Frequency Response of a Protein to Local Conformational Perturbations

PLoS Computational Biology

Volumn 9, Issue 9, 2013, Pages

  Eren, Dilek ^a   Alakent, Burak ^a  

^a BOGAZICI UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ATOMS; CHAINS; CRYSTAL STRUCTURE; DIHEDRAL ANGLE; DISCRETE FOURIER TRANSFORMS; FREQUENCY RESPONSE; HYDROPHOBICITY; MOLECULAR DYNAMICS; NATURAL FREQUENCIES; PROTEINS; SIGNAL TRANSDUCTION;

CRYSTALS STRUCTURES; FUNDAMENTAL FREQUENCIES; LOCAL PERTURBATION; NONBONDED INTERACTION; POLAR INTERACTIONS; PROTEIN-TYROSINE PHOSPHATASE 1B; SIDE-CHAINS; SIGNAL PROPAGATION; SIGNALLING PATHWAYS; TARGETED MOLECULAR DYNAMICS;

SPECTRAL DENSITY;

CARBON; CARBON ALPHA; PROTEIN TYROSINE PHOSPHATASE 1B; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; EQUILIBRIUM CONSTANT; FOURIER TRANSFORMATION; FREQUENCY ANALYSIS; FREQUENCY RESPONSE; HYDROPHOBICITY; LIGAND BINDING; MAGNITUDE ESTIMATION METHOD; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; PHASE TRANSITION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; SIMULATION; SPECTROMETRY; STATISTICAL ANALYSIS;

CLUSTER ANALYSIS; MOLECULAR DYNAMICS SIMULATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; PROTEINS;

EID: 84884678933     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003238     Document Type: Article

References (96)

