IMODFIT: Efficient and robust flexible fitting based on vibrational analysis in internal coordinates

Journal of Structural Biology

Volumn 184, Issue 2, 2013, Pages 261-270

  Lopéz Blanco, José Ramón ^a   Chacón, Pablo ^a  

^a INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

Author keywords

Coarse grained models; Flexible fitting; Hybrid methods; Internal coordinates; Molecular modeling; Normal mode analysis

Indexed keywords

ARTICLE; ATOM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DENSITY; ELECTRON MICROSCOPY; EXPERIMENTAL TEST; GEOMETRY; MACROMOLECULE; MECHANICAL TORSION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR MODEL; MOLECULAR SIZE; MOTION; NORMAL MODE ANALYSIS; PRIORITY JOURNAL; QUALITY CONTROL; STEREOCHEMISTRY;

COARSE-GRAINED MODELS; FLEXIBLE FITTING; HYBRID METHODS; INTERNAL COORDINATES; MOLECULAR MODELING; NORMAL MODE ANALYSIS;

ALGORITHMS; CHAPERONIN 60; COMPUTER SIMULATION; CRYOELECTRON MICROSCOPY; DATA INTERPRETATION, STATISTICAL; MICROTUBULES; MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY; RIBOSOMES; SOFTWARE;

EID: 84887256582     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2013.08.010     Document Type: Article

References (72)

