Finding rigid bodies in protein structures: Application to flexible fitting into cryoEM maps

Journal of Structural Biology

Volumn 177, Issue 2, 2012, Pages 520-531

  Pandurangan, Arun Prasad ^a   Topf, Maya ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Clustering; Cryo electron microscopy density fitting; Flexible fitting; Low resolution maps; Optimisation; Rigid bodies

Indexed keywords

ARTICLE; CONFORMATION; CRYO ELECTRON MICROSCOPY; ELECTRON MICROSCOPY; METHODOLOGY; NANOANALYSIS; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; RIBFIND;

CLUSTER ANALYSIS; CRYOELECTRON MICROSCOPY; DATA INTERPRETATION, STATISTICAL; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; PROTEINS; SOFTWARE;

EID: 84857033345     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2011.10.011     Document Type: Article

References (53)

1. Abyzov A., Bjornson R., Felipe M., Gerstein M. RigidFinder: a fast and sensitive method to detect rigid blocks in large macromolecular complexes. Proteins 2010, 78:309-324.
2. Alber F., Forster F., Korkin D., Topf M., Sali A. Integrating diverse data for structure determination of macromolecular assemblies. Annu. Rev. Biochem. 2008, 77:443-477.
3. Baker D., Sali A. Protein structure prediction and structural genomics. Science 2001, 294:93-96.
4. Baker M.L., Jiang W., Wedemeyer W.J., Rixon F.J., Baker D., Chiu W. Ab initio modeling of the herpesvirus VP26 core domain assessed by CryoEM density. PLoS Comput. Biol. 2006, 2:e146.
5. Beck M., Topf M., Frazier Z., Tjong H., Xu M., Zhang S., Alber F. Exploring the spatial and temporal organization of a cell's proteome. J. Struct. Biol. 2011, 173:483-496.
6. Braig K., Adams P.D., Brunger A.T. Conformational variability in the refined structure of the chaperonin GroEL at 2.8A resolution. Nat. Struct. Biol. 1995, 2:1083-1094.
7. Chandramouli P., Topf M., Menetret J.F., Eswar N., Cannone J.J., Gutell R.R., Sali A., Akey C.W. Structure of the mammalian 80S ribosome at 8.7A resolution. Structure 2008, 16:535-548.
8. Chen J.Z., Furst J., Chapman M.S., Grigorieff N. Low-resolution structure refinement in electron microscopy. J. Struct. Biol. 2003, 144:144-151.
9. Chiu W., Baker M.L., Jiang W., Dougherty M., Schmid M.F. Electron cryomicroscopy of biological machines at subnanometer resolution. Structure (Cambridge) 2005, 13:363-372.
10. Connell S.R., Topf M., Qin Y., Wilson D.N., Mielke T., Fucini P., Nierhaus K.H., Spahn C.M. A new tRNA intermediate revealed on the ribosome during EF4-mediated back-translocation. Nat. Struct. Mol. Biol. 2008, 15:910-915.
11. DiMaio F., Tyka M.D., Baker M.L., Chiu W., Baker D. Refinement of protein structures into low-resolution density maps using rosetta. J. Mol. Biol. 2009, 392:181-190.
12. Evans R.N., Blaha G., Bailey S., Steitz T.A. The structure of LepA, the ribosomal back translocase. Proc. Natl. Acad. Sci. USA 2008, 105:4673-4678.
13. Fabiola F., Chapman M.S. Fitting of high-resolution structures into electron microscopy reconstruction images. Structure (Cambridge) 2005, 13:389-400.
14. 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-D301.
15. Flores S.C., Gerstein M.B. FlexOracle: predicting flexible hinges by identification of stable domains. BMC Bioinf. 2007, 8:215.
16. Forster F., Webb B., Krukenberg K.A., Tsuruta H., Agard D.A., Sali A. Integration of small-angle X-ray scattering data into structural modeling of proteins and their assemblies. J. Mol. Biol. 2008, 382:1089-1106.
17. Frank, J., 2006. Three-Dimensional Electron Microscopy of Macromolecular Assemblies: Visualization of Biological Molecules in Their Native State. Oxford University Press, New York.
18. Frank J. Single-particle reconstruction of biological macromolecules in electron microscopy - 30years. Q. Rev. Biophys. 2009, 42:139-158.
19. Fujii T., Iwane A.H., Yanagida T., Namba K. Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 2010, 467:724-728.
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. Hayward S., Berendsen H.J. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins 1998, 30:144-154.
22. Jacobs D.J., Rader A.J., Kuhn L.A., Thorpe M.F. Protein flexibility predictions using graph theory. Proteins 2001, 44:150-165.
23. Jolley C.C., Wells S.A., Fromme P., Thorpe M.F. Fitting low-resolution cryo-EM maps of proteins using constrained geometric simulations. Biophys. J. 2008, 94:1613-1621.
24. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983, 22:2577-2637.
