Atomic structure of GRK5 reveals distinct structural features novel for G protein-coupled receptor kinases

Journal of Biological Chemistry

Volumn 290, Issue 34, 2015, Pages 20629-20647

  Komolov, Konstantin E ^a   Bhardwaj, Anshul ^a   Benovic, Jeffrey L ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL STRUCTURE; ENZYMES; NUCLEOTIDES; PROTEINS; TETHERLINES;

ALZHEIMER DISEASE; AUTOPHOSPHORYLATION; G PROTEIN COUPLED RECEPTORS; G PROTEIN-COUPLED RECEPTOR KINASE; HUMAN PATHOLOGIES; NUCLEOTIDE BINDING; STRUCTURAL ELEMENTS; STRUCTURAL FEATURE;

CRYSTAL ATOMIC STRUCTURE;

ADENYLYLIMIDODIPHOSPHATE; CALMODULIN; G PROTEIN COUPLED RECEPTOR KINASE; G PROTEIN COUPLED RECEPTOR KINASE 5; G PROTEIN COUPLED RECEPTOR KINASE 6; MONOMER; NUCLEOTIDE; RHODOPSIN KINASE; SANGIVAMYCIN; ANTINEOPLASTIC ANTIBIOTIC; GRK5 PROTEIN, HUMAN; PYRIMIDINE NUCLEOSIDE; RECOMBINANT PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; AUTOPHOSPHORYLATION; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; HUMAN; INTERACTIONS WITH NUCLEIC ACID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; ANIMAL; BACULOVIRIDAE; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION; GENETICS; MOLECULAR GENETICS; MUTATION; PHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SPODOPTERA;

ADENYLYL IMIDODIPHOSPHATE; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BACULOVIRIDAE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; G-PROTEIN-COUPLED RECEPTOR KINASE 5; GENE EXPRESSION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PYRIMIDINE NUCLEOSIDES; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SPODOPTERA;

EID: 84939838883     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.647297     Document Type: Article

References (81)

