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Originally published In Press as doi:10.1074/jbc.M009275200 on March 9, 2001

J. Biol. Chem., Vol. 276, Issue 21, 18066-18074, May 25, 2001
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Casein Kinase II Sites in the Intracellular C-terminal Domain of the Thyrotropin-releasing Hormone Receptor and Chimeric Gonadotropin-releasing Hormone Receptors Contribute to beta -Arrestin-dependent Internalization*

Aylin C. HanyalogluDagger §||, Milka Vrecl**, Karen M. KroegerDagger , Lauren E. C. MilesDagger , Hongwei QianDagger Dagger , Walter G. ThomasDagger Dagger §§, and Karin A. EidneDagger §¶¶

From the Dagger  7TM Receptor Laboratory, Western Australian Institute for Medical Research, § Keogh Institute for Medical Research, Sir Charles Gairdner Hospital, and  Animal Sciences, University of Western Australia, Perth, Western Australia 6009, Australia, ** Veterinary Faculty, University of Ljubljana, 1000 Ljubljana Slovenia, and Dagger Dagger  Baker Medical Research Institute, Melbourne 8008, Australia

We have previously shown that the mammalian gonadotropin-releasing hormone receptor (GnRHR), a unique G-protein-coupled receptor (GPCR) lacking an intracellular carboxyl tail (C-tail), does not follow a beta -arrestin-dependent internalization pathway. However, internalization of a chimeric GnRHR with the thyrotropin-releasing hormone receptor (TRHR) C-tail does utilize beta -arrestin. Here, we have investigated the sites within the intracellular C-tail domain that are important for conferring beta -arrestin-dependent internalization. In contrast to the chimeric GnRHR with a TRHR C-tail, a chimeric GnRHR with the catfish GnRHR C-tail is not beta -arrestin-dependent. Sequence comparisons between these chimeric receptors show three consensus phosphorylation sites for casein kinase II (CKII) in the TRHR C-tail but none in the catfish GnRHR C-tail. We thus investigated a role for CKII sites in determining GPCR internalization via beta -arrestin. Sequential introduction of three CKII sites into the chimera with the catfish C-tail (H354D,A366E,G371D) resulted in a change in the pattern of receptor phosphorylation and beta -arrestin-dependence, which only occurred when all three sites were introduced. Conversely, mutation of the putative CKII sites (T365A,T371A,S383A) in the C-tail of a beta -arrestin-sensitive GPCR, the TRHR, resulted in decreased receptor phosphorylation and a loss of beta -arrestin-dependence. Mutation of all three CKII sites was necessary before a loss of beta -arrestin-dependence was observed. Visualization of beta -arrestin/GFP redistribution confirmed a loss or gain of beta -arrestin sensitivity for receptor mutants. Internalization of receptors without C-tail CKII sites was promoted by a phosphorylation-independent beta -arrestin mutant (R169E), suggesting that these receptors do not contain the necessary phosphorylation sites required for beta -arrestin-dependent internalization. Apigenin, a specific CKII inhibitor, blocked the increase in receptor internalization by beta -arrestin, thus providing further support for the involvement of CKII. This study presents evidence of a novel role for C-tail CKII consensus sites in targeting these GPCRs to the beta -arrestin-dependent pathway.

* This work was supported by grants from the National Health and Medical Research Council of Australia and the Raine Foundation (to K. A. E).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

|| Recipient of a Keogh Institute of Medical Research postgraduate scholarship.

§§ Supported in part by a Block grant from the National Health and Medical Research Council of Australia to the Baker Medical Research Institute.

¶¶ To whom correspondence should be addressed: WAIMR, B Block, Sir Charles Gairdner Hospital, Hospital Ave., Nedlands, Perth, WA 6009, Australia. Tel.: 61 08 9346 1980; Fax: 61 08 9346 1818; E-mail: keidne@waimr.uwa.edu.au.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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