Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization

Molecular Pharmacology

Volumn 63, Issue 1, 2003, Pages 9-18

  Kohout, Trudy A ^a   Lefkowitz, Robert J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM SENSING RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; FATTY ACID; G PROTEIN COUPLED RECEPTOR KINASE; ISOPRENE; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN KINASE C; PROTEIN SUBUNIT; RETINA S ANTIGEN;

BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL ACTIVITY; CELL FUNCTION; CELL MEMBRANE; COVALENT BOND; DNA MODIFICATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SPECIFICITY; KNOCKOUT MOUSE; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; SHORT SURVEY; SIGNAL TRANSDUCTION;

ANIMALS; ARRESTINS; BETA-ADRENERGIC RECEPTOR KINASE; CALCIUM; CELL MEMBRANE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HUMANS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SUBSTRATE SPECIFICITY;

EID: 0037223063     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: 10.1124/mol.63.1.9     Document Type: Short Survey

References (88)

1. Alloway PG, Howard L, and Dolph PJ (2000) The formation of stable rhodopsinarrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 28:129-138.
2. Attramadal H, Arriza JL, Aoki C, Dawson TM, Codina J, Kwatra MM, Snyder SH, Caron MG, and Lefkowitz RJ (1992) β-Arrestin2, a novel member of the arrestin/β-arrestin gene family. J Biol Chem 267:17882-17890.
3. Benovic JL, DeBlasi A, Stone WC, Caron MG, and Lefkowitz RJ (1989) β-Adrenergic receptor kinase: Primary structure delineates a multigene family. Science (Wash DC) 246:235-240.
4. Benovic JL and Gomez J (1993) Molecular cloning and expression of GRK6. A new member of the G protein-coupled receptor kinase family. J Biol Chem 268:19521-19527.
5. Benovic JL, Kuhn H, Weyand I, Codina J, Caron MG, and Lefkowitz RJ (1987) 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.
6. Benovic JL, Onorato JJ, Arriza JL, Stone WC, Lohse M, Jenkins NA, Gilbert DJ, Copeland NG, Caron MG, and 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.
7. Benovic JL, Pike LJ, Cerione RA, Staniszewski C, Yoshimasa T, Codina J, Caron MG, and Lefkowitz RJ (1985) Phosphorylation of the mammalian β-adrenergic receptor by cyclic AMP-dependent protein kinase. Regulation of the rate of receptor phosphorylation and dephosphorylation by agonist occupancy and effects on coupling of the receptor to the stimulatory guanine nucleotide regulatory protein. J Biol Chem 260:7094-7101.
8. Berman DM and Gilman AG (1998) Mammalian RGS proteins: Barbarians at the gate. J Biol Chem 273:1269-1272.
9. Bockaert J and Pin JP (1999) Molecular tinkering of G protein-coupled receptors: An evolutionary success. EMBO (Eur Mol Biol Organ) J 18:1723-1729.
10. Bohn LM, Gainetdinov RR, Lin FT, Lefkowitz RJ, and Caron MG (2000) μ-Opioid receptor desensitization by β-arrestin-2 determines morphine tolerance but not dependence. Nature (Lond) 408:720-723.
11. Bohn LM, Lefkowitz RJ, Gainetdinov RR, Peppel K, Caron MG, and Lin FT (1999) Enhanced morphine analgesia in mice lacking β-arrestin 2. Science (Wash DC) 286:2495-2498.
12. q/11 by an RGS domain in the G protein-coupled receptor kinase, GRK2. J Biol Chem 274:34483-34492.
13. Chen CK, Burns ME, Spencer M, Niemi GA, Chen J, Hurley JB, Baylor DA, and Simon MI (1999) Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc Natl Acad Sci USA 96:3718-3722.
14. 2+-dependent interaction of recoverin with rhodopsin kinase. J Biol Chem 270:18060-18066.
15. Chuang TT, LeVine H 3rd, and De Blasi A (1995) Phosphorylation and activation of β-adrenergic receptor kinase by protein kinase C. J Biol Chem 270:18660-18665.
16. 2+/calmodulin. J Biol Chem 271:28691-28696.
17. Claing A, Laporte SA, Caron MG, and Lefkowitz RJ (2002) Endocytosis of G proteincoupled receptors: Roles of G protein-coupled receptor kinases and β-arrestin proteins. Prog Neurobiol 66:61-79.
