Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes

Structure

Volumn 13, Issue 3, 2005, Pages 373-380

  Ma, Jianpeng ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Rice University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; LIGAND; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ALPHA HELIX; ANALYTIC METHOD; ATOM; CONFORMATIONAL TRANSITION; ENERGY TRANSFER; MATHEMATICAL COMPUTING; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN STRUCTURE; REVIEW; STRUCTURE ANALYSIS;

EID: 14844286108     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2005.02.002     Document Type: Review

References (84)

1. A.R. Atilgan, S.R. Durell, R.L. Jernigan, M.C. Demirel, O. Keskin, and I. Bahar Anisotropy of fluctuation dynamics of proteins with an elastic network model Biophys. J. 80 2001 505 515
2. I. Bahar, A.R. Atilgan, and B. Erman Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential Fold. Des. 2 1997 173 181
3. E. Balog, T. Becker, M. Oettl, R. Lechner, R. Daniel, J. Finney, and J.C. Smith Direct determination of vibrational density of states change on ligand binding to a protein Phys. Rev. Lett. 93 2004 028103
4. N. Ban, P. Nissen, J. Hansen, P.B. Moore, and T.A. Steitz The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution Science 289 2000 905 920
5. F. Beuron, T.C. Flynn, J. Ma, H. Kondo, X. Zhang, and P.S. Freemont Motions and negative cooperativity between p97 domains revealed by cryoelectron microscopy and quantized elastic deformational model J. Mol. Biol. 327 2003 619 629
6. K. Braig, Z. Otwinowski, R. Hedge, D.C. Boisvert, A. Joachimiak, A.L. Horwich, and P.B. Sigler The crystal structure of the bacterial chaperonin GroEL at 2.8 Å Nature 371 1994 578 586
7. J. Brink, S.J. Ludtke, Y. Kong, S.J. Wakil, J. Ma, and W. Chiu Experimental verification of conformational variation of human fatty acid synthase as predicted by normal mode analysis Structure (Camb.) 12 2004 185 191
8. B. Brooks, and M. Karplus Normal modes for specific motions of macromolecules: application to the hinge-bending mode of lysozyme Proc. Natl. Acad. Sci. USA 82 1985 4995 4999
9. C.L. Brooks III, M. Karplus, and B.M. Pettitt Proteins: a theoretical perspective of dynamics, structure, and thermodynamics Adv. Chem. Phys. 71 1988 1 249
10. R.E. Bruccoleri, M. Karplus, and J.A. McCammon The hinge-bending mode of a lysozyme-inhibitor complex Biopolymers 25 1986 1767 1802
11. J.M. Carazo Accessing information on the conformational flexibility of molecular machines Structure 12 2004 170 171
12. P. Chacon, F. Tama, and W. Wriggers Mega-dalton biomolecular motion captured from electron microscopy reconstructions J. Mol. Biol. 326 2003 485 492
13. Q. Cui, G. Li, J. Ma, and M. Karplus A normal mode analysis of structural plasticity in the biomolecular motor F(1)-ATPase J. Mol. Biol. 340 2004 345 372
14. S. Cusack, J. Smith, J. Finney, B. Tidor, and M. Karplus Inelastic neutron scattering analysis of picosecond internal protein dynamics. Comparison of harmonic theory with experiment J. Mol. Biol. 202 1988 903 908
15. J. Deak, H.L. Chiu, C.M. Lewis, and R.J.D. Miller Ultrafast phase grating studies of heme proteins: observation of the low-frequency modes directing functionally important protein motions J. Phys. Chem. 102 1998 6621 6634
16. R. Diamond On the use of normal modes in thermal parameters refinement: theory and application to the bovine pancreatic trypsin inhibitor Acta Crystallogr. A 46 1990 425 435
17. P. Doruker, R.L. Jernigan, and I. Bahar Dynamic of large proteins through hierarchical levels of coarse-grained structures J. Comput. Chem. 23 2002 119 127
