Arrestins: Role in the desensitization, sequestration, and vesicular trafficking of g protein-coupled receptors

Progress in Molecular Biology and Translational Science

Volumn 118, Issue , 2013, Pages 93-113

  Walther, Cornelia ^a,b   Ferguson, Stephen S G ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84879094441     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394440-5.00004-8     Document Type: Chapter

References (101)

1. E.J. Neer Heterotrimeric G proteins: organizers of transmembrane signals Cell 80 1995 249 257
2. J.L. Seachrist, and S.S. Ferguson Regulation of G protein-coupled receptor endocytosis and trafficking by Rab GTPases Life Sci 74 2003 225 235
3. S.S. Ferguson Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling Pharmacol Rev 53 2001 1 24
4. J. Bockaert, L. Fagni, A. Dumuis, and P. Marin GPCR interacting proteins (GIP) Pharmacol Ther 103 2004 203 221
5. A.C. Magalhaes, H. Dunn, and S.S. Ferguson Regulation of GPCR activity, trafficking and localization by GPCR-interacting proteins Br J Pharmacol 165 2012 1717 1736
6. J. Bockaert, G. Roussignol, and C. Becamel GPCR-interacting proteins (GIPs): nature and functions Biochem Soc Trans 32 2004 851 855
7. S.L. Ritter, and R.A. Hall Fine-tuning of GPCR activity by receptor-interacting proteins Nat Rev Mol Cell Biol 10 2009 819 830
8. P. Maurice, J.L. Guillaume, A. Benleulmi-Chaachoua, A.M. Daulat, M. Kamal, and R. Jockers GPCR-interacting proteins, major players of GPCR function Adv Pharmacol 62 2011 349 380
9. C. Pfister, M. Chabre, and J. Plouet Retinal S antigen identified as the 48 K protein regulating light-dependent phosphodiesterase in rods Science 228 1985 891 893
10. S.S. Ferguson, L.S. Barak, J. Zhang, and M.G. Caron G-protein-coupled receptor regulation: role of G-protein-coupled receptor kinases and arrestins Can J Physiol Pharmacol 74 1996 1095 1110
11. J.G. Krupnick, and J.L. Benovic The role of receptor kinases and arrestins in G protein-coupled receptor regulation Annu Rev Pharmacol Toxicol 38 1998 289 319
12. P.H. McDonald, and R.J. Lefkowitz Beta-arrestins: new roles in regulating heptahelical receptors' functions Cell Signal 13 2001 683 689
13. K.L. Pierce, R.T. Premont, and R.J. Lefkowitz Seven-transmembrane receptors Nat Rev Mol Cell Biol 3 2002 639 650
14. S.K. Shenoy, and R.J. Lefkowitz Multifaceted roles of beta-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signalling Biochem J 375 2003 503 515
15. S.K. Shenoy, and R.J. Lefkowitz Trafficking patterns of beta-arrestin and G protein-coupled receptors determined by the kinetics of beta-arrestin deubiquitination J Biol Chem 278 2003 14498 14506
16. L. Barki-Harrington, and H.A. Rockman Beta-arrestins: multifunctional cellular mediators Physiology (Bethesda) 23 2008 17 22
17. S.K. Milano, H.C. Pace, Y.M. Kim, C. Brenner, and J.L. Benovic Scaffolding functions of arrestin-2 revealed by crystal structure and mutagenesis Biochemistry 41 2002 3321 3328
18. T.A. Kohout, and R.J. Lefkowitz Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization Mol Pharmacol 63 2003 9 18
19. K. Palczewski, J. Buczylko, M.W. Kaplan, A.S. Polans, and J.W. Crabb Mechanism of rhodopsin kinase activation J Biol Chem 266 1991 12949 12955
20. C.A. Moore, S.K. Milano, and J.L. Benovic Regulation of receptor trafficking by GRKs and arrestins Annu Rev Physiol 69 2007 451 482
