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J. Biol. Chem., Vol. 281, Issue 27, 18753-18762, July 7, 2006
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PACSINs Bind to the TRPV4 Cation Channel
PACSIN 3 MODULATES THE SUBCELLULAR LOCALIZATION OF TRPV4*
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Departments of Otolaryngology, Head and Neck Surgery and Molecular & Cellular Physiology, Stanford University School of Medicine, Stanford California 94305, Department of Physiology, Campus Gasthuisberg, Katholieke Universiteit Leuven, 3000 Leuven, Belgium, the ¶Department of Physiology, Radboud University Nijmegen, 6500 Nijmegen, The Netherlands, and the ||Cellular Neurobiology Unit, Center for Biochemistry and Center for Molecular Medicine, University of Cologne, D-50931 Cologne, Germany
TRPV4 is a cation channel that responds to a variety of stimuli including mechanical forces, temperature, and ligand binding. We set out to identify TRPV4-interacting proteins by performing yeast two-hybrid screens, and we isolated with the avian TRPV4 amino terminus the chicken orthologues of mammalian PACSINs 1 and 3. The PACSINs are a protein family consisting of three members that have been implicated in synaptic vesicular membrane trafficking and regulation of dynamin-mediated endocytotic processes. In biochemical interaction assays we found that all three murine PACSIN isoforms can bind to the amino terminus of rodent TRPV4. No member of the PACSIN protein family was able to biochemically interact with TRPV1 and TRPV2. Co-expression of PACSIN 3, but not PACSINs 1 and 2, shifted the ratio of plasma membrane-associated versus cytosolic TRPV4 toward an apparent increase of plasma membrane-associated TRPV4 protein. A similar shift was also observable when we blocked dynamin-mediated endocytotic processes, suggesting that PACSIN 3 specifically affects the endocytosis of TRPV4, thereby modulating the subcellular localization of the ion channel. Mutational analysis shows that the interaction of the two proteins requires both a TRPV4-specific proline-rich domain upstream of the ankyrin repeats of the channel and the carboxyl-terminal Src homology 3 domain of PACSIN 3. Such a functional interaction could be important in cell types that show distribution of both proteins to the same subcellular regions such as renal tubule cells where the proteins are associated with the luminal plasma membrane.
Received for publication, March 15, 2006 , and in revised form, April 17, 2006.
* This work was supported by National Institutes of Health Grant DC04563 (to S. H.), by Human Frontier Science Program Research Grant RPG0032/2004 (to R. J. M. B., B. N., and S. H.), and by Deutsche Forschungsgemeinschaft Grant PL 233/3-1 (to M. P.). 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.
1 These authors contributed equally to this work.
2 To whom correspondence should be addressed: Depts. of Otolaryngology and Molecular & Cellular Physiology, Stanford University School of Medicine, 801 Welch Rd., Stanford, CA 94305-5739. Tel.: 650-725-6500; Fax: 650-725-8502; E-mail: hellers{at}stanford.edu.
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