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© The Rockefeller University Press, 0021-9525/1997//783 $5.00
The Journal of Cell Biology, Volume 138, Number 4, , 1997 783-797

Article

Actin Filament Cables in Drosophila Nurse Cells Are Composed of Modules That Slide Passively Past One Another during Dumping



Gregory M. Guild, Patricia S. Connelly, Michael K. Shaw, and Lewis G. Tilney

Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104

At a late stage in Drosophila oogenesis, nurse cells rapidly expel their cytoplasm into the oocyte via intracellular bridges by a process called nurse cell dumping. Before dumping, numerous cables composed of actin filaments appear in the cytoplasm and extend inward from the plasma membrane toward the nucleus. This actin cage prevents the nucleus, which becomes highly lobed, from physically blocking the intracellular bridges during dumping. Each cable is composed of a linear series of modules composed of ~25 cross-linked actin filaments. Adjacent modules overlap in the cable like the units of an extension ladder. During cable formation, individual modules are nucleated from the cell surface as microvilli, released, and then cross-linked to an adjacent forming module. The filaments in all the modules in a cable are unidirectionally polarized. During dumping as the volume of the cytoplasm decreases, the nucleus to plasma membrane distance decreases, compressing the actin cables that shorten as adjacent modules slide passively past one another just as the elements of an extension ladder slide past one another for storage. In Drosophila, the modular construction of actin cytoskeletons seems to be a generalized strategy. The behavior of modular actin cytoskeletons has implications for other actin-based cytoskeletal systems, e.g., those involved in Listeria movement, in cell spreading, and in retrograde flow in growth cones and fibroblasts.

Please address all correspondence to Gregory M. Guild, Department of Biology, University of Pennsylvania, Philadelphia, PA 19104. Tel.: (215) 898-3433. Fax: (215) 898-8780. e-mail: gguild{at}sas.upenn.edu

1. Abbreviation used in this paper: S1, subfragment 1 of myosin.

We particularly remember Molly Tilney who edited and word processed this manuscript even though she was terminally ill. Her death devastated us. We thank Velia Fowler for putting up with one of us (L.G. Tilney) while on sabbatical in her laboratory. We also thank Shanika Samarasinghe, Victoria Mukovozov, and Rachel Dubroff for experimental help.


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