25. Lasker K., Topf M., Sali A., Wolfson H.J. Inferential optimization for simultaneous fitting of multiple components into a CryoEM map of their assembly. J. Mol. Biol. 2009, 388:180-194.
26. Lawson C.L., Baker M.L., Best C., Bi C., Dougherty M., Feng P., van Ginkel G., Devkota B., Lagerstedt I., Ludtke S.J., Newman R.H., Oldfield T.J., Rees I., Sahni G., Sala R., Velankar S., Warren J., Westbrook J.D., Henrick K., Kleywegt G.J., Berman H.M., Chiu W. EMDataBank.org: unified data resource for CryoEM. Nucleic Acids Res. 2011, 39:D456-D464.
27. Ma J. Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes. Structure (Cambridge) 2005, 13:373-380.
28. Miyazawa S., Jernigan R.L. Residue-residue potentials with a favorable contact pair term and an unfavorable high packing density term, for simulation and threading. J. Mol. Biol. 1996, 256:623-644.
29. Orengo C.A., Michie A.D., Jones S., Jones D.T., Swindells M.B., Thornton J.M. CATH - a hierarchic classification of protein domain structures. Structure 1997, 5:1093-1108.
30. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
31. Ranson N.A., Farr G.W., Roseman A.M., Gowen B., Fenton W.A., Horwich A.L., Saibil H.R. ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 2001, 107:869-879.
32. Rawi R., Whitmore L., Topf M. CHOYCE - a web server for constrained homology modelling with cryoEM maps. Bioinformatics 2010, 26:1673-1674.
33. Rossmann M.G., Morais M.C., Leiman P.G., Zhang W. Combining X-ray crystallography and electron microscopy. Structure (Cambridge) 2005, 13:355-362.
34. Sali A., Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234:779-815.
35. Schroder 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.
36. Spahn C.M., Penczek P.A. Exploring conformational modes of macromolecular assemblies by multiparticle cryo-EM. Curr. Opin. Struct. Biol. 2009, 19:623-631.
37. 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 Biol. Crystallogr. 2006, 62:1098-1100.
38. Tama F., Wriggers W., Brooks C.L. Exploring global distortions of biological macromolecules and assemblies from low-resolution structural information and elastic network theory. J. Mol. Biol. 2002, 321:297-305.
39. Taylor D.J., Devkota B., Huang A.D., Topf M., Narayanan E., Sali A., Harvey S.C., Frank J. Comprehensive molecular structure of the eukaryotic ribosome. Structure 2009, 17:1591-1604.
40. Topf M., Sali A. Combining electron microscopy and comparative protein structure modeling. Curr. Opin. Struct. Biol. 2005, 15:578-585.
41. Topf M., Baker M.L., John B., Chiu W., Sali A. Structural characterization of components of protein assemblies by comparative modeling and electron cryo-microscopy. J. Struct. Biol. 2005, 149:191-203.
42. Topf M., Baker M.L., Marti-Renom M.A., Chiu W., Sali A. Refinement of protein structures by iterative comparative modeling and CryoEM density fitting. J. Mol. Biol. 2006, 357:1655-1668.
43. 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.
44. 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.
45. Velazquez-Muriel J.A., Valle M., Santamaria-Pang A., Kakadiaris I.A., Carazo J.M. Flexible fitting in 3D-EM guided by the structural variability of protein superfamilies. Structure 2006, 14:1115-1126.
46. Volkmann N., Hanein D., Ouyang G., Trybus K.M., DeRosier D.J., Lowey S. Evidence for cleft closure in actomyosin upon ADP release. Nat. Struct. Biol. 2000, 7:1147-1155.
47. Wendt T., Taylor D., Trybus K.M., Taylor K. Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2. Proc. Natl. Acad. Sci. USA 2001, 98:4361-4366.
48. Woetzel N., Lindert S., Stewart P.L., Meiler J. BCL::EM-Fit: rigid body fitting of atomic structures into density maps using geometric hashing and real space refinement. J. Struct. Biol. 2011, 175:264-276.
49. Wriggers W. Using Situs for the integration of multi-resolution structures. Biophys. Rev. 2010, 2:21-27.
50. Wriggers W., Schulten K. Protein domain movements: detection of rigid domains and visualization of hinges in comparisons of atomic coordinates. Proteins 1997, 29:1-14.
51. Wriggers W., Chacon P. Modeling tricks and fitting techniques for multiresolution structures. Structure (Cambridge) 2001, 9:779-788.
52. Zhang S., Vasishtan D., Xu M., Topf M., Alber F. A fast mathematical programming procedure for simultaneous fitting of assembly components into cryoEM density maps. Bioinformatics 2010, 26:i261-i268.
53. 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.