1. Daniel RM, Dunn RV, Finney JL, Smith JC, (2003) The role of dynamics in enzyme activity. Annu Rev Biophys Biomol Struct 32: 69-92.
2. Henzler-Wildman KA, Thai V, Lei M, Ott M, Wolf-Watz M, et al. (2007) Intrinsic motions along an enzymatic reaction trajectory. Nature 450: 838-844.
3. Bakan A, Bahar I, (2009) The intrinsic dynamics of enzymes plays a dominant role in determining the structural changes induced upon inhibitor binding. Proc Natl Acad Sci U S A 106: 14349-14354.
4. Alakent B, Kurkcuoglu Z, Doruker P, (2012) Functional Dynamics of Proteins Elucidated by Statistical Analysis of Simulation Data. Current Physical Chemistry 2: 443-451.
5. Ansari A, Berendzen J, Bowne SF, Frauenfelder H, Iben IE, et al. (1985) Protein states and proteinquakes. Proc Natl Acad Sci U S A 82: 5000-5004.
6. Elber R, Karplus M, (1987) Multiple conformational states of proteins: a molecular dynamics analysis of myoglobin. Science 235: 318-321.
7. Garcia AE, (1992) Large-amplitude nonlinear motions in proteins. Phys Rev Lett 68: 2696-2699.
8. Tilton RF Jr, Dewan JC, Petsko GA, (1992) Effects of temperature on protein structure and dynamics: X-ray crystallographic studies of the protein ribonuclease-A at nine different temperatures from 98 to 320 K. Biochemistry 31: 2469-2481.
9. Vitkup D, Ringe D, Petsko GA, Karplus M, (2000) Solvent mobility and the protein 'glass' transition. Nat Struct Biol 7: 34-38.
10. Jeffrey PD, Russo AA, Polyak K, Gibbs E, Hurwitz J, et al. (1995) Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376: 313-320.
11. Sawaya MR, Kraut J, (1997) Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence. Biochemistry 36: 586-603.
12. Brown NR, Noble ME, Lawrie AM, Morris MC, Tunnah P, et al. (1999) Effects of phosphorylation of threonine 160 on cyclin-dependent kinase 2 structure and activity. J Biol Chem 274: 8746-8756.
13. Kumar S, Ma B, Tsai CJ, Sinha N, Nussinov R, (2000) Folding and binding cascades: dynamic landscapes and population shifts. Protein Sci 9: 10-19.
14. Tsai CJ, del Sol A, Nussinov R, (2008) Allostery: absence of a change in shape does not imply that allostery is not at play. J Mol Biol 378: 1-11.
15. Cui Q, Karplus M, (2008) Allostery and cooperativity revisited. Protein Sci 17: 1295-1307.
16. Rod TH, Radkiewicz JL, Brooks CL, (2003) Correlated motion and the effect of distal mutations in dihydrofolate reductase. Proc Natl Acad Sci U S A 100: 6980-6985.
17. Schmid FF, Meuwly M, (2007) All-atom simulations of structures and energetics of c-di-GMP-bound and free PleD. J Mol Biol 374: 1270-1285.
18. Cansu S, Doruker P, (2008) Dimerization affects collective dynamics of triosephosphate isomerase. Biochemistry 47: 1358-1368.
19. Nguyen PH, (2006) Complexity of free energy landscapes of peptides revealed by nonlinear principal component analysis. Proteins 65: 898-913.
20. Das P, Moll M, Stamati H, Kavraki LE, Clementi C, (2006) Low-dimensional, free-energy landscapes of protein-folding reactions by nonlinear dimensionality reduction. Proc Natl Acad Sci U S A 103: 9885-9890.
21. Lange OF, Grubmuller H, (2008) Full correlation analysis of conformational protein dynamics. Proteins 70: 1294-1312.
22. Sakuraba S, Joti Y, Kitao A, (2010) Detecting coupled collective motions in protein by independent subspace analysis. J Chem Phys 133: 185102.
23. Moritsugu K, Njunda BM, Smith JC, (2010) Theory and normal-mode analysis of change in protein vibrational dynamics on ligand binding. J Phys Chem B 114: 1479-1485.
24. Alakent B, Baskan S, Doruker P, (2011) Effect of ligand binding on the intraminimum dynamics of proteins. J Comput Chem 32: 483-496.
25. Bode C, Kovacs IA, Szalay MS, Palotai R, Korcsmaros T, et al. (2007) Network analysis of protein dynamics. FEBS Lett 581: 2776-2782.
26. Kong Y, Karplus M, (2007) The signaling pathway of rhodopsin. Structure 15: 611-623.
27. Zhang Z, Wriggers W, (2006) Local feature analysis: a statistical theory for reproducible essential dynamics of large macromolecules. Proteins 64: 391-403.
28. Laine E, Auclair C, Tchertanov L, (2012) Allosteric communication across the native and mutated KIT receptor tyrosine kinase. PLoS Comput Biol 8: e1002661.
29. Kamberaj H, van der Vaart A, (2009) Extracting the Causality of Correlated Motions from Molecular Dynamics Simulations. Biophys J 97: 1747-1755.
30. Ota N, Agard DA, (2005) Intramolecular signaling pathways revealed by modeling anisotropic thermal diffusion. J Mol Biol 351: 345-354.
31. Sharp K, Skinner JJ, (2006) Pump-probe molecular dynamics as a tool for studying protein motion and long range coupling. Proteins 65: 347-361.
32. Leitner DM, (2008) Energy flow in Proteins. Annu Rev Phys Chem 59: 233-259.
33. Ho BK, Perahia D, Buckle AM, (2012) Hybrid approaches to molecular simulation. Curr Opin Struct Biol 22: 386-393.
34. Ho BK, Agard DA, (2009) Probing the flexibility of large conformational changes in protein structures through local perturbations. PLoS Comput Biol 5: e1000343.