1. Agirrezabala X., Liao H.Y., Schreiner E., Fu J., Ortiz-Meoz R.F., Schulten K., Green R., Frank J. Structural characterization of mRNA-tRNA translocation intermediates. Proc. Natl. Acad. Sci. USA 2012, 109:6094-6099.
2. Ahmed A., Tama F. Consensus among multiple approaches as a reliability measure for flexible fitting into cryo-EM data. J. Struct. Biol. 2013, 182:67-77.
3. Ahmed A., Whitford P.C., Sanbonmatsu K.Y., Tama F. Consensus among flexible fitting approaches improves the interpretation of cryo-EM data. J. Struct. Biol. 2012, 177:561-570.
4. Alushin G.M., Ramey V.H., Pasqualato S., Ball D.A., Grigorieff N., Musacchio A., Nogales E. The Ndc80 kinetochore complex forms oligomeric arrays along microtubules. Nature 2010, 467:805-810.
5. Bahar I., Lezon T.R., Bakan A., Shrivastava I.H. Normal Mode Analysis of biomolecular structures: functional mechanisms of membrane proteins. Chem. Rev. 2010, 110:1463-1497.
6. Bray J.K., Weiss D.R., Levitt M. Optimized torsion-angle normal modes reproduce conformational changes more accurately than cartesian modes. Biophys. J. 2011, 101:2966-2969.
7. Brooks B., Karplus M. Normal modes for specific motions of macromolecules: application to the hinge-bending mode of lysozyme. Proc. Natl. Acad. Sci. USA 1985, 82:4995-4999.
8. Chacón P., Wriggers W. Multi-resolution contour-based fitting of macromolecular structures. J. Mol. Biol. 2002, 317:375-384.
9. Chan K.Y., Trabuco L.G., Schreiner E., Schulten K. Cryo-electron microscopy modeling by the molecular dynamics flexible fitting method. Biopolymers 2012, 97:678-686.
10. Chen J.Z., Fürst J., Chapman M.S., Grigorieff N. Low-resolution structure refinement in electron microscopy. J. Struct. Biol. 2003, 144:144-151.
11. Chen V.B., Arendall W.B., Headd J.J., Keedy D.A., Immormino R.M., Kapral G.J., Murray L.W., Richardson J.S., Richardson D.C. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 2010, 66:12-21.
12. Clare D.K., Stagg S., Quispe J., Farr G.W., Horwich A.L., Saibil H.R. Multiple states of a nucleotide-bound group 2 chaperonin. Structure 2008, 16:528-534.
13. Clare D.K., Vasishtan D., Stagg S., Quispe J., Farr G.W., Topf M., Horwich A.L., Saibil H.R. ATP-triggered conformational changes delineate substrate-binding and -folding mechanics of the GroEL chaperonin. Cell 2012, 149:113-123.
14. Cui Q., Bahar I. Normal Mode Analysis Theoretical and Applications to Biological and Chemical Systems 2007, Chapman and Hall, CRC.
15. Darst S.A., Opalka N., Chacon P., Polyakov A., Richter C., Zhang G., Wriggers W. Conformational flexibility of bacterial RNA polymerase. Proc. Natl. Acad. Sci. USA 2002, 99:4296-4301.
16. Fabiola F., Chapman M.S. Fitting of high-resolution structures into electron microscopy reconstruction images. Structure 2005, 13:389-400.
17. Flores S., Echols N., Milburn D., Hespenheide B., Keating K., Lu J., Wells S., Yu E.Z., Thorpe M., Gerstein M. The database of macromolecular Motions: new features added at the decade mark. Nucleic Acids Res. 2006, 34:D296-301.
18. Garzón J.I., Kovacs J., Abagyan R., Chacón P. ADP_EM: fast exhaustive multi-resolution docking for high-throughput coverage. Bioinformatics 2007, 23:427-433.
19. Go N., Noguti T., Nishikawa T. Dynamics of a small globular protein in terms of low-frequency vibrational modes. Proc. Natl. Acad. Sci. USA 1983, 80:3696-3700.
20. Grubisic I., Shokhirev M.N., Orzechowski M., Miyashita O., Tama F. Biased coarse-grained molecular dynamics simulation approach for flexible fitting of X-ray structure into cryo electron microscopy maps. J. Struct. Biol. 2010, 169:95-105.
21. Hinsen K., Reuter N., Navaza J., Stokes D.L., Lacapere J.J. Normal mode-based fitting of atomic structure into electron density maps: application to sarcoplasmic reticulum Ca-ATPase. Biophys. J. 2005, 88:818-827.
22. Hyeon C., Lorimer G.H., Thirumalai D. Dynamics of allosteric transitions in GroEL. Proc. Natl. Acad. Sci. USA 2006, 103:18939-18944.
23. Jolley C.C., Wells S., Fromme P., Thorpe M.F. Fitting low-resolution cryo-EM maps of proteins using constrained geometric simulations. Biophys. J. 2008, 94:1613-1621.
24. Kovacs J.A., Cavasotto C.N., Abagyan R. Conformational sampling of protein flexibility in generalized coordinates: application to ligand docking. J. Comput. Theor. Nanosci. 2005, 2:354-361.
