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J. Biol. Chem., Vol. 278, Issue 28, 26086-26093, July 11, 2003

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Sequential Interaction of Actin-related Proteins 2 and 3 (Arp2/3) Complex with Neural Wiscott-Aldrich Syndrome Protein (N-WASP) and Cortactin during Branched Actin Filament Network Formation^*

Takehito Uruno , Jiali Liu , Yansong Li , Nicole Smith  and Xi Zhan   ¶

From the Department of Experimental Pathology, Jerome H. Holland Laboratory for the Biomedical Sciences, American Red Cross, Rockville, Maryland 20855 and the Department of Cell Biology and Anatomy, The George Washington University, Washington D. C. 20037

The WASP and cortactin families constitute two distinct classes of Arp2/3 modulators in mammalian cells. Physical and functional interactions among the Arp2/3 complex, VCA (a functional domain of N-WASP), and cortactin were examined under conditions that were with or without actin polymerization. In the absence of actin, cortactin binds significantly weaker to the Arp2/3 complex than VCA. At concentrations of VCA 20-fold lower than cortactin, the association of cortactin with the Arp2/3 complex was nearly abolished. Analysis of the cells infected with Shigella demonstrated that N-WASP located at the tip of the bacterium, whereas cortactin accumulated in the comet tail. Interestingly, cortactin promotes Arp2/3 complex-mediated actin polymerization and actin branching in the presence of VCA at a saturating concentration, and cortactin acquired 20 nM affinity for the Arp2/3 complex during actin polymerization. The interaction of VCA with the Arp2/3 complex was reduced in the presence of both cortactin and actin. Moreover, VCA reduced its affinity for Arp2/3 complex at branching sites that were stabilized by phalloidin. These data imply a novel mechanism for the de novo assembly of a branched actin network that involves a coordinated sequential interaction of N-WASP and cortactin with the Arp2/3 complex.

Received for publication, February 25, 2003 , and in revised form, May 2, 2003.

^* This work was supported by National Institutes of Health Research Grants RO1 HL52753-09, RO1 CA91984-01, Department of Defense Grant DAMD17-01-1-0125, and American Heart Association Established Investigator Grant 0040135N. The costs of publication of this article were defrayed in part by the payment of page charges. This 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. Tel.: 301-738-0568; Fax: 301-738-0879; E-mail: zhanx{at}usa.redcross.org.

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