21. R.T. Premont, and R.R. Gainetdinov Physiological roles of G protein-coupled receptor kinases and arrestins Annu Rev Physiol 69 2007 511 534
22. E. Reiter, and R.J. Lefkowitz GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling Trends Endocrinol Metab 17 2006 159 165
23. J.A. Pitcher, N.J. Freedman, and R.J. Lefkowitz G protein-coupled receptor kinases Annu Rev Biochem 67 1998 653 692
24. J.L. Benovic, H. Kuhn, I. Weyand, J. Codina, M.G. Caron, and R.J. Lefkowitz Functional desensitization of the isolated beta-adrenergic receptor by the beta-adrenergic receptor kinase: potential role of an analog of the retinal protein arrestin (48-kDa protein) Proc Natl Acad Sci USA 84 1987 8879 8882
25. J. Kim, S. Ahn, and X.R. Ren Functional antagonism of different G protein-coupled receptor kinases for beta-arrestin-mediated angiotensin II receptor signaling Proc Natl Acad Sci USA 102 2005 1442 1447
26. X.R. Ren, E. Reiter, S. Ahn, J. Kim, W. Chen, and R.J. Lefkowitz Different G protein-coupled receptor kinases govern G protein and beta-arrestin-mediated signaling of V2 vasopressin receptor Proc Natl Acad Sci USA 102 2005 1448 1453
27. N. Aiyar, J. Disa, K. Dang, A.N. Pronin, J.L. Benovic, and P. Nambi Involvement of G protein-coupled receptor kinase-6 in desensitization of CGRP receptors Eur J Pharmacol 403 2000 1 7
28. M. Tiberi, S.R. Nash, L. Bertrand, R.J. Lefkowitz, and M.G. Caron Differential regulation of dopamine D1A receptor responsiveness by various G protein-coupled receptor kinases J Biol Chem 271 1996 3771 3778
29. A.B. Tobin, A.J. Butcher, and K.C. Kong Location, location, location.site-specific GPCR phosphorylation offers a mechanism for cell-type-specific signalling Trends Pharmacol Sci 29 2008 413 420
30. K.N. Nobles, K. Xiao, and S. Ahn Distinct phosphorylation sites on the beta(2)-adrenergic receptor establish a barcode that encodes differential functions of beta-arrestin Sci Signal 4 2011 ra51
31. J.M. Busillo, S. Armando, R. Sengupta, O. Meucci, M. Bouvier, and J.L. Benovic Site-specific phosphorylation of CXCR4 is dynamically regulated by multiple kinases and results in differential modulation of CXCR4 signaling J Biol Chem 285 2010 7805 7817
32. D.A. Zidar, J.D. Violin, E.J. Whalen, and R.J. Lefkowitz Selective engagement of G protein coupled receptor kinases (GRKs) encodes distinct functions of biased ligands Proc Natl Acad Sci USA 106 2009 9649 9654
33. R.H. Oakley, S.A. Laporte, J.A. Holt, L.S. Barak, and M.G. Caron Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor-beta-arrestin complexes after receptor endocytosis* J Biol Chem 276 2001 19452 19460
34. R.H. Oakley, S.A. Laporte, J.A. Holt, M.G. Caron, and L.S. Barak Differential affinities of visual arrestin, beta arrestin1, and beta arrestin2 for G protein-coupled receptors delineate two major classes of receptors J Biol Chem 275 2000 17201 17210
35. V.V. Gurevich, and J.L. Benovic Visual arrestin interaction with rhodopsin. Sequential multisite binding ensures strict selectivity toward light-activated phosphorylated rhodopsin J Biol Chem 268 1993 11628 11638
36. H. Kuhn, S.W. Hall, and U. Wilden Light-induced binding of 48-kDa protein to photoreceptor membranes is highly enhanced by phosphorylation of rhodopsin FEBS Lett 176 1984 473 478
37. H. Attramadal, J.L. Arriza, and C. Aoki Beta-arrestin2, a novel member of the arrestin/beta-arrestin gene family J Biol Chem 267 1992 17882 17890
