The sustainability of interactions between the orexin-1 receptor and β-arrestin-2 is defined by a single C-terminal cluster of hydroxy amino acids and modulates the kinetics of ERK MAPK regulation

Biochemical Journal

Volumn 387, Issue 3, 2005, Pages 573-584

  Milasta, Sandra ^a   Evans, Nicholas A ^b   Ormiston, Laura ^a   Wilson, Shelagh ^b   Lefkowitz, Robert J ^c   Milligan, Graeme ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

arrestin; Extracellular signal regulated kinase (ERK); G protein coupled receptor; Mitogen activated protein kinase (MAPK); Orexin; Receptor internalization

Indexed keywords

AMINO ACIDS; FLUORESCENCE; MUTAGENESIS; PROTEINS;

AGONIST-DEPENDENT MANNER; ENDOSOMES; GREEN FLUORESCENCE; PHOSPHORYLATION;

CELLS;

AMINO ACID; BETA ARRESTIN; BETA ARRESTIN 2; CALCIUM; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; OREXIN 1 RECEPTOR; SERINE; THREONINE; UNCLASSIFIED DRUG;

AGONIST; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; ENDOSOME; ENZYME KINETICS; ENZYME PHOSPHORYLATION; FIBROBLAST; HUMAN; HUMAN CELL; INTERNALIZATION; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ARRESTINS; CELL LINE; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; HUMANS; KINETICS; MICE; MOLECULAR SEQUENCE DATA; POINT MUTATION; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE;

EID: 18844411824     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041745     Document Type: Article

References (46)

