Role of the amino terminus of G protein-coupled receptor kinase 2 in receptor phosphorylation

Biochemistry

Volumn 48, Issue 30, 2009, Pages 7325-7333

  Pao, Christina S ^a,b   Barker, Breann L ^a   Benovic, Jeffrey L ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENERGIC RECEPTORS; AMINO TERMINUS; AMPHIPATHIC; CATALYTIC ACTIVITY; CIRCULAR DICHROISM; G PROTEIN COUPLED RECEPTORS; G PROTEIN-COUPLED RECEPTOR KINASE; G PROTEIN-COUPLED RECEPTOR KINASE 2; INTRAMOLECULAR INTERACTIONS; KINASE ACTIVITY; POINT MUTATIONS; RECEPTOR BINDING; RECEPTOR INTERACTION; RECEPTOR SUBSTRATES; SECONDARY STRUCTURE PREDICTION; SYNTHETIC PEPTIDE; WILD TYPES; X RAY CRYSTAL STRUCTURES;

AMINATION; AMINO ACIDS; DICHROISM; ORGANIC ACIDS; PHOSPHORYLATION; SUBSTRATES;

AMINES;

AMINO ACID; G PROTEIN COUPLED RECEPTOR KINASE 2; RHODOPSIN; SYNTHETIC PEPTIDE; TUBULIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CIRCULAR DICHROISM; ENZYME ACTIVITY; MOLECULAR INTERACTION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECONDARY STRUCTURE; RECEPTOR BINDING;

AMINO ACID SEQUENCE; ANIMALS; ENZYME ACTIVATION; G-PROTEIN-COUPLED RECEPTOR KINASE 2; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; POINT MUTATION; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, ADRENERGIC, BETA-2; RHODOPSIN; SEQUENCE ALIGNMENT;

EID: 68049097974     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900408g     Document Type: Article

References (39)