38. V.V. Gurevich, S.B. Dion, and J.J. Onorato Arrestin interactions with G protein-coupled receptors. Direct binding studies of wild type and mutant arrestins with rhodopsin, beta 2-adrenergic, and m2 muscarinic cholinergic receptors J Biol Chem 270 1995 720 731
39. M.J. Lohse, S. Andexinger, and J. Pitcher Receptor-specific desensitization with purified proteins. Kinase dependence and receptor specificity of beta-arrestin and arrestin in the beta 2-adrenergic receptor and rhodopsin systems J Biol Chem 267 1992 8558 8564
40. M.J. Lohse, J.L. Benovic, J. Codina, M.G. Caron, and R.J. Lefkowitz Beta-arrestin: a protein that regulates beta-adrenergic receptor function Science 248 1990 1547 1550
41. H. Qian, L. Pipolo, and W.G. Thomas Association of beta-arrestin 1 with the type 1A angiotensin II receptor involves phosphorylation of the receptor carboxyl terminus and correlates with receptor internalization Mol Endocrinol 15 2001 1706 1719
42. Q. Wang, and L.E. Limbird Regulated interactions of the alpha 2A adrenergic receptor with spinophilin, 14-3-3zeta, and arrestin 3 J Biol Chem 277 2002 50589 50596
43. N.D. Holliday, C.W. Lam, I.R. Tough, and H.M. Cox Role of the C terminus in neuropeptide Y Y1 receptor desensitization and internalization Mol Pharmacol 67 2005 655 664
44. V.V. Gurevich, and E.V. Gurevich The structural basis of arrestin-mediated regulation of G-protein-coupled receptors Pharmacol Ther 110 2006 465 502
45. S. Milasta, N.A. Evans, L. Ormiston, S. Wilson, R.J. Lefkowitz, and G. Milligan The sustainability of interactions between the orexin-1 receptor and beta-arrestin-2 is defined by a single C-terminal cluster of hydroxy amino acids and modulates the kinetics of ERK MAPK regulation Biochem J 387 2005 573 584
46. L. Min, C. Galet, and M. Ascoli The association of arrestin-3 with the human lutropin/choriogonadotropin receptor depends mostly on receptor activation rather than on receptor phosphorylation J Biol Chem 277 2002 702 710
47. S. Mukherjee, V.V. Gurevich, and A. Preninger Aspartic acid 564 in the third cytoplasmic loop of the luteinizing hormone/choriogonadotropin receptor is crucial for phosphorylation-independent interaction with arrestin2 J Biol Chem 277 2002 17916 17927
48. F.T. Lin, W. Chen, S. Shenoy, M. Cong, S.T. Exum, and R.J. Lefkowitz Phosphorylation of beta-arrestin2 regulates its function in internalization of beta(2)-adrenergic receptors Biochemistry 41 2002 10692 10699
49. F.T. Lin, K.M. Krueger, and H.E. Kendall Clathrin-mediated endocytosis of the beta-adrenergic receptor is regulated by phosphorylation/dephosphorylation of beta-arrestin1 J Biol Chem 272 1997 31051 31057
50. E. Galliera, V.R. Jala, and J.O. Trent Beta-arrestin-dependent constitutive internalization of the human chemokine decoy receptor D6 J Biol Chem 279 2004 25590 25597
51. C. Doll, J. Konietzko, F. Poll, T. Koch, V. Hollt, and S. Schulz Agonist-selective patterns of micro-opioid receptor phosphorylation revealed by phosphosite-specific antibodies Br J Pharmacol 164 2011 298 307
52. C.E. Groer, K. Tidgewell, and R.A. Moyer An opioid agonist that does not induce mu-opioid receptor-arrestin interactions or receptor internalization Mol Pharmacol 71 2007 549 557
53. Y.A. Berchiche, S. Gravel, M.E. Pelletier, G. St-Onge, and N. Heveker Different effects of the different natural CC chemokine receptor 2b ligands on beta-arrestin recruitment, G alpha i signaling, and receptor internalization Mol Pharmacol 79 2011 488 498