35. Dubay KH, Bothma JP, Geissler PL, (2011) Long-range intra-protein communication can be transmitted by correlated side-chain fluctuations alone. PLoS Comput Biol 7: e1002168.
36. Atilgan C, Atilgan AR, (2009) Perturbation-response scanning reveals ligand entry-exit mechanisms of ferric binding protein. PLoS Comput Biol 5: e1000544.
37. Gerek ZN, Ozkan SB, (2011) Change in allosteric network affects binding affinities of PDZ domains: analysis through perturbation response scanning. PLoS Comput Biol 7: e1002154.
38. Lu H-M, Liang J, (2009) Perturbation-based Markovian Transmission Model for Probing Allosteric Dynamics of Large Macromolecular Assembling: A Study of GroEL-GroES,. PLoS Comput Biol 5: e1000526.
39. Neel BG, Tonks NK, (1997) Protein tyrosine phosphatases in signal transduction. Curr Opin Cell Biol 9: 193-204.
40. Zhang ZY, Zhou B, Xie L, (2002) Modulation of protein kinase signaling by protein phosphatases and inhibitors. Pharmacol Ther 93: 307-317.
41. Elchebly M, Payette P, Michaliszyn E, Cromlish W, Collins S, et al. (1999) Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283: 1544-1548.
42. Zabolotny JM, Bence-Hanulec KK, Stricker-Krongrad A, Haj F, Wang Y, et al. (2002) PTP1B regulates leptin signal transduction in vivo. Dev Cell 2: 489-495.
43. Stuible M, Doody KM, Tremblay ML, (2008) PTP1B and TC-PTP: regulators of transformation and tumorigenesis. Cancer Metastasis Rev 27: 215-230.
44. Barford D, Flint AJ, Tonks NK, (1994) Crystal structure of human protein tyrosine phosphatase 1B. Science 263: 1397-1404.
45. Jia Z, Barford D, Flint AJ, Tonks NK, (1995) Structural basis for phosphotyrosine peptide recognition by protein tyrosine phosphatase 1B. Science 268: 1754-1758.
46. Pedersen AK, Peters GG, Moller KB, Iversen LF, Kastrup JS, (2004) Water-molecule network and active-site flexibility of apo protein tyrosine phosphatase 1B. Acta Crystallogr D Biol Crystallogr 60: 1527-1534.
47. Khajehpour M, Wu L, Liu S, Zhadin N, Zhang ZY, et al. (2007) Loop dynamics and ligand binding kinetics in the reaction catalyzed by the Yersinia protein tyrosine phosphatase. Biochemistry 46: 4370-4378.
48. Wiesmann C, Barr KJ, Kung J, Zhu J, Erlanson DA, et al. (2004) Allosteric inhibition of protein tyrosine phosphatase 1B. Nat Struct Mol Biol 11: 730-737.
49. Montalibet J, Skorey K, McKay D, Scapin G, Asante-Appiah E, et al. (2006) Residues distant from the active site influence protein-tyrosine phosphatase 1B inhibitor binding. J Biol Chem 281: 5258-5266.
50. Picha KM, Patel SS, Mandiyan S, Koehn J, Wennogle LP, (2007) The role of the C-terminal domain of protein tyrosine phosphatase-1B in phosphatase activity and substrate binding. J Biol Chem 282: 2911-2917.
51. Peters GH, Frimurer TM, Andersen JN, Olsen OH, (1999) Molecular dynamics simulations of protein-tyrosine phosphatase 1B. I. ligand-induced changes in the protein motions. Biophys J 77: 505-515.
52. Olmez EO, Alakent B, (2011) Alpha7 helix plays an important role in the conformational stability of PTP1B. J Biomol Struct Dyn 28: 675-693.
53. Ozcan A, Olmez EO, Alakent B, (2013) Effects of protonation state of Asp181 and position of active site water molecules on the conformation of PTP1B. Proteins 81: 788-804.
54. Manolakis DG, Ingle VK (2011) Applied digital signal processing: theory and practice. New York: Cambridge University Press. xv, 991 p. p.
55. Ikeguchi M, Ueno J, Sato M, Kidera A, (2005) Protein structural change upon ligand binding: linear response theory. Phys Rev Lett 94: 078102.
56. Nishihara Y, Kata S, Hayashi S, (2010) Protein collective motions coupled to ligand migration in myoglobin. Biophys J 98: 1649-1657.
57. Montgomery DC, Runger GC (2011) Applied statistics and probability for engineers. Hoboken, NJ: Wiley. xv, 768 p. p.
58. Altis A, Nguyen PH, Hegger R, Stock G, (2007) Dihedral angle principal component analysis of molecular dynamics simulations. J Chem Phys 126: 244111.
59. van Montfort RL, Congreve M, Tisi D, Carr R, Jhoti H, (2003) Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423: 773-777.
60. Pannifer ADB, Flint AJ, Tonks NK, Barford D, (1998) Visualization of the cysteinyl-phosphate intermediate of a protein-tyrosine phosphatase by X-ray crystallography. Journal of Biological Chemistry 273: 10454-10462.
61. Andersen JN, Mortensen OH, Peters GH, Drake PG, Iversen LF, et al. (2001) Structural and evolutionary relationships among protein tyrosine phosphatase domains. Mol Cell Biol 21: 7117-7136.
62. Hoff RH, Hengge AC, Wu L, Keng YF, Zhang ZY, (2000) Effects on General Acid Catalysis from Mutations of the Invariant Trypothan and Arginine Residues in the Protein Tyrosine Phosphatase from Yersinia. Biochemistry 39: 46-54.
63. Zhao Y, Wu L, Noh SJ, Guan KL, Zhang ZY, (1998) Altering the Nucleophile Specificity of a Protein-Tyrosine Phosphatase-Catalyzed Reaction: Probing the Function of the Invariant Glutamine Residues. J Biol Chem 273: 5484-5492.
