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Reticulomyxa: a New Model System of Intracellular Transport

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Reticulomyxa: a New Model System of Intracellular Transport y. Cell Sci. Suppl. 5, 145-159 (1986) 145 Printed in Great Britain © The Company of Biologists Limited 1986 RETICULOMYXA: A NEW MODEL SYSTEM OF INTRACELLULAR TRANSPORT MICHAEL P. KOONCE, URSULA EUTENEUER a n d MANFRED SCHLIWA Department of Zoology, University of California, Berkeley, CA 94720, USA SUMMARY Reticulomyxa is a large multinucleated freshwater protozoan that provides a new model system in which to study intracellular transport and cytoskeletal dynamics. Within the cell body and reticulopodial network, rapid, visually striking saltatory organelle motility as well as bulk cytoplasmic streaming can be readily observed. In addition, the cytoskeletal elements within these strands undergo dynamic splaying and fusing rearrangements, which can be visualized by video­ enhanced light microscopy. A reactivatable lysed cell model has been developed that appears to preserve, and therefore permits examination of, these three forms of motility in a more controlled environment. Individual organelle movements are microtubule-based and have similarities to, but also differences from, the recently described kinesin-based transport. This lysed cell model can be further manipulated to provide native, ordered, completely exposed networks of either microtubules or microfilaments, or a combination of both, and thus may serve as a versatile motility assay system in which to examine the movement of exogenously added isolated organelles or latex beads. INTRODUCTION The transport of organelles from one subcellular region to another is a fundamental process of nearly every eukaryotic cell. Many pharmacological and correlative light- and electron-microscopical studies have demonstrated that microtubules and microfilaments play an integral role in this phenomenon (reviewed by Schliwa, 1984). In general, the directed, often saltatory, movement of individual organelles is representative of microtubule-based transport systems in animal cells including neurons (Allen et al. 1982; Brady & Lasek, 1982; Smith et al. 1975), chromatophores (Murphy & Tilney, 1974; Schliwa, 1982), cultured cells (Hayden et al. 1983) and protozoans (Travis et al. 1983). Recent detailed studies of organelle-microtubule interactions in the squid giant axon have resulted in the identification and isolation of at least one novel microtubule-associated translocator, kinesin (Vale et al. 1985a). On the other hand, microfilament (or actomyosin)-based transport is most common in plant cells as an often rapid bulk streaming of cytoplasm (Kamiya, 1981). The characean green algae have served as especially useful models for such transport (Sheetz & Spudich, 1983; Kachar, 1985). There is not, however, a simple dichotomy between plant and animal organelle transport systems, since examples of microtubule-based movements in plants (Gunning & Hardham, 1982; Menzel & Schliwa, 1986) and the involvement of microfilaments in these processes in animal cells (Brady et al. 1984) have been reported. However, little is known regarding the association and possible interaction of these two transport systems 146 M. P. Koonce, U. Euteneuer and M. Schliwa within the same cell (see, however, Burnside & Nagle, 1983; Menzel & Schliwa, 1986). Can they act together in a coordinate fashion or do they always mediate separate and distinct forms of motility? If the two mechanisms are usually separate, can one act in a role that is supportive of the other? In addition, are transport mechanisms universal and in what ways might they be tailored to a particular cell type? Here we describe a new, versatile model system of intracellular transport that will permit examination of these questions. Reticulomyxa is a giant freshwater protozoan with striking intracellular transport. Both directed saltatory organelle movements and bulk cytoplasmic streaming are found within the cell body and a peripheral reticulopodial network of fine strands (Koonce et al. 1986). The large size of this organism, the speed and extent of these two forms of organelle movement, and the structural simplicity and order of the cytoskeleton make Reticulomyxa a good candidate for studies not only on the mechanisms of intracellular transport, but also on the interactions between, and functions of, the two organelle transport systems within the same cell. This paper reviews some of the unique morphological and structural features of this organism and describes the development of a reactivatable lysed cell model that preserves both saltatory and streaming-like forms of motility. With this model system, it is possible to address questions about the independent functions of each cytoskeletal system as well as their cumulative action in organelle transport. MATERIALS