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J. Biol. Chem., Vol. 279, Issue 19, 20076-20087, May 7, 2004
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, Slows Actin Filament Barbed End Elongation, Competes with Capping Protein, Accelerates Polymerization from Monomers, and Severs Filaments*
From the Department of Biochemistry, Dartmouth Medical School, Hanover, New Hampshire 03755
Formins are a conserved class of proteins expressed in all eukaryotes, with known roles in generating cellular actin-based structures. The mammalian formin, FRL
, is enriched in hematopoietic cells and tissues, but its biochemical properties have not been characterized. We show that a construct composed of the C-terminal half of FRL (FRL-C) is a dimer and has multiple effects on muscle actin, including tight binding to actin filament sides, partial inhibition of barbed end elongation, inhibition of barbed end binding by capping protein, acceleration of polymerization from monomers, and actin filament severing. These multiple activities can be explained by a model in which FRL-C binds filament sides but prefers the topology of sides at the barbed end (end-sides) to those within the filament. This preference allows FRL-C to nucleate new filaments by side stabilization of dimers, processively advance with the elongating barbed end, block interaction between C-terminal tentacles of capping protein and filament end-sides, and sever filaments by preventing subunit re-association as filaments bend. Another formin, mDia1, does not reduce the barbed end elongation rate but does block capping protein, further supporting an end-side binding model for formins. Profilin partially relieves barbed end elongation inhibition by FRL-C. When non-muscle actin is used, FRL-C's effects are largely similar. FRL-C's ability to sever filaments is the first such activity reported for any formin. Because we find that mDia1-C does not sever efficiently, severing may not be a property of all formins.
Received for publication, November 20, 2003 , and in revised form, February 23, 2004.
* 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.
Supported by the Norris Cotton Cancer Center, American Cancer Society Institute Grant IRG-82-003-18, a Pew Biomedical Scholars award, and National Institutes of Health Grant P20RR16437 from the Centers of Biomedical Research Excellence (COBRE) Program of the National Center for Research Resources. To whom correspondence should be addressed. Tel.: 603-650-1420; Fax: 603-650-1128; E-mail: henry.n.higgs{at}dartmouth.edu.
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