54. P.J. Dolph, R. Ranganathan, N.J. Colley, R.W. Hardy, M. Socolich, and C.S. Zuker Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo Science 260 1993 1910 1916
55. L.M. Bohn, R.J. Lefkowitz, R.R. Gainetdinov, K. Peppel, M.G. Caron, and F.T. Lin Enhanced morphine analgesia in mice lacking beta-arrestin 2 Science 286 1999 2495 2498
56. S.J. Perry, G.S. Baillie, and T.A. Kohout Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by beta-arrestins Science 298 2002 834 836
57. G.S. Baillie, A. Sood, and I. McPhee Beta-arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi Proc Natl Acad Sci USA 100 2003 940 945
58. C.D. Nelson, S.J. Perry, D.S. Regier, S.M. Prescott, M.K. Topham, and R.J. Lefkowitz Targeting of diacylglycerol degradation to M1 muscarinic receptors by beta-arrestins Science 315 2007 663 666
59. S.S. Ferguson Phosphorylation-independent attenuation of GPCR signalling Trends Pharmacol Sci 28 2007 173 179
60. S.S. Ferguson, W.E. Downey 3rd., A.M. Colapietro, L.S. Barak, L. Menard, and M.G. Caron Role of beta-arrestin in mediating agonist-promoted G protein-coupled receptor internalization Science 271 1996 363 366
61. A. Claing, S.A. Laporte, M.G. Caron, and R.J. Lefkowitz Endocytosis of G protein-coupled receptors: roles of G protein-coupled receptor kinases and beta-arrestin proteins Prog Neurobiol 66 2002 61 79
62. A. Marchese, C. Chen, Y.M. Kim, and J.L. Benovic The ins and outs of G protein-coupled receptor trafficking Trends Biochem Sci 28 2003 369 376
63. A. Rapacciuolo, S. Suvarna, and L. Barki-Harrington Protein kinase A and G protein-coupled receptor kinase phosphorylation mediates beta-1 adrenergic receptor endocytosis through different pathways J Biol Chem 278 2003 35403 35411
64. O.B. Goodman Jr., J.G. Krupnick, V.V. Gurevich, J.L. Benovic, and J.H. Keen Arrestin/clathrin interaction. Localization of the arrestin binding locus to the clathrin terminal domain J Biol Chem 272 1997 15017 15022
65. J.G. Krupnick, O.B. Goodman Jr., J.H. Keen, and J.L. Benovic Arrestin/clathrin interaction. Localization of the clathrin binding domain of nonvisual arrestins to the carboxy terminus J Biol Chem 272 1997 15011 15016
66. J.G. Krupnick, F. Santini, A.W. Gagnon, J.H. Keen, and J.L. Benovic Modulation of the arrestin-clathrin interaction in cells. Characterization of beta-arrestin dominant-negative mutants J Biol Chem 272 1997 32507 32512
67. O.B. Goodman Jr., J.G. Krupnick, and F. Santini Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor Nature 383 1996 447 450
68. S.A. Laporte, R.H. Oakley, J.A. Holt, L.S. Barak, and M.G. Caron The interaction of beta-arrestin with the AP-2 adaptor is required for the clustering of beta 2-adrenergic receptor into clathrin-coated pits J Biol Chem 275 2000 23120 23126
69. S.A. Laporte, R.H. Oakley, and J. Zhang The beta2-adrenergic receptor/betaarrestin complex recruits the clathrin adaptor AP-2 during endocytosis Proc Natl Acad Sci USA 96 1999 3712 3717
70. R. Pals-Rylaarsdam, V.V. Gurevich, K.B. Lee, J.A. Ptasienski, J.L. Benovic, and M.M. Hosey Internalization of the m2 muscarinic acetylcholine receptor. Arrestin-independent and -dependent pathways J Biol Chem 272 1997 23682 23689
71. K. Kraft, H. Olbrich, I. Majoul, M. Mack, A. Proudfoot, and M. Oppermann Characterization of sequence determinants within the carboxyl-terminal domain of chemokine receptor CCR5 that regulate signaling and receptor internalization J Biol Chem 276 2001 34408 34418