1. 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
2. Gurevich, E. V., Tesmer, J. J., Mushegian, A., and Gurevich, V. V. (2012) G protein-coupled receptor kinases: more than just kinases and not only for GPCRs. Pharmacol. Ther. 133, 40-69
3. Premont, R. T., and Gainetdinov, R. R. (2007) Physiological roles of G protein-coupled receptor kinases and arrestins. Annu. Rev. Physiol. 69, 511-534
4. Martini, J. S., Raake, P., Vinge, L. E., DeGeorge, B. R., Jr., DeGeorge, B., Jr., Chuprun, J. K., Harris, D. M., Gao, E., Eckhart, A. D., Pitcher, J. A., and Koch, W. J. (2008) Uncovering G protein-coupled receptor kinase-5 as a histone deacetylase kinase in the nucleus of cardiomyocytes. Proc. Natl. Acad. Sci. U.S.A. 105, 12457-12462
5. Gold, J. I., Martini, J. S., Hullmann, J., Gao, E., Chuprun, J. K., Lee, L., Tilley, D. G., Rabinowitz, J. E., Bossuyt, J., Bers, D. M., and Koch, W. J. (2013) Nuclear translocation of cardiac G protein-coupled receptor kinase 5 downstream of select Gq -activating hypertrophic ligands is a calmodulin-dependent process. PLoS One 8, e57324
6. Jiang, X., Benovic, J. L., and Wedegaertner, P. B. (2007) Plasma membrane and nuclear localization of G protein coupled receptor kinase 6A. Mol. Biol. Cell 18, 2960-2969
7. Ungerer, M., Böhm, M., Elce, J. S., Erdmann, E., and Lohse, M. J. (1993) Altered expression of β-adrenergic receptor kinase and β1-adrenergic receptors in the failing human heart. Circulation 87, 454-463
8. Gros, R., Benovic, J. L., Tan, C. M., and Feldman, R. D. (1997) G-protein-coupled receptor kinase activity is increased in hypertension. J. Clin. Invest. 99, 2087-2093
9. Huang, Z. M., Gold, J. I., and Koch, W. J. (2011) G protein-coupled receptor kinases in normal and failing myocardium. Front. Biosci. 16, 3047-3060
10. Gold, J. I., Gao, E., Shang, X., Premont, R. T., and Koch, W. J. (2012) Determining the absolute requirement of G protein-coupled receptor kinase 5 for pathological cardiac hypertrophy: short communication. Circ. Res. 111, 1048-1053
11. Harris, D. M., Cohn, H. I., Pesant, S., and Eckhart, A. D. (2008) GPCR signalling in hypertension: role of GRKs. Clin. Sci. 115, 79-89
12. Wang, W. C., Mihlbachler, K. A., Bleecker, E. R., Weiss, S. T., and Liggett, S. B. (2008) A polymorphism of G-protein coupled receptor kinase5 alters agonist-promoted desensitization of β2-adrenergic receptors. Pharmacogenet. Genomics 18, 729-732
13. nd (2008) A GRK5 polymorphism that inhibits β-adrenergic receptor signaling is protective in heart failure. Nat. Med. 14, 510-517
14. Li, H., Gan, W., Lu, L., Dong, X., Han, X., Hu, C., Yang, Z., Sun, L., Bao, W., Li, P., He, M., Sun, L., Wang, Y., Zhu, J., Ning, Q., et al. (2013) A genomewide association study identifies GRK5 and RASGRP1 as type 2 diabetes loci in Chinese Hans. Diabetes 62, 291-298
15. Kim, J. I., Chakraborty, P., Wang, Z., and Daaka, Y. (2012) G-protein coupled receptor kinase 5 regulates prostate tumor growth. J. Urol. 187, 322-329
16. Chakraborty, P. K., Zhang, Y., Coomes, A. S., Kim, W.-J., Stupay, R., Lynch, L. D., Atkinson, T., Kim, J. I., Nie, Z., and Daaka, Y. (2014) G protein-coupled receptor kinase GRK5 phosphorylates moesin and regulates metastasis in prostate cancer. Cancer Res. 74, 3489-3500
17. Bychkov, E. R., Gurevich, V. V., Joyce, J. N., Benovic, J. L., and Gurevich, E. V. (2008) Arrestins and two receptor kinases are upregulated in Parkinson's disease with dementia. Neurobiol. Aging 29, 379-396
18. Arawaka, S., Wada, M., Goto, S., Karube, H., Sakamoto, M., Ren, C.-H., Koyama, S., Nagasawa, H., Kimura, H., Kawanami, T., Kurita, K., Tajima, K., Daimon, M., Baba, M., Kido, T., et al. (2006) The role of G-protein-coupled-receptor kinase 5 in pathogenesis of sporadic Parkinson's disease. J. Neurosci. 26, 9227-9238
19. Suo, Z., Cox, A. A., Bartelli, N., Rasul, I., Festoff, B. W., Premont, R. T., and Arendash, G. W. (2007) GRK5 deficiency leads to early Alzheimer-like pathology and working memory impairment. Neurobiol. Aging 28, 1873-1888
20. Chen, Y., Wang, F., Long, H., Chen, Y., Wu, Z., and Ma, L. (2011) GRK5 promotes F-actin bundling and targets bundles to membrane structures to control neuronal morphogenesis. J. Cell Biol. 194, 905-920
21. q/11 interaction. A novel surface on a regulator of G protein signaling homology domain for binding G α subunits. J. Biol. Chem. 278, 6050-6058
