Abstract
G-protein-coupled receptors (GPCRs) are the primary interaction partners for arrestins. The visual arrestins, arrestin1 and arrestin4, physiologically bind to only very few receptors, i.e., rhodopsin and the color opsins, respectively. In contrast, the ubiquitously expressed nonvisual variants β-arrestin1 and 2 bind to a large number of receptors in a fairly nonspecific manner. This binding requires two triggers, agonist activation and receptor phosphorylation by a G-protein-coupled receptor kinase (GRK). These two triggers are mediated by two different regions of the arrestins, the “phosphorylation sensor” in the core of the protein and a less well-defined “activation sensor.” Binding appears to occur mostly in a 1:1 stoichiometry, involving the N-terminal domain of GPCRs, but in addition a second GPCR may loosely bind to the C-terminal domain when active receptors are abundant.
Arrestin binding initially uncouples GPCRs from their G-proteins. It stabilizes receptors in an active conformation and also induces a conformational change in the arrestins that involves a rotation of the two domains relative to each other plus changes in the polar core. This conformational change appears to permit the interaction with further downstream proteins. The latter interaction, demonstrated mostly for β-arrestins, triggers receptor internalization as well as a number of nonclassical signaling pathways.
Open questions concern the exact stoichiometry of the interaction, possible specificity with regard to the type of agonist and of GRK involved, selective regulation of downstream signaling (=biased signaling), and the options to use these mechanisms as therapeutic targets.
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References
Abe T, Yamaki K, Tsuda M, Singh VK, Suzuki S, McKinnon R, Klein DC, Donoso LA, Shinohara T (1989) Rat pineal S-antigen: sequence analysis reveals presence of α-transducin homologous sequence. FEBS Lett 2:307–311
Alvarez CE (2008) On the origins of arrestin and rhodopsin. BMC Evol Biol 8:222
Ambrosio M, Lohse MJ (2010) Microscopy: GPCR dimers moving closer. Nat Chem Biol 6:570–571
Arshavsky VY (2002) Rhodopsin phosphorylation: from terminating single photon responses to photoreceptor dark adaptation. Trends Neurosci 25:124–126
Arshavsky VY, Bownds MD (1992) Regulation of deactivation of photoreceptor G protein by its target enzyme and cGMP. Nature 357:416–417
Attramadal H, Lohse MJ, Caron MG, Lefkowitz RJ (1992a) βArrestin2 – a novel member of a family of proteins that regulate receptor coupling to G proteins. Clin Res 40:A190
Attramadal H, Arriza JL, Aoki C, Dawson TM, Codina J, Kwatra MM, Snyder SH, Caron MG, Lefkowitz RJ (1992b) β-arrestin2, a novel member of the arrestin/β-arrestin gene family. J Biol Chem 267:17882–17890
Aubry L, Klein G (2013) True arrestins and arrestin-fold proteins: a structure-based appraisal. Prog Mol Biol Transl Sci 118:21–56
Aubry L, Guetta D, Klein G (2009) The arrestin fold: variations on a theme. Curr Genomics 10:133–142
Barak LS, Ferguson SS, Zhang J, Caron MG (1997) A β-arrestin/green fluorescent protein biosensor for detecting G protein-coupled receptor activation. J Biol Chem 272:27497–27500
Bayburt TH, Leitz AJ, Xie G, Oprian DD, Sligar SG (2007) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J Biol Chem 282:14875–14881
Bayburt TH, Vishnivetskiy SA, McLean MA, Morizumi T, Huang CC, Tesmer JJ, Ernst OP, Sligar SG, Gurevich VV (2011) Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding. J Biol Chem 286:1420–1428
Benovic JL, Strasser RH, Caron MG, Lefkowitz RJ (1986a) β-Adrenergic receptor kinase: identification of a novel protein kinase that phosphorylates the agonist-occupied form of the receptor. Proc Natl Acad Sci USA 83:2797–2801
Benovic JL, Mayor F Jr, Somers RL, Caron MG, Lefkowitz RJ (1986b) Light-dependent phosphorylation of rhodopsin by β-adrenergic receptor kinase. Nature 322:869–872
Benovic JL, Mayor F Jr, Staniszewski C, Lefkowitz RJ, Caron MG (1987a) Purification and characterization of the ß-adrenergic receptor kinase. J Biol Chem 262:9026–9032
Benovic JL, Kühn H, Weyand I, Codina J, Caron MG, Lefkowitz RJ (1987b) Functional desensitization of the isolated β-adrenergic receptor by the β-adrenergic receptor kinase: Potential role of an analog of the retinal protein arrestin (48 kDa protein). Proc Natl Acad Sci USA 84:8879–8882
Benovic JL, Staniszewski C, Mayor F Jr, Caron MG, Lefkowitz RJ (1988) β-Adrenergic receptor kinase. Activity of partial agonists for stimulation of adenylate cyclase correlates with ability to promote receptor phosphorylation. J Biol Chem 263:3893–3897
Benovic JL, DeBlasi A, Stone WC, Caron MG, Lefkowitz RJ (1989) β-Adrenergic receptor kinase: primary structure delineates a multigene family. Science 246:235–240
Benovic JL, Onorato JJ, Arriza JL, Stone CW, Lohse MJ, Jenkins N, Gilbert NG, Caron MG, Lefkowitz RJ (1991) Cloning, expression and chromosomal localization of β-adrenergic receptor kinase 2: a new member of the receptor kinase family. J Biol Chem 266:14939–14946
Bertrand L, Parent S, Caron M, Legault M, Joly E, Angers S, Bouvier M, Brown M, Houle B, Ménard L (2002) The BRET2/arrestin assay in stable recombinant cells: a platform to screen for compounds that interact with G protein-coupled receptors (GPCRs). J Recept Signal Transduct Res 22:533–541
Blaukat A, Alla SA, Lohse MJ, Müller-Esterl W (1996) Ligand-induced phosphorylation/dephosphorylation of the endogenous bradykinin B2 receptor from human fibroblasts. J Biol Chem 271:32366–32374
Bockaert J, Pin JP (1999) Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J 18:1723–1729
Bonner TI, Buckley NJ, Young AC, Brann MR (1987) Identification of a family of muscarinic acetylcholine receptor genes. Science 237:527–532
Broekhuyse RM, Tolhuizen EF, Janssen AP, Winkens HJ (1985) Light induced shift and binding of S-antigen in retinal rods. Curr Eye Res 4:613–618
Calebiro D, Nikolaev VO, Gagliani MC, de Filippis T, Dees C, Tacchetti C, Persani L, Lohse MJ (2009) Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol 7:e1000172