72. A.L. Matharu, S.J. Mundell, J.L. Benovic, and E. Kelly Rapid agonist-induced desensitization and internalization of the A(2B) adenosine receptor is mediated by a serine residue close to the COOH terminus J Biol Chem 276 2001 30199 30207
73. C. Walther, S. Nagel, L.E. Gimenez, K. Morl, V.V. Gurevich, and A.G. Beck-Sickinger Ligand-induced internalization and recycling of the human neuropeptide Y2 receptor is regulated by its carboxyl-terminal tail J Biol Chem 285 2010 41578 41590
74. M.G. Scott, E. Le Rouzic, and A. Perianin Differential nucleocytoplasmic shuttling of beta-arrestins. Characterization of a leucine-rich nuclear export signal in beta-arrestin2 J Biol Chem 277 2002 37693 37701
75. T.A. Kohout, F.S. Lin, S.J. Perry, D.A. Conner, and R.J. Lefkowitz Beta-arrestin 1 and 2 differentially regulate heptahelical receptor signaling and trafficking Proc Natl Acad Sci USA 98 2001 1601 1606
76. J. Zhang, L.S. Barak, P.H. Anborgh, S.A. Laporte, M.G. Caron, and S.S. Ferguson Cellular trafficking of G protein-coupled receptor/beta-arrestin endocytic complexes J Biol Chem 274 1999 10999 11006
77. P.H. Anborgh, J.L. Seachrist, L.B. Dale, and S.S. Ferguson Receptor/beta-arrestin complex formation and the differential trafficking and resensitization of beta2-adrenergic and angiotensin II type 1A receptors Mol Endocrinol 14 2000 2040 2053
78. C. Krasel, U. Zabel, K. Lorenz, S. Reiner, S. Al-Sabah, and M.J. Lohse Dual role of the beta2-adrenergic receptor C terminus for the binding of beta-arrestin and receptor internalization J Biol Chem 283 2008 31840 31848
79. D.J. Vaughan, E.E. Millman, and V. Godines Role of the G protein-coupled receptor kinase site serine cluster in beta2-adrenergic receptor internalization, desensitization, and beta-arrestin translocation J Biol Chem 281 2006 7684 7692
80. K.B. Lee, J.A. Ptasienski, R. Pals-Rylaarsdam, V.V. Gurevich, and M.M. Hosey Arrestin binding to the M(2) muscarinic acetylcholine receptor is precluded by an inhibitory element in the third intracellular loop of the receptor J Biol Chem 275 2000 9284 9289
81. R. Pals-Rylaarsdam, and M.M. Hosey Two homologous phosphorylation domains differentially contribute to desensitization and internalization of the m2 muscarinic acetylcholine receptor J Biol Chem 272 1997 14152 14158
82. Y. Qiu, H.H. Loh, and P.Y. Law Phosphorylation of the delta-opioid receptor regulates its beta-arrestins selectivity and subsequent receptor internalization and adenylyl cyclase desensitization J Biol Chem 282 2007 22315 22323
83. C.E. Kule, V. Karoor, and J.N. Day Agonist-dependent internalization of the angiotensin II type one receptor (AT1): role of C-terminus phosphorylation in recruitment of beta-arrestins Regul Pept 120 2004 141 148
84. S. Reiner, N. Ziegler, and C. Leon Beta-arrestin-2 interaction and internalization of the human P2Y1 receptor are dependent on C-terminal phosphorylation sites Mol Pharmacol 76 2009 1162 1171
85. O.J. Kim, B.R. Gardner, and D.B. Williams The role of phosphorylation in D1 dopamine receptor desensitization: evidence for a novel mechanism of arrestin association J Biol Chem 279 2004 7999 8010
86. L.E. Kilpatrick, S.J. Briddon, S.J. Hill, and N.D. Holliday Quantitative analysis of neuropeptide Y receptor association with beta-arrestin2 measured by bimolecular fluorescence complementation Br J Pharmacol 160 2010 892 906
