Dynamics-Driven Allostery in Protein Kinases

Trends in Biochemical Sciences

Volumn 40, Issue 11, 2015, Pages 628-647

  Kornev, Alexandr P ^a   Taylor, Susan S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Allostery; Community analysis; Protein dynamics; Protein kinases

Indexed keywords

PROTEIN KINASE;

ALLOSTERISM; ALPHA HELIX; AMINO TERMINAL SEQUENCE; BETA CHAIN; CARBOXY TERMINAL SEQUENCE; ENZYME ANALYSIS; ENZYME STRUCTURE; G LOOP STRUCTURE; HUMAN; HYDROPHILICITY; MATHEMATICAL COMPUTING; MOLECULAR DYNAMICS; N LOBE STRUCTURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; REVIEW; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; CHEMICAL PHENOMENA; METABOLISM; PHOSPHORYLATION;

ALLOSTERIC REGULATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; PHOSPHORYLATION; PROTEIN KINASES;

EID: 84951747918     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2015.09.002     Document Type: Review

References (105)

1. Monod J., et al. Allosteric proteins and cellular control systems. J. Mol. Biol. 1963, 6:306-329.
2. Gunasekaran K., et al. Is allostery an intrinsic property of all dynamic proteins?. Proteins 2004, 57:433-443.
3. Nussinov R., Tsai C.J. Allostery in disease and in drug discovery. Cell 2013, 153:293-305.
4. Lu S., et al. Harnessing allostery: a novel approach to drug discovery. Med. Res. Rev. 2014, 34:1242-1285.
5. Motlagh H.N., et al. Interplay between allostery and intrinsic disorder in an ensemble. Biochem. Soc. Trans. 2012, 40:975-980.
6. Cooper A., Dryden D.T. Allostery without conformational change. A plausible model. Eur. Biophys. J. 1984, 11:103-109.
7. Frederick K.K., et al. Conformational entropy in molecular recognition by proteins. Nature 2007, 448:325-329.
8. Petit C.M., et al. Hidden dynamic allostery in a PDZ domain. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18249-18254.
9. Popovych N., et al. Dynamically driven protein allostery. Nat. Struct. Mol. Biol. 2006, 13:831-838.
10. McElroy C., et al. TROSY-NMR studies of the 91kDa TRAP protein reveal allosteric control of a gene regulatory protein by ligand-altered flexibility. J. Mol. Biol. 2002, 323:463-473.
11. Manning G., et al. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
12. Wu P., et al. FDA-approved small-molecule kinase inhibitors. Trends Pharmacol. Sci. 2015, 36:422-439.
13. Cohen P. The origins of protein phosphorylation. Nat. Cell Biol. 2002, 4:E127-E130.
14. Johnson L.N., Lewis R.J. Structural basis for control by phosphorylation. Chem. Rev. 2001, 101:2209-2242.
15. Kuriyan J., Eisenberg D. The origin of protein interactions and allostery in colocalization. Nature 2007, 450:983-990.
16. Taylor S.S., et al. Assembly of allosteric macromolecular switches: lessons from PKA. Nat. Rev. Mol. Cell Biol. 2012, 13:646-658.
17. Antal C.E., et al. Intramolecular C2 domain-mediated autoinhibition of protein kinase C βII. Cell Rep. 2015, 12:1252-1260.
18. Jura N., et al. Catalytic control in the EGF receptor and its connection to general kinase regulatory mechanisms. Mol. Cell 2011, 42:9-22.
19. Heredia V.V., et al. Glucose-induced conformational changes in glucokinase mediate allosteric regulation: transient kinetic analysis. Biochemistry 2006, 45:7553-7562.
20. Donaldson T.L., Quinn J.A. Kinetic constants determined from membrane transport measurements: carbonic anhydrase activity at high concentrations. Proc. Natl. Acad. Sci. U.S.A. 1974, 71:4995-4999.
21. Lieser S.A., et al. Phosphoryl transfer step in the C-terminal Src kinase controls Src recognition. J. Biol. Chem. 2005, 280:7769-7776.
22. Grant B.D., et al. Kinetic analyses of mutations in the glycine-rich loop of cAMP-dependent protein kinase. Biochemistry 1998, 37:7708-7715.
23. Akamine P., et al. Dynamic features of cAMP-dependent protein kinase revealed by apoenzyme crystal structure. J. Mol. Biol. 2003, 327:159-171.