Calebiro D, Nikolaev VO, Persani L, Lohse MJ (2010) Signaling by internalized G-protein-coupled receptors. Trends Pharmacol Sci 31:221–228
Charest PG, Terrillon S, Bouvier M (2005) Monitoring agonist-promoted conformational changes of β-arrestin in living cells by intramolecular BRET. EMBO Rep 6:334–340
Clark RB, Rich TC (2003) Probing the roles of protein kinases in g-protein-coupled receptor desensitization. Mol Pharmacol 64:1015–1017
Craft CM, Whitmore DH (1995) The arrestin superfamily: cone arrestins are a fourth family. FEBS Lett 362:247–255
Craft CM, Whitmore DH, Wiechmann AF (1994) Cone arrestin identified by targeting expression of a functional family. J Biol Chem 269:4613–4619
Damian M, Martin A, Mesnier D, Pin JP, Banères JL (2006) Asymmetric conformational changes in a GPCR dimer controlled by G-proteins. EMBO J 25:5693–5702
De Lean A, Stadel JM, Lefkowitz RJ (1980) A ternary complex model explains the agonist-specific binding properties of the adenylate cyclase-coupled β-adrenergic receptor. J Biol Chem 255:7108–7117
DeFea KA, Zalevsky J, Thoma MS, Déry O, Mullins RD, Bunnett NW (2000) β-Arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2. J Cell Biol 148:1267–1281
Dicker F, Quitterer U, Winstel R, Honold K, Lohse MJ (1999) Phosphorylation-independent inhibition of PTH receptor function by G-protein-coupled receptor kinases. Proc Natl Acad Sci USA 96:5476–5481
Dinculescu A, McDowell JH, Amici SA, Dugger DR, Richards N, Hargrave PA, Smith WC (2002) Insertional mutagenesis and immunochemical analysis of visual arrestin interaction with rhodopsin. J Biol Chem 277:11703–11708
Dixon RAF, Kobilka BK, Strader DJ, Benovic JL, Dohlman HG, Frielle T, Bolanowski MA, Bennett CD, Rands E, Diehl RE, Mumford RA, Slater EE, Sigal ES, Caron MG, Lefkowitz RJ, Strader CD (1986) Cloning of the gene and cDNA for mammalian β-adrenergic receptor and homology with rhodopsin. Nature 321:75–79
Dohlman HG, Bouvier M, Benovic JL, Caron MG, Lefkowitz RJ (1987) The multiple membrane spanning topography of the β2-adrenergic receptor. Localization of the sites of binding, glycosylation, and regulatory phosphorylation by limited proteolysis. J Biol Chem 262:14282–14288
Dorey C, Faure JP (1977) Isolement et caractérisation partielle d’un antigène rétinien responsable de l’uveorétinite autoimmune expérimentale. Ann Immunol (Paris) 128:229–232
Drake MT, Violin JD, Whalen EJ, Wisler JW, Shenoy SK, Lefkowitz RJ (2008) β-Arrestin-biased agonism at the β2-adrenergic receptor. J Biol Chem 283:5669–5676
Elschnig A (1910) Studien zur sympathischen Ophthalmie: 2. Die antigene Wirkung des Augenpigmentes. Albrecht Von Graefes Arch Ophthalmol 76:509–546
Engelman DM, Goldman A, Steitz TA (1982) The identification of helical segments in the polypeptide chain of bacteriorhodopsin. Methods Enzymol 88:81–88
Engelman DM, Goldman A, Steitz TA (1986) Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu Rev Biophys Biophys Chem 15:321–353
Faure JP, Mirshahi M, Dorey C, Thillaye B, de Kozak Y, Bouchaix C (1984) Production and specificity of monoclonal antibodies to retinal S antigen. Curr Eye Res 3:867–872
Ferguson SS, Downey WE III, Colapietro AM, Barak LS, Menard L, Caron MG (1996) Role of β-arrestin in mediating agonist-promoted G-protein-coupled receptor internalization. Science 271:363–366
Ferrandon S, Feinstein TN, Castro M, Wang B, Bouley R, Potts JT, Gardella TJ, Vilardaga JP (2009) Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat Chem Biol 5:734–742
Fotiadis D, Jastrzebska B, Philippsen A, Müller DJ, Palczewski K, Engel A (2006) Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr Opin Struct Biol 16:252–259
Fukuda K, Kubo T, Akiba I, Maeda A, Mishina M, Numa S (1987) Molecular distinction between muscarinic acetylcholine receptor subtypes. Nature 327:623–625
Fung BK, Hurley JB, Stryer L (1981) Flow of information in the light-triggered cyclic nucleotide cascade of vision. Proc Natl Acad Sci USA 78:152–156
Galliera E, Jala VR, Trent JO, Bonecchi R, Signorelli P, Lefkowitz RJ, Mantovani A, Locati M, Haribabu B (2004) β-Arrestin-dependent constitutive internalization of the human chemokine decoy receptor D6. J Biol Chem 279:25590–25597
Gilman AG (1984) G proteins and dual control of adenylate cyclase. Cell 36:577–579
Gimenez LE, Vishnivetskiy SA, Baameur F, Gurevich VV (2012) Manipulation of very few receptor discriminator residues greatly enhances receptor specificity of non-visual arrestins. J Biol Chem 287:29495–29505
Godovac-Zimmermann J, Soskic V, Poznanovic S, Brianza F (1999) Functional proteomics of signal transduction by membrane receptors. Electrophoresis 20:952–961
Goodman OB Jr, Krupnick JG, Santini F, Gurevich VV, Penn RB, Gagnon AW, Keen JH, Benovic JL (1996) β-Arrestin acts as a clathrin adapter in endocytosis of the β2-adrenergic receptor. Nature 383:447–450
Granzin J, Wilden U, Choe HW, Labahn J, Krafft B, Büldt G (1998) X-ray crystal structure of arrestin from bovine rod outer segments. Nature 391:918–921
Granzin J, Cousin A, Weirauch M, Schlesinger R, Büldt G, Batra-Safferling R (2012) Crystal structure of p44, a constitutively active splice variant of visual arrestin. J Mol Biol 416:611–618
Gray-Keller MP, Detwiler PB, Benovic JL, Gurevich VV (1997) Arrestin with a single amino acid substitution quenches light-activated rhodopsin in a phosphorylation-independent fashion. Biochemistry 36:7058–7063
Gurevich VV, Benovic JL (1992) Cell-free expression of visual arrestin: truncation mutagenesis identifies multiple domains involved in rhodopsin interaction. J Biol Chem 267:21919–21923
Gurevich VV, Benovic JL (1993) Visual arrestin interaction with rhodopsin. Sequential multisite binding ensures strict selectivity toward light-activated phosphorylated rhodopsin. J Biol Chem 268:11628–11638
Gurevich VV, Benovic JL (1995) Visual arrestin binding to rhodopsin. Diverse functional roles of positively charged residues within the phosphorylation-recognition region of arrestin. J Biol Chem 270:6010–6016
Gurevich VV, Benovic JL (1997) Mechanism of phosphorylation-recognition by visual arrestin and the transition of arrestin into a high affinity binding state. Mol Pharmacol 51:161–169
