Espin cross-links cause the elongation of microvillus-type parallel actin bundles in vivo

doi:10.1083/jcb.200309093

Published online 1 December 2003. doi:10.1083/jcb.200309093

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© The Rockefeller University Press, 0021-9525/2003/12/1045 $8.00
The Journal of Cell Biology, Volume 163, Number 5, 1045-1055

Article

Espin cross-links cause the elongation of microvillus-type parallel actin bundles in vivo

Patricia A. Loomis, Lili Zheng, Gabriella Sekerková, Benjarat Changyaleket, Enrico Mugnaini and James R. Bartles

Department of Cell and Molecular Biology, Feinberg School of Medicine, and Institute for Neuroscience, Northwestern University, Chicago, IL 60611

Address correspondence to James R. Bartles, Dept. of Cell and Molecular Biology, Ward Building 11-185, Feinberg School of Medicine, Northwestern University, 303 East Chicago Ave., Chicago, IL 60611. Tel.: (312) 503-1545. Fax: (312) 503-7912. email: j-bartles{at}northwestern.edu

The espin actin-bundling proteins, which are the target of thejerker deafness mutation, caused a dramatic, concentration-dependentlengthening of LLC-PK1-CL4 cell microvilli and their parallelactin bundles. Espin level was also positively correlated withstereocilium length in hair cells. Villin, but not fascin orfimbrin, also produced noticeable lengthening. The espin COOH-terminalpeptide, which contains the actin-bundling module, was necessaryand sufficient for lengthening. Lengthening was blocked by 100nM cytochalasin D. Espin cross-links slowed actin depolymerizationin vitro less than twofold. Elimination of an actin monomer-bindingWASP homology 2 domain and a profilin-binding proline-rich domainfrom espin did not decrease lengthening, but made it possibleto demonstrate that actin incorporation was restricted to themicrovillar tip and that bundles continued to undergo actintreadmilling at $~$ 1.5 s^-1 during and after lengthening. Thus,through relatively subtle effects on actin polymerization/depolymerizationreactions in a treadmilling parallel actin bundle, espin cross-linkscause pronounced barbed-end elongation and, thereby, make alonger bundle without joining shorter modules.

Key Words: microvilli; stereocilia; hair cell; deafness; jerker

Abbreviations used in this paper: PAB, parallel actin bundle;CL4, LLC-PK1-CL4; CMV, cytomegalovirus; S1, myosin subfragment1; WH2, WASP homology 2.

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