64. Boyd SP, Vandenberghe L (2004) Convex optimization. Cambridge, UK; New York: Cambridge University Press. xiii, 716 p. p.
65. Hu Z, Bowen D, Southerland WM, del Sol A, Pan Y, et al. (2007) Ligand binding and circular permutation modify residue interaction network in DHFR. PLoS Comput Biol 3: e117.
66. Aftabuddin M, Kundu S, (2007) Hydrophobic, hydrophilic, and charged amino acid networks within protein. Biophys J 93: 225-231.
67. Bikadi Z, Demko L, Hazai E, (2007) Functional and structural characterization of a protein based on analysis of its hydrogen bonding network by hydrogen bonding plot. Arch Biochem Biophys 461: 225-234.
68. Dutta P, Horn PM, (1981) Low-frequency fluctuations in solids: 1/f noise. Reviews of Modern Physics 53: 497-516.
69. Dewey TG, Bann JG, (1992) Protein dynamics and 1/f noise. Biophys J 63: 594-598.
70. Carlini P, Bizzarri AR, Cannistraro S, (2002) Temporal fluctuations in the potential energy of proteins: 1/fα noise and diffusion. Physica D 165: 242-250.
71. Bouchaud JP, Comtet A, Georges A, Le Doussal P, (1987) Anomalous diffusion in random media of any dimensionality. Journal de Physique 48: 1445-1450.
72. Alakent B, Doruker P, Camurdan MC, (2004) Time series analysis of collective motions in proteins. J Chem Phys 120: 1072-1088.
73. Kannan N, Vishveshwara S, (1999) Identification of side-chain clusters in protein structures by a graph spectral method. J Mol Biol 292: 441-464.
74. Davis IW, Arendall WB, Richardson DC, Richardson JS, (2006) The backrub motion: how protein backbone shrugs when a sidechain dances. Structure 14: 265-274.
75. Cote Y, Senet P, Delarue P, Maisuradze GG, Scheraga HA, (2012) Anomalous diffusion and dynamical correlation between the side chains and the main chain of proteins in their native state. Proc Natl Acad Sci U S A 109: 10346-10351.
76. Hartigan JA (1975) Clustering algorithms. New York,: Wiley. xiii, 351 p. p.
77. Tehver R, Chen J, Thirumalai D, (2009) Allostery Wiring Diagrams in the Transitions that Drive the GroEL Reaction Cycle. J Mol Biol 387: 390-406.
78. Schneider R, Beumer C, Simard JR, Grutter C, Rauh D, (2013) Selective Detection of Allosteric Phosphatase Inhibitors. J Am Chem Soc 135: 6838-6841.
79. Critton DA, Tautz L, Page R, (2011) Visualizing active-site dynamics in single crystals of HePTP: opening of the WPD loop involves coordinated movement of the E loop. J Mol Biol 405: 619-629.
80. Ovchinnikov V, Karplus M, (2012) Analysis and Elimination of a Bias in Targeted Molecular Dynamics Simulations of Conformational Transitions: Application to Calmodulin. J Phys Chem B 116: 8584-8603.
81. Parker TS, Chua LO, (1987) Chaos- a Tutorial for Engineers. Proceedings of the Ieee 75: 982-1008.
82. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
83. Zhang ZY, Dixon JE, (1993) Active site labeling of the Yersinia protein tyrosine phosphatase: the determination of the pKa of the active site cysteine and the function of the conserved histidine 402. Biochemistry 32: 9340-9345.
84. Lohse DL, Denu JM, Santoro N, Dixon JE, (1997) Roles of aspartic acid-181 and serine-222 in intermediate formation and hydrolysis of the mammalian protein-tyrosine-phosphatase PTP1. Biochemistry 36: 4568-4575.
85. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38, 33-38, 27-38.
86. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, et al. (1995) A Smooth Particle Mesh Ewald Method. J Chem Phys 103: 8577-8593.
87. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
88. Brooks BR, Brooks CL, Mackerell AD, Nilsson L, Petrella RJ, et al. (2009) CHARMM: the biomolecular simulation program. J Comput Chem 30: 1545-1614.
89. Foloppe N, Sagemark J, Nordstrand K, Berndt KD, Nilsson L, (2001) Structure, dynamics and electrostatics of the active site of glutaredoxin 3 from Escherichia coli: comparison with functionally related proteins. J Mol Biol 310: 449-470.
90. van der Vaart A, Karplus M, (2005) Simulation of Conformational Transitions by the Restricted Perturbation-Targeted Molecular Dynamics Method,. J Chem Phys 112: 113903.
91. Schubert HL, Fauman EB, Stuckey JA, Dixon JE, Saper MA, (1995) A ligand-induced conformational change in the Yersinia protein tyrosine phosphatase. Protein Sci 4: 1904-1913.
92. Jackson JE, (1980) Principal Components and Factor-Analysis. 1. Principal Components. Journal of Quality Technology 12: 201-213.
93. Amadei A, Linssen AB, Berendsen HJ, (1993) Essential dynamics of proteins. Proteins 17: 412-425.
94. Tama F, Sanejouand YH, (2001) Conformational change of proteins arising from normal mode calculations. Protein Eng 14: 1-6.
95. Luyben WL (1990) Process modeling, simulation, and control for chemical engineers. New York: McGraw-Hill. xxiii, 725 p. p.
96. Brosilow C, Joseph B (2002) Techniques of model-based control. Upper Saddle River, N.J.: Prentice Hall. xxi, 680 p. p.