AND METHODS Reticulomyxa culture Reticulomyxa (Nauss, 1949) was found growing on the sides and bottom of a freshwater aquarium. It is easily maintained and can be grown to large amounts (several ml of packed cells per week) in Petri dishes on a diet of either flaked fish food (TetraMin) or wheat germ. Twice weekly, dishes are cleaned of debris and refilled with fresh tap water. Food is added as needed. Under crowded conditions, organisms stream up the sides of dishes and onto the undersurface of the air-water interface, where they continue to thrive. Light microscopy For light-microscopic experiments, small pieces of cell body were placed on coverslips in Petri dishes containing either tap water or lOmM-Hepes, 2mM-MgCl2, pH 7-0 and permitted to attach and extend networks (usually < 1 h). The coverslips were then inverted onto slides with coverslip pieces as spacers. The longitudinal sides of this sandwich were sealed with VALAP, leaving the ends open for perfusion of solutions. Preparations were viewed in a Zeiss Photomicroscope III equipped with phase-contrast, polarization, or differential interference contrast (DIC) optics. For video enhancement, images were projected into a Dage-MTI series 67 videocamera (Dage-MTI Inc., Michigan City, IN) and further manipulated with an Interactive Video Image 1 processor (Interactive Video, Concord MA) as described elsewhere (Koonce & Schliwa, 1986). Low light level images were obtained with a Dage-MTI ISIT camera. Real time recordings were made with a Panasonic VHS recorder (nv-8050) and photographs of the enhanced images were taken directly from the video monitor with a 35 mm camera and Kodak Plus-X film. For lysis, preparations were perfused with 5% hexylene glycol, 1 mM-sodium ortho vanadate, and 0-15% Brij 58 in a buffer consisting of 30mM-Pipes, 12-5 % Hepes, 4mM-EGTA, and 1 mM-MgCl2 (50% PHEM; Schliwa & van Blerkom, 1981), at pH7-0. Movement was immediately arrested, and thin regions of network were completely lysed within 1 min. Preparations were then rinsed with buffer alone followed by the experimental solutions. All experiments were performed at room temperature. Reticulomyxa: a model of intracellular transport 147 Immunofluorescence Lysed preparations were fixed with 1 % glutaraldehyde, rinsed with buffer, and processed as described (Koonce et al. 1986). Monoclonal tubulin antibodies made against Drosophila alpha tubulin were kindly provided by Dr Margaret Fuller. Microfilaments were visualized with rhodamine-phalliodin, kindly provided by Dr T. Wieland. Electron microscopy For whole-mount preparations, networks extended on Formvar-coated gold finder grids were either fixed directly, or lysed and then fixed with 1 % glutaraldehyde in 50% PHEM, pH 7-0, and processed as described (Koonce & Schliwa, 1986). Preparations were viewed in a Kratos high- voltage electron microscope (National Center For Electron Microscopy, Lawrence Berkeley Laboratories) operated at 1500kV. Stereo pairs were taken with tilt angles of 12°. Bead experiments Reticulomyxa supernatant was prepared by homogenization of cell bodies at 0°C in a Dounce homogenizer in PHEM buffer supplemented with 40mM-beta-glycerophosphate, 20/igml-1 DNase I, 2mM-ATP, and a protease inhibitor cocktail of 40jugml soybean trypsin inhibitor II, 40/igml-1 L-l-tosylamide-2-phenyl-ethylchloromethyl ketone (TAME), 40jUgml-1 benzyl arginyl- methyl ester (BAME), 4ugmP1 leupeptin, 4/igml_1 pepstatin, 200 Mg ml-1 antipain, lmM-phenyl- methylsulphonyl fluoride (PMSF), and 0-2 TI units ml-1 aprotinin. The homogenate was spun for 15 min at 80 OOOg in a Beckman airfuge at 2°C. The clear supernatant was removed by aspiration, avoiding both the pellet and the floating layer of lipid. Protein concentration of this supernatant was approximately l-2mgml_1. Carboxylated latex beads 0-19/um in diameter (Polyscience Inc., Warrington, PA) were incubated in this supernatant for 15 min at 0°C and either added directly to the lysed-stripped networks (including supernatant), or first rinsed twice in buffer alone, then added. Beads were also incubated in 1 mg ml-1 bovine serum albumin as a control. RESULTS Reticulomyxa is a giant multinucleated protozoan (Class Rhizopoda, Order Granuloreticulosea; Levine et al. 1980) consisting of a large naked cell body of thick interconnected strands 50-200 [im in diameter (Fig. 1A,B) surrounded by a dynamic, highly reticulate network of fine strands (Fig. 1C). Typical individuals cover an area from 1-4 cm2 but often form contiguous arrays many times larger. Conspicuous within both the cell body and reticulopodial network are rapid organelle movements. Constant bulk cytoplasmic streaming, which carries organelles, vacuoles and nuclei at rates of up to 20 jim s-1 is prominent within, though not confined to, the cell body. Streaming is bidirectional, often with several ‘lanes’ of countercurrent
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