1. Sakurai, T., Amemiya, A., Ishii, M., Matsuzaki, I., Chemelli, R. M., Tanaka, H., Williams, S. C., Richardson, J. A., Kozlowski, G, P., Wilson, S. et al. (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573-585
2. Samson, W. K. and Resch, Z. T. (2000) The hypocretin/orexin story. Trends Endocrinol. Metab. 11, 257-262
3. Smart, D., Jerman, J. C., Brough, S. J., Rushton, S. L., Murdock, P. R., Jewitt, F., Elshourbagy, N. A., Ellis, C. E., Middlemiss, D. N. and Brown, F. (1999) Characterization of recombinant human orexin receptor pharmacology in a Chinese hamster ovary cell-line using FLIPR. Br. J. Pharmacol. 128, 1-3
4. 2+ influx pathway necessary for coupling to phospholipase C. J. Biol. Chem, 275, 30806-30812
5. Haynes, A. C., Jackson, B., Chapman, H., Tadayyon, M., Johns, A., Porter, R. A. and Arch, J. R. (2000) A selective orexin-1 receptor antagonist reduces food consumption in male and female rats. Regul. Pept. 96, 45-51
6. Smart, D., Sabido-David, C., Brough, S. J., Jewitt, F., Johns, A., Porter, R. A. and Jerman, J. C. (2001) SB-334867-A: the first selective orexin-1 receptor antagonist. Br. J. Pharmacol. 132, 1179-1182
7. Chiesi, M., Huppertz, C. and Hofbauer, K. G. (2001) Pharmacotherapy of obesity: targets and perspectives. Trends Pharmacol. Sci. 22, 247-254
8. Smart, D., Haynes, A. C., Williams, G. and Arch, J. R. (2002) Orexins and the treatment of obesity. Eur. J. Pharmacol. 440, 199-212
9. Ferguson, S. S. (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol. Rev. 53, 1-24
10. Goodman, Jr, O. B., Krupnick, J. G., Santini, F. Gurevich, V. V., Penn, R. B., Gagnon, A. W., Keen, J. H. and Benovic, J. L. (1996) β-Arrestin acts as a clathrin adaptor in endocytosis of the β2-adrenergic receptor. Nature (London) 383, 447-450
11. Laporte, S. A., Oakley, R. H., Holt, J. A., Barak, L. S. and Caron, M. G. (2000) The interaction of β-arrestin with the AP-2 adaptor is required for the clustering of β 2-adrenergic receptor into clathrin-coated pits. J. Biol. Chem. 275, 23120-23126
12. Goodman, Jr, O. B., Krupnick, J. G., Gurevich, V. V., Benovic, J. L. and Keen, J. H. (1997) Arrestin/clathrin interaction: localization of the arrestin binding locus to the clathrin terminal domain. J. Biol. Chem. 272, 15017-15022
13. Oakley, R. H., Laporte, S. A., Holt, J. A, Barak, L. S. and Caron, M. G. (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
14. Oakley, R. H., Laporte, S. A., Holt, J. A, Barak, L. S. and Caron, M. G. (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
15. Evans, N. A., Groarke, D. A., Warrack, J., Greenwood, C. J., Dodgson, K., Milligan, G. and Wilson, S. (2001) Visualizing differences in ligand-induced β-arrestin-GFP interactions and trafficking between three recently characterized G protein-coupled receptors. J. Neurochem. 77, 476-485
16. DeGraff, J. L., Gurevich, V. V. and Benovic, J. L. (2002) The third intracellular loop of α2-adrenergic receptors determines subtype specificity of arrestin interaction. J. Biol. Chem. 277, 43247-43252
17. 2 muscarinic acetylcholine receptor is precluded by an inhibitory element in the third intracellular loop of the receptor. J. Biol. Chem. 275, 9284-9289
18. Bennett, T. A., Maestas, D. C. and Prossnitz, E. R. (2000) Arrestin binding to the G protein-coupled n-formyl peptide receptor is regulated by the conserved 'DRY' sequence. J. Biol. Chem. 275, 24590-24594
19. Groarke, D. A., Drmota, T., Bahia, D. S., Evans, N. A., Wilson, S. and Milligan, G. (2001) Analysis of the C-terminal tail of the rat thyrotropin-releasing hormone receptor-1 In interactions and cointernalization with α-arrestin 1-green fluorescent protein. Mol. Pharmacol. 59, 375-385
20. Hanyaloglu, A. C., Vrecl, M., Kroeger, K. M., Miles, L. E., Qian, H., Thomas, W. G. and Eidne, K. A. (2001) Casein kinase II sites in the intracellular C-terminal domain of the thyrotropin-releasing hormone receptor and chimeric gonadotropin-releasing hormone receptors contribute to β-arrestin-dependent internalization. J. Biol. Chem. 276, 18066-18074
21. Shenoy, S. K. and Lefkowitz, R. J. (2003) Multifaceted roles of β-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signalling. Biochem. J. 375, 503-515
22. Hall, R. A. and Lefkowitz, R. J. (2002) Regulation of G protein-coupled receptor signaling by scaflold proteins, Circ. Res, 91, 672-680
23. Luttrell, L. M., Ferguson, S. S., Daaka, Y. Miller, W. E., Maudsiey, S., Delia Rocca, G. J., Lin, F., Kawakatsu, H., Owada, K., Luttrell, D. K. et al. (1999) β-Arrestin-dependent formation of β2 adrenergic receptor-src protein kinase complexes. Science 283, 655-661
24. DeFea, K. A., Zalevsky, J., Thoma, M. S., Dery, O., Mullins, R. D. and Bunnett, N. W. (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