Gurevich VV, Gurevich EV (2004) The molecular acrobatics of arrestin activation. Trends Pharmacol Sci 25:105–111
Gurevich VV, Gurevich EV (2006) The structural basis of arrestin-mediated regulation of G-protein-coupled receptors. Pharmacol Ther 110:465–502
Gurevich VV, Gurevich EV (2013) Structural determinants of arrestin functions. Prog Mol Biol Transl Sci 118:57–92
Gurevich VV, Richardson RM, Kim CM, Hosey MM, Benovic JL (1993) Binding of wild type and chimeric arrestins to the m2 muscarinic cholinergic receptor. J Biol Chem 268:16879–16882
Gurevich VV, Chen C-Y, Kim CM, Benovic JL (1994) Visual arrestin binding to rhodopsin. Intramolecular interaction between the basic N terminus and acidic C terminus of arrestin may regulate binding selectivity. J Biol Chem 269:8721–8727
Gurevich VV, Dion SB, Onorato JJ, Ptasienski J, Kim CM, Sterne-Marr R, Hosey MM, Benovic JL (1995) Arrestin interactions with G protein-coupled receptors. Direct binding studies of wild type and mutant arrestins with rhodopsin, β2-adrenergic, and m2 muscarinic cholinergic receptors. J Biol Chem 270:720–731
Gurevich VV, Pals-Rylaarsdam R, Benovic JL, Hosey MM, Onorato JJ (1997) Agonist-receptor-arrestin, an alternative ternary complex with high agonist affinity. J Biol Chem 272:28849–28852
Gurevich VV, Hanson SM, Song X, Vishnivetskiy SA, Gurevich EV (2011) The functional cycle of visual arrestins in photoreceptor cells. Prog Retin Eye Res 30:405–430
Han M, Gurevich VV, Vishnivetskiy SA, Sigler PB, Schubert C (2001) Crystal structure of β-arrestin at 1.9 A: possible mechanism of receptor binding and membrane translocation. Structure 9:869–880
Han SO, Kommaddi RP, Shenoy SK (2013) Distinct roles for β-arrestin2 and arrestin-domain-containing proteins in β2 adrenergic receptor trafficking. EMBO Rep 14:164–171
Hanson SM, Francis DJ, Vishnivetskiy SA, Kolobova EA, Hubbell WL, Klug CS, Gurevich VV (2006) Differential interaction of spin-labeled arrestin with inactive and active phosphorhodopsin. Proc Natl Acad Sci USA 103:4900–4905
Hanson SM, Gurevich EV, Vishnivetskiy SA, Ahmed MR, Song X, Gurevich VV (2007a) Each rhodopsin molecule binds its own arrestin. Proc Natl Acad Sci USA 104:3125–3128
Hanson SM, Van Eps N, Francis DJ, Altenbach C, Vishnivetskiy SA, Arshavsky VY, Klug CS, Hubbell WL, Gurevich VV (2007b) Structure and function of the visual arrestin oligomer. EMBO J 26:1726–1736
Hanson SM, Vishnivetskiy SA, Hubbell WL, Gurevich VV (2008) Opposing effects of inositol hexakisphosphate on rod arrestin and arrestin2 self-association. Biochemistry 47:1070–1075
Hargrave PA, McDowell JH, Curtis DR, Wang JK, Juszczak E, Fong SL, Rao JK, Argos P (1983) The structure of bovine rhodopsin. Biophys Struct Mech 9:235–244
Hein P, Frank M, Hoffmann C, Lohse MJ, Bünemann M (2005) Dynamics of receptor/G protein coupling in living cells. EMBO J 24:4106–4114
Hein P, Rochais F, Hoffmann C, Dorsch S, Nikolaev VO, Engelhardt S, Berlot CH, Lohse MJ, Bünemann M (2006) Gs Activation is time-limiting in initiating receptor-mediated signaling. J Biol Chem 281:33345–33351
Hekman M, Feder D, Keenan AK, Gal A, Klein HW, Pfeuffer T, Levitzki A, Helmreich EJM (1984) Reconstitution of β-adrenergic receptor with components of adenylate cyclase. EMBO J 3:3339–3345
Henderson R, Unwin PN (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257:28–32
Hirsch JA, Schubert C, Gurevich VV, Sigler PB (1999) The 2.8 Å crystal structure of visual arrestin: a model for arrestin’s regulation. Cell 97:257–269
Hoffmann C, Ziegler N, Reiner S, Krasel C, Lohse MJ (2008a) Agonist-selective, receptor-specific interaction of human P2Y receptors with β-arrestin-1 and -2. J Biol Chem 283:30933–30941
Hoffmann C, Zürn A, Bünemann M, Lohse MJ (2008b) Conformational changes in G-protein-coupled receptors – the quest for functionally selective conformations is open. Br J Pharmacol 153:S358–S366
Ibrahim IA, Kurose H (2012) β-arrestin-mediated signaling improves the efficacy of therapeutics. J Pharmacol Sci 118:408–412
Irannejad R, Tomshine JC, Tomshine JR, Chevalier M, Mahoney JP, Steyaert J, Rasmussen SG, Sunahara RK, El-Samad H, Huang B, von Zastrow M (2013) Conformational biosensors reveal GPCR signalling from endosomes. Nature 495:534–538
Jala VR, Shao WH, Haribabu B (2005) Phosphorylation-independent β-arrestin translocation and internalization of leukotriene B4 receptors. J Biol Chem 280:4880–4887
Jorgensen R, Martini L, Schwartz TW, Elling CE (2005) Characterization of glucagon-like peptide-1 receptor β-arrestin 2 interaction: a high-affinity receptor phenotype. Mol Endocrinol 19:812–823
Kang DS, Tian X, Benovic JL (2013) β-Arrestins and G protein-coupled receptor trafficking. Methods Enzymol 521:91–108
Kennedy MJ, Lee KA, Niemi GA, Craven KB, Garwin GG, Saari JC, Hurley JB (2001) Multiple phosphorylation of rhodopsin and the in vivo chemistry underlying rod photoreceptor dark adaptation. Neuron 31:87–101
Key TA, Bennett TA, Foutz TD, Gurevich VV, Sklar LA, Prossnitz ER (2001) Regulation of formyl peptide receptor agonist affinity by reconstitution with arrestins and heterotrimeric G proteins. J Biol Chem 276:49204–49212
Kieselbach T, Irrgang KD, Ruppel H (1994) A segment corresponding to amino acids Val170-Arg182 of bovine arrestin is capable of binding to phosphorylated rhodopsin. Eur J Biochem 226:87–97
Kim KS, Abraham D, Williams B, Violin JD, Mao L, Rockman HA (2012a) β-Arrestin-biased AT1R stimulation promotes cell survival during acute cardiac injury. Am J Physiol Heart Circ Physiol 303:H1001–H1010
Kim M, Vishnivetskiy SA, Van Eps N, Alexander NS, Cleghorn WM, Zhan X, Hanson SM, Morizumi T, Ernst OP, Meiler J, Gurevich VV, Hubbell WL (2012b) Conformation of receptor-bound visual arrestin. Proc Natl Acad Sci USA 109:18407–18412
Kim YJ, Hofmann KP, Ernst OP, Scheerer P, Choe HW, Sommer ME (2013) Crystal structure of pre-activated arrestin p44. Nature 497:142–146
Klenk C, Vetter T, Zürn A, Vilardaga JP, Friedman PA, Wang B, Lohse MJ (2010) Formation of a ternary complex between NHERF1, β-arrestin, and parathyroid hormone receptor. J Biol Chem 285:30355–30362
