Why Are Two Different Cross-linkers Necessary for Actin Bundle Formation In Vivo and What Does Each Cross-link Contribute?

doi:10.1083/jcb.143.1.121

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© The Rockefeller University Press, 0021-9525/1998//121 $5.00
The Journal of Cell Biology, Volume 143, Number 1, , 1998 121-133

Regular Articles

Why Are Two Different Cross-linkers Necessary for Actin Bundle Formation In Vivo and What Does Each Cross-link Contribute?

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

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

In developing Drosophila bristles two species of cross-linker,the forked proteins and fascin, connect adjacent actin filamentsinto bundles. Bundles form in three phases: (a) tiny bundlesappear; (b) these bundles aggregate into larger bundles; and(c) the filaments become maximally cross-linked by fascin. Inmutants that completely lack forked, aggregation of the bundlesdoes not occur so that the mature bundles consist of <50filaments versus $~$ 700 for wild type. If the forked concentrationis genetically reduced to half the wild type, aggregation ofthe tiny bundles occurs but the filaments are poorly orderedalbeit with small patches of fascin cross-linked filaments.In mutants containing an excess of forked, all the bundlestend to aggregate and the filaments are maximally crossbridged by fascin. Alternatively, if fascin is absent, phases 1 and 2 occur normally but the resultant bundles are twisted andthe filaments within them are poorly ordered. By extractingfully elongated bristles with potassium iodide which removesfascin but leaves forked, the bundles change from being straightto twisted and the filaments within them become poorly ordered.From these observations we conclude that (a) forked is usedearly in development to aggregate the tiny bundles into largerbundles; and (b) forked facilitates fascin entry into the bundlesto maximally cross-link the actin filaments into straight, compact,rigid bundles. Thus, forked aligns the filaments and then directsfascin binding so that inappropriate cross-linking does notoccur.

Key Words: actin • Drosophila • bristles • cross-links • fascin • forked

Many thanks to N. Petersen and L. Cooley for their gifts offly strains and antibodies against the forked protein and fascin,respectively. We are especially grateful to M. Mooseker whofor two summers gave advice, encouragement, space, and equipmentwhile L.G. Tilney was in Woods Hole. We would also like tothank the reviewers of this manuscript for fair and just criticism,and our editor D. DeRosier (Brandeis University) for helpingto improve the manuscript.

Address all correspondence to G. Guild, Department of Biology,University of Pennsylvania, Philadelphia, Pennsylvania 19104.Tel.: (215) 898-6388. Fax: (215) 898-8780. E-mail: gguild{at}sas.upenn.edu

1. Abbreviation used in this paper: KI, potassium iodide.

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