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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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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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
Transduction of Receptor Signals by {beta}-Arrestins.
R. J. Lefkowitz and S. K. Shenoy (2005)
Science 308, 512-517
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
{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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
Recruitment of the Extracellular Signal-Regulated Kinase/Ribosomal S6 Kinase Signaling Pathway to the NFATc4 Transcription Activation Complex.
T. T. C. Yang, Q. Xiong, I. A. Graef, G. R. Crabtree, and C.-W. Chow (2005)
Mol. Cell. Biol. 25, 907-920
   Abstract »    Full Text »    PDF »
Functional antagonism of different G protein-coupled receptor kinases for {beta}-arrestin-mediated angiotensin II receptor signaling.
J. Kim, S. Ahn, X.-R. Ren, E. J. Whalen, E. Reiter, H. Wei, and R. J. Lefkowitz (2005)
PNAS 102, 1442-1447
   Abstract »    Full Text »    PDF »
Different G protein-coupled receptor kinases govern G protein and {beta}-arrestin-mediated signaling of V2 vasopressin receptor.
X.-R. Ren, E. Reiter, S. Ahn, J. Kim, W. Chen, and R. J. Lefkowitz (2005)
PNAS 102, 1448-1453
   Abstract »    Full Text »    PDF »
Multiple Independent Functions of Arrestins in the Regulation of Protease-Activated Receptor-2 Signaling and Trafficking.
L. Stalheim, Y. Ding, A. Gullapalli, M. M. Paing, B. L. Wolfe, D. R. Morris, and J. Trejo (2005)
Mol. Pharmacol. 67, 78-87
   Abstract »    Full Text »    PDF »
Constitutive Protease-activated Receptor-2-mediated Migration of MDA MB-231 Breast Cancer Cells Requires Both {beta}-Arrestin-1 and -2.
L. Ge, S. K. Shenoy, R. J. Lefkowitz, and K. DeFea (2004)
J. Biol. Chem. 279, 55419-55424
   Abstract »    Full Text »    PDF »

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