18. E.G. Emberly, R. Mukhopadhyay, N.S. Wingreen, and C. Tang Flexibility of alpha-helices: results of a statistical analysis of database protein structures J. Mol. Biol. 327 2003 229 237
19. T.C. Flynn, and J. Ma Theoretical analysis of twist/bend ratio and mechanical moduli of bacterial flagellar hook and filament Biophys. J. 86 2004 3204 3210
20. Y.Q. Gao, W. Yang, R.A. Marcus, and M. Karplus A model for the cooperative free energy transduction and kinetics of ATP hydrolysis by F1-ATPase Proc. Natl. Acad. Sci. USA 100 2003 11339 11344
21. C.S. Goh, D. Milburn, and M. Gerstein Conformational changes associated with protein-protein interactions Curr. Opin. Struct. Biol. 14 2004 104 109
22. T. Haliloglu, I. Bahar, and B. Erman Gaussian dynamics of folded proteins Phys. Rev. Lett. 79 1997 3090 3093
23. K. Hinsen Analysis of domain motions by approximate normal mode calculations Proteins 33 1998 417 429
24. K. Hinsen, A.J. Petrescu, S. Dellerue, M.C. Bellissent-Funel, and G.R. Kneller Harmonicity in slow protein dynamics Chem. Phys. 261 2000 25 37
25. A. Horovitz, and O. Yifrach On the relationship between the hill coefficients for steady-state and transient kinetic data: A criterion for concerted transitions in allosteric proteins Bull. Math. Biol. 62 2000 241 246
26. A. Horovitz, Y. Fridmann, G. Kafri, and O. Yifrach Review: allostery in chaperonins J. Struct. Biol. 135 2001 104 114
27. M. Karplus, and Y.Q. Gao Biomolecular motors: the F1-ATPase paradigm Curr. Opin. Struct. Biol. 14 2004 250 259
28. D. Kern, and E.R. Zuiderweg The role of dynamics in allosteric regulation Curr. Opin. Struct. Biol. 13 2003 748 757
29. O. Keskin, I. Bahar, D. Flatow, D.G. Covell, and R.L. Jernigan Molecular mechanisms of chaperonin GroEL-GroES function Biochemistry 41 2002 491 501
30. A. Kidera, K. Inaka, M. Matsushima, and N. Go Normal mode refinement: crystallographic refinement of protein dynamic structure applied to human lysozyme Biopolymers 32 1992 315 319
31. Y. Kong, D. Ming, Y. Wu, J.K. Stoops, Z.H. Zhou, and J. Ma Conformational flexibility of pyruvate dehydrogenase complexes: a computational analysis by quantized elastic deformational model J. Mol. Biol. 330 2003 129 135
32. J. Kottalam, and D.A. Case Langevin modes of macromolecules: applications to crambin and DNA hexamers Biopolymers 29 1990 1409 1421
33. W.G. Krebs, V. Alexandrov, C.A. Wilson, N. Echols, H. Yu, and M. Gerstein Normal mode analysis of macromolecular motions in a database framework: developing mode concentration as a useful classifying statistic Proteins 48 2002 682 695
34. S. Kumar, B. Ma, C.J. Tsai, N. Sinha, and R. Nussinov Folding and binding cascades: dynamic landscapes and population shifts Protein Sci. 9 2000 10 19
35. S. Kundu, J.S. Melton, D.C. Sorensen, and G.N. Phillips Jr. Dynamics of proteins in crystals: comparison of experiment with simple models Biophys. J. 83 2002 723 732
36. G. Lamm, and A. Szabo Langevin modes of macromolecules J. Chem. Phys. 85 1986 7334 7348
37. A. Leo-Macias, P. Lopez-Romero, D. Lupyan, D. Zerbino, and A.R. Ortiz An analysis of core deformations in protein superfamilies Biophys. J. 88 2005 1291 1299
38. M. Levitt, C. Sander, and P.S. Stern Protein normal-mode dynamics: trypsin inhibitor, crambin, ribonuclease and lysozyme J. Mol. Biol. 181 1985 423 447
39. G. Li, and Q. Cui A coarse-grained normal mode approach for macromolecules: an efficient implementation and application to Ca(2+)-ATPase Biophys. J. 83 2002 2457 2474
40. W.N. Lipscomb Structure and catalysis of enzymes Annu. Rev. Biochem. 52 1983 17 34