18. Cong M, Perry SJ, Lin FT, Fraser ID, Hu LA, Chen W, Pitcher JA, Scott JD, and Lefkowitz RJ (2001) Regulation of membrane targeting of the G protein-coupled receptor kinase 2 by protein kinase A and its anchoring protein AKAP79. J Biol Chem 276:15192-15199.
19. Conner DA, Mathier MA, Mortensen RM, Christe M, Vatner SF, Seidman CE, and Seidman JG (1997) β-Arrestin1 knockout mice appear normal but demonstrate altered cardiac responses to β-adrenergic stimulation. Circ Res 81:1021-1026.
20. De Castro E, Nef S, Fiumelli H, Lenz SE, Kawamura S, and Nef P (1995) Regulation of rhodopsin phosphorylation by a family of neuronal calcium sensors. Biochem Biophys Res Commun 216:133-140.
21. Dhami GK, Anborgh PH, Dale LB, Sterne-Marr R, and Ferguson SS (2002) Phosphorylation-independent regulation of metabotropic glutamate receptor signaling by G protein-coupled receptor kinase 2. J Biol Chem 277:25266-25272.
22. Diviani D, Lattion AL, Larbi N, Kunapuli P, Pronin A, Benovic JL, and Cotecchia S (1996) Effect of different G protein-coupled receptor kinases on phosphorylation and desensitization of the α1B-adrenergic receptor. J Biol Chem 271:5049-5058.
23. Eckhart AD, Duncan SJ, Penn RB, Benovic JL, Lefkowitz RJ, and Koch WJ (2000) Hybrid transgenic mice reveal in vivo specificity of G protein-coupled receptor kinases in the heart. Circ Res 86:43-50.
24. Eckhart AD, Ozaki T, Tevaearai H, Rockman HA, and Koch WJ (2002) Vascular-targeted overexpression of G protein-coupled receptor kinase-2 in transgenic mice attenuates β-adrenergic receptor signaling and increases resting blood pressure. Mol Pharmacol 61:749-758.
25. Elorza A, Sarnago S, and Mayor F Jr (2000) Agonist-dependent modulation of G protein-coupled receptor kinase 2 by mitogen-activated protein kinases. Mol Pharmacol 57:778-783.
26. Fan G, Shumay E, Malbon CC, and Wang H (2001) c-Src tyrosine kinase binds the β2-adrenergic receptor via phospho-Tyr-350, phosphorylates G-protein-linked receptor kinase 2 and mediates agonist-induced receptor desensitization. J Biol Chem 276:13240-13247.
27. Felder RA, Sanada H, Xu J, Yu PY, Wang Z, Watanabe H, Asico LD, Wang W, Zheng S, Yamaguchi I, et al. (2002) G protein-coupled receptor kinase 4 gene variants in human essential hypertension. Proc Natl Acad Sci USA 99:3872-3877.
28. Ferguson SS (2001) Evolving concepts in G protein-coupled receptor endocytosis: The role in receptor desensitization and signaling. Pharmacol Rev 53:1-24.
29. Flannery PJ and Spurney RF (2001) Domains of the parathyroid hormone (PTH) receptor required for regulation by G protein-coupled receptor kinases (GRKs). Biochem Pharmacol 62:1047-1058.
30. Fong AM, Premont RT, Richardson RM, Yu YR, Lefkowitz RJ, and Patel DD (2002) Defective lymphocyte chemotaxis in β-arrestin2- and GRK6-deficient mice. Proc Natl Acad Sci USA 99:7478-7483.
31. Fraser ID, Cong M, Kim J, Rollins EN, Daaka Y, Lefkowitz RJ, and Scott JD (2000) Assembly of an A kinase-anchoring protein-β2-adrenergic receptor complex facilitates receptor phosphorylation and signaling. Curr Biol 10:409-412.
32. Freedman NJ, Ament AS, Oppermann M, Stoffel RH, Exum ST, and Lefkowitz RJ (1997) Phosphorylation and desensitization of human endothelin A and B receptors. Evidence for G protein-coupled receptor kinase specificity. J Biol Chem 272:17734-17743.
33. Freedman NJ and Lefkowitz RJ (1996) Desensitization of G protein-coupled receptors. Recent Prog Horm Res 51:319-351.
34. Gainetdinov RR, Bohn LM, Walker JK, Laporte SA, Macrae AD, Caron MG, Lefkowitz RJ, and Premont RT (1999) Muscarinic supersensitivity and impaired receptor desensitization in G protein-coupled receptor kinase 5-deficient mice. Neuron 24:1029-1036.