1. Marinissen, M. J., and Gutkind, J. S. (2001) G-protein-coupled receptors and signaling networks: Emerging paradigms. Trends Pharmacol. Sci. 22, 368-376.
2. Gainetdinov, R. R., Premont, R. T., Bohn, L. M., Lefkowitz, R. J., and Caron, M. G. (2004) Desensitization of G protein-coupled receptors and neuronal functions. Annu. Rev. Neurosci. 27, 107-144.
3. Ferguson, S. S. (2001) Evolving concepts in G protein-coupled receptor endocytosis: The role in receptor desensitization and signaling. Pharmacol. Rev. 53, 1-24.
4. Moore, C. A., Milano, S. K., and Benovic, J. L. (2007) Regulation of receptor trafficking by GRKs and arrestins. Annu. Rev. Physiol. 69, 451-482.
5. Pitcher, J. A., Freedman, N. J., and Lefkowitz, R. J. (1998) G protein-coupled receptor kinases. Annu. Rev. Biochem. 67, 653-692.
6. Krupnick, J. G., and Benovic, J. L. (1998) The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu. Rev. Pharmacol. Toxicol. 38, 289-319.
7. DeWire, S. M., Ahn, S., Lefkowitz, R. J., and Shenoy, S. K. (2007) β-Arrestins and cell signaling. Annu. Rev. Physiol. 69, 483-510.
8. Pitcher, J. A., Inglese, J., Higgins, J. B., Arriza, J. L., Casey, P. J., Kim, C., Benovic, J. L., Kwatra, M. M., Caron, M. G., and Lefkowitz, R. J. (1992) Role of βγ subunits of G proteins in targeting the β-adrenergic receptor kinase to membrane-bound receptors. Science 257, 1264-1267.
9. Onorato, J. J., Gillis, M. E., Liu, Y., Benovic, J. L., and Ruoho, A. E. (1995) The β-adrenergic receptor kinase (GRK2) is regulated by phospholipids. J. Biol. Chem. 270, 21346-21353.
10. Carman, C. V., Barak, L. S., Chen, C., Liu-Chen, L. Y., Onorato, J. J., Kennedy, S. P., Caron, M. G., and Benovic, J. L. (2000) Mutational analysis of Gβγ and phospholipid interaction with G protein-coupled receptor kinase 2. J. Biol. Chem. 275, 10443-10452.
11. Kohout, T. A., and Lefkowitz, R. J. (2003) Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization. Mol. Pharmacol. 63, 9-18.
12. Ribas, C., Penela, P., Murga, C., Salcedo, A., Garcia-Hoz, C., Jurado-Pueyo, M., Aymerich, I., and Mayor, F., Jr. (2007) The G protein-coupled receptor kinase (GRK) interactome: Role of GRKs in GPCR regulation and signaling. Biochim. Biophys. Acta 1768, 913-922.
13. Lodowski, D. T., Barnhill, J. F., Pyskadlo, R. M., Ghirlando, R., Sterne-Marr, R., and Tesmer, J. J. (2005) The role of Gβγ and domain interfaces in the activation of G protein-coupled receptor kinase 2. Biochemistry 44, 6958-6970.
14. Lodowski, D. T., Pitcher, J. A., Capel, W. D., Lefkowitz, R. J., and Tesmer, J. J. (2003) Keeping G proteins at bay: A complex between G protein-coupled receptor kinase 2 and Gβγ. Science 300, 1256-1262.
15. Tesmer, V. M., Kawano, T., Shankaranarayanan, A., Kozasa, T., and Tesmer, J. J. (2005) Snapshot of activated G proteins at the membrane: The Gαq-GRK2-Gβγ complex. Science 310, 1686-1690.
16. Lodowski, D. T., Tesmer, V. M., Benovic, J. L., and Tesmer, J. J. (2006) The structure of G protein-coupled receptor kinase (GRK)-6 defines a second lineage of GRKs. J. Biol. Chem. 281, 16785-16793.
17. Singh, P., Wang, B., Maeda, T., Palczewski, K., and Tesmer, J. J. (2008) Structures of rhodopsin kinase in different ligand states reveal key elements involved in G protein-coupled receptor kinase activation. J. Biol. Chem. 283, 14053-14062.
18. Sterne-Marr, R., Tesmer, J. J., Day, P. W., Stracquatanio, R. P., Cilente, J. A., O'Connor, K. E., Pronin, A. N., Benovic, J. L., and Wedegaertner, P. B. (2003) G protein-coupled receptor kinase 2/Gαq/11 interaction. A novel surface on a regulator of G protein signaling homology domain for binding Gα subunits. J. Biol. Chem. 278, 6050-6058.
19. Yu, Q. M., Cheng, Z. J., Gan, X. Q., Bao, G. B., Li, L., and Pei, G. (1999) The amino terminus with a conserved glutamic acid of G protein-coupled receptor kinases is indispensable for their ability to phosphorylate photoactivated rhodopsin. J. Neurochem. 73, 1222-1227.
20. Noble, B., Kallal, L. A., Pausch, M. H., and Benovic, J. L. (2003) Development of a yeast bioassay to characterize G protein-coupled receptor kinases. Identification of an NH2-terminal region essential for receptor phosphorylation. J. Biol. Chem. 278, 47466-47476.