41. J. Ma New advances in normal mode analysis of supermolecular complexes and applications to structural refinement Curr. Protein Pept. Sci. 5 2004 119 123
42. J. Ma, and M. Karplus Ligand-induced conformational changes in ras p21: a normal mode and energy minimization analysis J. Mol. Biol. 274 1997 114 131
43. J. Ma, and M. Karplus The allosteric mechanism of the chaperonin GroEL: a dynamic analysis Proc. Natl. Acad. Sci. USA 95 1998 8502 8507
44. J. Ma, P.B. Sigler, Z. Xu, and M. Karplus A dynamic model for the allosteric mechanism of GroEL J. Mol. Biol. 302 2000 303 313
45. J. Ma, T.C. Flynn, Q. Cui, A. Leslie, J.E. Walker, and M. Karplus A dynamic analysis of the rotation mechanism for conformational change in F1-ATPase Structure 10 2002 921 931
46. A.D. MacKerell, D. Bashford Jr., M. Bellott, R.L. Dunbrack Jr., J.D. Evanseck, M.J. Field, S. Fischer, J. Gao, H. Guo, and S. Ha All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B102 1998 3586 3616
47. D.A. McQuarrie Statistical Mechanics 1976 Harper & Row New York
48. D. Ming, Y. Kong, M. Lambert, Z. Huang, and J. Ma How to describe protein motion without amino-acid sequence and atomic coordinates Proc. Natl. Acad. Sci. USA 99 2002 8620 8625
49. D. Ming, Y. Kong, S.J. Wakil, J. Brink, and J. Ma Domain movements in human fatty acid synthase by quantized elastic deformational model Proc. Natl. Acad. Sci. USA 99 2002 7895 7899
50. D. Ming, Y. Kong, Y. Wu, and J. Ma Simulation of F-actin filaments of several microns Biophys. J. 85 2003 27 35
51. D. Ming, Y. Kong, Y. Wu, and J. Ma Substructure synthesis method for simulating large molecular complexes Proc. Natl. Acad. Sci. USA 100 2003 104 109
52. O. Miyashita, J.N. Onuchic, and P.G. Wolynes Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins Proc. Natl. Acad. Sci. USA 100 2003 12570 12575
53. A.G. Murzin, S.E. Brenner, T. Hubbard, and C. Chothia SCOP: a structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247 1995 536 540
54. J.N. Onuchic, Z. Luthey-Schulten, and P.G. Wolynes Theory of protein folding: the energy landscape perspective Annu. Rev. Phys. Chem. 48 1997 545 600
55. M.F. Perutz The Croonian Lecture, 1968. The haemoglobin molecule Proc. R. Soc. Lond. B. Biol. Sci. 173 1969 113 140
56. M.F. Perutz Structure and function of hemoglobin Harvey Lect. 63 1969 213 261
57. V. Reat, R. Dunn, M. Ferrand, J.L. Finney, R.M. Daniel, and J.C. Smith Solvent dependence of dynamic transitions in protein solutions Proc. Natl. Acad. Sci. USA 97 2000 9961 9966
58. Y. Seno, and N. Go Deoxymyoglobin studied by the conformational normal mode analysis II. The conformational change upon oxgenation J. Mol. Biol. 216 1990 111 126
59. Y. Seno, and N. Go Deoxymyoglobin studied by the conformational normal mode analysis. I. Dynamics of globin and the heme-globin interaction J. Mol. Biol. 216 1990 95 109
60. J.C. Smith Protein dynamics: comparison of simulations with inelastic neutron scattering experiments Q. Rev. Biophys. 24 1991 227 291
61. J. Smith, K. Kuczera, and M. Karplus Dynamics of myoglobin: comparison of simulation results with neutron scattering spectra Proc. Natl. Acad. Sci. USA 87 1990 1601 1605
62. K. Suhre, and Y.H. Sanejouand On the potential of normal-mode analysis for solving difficult molecular-replacement problems Acta Crystallogr. D Biol. Crystallogr. 60 2004 796 799
63. F. Tama, and C.L. Brooks III. The mechanism and pathway of pH induced swelling in cowpea chlorotic mottle virus J. Mol. Biol. 318 2002 733 747
