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Acting like Actin

T. Roberts,M. Stewart

Published 2000 in Journal of Cell Biology

ABSTRACT

The crawling movement of eukaryotic cells requires establishment of cell polarity, extension of the leading edge, attachment to the substratum, and retraction of the cell body. Each of these events depends on the dynamics of the actin cytoskeleton that are orchestrated by a host of signaling molecules and actin-binding proteins. Indeed, amoeboid cell motility involves so many biochemical components and requires such precise coordination that it can be difficult to formulate models to account completely for the integration of protrusion, adhesion, and retraction at the molecular level. However, the amoeboid sperm of nematodes are a simpler, more specialized system in which the role usually played by actin has been taken over by the 14-kD major sperm protein (MSP) 1 . This model system has given insights into the general mechanism of how cells crawl, and has indicated that, at least in nematode sperm, locomotion appears to be produced primarily by a pushpull mechanism based on MSP assembly dynamics. Nematode sperm not only provide a unique molecular perspective for studying amoeboid cell motility, but also offer advantages as an experimental system that, in many ways, complement those of actin-based cells. For example, many of the molecules that organize and regulate the actin cytoskeleton have been identified, and attention is shifting to understanding how those molecules interact to produce movement (for reviews see Machesky and Insall, 1999; Svitkina and Borisy, 1999; Borisy and Svitkina, 2000). This task is complicated by the versatility of actin, which, in addition to locomotion, is also engaged in determination of cell shape, establishment of polarity, endocytosis, movement of organelles, rearrangement of surface components, and cytokinesis. Nematode sperm, by contrast, are simple cells that use their MSP motility system exclusively for locomotion. Moreover, in Ascaris sperm, the cytoskeleton is organized so that it can be observed directly in crawling cells. This combination of features has made it possible to take apart and rebuild the MSP machinery and compare its operation to that of actin-based cells as a way of identifying the fundamental principles of amoeboid cell motility. Although nematode sperm contain no F-actin, the cells display the classic features of amoeboid locomotion. For example, Ascaris sperm extend a persistent flattened lamellipodium that attaches to the substrate and pulls along a trailing, organelle-packed cell body. The lamellipodium is packed with filaments that assemble along the leading edge and flow rearward as the cell progresses in the same general pattern observed for the actin cytoskeleton in a number of other crawling cells (for reviews see Mitchison and Cramer, 1996; Theriot, 1996). Indeed, MSPand actinbased cell crawling are so nearly identical that, although the two systems use different sets of molecular components to generate movement, they must employ very similar mechanical principles.

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