25. Kovacs J.A., Yeager M., Abagyan R. Damped-dynamics flexible fitting. Biophys. J. 2008, 95:3192-3207.
26. Lau W.C., Rubinstein J.L. Subnanometre-resolution structure of the intact Thermus thermophilus H+-driven ATP synthase. Nature 2012, 481:214-218.
27. Levitt M., Sander C., Stern P.S. Protein normal-mode dynamics: trypsin inhibitor, crambin, ribonuclease and lysozyme. J. Mol. Biol. 1985, 181:423-447.
28. López-Blanco J.R., Garzón J.I., Chacón P. IMod: multipurpose Normal Mode Analysis in internal coordinates. Bioinformatics 2011, 27:2843-2850.
29. López-Blanco J.R., Reyes R., Aliaga J.I., Badia R.M., Chacón P., Quintana-Ortí E.S. Exploring large macromolecular functional motions on clusters of multicore processors. J. Comput. Phys. 2013, 246:275-288.
30. Lu M., Poon B., Ma J. A new method for coarse-grained elastic normal-mode analysis. J. Chem. Theory Comput. 2006, 2:464-471.
31. Ludtke S.J., Lawson C.L., Kleywegt G.J., Berman H., Chiu W. The 2010 cryo-EM modeling challenge. Biopolymers 2012, 97:651-654.
32. Ma J., Sigler P.B., Xu Z., Karplus M. A dynamic model for the allosteric mechanism of GroEL. J. Mol. Biol. 2000, 302:303-313.
33. Martin-Benito J., Gomez-Reino J., Stirling P.C., Lundin V.F., Gomez-Puertas P., Boskovic J., Chacón P., Fernandez J.J., Berenguer J., Leroux M.R., Valpuesta J.M. Divergent substrate-binding mechanisms reveal an evolutionary specialization of eukaryotic prefoldin compared to its archaeal counterpart. Structure 2007, 15:101-110.
34. Mendez R., Bastolla U. Torsional network model: normal modes in torsion angle space better correlate with conformation changes in proteins. Phys. Rev. Lett. 2010, 104:228103-228107.
35. Mitra K., Schaffitzel C., Shaikh T., Tama F., Jenni S., Brooks Iii C.L., Ban N., Frank J. Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 2005, 438:318-324.
36. Noguti T., Go N. Dynamics of native globular proteins in terms of dihedral angles. J. Phys. Soc. Jpn. 1983, 52:3283-3288.
37. Oot R.A., Huang L.S., Berry E.A., Wilkens S. Crystal structure of the yeast vacuolar ATPase heterotrimeric EGC(head) peripheral stalk complex. Structure 2012, 20:1881-1892.
38. Opalka N., Chlenov M., Chacón P., Rice W.J., Wriggers W., Darst S.A. Structure and function of the transcription elongation factor GreB bound to bacterial RNA polymerase. Cell 2003, 114:335-345.
39. Orzechowski M., Tama F. Flexible fitting of high-resolution X-ray structures into cryoelectron microscopy maps using biased molecular dynamics simulations. Biophys. J. 2008, 95:5692-5705.
40. Press W.H., Teukolsky S.A., Vetterling W.T., Flannery B.P. Numerical recipes. The Art of Scientific Computing 2007, Cambridge University Press. third ed.
41. Ranson N.A., Clare D.K., Farr G.W., Houldershaw D., Horwich A.L., Saibil H.R. Allosteric signaling of ATP hydrolysis in GroEL-GroES complexes. Nat. Struct. Mol. Biol. 2006, 13:147-152.
42. Ratje A.H., Loerke J., Mikolajka A., Brünner M., Hildebrand P.W., Starosta A.L., Dönhöfer A., Connell S.R., Fucini P., Mielke T., Whitford P.C., Onuchic J.N., Yu Y., Sanbonmatsu K.Y., Hartmann R.K., Penczek P.A., Wilson D.N., Spahn C.M.T. Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature 2010, 468:713-716.
43. Roseman A.M., Chen S., White H., Braig K., Saibil H.R. The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 1996, 87:241-251.
44. Rusu M., Birmanns S., Wriggers W. Biomolecular pleiomorphism probed by spatial interpolation of coarse models. Bioinformatics 2008, 24:2460-2466.
45. Schröder G.F., Brunger A.T., Levitt M. Combining efficient conformational sampling with a deformable elastic network model facilitates structure refinement at low resolution. Structure 2007, 15:1630-1641.
46. Shakeel S., Seitsonen J.J., Kajander T., Laurinmäki P., Hyypiä T., Susi P., Butcher S.J. Structural and functional analysis of coxsackievirus A9 integrin αvβ6 bindingand uncoating. J. Virol. 2013, 7:3943-3951.
47. Siebert X., Navaza J. UROX 2.0: an interactive tool for fitting atomic models into electron-microscopy reconstructions. Acta Crystallogr. D 2009, 65:651-658.
48. Skjaerven L., Hollup S.M., Reuter N. Normal Mode Analysis for proteins. J. Mol. Struct. (Theochem) 2009, 898:42-48.
