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J. Biol. Chem., Vol. 278, Issue 26, 23738-23746, June 27, 2003

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Caveolin Interacts with the Angiotensin II Type 1 Receptor during Exocytic Transport but Not at the Plasma Membrane^*

Bruce D. Wyse  , Ian A. Prior  , Hongwei Qian ¶, Isabel C. Morrow  ||, Susan Nixon  ||, Cornelia Muncke  , Teymuras V. Kurzchalia **, Walter G. Thomas ¶, Robert G. Parton  || and John F. Hancock   

From the Institute for Molecular Bioscience, the Department of Molecular and Cellular Pathology, and the ^||Centre for Microscopy and Microanalysis and School of Biomedical Sciences, University of Queensland, Brisbane, 4072 Queensland, Australia, the ^¶Baker Heart Research Institute, Melbourne, 3004 Victoria, Australia, and the ^**Max Planck Institute for Molecular Cell Biology and Genetics, Dresden D-01307, Germany

The mechanisms involved in angiotensin II type 1 receptor (AT₁-R) trafficking and membrane localization are largely unknown. In this study, we examined the role of caveolin in these processes. Electron microscopy of plasma membrane sheets shows that the AT₁-R is not concentrated in caveolae but is clustered in cholesterol-independent microdomains; upon activation, it partially redistributes to lipid rafts. Despite the lack of AT₁-R in caveolae, AT₁-R·caveolin complexes are readily detectable in cells co-expressing both proteins. This interaction requires an intact caveolin scaffolding domain because mutant caveolins that lack a functional caveolin scaffolding domain do not interact with AT₁-R. Expression of an N-terminally truncated caveolin-3, CavDGV, that localizes to lipid bodies, or a point mutant, Cav3-P104L, that accumulates in the Golgi mislocalizes AT₁-R to lipid bodies and Golgi, respectively. Mislocalization results in aberrant maturation and surface expression of AT₁-R, effects that are not reversed by supplementing cells with cholesterol. Similarly mutation of aromatic residues in the caveolin-binding site abrogates AT₁-R cell surface expression. In cells lacking caveolin-1 or caveolin-3, AT₁-R does not traffic to the cell surface unless caveolin is ectopically expressed. This observation is recapitulated in caveolin-1 null mice that have a 55% reduction in renal AT₁-R levels compared with controls. Taken together our results indicate that a direct interaction with caveolin is required to traffic the AT₁-R through the exocytic pathway, but this does not result in AT₁-R sequestration in caveolae. Caveolin therefore acts as a molecular chaperone rather than a plasma membrane scaffold for AT₁-R.

Received for publication, December 18, 2002 , and in revised form, April 8, 2003.

^* This work is supported by grants from the National Health and Medical Research Council of Australia (to J. F. H. and R. G. P.) and Queensland Cancer Fund (to J. F. H.). The Institute for Molecular Bioscience is a Special Research Center of the Australian Research Council. 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. Tel.: 61-7-3346-2033; Fax: 61-7-3346-2101; E-mail: j.hancock{at}mailbox.uq.edu.au.

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