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J. Biol. Chem., Vol. 281, Issue 50, 38825-38833, December 15, 2006

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SNARE Status Regulates Tether Recruitment and Function in Homotypic COPII Vesicle Fusion^*

Marvin Bentley¹, Yingjian Liang¹, Karl Mullen¹, Dalu Xu², Elizabeth Sztul, and Jesse C. Hay³

From the Division of Biological Sciences, the University of Montana, Missoula, Montana 59812-4824 and the Department of Cell Biology, the University of Alabama at Birmingham, Birmingham, Alabama 35294

In mammals, coat complex II (COPII)-coated transport vesicles deliver secretory cargo to vesicular tubular clusters (VTCs) that facilitate cargo sorting and transport to the Golgi. We documented in vitro tethering and SNARE-dependent homotypic fusion of endoplasmic reticulum-derived COPII transport vesicles to form larger cargo containers characteristic of VTCs ( Xu, D., and Hay, J. C. (2004) J. Cell Biol. 167, 997-1003[Abstract/Free Full Text] ). COPII vesicles thus appear to contain all necessary components for homotypic tethering and fusion, providing a pathway for de novo VTC biogenesis. Here we demonstrate that antibodies against the endoplasmic reticulum/Golgi SNARE Syntaxin 5 inhibit COPII vesicle homotypic tethering as well as fusion, implying an unanticipated role for SNAREs upstream of fusion. Inhibition of SNARE complex access and/or disassembly with dominant-negative -soluble NSF attachment protein (SNAP) also inhibited tethering, implicating SNARE status as a critical determinant in COPII vesicle tethering. The tethering-defective vesicles generated in the presence of dominant-negative -SNAP specifically lacked the Rab1 effectors p115 and GM130 but not other peripheral membrane proteins. Furthermore, Rab effectors, including p115, were shown to be required for homotypic COPII vesicle tethering. Thus, our results demonstrate a requirement for SNARE-dependent tether recruitment and function in COPII vesicle fusion. We anticipate that recruitment of tether molecules by an upstream SNARE signal ensures that tethering events are initiated only at focal sites containing appropriately poised fusion machinery.

Received for publication, June 23, 2006 , and in revised form, September 26, 2006.

^* This work was supported by National Institutes of Health Grant RO1 GM59378 (to J. C. H.) and by National Institutes of Health COBRE Center for Structural and Functional Neuroscience Grant RR015583. 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 Present address: Institute of Biochemistry II, Frankfurt Medical School, 60590 Frankfurt am Main, Germany.

³ To whom correspondence should be addressed. Tel.: 406-243-2381; Fax: 406-243-4184; E-mail: jesse.hay{at}umontana.edu.

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