Dynamic architecture of a protein kinase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 43, 2014, Pages E4623-E4631

  McClendon, Christopher L ^a   Kornev, Alexandr P ^a,b   Gilson, Michael K ^a   Taylora, Susan S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b San Diego   (United States)

Author keywords

Community analysis; Molecular dynamics; Phosphorylation

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; ADENOSINE TRIPHOSPHATE; LIGAND; MAGNESIUM; PROTEIN KINASE;

ARTICLE; ENZYME STRUCTURE; HYDROPHOBICITY; ALLOSTERISM; CHEMISTRY; DNA TEMPLATE; ENZYME ACTIVE SITE; METABOLISM; MOLECULAR DYNAMICS; MUTAGENESIS; REPRODUCIBILITY;

ADENOSINE TRIPHOSPHATE; ALLOSTERIC REGULATION; CATALYTIC DOMAIN; LIGANDS; MAGNESIUM; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS; PROTEIN KINASES; REPRODUCIBILITY OF RESULTS; TEMPLATES, GENETIC;

EID: 84908265376     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1418402111     Document Type: Article

References (97)

1. Johnson DA, Akamine P, Radzio-Andzelm E, Madhusudan M, Taylor SS (2001) Dynamics of cAMP-dependent protein kinase. Chem Rev 101(8):2243-2270.
2. Huse M, Kuriyan J (2002) The conformational plasticity of protein kinases. Cell 109(3):275-282.
3. Taylor SS, Keshwani MM, Steichen JM, Kornev AP (2012) Evolution of the eukaryotic protein kinases as dynamic molecular switches. Philos Trans R Soc Lond B Biol Sci 367(1602):2517-2528.
4. Shaw AS, Kornev AP, Hu J, Ahuja LG, Taylor SS (2014) Kinases and pseudokinases: Lessons from RAF. Mol Cell Biol 34(9):1538-1546.
5. Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: Conserved features and deduced phylogeny of the catalytic domains. Science 241(4861):42-52.
6. Knighton DR, et al. (1991) Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253(5018):407-414.
7. Taylor SS, Kornev AP (2011) Protein kinases: Evolution of dynamic regulatory proteins. Trends Biochem Sci 36(2):65-77.
8. Kornev AP, Haste NM, Taylor SS, Eyck LF (2006) Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism. Proc Natl Acad Sci USA 103(47):17783-17788.
9. Kornev AP, Taylor SS, Ten Eyck LF (2008) A helix scaffold for the assembly of active protein kinases. Proc Natl Acad Sci USA 105(38):14377-14382.
10. Bernhard S, Noé F (2010) Optimal identification of semi-rigid domains in macromolecules from molecular dynamics simulation. PLoS ONE 5(5):e10491.
11. Tsigelny I, et al. (1999) 600 ps molecular dynamics reveals stable substructures and flexible hinge points in cAMP dependent protein kinase. Biopolymers 50(5):513-524.
12. Nagar B, et al. (2003) Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 112(6):859-871.
13. Shudler M, Niv MY (2009) BlockMaster: Partitioning protein kinase structures using normal-mode analysis. J Phys Chem A 113(26):7528-7534.
14. Girvan M, Newman ME (2002) Community structure in social and biological networks. Proc Natl Acad Sci USA 99(12):7821-7826.
15. Clauset A, Newman ME, Moore C (2004) Finding community structure in very large networks. Phys Rev E Stat Nonlin Soft Matter Phys 70(6 Pt 2):066111.
16. Newman ME (2006) Modularity and community structure in networks. Proc Natl Acad Sci USA 103(23):8577-8582.
17. Fortunato S (2010) Community detection in graphs. Phys Rep 486(3-5):75-174.
18. Sethi A, Eargle J, Black AA, Luthey-Schulten Z (2009) Dynamical networks in tRNA: protein complexes. Proc Natl Acad Sci USA 106(16):6620-6625.
19. Kappel K, Wereszczynski J, Clubb RT, McCammon JA (2012) The binding mechanism, multiple binding modes, and allosteric regulation of Staphylococcus aureus Sortase A probed by molecular dynamics simulations. Protein Sci 21(12):1858-1871.
20. Kannan N, Haste N, Taylor SS, Neuwald AF (2007) The hallmark of AGC kinase functional divergence is its C-terminal tail, a cis-acting regulatory module. Proc Natl Acad Sci USA 104(4):1272-1277.
