Ezrin Is an Effector of Hepatocyte Growth Factor-mediated Migration and Morphogenesis in Epithelial Cells

doi:10.1083/jcb.138.2.423

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© The Rockefeller University Press, 0021-9525/1997//423 $5.00
The Journal of Cell Biology, Volume 138, Number 2, , 1997 423-434

Article

Ezrin Is an Effector of Hepatocyte Growth Factor–mediated Migration and Morphogenesis in Epithelial Cells

Tiziana Crepaldi^*^,, Alexis Gautreau^*, Paolo M. Comoglio, Daniel Louvard^*, and Monique Arpin^*

^* Institut Curie-UMR 144 Centre National de la Recherche Scientifique, Laboratoire de Morphogenèse et Signalisation Cellulaires, 75231 Paris Cedex 05, France; and Institute for Cancer Research and Department of Biomedical Sciences, University of Torino Medical School, 10060 Torino, Italy

The dissociation, migration, and remodeling of epithelialmonolayers induced by hepatocyte growth factor (HGF) entailmodifications in cell adhesion and in the actin cytoskeletonthrough unknown mechanisms. Here we report that ezrin, a membrane–cytoskeletonlinker, is crucial to HGF-mediated morphogenesis in a polarizedkidney-derived epithelial cell line, LLC-PK1. Ezrin is a substratefor the tyrosine kinase HGF receptor both in vitro and in vivo.HGF stimulation causes enrichment of ezrin recovered in thedetergent-insoluble cytoskeleton fraction. Overproduction of wild-type ezrin, by stable transfection in LLC-PK1 cells,enhances cell migration and tubulogenesis induced by HGF stimulation.Overproduction of a truncated variant of ezrin causes mislocalizationof endogenous ezrin from microvilli into lateral surfaces. Thisis concomitant with altered cell shape, characterized by loss of microvilli and cell flattening. Moreover, the truncatedvariant of ezrin impairs the morphogenic and motogenic responseto HGF, thus suggesting a dominant-negative mechanism of action.Site-directed mutagenesis of ezrin codons Y145 and Y353 to phenylalaninedoes not affect the localization of ezrin at microvilli, butperturbs the motogenic and morphogenic responses to HGF. Theseresults provide evidence that ezrin displays activities thatcan control cell shape and signaling.

Abbreviations used in this paper: BrdU, 5-bromo-2'-deoxyuridine; CSLM, confocal laser scanning microscopy; ERM, ezrin-radixin-moesin; GST, glutathione-S-transferase; HGF, hepatocyte growth factor; HGF-R, HGF-receptor; VSVG, vesicular stomatitis virus glycoprotein G.

T. Crepaldi was supported by a fellowship from the EuropeanCommunity (BMH1-CT-94-7309). This work was supported by grantsfrom the Association pour la Recherche sur le Cancer (1825),the Ligue Nationale Française contre le Cancer, theHuman Capital Mobility (ERB CHR-XCT 940 430), the Biomed Program(BMH4-CT95-0090), and the Associazione Italiana delle Ricerchesul Cancro.

Please address all correspondence to Monique Arpin, InstitutCurie-UMR 144 CNRS, Laboratoire de Morphogenèse etSignalisation Cellulaires, 26 rue d'Ulm, 75231 Paris Cedex05, France. Tel.: (33) 1-42-34-63-72. Fax: (33) 1-42-34-63-77.e-mail: marpin{at}curie.fr

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