Kohl B, Hofmann KP (1987) Temperature dependence of G-protein activation in photoreceptor membranes. Transient extra metarhodopsin II on bovine disk membranes. Biophys J 52:271–277
Krasel C, Bünemann M, Lorenz K, Lohse MJ (2005) β-Arrestin binding to the β2-adrenergic receptor requires both receptor phosphorylation and receptor activation. J Biol Chem 280:9528–9535
Krasel C, Zabel U, Lorenz K, Reiner S, Al-Sabah S, Lohse MJ (2008) Dual role of the β2-adrenergic receptor C-terminus for the binding of β-arrestin and receptor internalization. J Biol Chem 283:31840–31848
Krueger KM, Daaka Y, Pitcher JA, Lefkowitz RJ (1997) The role of sequestration in G protein-coupled receptor resensitization. Regulation of β2-adrenergic receptor dephosphorylation by vesicular acidification. J Biol Chem 272:5–8
Krupnick JG, Benovic JL (1998) The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu Rev Pharmacol Toxicol 38:289–319
Kubo T, Fukuda K, Mikami A, Maeda A, Takahashi H, Mishina M, Haga T, Haga K, Ichiyama A, Kangawa K, Kojima M, Matsuo H, Hirose T, Numa S (1986) Cloning, sequencing and expression of complementary DNA encoding the muscarinic acetylcholine receptor. Nature 323:411–416
Kühn H (1974) Light-dependent phosphorylation of rhodopsin in living frogs. Nature 250:588–590
Kühn H (1978) Light-regulated binding of rhodopsin kinase and other proteins to cattle photoreceptor membranes. Biochemistry 17:4389–4395
Kühn H (1984) Interactions between photoexcited rhodopsin and light-activated enzymes in rods. In: Osborne N, Chader J (eds) Progress in retinal research, vol 3. Pergamon, New York, pp 123–156
Kühn H, Dreyer WJ (1972) Light-dependent phosphorylation of rhodopsin by ATP. FEBS Lett 20:1–6
Kühn H, Wilden U (1987) Deactivation of photoactivated rhodopsin by rhodopsin-kinase and arrestin. J Recept Res 7:283–298
Kühn H, Hall SW, Wilden U (1984) Light-induced binding of 48-kDa protein to photoreceptor membranes is highly enhanced by phosphorylation of rhodopsin. FEBS Lett 176:473–478
Lamb TD, Pugh EN Jr (2004) Dark adaptation and the retinoid cycle of vision. Prog Retin Eye Res 23:307–380
Leduc M, Hou X, Hamel D, Sanchez M, Quiniou C, Honoré JC, Roy O, Madaan A, Lubell W, Varma DR, Mancini J, Duhamel F, Peri KG, Pichette V, Heveker N, Chemtob S (2013) Restoration of renal function by a novel prostaglandin EP4 receptor-derived peptide in models of acute renal failure. Am J Physiol Regul Integr Comp Physiol 304:R10–R22
Lefkowitz RJ, Shenoy SK (2005) Transduction of receptor signals by β-arrestins. Science 308:512–517
Lefkowitz RJ, Stadel JM, Caron MG (1983) Adenylate cyclase-coupled β-adrenergic receptors: structure and mechanisms of activation and desensitization. Annu Rev Biochem 52:159–186
Liggett SB (2011) Phosphorylation barcoding as a mechanism of directing GPCR signaling. Sci Signal 4:pe36
Liggett SB, Ostrowski J, Chesnut LC, Kurose H, Raymond JR, Caron MG, Lefkowitz RJ (1992) Sites in the third intracellular loop of the alpha 2A-adrenergic receptor confer short term agonist-promoted desensitization. Evidence for a receptor kinase-mediated mechanism. J Biol Chem 267:4740–4746
Lin FT, Miller WE, Luttrell LM, Lefkowitz RJ (1999) Feedback regulation of beta-arrestin1 function by extracellular signal-regulated kinases. J Biol Chem 274:15971–15974
Lin FT, Chen W, Shenoy S, Cong M, Exum ST, Lefkowitz RJ (2002) Phosphorylation of β-arrestin2 regulates its function in internalization of β2-adrenergic receptors. Biochemistry 41:10692–10699
Lin CH, MacGurn JA, Chu T, Stefan CJ, Emr SD (2008) Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135:714–725
Lohse MJ (1993) Molecular mechanisms of membrane receptor desensitization. Biochim Biophys Acta 1179:171–188
Lohse MJ (2010) Dimerization in GPCR mobility and signaling. Curr Opin Pharmacol 10:53–58
Lohse MJ, Calebiro D (2013) Receptor signals come in waves. Nature 495:457–458
Lohse MJ, Klenk C (2008) Blocking them all: β-arrestins inhibit cellular signaling. Mol Cell 31:619–621
Lohse MJ, Lenschow V, Schwabe U (1984) Two affinity states of Ri adenosine receptors in brain membranes: analysis of guanine nucleotide and temperature effects on radioligand binding. Mol Pharmacol 26:1–9
Lohse MJ, Lefkowitz RJ, Caron MG, Benovic JL (1989) Inhibition of β-adrenergic receptor kinase prevents rapid homologous desensitization of β2-adrenergic receptors. Proc Natl Acad Sci USA 86:3011–3015
Lohse MJ, Benovic JL, Caron MG, Lefkowitz RJ (1990a) Multiple pathways of rapid β2-adrenergic receptor desensitization: delineation with specific inhibitors. J Biol Chem 265:3202–3209
Lohse MJ, Benovic JL, Codina J, Caron MG, Lefkowitz RJ (1990b) β-Arrestin: a protein that regulates β-adrenergic function. Science 248:1547–1550
Lohse MJ, Andexinger S, Pitcher J, Trukawinski S, Codina J, Faure JP, Caron MG, Lefkowitz RJ (1992) Receptor-specific desensitization with purified proteins: kinase dependence and receptor-specificity of β-arrestin and arrestin in the β2-adrenergic receptor and rhodopsin systems. J Biol Chem 267:8558–8564
Lohse MJ, Krasel C, Winstel R, Mayor F Jr (1996) G-protein-coupled receptor kinases. Kidney Int 49:1047–1052
Lohse MJ, Nikolaev VO, Hein P, Hoffmann C, Vilardaga JP, Bünemann M (2008) Optical techniques to analyze real-time activation and signaling of G-protein-coupled receptors. Trends Pharmacol Sci 29:159–165
Lorenz W, Inglese J, Palczewski K, Onorato JJ, Caron MG, Lefkowitz RJ (1991) The receptor kinase family: primary structure of rhodopsin kinase reveals similarities to the β-adrenergic receptor kinase. Proc Natl Acad Sci USA 88:8715–8719
Luttrell LM, Roudabush FL, Choy EW, Miller WE, Field ME, Pierce KL, Lefkowitz RJ (2001) Activation and targeting of extracellular signal-regulated kinases by β-arrestin scaffolds. Proc Natl Acad Sci USA 98:2449–2454
Malik RU, Ritt M, DeVree BT, Neubig RR, Sunahara RK, Sivaramakrishnan S (2013) Detection of G protein-selective G protein-coupled receptor (GPCR) conformations in live cells. J Biol Chem 288:17167–17178
Marion S, Oakley RH, Kim KM, Caron MG, Barak LS (2006) A β-arrestin binding determinant common to the second intracellular loops of rhodopsin family G protein-coupled receptors. J Biol Chem 281:2932–2938