24. Adams J.A. Kinetic and catalytic mechanisms of protein kinases. Chem. Rev. 2001, 101:2271-2290.
25. Johnson D.A., et al. Dynamics of cAMP-dependent protein kinase. Chem. Rev. 2001, 101:2243-2270.
26. Masterson L.R., et al. Dynamics connect substrate recognition to catalysis in protein kinase A. Nat. Chem. Biol. 2010, 6:821-828.
27. Bao Z.Q., et al. Briefly bound to activate: transient binding of a second catalytic magnesium activates the structure and dynamics of CDK2 kinase for catalysis. Structure 2011, 19:675-690.
28. Kornev A.P., et al. Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17783-17788.
29. Kornev A.P., et al. A helix scaffold for the assembly of active protein kinases. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:14377-14382.
30. Taylor S.S., Kornev A.P. Protein kinases: evolution of dynamic regulatory proteins. Trends Biochem. Sci. 2011, 36:65-77.
31. Vadas O., et al. Structural basis for activation and inhibition of class I phosphoinositide 3-kinases. Sci. Signal. 2011, 4:re2.
32. Kannan N., Neuwald A.F. Did protein kinase regulatory mechanisms evolve through elaboration of a simple structural component?. J. Mol. Biol. 2005, 351:956-972.
33. Torkamani A., et al. Congenital disease SNPs target lineage specific structural elements in protein kinases. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:9011-9016.
34. Walker J.E., et al. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982, 1:945-951.
35. Ramakrishnan C., et al. A conformational analysis of Walker motif A [GXXXXGKT (S)] in nucleotide-binding and other proteins. Protein Eng. 2002, 15:783-798.
36. Iyer G.H., et al. Consequences of lysine 72 mutation on the phosphorylation and activation state of cAMP-dependent kinase. J. Biol. Chem. 2005, 280:8800-8807.
37. Boyken S.E., et al. A conserved isoleucine maintains the inactive state of Bruton's tyrosine kinase. J. Mol. Biol. 2014, 426:3656-3669.
38. Rodriguez-Viciana P., et al. Germline mutations in genes within the MAPK pathway cause cardio-facio-cutaneous syndrome. Science 2006, 311:1287-1290.
39. Hu J., et al. Kinase regulation by hydrophobic spine assembly in cancer. Mol. Cell. Biol. 2015, 35:264-276.
40. Scheeff E.D., Bourne P.E. Structural evolution of the protein kinase-like superfamily. PLoS Comput. Biol. 2005, 1:e49.
41. Taylor S.S., et al. PKA: a portrait of protein kinase dynamics. Biochim. Biophys. Acta 2004, 1697:259-269.
42. Meharena H.S., et al. Deciphering the structural basis of eukaryotic protein kinase regulation. PLoS Biol. 2013, 11:e1001680.
43. Azam M., et al. Activation of tyrosine kinases by mutation of the gatekeeper threonine. Nat. Struct. Mol. Biol. 2008, 15:1109-1118.
44. Hu J., et al. Allosteric activation of functionally asymmetric RAF kinase dimers. Cell 2013, 154:1036-1046.
45. Taylor S.S., et al. Evolution of the eukaryotic protein kinases as dynamic molecular switches. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2012, 367:2517-2528.
46. Thompson E.E., et al. Comparative surface geometry of the protein kinase family. Protein Sci. 2009, 18:2016-2026.
47. Kannan N., et al. The hallmark of AGC kinase functional divergence is its C-terminal tail, a cis-acting regulatory module. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1272-1277.
48. Jeffrey P.D., et al. Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 1995, 376:313-320.
49. Zhang X., et al. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 2006, 125:1137-1149.
50. Hindie V., et al. Structure and allosteric effects of low-molecular-weight activators on the protein kinase PDK1. Nat. Chem. Biol. 2009, 5:758-764.
51. McPherson R.A., et al. A different function for a critical tryptophan in c-Raf and Hck. Oncogene 2000, 19:3616-3622.
52. Herberg F.W., et al. Importance of the A-helix of the catalytic subunit of cAMP-dependent protein kinase for stability and for orienting subdomains at the cleft interface. Protein Sci. 1997, 6:569-579.
