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Science 290 (5496): 1574-1577

Copyright © 2000 by the American Association for the Advancement of Science

beta -Arrestin 2: A Receptor-Regulated MAPK Scaffold for the Activation of JNK3

Patricia H. McDonald,1* Chi-Wing Chow,2* William E. Miller,1* Stéphane A. Laporte,3 Michael E. Field,1 Fang-Tsyr Lin,1 Roger J. Davis,2 Robert J. Lefkowitz1dagger

beta -Arrestins, originally discovered in the context of heterotrimeric guanine nucleotide binding protein-coupled receptor (GPCR) desensitization, also function in internalization and signaling of these receptors. We identified c-Jun amino-terminal kinase 3 (JNK3) as a binding partner of beta -arrestin 2 using a yeast two-hybrid screen and by coimmunoprecipitation from mouse brain extracts or cotransfected COS-7 cells. The upstream JNK activators apoptosis signal-regulating kinase 1 (ASK1) and mitogen-activated protein kinase (MAPK) kinase 4 were also found in complex with beta -arrestin 2. Cellular transfection of beta -arrestin 2 caused cytosolic retention of JNK3 and enhanced JNK3 phosphorylation stimulated by ASK1. Moreover, stimulation of the angiotensin II type 1A receptor activated JNK3 and triggered the colocalization of beta -arrestin 2 and active JNK3 to intracellular vesicles. Thus, beta -arrestin 2 acts as a scaffold protein, which brings the spatial distribution and activity of this MAPK module under the control of a GPCR.

1 Howard Hughes Medical Institute and Departments of Medicine, Cardiology, and Biochemistry, Duke University Medical Center, Box 3821, Durham, NC 27710, USA.
2 Howard Hughes Medical Institute and Program in Molecular Medicine, Department of Biochemistry and Molecular Biology, University of Massachusetts Medical School, Worcester, MA 01605, USA.
3 Department of Cell Biology, Duke University Medical Center, Box 3287, Durham, NC 27710, USA.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed.



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{beta}-Arrestin2 functions as a phosphorylation-regulated suppressor of UV-induced NF-{kappa}B activation.
B. Luan, Z. Zhang, Y. Wu, J. Kang, and G. Pei (2005)
EMBO J. 24, 4237-4246
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Differential cardioprotective/cardiotoxic effects mediated by {beta}-adrenergic receptor subtypes.
D. Bernstein, G. Fajardo, M. Zhao, T. Urashima, J. Powers, G. Berry, and B. K. Kobilka (2005)
Am J Physiol Heart Circ Physiol 289, H2441-H2449
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Seven-Transmembrane Receptor Signaling Through {beta}-Arrestin.
S. K. Shenoy and R. J. Lefkowitz (2005)
Sci. STKE 2005, cm10
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The Origins of Diversity and Specificity in G Protein-Coupled Receptor Signaling.
S. Maudsley, B. Martin, and L. M. Luttrell (2005)
J. Pharmacol. Exp. Ther. 314, 485-494
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Dynamic Interaction between the Dual Specificity Phosphatase MKP7 and the JNK3 Scaffold Protein {beta}-Arrestin 2.
E. A. Willoughby and M. K. Collins (2005)
J. Biol. Chem. 280, 25651-25658
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Constitutively Active Cytoplasmic c-Jun N-Terminal Kinase 1 Is a Dominant Regulator of Dendritic Architecture: Role of Microtubule-Associated Protein 2 as an Effector.
B. Bjorkblom, N. Ostman, V. Hongisto, V. Komarovski, J.-J. Filen, T. A. Nyman, T. Kallunki, M. J. Courtney, and E. T. Coffey (2005)
J. Neurosci. 25, 6350-6361
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Involvement of Actin in Agonist-induced Endocytosis of the G Protein-coupled Receptor for Thromboxane A2: OVERCOMING OF ACTIN DISRUPTION BY ARRESTIN-3 BUT NOT ARRESTIN-2.
G. Laroche, M. D. Rochdi, S. A. Laporte, and J.-L. Parent (2005)
J. Biol. Chem. 280, 23215-23224
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The Glucagon-like Peptide-2 Receptor C Terminus Modulates {beta}-Arrestin-2 Association but Is Dispensable for Ligand-induced Desensitization, Endocytosis, and G-protein-dependent Effector Activation.
J. L. Estall, J. A. Koehler, B. Yusta, and D. J. Drucker (2005)
J. Biol. Chem. 280, 22124-22134
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Paired Activation of Two Components within Muscarinic M3 Receptor Dimers Is Required for Recruitment of {beta}-Arrestin-1 to the Plasma Membrane.
F. Novi, L. Stanasila, F. Giorgi, G. U. Corsini, S. Cotecchia, and R. Maggio (2005)
J. Biol. Chem. 280, 19768-19776
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Roles of Phosphorylation-dependent and -independent Mechanisms in the Regulation of M1 Muscarinic Acetylcholine Receptors by G Protein-coupled Receptor Kinase 2 in Hippocampal Neurons.
J. M. Willets, S. R. Nahorski, and R. A. J. Challiss (2005)
J. Biol. Chem. 280, 18950-18958
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Complete Inhibition of Anisomycin and UV Radiation but Not Cytokine Induced JNK and p38 Activation by an Aryl-substituted Dihydropyrrolopyrazole Quinoline and Mixed Lineage Kinase 7 Small Interfering RNA.
X. Wang, M. M. Mader, J. E. Toth, X. Yu, N. Jin, R. M. Campbell, J. K. Smallwood, M. E. Christe, A. Chatterjee, T. Goodson Jr., et al. (2005)
J. Biol. Chem. 280, 19298-19305
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Transduction of Receptor Signals by {beta}-Arrestins.
R. J. Lefkowitz and S. K. Shenoy (2005)
Science 308, 512-517
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Receptor-specific Ubiquitination of {beta}-Arrestin Directs Assembly and Targeting of Seven-transmembrane Receptor Signalosomes.
S. K. Shenoy and R. J. Lefkowitz (2005)
J. Biol. Chem. 280, 15315-15324
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Role of the JIP4 Scaffold Protein in the Regulation of Mitogen-Activated Protein Kinase Signaling Pathways.
N. Kelkar, C. L. Standen, and R. J. Davis (2005)
Mol. Cell. Biol. 25, 2733-2743
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G Protein-coupled Receptor Kinase Regulates Dopamine D3 Receptor Signaling by Modulating the Stability of a Receptor-Filamin-{beta}-Arrestin Complex: A CASE OF AUTORECEPTOR REGULATION.
K.-M. Kim, R. R. Gainetdinov, S. A. Laporte, M. G. Caron, and L. S. Barak (2005)
J. Biol. Chem. 280, 12774-12780
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{beta}-Arrestin 2-Dependent Angiotensin II Type 1A Receptor-Mediated Pathway of Chemotaxis.
D. L. Hunton, W. G. Barnes, J. Kim, X.-R. Ren, J. D. Violin, E. Reiter, G. Milligan, D. D. Patel, and R. J. Lefkowitz (2005)
Mol. Pharmacol. 67, 1229-1236
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Sunday Driver links axonal transport to damage signaling.
V. Cavalli, P. Kujala, J. Klumperman, and L. S.B. Goldstein (2005)
J. Cell Biol. 168, 775-787
   Abstract »    Full Text »    PDF »
Phosphorylation-independent {beta}-Arrestin Translocation and Internalization of Leukotriene B4 Receptors.
V. R. Jala, W.-H. Shao, and B. Haribabu (2005)
J. Biol. Chem. 280, 4880-4887
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