bipolar filaments and is found a t the leading edges of locomoting amebae [Fukui et al., 19891, suggesting that this protein, like myosin I in Acanthamoeba castellanii [Adams and Pollard, 1989; Miyata et al., 19891, may mediate the sliding of membranes along actin filaments (and vice versa) during pseudopod extension. Other actin-based motor proteins also may exist in Dictyostelium but are known a t present only from deduced cDNA sequences [Titus et al., 19891. Electron microscopic analyses of the interface between the cortical cytoskeleton and the plasma membrane in D. discoideum show contacts between the membrane and the sides, a s well a s the ends, of actin filaments [Bennett and Condeelis, 1984; Goodloe-Holland and Luna, 19841. Filaments that bind the plasma membrane end-on do so at their barbed ends [Bennett and Condeelis, 19841; laterally-associated actin filaments are either tightly apposed to the membrane [Goodloe-Holland and Luna, 1984; Luna et al., 19891or linked via rod-shaped bridges about 15 nm in length [Bennett and Condeelis, 19841. Ponticulin, a 17,000dalton transmembrane glycoprotein [Wuestehube and Luna, 19871, is a candidate polypeptide for the mediation of close associations between the membrane and the sides of actin filaments (see Luna et al., 1990). A cytoplasmic domain of ponticulin binds directly to F-actin [Wuestehube and Luna, 1987; Chia et al., in preparation] and this protein is required for the actin nucleation activity of purified plasma membranes [Shariff and Luna, 19901. Actin-binding proteins that are peripherally-associated with plasma membranes include ABP-240 and ABP-220 [Bennett and Condeelis, 1988; Condeelis et al., 19881. The localization of these large, elongated proteins to the cell periphery and the recognition of ABP-240 and ABP-220 by antibodies directed against chicken filament and fodrin, respectively [Bennett and Condeelis, 1988; Hock and Condeelis, 19871, suggest that these proteins are likely to be components of at least some of the lateral bridges observed between actin filaments and the membrane. Histactophilin, a 17,000-dalton peripheral membrane protein [Schleicher et al., 19841, is thought to bind along the length of the actin filament below, but not above, pH 7.2 [Scheel et al., 19891. Thus, changes in intracellular pH could regulate histactophilin-mediated lateral linkages between actin filaments and the membrane. No protein has yet been proposed as a component of the end-on linkages between actin filaments and membranes. However, a 24,000-dalton membrane protein known a s p24 binds both monomeric actin and actin filaments in vitro [Stratford and Brown, 19851, dual activities t h a t are characteristic of cytoplasmic capping proteins (see above).

The D. discoideum cytoskeletal proteins described here appear to be very similar to actin-binding proteins isolated from other organisms. For instance, molecular cloning has demonstrated a large degree of homology among sequences at the amino-termini of Dictyostelium alpha-actinin, chicken fibroblast alpha-actinin, ABP-120, and human dystrophin [Noegel et al., 1987, 19891. This evolutionarily-conserved domain recently has been shown to contain a n actin binding site t h a t may be a general motif of actin filament cross-linking proteins [Bresnick et al., 19901. Also, regions of amino acid sequence conservation have been reported for Dictyostelium severin, Physarum fragmin, human gelsolin, and chicken villin [Andre et al., 1988; Schleicher et al., 19881. As these proteins are all calcium-activated F-actin severing proteins, i t is likely that the regions of highest sequence similarity are involved directly in severing actin filaments. Similarly, as reported by Hartmann et al. [1990], Dictyostelium cap 32134 appears to be a member of a group of highly conserved heterodimeric actin capping proteins. In addition, regions of homology among the myosin polypeptides, particularly in the actin- and ATP-binding head domains, have been reported [Chisholm et al., 1988; J u n g et al., 1989; Tafuri et al., 1989; Titus et al., 1989; Warrick et al., 19861. Of the Dictyostelium actin-binding proteins in Figure 1 for which the cDNA sequence is not yet available, antigenic cross-reactivity has been used to demonstrate the existence of vertebrate analogues of p30a [Johns et al., 19881, ponticulin [Wuestehube et al., 19891, ABP-240 (filamin) [Condeelis et al., 1988; Hock and Condeelis, 19871, and ABP-220 (fodrin) [Bennett and Condeelis, 1988; also see Furukawa and Fechheimer, 19901. Over the next few years, even more actin-binding proteins should be discovered and characterized in Dictyostelium. For instance, no one has yet described the Dictyostelium analogues of actin monomer sequestering proteins, such as profilin [Pollard and Cooper, 1986; Stossel, 19891. Yet, almost half of the cytoplasmic actin in Dictyostelium (nearly 50 pM) is nonfilamentous [Podolski and Steck, 19901; this concentration is nearly two orders of magnitude higher than is possible in the absence of monomer-sequestering proteins. Furthermore, these proteins are ubiquitous and have been isolated from eukaryotes ranging from yeast through Acanthamoeba to vertebrate spleen and brain [Pollard and Cooper, 19861. Another group of proteins that are missing from Figure 1 (but which should exist in Dictyostelium) are proteins, such as tropomyosin [Broschat et al., 19891 and tropomodulin [Fowler, 19871, that regulate the stability of actin filaments. Although much work still remains to be done on the biochemical characterization of cytoskeletal proteins in Dictyostelium, the emphasis in the future will shift to correlating the activities of cytoskeletal proteins in vitro with their functions in vivo. One useful approach is to correlate biochemical changes in cytoskeletal com-

ACTIN-ASSOCIATED PROTEINS IN DICTYOSTELIUM position and activity with morphological changes following chemotactic stimulation [Condeelis et al., 19901. The techniques of gene disruption and inhibition of gene function by antisense RNA are being used to elucidate the cellular functions of myosin I, myosin 11, severin, and alpha-actinin [De Lozanne, 1989; J u n g and Hammer, 1989; Knecht, 1989; Noegel et al., 1989; Spudich, 19891. Finally, the behavioral analysis of mutants in one or more cytoskeletal proteins is another potent approach to the elucidation of function in vivo [Gerisch et al., 19891. The future is likely to see refinements of each of these approaches including technological advances in plasmid construction, control of insert expression, and the development of mutants with temperature-sensitive defects in cytoskeletal functions. Although components of the actin-based cytoskeleton have been stressed here, it is clear that the microtubule-based motors, dynein [Koonce and McIntosh, 19901and kinesin [McCaffrey and Vale, 19891, also will figure in our eventual comprehensive understanding of cell motility in Dictyostelium.

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Actin-associated proteins in Dictyostelium discoideum.

The cellular slime mold Dictyostelium discoideum is becoming the premier system for the explication of the biochemical and cellular events that occur ...
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