22. 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
23. Pronin, A. N., Satpaev, D. K., Slepak, V. Z., and Benovic, J. L. (1997) Regulation of G protein-coupled receptor kinases by calmodulin and localization of the calmodulin binding domain. J. Biol. Chem. 272, 18273-18280
24. 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
25. Lodowski, D. T., Barnhill, J. F., Pyskadlo, R. M., Ghirlando, R., Sterne- Marr, R., and Tesmer, J. J. (2005) The role of G ôô and domain interfaces in the activation of G protein-coupled receptor kinase 2. Biochemistry 44, 6958-6970
26. 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
27. q -GRK2-Gβγ complex. Science 310, 1686-1690
28. 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
29. Pao, C. S., Barker, B. L., and Benovic, J. L. (2009) Role of the amino terminusof G protein-coupled receptor kinase 2 in receptor phosphorylation. Biochemistry 48, 7325-7333
30. Boguth, C. A., Singh, P., Huang, C. C., and Tesmer, J. J. (2010) Molecular basis for activation of G protein-coupled receptor kinases. EMBO J. 29, 3249-3259
31. Huang, C.-C., Orban, T., Jastrzebska, B., Palczewski, K., and Tesmer, J. J. (2011) Activation of G protein-coupled receptor kinase 1 involves interactions between its N-terminal region and its kinase domain. Biochemistry 50, 1940-1949
32. Pronin, A. N., Loudon, R. P., and Benovic, J. L. (2002) Characterization of G protein-coupled receptor kinases. Methods Enzymol. 343, 547-559
33. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
34. McCoy, A. J. (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr. 63, 32-41
35. Afonine, P. V., Grosse-Kunstleve, R. W., Echols, N., Headd, J. J., Moriarty, N. W., Mustyakimov, M., Terwilliger, T. C., Urzhumtsev, A., Zwart, P. H., and Adams, P. D. (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367
36. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
37. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
38. Karplus, P. A., and Diederichs, K. (2012) Linking crystallographic model and data quality. Science 336, 1030-1033
39. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256-2268
40. Hayward, S., Kitao, A., and Berendsen, H. J. (1997) Model-free methods of analyzing domain motions in proteins from simulation: a comparison of normal mode analysis and molecular dynamics simulation of lysozyme. Proteins 27, 425-437
41. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, Version 1.3r1, Schrödinger, L.LC. New York
42. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32, W665-W667
43. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., Mc- Coy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954
44. Laskowski, R. A., and Swindells, M. B. (2011) LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J. Chem. Inf. Model. 51, 2778-2786
45. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S. E., Rowe, A. J., and Horton, J. C., eds) pp. 90-125, Royal Society of Chemistry, Cambridge, UK
46. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
47. Loomis, C. R., and Bell, R. M. (1988) Sangivamycin, a nucleoside analogue, is a potent inhibitor of protein kinase C. J. Biol. Chem. 263, 1682-1692
48. Tesmer, J. J. (2009) Structure and function of regulator of G protein signaling homology domains. Prog. Mol. Biol. Transl. Sci. 86, 75-113
49. Pronin, A. N., Carman, C. V., and Benovic, J. L. (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
50. Thiyagarajan, M. M., Stracquatanio, R. P., Pronin, A. N., Evanko, D. S., Benovic, J. L., and Wedegaertner, P. B. (2004) A predicted amphipathic helix mediates plasma membrane localization of GRK5. J. Biol. Chem. 279, 17989-17995
51. Pitcher, J. A., Fredericks, Z. L., Stone, W. C., Premont, R. T., Stoffel, R. H., Koch, W. J., and Lefkowitz, R. J. (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
52. Tesmer, J. J., Nance, M. R., Singh, P., and Lee, H. (2012) Structure of a monomeric variant of rhodopsin kinase at 2.5 Å resolution. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68, 622-625
53. Xu, H., Jiang, X., Shen, K., Fischer, C. C., and Wedegaertner, P. B. (2014) The regulator of G protein signaling (RGS) domain of G protein-coupled receptor kinase 5 (GRK5) regulates plasma membrane localization and function. Mol. Biol. Cell 25, 2105-2115
54. Taylor, S. S., Yang, J., Wu, J., Haste, N. M., Radzio-Andzelm, E., and Anand, G. (2004) PKA: A portrait of protein kinase dynamics. Biochim. Biophys. Acta 1697, 259-269