Martini L, Hastrup H, Holst B, Fraile-Ramos A, Marsh M, Schwartz TW (2002) NK1 receptor fused to β-arrestin displays a single-component, high-affinity molecular phenotype. Mol Pharmacol 62:30–37
Mary S, Damian M, Louet M, Floquet N, Fehrentz JA, Marie J, Martinez J, Banères JL (2012) Ligands and signaling proteins govern the conformational landscape explored by a G protein-coupled receptor. Proc Natl Acad Sci USA 109:8304–8309
Matesic D, Liebman PA (1987) cGMP-dependent cation channel of retinal rod outer segments. Nature 326:600–603
Maurice P, Kamal M, Jockers R (2011) Asymmetry of GPCR oligomers supports their functional relevance. Trends Pharmacol Sci 32:514–520
McDonald PH, Chow CW, Miller WE, Laporte SA, Field ME, Lin FT, Davis RJ, Lefkowitz RJ (2000) β-Arrestin 2: a receptor-regulated MAPK scaffold for the activation of JNK3. Science 290:1574–1577
McDowell JH, Kühn H (1977) Light-induced phosphorylation of rhodopsin in cattle photoreceptor membranes: substrate activation and inactivation. Biochemistry 16:4054–4060
Menard L, Ferguson SS, Zhang J, Lin FT, Lefkowitz RJ, Caron MG, Barak LS (1997) Synergistic regulation of β2-adrenergic receptor sequestration: intracellular complement of β-adrenergic receptor kinase and β-arrestin determine kinetics of internalization. Mol Pharmacol 51:800–808
Miki N, Keirns JJ, Marcus FR, Freeman J, Bitensky MW (1973) Regulation of cyclic nucleotide concentrations in photoreceptors: an ATP-dependent stimulation of cyclic nucleotide phosphodiesterase by light. Proc Natl Acad Sci USA 70:3820–3824
Miki N, Baraban JM, Keirns JJ, Boyce JJ, Bitensky MW (1975) Purification and properties of the light-activated cyclic nucleotide phosphodiesterase of rod outer segments. J Biol Chem 250:6320–6327
Milano SK, Pace HC, Kim YM, Brenner C, Benovic JL (2002) Scaffolding functions of arrestin-2 revealed by crystal structure and mutagenesis. Biochemistry 41:3321–3328
Moore CA, Milano SK, Benovic JL (2007) Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol 69:451–482
Mukherjee S, Palczewski K, Gurevich V, Benovic JL, Banga JP, Hunzicker-Dunn M (1999) A direct role for arrestins in desensitization of the luteinizing hormone/choriogonadotropin receptor in porcine ovarian follicular membranes. Proc Natl Acad Sci USA 96:493–498
Mukherjee S, Gurevich VV, Preninger A, Hamm HE, Bader MF, Fazleabas AT, Birnbaumer L, Hunzicker-Dunn M (2002) 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 277:17916–17927
Müller S, Hekman M, Lohse MJ (1993) Specific enhancement of β-adrenergic receptor kinase activity by defined G-protein β and γ subunits. Proc Natl Acad Sci USA 90:10439–10443
Mullershausen F, Zecri F, Cetin C, Billich A, Guerini D, Seuwen K (2009) Persistent signaling induced by FTY720-phosphate is mediated by internalized S1P1 receptors. Nat Chem Biol 5:428–434
Murakami A, Yajima T, Sakuma H, McLaren MJ, Inana G (1993) X-arrestin: a new retinal arrestin mapping to the X-chromosome. FEBS Lett 334:203–209
Nabhan JF, Pan H, Lu Q (2010) Arrestin domain-containing protein 3 recruits the NEDD4 E3 ligase to mediate ubiquitination of the β2-adrenergic receptor. EMBO Rep 11:605–611
Nathans J, Hogness DS (1983) Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell 34:807–814
Nathans J, Hogness DS (1984) Isolation and nucleotide sequence of the gene encoding human rhodopsin. Proc Natl Acad Sci USA 81:4851–4855
Nikko E, Sullivan JA, Pelham HR (2008) Arrestin-like proteins mediate ubiquitination and endocytosis of the yeast metal transporter Smf1. EMBO Rep 9:1216–1221
Nikolaev VO, Hoffmann C, Bünemann M, Lohse MJ, Vilardaga JP (2006) Molecular basis of partial agonism at the neurotransmitter α2A-adrenergic receptor and Gi-protein heterotrimer. J Biol Chem 281:24506–24511
Nikonov SS, Brown BM, Davis JA, Zuniga FI, Bragin A, Pugh EN Jr, Craft CM (2008) Mouse cones require an arrestin for normal inactivation of phototransduction. Neuron 59:462–474
Nobles KN, Xiao K, Ahn S, Shukla AK, Lam CM, Rajagopal S, Strachan RT, Huang TY, Bressler EA, Hara MR, Shenoy SK, Gygi SP, Lefkowitz RJ (2011) Distinct phosphorylation sites on the β2-adrenergic receptor establish a barcode that encodes differential functions of β-arrestin. Sci Signal 4:ra51
Nygaard R, Zou Y, Dror RO, Mildorf TJ, Arlow DH, Manglik A, Pan AC, Liu CW, Fung JJ, Bokoch MP, Thian FS, Kobilka TS, Shaw DE, Mueller L, Prosser RS, Kobilka BK (2013) The dynamic process of β2-adrenergic receptor activation. Cell 152:532–542
Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG (1999) Association of β-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J Biol Chem 274:32248–32257
Oakley RH, Laporte SA, Holt JA, Caron MG, Barak LS (2000) Differential affinities of visual arrestin, β-arrestin1, and β-arrestin2 for G protein-coupled receptors delineate two major classes of receptors. J Biol Chem 275:17201–17210
Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG (2001) Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor-β-arrestin complexes after receptor endocytosis. J Biol Chem 276:19452–19460
Ohguro H, Johnson RS, Ericsson LH, Walsh KA, Palczewski K (1994a) Control of rhodopsin multiple phosphorylation. Biochemistry 33:1023–1028
Ohguro H, Palczewski K, Walsh KA, Johnson RS (1994b) Topographic study of arrestin using differential chemical modifications and hydrogen/deuterium exchange. Protein Sci 3:2428–2434
Ovchinnikov YA (1982) Rhodopsin and bacteriorhodopsin: structure-function relationship. FEBS Lett 148:179–191
Ovchinnikov YA, Abdulaev NG, Feigina MY, Artamonov ID, Zolotarev AS, Kostina MB, Bogachuk AS, Miroshnikov AI, Martinov VI, Kudelin AB (1982) Bioorg Khim 8:1011–1014
Ozawa K, Whalen EJ, Nelson CD, Mu Y, Hess DT, Lefkowitz RJ, Stamler JS (2008) S-nitrosylation of β-arrestin regulates β-adrenergic receptor trafficking. Mol Cell 31:395–405
Palczewski K, Buczyłko J, Imami NR, McDowell JH, Hargrave PA (1991a) Role of the carboxyl-terminal region of arrestin in binding to phosphorylated rhodopsin. J Biol Chem 266:15334–15339
