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J. Biol. Chem., Vol. 278, Issue 46, 45978-45986, November 14, 2003
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A Novel Endocytic Recycling Signal That Distinguishes the Membrane Trafficking of Naturally Occurring Opioid Receptors*
From the Departments of Psychiatry and Cellular & Molecular Pharmacology, University of California, San Francisco, California 94143-2140
and µ opioid receptors are homologous G protein-coupled receptors that are differentially sorted between divergent degradative and recycling membrane pathways following agonist-induced endocytosis. Whereas opioid receptors are selectively sorted to lysosomes, µ opioid receptors recycle rapidly to the plasma membrane by a process that has been proposed to occur via bulk membrane flow. We have observed that µ opioid receptors do not recycle by default and have defined a specific sequence present in the cytoplasmic tail of the cloned µ opioid receptor that is both necessary and sufficient for rapid recycling of internalized receptors. This sequence is completely distinct from a sequence shown previously to be required for recycling of the 
2 adrenergic receptor yet is functionally interchangeable when tested in chimeric mutant receptors. These results indicate that signal-dependent recycling is a more common property of G protein-coupled receptors than previously appreciated and demonstrate that such a modular recycling signal distinguishes the regulation of homologous receptors that are naturally co-expressed.
Received for publication, April 30, 2003 , and in revised form, August 15, 2003.
* This work was supported by a research grant from the National Institutes of Health (to M. v. Z.) and by a National Institutes of Health individual national research service award (to M. T.). 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.
To whom correspondence should be addressed: N-216 Genentech Hall, University of California, 600 16th St., San Francisco, CA 94143-2140. Tel.: 415-476-7855; Fax: 415-504-0169; E-mail: mbt2m{at}itsa.ucsf.edu.
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