55. Zhang, P., Smith-Nguyen, E. V., Keshwani, M. M., Deal, M. S., Kornev, A. P., and Taylor, S. S. (2012) Structure and allostery of the PKA RIIβ tetrameric holoenzyme. Science 335, 712-716
56. Yang, J., Ten Eyck, L. F., Xuong, N. H., and Taylor, S. S. (2004) Crystal structure of a cAMP-dependent protein kinase mutant at 1.26 Å: new insights into the catalytic mechanism. J. Mol. Biol. 336, 4734-4787
57. Bastidas, A. C., Deal, M. S., Steichen, J. M., Keshwani, M. M., Guo, Y., and Taylor, S. S. (2012) Role of N-terminal myristylation in the structure and regulation of cAMP-dependent protein kinase. J. Mol. Biol. 422, 215-229
58. Yang, J., Cron, P., Good, V. M., Thompson, V., Hemmings, B. A., and Barford, D. (2002) Crystal structure of an activated Akt/protein kinase B ternary complex with GSK3-peptide and AMP-PNP. Nat. Struct. Biol. 9, 940-944
59. Shaltiel, S., Cox, S., and Taylor, S. S. (1998) Conserved water molecules contribute to the extensive network of interactions at the active site of protein kinase A. Proc. Natl. Acad. Sci. U.S.A. 95, 484-491
60. Huse, M., and Kuriyan, J. (2002) The conformational plasticity of protein kinases. Cell 109, 275-282
61. Hemmer, W., McGlone, M., Tsigelny, I., and Taylor, S. S. (1997) Role of the glycine triad in the ATP-binding site of cAMP-dependent protein kinase. J. Biol. Chem. 272, 16946-16954
62. Akamine, P., Madhusudan, Wu, J., Xuong, N.-H., Ten Eyck, L. F., and Taylor, S. S. (2003) Dynamic features of cAMP-dependent protein kinase revealed by apoenzyme crystal structure. J. Mol. Biol. 327, 159-171
63. 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 cisacting regulatory module. Proc. Natl. Acad. Sci. U.S.A. 104, 1272-1277
64. 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
65. Yang, J., Kennedy, E. J., Wu, J., Deal, M. S., Pennypacker, J., Ghosh, G., and Taylor, S. S. (2009) Contribution of noncatalytic core residues to activity and regulation in protein kinase A. J. Biol. Chem. 284, 6241-6248
66. Batkin, M., Schvartz, I., and Shaltiel, S. (2000) Snapping of the carboxyl terminal tail of the catalytic subunit of PKA onto its core: characterization of the sites by mutagenesis. Biochemistry 39, 5366-5373
67. Zhou, J., and Adams, J. A. (1997) Participation of ADP dissociation in the rate-determining step in cAMP-dependent protein kinase. Biochemistry 36, 15733-15738
68. Bastidas, A. C., Wu, J., and Taylor, S. S. (2015) Molecular features of product release for the PKA catalytic cycle. Biochemistry 54, 2-10
69. Thal, D. M., Homan, K. T., Chen, J., Wu, E. K., Hinkle, P. M., Huang, Z. M., Chuprun, J. K., Song, J., Gao, E., Cheung, J. Y., Sklar, L. A., Koch, W. J., and Tesmer, J. J. (2012) Paroxetine is a direct inhibitor of G protein-coupled receptor kinase 2 and increases myocardial contractility. ACS Chem. Biol. 7, 1830-1839
70. 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, 11209-11212
71. Buczyłko, J., Gutmann, C., and Palczewski, K. (1991) Regulation of rhodopsin kinase by autophosphorylation. Proc. Natl. Acad. Sci. U.S.A. 88, 2568-2572
72. 2+-binding proteins on G protein-coupled receptor kinases. Biochemistry 37, 13650-13659
73. Tidow, H., and Nissen, P. (2013) Structural diversity of calmodulin binding to its target sites. FEBS J. 280, 5551-5565
74. O'Neil, K. T., and DeGrado, W. F. (1990) How calmodulin binds its targets: sequence independent recognition of amphiphilic α-helices. Trends Biochem. Sci. 15, 59-64
75. Blundell, T. L., and Johnson, L. N. (1976) Protein Crystallography, pp. 375-377, Academic Press, London
76. Arndt, U. W., Crowther, R. A., and Mallett, J. F. (1968) A computer-linked cathode-ray tube microdensitometer for x-ray crystallography. J. Sci. Instrum. 1, 510-516
77. Diederichs, K., and Karplus, P. A. (1997) Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat. Struct. Biol. 4, 269-275
78. Weiss, M. S. (2001) Global indicators of X-ray data quality. J. Appl. Crystallogr. 34, 130-135
79. Brünger, A. T. (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475
80. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797
81. Homan, K. T., Waldschmidt, H. V., Glukhova, A., Cannavo, A., Song, J., Cheung, J. Y., Koch, W. J., Larsen, S. D., and Tesmer, J, J. (2015) Crystal structure of G protein-coupled receptor kinase 5 in complex with a rationally designed inhibitor. J. Biol. Chem. 290, M115.647370