Palczewski K, Buczyłko J, Kaplan MW, Polans AS, Crabb JW (1991b) Mechanism of rhodopsin kinase activation. J Biol Chem 266:12949–12955
Palczewski K, Pulvermüller A, Buczyłko J, Hofmann KP (1991c) Phosphorylated rhodopsin and heparin induce similar conformational changes in arrestin. J Biol Chem 266:18649–18654
Palczewski K, Buczylko J, Ohguro H, Annan RS, Carr SA, Crabb JW, Kaplan MW, Johnson RS, Walsh KA (1994) Characterization of a truncated form of arrestin isolated from bovine rod outer segments. Protein Sci 3:314–324
Pals-Rylaarsdam R, Gurevich VV, Lee KB, Ptasienski JA, Benovic JL, Hosey MM (1997) Internalization of the m2 muscarinic acetylcholine receptor. Arrestin-independent and -dependent pathways. J Biol Chem 272:23682–23689
Patwari P, Lee RT (2012) An expanded family of arrestins regulate metabolism. Trends Endocrinol Metab 23:216–222
Patwari P, Emilsson V, Schadt EE, Chutkow WA, Lee S, Marsili A, Zhang Y, Dobrin R, Cohen DE, Larsen PR, Zavacki AM, Fong LG, Young SG, Lee RT (2011) The arrestin domain-containing 3 protein regulates body mass and energy expenditure. Cell Metab 14:671–683
Peralta EG, Winslow JW, Peterson GL, Smith DH, Ashkenazi A, Ramachandran J, Schimerlik MI, Capon DJ (1987) Primary structure and biochemical properties of an M2 muscarinic receptor. Science 236:600–605
Pfister C, Chabre M, Plouet J, Tuyen VV, De Kozak Y, Faure JP, Kühn H (1985) Retinal S antigen identified as the 48K protein regulating light-dependent phosphodiesterase in rods. Science 228:891–893
Pfleger KD, Eidne KA (2003) New technologies: bioluminescence resonance energy transfer (BRET) for the detection of real time interactions involving G-protein coupled receptors. Pituitary 6:141–151
Pfleger KD, Dalrymple MB, Dromey JR, Eidne KA (2007) Monitoring interactions between G-protein-coupled receptors and β-arrestins. Biochem Soc Trans 35:764–766
Pin JP, Neubig R, Bouvier M, Devi L, Filizola M, Javitch JA, Lohse MJ, Milligan G, Palczewski K, Parmentier M, Spedding M (2007) International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers. Pharmacol Rev 59:5–13
Pippig S, Andexinger S, Daniel K, Puzicha M, Caron MG, Lefkowitz RJ, Lohse MJ (1993) Overexpression of β-adrenergic receptor kinase and β-arrestin augment homologous desensitization of β2-adrenergic receptors. J Biol Chem 268:3201–3208
Pippig S, Andexinger S, Lohse MJ (1995) Sequestration and recycling of β2-adrenergic receptors permit receptor resensitization. Mol Pharmacol 47:666–676
Pitcher J, Lohse MJ, Codina J, Caron MG, Lefkowitz RJ (1992a) Desensitization of the isolated β2-adrenergic receptor by βAR kinase, cAMP-dependent protein kinase and protein kinase C occurs via distinct molecular mechanisms. Biochemistry 31:3193–3197
Pitcher JA, Inglese J, Higgins JB, Arriza JL, Casey PJ, Kim C, Benovic JL, Kwatra MM, Caron MG, Lefkowitz RJ (1992b) Role of βγ-subunits of G proteins in targeting the β-adrenergic receptor kinase to membrane-bound receptors. Science 257:1264–1267
Pitcher JA, Freedman NJ, Lefkowitz RJ (1998) G protein-coupled receptor kinases. Annu Rev Biochem 67:653–692
Pulvermüller A, Maretzki D, Rudnicka-Nawrot M, Smith WC, Palczewski K, Hofmann KP (1997) Functional differences in the interaction of arrestin and its splice variant, p44, with rhodopsin. Biochemistry 36:9253–9260
Pulvermüller A, Schröder K, Fischer T, Hofmann KP (2000) Interactions of metarhodopsin II. Arrestin peptides compete with arrestin and transducin. J Biol Chem 275:37679–37685
Qi AD, Houston-Cohen D, Naruszewicz I, Harden TK, Nicholas RA (2011) Ser352 and Ser354 in the carboxyl terminus of the human P2Y1 receptor are required for agonist-promoted phosphorylation and internalization in MDCK cells. Br J Pharmacol 162:1304–1313
Rajagopal S, Rajagopal K, Lefkowitz RJ (2010) Teaching old receptors new tricks: biasing seven-transmembrane receptors. Nat Rev Drug Discov 9:373–386
Rapoport B, Kaufman KD, Chazenbalk GD (1992) Cloning of a member of the arrestin family from a human thyroid cDNA library. Mol Cell Endocrinol 84:R39–R43
Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D, Mathiesen JM, Shah ST, Lyons JA, Caffrey M, Gellman SH, Steyaert J, Skiniotis G, Weis WI, Sunahara RK, Kobilka BK (2011) Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477:549–555
Reiner S, Ziegler N, Leon C, Lorenz K, von Hayn K, Gachet C, Lohse MJ, Hoffmann C (2009) β-Arrestin-2 interaction and internalization of the human P2Y1-receptor are dependent on C-terminal phosphorylation sites. Mol Pharmacol 76:1162–1171
Reiner S, Ambrosio M, Hoffmann C, Lohse MJ (2010) Differential signaling of the endogenous agonists at the β2-adrenergic receptor. J Biol Chem 285:36188–36198
Reiter E, Ahn S, Shukla AK, Lefkowitz RJ (2012) Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors. Annu Rev Pharmacol Toxicol 52:179–197
Ridge KD, Abdulaev NG, Sousa M, Palczewski K (2003) Phototransduction: crystal clear. Trends Biochem Sci 28:479–487
Sakuma H, Inana G, Murakami A, Higashide T, McLaren MJ (1996) Immunolocalization of X-arrestin in human cone photoreceptors. FEBS Lett 382:105–110
Sakuma H, Murakami A, Fujimaki T, Inana G (1998) Isolation and characterization of the human X-arrestin gene. Gene 224:87–95
Sanni SJ, Hansen JT, Bonde MM, Speerschneider T, Christensen GL, Munk S, Gammeltoft S, Hansen JL (2010) β-Arrestin 1 and 2 stabilize the angiotensin II type I receptor in distinct high-affinity conformations. Br J Pharmacol 161:150–161
Satoh AK, Xia H, Yan L, Liu CH, Hardie RC, Ready DF (2010) Arrestin translocation is stoichiometric to rhodopsin isomerization and accelerated by phototransduction in Drosophila photoreceptors. Neuron 67:997–1008
Saulière A, Bellot M, Paris H, Denis C, Finana F, Hansen JT, Altié MF, Seguelas MH, Pathak A, Hansen JL, Sénard JM, Galés C (2012) Deciphering biased-agonism complexity reveals a new active AT1 receptor entity. Nat Chem Biol 8:622–630
Schleicher A, Kühn H, Hofmann KP (1989) Kinetics, binding constant, and activation energy of the 48-kDa protein-rhodopsin complex by extra-metarhodopsin II. Biochemistry 28:1770–1775
Schubert C, Hirsch JA, Gurevich VV, Engelman DM, Sigler PB, Fleming KG (1999) Visual arrestin activity may be regulated by self-association. J Biol Chem 274:21186–21190