53. Bayliss R., et al. Structural basis of Aurora-A activation by TPX2 at the mitotic spindle. Mol. Cell 2003, 12:851-862.
54. Niefind K., et al. Crystal structure of human protein kinase CK2: insights into basic properties of the CK2 holoenzyme. EMBO J. 2001, 20:5320-5331.
55. Canagarajah B.J., et al. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 1997, 90:859-869.
56. Sun C., et al. Reversible and adaptive resistance to BRAF(V600E) inhibition in melanoma. Nature 2014, 508:118-122.
57. Tsigelny I., et al. 600 ps molecular dynamics reveals stable substructures and flexible hinge points in cAMP dependent protein kinase. Biopolymers 1999, 50:513-524.
58. Ruan Z., Kannan N. Mechanistic insights into R776H mediated activation of epidermal growth factor receptor kinase. Biochemistry 2015, 54:4216-4225.
59. Rajakulendran T., et al. A dimerization-dependent mechanism drives RAF catalytic activation. Nature 2009, 461:542-545.
60. Fan Y.X., et al. Mutational activation of ErbB2 reveals a new protein kinase autoinhibition mechanism. J. Biol. Chem. 2008, 283:1588-1596.
61. Moore M.J., et al. Structural basis for peptide binding in protein kinase A. Role of glutamic acid 203 and tyrosine 204 in the peptide-positioning loop. J. Biol. Chem. 2003, 278:10613-10618.
62. Yang J., et al. Allosteric network of cAMP-dependent protein kinase revealed by mutation of Tyr204 in the P+1 loop. J. Mol. Biol. 2005, 346:191-201.
63. Masterson L.R., et al. Allosteric cooperativity in protein kinase A. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:506-511.
64. Yang J., et al. A conserved glu-arg salt bridge connects coevolved motifs that define the eukaryotic protein kinase fold. J. Mol. Biol. 2012, 415:666-679.
65. Dar A.C., et al. Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR. Cell 2005, 122:887-900.
66. Kim C., et al. PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation. Cell 2007, 130:1032-1043.
67. Song H.W., et al. Phosphoprotein-protein interactions revealed by the crystal structure of kinase-associated phosphatase in complex with PhosphoCDK2. Mol. Cell 2001, 7:615-626.
68. Hantschel O., et al. A myristoyl/phosphotyrosine switch regulates c-Abl. Cell 2003, 112:845-857.
69. Deminoff S.J., et al. Distal recognition sites in substrates are required for efficient phosphorylation by the cAMP-dependent protein kinase. Genetics 2009, 182:529-539.
70. Masterson L.R., et al. Dynamically committed, uncommitted, and quenched states encoded in protein kinase A revealed by NMR spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:6969-6974.
71. Masterson L.R., et al. Allostery and binding cooperativity of the catalytic subunit of protein kinase A by NMR spectroscopy and molecular dynamics simulations. Adv. Protein Chem. Struct. Biol. 2012, 87:363-389.
72. Srivastava A.K., et al. Synchronous opening and closing motions are essential for cAMP-dependent protein kinaseA signaling. Structure 2014, 22:1735-1743.
73. Prowse C.N., Lew J. Mechanism of activation of ERK2 by dual phosphorylation. J. Biol. Chem. 2001, 276:99-103.
74. Yang J., et al. Crystal structure of a cAMP-dependent protein kinase mutant at 1.26 angstrom: New insights into the catalytic mechanism. J. Mol. Biol. 2004, 336:473-487.
75. Bastidas A.C., et al. Influence of N-myristylation and ligand binding on the flexibility of the catalytic subunit of protein kinase A. Biochemistry 2013, 52:6368-6379.
76. Zhang J., et al. Targeting Bcr-Abl by combining allosteric with ATP-binding-site inhibitors. Nature 2010, 463:501-506.
77. Piserchio A., et al. Assignment of backbone resonances in a eukaryotic protein kinase - ERK2 as a representative example. Methods Mol. Biol. 2012, 831:359-368.
78. Palmer A.G. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 2004, 104:3623-3640.
