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J. Biol. Chem., Vol. 279, Issue 52, 54291-54303, December 24, 2004

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A Library of 7TM Receptor C-terminal Tails

INTERACTIONS WITH THE PROPOSED POST-ENDOCYTIC SORTING PROTEINS ERM-BINDING PHOSPHOPROTEIN 50 (EBP50), N-ETHYLMALEIMIDE-SENSITIVE FACTOR (NSF), SORTING NEXIN 1 (SNX1), AND G PROTEIN-COUPLED RECEPTOR-ASSOCIATED SORTING PROTEIN (GASP)^*

Arne Heydorn, Birgitte P. Søndergaard, Bjarne Ersbøll, Birgitte Holst, Finn Cilius Nielsen¶, Carol Renfrew Haft||, Jennifer Whistler**, and Thue W. Schwartz

From the Laboratory for Molecular Pharmacology, Department of Pharmacology, Panum Institute, University of Copenhagen, DK-2200 Copenhagen, Denmark, Informatics and Mathematical Modeling, The Technical University of Denmark, DK-2800 Lyngby, Denmark, ^¶Department of Clinical Biochemistry, Rigshospitalet, DK-2200 Copenhagen, Denmark, ^||NIDDK, National Institutes of Health, Bethesda, Maryland 20892-5460, ^**Ernest Gallo Research Center, University of California (UCSF), San Francisco, California 94608, and 7TM Pharma A/S, Fremtidsvej 3, DK-2970 Hørsholm, Denmark

Adaptor and scaffolding proteins determine the cellular targeting, the spatial, and thereby the functional association of G protein-coupled seven-transmembrane receptors with co-receptors, transducers, and downstream effectors and the adaptors determine post-signaling events such as receptor sequestration through interactions, mainly with the C-terminal intracellular tails of the receptors. A library of tails from 59 representative members of the super family of seven-transmembrane receptors was probed as glutathione S-transferase fusion proteins for interactions with four different adaptor proteins previously proposed to be involved in post-endocytotic sorting of receptors. Of the two proteins suggested to target receptors for recycling to the cell membrane, which is the route believed to be taken by a majority of receptors, ERM (ezrin-radixin-moesin)-binding phosphoprotein 50 (EBP50) bound only a single receptor tail, i.e. the ₂-adrenergic receptor, whereas N-ethylmaleimide-sensitive factor bound 11 of the tail-fusion proteins. Of the two proteins proposed to target receptors for lysosomal degradation, sorting nexin 1 (SNX1) bound 10 and the C-terminal domain of G protein-coupled receptor-associated sorting protein bound 23 of the 59 tail proteins. Surface plasmon resonance analysis of the binding kinetics of selected hits from the glutathione S-transferase pull-down experiments, i.e. the tails of the virally encoded receptor US28 and the -opioid receptor, confirmed the expected nanomolar affinities for interaction with SNX1. Truncations of the NK₁ receptor revealed that an extended binding epitope is responsible for the interaction with both SNX1 and G protein-coupled receptor-associated sorting protein as well as with N-ethylmaleimide-sensitive factor. It is concluded that the tail library provides useful information on the general importance of certain adaptor proteins, for example, in this case, ruling out EBP50 as being a broad spectrum-recycling adaptor.

Received for publication, June 3, 2004 , and in revised form, September 16, 2004.

^* This work was supported by grants from the Danish Technical Research Council (STVF) and the Danish Medical Research Council (SSVF). 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 Supplemental Figs. S1 and S2.

To whom correspondence should be addressed. Tel.: 45-3532-7602; Fax: 45-3532-7610; E-mail: schwartz{at}molpharm.dk.

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