Seifert R, Dove S (2009) Functional selectivity of GPCR ligand stereoisomers: new pharmacological opportunities. Mol Pharmacol 75:13–18
Sharman JL, Mpamhanga CP (2011) IUPHAR-DB: an open-access, expert-curated resource for receptor and ion channel research. ACS Chem Neurosci 2:232–235
Shenoy SK, Lefkowitz RJ (2005) Seven-transmembrane receptor signaling through β-arrestin. Sci STKE 2005:cm10
Shenoy SK, Lefkowitz RJ (2011) β-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol Sci 32:521–533
Shenoy SK, Modi AS, Shukla AK, Xiao K, Berthouze M, Ahn S, Wilkinson KD, Miller WE, Lefkowitz RJ (2009) β-Arrestin-dependent signaling and trafficking of 7-transmembrane receptors is reciprocally regulated by the deubiquitinase USP33 and the E3 ligase Mdm2. Proc Natl Acad Sci USA 106:6650–6655
Shi H, Rojas R, Bonifacino JS, Hurley JH (2006) The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat Struct Mol Biol 13:540–548
Shinohara T, Dietzschold B, Craft CM, Wistow G, Early JJ, Donoso LA, Horwitz J, Tao R (1987) Primary and secondary structure of bovine retinal S antigen (48 kDa protein). Proc Natl Acad Sci USA 84:6875–6979
Shukla AK, Manglik A, Kruse AC, Xiao K, Reis RI, Tseng WC, Staus DP, Hilger D, Uysal S, Huang LY, Paduch M, Tripathi-Shukla P, Koide A, Koide S, Weis WI, Kossiakoff AA, Kobilka BK, Lefkowitz RJ (2013) Structure of active β-arrestin-1 bound to a G-protein-coupled receptor phosphopeptide. Nature 497:137–141
Sibley DR, Lefkowitz RJ (1985) Molecular mechanisms of receptor desensitization using the β-adrenergic receptor-coupled adenylate cyclase system as a model. Nature 317:124–129
Sibley DR, Benovic JL, Caron MG, Lefkowitz RJ (1987) Regulation of transmembrane signaling by receptor phosphorylation. Cell 48:913–922
Simpson LM, Wall ID, Blaney FE, Reynolds CA (2011) Modeling GPCR active state conformations: the β2-adrenergic receptor. Proteins 79:1441–1457
Smith WC, Milam AH, Dugger D, Arendt A, Hargrave PA, Palczewski K (1994) A splice variant of arrestin. Molecular cloning and localization in bovine retina. J Biol Chem 269:15407–15410
Soergel DG, Subach RA, Cowan CL, Violin JD, Lark MW (2013) First clinical experience with TRV027: pharmacokinetics and pharmacodynamics in healthy volunteers. J Clin Pharmacol 53:892–899
Söhlemann P, Hekman M, Puzicha M, Buchen C, Lohse MJ (1995) Binding of purified recombinant β-arrestin to G-protein-coupled receptors. Eur J Biochem 232:464–472
Sommer ME, Hofmann KP, Heck M (2011) Arrestin-rhodopsin binding stoichiometry in isolated rod outer segment membranes depends on the percentage of activated receptors. J Biol Chem 286:7359–7369
Sommer ME, Hofmann KP, Heck M (2012) Distinct loops in arrestin differentially regulate ligand binding within the GPCR opsin. Nat Commun 3:995
Song X, Raman D, Gurevich EV, Vishnivetskiy SA, Gurevich VV (2006) Visual and both non-visual arrestins in their “inactive” conformation bind JNK3 and Mdm2 and relocalize them from the nucleus to the cytoplasm. J Biol Chem 281:21491–21499
Song X, Vishnivetskiy SA, Seo J, Chen J, Gurevich EV, Gurevich VV (2011) Arrestin-1 expression level in rods: balancing functional performance and photoreceptor health. Neuroscience 174:37–49
Soskic V, Nyakatura E, Roos M, Müller-Esterl W, Godovac-Zimmermann J (1999) Correlations in palmitoylation and multiple phosphorylation of rat bradykinin B2 receptor in Chinese hamster ovary cells. J Biol Chem 274:8539–8545
Sterne-Marr R, Gurevich VV, Goldsmith P, Bodine RC, Sanders C, Donoso LA, Benovic JL (1993) Polypeptide variants of β-arrestin and arrestin3. J Biol Chem 268:15640–15648
Strissel KJ, Sokolov M, Trieu LH, Arshavsky VY (2006) Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin. J Neurosci 26:1146–1153
Strulovici B, Cerione RA, Kilpatrick BF, Caron MG, Lefkowitz RJ (1984) Direct demonstration of impaired functionality of a purified desensitized ß-adrenergic receptor in a reconstituted system. Science 225:837–840
Sutton RB, Vishnivetskiy SA, Robert J, Hanson SM, Raman D, Knox BE, Kono M, Navarro J, Gurevich VV (2005) Crystal structure of cone arrestin at 2.3A: evolution of receptor specificity. J Mol Biol 354:1069–1080
Thompson P, Findlay JBC (1984) Phosphorylation of bovine rhodopsin. Biochem J 220:773–780
Tohgo A, Choy EW, Gesty-Palmer D, Pierce KL, Laporte S, Oakley RH, Caron MG, Lefkowitz RJ, Luttrell LM (2003) The stability of the G protein-coupled receptor-β-arrestin interaction determines the mechanism and functional consequence of ERK activation. J Biol Chem 278:6258–6267
Tran TM, Friedman J, Qunaibi E, Baameur F, Moore RH, Clark RB (2004) Characterization of agonist stimulation of cAMP-dependent protein kinase and G protein-coupled receptor kinase phosphorylation of the β2-adrenergic receptor using phosphoserine-specific antibodies. Mol Pharmacol 65:196–206
Tsukamoto H, Sinha A, DeWitt M, Farrens DL (2010) Monomeric rhodopsin is the minimal functional unit required for arrestin binding. J Mol Biol 399:501–511
Unwin N, Henderson R (1984) The structure of proteins in biological membranes. Sci Am 250:78–94
Vayttaden SJ, Friedman J, Tran TM, Rich TC, Dessauer CW, Clark RB (2010) Quantitative modeling of GRK-mediated β2AR regulation. PLoS Comput Biol 6:e1000647
Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF, Babu MM (2013) Molecular signatures of G-protein-coupled receptors. Nature 494:185–194
Vilardaga JP, Frank M, Krasel C, Dees C, Nissenson RA, Lohse MJ (2001) Differential conformational requirements for activation of G proteins and regulatory proteins arrestin and G protein-coupled receptor kinase in the G protein-coupled receptor for parathyroid hormone (PTH)/PTH-related protein. J Biol Chem 276:33435–33443
Vilardaga JP, Krasel C, Chauvin S, Bambino T, Lohse MJ, Nissenson RA (2002) Internalization determinants of the parathyroid hormone receptor differentially regulate β-arrestin/receptor association. J Biol Chem 277:8121–8129
Vilardaga JP, Bünemann M, Krasel C, Castro M, Lohse MJ (2003) Measurement of the millisecond activation switch of G-protein-coupled receptors in living cells. Nat Biotechnol 21:807–812