35. Hisatomi O, Matsuda S, Satoh T, Kotaka S, Imanishi Y, and Tokunaga F (1998) A novel subtype of G-protein-coupled receptor kinase, GRK7, in teleost cone photo-receptors. FEBS Lett 424:159-164.
36. Houslay MD (2001) PDE4 cAMP-specific phosphodiesterases. Prog Nucleic Acid Res Mol Biol 69:249-315.
37. Iaccarino G, Rockman HA, Shotwell KF, Tomhave ED, and Koch WJ (1998) Myocardial overexpression of GRK3 in transgenic mice: Evidence for in vivo selectivity of GRKs. Am J Physiol 275:H1298-H1306.
38. Inglese J, Koch WJ, Caron MG, and Lefkowitz RJ (1992) Isoprenylation in regulation of signal transduction by G-protein-coupled receptor kinases. Nature (Lond) 359:147-150.
39. Jaber M, Koch WJ, Rockman H, Smith B, Bond RA, Sulik KK, Ross J Jr, Lefkowitz RJ, Caron MG, and Giros B (1996) Essential role of β-adrenergic receptor kinase 1 in cardiac development and function. Proc Natl Acad Sci USA 93:12974-12979.
40. Kiselev A, Socolich M, Vinos J, Hardy RW, Zuker CS, and Ranganathan R (2000) A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron 28:139-152.
41. Klenchin VA, Calvert PD, and Bownds MD (1995) Inhibition ofrhodopsin kinase by recoverin. Further evidence for a negative feedback system in phototransduction. J Biol Chem 270:16147-16152.
42. Koch WJ, Inglese J, Stone WC, and Lefkowitz RJ (1993) The binding site for the βγ subunits of heterotrimeric G proteins on the β-adrenergic receptor kinase. J Biol Chem 268:8256-8260.
43. Koch WJ, Rockman HA, Samama P, Hamilton RA, Bond RA, Milano CA, and Lefkowitz RJ (1995) Cardiac function in mice overexpressing β-adrenergic receptor kinase or a βARK inhibitor. Science (Wash DC) 268:1350-1353.
44. Kohout TA, Lin FS, Perry SJ, Conner DA, and Lefkowitz RJ (2001) β-Arrestin 1 and 2 differentially regulate heptahelical receptor signaling and trafficking. Proc Natl Acad Sci USA 98:1601-1606.
45. Krupnick JG and Benovic JL (1998) The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu Rev Pharmacol Toxicol 38:289-319.
46. Kunapuli P, Gurevich VV, and Benovic JL (1994) Phospholipid-stimulated autophosphorylation activates the G protein-coupled receptor kinase GRK5. J Biol Chem 269:10209-10212.
47. 2+-binding proteins on G protein-coupled receptor kinases. Biochemistry 37:13650-13659.
48. Lin FT, Krueger KM, Kendall HE, Daaka Y, Fredericks ZL, Pitcher JA, and Lefkowitz RJ (1997) Clathrin-mediated endocytosis of the β-adrenergic receptor is regulated by phosphorylation/dephosphorylation of β-arrestin1. J Biol Chem 272:31051-31057.
49. Lin FT, Miller WE, Luttrell LM, and Lefkowitz RJ (1999) Feedback regulation of β-arrestin1 function by extracellular signal-regulated kinases. J Biol Chem 274:15971-15974.
50. Lohse MJ, Andexinger S, Pitcher J, Trukawinski S, Codina J, Faure JP, Caron MG, and 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.
51. Lombardi MS, Kavelaars A, Cobelens PM, Schmidt RE, Schedlowski M, and Heijnen CJ (2001) Adjuvant arthritis induces down-regulation of G protein-coupled receptor kinases in the immune system. J Immunol 166:1635-1640.
52. Lyubarsky AL, Chen C, Simon MI, and Pugh EN Jr (2000) Mice lacking G-protein receptor kinase 1 have profoundly slowed recovery of cone-driven retinal responses. J Neurosci 20:2209-2217.
53. Mundell SJ, Loudon RP, and Benovic JL (1999) Characterization of G protein-coupled receptor regulation in antisense mRNA-expressing cells with reduced arrestin levels. Biochemistry 38:8723-8732.
