GRK2 activation by receptors: Role of the kinase large lobe and carboxyl-terminal tail

Biochemistry

Volumn 48, Issue 20, 2009, Pages 4285-4293

  Sterne Marr, Rachel ^a   Leahey, P Alex ^a   Bresee, Jamee E ^a   Dickson, Heather M ^a   Ho, Wesley ^a   Ragusa, Michael J ^a   Donnelly, Ryan M ^a   Amie, Sarah M ^a   Krywy, Janet A ^a   Brookins Danz, Elizabeth D ^a   Orakwue, Somtochukwu C ^a   Carr, Michael J ^a   Yoshino Koh, Kae ^b   Li, Qianzhi ^c   Tesmer, John J G ^b  

^a SIENA COLLEGE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ADRENERGIC RECEPTORS; ATOMIC STRUCTURE; CARBOXYL-TERMINAL; G-PROTEIN COUPLED RECEPTORS; INTRACELLULAR LOOP; KINASE ACTIVITY; KINASE DOMAINS; MICHAELIS-MENTEN KINETIC; RECEPTOR BINDING; SIDE CHAINS;

CELL MEMBRANES; CYTOLOGY; SUBSTRATES;

CRYSTAL ATOMIC STRUCTURE;

BETA 2 ADRENERGIC RECEPTOR; G PROTEIN COUPLED RECEPTOR KINASE 2; RHODOPSIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RECEPTOR BINDING; STRUCTURE ANALYSIS;

ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; CRYSTALLOGRAPHY, X-RAY; G-PROTEIN-COUPLED RECEPTOR KINASE 2; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PEPTIDES; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ADRENERGIC, BETA-2; RHODOPSIN;

EID: 66149172246     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900151g     Document Type: Article

References (40)