79. Kim J., et al. Dysfunctional conformational dynamics of protein kinase A induced by a lethal mutant of phospholamban hinder phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:3716-3721.
80. Olah G.A., et al. Solution structure of the cAMP-dependent protein kinase catalytic subunit and its contraction upon binding the protein kinase inhibitor peptide. Biochemistry 1993, 32:3649-3657.
81. Herberg F.W., et al. Dissection of the nucleotide and metal-phosphate binding sites in cAMP-dependent protein kinase. Biochemistry 1999, 38:6352-6360.
82. Li F., et al. Evidence for an internal entropy contribution to phosphoryl transfer: a study of domain closure, backbone flexibility, and the catalytic cycle of cAMP-dependent protein kinase. J. Mol. Biol. 2002, 315:459-469.
83. Wand A.J., et al. A surprising role for conformational entropy in protein function. Top. Curr. Chem. 2013, 337:69-94.
84. Xiao Y., et al. Phosphorylation releases constraints to domain motion in ERK2. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:2506-2511.
85. Tirion M.M. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys. Rev. Lett. 1996, 77:1905-1908.
86. Mahajan S., Sanejouand Y.H. On the relationship between low-frequency normal modes and the large-scale conformational changes of proteins. Arch. Biochem. Biophys. 2015, 567:59-65.
87. Shudler M., Niv M.Y. BlockMaster: partitioning protein kinase structures using normal-mode analysis. J. Phys. Chem. A 2009, 113:7528-7534.
88. Bhattacharyya M., Vishveshwara S. Probing the allosteric mechanism in pyrrolysyl-tRNA synthetase using energy-weighted network formalism. Biochemistry 2011, 50:6225-6236.
89. Sethi A., et al. Dynamical networks in tRNA:protein complexes. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:6620-6625.
90. Kappel K., et al. The binding mechanism, multiple binding modes, and allosteric regulation of Staphylococcus aureus sortase A probed by molecular dynamics simulations. Protein Sci. 2012, 21:1858-1871.
91. Vijayabaskar M.S., Vishveshwara S. Interaction energy based protein structure networks. Biophys. J. 2010, 99:3704-3715.
92. James K.A., Verkhivker G.M. Structure-based network analysis of activation mechanisms in the ErbB family of receptor tyrosine kinases: the regulatory spine residues are global mediators of structural stability and allosteric interactions. PLoS ONE 2014, 9:e113488.
93. Palla G., et al. Uncovering the overlapping community structure of complex networks in nature and society. Nature 2005, 435:814-818.
94. McClendon C.L., et al. Dynamic architecture of a protein kinase. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:E4623-E4631.
95. Girvan M., Newman M.E. Community structure in social and biological networks. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:7821-7826.
96. McClendon C.L., et al. Quantifying correlations between allosteric sites in thermodynamic ensembles. J. Chem. Theory Comput. 2009, 5:2486-2502.
97. Kannan N., et al. Analogous regulatory sites within the alpha C-beta 4 loop regions of ZAP-70 tyrosine kinase and AGC kinases. Biochim. Biophys. Acta 2008, 1784:27-32.
98. Hanks S.K., et al. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 1988, 241:42-52.
99. Knighton D.R., et al. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 1991, 253:407-414.
100. Changeux J.P. Allostery and the Monod-Wyman-Changeux model after 50 years. Annu. Rev. Biophys. 2012, 41:103-133.
101. Bhattacharyya R.P., et al. Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu. Rev. Biochem. 2006, 75:655-680.
102. Lockless S.W., Ranganathan R. Evolutionarily conserved pathways of energetic connectivity in protein families. Science 1999, 286:295-299.
103. Suel G.M., et al. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat. Struct. Biol. 2003, 10:59-69.
104. Berman H.M., et al. The Protein Data Bank. Nucleic Acids Res. 2000, 28:235-242.
105. Poulikakos P.I., et al. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 2010, 464:427-430.