21. Shan Y, et al. (2009) A conserved protonation-dependent switch controls drug binding in the Abl kinase. Proc Natl Acad Sci USA 106(1):139-144.
22. Shan Y, et al. (2011) How does a drug molecule find its target binding site? J Am Chem Soc 133(24):9181-9183.
23. Shan Y, et al. (2012) Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 149(4):860-870.
24. Shan Y, Arkhipov A, Kim ET, Pan AC, Shaw DE (2013) Transitions to catalytically inactive conformations in EGFR kinase. Proc Natl Acad Sci USA 110(18):7270-7275.
25. Shukla D, Meng Y, Roux B, Pande VS (2014) Activation pathway of Src kinase reveals intermediate states as targets for drug design. Nat Commun 5:3397.
26. Masterson LR, et al. (2011) Dynamically committed, uncommitted, and quenched states encoded in protein kinase A revealed by NMR spectroscopy. Proc Natl Acad Sci USA 108(17):6969-6974.
27. Herberg FW, Doyle ML, Cox S, Taylor SS (1999) Dissection of the nucleotide and metalphosphate binding sites in cAMP-dependent protein kinase. Biochemistry 38(19):6352-6360.
28. Khavrutskii IV, Grant B, Taylor SS, McCammon JA (2009) A transition path ensemble study reveals a linchpin role for Mg(2+) during rate-limiting ADP release from protein kinase A. Biochemistry 48(48):11532-11545.
29. Bastidas AC, et al. (2013) Phosphoryl transfer by protein kinase A is captured in a crystal lattice. J Am Chem Soc 135(12):4788-4798.
30. McClendon CL, Friedland G, Mobley DL, Amirkhani H, Jacobson MP (2009) Quantifying correlations between allosteric sites in thermodynamic ensembles. J Chem Theory Comput 5(9):2486-2502.
31. Barrett CP, Noble ME (2005) Molecular motions of human cyclin-dependent kinase 2. J Biol Chem 280(14):13993-14005.
32. Lu B, Wong CF, McCammon JA (2005) Release of ADP from the catalytic subunit of protein kinase A: A molecular dynamics simulation study. Protein Sci 14(1):159-168.
33. Masterson LR, et al. (2010) Dynamics connect substrate recognition to catalysis in protein kinase A. Nat Chem Biol 6(11):821-828.
34. Thompson EE, et al. (2009) Comparative surface geometry of the protein kinase family. Protein Sci 18(10):2016-2026.
35. Zheng J, et al. (1993) Crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MgATP and peptide inhibitor. Biochemistry 32(9):2154-2161.
36. Yang J, et al. (2009) Contribution of non-catalytic core residues to activity and regulation in protein kinase A. J Biol Chem 284(10):6241-6248.
37. Herberg FW, Zimmermann B, McGlone M, Taylor SS (1997) 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 6(3):569-579.
38. Thompson EE, et al. (2009) Comparative surface geometry of the protein kinase family. Protein Sci 18(10):2016-2026.
39. Gosal G, Kochut KJ, Kannan N (2011) ProKinO: An ontology for integrative analysis of protein kinases in cancer. PLoS ONE 6(12):e28782.
40. Kannan N, Neuwald AF, Taylor SS (2008) Analogous regulatory sites within the alphaC-beta4 loop regions of ZAP-70 tyrosine kinase and AGC kinases. Biochim Biophys Acta 1784(1):27-32.
41. Meharena HS, et al. (2013) Deciphering the structural basis of eukaryotic protein kinase regulation. PLoS Biol 11(10):e1001680.
42. Kannan N, Neuwald AF (2005) Did protein kinase regulatory mechanisms evolve through elaboration of a simple structural component? J Mol Biol 351(5):956-972.
43. Ilouz R, et al. (2012) Localization and quaternary structure of the PKA RIβ holoenzyme. Proc Natl Acad Sci USA 109(31):12443-12448.
44. Kim C, Xuong NH, Taylor SS (2005) Crystal structure of a complex between the catalytic and regulatory (RIalpha) subunits of PKA. Science 307(5710):690-696.
45. Wu J, Brown SH, von Daake S, Taylor SS (2007) PKA type IIalpha holoenzyme reveals a combinatorial strategy for isoform diversity. Science 318(5848):274-279.
46. Zhang P, et al. (2012) Structure and allostery of the PKA RIIβ tetrameric holoenzyme. Science 335(6069):712-716.
47. Dar AC, Dever TE, Sicheri F (2005) Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR. Cell 122(6):887-900.