49. Suhre K., Navaza J., Sanejouand Y.H. NORMA: a tool for flexible fitting of high-resolution protein structures into low-resolution electron-microscopy-derived density maps. Acta Crystallogr. D 2006, 62:1098-1100.
50. Tama F., Brooks C.L. Symmetry, form, and shape: guiding principles for robustness in macromolecular machines. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:115-133.
51. Tama F., Miyashita O., Brooks C.L. Flexible multi-scale fitting of atomic structures into low-resolution electron density maps with elastic network Normal Mode Analysis. J. Mol. Biol. 2004, 337:985-999.
52. Tama F., Miyashita O., Brooks C.L. Normal mode based flexible fitting of high-resolution structure into low-resolution experimental data from cryo-EM. J. Struct. Biol. 2004, 147:315-326.
53. Tama F., Ren G., Brooks C.L., Mitra A.K. Model of the toxic complex of anthrax: responsive conformational changes in both the lethal factor and the protective antigen heptamer. Protein Sci. 2006, 15:2190-2200.
54. Tan R.K.Z., Devkota B., Harvey S.C. YUP.SCX: coaxing atomic models into medium resolution electron density maps. J. Struct. Biol. 2008, 163:163-174.
55. Tirion M.M. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys. Rev. Lett. 1996, 77:1905-1908.
56. Topf M., Sali A. Combining electron microscopy and comparative protein structure modeling. Curr. Opin. Struct. Biol. 2005, 15:578-585.
57. Topf M., Lasker K., Webb B., Wolfson H., Chiu W., Sali A. Protein structure fitting and refinement guided by cryo-EM density. Structure 2008, 16:295-307.
58. Trabuco L.G., Villa E., Mitra K., Frank J., Schulten K. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 2008, 16:673-683.
59. Trabuco L.G., Villa E., Schreiner E., Harrison C.B., Schulten K. Molecular dynamics flexible fitting: a practical guide to combine cryo-electron microscopy and X-ray crystallography. Methods 2009, 49:174-180.
60. Valle M., Zavialov A., Sengupta J., Rawat U., Ehrenberg M., Frank J. Locking and unlocking of ribosomal motions. Cell 2003, 114:123-134.
61. Vashisth H., Skiniotis G., Brooks C.L. Using enhanced sampling and structural restraints to refine atomic structures into low-resolution electron microscopy maps. Structure 2012, 20:1453-1462.
62. Velazquez-Muriel J.A., Carazo J.M. Flexible fitting in 3D-EM with incomplete data on superfamily variability. J. Struct. Biol. 2007, 158:165-181.
63. Villa E., Sengupta J., Trabuco L.G., LeBarron J., Baxter W.T., Shaikh T.R., Grassucci R.A., Nissen P., Ehrenberg M., Schulten K., Frank J. Ribosome-induced changes in elongation factor Tu conformation control GTP hydrolysis. Proc. Natl. Acad. Sci. USA 2009, 106:1063-1068.
64. Wang Z., Schroder G.F. Real-space refinement with DireX: from global fitting to side-chain improvements. Biopolymers 2012, 97:687-697.
65. Whitford P.C., Geggier P., Altman R.B., Blanchard S.C., Onuchic J.N., Sanbonmatsu K.Y. Accommodation of aminoacyl-tRNA into the ribosome involves reversible excursions along multiple pathways. RNA 2010, 16:1196-1204.
66. Whitford P.C., Ahmed A., Yu Y., Hennelly S.P., Tama F., Spahn C.M.T., Onuchic J.N., Sanbonmatsu K.Y. Excited states of ribosome translocation revealed through integrative molecular modeling. Proc. Natl. Acad. Sci. USA 2011, 108:18943-18948.
67. Wriggers W., Chacón P. Modeling tricks and fitting techniques for multiresolution structures. Structure 2001, 9:779-788.
68. Wriggers W., Chacón P., Kovacs J.A., Tama F., Birmanns S. Topology representing neural networks reconcile biomolecular shape, structure, and dynamics. Neurocomputing 2004, 56:365-379.
69. Xu Z., Horwich A.L., Sigler P.B. The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 1997, 388:741-750.
70. Yamashita H., Endo S., Wako H., Kidera A. Sampling efficiency of molecular dynamics and Monte Carlo method in protein simulation. Chem. Phys. Lett. 2001, 342:382-386.
71. Zheng W. Accurate flexible fitting of high-resolution protein structures into cryo-electron microscopy maps using coarse-grained pseudo-energy minimization. Biophys. J. 2011, 100:478-488.
72. Zhu J., Cheng L., Fang Q., Zhou Z.H., Honig B. Building and refining protein models within cryo-electron microscopy density maps based on homology modeling and multiscale structure refinement. J. Mol. Biol. 2010, 397:835-851.