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J. Biol. Chem., Vol. 278, Issue 49, 49031-49043, December 5, 2003

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Tuba, a Novel Protein Containing Bin/Amphiphysin/Rvs and Dbl Homology Domains, Links Dynamin to Regulation of the Actin Cytoskeleton^*

Marco A. Salazar¶, Adam V. Kwiatkowski||**, Lorenzo Pellegrini, Gianluca Cestra, Margaret H. Butler, Kent L. Rossman, Daniel M. Serna||, John Sondek, Frank B. Gertler||, and Pietro De Camilli¶¶

From the Department of Cell Biology and the Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, Connecticut 06519, the ^||Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 01239, and the Department of Biophysics and Biochemistry and the Lineberger Cancer Center, University of North Carolina, Chapel Hill, North Carolina 27599

Tuba is a novel scaffold protein that functions to bring together dynamin with actin regulatory proteins. It is concentrated at synapses in brain and binds dynamin selectively through four N-terminal Src homology-3 (SH3) domains. Tuba binds a variety of actin regulatory proteins, including N-WASP, CR16, WAVE1, WIRE, PIR121, NAP1, and Ena/VASP proteins, via a C-terminal SH3 domain. Direct binding partners include N-WASP and Ena/VASP proteins. Forced targeting of the C-terminal SH3 domain to the mitochondrial surface can promote accumulation of F-actin around mitochondria. A Dbl homology domain present in the middle of Tuba upstream of a Bin/amphiphysin/Rvs (BAR) domain activates Cdc42, but not Rac and Rho, and may thus cooperate with the C terminus of the protein in regulating actin assembly. The BAR domain, a lipid-binding module, may functionally replace the pleckstrin homology domain that typically follows a Dbl homology domain. The properties of Tuba provide new evidence for a close functional link between dynamin, Rho GTPase signaling, and the actin cytoskeleton.

Received for publication, July 25, 2003 , and in revised form, September 16, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AY196211 and AY383729.

^* This work was supported in part by National Institutes of Health Grants NS36251 and CA46128 and United States Army Medical Research and Development Command Grant DAMD17-97-7068) (to P. D. C.); by National Institutes of Health Grant GM58801, a W. M. Keck Distinguished Young Scholar Award, and a McKnight Scholar Award (to F. B. G.); and by National Institutes of Health Grant GM62299 (to J. S.). 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.

Both authors contributed equally to this work.

^¶ Supported by a research supplement for underrepresented minorities from NCI, National Institutes of Health.

^** Supported by an Anna Fuller predoctoral fellowship.

Supported by a fellowship from Telethon (Italy).

^¶¶ To whom correspondence should be addressed: Dept. of Cell Biology and Howard Hughes Medical Inst., Yale University School of Medicine, 295 Congress Ave., BCMM 236, New Haven, CT 06519. Tel.: 203-737-4461; Fax: 203-737-4436; E-mail: pietro.decamilli{at}yale.edu.

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