87. L.E. Kilpatrick, S.J. Briddon, and N.D. Holliday Fluorescence correlation spectroscopy, combined with bimolecular fluorescence complementation, reveals the effects of beta-arrestin complexes and endocytic targeting on the membrane mobility of neuropeptide Y receptors Biochim Biophys Acta 1823 2012 1068 1081
88. J.L. DeGraff, V.V. Gurevich, and J.L. Benovic The third intracellular loop of alpha 2-adrenergic receptors determines subtype specificity of arrestin interaction J Biol Chem 277 2002 43247 43252
89. G. Wu, J.G. Krupnick, J.L. Benovic, and S.M. Lanier Interaction of arrestins with intracellular domains of muscarinic and alpha2-adrenergic receptors J Biol Chem 272 1997 17836 17842
90. S.K. Shenoy, P.H. McDonald, T.A. Kohout, and R.J. Lefkowitz Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin Science 294 2001 1307 1313
91. C.D. Nelson, J.J. Kovacs, K.N. Nobles, E.J. Whalen, and R.J. Lefkowitz Beta-arrestin scaffolding of phosphatidylinositol 4-phosphate 5-kinase Ialpha promotes agonist-stimulated sequestration of the beta2-adrenergic receptor J Biol Chem 283 2008 21093 21101
92. R.H. Oakley, S.A. Laporte, J.A. Holt, L.S. Barak, and M.G. Caron Association of beta-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization J Biol Chem 274 1999 32248 32257
93. G. Innamorati, C. Le Gouill, M. Balamotis, and M. Birnbaumer The long and the short cycle. Alternative intracellular routes for trafficking of G-protein-coupled receptors J Biol Chem 276 2001 13096 13103
94. L. Pan, E.V. Gurevich, and V.V. Gurevich The nature of the arrestin x receptor complex determines the ultimate fate of the internalized receptor J Biol Chem 278 2003 11623 11632
95. K.L. Pierce, and R.J. Lefkowitz Classical and new roles of beta-arrestins in the regulation of G-protein-coupled receptors Nat Rev Neurosci 2 2001 727 733
96. J. Zhang, L.S. Barak, K.E. Winkler, M.G. Caron, and S.S. Ferguson A central role for beta-arrestins and clathrin-coated vesicle-mediated endocytosis in beta2-adrenergic receptor resensitization. Differential regulation of receptor resensitization in two distinct cell types J Biol Chem 272 1997 27005 27014
97. G. Tulipano, R. Stumm, M. Pfeiffer, H.J. Kreienkamp, V. Hollt, and S. Schulz Differential beta-arrestin trafficking and endosomal sorting of somatostatin receptor subtypes J Biol Chem 279 2004 21374 21382
98. J.D. Pediani, J.F. Colston, D. Caldwell, G. Milligan, C.J. Daly, and J.C. McGrath Beta-arrestin-dependent spontaneous alpha1a-adrenoceptor endocytosis causes intracellular transportation of alpha-blockers via recycling compartments Mol Pharmacol 67 2005 992 1004
99. L.B. Dale, M. Bhattacharya, J.L. Seachrist, P.H. Anborgh, and S.S. Ferguson Agonist-stimulated and tonic internalization of metabotropic glutamate receptor 1a in human embryonic kidney 293 cells: agonist-stimulated endocytosis is beta-arrestin1 isoform-specific Mol Pharmacol 60 2001 1243 1253
100. A. Claing, W. Chen, and W.E. Miller Beta-arrestin-mediated ADP-ribosylation factor 6 activation and beta 2-adrenergic receptor endocytosis J Biol Chem 276 2001 42509 42513
101. P.H. McDonald, N.L. Cote, F.T. Lin, R.T. Premont, J.A. Pitcher, and R.J. Lefkowitz Identification of NSF as a beta-arrestin1-binding protein. Implications for beta2-adrenergic receptor regulation J Biol Chem 274 1999 10677 10680