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Originally published In Press as doi:10.1074/jbc.C100418200 on August 10, 2001

J. Biol. Chem., Vol. 276, Issue 39, 36163-36167, September 28, 2001
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Tyrosine Phosphorylation of Villin Regulates the Organization of the Actin Cytoskeleton*

Liwei Zhai, Peilin Zhao, Alfredo Panebra, Anthony L. GuerrerioDagger , and Seema Khurana§

From the Department of Physiology, University of Tennessee Health Science Center, Memphis, Tennessee 38163 and the Dagger  Department of Biophysics and Biophysical Chemistry, Johns Hopkins University, Baltimore, Maryland 21205

We have previously shown that tyrosine phosphorylation of the actin-regulatory protein villin is accompanied by the redistribution of phosphorylated villin and a concomitant decrease in the F-actin content of intestinal epithelial cells. The temporal and spatial correlation of these two events suggested that tyrosine phosphorylation of villin may be involved in the rearrangement of the microvillar cytoskeleton. This hypothesis was investigated by analyzing the effects of tyrosine phosphorylation of villin on the kinetics of actin polymerization by reconstituting in vitro the tyrosine phosphorylation of villin and its association with actin. Full-length recombinant human villin was phosphorylated in vitro by expression in the TKX1-competent cells that carry an inducible tyrosine kinase gene. The actin-binding properties of villin were examined using a co-sedimentation assay. Phosphorylation of villin did not change the stoichiometry (1:2) but decreased the binding affinity (4.4 µM for unphosphorylated versus 0.6 µM for phosphorylated) of villin for actin. Using a pyrene-actin-based fluorescence assay, we demonstrated that tyrosine phosphorylation had a negative effect on actin nucleation by villin. In contrast, tyrosine phosphorylation enhanced actin severing by villin. Electron microscopic analysis showed complementary morphological changes. Phosphorylation inhibited the actin bundling and enhanced the actin severing functions of villin. Taken together our data show that tyrosine phosphorylation of villin decreases the amount of villin bound to actin filaments, inhibits the actin-polymerizing properties of villin, and promotes the actin-depolymerizing functions instead. These observations suggest a role for tyrosine phosphorylation in modulating the microvillar cytoskeleton in vivo by villin in response to specific physiological stimuli.

* This work has been supported by grants from the American Digestive Health Foundation (Industry Research Scholar award) and the NIDDK, National Institutes of Health (DK-54755) (to S. K.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ To whom correspondence should be addressed: Dept. of Physiology, University of Tennessee Health Science Center, Nash 402, 894 Union Ave., Memphis, TN 38163. Tel.: 901-448-3410; Fax: 901-448-3505; E-mail: skhurana@utmem.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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Copyright © 2001 by the American Society for Biochemistry and Molecular Biology.