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Vol. 14, Issue 10, 3953-3966, October 2003

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Actin Filament Turnover Regulated by Cross-linking Accounts for the Size, Shape, Location, and Number of Actin Bundles in Drosophila Bristles

Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6018

Submitted March 18, 2003; Revised June 16, 2003; Accepted June 23, 2003
Monitoring Editor: Anthony Bretscher

Drosophila bristle cells are shaped during growth by longitudinal bundles of cross-linked actin filaments attached to the plasma membrane. We used confocal and electron microscopy to examine actin bundle structure and found that during bristle elongation, snarls of uncross-linked actin filaments and small internal bundles also form in the shaft cytoplasm only to disappear within 4 min. Thus, formation and later removal of actin filaments are prominent features of growing bristles. These transient snarls and internal bundles can be stabilized by culturing elongating bristles with jasplakinolide, a membrane-permeant inhibitor of actin filament depolymerization, resulting in enormous numbers of internal bundles and uncross-linked filaments. Examination of bundle disassembly in mutant bristles shows that plasma membrane association and cross-bridging adjacent actin filaments together inhibits depolymerization. Thus, highly cross-bridged and membrane-bound actin filaments turn over slowly and persist, whereas poorly cross-linked filaments turnover more rapidly. We argue that the selection of stable bundles relative to poorly cross-bridged filaments can account for the size, shape, number, and location of the longitudinal actin bundles in bristles. As a result, filament turnover plays an important role in regulating cytoskeleton assembly and consequently cell shape.

^* Corresponding author. E-mail address: gguild{at}sas.upenn.edu.

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