54. Neer EJ (1995) Heterotrimeric G proteins: Organizers of transmembrane signals. Cell 80:249-257.
55. Orsini MJ, Parent JL, Mundell SJ, and Benovic JL (1999) Trafficking of the HIV coreceptor CXCR4. Role of arrestins and identification of residues in the C-terminal tail that mediate receptor internalization. J Biol Chem 274:31076-31086.
56. Paing MM, Stutts AB, Kohout TA, Lefkowitz RJ, and Trejo J (2002) β-Arrestins regulate protease-activated receptor-1 desensitization but not internalization or down-regulation. J Biol Chem 277:1292-1300.
57. Penela P, Elorza A, Sarnago S, and Mayor F Jr (2001) β-arrestin- and c-Src-dependent degradation of G-protein-coupled receptor kinase 2. EMBO (Eur Mol Biol Organ) J 20:5129-5138.
58. Penela P, Ruiz-Gomez A, Castano JG, and Mayor F Jr (1998) Degradation of the G protein-coupled receptor kinase 2 by the proteasome pathway. J Biol Chem 273:35238-35244.
59. Peppel K, Boekhoff I, McDonald P, Breer H, Caron MG, and Lefkowitz RJ (1997) G protein-coupled receptor kinase 3 (GRK3) gene disruption leads to loss of odorant receptor desensitization. J Biol Chem 272:25425-25428.
60. Perry SJ, Baillie GS, Kohout TA, McPhee I, Magiera MM, Ang KL, Miller WE, McLean AJ, Conti M, Houslay MD, et al. (2002) Targeting of cyclic AMP degradation to β2-adregenic receptors by β-arrestins. Science (Wash DC) 298:834-836.
61. Perry SJ and Lefkowitz RJ (2002) Arresting developments in heptahelical receptor signaling and regulation. Trends Cell Biol 12:130-138.
62. Pitcher J, Lohse MJ, Codina J, Caron MG, and Lefkowitz RJ (1992a) Desensitization of the isolated β2-adrenergic receptor by β-adrenergic receptor kinase, cAMP-dependent protein kinase and protein kinase C occurs via distinct molecular mechanisms. Biochemistry 31:3193-3197.
63. Pitcher JA, Fredericks ZL, Stone WC, Premont RT, Stoffel RH, Koch WJ and Lefkowitz RJ (1996) Phosphatidylinositol 4,5-bisphosphate (PIP2)-enhanced G protein-coupled receptor kinase (GRK) activity. Location, structure and regulation of the PIP2 binding site distinguishes the GRK subfamilies. J Biol Chem 271:24907-24913.
64. Pitcher JA, Freedman NJ, and Lefkowitz RJ (1998) G protein-coupled receptor kinases. Annu Rev Biochem 67:653-692.
65. Pitcher JA, Inglese J, Higgins JB, Arriza JL, Casey PJ, Kim C, Benovic JL, Kwatra MM, Caron MG, and Lefkowitz RJ (1992b) Role of βγ subunits of G proteins in targeting the β-adrenergic receptor kinase to membrane-bound receptors. Science (Wash DC) 257:1264-1267.
66. Pitcher JA, Tesmer JJ, Freeman JL, Capel WD, Stone WC, and Lefkowitz RJ (1999) Feedback inhibition of G protein-coupled receptor kinase 2 (GRK2) activity by extracellular signal-regulated kinases. J Biol Chem 274:34531-34534.
67. Pitcher JA, Touhara K, Payne ES, and Lefkowitz RJ (1995) Pleckstrin homology domain-mediated membrane association and activation of the β-adrenergic receptor kinase requires coordinate interaction with G βγ subunits and lipid. J Biol Chem 270:11707-11710.
68. Premont RT, Koch WJ, Inglese J, and Lefkowitz RJ (1994) Identification, purification and characterization of GRK5, a member of the family of G protein-coupled receptor kinases. J Biol Chem 269:6832-6841.
69. Premont RT, Macrae AD, Stoffel RH, Chung N, Pitcher JA, Ambrose C, Inglese J, MacDonald ME, and Lefkowitz RJ (1996) Characterization of the G protein-coupled receptor kinase GRK4. Identification of four splice variants. J Biol Chem 271:6403-6410.
70. Pronin AN and Benovic JL (1997) Regulation of the G protein-coupled receptor kinase GRK5 by protein kinase C. J Biol Chem 272:3806-3812.