48. Song H, et al. (2001) Phosphoprotein-protein interactions revealed by the crystal structure of kinase-associated phosphatase in complex with phosphoCDK2. Mol Cell 7(3):615-626.
49. Jura N, et al. (2011) Catalytic control in the EGF receptor and its connection to general kinase regulatory mechanisms. Mol Cell 42(1):9-22.
50. Deminoff SJ, Ramachandran V, Herman PK (2009) Distal recognition sites in substrates are required for efficient phosphorylation by the cAMP-dependent protein kinase. Genetics 182(2):529-539.
51. Zhang J, et al. (2010) Targeting Bcr-Abl by combining allosteric with ATP-binding-site inhibitors. Nature 463(7280):501-506.
52. Kannan N, Taylor SS, Zhai Y, Venter JC, Manning G (2007) Structural and functional diversity of the microbial kinome. PLoS Biol 5(3):e17.
53. Hu J, et al. (2013) Allosteric activation of functionally asymmetric RAF kinase dimers. Cell 154(5):1036-1046.
54. Azam M, Seeliger MA, Gray NS, Kuriyan J, Daley GQ (2008) Activation of tyrosine kinases by mutation of the gatekeeper threonine. Nat Struct Mol Biol 15(10):1109-1118.
55. Meng Y, Roux B (2014) Locking the active conformation of c-Src kinase through the phosphorylation of the activation loop. J Mol Biol 426(2):423-435.
56. Roskoski R, Jr (2013) Anaplastic lymphoma kinase (ALK): Structure, oncogenic activation, and pharmacological inhibition. Pharmacol Res 68(1):68-94.
57. Gibbs CS, Zoller MJ (1991) Rational scanning mutagenesis of a protein kinase identifies functional regions involved in catalysis and substrate interactions. J Biol Chem 266(14):8923-8931.
58. Shaltiel S, Cox S, Taylor SS (1998) Conserved water molecules contribute to the extensive network of interactions at the active site of protein kinase A. Proc Natl Acad Sci USA 95(2):484-491.
59. Yang J, et al. (2012) A conserved Glu-Arg salt bridge connects coevolved motifs that define the eukaryotic protein kinase fold. J Mol Biol 415(4):666-679.
60. Steichen JM, et al. (2010) Global consequences of activation loop phosphorylation on protein kinase A. J Biol Chem 285(6):3825-3832.
61. Gibbs CS, Knighton DR, Sowadski JM, Taylor SS, Zoller MJ (1992) Systematic mutational analysis of cAMP-dependent protein kinase identifies unregulated catalytic subunits and defines regions important for the recognition of the regulatory subunit. J Biol Chem 267(7):4806-4814.
62. Batkin M, Schvartz I, 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(18):5366-5373.
63. Romano RA, Kannan N, Kornev AP, Allison CJ, Taylor SS (2009) A chimeric mechanism for polyvalent trans-phosphorylation of PKA by PDK1. Protein Sci 18(7):1486-1497.
64. Yonemoto W, McGlone ML, Grant B, Taylor SS (1997) Autophosphorylation of the catalytic subunit of cAMP-dependent protein kinase in Escherichia coli. Protein Eng 10(8):915-925.
65. Bastidas AC, et al. (2012) Role of N-terminal myristylation in the structure and regulation of cAMP-dependent protein kinase. J Mol Biol 422(2):215-229.
66. Bastidas AC, Pierce LC, Walker RC, Johnson DA, Taylor SS (2013) Influence of N-myristylation and ligand binding on the flexibility of the catalytic subunit of protein kinase A. Biochemistry 52(37):6368-6379.
67. Wu J, et al. (2005) Crystal structure of the E230Q mutant of cAMP-dependent protein kinase reveals an unexpected apoenzyme conformation and an extended N-terminal A helix. Protein Sci 14(11):2871-2879.
68. Grant BD, Tsigelny I, Adams JA, Taylor SS (1996) Examination of an active-site electrostatic node in the cAMP-dependent protein kinase catalytic subunit. Protein Sci 5(7):1316-1324.
69. Herberg FW, Zimmermann B, McGlone M, Taylor SS (1997) 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 6(3):569-579.
70. Moore MJ, Adams JA, Taylor SS (2003) 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 278(12):10613-10618.
71. Masterson LR, Mascioni A, Traaseth NJ, Taylor SS, Veglia G (2008) Allosteric cooperativity in protein kinase A. Proc Natl Acad Sci USA 105(2):506-511.