64. F. Tama, W. Wriggers, and C.L. Brooks Exploring global distortions of biological macromolecules and assemblies from low-resolution structural information and elastic network theory J. Mol. Biol. 321 2002 297 305
65. F. Tama, M. Valle, J. Frank, and C.L. Brooks III. Dynamic reorganization of the functionally active ribosome explored by normal mode analysis and cryo-electron microscopy Proc. Natl. Acad. Sci. USA 100 2003 9319 9323
66. F. Tama, O. Miyashita, and C.L. Brooks III. Normal mode based flexible fitting of high-resolution structure into low-resolution experimental data from cryo-EM J. Struct. Biol. 147 2004 315 326
67. R. Tatsumi, Y. Fukunishi, and H. Nakamura A hybrid method of molecular dynamics and harmonic dynamics for docking of flexible ligand to flexible receptor J. Comput. Chem. 25 2004 1995 2005
68. D. Thirumalai, and G.H. Lorimer Chaperonin-mediated protein folding Annu. Rev. Biophys. Biomol. Struct. 30 2001 245 269
69. A. Thomas, M.J. Field, L. Mouawad, and D. Perahia Analysis of the low frequency normal modes of the T-state of aspartate transcarbamylase J. Mol. Biol. 257 1996 1070 1087
70. A. Thomas, M.J. Field, and D. Perahia Analysis of the low-frequency normal modes of the R state of aspartate transcarbamylase and a comparison with the T state modes J. Mol. Biol. 261 1996 490 506
71. A. Thomas, K. Hinsen, M.J. Field, and D. Perahia Tertiary and quaternary conformational changes in aspartate transcarbamylase: a normal mode study Proteins 34 1999 96 112
72. M.M. Tirion Large amplitude elastic motions in proteins from a single-parameter, atomic analysis Phys. Rev. Lett. 77 1996 1905 1908
73. M.M. Tirion, D. ben-Avraham, M. Lorenz, and K.C. Holmes Normal modes as refinement parameters for the F-actin model Biophys. J. 68 1995 5 12
74. Trakhanov, S., Vyas, N.K., Kristensen, D.M., Ma, J., and Quiocho, F.A. (2005). The ligand free and bound structures of the binding protein (LivJ) of the E. coli ABC Leu/Ile/Val transport system: trajectory and dynamics of interdomain rotation and polar versus nonpolar interactions in ligand binding.Biochemistry, in press.
75. Y. Wang, A.J. Rader, I. Bahar, and R.L. Jernigan Global ribosome motions revealed with elastic network model J. Struct. Biol. 147 2004 302 314
76. Y. Wu, and J. Ma Normal-mode-based refinement of an F-actin model against fibre diffraction data Fibre Diff. Rev. 12 2004 25 28
77. Y. Wu, and J. Ma Refinement of F-actin model against fibre diffraction data by long-range normal modes Biophys. J. 86 2004 116 124
78. Z. Xu, and P.B. Sigler GroEL/GroES: structure and function of a two-stroke folding machine J. Struct. Biol. 124 1998 129 141
79. 7 chaperonin complex Nature 388 1997 741 750
80. C. Xu, D. Tobi, and I. Bahar Allosteric changes in protein structure computed by a simple mechanical model: hemoglobin T↔R2 transition J. Mol. Biol. 333 2003 153 168
81. W. Yang, Y.Q. Gao, Q. Cui, J. Ma, and M. Karplus The missing link between thermodynamics and structure in F1-ATPase Proc. Natl. Acad. Sci. USA 100 2003 874 879
82. Z. Zhang, Y. Shi, and H. Liu Molecular dynamics simulations of peptides and proteins with amplified collective motions Biophys. J. 84 2003 3583 3593
83. W. Zheng, and S. Doniach A comparative study of motor-protein motions by using a simple elastic-network model Proc. Natl. Acad. Sci. USA 100 2003 13253 13258
84. Z.H. Zhou, W. Liao, R.H. Cheng, J.E. Lawson, D.B. McCarthy, L.J. Reed, and J.K. Stoops Direct evidence for the size and conformational variability of the pyruvate dehydrogenase complex revealed by three-dimensional electron microscopy. The "breathing" core and its functional relationship to protein dynamics J. Biol. Chem. 276 2001 21704 21713