71. Pronin AN, Carman CV, and Benovic JL (1998) Structure-function analysis of G protein-coupled receptor kinase-5. Role of the carboxyl terminus in kinase regulation. J Biol Chem 273:31510-31518.
72. Pronin AN, Satpaev DK, Slepak VZ, and Benovic JL (1997) Regulation of G protein-coupled receptor kinases by calmodulin and localization of the calmodulin binding domain. J Biol Chem 272:18273-18280.
73. Rockman HA, Choi DJ, Akhter SA, Jaber M, Giros B, Lefkowitz RJ, Caron MG, and Koch WJ (1998) Control of myocardial contractile function by the level of β-adrenergic receptor kinase 1 in gene-targeted mice. J Biol Chem 273:18180-18184.
74. Rockman HA, Choi DJ, Rahman NU, Akhter SA, Lefkowitz RJ, and Koch WJ (1996) Receptor-specific in vivo desensitization by the G protein-coupled receptor kinase-5 in transgenic mice. Proc Natl Acad Sci USA 93:9954-9959.
75. Roth NS, Campbell PT, Caron MG, Lefkowitz RJ, and Lohse MJ (1991) Comparative rates of desensitization of β-adrenergic receptors by the β-adrenergic receptor kinase and the cyclic AMP-dependent protein kinase. Proc Natl Acad Sci USA 88:6201-6204.
76. Sallese M, Iacovelli L, Cumashi A, Capobianco L, Cuomo L, and De Blasi A (2000a) Regulation of G protein-coupled receptor kinase subtypes by calcium sensor proteins. Biochim Biophys Acta 1498:112-121.
77. Sallese M, Mariggio S, D'Urbano E, Iacovelli L, and De Blasi A (2000b) Selective regulation of Gq signaling by G protein-coupled receptor kinase 2: Direct interaction of kinase N terminus with activated Gαq. Mol Pharmacol 57:826-831.
78. Sarnago S, Elorza A, and Mayor F (1999) Agonist-dependent phosphorylation of the G protein-coupled receptor kinase 2 (GRK2) by src tyrosine kinase. J Biol Chem 274:34411-34416.
79. Shenoy SK, McDonald PH, Kohout TA, and Lefkowitz RJ (2001) Regulation of receptor fate by ubiquitination of activated β2-adrenergic receptor and β-arrestin. Science (Wash DC) 294:1307-1313.
80. Shetzline MA, Premont RT, Walker JK, Vigna SR, and Caron MG (1998) A role for receptor kinases in the regulation of class II G protein-coupled receptors. Phosphorylation and desensitization of the secretin receptor. J Biol Chem 273:6756-6762.
81. Shetzline MA, Walker JK, Valenzano KJ, and Premont RT (2002) Vasoactive intestinal polypeptide type-1 receptor regulation. Desensitization, phosphorylation, and sequestration. J Biol Chem 277:25519-25526.
82. Stoffel RH, Randall RR, Premont RT, Lefkowitz RJ, and Inglese J (1994) Palmitoylation of G protein-coupled receptor kinase, GRK6. Lipid modification diversity in the GRK family. J Biol Chem 269:27791-27794.
83. Ungerer M, Parruti G, Bohm M, Puzicha M, DeBlasi A, Erdmann E, and Lohse MJ (1994) Expression of β-arrestins and β-adrenergic receptor kinases in the failing human heart. Circ Res 74:206-213.
84. Walker JK, Peppel K, Lefkowitz RJ, Caron MG, and Fisher JT (1999) Altered airway and cardiac responses in mice lacking G protein-coupled receptor kinase 3. Am J Physiol 276:R1214-R1221.
85. Weiss ER, Raman D, Shirakawa S, Ducceschi MH, Bertram PT, Wong F, Kraft TW, and Osawa S (1998) The cloning of GRK7, a candidate cone opsin kinase, from cone- and rod-dominant mammalian retinas. Mol Vis 4:27.
86. Wilden U, Hall SW, and Kuhn 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.
87. Winstel R, Freund S, Krasel C, Hoppe E, and Lohse MJ (1996) Protein kinase cross-talk: Membrane targeting of the β-adrenergic receptor kinase by protein kinase C. Proc Natl Acad Sci USA 93:2105-2109.
88. Xu J, Dodd RL, Makino CL, Simon MI, Baylor DA, and Chen J (1997) Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature (Lond) 389:505-509.