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J. Biol. Chem., Vol. 279, Issue 44, 46104-46112, October 29, 2004

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TSAP6 Facilitates the Secretion of Translationally Controlled Tumor Protein/Histamine-releasing Factor via a Nonclassical Pathway^*

Nathalie Amzallag, Brent J. Passer, David Allanic, Elodie Segura||, Clotilde Théry||, Bruno Goud**, Robert Amson, and Adam Telerman¶

From the Molecular Engines Laboratories, 20 Rue Bouvier, 75011 Paris and Institut Curie, ^||INSERM U365, ^**CNRS UMR144, 12 Rue Lhomond, 75005 Paris, France

Translationally controlled tumor protein (TCTP) is cytoplasmic and structurally related to guanine-nucleotide free chaperones. TCTP (also called histamine-releasing factor) has been described previously as a secreted protein that participates in inflammatory responses by promoting the release of histamine. How TCTP is eventually exported out of the cell to promote such activities is unknown. Here we show that TCTP secretion was insensitive to either brefeldin A or monensin, suggesting that it proceeds via an endoplasmic reticulum/Golgi-independent or nonclassical pathway. Moreover, our analyses also suggest that secreted TCTP originates from pre-existing pools. TSAP6, a p53-inducible 5–6 transmembrane protein, was found to interact with TCTP in a yeast two-hybrid hunt. GST pull down assays confirmed their direct interaction, and immunofluorescence analysis revealed their partial co-distribution to vesicular-like structures at the plasma membrane and around the nucleus. Functionally, the overexpression of TSAP6 consistently leads to enhanced secretion of both endogenously and exogenously expressed TCTP. Finally, we found TCTP in preparations of small secreted vesicles called exosomes, which have been suggested as a possible pathway for nonclassical secretion. Overexpression of TSAP6 also increased TCTP levels in exosome preparations. Altogether, these data identify a novel role for TSAP6 in the export of TCTP and indicate that this multipass membrane protein could have a general role in the regulation of vesicular trafficking and secretion.

Received for publication, April 30, 2004 , and in revised form, August 13, 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.

The on-line version of this article (available at http://www.jbc.org) contains Figs. S1 and S2.

Both authors contributed equally to this work.

^¶ To whom correspondence should be addressed: Molecular Engines Laboratories, 20, Rue Bouvier, 75011 Paris, France. E-mail: atelerman{at}molecular-engines.com.

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