1. Neves, S. R., and Iyengar, R. (2002) Modeling of signaling networks. BioEssays 24, 1110-1117. (Pubitemid 35464942)
2. Pitcher, J. A., Freedman, N. J., and Lefkowitz, R. J. (1998)G-protein-coupled receptor kinases. Annu. Rev. Biochem. 67, 653-692.
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. Hanks, S. K., and Hunter, T. (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. FASEB J. 9, 576-596.
5. Kannan, N., Haste, N., Taylor, S. S., and Neuwald, A. F. (2007) The hallmark of AGC kinase functional divergence is its C-terminal tail, a cis-acting regulatory module. Proc. Natl. Acad. Sci. U.S.A. 104, 1272-1277.
6. 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.
7. 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. (Pubitemid 43909634)
8. 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.
9. Huse, M., and Kuriyan, J. (2002) The conformational plasticity of protein kinases. Cell 109, 275-282. (Pubitemid 34606870)
10. Kornev, A. P., Haste, N. M., Taylor, S. S., and Eyck, L. F. (2006) Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism. Proc. Natl. Acad. Sci. U.S.A. 103, 17783-17788.
11. Fowles, C., Sharma, R., and Akhtar, M. (1988) Mechanistic studies on phosphorylation of photoexcited rhodopsin. FEBS Lett. 238, 56-60. (Pubitemid 18229477)
12. Palczewski, K., Buczylko, J., Kaplan, M. W., Polans, A. S., and Crabb, J. W. (1991) Mechanism of rhodopsin kinase activation J. Biol. Chem. 266, 12949-12955. (Pubitemid 21907292)
13. 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.
14. McCarthy, N. E., and Akhtar, M. (2002) Activation of rhodopsin kinase. Biochem. J. 363, 359-364.
15. 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. (Pubitemid 23090939)
16. 2-terminal region essential for receptor phosphorylation. J. Biol. Chem. 278, 47466-47476.
17. q to attenuate signaling. J. Biol. Chem. 279, 16614-16620.
18. Narayana, N., Cox, S., Nguyen-huu, X., Ten Eyck, L. F., and Taylor, S. S. (1997) A binary complex of the catalytic subunit of cAMP-dependent protein kinase and adenosine further defines conformational flexibility. Structure 5, 921-935. (Pubitemid 27324510)
19. Smith, C. M., Radzio-Andzelm, E., Madhusudan, Akamine, P., and Taylor, S. S. (1999) The catalytic subunit of cAMP-dependent protein kinase: Prototype for an extended network of communication. Prog. Biophys. Mol. Biol. 71, 313-341.
20. Gan, X. Q., Wang, J. Y., Yang, Q. H., Li, Z., Liu, F., Pei, G., and Li, L. (2000) Interaction between the conserved region in the C-terminal domain of GRK2 and rhodopsin is necessary for GRK2 to catalyze receptor phosphorylation. J. Biol. Chem. 275, 8469-8474. (Pubitemid 30180192)
21. Kunapuli, P., Gurevich, V. V., and Benovic, J. L. (1994) Phospholipid-stimulated autophosphorylation activates the G protein-coupled receptor kinase GRK5. J. Biol. Chem. 269, 10209-10212. (Pubitemid 24198207)
22. Gan, X., Ma, Z., Deng, N., Wang, J., Ding, J., and Li, L. (2004) Involvement of the C-terminal proline-rich motif of G protein-coupled receptor kinases in recognition of activated rhodopsin J. Biol. Chem. 279, 49741-49746. (Pubitemid 39577778)
23. Cerione, R. A., Strulovici, B., Benovic, J. L., Strader, C. D., Caron, M. G., and Lefkowitz, R. J. (1983) Reconstitution of β-adrenergic receptors in lipid vesicles: Affinity chromatography-purified receptors confer catecholamine responsiveness on a heterologous adenylate cyclase system. Proc. Natl. Acad. Sci. U.S.A. 80, 4899-4903.
24. 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.
25. Sterne-Marr, R., Dhami, G. K., Tesmer, J. J., and Ferguson, S. S. (2004) Characterization of GRK2 RH domain-dependent regulation of GPCR coupling to heterotrimeric G proteins. Methods Enzymol. 390, 310-336. (Pubitemid 39370660)
26. 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. (Pubitemid 40632414)
27. 2. Acta Crystallogr. D59, 936-939.
28. Shichi, H., and Somers, R. L. (1978) Light-dependent phosphorylation of rhodopsin. Purification and properties of rhodopsin kinase. J. Biol. Chem. 253, 7040-7046.
29. Der-Sarkissian, A., Jao, C. C., Chen, J., and Langen, R. (2003) Structural organization of α-synuclein fibrils studied by site-directed spin labeling. J. Biol. Chem. 278, 37530-37535. (Pubitemid 37175274)
30. 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.
31. 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. (in press).
32. 2-adrenoceptor as substrates and inhibitors of the β-adrenoceptor kinase. Br. J. Clin. Pharmacol. 30(Suppl. 1), 3S-12S.
33. Onorato, J. J., Palczewski, K., Regan, J. W., Caron, M. G., Lefkowitz, R. J., and Benovic, J. L. (1991) Role of acidic amino acids in peptide substrates of the β-adrenergic receptor kinase and rhodopsin kinase. Biochemistry 30, 5118-5125.
34. 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. (Pubitemid 28377594)
35. Pronin, A. N., Morris, A. J., Surguchov, A., and Benovic, J. L. (2000) Synucleins are a novel class of substrates for G protein-coupled receptor kinases. J. Biol. Chem. 275, 26515-26522.
36. Benovic, J. L., Mayor, F.Jr., Staniszewski, C., Lefkowitz, R. J., and Caron, M. G. (1987) Purification and characterization of the β-adrenergic receptor kinase. J. Biol. Chem. 262, 9026-9032.
37. 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.
38. Iino, M., Furugohri, T., Fukuzawa, A., and Shibano, T. (1997) Asp278 of human β-adrenergic receptor kinase 1 is essential for phosphorylation activity. Biochem. Biophys. Res. Commun. 239, 548-551. (Pubitemid 27489001)
39. Biondi, R. M., and Nebreda, A. R. (2003) Signalling specificity of Ser/Thr protein kinases through docking-site-mediated interactions. Biochem. J. 372, 1-13.
40. Palczewski, K., Ohguro, H., Premont, R. T., and Inglese, J. (1995) Rhodopsin kinase autophosphorylation. Characterization of site-specific mutations. J. Biol. Chem. 270, 15294-15298.