72. Halabi N, Rivoire O, Leibler S, Ranganathan R (2009) Protein sectors: Evolutionary units of three-dimensional structure. Cell 138(4):774-786.
73. Jacobson MP, et al. (2004) A hierarchical approach to all-atom protein loop prediction. Proteins 55(2):351-367.
74. Jiménez JS, Kupfer A, Gani V, Shaltiel S (1982) Salt-induced conformational changes in the catalytic subunit of adenosine cyclic 3′,5′-phosphate dependent protein kinase. Use for establishing a connection between one sulfhydryl group and the gamma-P subsite in the ATP site of this subunit. Biochemistry 21(7):1623-1630.
75. Nelson NC, Taylor SS (1981) Differential labeling and identification of the cysteine-containing tryptic peptides of catalytic subunit from porcine heart cAMP-dependent protein kinase. J Biol Chem 256(8):3743-3750.
76. Zheng J, et al. (1993) Crystal structures of the myristylated catalytic subunit of cAMP-dependent protein kinase reveal open and closed conformations. Protein Sci 2(10):1559-1573.
77. Jacobson MP, Kaminski GA, Friesner RA, Rapp CS (2002) Force field validation using protein side chain prediction. J Phys Chem B 106(44):11673-11680.
78. Case DA, et al. (2011) Amber11 (Univ of California, San Francisco).
79. Case DA, et al. (2012) Amber12 (Univ of California, San Francisco).
80. Hornak V, et al. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65(3):712-725.
81. Lindorff-Larsen K, et al. (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78(8):1950-1958.
82. Li DW, Brüschweiler R (2010) NMR-based protein potentials. Angew Chem Int Ed Engl 49(38):6778-6780.
83. Horn HW, et al. (2004) Development of an improved four-site water model for biomolecular simulations: TIP4P-Ew. J Chem Phys 120(20):9665-9678.
84. Meagher KL, Redman LT, Carlson HA (2003) Development of polyphosphate parameters for use with the AMBER force field. J Comput Chem 24(9):1016-1025.
85. Homeyer N, Horn AHC, Lanig H, Sticht H (2006) AMBER force-field parameters for phosphorylated amino acids in different protonation states: Phosphoserine, phosphothreonine, phosphotyrosine, and phosphohistidine. J Mol Model 12(3):281-289.
86. Bryce RA (2014) AMBER parameter Database. Available at www.pharmacy.manchester.ac.uk/bryce/amber. Accessed 22 September 2014.
87. Ryckaert JP, Ciccotti G, Berendsen HJC (1977) Numerical-integration of Cartesian equations of motion of a system with constraints-Molecular-dynamics of N-alkanes. J Comput Phys 23(3):327-341.
88. Götz AW, et al. (2012) Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized born. J Chem Theory Comput 8(5):1542-1555.
89. Le Grand S, Gotz AW, Walker RC (2013) SPFP: Speed without compromise-A mixed precision model for GPU accelerated molecular dynamics simulations. Comput Phys Commun 184(2):374-380.
90. Darden T, York D, Pedersen L (1993) Particle mesh Ewald - An N.Log(N) method for Ewald sums in large systems. J Chem Phys 98(12):10089-10092.
91. Nose S (1984) A unified formulation of the constant temperature molecular-dynamics methods. J Chem Phys 81(1):511-519.
92. Hoover WG (1985) Canonical dynamics: Equilibrium phase-space distributions. Phys Rev A 31(3):1695-1697.
93. Morcos F, et al. (2010) Modeling conformational ensembles of slow functional motions in Pin1-WW. PLOS Comput Biol 6(12):e1001015.
94. Wan X, Ma Y, McClendon CL, Huang LJ, Huang N (2013) Ab initio modeling and experimental assessment of Janus Kinase 2 (JAK2) kinase-pseudokinase complex structure. PLOS Comput Biol 9(4):e1003022.
95. McClendon CL, Hua L, Barreiro A, Jacobson MP (2012) Comparing conformational ensembles using the Kullback-Leibler divergence expansion. J Chem Theory Comput 8(6):2115-2126.
96. Newman MEJ (2004) Analysis of weighted networks. Phys Rev E Stat Nonlin Soft Matter Phys 70(5 Pt 2):056131.
97. Morcos F, et al. (2011) Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc Natl Acad Sci USA 108(49):E1293-E1301.