25. Tohgo, A., Choy, E. W., Gesty-Palmer, D., Pierce, K. L., Laporte, S., Oakley, R. H., Caron, M. G., Lefkowitz, R. J. and Luttrell, L. M. (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
26. Fong, T. M. (1999) Overview of mutagenesis techniques. In Structure-Function Analysis of G Protein-Coupled Receptors (Wess, J., ed.), pp. 12-20, Wiley-Liss, New York
27. Kohout, T. A., Lin, F. S., Perry, S. J., Conner, D. A. and Lefkowitz, R. J. (2001) β-Arrestin 1 and 2 differentially regulate heptahelical receptor signaling and trafficking. Proc. Natl. Acad. Sci. U.S.A. 98, 1601-1606
28. Vines, C. M., Revankar, C. M., Maestas, D. C., LaRusch, L. L., Cimino, D. F., Kohout, T. A., Lefkowitz, R. J. and Prossnitz, E. R. (2003) N-formyl peptide receptors internalize but do not recycle in the absence of arrestins. J. Biol. Chem. 278, 41581-41584
29. Offermanns, S., Zhao, L. P., Gohla, A., Sarosi, I., Simon, M. I. and Wilkie, T. M. (1998) Embryonic cardiomyocyte hypoplasia and craniofacial defects in Gαq/Gα11-mutant mice. EMBO J. 17, 4304-4312
30. Mao, J., Yuan, H., Xie, W., Simon, M. I. and Wu, D. (1998) Specific Involvement of G proteins in regulation of serum response factor-mediated gene transcription by different receptors. J. Biol. Chem. 273, 27118-27123
31. Cao, T. T., Deacon, H. W., Reczek, D., Bretscher, A. and von Zastrow, M. (1999) A kinase-regulated PDZ-domain interaction controls endocytic sorting of the β2-adrenergic receptor. Nature (London) 401, 286-290
32. Adie, E. J., Kalinka, S., Smith, L., Francis, M. J., Marenghi, A., Cooper, M. E., Briggs, M. Michael, N. P., Milligan, G. and Game, S. (2002) A pH-sensitive fluor, Cypher 5, used to monitor agonist-induced G protein-coupled receptor internalization in live cells. Biotechniques 33, 1152-1157
33. Charest, P. G. and Bouvier, M. (2003) Palmitoylation of the V2 vasopressin receptor carboxyl tail enhances β-arrestin recruitment leading to efficient receptor endocytosis and ERK1/2 activation. J. Biol. Chem. 278, 41541-41551
34. Liu, S., Carrillo, J. J., Pediani, J. D. and Milligan, G. (2002) Effective information transfer from the α1b-adrenoceptor to Gα 11 requires both β/γ interactions and an aromatic group four amino acids from the C terminus of the G protein. J. Biol. Chem. 277, 25707-25714
35. Milligan, G. (2003) High-content assays for ligand regulation of G-protein-coupled receptors. Drug Discov. Today 8, 579-585
36. 2A receptor desensitization and resensltization-reveal an arrestin-, GRK2-, and GRK5-independent mode of regulation in human embryonic kidney 293 cells. Mol. Pharmacol. 60, 1020-1030
37. Ahn, S., Wei, H., Garrison, T. R. and Lefkowitz, R. J. (2004) Reciprocal regulation of angiotensin receptor-activated extracellular signal-regulated kinases by β-arrestins 1 and 2. J. Biol. Chem. 279, 7807-7811
38. q/1- coordinately activate RhoA and stress fiber formation following receptor stimulation. J. Biol. Chem., DOI 10.1074/jbc.M412924200
39. Seta, K., Nanamori, M., Modrall, J. G., Neubig, R. R. and Sadoshima, J. (2002) AT1 receptor mutant lacking heterotrimeric G protein coupling activates the Src-Ras-ERK pathway without nuclear translocation of ERKs. J. Biol. Chem. 277, 9268-9277
40. Tohgo, A., Pierce, K. L., Choy, E. W., Lefkowitz, R. J, and Luttrell, L. M. (2002) β-Arrestin scaffolding of the ERK cascade enhances cytosolic ERK activity but inhibits ERK-mediated transcription following angiotensin AT1a receptor stimulation. J. Biol. Chem. 277, 9429-9436
41. Ahn, S., Nelson, C. D., Garrison, T R., Miller, W. E. and Lefkowitz, R. J. (2003) Desensitization, internalization, and signaling functions of β-arrestins demonstrated by RNA interference. Proc. Natl. Acad. Sci. U.S.A. 100, 1740-1744
42. Wei, H., Ahn, S., Shenoy, S. K., Karnik, S. S., Hunyady, L., Luttrell, L. M. and Lefkowitz, R. J. (2003) Independent β-arrestin 2 and G protein-mediated pathways for angiotensin II activation of extracellular signal-regulated kinases 1 and 2. Proc. Natl. Acad. Sci. U.S.A. 100, 10782-10787
43. Ahn, S., Maudsley, S., Luttrell, L. M., Lefkowitz, R. J. and Daaka, Y. (1999) Src-mediated tyrosine phosphorylation of dynamin is required for β2-adrenergic receptor internalization and mitogen-aclivated protein kinase signaling. J. Biol. Chem. 274, 1185-1188
44. McDonald, P. H., Chow, C. W., Miller, W. E., Laporte, S. A., Field, M. E., Lin, F. I, Davis, R. J. and Lefkowitz, R. J, (2000) β-Arrestin 2: a receptor-regulated MAPK scaffold for the activation of JNK3, Science 290, 1574-1577
45. Miller, W. E. and Lefkowitz, R. J. (2001) Expanding roles for β-arrestins as scaffolds and adapters in GPCR signaling and trafficking. Curr. Opin. Cell Biol. 13, 139-145
46. Luttrell, L. M. and Lefkowitz, R. J. (2002) The role of β-arrestins inthe termination and transduction of G-protein-coupled receptor signals. J. Cell Sci. 115, 455-465