21. Benovic, J. L., Onorato, J., Lohse, M. J., Dohlman, H. G., Staniszewski, C., Caron, M. G., and Lefkowitz, R. J. (1990) Synthetic peptides of the hamster β2-adrenoceptor as substrates and inhibitors of the β-adrenoceptor kinase. Br. J. Clin. Pharmacol. 30 (Suppl. 1), 3S-12S.
22. Pao, C. S., and Benovic, J. L. (2005) Structure/function analysis of α2A-adrenergic receptor interaction with G protein-coupled receptor kinase 2. J. Biol. Chem. 280, 11052-11058.
23. Dhami, G. K., Babwah, A. V., Sterne-Marr, R., and Ferguson, S. S. (2005) Phosphorylation-independent regulation of metabotropic glutamate receptor 1 signaling requires G protein-coupled receptor kinase 2 binding to the second intracellular loop. J. Biol. Chem. 280, 24420-24427.
24. Palczewski, K., Buczylko, J., Lebioda, L., Crabb, J. W., and Polans, A. S. (1993) Identification of the N-terminal region in rhodopsin kinase involved in its interaction with rhodopsin. J. Biol. Chem. 268, 6004-6013.
25. Dhami, G. K., Dale, L. B., Anborgh, P. H., O'Connor-Halligan, K. E., Sterne-Marr, R., and Ferguson, S. S. (2004) G protein-coupled receptor kinase 2 regulator of G protein signaling homology domain binds to both metabotropic glutamate receptor 1a and Gαq to attenuate signaling. J. Biol. Chem. 279, 16614-16620.
26. Higgins, M. K., Oprian, D. D., and Schertler, G. F. (2006) Recoverin binds exclusively to an amphipathic peptide at the N terminus of rhodopsin kinase, inhibiting rhodopsin phosphorylation without affecting catalytic activity of the kinase. J. Biol. Chem. 281, 19426-19432.
27. Sterne-Marr, R., Leahey, P. A., Bresee, J. E., Dickson, H. M., Ho, W., Ragusa, M. J., Donnelly, R. M., Amie, S. M., Krywy, J. A., Brookins-Danz, E. D., Orakwue, S. C., Carr, M. J., Yoshino-Koh, K., Li, Q., and Tesmer, J. J. (2009) GRK2 activation by receptors: Role of the kinase large lobe and carboxyl-terminal tail. Biochemistry 48, 4285-4293.
28. Huang, C. C., Yoshino-Koh, K., and Tesmer, J. J. (2009) A surface of the kinase domain critical for the allosteric activation of G protein-coupled receptor kinases. J. Biol. Chem. 284, 17206-17215.
29. Kim, C. M., Dion, S. B., Onorato, J. J., and Benovic, J. L. (1993) Expression and characterization of two β-adrenergic receptor kinase isoforms using the baculovirus expression system. Receptor 3, 39-55.
30. Kobilka, B. K. (1995) Amino and carboxyl terminal modifications to facilitate the production and purification of a G protein-coupled receptor. Anal. Biochem. 231, 269-271.
31. Chen, Y. H., Yang, J. T., and Chau, K. H. (1974) Determination of the helix and β form of proteins in aqueous solution by circular dichroism. Biochemistry 13, 3350-3359.
32. Benovic, J. L., DeBlasi, A., Stone, W. C., Caron, M. G., and Lefkowitz, R. J. (1989) β-Adrenergic receptor kinase: Primary structure delineates a multigene family. Science 246, 235-240.
33. Carman, C. V., Som, T., Kim, C. M., and Benovic, J. L. (1998) Binding and phosphorylation of tubulin by G protein-coupled receptor kinases. J. Biol. Chem. 273, 20308-20316.
34. Pitcher, J. A., Hall, R. A., Daaka, Y., Zhang, J., Ferguson, S. S., Hester, S., Miller, S., Caron, M. G., Lefkowitz, R. J., and Barak, L. S. (1998) The G protein-coupled receptor kinase 2 is a microtubule-associated protein kinase that phosphorylates tubulin. J. Biol. Chem. 273, 12316-12324.
35. Chen, C. Y., Dion, S. B., Kim, C. M., and Benovic, J. L. (1993) β-Adrenergic receptor kinase. Agonist-dependent receptor binding promotes kinase activation. J. Biol. Chem. 268, 7825-7831.
36. Zhang, Y. X., Yan, S. L., and Zhou, H. M. (1996) Inactivation and conformational changes of aminoacyclase in trifluoroethanol solutions. J. Protein Chem. 15, 631-637.
37. Segawa, S., Fukuno, T., Fujiwara, K., and Noda, Y. (1991) Local structures in unfolded lysozyme and correlation with secondary structures in the native conformation: Helix-forming or -breaking propensity of peptide segments. Biopolymers 31, 497-509.
38. Mariggio, S., Garcia-Hoz, C., Sarnago, S., De Blasi, A., Mayor, F., Jr., and Ribas, C. (2006) Tyrosine phosphorylation of G-protein-coupled-receptor kinase 2 (GRK2) by c-Src modulates its interaction with Gαq. Cell. Signalling 18, 2004-2012.
39. Ames, J. B., Levay, K., Wingard, J. N., Lusin, J. D., and Slepak, V. Z. (2006) Structural basis for calcium-induced inhibition of rhodopsin kinase by recoverin. J. Biol. Chem. 281, 37237-37245.