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Originally published In Press as doi:10.1074/jbc.M313310200 on April 27, 2004

J. Biol. Chem., Vol. 279, Issue 27, 28756-28765, July 2, 2004
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Hetero-oligomerization between {beta}2- and {beta}3-Adrenergic Receptors Generates a {beta}-Adrenergic Signaling Unit with Distinct Functional Properties*

Andreas Breit{ddagger}, Monique Lagacé, and Michel Bouvier, Holds a Canada Research Chair in Signal Transduction and Molecular Pharmacology§

From the Département de Biochimie et Groupe de Recherche sur le Système Nerveux Autonome, Université de Montréal, Montréal, Québec H3C 3J7, Canada

The ability of the closely related {beta}2- and {beta}3-adrenergic receptors (AR) to form hetero-oligomers was assessed by bioluminescence resonance energy transfer. Quantitative bioluminescence resonance energy transfer titration curves revealed that the {beta}2AR has identical propensity to hetero-oligomerize with the {beta}3AR than to form homo-oligomers. To determine the influence of heterooligomerization, a HEK293 cell line stably expressing an excess of {beta}3AR over {beta}2AR was generated so that all {beta}2AR are engaged in hetero-oligomerization with {beta}3AR, providing a tool to study the effect of hetero-oligomerization on {beta}2AR function in the absence of any {beta}2AR homooligomer. The hetero-oligomerization had no effect on the ligand binding properties of various {beta}2AR ligands and did not affect the potency of isoproterenol to stimulate adenylyl cyclase. Despite the unaltered ligand binding properties of the {beta}2/3AR hetero-oligomer, the stable association of the {beta}2AR with the {beta}3AR completely blocked agonist-stimulated internalization of the {beta}2AR. Given that the {beta}3AR is resistant to agonist-promoted endocytosis, the results indicate that the {beta}3AR acted as a dominant negative of the {beta}2AR endocytosis process. Consistent with this notion, the {beta}2/3AR hetero-oligomer displayed a lower propensity to recruit {beta}-arrestin-2 than the {beta}2AR. The hetero-oligomerization also led to a change in G protein coupling selectivity. Indeed, in contrast to {beta}2AR and {beta}3AR, which regulate adenylyl cyclase and extracellular signal-regulated kinase activity through a coupling to Gs and Gi/o, no Gi/o coupling was observed for the {beta}2/3AR hetero-oligomer. Together, these results demonstrate that hetero-oligomerization between {beta}2AR and {beta}3AR forms a {beta}-adrenergic signaling unit that possesses unique functional properties.


Received for publication, December 5, 2003 , and in revised form, April 6, 2004.

* This work was supported in part by grants from the Canadian Institute for Health Research and from the Heart and Stroke Foundation of Canada. 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.

{ddagger} Supported by a post-doctoral fellowship from AstraZeneca (Montréal).

§ To whom correspondence should be addressed. Tel.: 514-343-6372; Fax: 514-343-2210; E-mail: michel.bouvier{at}umontreal.ca.


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