Vishnivetskiy SA, Paz CL, Schubert C, Hirsch JA, Sigler PB, Gurevich VV (1999) How does arrestin respond to the phosphorylated state of rhodopsin? J Biol Chem 274:11451–11454
Vishnivetskiy SA, Hirsch JA, Velez MG, Gurevich YV, Gurevich VV (2002) Transition of arrestin into the active receptor-binding state requires an extended interdomain hinge. J Biol Chem 277:43961–43967
Vishnivetskiy SA, Hosey MM, Benovic JL, Gurevich VV (2004) Mapping the arrestin-receptor interface. Structural elements responsible for receptor specificity of arrestin proteins. J Biol Chem 279:1262–1268
Vishnivetskiy SA, Raman D, Wei J, Kennedy MJ, Hurley JB, Gurevich VV (2007) Regulation of arrestin binding by rhodopsin phosphorylation level. J Biol Chem 282:32075–32083
Vishnivetskiy SA, Gimenez LE, Francis DJ, Hanson SM, Hubbell WL, Klug CS, Gurevich VV (2011) Few residues within an extensive binding interface drive receptor interaction and determine the specificity of arrestin proteins. J Biol Chem 286:24288–24299
Vishnivetskiy SA, Baameur F, Findley KR, Gurevich VV (2013) Critical role of the central 139-loop in stability and binding selectivity of arrestin-1. J Biol Chem 288:11741–11750
Vrecl M, Jorgensen R, Pogacnik A, Heding A (2004) Development of a BRET2 screening assay using β-arrestin 2 mutants. J Biomol Screen 9:322–333
Wacker WB (1991) Proctor Lecture. Experimental allergic uveitis. Investigations of retinal autoimmunity and the immunopathologic responses evoked. Invest Ophthalmol Vis Sci 32:3119–3128
Wacker WB, Lipton MM (1965) Experimental allergic uveitis: homologous retina as uveitogenic antigen. Nature 206:253–254
Wacker WB, Donoso LA, Kalsow CM, Yankeelov JA Jr, Organisciak DT (1977) Experimental allergic uveitis. Isolation, characterization, and localization of a soluble uveitopathogenic antigen from bovine retina. J Immunol 119:1949–1958
West GM, Chien EY, Katritch V, Gatchalian J, Chalmers MJ, Stevens RC, Griffin PR (2011) Ligand-dependent perturbation of the conformational ensemble for the GPCR β2-adrenergic receptor revealed by HDX. Structure 19:1424–1432
Wheeler D, Sneddon WB, Wang B, Friedman PA, Romero G (2007) NHERF-1 and the cytoskeleton regulate the traffic and membrane dynamics of G protein-coupled receptors. J Biol Chem 282:25076–25087
Whitlock GG, Lamb TD (1999) Variability in the time course of single photon responses from toad rods: termination of rhodopsin's activity. Neuron 23:337–351
Whorton MR, Bokoch MP, Rasmussen SG, Huang B, Zare RN, Kobilka B, Sunahara RK (2007) A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc Natl Acad Sci USA 104:7682–7687
Whorton MR, Jastrzebska B, Park PS, Fotiadis D, Engel A, Palczewski K, Sunahara RK (2008) Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J Biol Chem 283:4387–4394
Wilden U (1995) Duration and amplitude of the light-induced cGMP hydrolysis in vertebrate photoreceptors are regulated by multiple phosphorylation of rhodopsin and by arrestin binding. Biochemistry 34:1446–1454
Wilden U, Kühn H (1982) Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites. Biochemistry 21:3014–3022
Wilden U, Hall SW, Kühn H (1986) Phosphodiesterase activation by photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the intrinsic 48-kDa protein of rod outer segments. Proc Natl Acad Sci USA 83:1174–1178
Willets JM, Mistry R, Nahorski SR, Challiss RA (2003) Specificity of G protein-coupled receptor kinase 6-mediated phosphorylation and regulation of single-cell M3 muscarinic acetylcholine receptor signaling. Mol Pharmacol 64:1059–1066
Williams JT, Ingram SL, Henderson G, Chavkin C, von Zastrow M, Schulz S, Koch T, Evans CJ, Christie MJ (2013) Regulation of μ-opioid receptors: desensitization, phosphorylation, internalization, and tolerance. Pharmacol Rev 65:223–254
Xiao K, Shenoy SK, Nobles K, Lefkowitz RJ (2004) Activation-dependent conformational changes in β-arrestin 2. J Biol Chem 279:55744–55753
Yamaki K, Takahashi Y, Sakuragi S, Matsubara K (1987) Molecular cloning of the S-antigen cDNA from bovine retina. Biochem Biophys Res Commun 142:904–910
Yamaki K, Tsuda M, Kikuchi T, Chen K-H, Huang K-P, Shinohara T (1990) Structural organization of the human S-antigen gene: cDNA, amino acid, intron, exon, promoter, in vitro transcription, retina, and pineal gland. J Biol Chem 265:20757–20762
Yamazaki A, Halliday KR, George JS, Nagao S, Kuo CH, Ailsworth KS, Bitensky MW (1985) Homology between light-activated photoreceptor phosphodiesterase and hormone-activated adenylate cyclase systems. Adv Cyclic Nucleotide Protein Phosphorylation Res 19:113–124
Yu SS, Lefkowitz RJ, Hausdorff WP (1993) β-Adrenergic receptor sequestration. A potential mechanism of receptor resensitization. J Biol Chem 268:337–341
Zhan X, Gimenez LE, Gurevich VV, Spiller BW (2011) Crystal structure of arrestin-3 reveals the basis of the difference in receptor binding between two non-visual subtypes. J Mol Biol 406:467–478
Zhang J, Ferguson SS, Barak LS, Ménard L, Caron MG (1996) Dynamin and β-arrestin reveal distinct mechanisms for G protein-coupled receptor internalization. J Biol Chem 271:18302–18305
Zuckerman R, Cheasty JE (1986) A 48 kDa protein arrests cGMP phosphodiesterase activation in retinal rod disk membranes. FEBS Lett 201:35–41
Zuckerman R, Buzdygon B, Philp N, Liebman P, Sitaramayya A (1985) Arrestin: an ATP/ADP exchange protein that regulates cGMP phosphodiesterase activity in retinal rod disk membranes (RDM). Biophys J 47:37a
Zürn A, Zabel U, Vilardaga JP, Schindelin H, Lohse MJ, Hoffmann C (2009) Fluorescence resonance energy transfer analysis of α2A-adrenergic receptor activation reveals distinct agonist-specific conformational changes. Mol Pharmacol 75:534–541
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Lohse, M.J., Hoffmann, C. (2014). Arrestin Interactions with G Protein-Coupled Receptors. In: Gurevich, V. (eds) Arrestins - Pharmacology and Therapeutic Potential. Handbook of Experimental Pharmacology, vol 219. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-41199-1_2
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